THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): i Date of Publication: 31 Aug.2009 © National University of

EDITORIAL

The Raffl es Bulletin of Zoology had an productive year for 2009—18 papers in 57(1) and 23 papers in this issue, 57(2). This is a total of 41 papers published in the two regular issues of the Bulletin and an additional 15 in the second supplement, which was published on 31 July 2009. We are also expecting to publish perhaps three more supplements this year, including a checklist of world decapod genera.

Our Associate Editor for Crustacea, Dr. Tohru Naruse, has left the National University of Singapore (NUS) for a faculty position at the University of Ryukyus. Although he is now no longer in Sinagpore, he has kindly agreed to continue serving as an Associate Editor for crustacean manuscripts. We also take this opportunity to welcome a new Associate Board member, Dr. Tran Anh Duc, from the Hanoi University of Science, Hanoi, . Dr. Tran is a recent graduate of NUS and specialises in aquatic Heteroptera (for example, see Polhemus et al., 2009, and Zettel & Tran, 2009).

Research into the history of the Bulletin has revealed that several volumes had publication dates inconsistent with the publisher’s dates as printed on the wrapper(s) of the Bulletin. This has pushed back the dates of publications of several volumes (by a year) and brought forward by a year the date of publication of one volume. The volumes relevant to brachyuran taxonomy have been dealt with in a paper in the second crustacean supplement (Low et al., 2009a). A more detailed and complete review of this issue will be published in an upcoming supplement of the Bulletin (Low et al., 2009b).

Low et al. (2009a) also surveyed all brachyuran papers published by the Bulletin and found the RBZ has been publishing an average of 3.5 new of crabs over a period of eight decades, since the Bulletin’s inception in 1928. This is no mean feat and is an indication of the hard work and effort by authors, the Editorial Board and staff.

These same qualities and quantities of hard work have seen the RBZ’s impact factor rise to 0.800 in 2008, up from 0.648 in 2007. We to authors and the Editorial Board their effort and look forward to even greater things in 2010!

Tan Swee Hee Managing Editor Raffl es Bulletin of Zoology

LITERATURE CITED

Low, M. E. Y., S. H. Tan & P. K. L. Ng, 2009a. The Raffl es Bulletin, 1928–2009: Eight decades of brachyuran crab research (Crustacea: ). Raffl es Bulletin of Zoology, Supplement No. 20: 291–307. Low, M. E. Y., S. H. Tan & P. K. L. Ng, 2009b. Dates of publication of the Bulletin of the Raffl es Museum and the Bulletin of the National Museum, predecessors to the Raffl es Bulletin of Zoology. Raffl es Bulletin of Zoology, Supplement No. 21 (in press). Polhemus, J. T., A. D. Tran & D. A. Polhemus, 2009. The Eotrechus (Heteroptera: Gerridae) in Vietnam, with descriptions of two new species. Raffl es Bulletin of Zoology, 57(1): 29–37. Zettel, H. & A. D. Tran, 2009. First inventory of the water bugs (Heteroptera: Nepomorpha, Gerromorpha) of Langkawi Island, Kedah, . Raffl es Bulletin of Zoology, 57(2): 277–292.

i THE RAFFLES BULLETIN OF ZOOLOGY 2009

THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 239–249 Date of Publication: 31 Aug.2009 © National University of Singapore

THE LARVA AND PUPARIUM OF THE ORIENTAL PEGADOMYIA PRUINOSA KERTÉSZ, WITH A WORLD LIST OF THE DESCRIBED PACHYGASTRINAE LARVAE (DIPTERA: STRATIOMYIDAE)

Alena Bu ánková Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlá ská 2, 611 37 Brno, Czech Republic Email: [email protected]

Damir Kovac Forschungsinstitut Senckenberg, Senckenberganlage 25, D-60325 Frankfurt a.M., Germanay Email: [email protected]

Rudolf Rozkošný Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlá ská 2, 611 37 Brno, Czech Republic Email: [email protected]

ABSTRACT. – The larva and puparium of Pegadomyia pruinosa Kertész, 1916, are described and compared with the other known saproxylic larvae from the subfamily Pachygastrinae. Diagnostic characters at the subfamily level as well as specifi c distinguishing characters of the pachygastrine larvae are summarized and a list of the described larvae for the world is given. An original identifi cation key to the Oriental and East Palaearctic larvae (14 spp.) is proposed. Basic diagnostic characters of the described larva and puparium are illustrated and documented by SEM images.

KEY WORDS. – Stratiomyidae, Pegadomyia, larva, puparium, saproxylic, Malaysia, .

INTRODUCTION 1991). They are often gregarious, with several to many occurring together at the same site. Essentially, they are Woodley (2001) recorded 561 species of world micropantophagous scavengers and they may even shown Pachygastrinae and 19 species and 1 subspecies were certain sapronecrophagous tendencies feeding upon dead subsequently described by Krivosheina (2002: one species; saproxylic and their larvae (cf. Mamaev et al., 2004: three species, one subspecies), Krivosheina & 1977). Larvae of Holarctic Pachygastrinae apparently Freidberg (2004: two species), Rozkošný & Kozánek (2007: feed on fermenting sap, fungus spores or decay-producing 7 spp.), Rozkošný & Kovac (2007: one species; 2008: four microorgasnisms (Teskey, 1976). In the gut contents of species) and Woodley (2008: one species). However, larvae a larva of Camptopteromyia fractipennis sporangia with are described for only 48 species (see Table 1), i.e. for 8.3 spores of fungi, bacteria and unidentifi ed organic debris % of the world fauna of this subfamily. were found (Rozkošný & Kovac, 1991).

Larvae of Pachygastrinae are generally found under the Keys to the known larvae of Nearctic genera of this bark of dead or decaying trees, rarely also in soil, at roots subfamily were published by Kraft & Cook (1961), of plants, in decaying remains of vegetation or under McFadden (1967) and James (1981), and keys to the known specialised conditions; e.g. larvae of Eupachygaster larvae at the species level are to be found in the fi rst two alexanderi (Bréthes, 1922) were reared from rotting Opuntia papers; the known Nearctic Zabrachia larvae were keyed sulphurea in Argentina (cf. Blanchard, 1923; James, 1967), by James (1965). Larvae of Palaearctic genera may be Zabrachia stoichodes James, 1965, and Cactobia opuntiae distinguished according to Krivosheina (1977), Mamaev James, 1966, from cacti in the southwestern United States et al. (1977) and Rozkošný (1997). A key to Palaearctic and Mexico, larvae of Zabrachia yuccae James, 1965, Neopachygaster larvae is given by Krivosheina (1976) and from yucca in Arizona and those of Camptopteromyia those to Zabrachia by Krivosheina & Rozkošný (1990). A fractipennis de Meijere, 1914, were collected inside the key to fi ve Neotropical pachygastrine larvae was published internodes of bamboo in Malaysia (Rozkošný & Kovac, by Xeres et al. (2003b).

239 Bucánková et at.: Larva and Puparium of Pegadomyia pruinosa

Table 1. World list of the known larvae of Pachygastrinae. Abbreviations used: AF, African; AU, Australasian; NE, Neartic; NT, Neo- tropical; OR, Oriental; PA, Palaeartic.

Species Distribution Author Synonyms Alliophlebs elliptica Becker, 1908 PA: Canary Is. Rozkošný & Baez, 1986 Aspidacantha atra Kertész, 1916 AF: Ethiopia, Tanzania, Uganda, Krivosheina, 1975 Zaire, Zimbabwe PA: Egypt, Israel, Turkmenistan Berkshiria albistylum Johnson, 1914 NE: Canada, USA Kraft & Cook, 1961 Berkshiria hungarica (Kertész, 1921) PA: Europe, W Siberia Krivosheina, 1965; Pseudowallacea Rozkošný, 1983 Camptopteromyia fractipennis de OR: (Java), W Malaysia Rozkošný & Kovac, 1991 Meijere, 1914 Cechorismenus fl avicornis Kertész, 1916 PA: Far East of Russia Krivosheina, 1977 OR: Chalcidomorphina aurata Enderlein, 1914 NT: from Mexico to Peru and Brazil Pujol-Luz & Xeres, 1999 Cosmariomyia argyrosticta Kertész, 1914 NT: Argentina, Brazil, Costa Rica, Xeres et al., 2002 El Salvador Craspedometopon basale (Matsumura, PA : Far East of Russia, Korea, Krivosheina, 1977 C. ussuricum 1915) Krivosheina, 1973 Dactylodeictes lopesi Lindner, 1964 NT: from Mexico to Brazil Xeres et al., 2002 Damaromyia tasmanica Kertész, 1916 AU: Australia, Tasmania James, 1950 Eidalimus fuscus (Kraft & Cook, 1961) NE: Canada, USA Kraft & Cook, 1961 Eupachygaster Eidalimus henshawi (Malloch, 1917) NE: USA NT: Cuba, Mexico Kraft & Cook, 1961 Eupachygaster Engicerus major Lindner, 1964 NT Brazil Xeres et al. 2003a Eupachygster alexanderi (Brèthes, 1922) NT: Argentina Blanchard, 1923 Eupachygaster tarsalis (Zetterstedt, 1842) PA: Europe, Azerbaijan, Krivosheina, 1975; Turkmenistan Rozkošný, 1983 Gabaza nigrotibialis (Pleske, 1930) PA: Far East of Russia Krivosheina, 1977; Wallacea Mamaev et al., 1977 Gowdeyana punctifera (Malloch, 1915) NE: USA Kraft & Cook, 1961 Eupachygaster NT: Mexico punctifer Maackiana laminiformis Krivosheina, 1973 PA: Far East of Russia Krivosheina, 1977 Manotes crassimanus James, 1980 NT: Brazil, Mexico Lopes et al., 2006 Neopachygaster intermedia (Krivosheina, PA: Mongolia, Uzbekistan Krivosheina, 1965, 1976 1965) Neopachygaster maculicornis (Hine, 1902) NE: Canada, USA Kraft & Cook, 1961 Neopachygaster meromelas (Dufour, 1841) PA: Europe Krivosheina, 1965; Pachygaster Rozkošný, 1983 orbitalis Neopachygaster occidentalis Kraft & Cook, NE: Canada, USA Kraft & Cook, 1961 1961 Neopachygaster reniformis Hull, 1942 NE: Canada, USA Kraft & Cook, 1961 Neopachygaster secernibilis Krivosheina PA: Far East of Russia Krivosheina, 1976 1973 Neopachygaster stackelbergi Krivosheina PA: Far East of Russia Krivosheina, 1976 1973 Neopachygaster vitrea Hull, 1930 NE: USA Kraft & Cook, 1961 Ornopyramis tener Krivosheina, 1973 PA: Far East of Russia Krivosheina, 1977 Pachygaster atra (Panzer, 1798) PA: Europe, Israel, Turkey Dušek & Rozkošný, 1975; Rozkošný, 1983 Pachygaster leachii Curtis, 1824 PA: Europe, Azerbaijan, Georgia Brindle, 1962; Krivosheina Praomyia & Rozkošný, 1985 Pachygaster piriventris Rozkošný & OR: W Malaysia, Thailand Rozkošný & Kovac, 1998 Kovac, 1998 Pachygaster pulchra Loew, 1863 NE: USA Kraft & Cook, 1961 Pedinocera longicornis Kertész, 1909 NT: Brazil, Peru Lopes et al., 2006

240 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Continued.

Species Distribution Author Synonyms Popanomyia femoralis Kertész, 1909 NT: Brazil, Panama, Peru Xeres et al., 2003a Pegadomyia pruinosa Kertész, 1916 OR: Malaysia, Thailand This paper Psephiocera modesta (Lindner, 1949) NT: Brazil Xeres et al., 2003b Vittiger schnusei Kertész, 1909 NT: Barzil, Peru Xeres & Pujol-Luz, 2001 Xylopachygaster mamaevi Krivosheina, PA: Far East of Russia Krivosheina, 1977 1973 Zabrachia magnicornis Cresson, 1919 NE: USA James, 1965 NT: Mexico Zabrachia minutissima (Zetterstedt, 1838) PA: Europe, Israel, Kazakhstan, Krivosheina & Rozkošný, Uzbekistan, Siberia, Far East of 1985, 1990 Russia, Japan Zabrachia occidentalis Rozkošný & Baez, PA: Canary Is. Rozkošný & Baez, 1986 1983 Zabrachia plicata Kraft & Cook, 1961 NE: Canada, USA Kraft & Cook, 1961 Zabrachia polita Coquillett, 1901 NE: Canada, USA Kraft & Cook, 1961 Zabrachia stackelbergi Krivosheina & PA: Far East of Russia Krivosheina & Rozkošný, Rozkošný, 1990 1990 Zabrachia stoichoides James, 1965 NT: Mexico James, 1965 Zabrachia tenella (Jaenicke, 1866) PA: Europe, Siberia, Far East of Krivosheina & Rozkošný, Russia incl. Kunashir I. 1985, 1990 Zabrachia yuccae James, 1965 NE: USA James, 1965

Numbers of pachygastrine larvae described in different besides apical segment of antenna, (5) shape of sublabral biogeographical regions vary considerably (cf. Table 1). appendage, (6) structure of mandibular-maxillary complex, The highest number of larvae is known from the Palaearctic (7) arrangement of maxillary palpus, (8) form of constant Region (18 species and eight of them described from the setae (clavate, pointed, density and length of pubescence), (9) Russian Far East), one additional species penetrates to length of lateral setae on body segments, (10) arrangement the Palaearctic Region from Africa and one species from of plaques on body segments (ornamentation on dorsal and the Oriental Region. Ten known larvae originate from the ventral surface), (11) confi guration of anterodorsal and dorsal Nearctic Region, and three additional larvae are known from setae on thoracic segment 1, (12) number of branches of outer both the Neotropical and Nearctic Regions. Eleven larvae are ventral setae on thoracic segments 1-3, (13) abbreviation of described from the Neotropical Region, three are Oriental outer dorsal setae on abdominal segments, (14) confi guration and one Australian. of setae on lateral wall of abdominal segments, (15) shape of sternal patch on abdominal segment 6, (16) position According to present knowledge the known larvae of of posterior spiracular opening on anal segment, (17), Pachygastrinae may be characterised by combination of the length of transverse integumentary fold above posterior following characters: (1) anal segment rounded posteriorly spiracular opening, (18) relative length of marginal setae as in other terrestrial larvae, (2) posterior spiracular opening on anal segment and their position, (19) length of anal slit, usually placed dorsally (with a few exceptions), without any (20) presence of marginal structures along anal slit, (21) pinnate fl oat hairs, (3) subapical sensilla on antenna usually confi guration of ventral setae on anal segment, (22) number absent (but distinct in Pegadomyia), (3) setae CF2 and V2 of visible pupal respiratory horns on abdominal segments, on head inserted far before eye prominence, (4) lateral seta (23) position of pupal respiratory horns relative to setae on on head placed close to anterior margin of eye, (5) marginal lateral wall of abdominal segments. setae of body segments considerably elongate in many species (though not in all), (6) elongate or rounded sternal patch In a recent revision of Pegadomyia Kertész, 1916 (see confi ned to abdominal segment 6, (7) fi ve ventral setae on Rozkošný & Kovac, 2008) this genus was split into two anal segment, (8) arboreal mode of life (under the bark of genera. Pegadomyia proper now includes 4 exclusively trees) distinctly predominating in the known larvae. Oriental species and Pseudopegadomyia Rozkošný & Kovac, 2008, contains three species, two of them distributed mainly Summed up from the descriptions published until now, the in the Australasian and Oceanic Regions, and the third, Ps. following characters may be used to distinguish between jamesi Rozkošný & Kovac, 2008, on western islands of the pachygastrine larvae (and puparia): (1) Head index (length to . No remarks concerning biology or morphology maximum width) and shape of head (especially presence of of the larva or puparium belonging to Pegadomyia have been postocular or basal lobes), (2) relative length of head setae, published. Damir Kovac succeeded in rearing Pegadomyia (3) number of clypeofrontal setae, (4) presence of sensila pruinosa Kertész, 1916, from larvae collected under the

241 Bucánková et at.: Larva and Puparium of Pegadomyia pruinosa bark of trees in Malaysia and Thailand. The larva and antenna (Fig. 21) placed at latero-apical corner of head puparium could thus be described, illustrated and compared capsule, two-segmented. Basal segment short and semi- with the other known saproxylic larvae of the subfamily spherical, apical segment at least 3.0 times longer and conical. Pachygastrinae. Rod-like sensillum present, being somewhat shorter than apical segment and placed lateral to it. Eyes situated laterally beyond middle of head on slightly convex eye elevations MATERIAL AND METHODS distinct especially in dorsal view. Basal lobe distinct on each side of head capsule. Labrum relatively narrow (Fig. Material examined: – WEST MALAYSIA: Ulu Gombak, Field 16), with a very characteristic sublabral appendage hanging Studies Centre, under the bark of a fallen tree, 1 May 2002, 7 on its ventral surface (Figs. 13, 22). Mandibular-maxillary mature larvae, 2 larvae of penultimate instar, 2 males emerged 27 complex elongate and margined by several rows of fl attened May 2005; THAILAND, Mae Hong Son Province, near Ban Nam and mostly serrate setae (Fig. 9). Maxillary palpus with 3 Rin, under the bark of a fallen tree, Nov.2003, 2 larvae, a female rounded sensorial papillae at apex (Figs 13, 23). Molar area emerged 2 Oct.2003; 2 Nov.2004, 3 larvae, a female emerged 31 Mar.2005 and a male 3 Apr.2005; all D. Kovac lgt. Deposited in transversely ridged, basal sclerite small (Fig. 9). the Faculty of Science, Masaryk University, Brno, Czech Republic (9 larvae and 4 puparia) and in the Forschungsinstitut Senckenberg, Chaetotaxy (Figs. 1–2): Two labral setae (or at least their Frankfurt a.M, Germany (2 larvae, 3 puparia). insertions) visible on sides of labrum. Of two pairs of clypeofrontal setae (CF1 and CF2) fi rst shorter and placed Rearing and preparation. – Larvae were collected individually in front of antennae; CF2 placed in middle between antenna and reared in separate dishes containing substrate (rotting and eye. Long lateral seta (L) visible below eye and much wood and pieces of bark) from the original locality. A portion shorter dorsolateral seta (DL) at upper posterior margin of of the larvae and puparia was preserved in 70% ethanol for eye. Two pairs of ventrolateral setae VL1, VL2) developed further study. Preparation for scanning electronic micrographs in distal third of head laterally and two pairs of ventral (SEM) was as follows: after cleaning and preservation in setae inserted ventrally near mouth opening. Last pair of alcohol, the immature stages were dehydrated in a graded ventrolateral setae (VL3) located almost at same level as series of ethanol solutions, dried by the critical point lateral setae, last ventral seta (V3) near posterior margin of technique with CO2 , and coated with palladium-gold before oval ventral plate. observation under the scanning microscope. Measurements are given without the length of marginal setae which may Colouring and ornamentation: Ground colour yellow but be different in length in individual larval instars. central third (clypeofrons) more brownish, also labrum Terminology. – Terminology including the chaetotaxy darkened along sides. Ventral surface yellow, only suboval follows the monograph by Rozkošný (1982) and a general ventral plate somewhat darker. No ornamentation consisting review of the dipteran larval morphology by Courtney et al. of brownish plaques present. (2000). The term plaque is used in the same sense as James (1965) used it, following some earlier authors. Such cuticular Thoracic segments. – 1st segment narrower than next two, structures are larger and mostly darker than the other small anterior spiracle on fi rst thoracic segment large, subtriangular surface plates. and prominent, with a distinct cleft.

Abbreviations. – a – antenna, ac – apical segment, AD Chaetotaxy (Figs 1-2): Setae short plumate, reaching 1/3-1/2 – anterodorsal seta, AMS – apical mandibular setae, AP segment length, only dorsolateral setae (DL) long. Two pairs – apical seta, as – anterior spiracle, asl – anal slit, AV of anterodorsal setae (AD1, AD2) placed in transverse row – anteroventral seta, bl – basal lobe, bs – basal segment, near anterior margin of thoracic segment 1, three pairs of bsc – basal sclerite, CF – clypeofrontal seta, D – dorsal seta, dorsal setae (D1, D2 and D3) arranged in Y-shaped formation. DC – dorsocentral seta, DL – dorsolateral seta, e – eye, L On thoracic segment 2 and 3 only 3 pairs of dorsal setae – lateral seta, lb – labrum, ma – molar area, mf – maxillary developed in a transverse row. Two pairs of ventral setae on fringe, MMS – marginal mandibular setae, mp – maxillary each thoracic segment represent so called thoracic leg groups, palpus, pso – posterior spiracular opening, sa – sublabral V1 simple and V2 doubled (Fig. 12). Dorsolateral (DL) and appendage, SAP – subapical seta, sn – sensilla, sp – sternal ventrolateral seta (VL) present near each lateral margin. patch, V – ventral seta, VL – ventrolateral seta. Colouring and ornamentation: Thoracic segments darker than head, especially along anterior margin of prothorax DESCRIPTION OF LARVA and in longitudinal dorsolateral bands but lateral margins of segments more yellow. Ventral surface generally paler. Measurements. – length 6.6-8.1 mm, maximum width 1.6- Ornamentation (Fig. 1) consisting of brownish and usually 2.1 mm (based on 7 larvae). larger scales (plaques) visible in dorsolateral depression on each side as a longitudinal row of 4 plaques, anteriorly two Head. – (Figs 1-2, 12-16): about 1.6 times as long as wide additional plaques shifted more laterally; 3-4 small plaques in dorsal view and even longer in ventral view. Somewhat more or less visible in an irregular transverse row on each arched clypeus well separated by a clypeofrontal suture side at boundary of last fourth of segment. About 18-20 on each side, occupying about central third of head. Small mostly rounded plaques along posterior margin of segment.

242 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Figs. 1–7. Pegadomyia pruinosa (mature larva): 1, Head and thoracic segment 1 in dorsal view; 2, Head and thoracic segment 1 in ventral view; 3, Last two abdominal segments in dorsal view; 4, Last three abdominal segments in ventral view; 5, Ornamentation of abdominal segment 3 in dorsal view; 6, anal segment in dorsal view; 7, Abdominal segment 3 in ventral view. Scales bars = 1.0 mm.

243 Bucánková et at.: Larva and Puparium of Pegadomyia pruinosa

Figs. 8–9. Pegadomyia pruinosa (mature larva). 8, Diagram of setae on lateral wall of abdominal segments 1-7; 9, Mandibular-maxillary complex from inner side.

Figs. 10–11. Pegadomyia pruinosa (penultimate larval instar) in dorsal (10) and ventral view (11). Scale bars = 0.5 mm.

244 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Figs. 12–15. Pegadomyia pruinosa (mature larva). 12, Head and thoracic segment 1 in lateral view; 13, Mouthparts in ventral view; 14, Anterior part of head in lateral view; 15, Anterior part of head in dorsal view.

Figs. 16–19. Pegadomyia pruinosa (mature larva). 16, Head and four anterior body segments in ventral view; 17, Abdominal segment 6 in lateral view; 18, last four abdominal segments in ventral view; 19, Anal slit with crossed setulae.

245 Bucánková et at.: Larva and Puparium of Pegadomyia pruinosa

Figs. 20–23. Pegadomyia pruinosa (mature larva). 20, Pubescent seta on thoracic segment 1; 21, Two-segmented antenna with sensilla; 22, Sublabral appendage; 23, Maxillary palpus.

Plaques on thoracic segment 2 scattered almost circularly in Chaetotaxy (Figs. 3, 4): Three pairs of setae developed in dorsolateral depression (12 plaques on each side) and also transverse rows on dorsal as well as ventral surface, in contrast a transverse row along posterior margin well developed. to thoracic segments, setae gradually shifted to posterior In addition longitudinally oriented pair of elongate-oval, margin of segments 1–7. Dorsal setae convergent, inner large plaques distinct at sides of central third of segment. dorsals (D1) longest, outer dorsal (D3) very short. Length Each of these large plaques with a small rounded plaque of all ventral setae nearly equal, setae divergent. On each in a transverse mid-line. Thoracic segment 3 only with a lateral wall 4 setae visible Figs 8, 17), one dorsolateral (DL), dorsolateral group of plaques but these more transverse, one lateral (L) and two ventrolateral (VL1, VL2). Lateral occupying almost lateral third of segment. Transverse row seta longest, much longer than length of relevant abdominal along posterior margin again well developed. Ventral side of segment. Last abdominal (anal) segment only with one pair thoracic segments with almost same confi guration of plaques of medial dorsal setae. All marginal setae inserted below including large longitudinal plaques of thoracic segment 2 middle of anal segment, second lateral and subapical setae but with two small oval plaques between ventral setae on as long as lateral setae of abdominal segments, fi rst lateral segment 3 on each side. and apical setae distinctly shorter. Insertions of ventral setae placed on oval wall around anal slit, V1 in middle basally, Abdominal segments (Figs. 3–4). – Segments 1–7 each of V2 almost in middle between margin and anal cleft though almost same shape, last abdominal (anal) segment broadly shifted more centrally, V4 and V5 in middle third below anal rounded posteriorly. Cleft of breathing chamber (posterior area. Only convergent V3 placed close to anal cleft. spiracular opening) placed dorsally on anal segment, somewhat convex, partly hidden by a fold of integument Colouring and ornamentation: Ground colour as in thoracic in front of it and somewhat shifted to posterior margin of segments, i.e. brownish, lateral margins and posterior margin segment (placed at beginning of apical fourth); transverse of anal segment more yellow. Dorsal ornamentation on fold distinct only in middle third (or less) of anal segment. abdominal segments 1–7 as described in thoracic segment Longitudinally oval sternal patch (special structure with 2 but dorsolateral groups consisting of 9 differently large unknown function) placed in middle of segment 6 (Fig. 4). plaques and large longitudinal plaques at sides of central Anal slit slightly longer than middle third (Figs. 18–19), third split in middle into 2 elongate scales (Fig. 5). Additional margined with a fringe of long and fine, inner, crossed small plaques developed symetrically below them and a setae. pair of small plaques visible on segments 2–7 in middle or

246 THE RAFFLES BULLETIN OF ZOOLOGY 2009 above it in central position. All abdominal segments 1–7 is fully confi rmed by our examination of younger larvae. The with an additional dorsal row of 22–24 small plaques along larva of the penultimate instar of Pegadomyia pruinosa is anterior margin, 6–8 of them in central third slightly shifted smaller (length: 4.5–5.2 mm, maximum width: 0.8–0.9 mm), posteriorly. Similar row of small plaques along posterior uniformly yellowish, without any cuticular ornamentation margin as well. Ventral side of abdominal segments 1–7 and with simple (not doubled) outer ventral setae on with very characteristic longitudinal and relatively narrow thoracic segments 1 and 2. Mature larvae possess complete plaques (Fig. 7) as on thoracic segment 2. Rows of small mouthparts, well developed ornamentation consisting of plaques along anterior and posterior margin distinct also on enlarged and darkened cuticular plaques and a defi nitively ventral surface. Anal segment (Fig. 6) with relatively small developed, complete armature of constant setae. and mostly rounded plaques, dorsolateral group consisiting of 7 plaques on each side and a pair of broadly separated, The European pachygastrines usually possess 6 pairs of enlarged plaques near anterior margin and two dorsomedial pupal respiratory horns on abdominal segments 1–6 like longitudinal rows (inner between large anterior plaques and in the Beridinae whereas the Sarginae and Clitellariinae dorsal spiracular opening and outer below dorsal setae). display only 4 pairs of pupal respiratory horns on abdominal Ventral surface with 18 small plaques forming a submarginal segments 2–5 (cf. Rozkošný 1982). A tendency to a reduction group on each side and 2 longitudinal rows of plaques along of pupal respiratory horn number will very probably be more the anal elevation on each side. Two pairs of droplike plaques distributed in exotic Pachygastrinae and may even vary in a transverse row near anterior margin. within some species.

DESCRIPTION OF PUPARIUM A KEY TO THE IDENTIFICATION OF ORIENTAL AND EAST PALAEARCTIC Measurements: length 9.1–9.8 mm, maximum width 2.5–2.7 PACHYGASTRINE LARVAE AND PUPARIA mm (based on 4 puparia). Puparium formed from skin of last instar larva. Integument more rigid and somewhat 1 Posterior spiracular opening close to posterior margin of anal more darkened than in larva, mouthparts obliterated and segment, nearly apical in position ...... 2 prothoracic spiracles more sclerotized, crossed setulae along – Posterior spiracular opening placed well before posterior margin inner margin of anal slit invisible. All surface structures of anal segment in dorsal position (Fig. 3) ...... 3 2 Structures bordering anal slit rounded; subapical seta not visible including setae and ornamentation as described in mature in dorsal view ...... Craspedometopon basale (Matsumura) larva. Microscopically short, stalk-like pupal respiratory horns – Structures bordering anal slit subquadrate; subapical seta well on abdominal segments 2–6 placed between dorsolateral and visible in dorsal view ...... lateral setae or even indistinct in some puparia...... Maackiana laminiformis Krivosheina 3 Sternal patch on abdominal segment 6 rounded, placed well in front of transverse row of ventral setae ...... DISCUSSION ...... Gabaza nigrotibialis (Kertész) – Sternal patch on abdominal segment 6 oval, at least touching The mature larva of Pegadomyia is characteristic, fi rst of transverse line of ventral setae (Fig. 4) ...... 4 4 Subapical and apical setae of same length, at least 2/3 as long all, by long lateral setae on all body parts: lateral setae on as anal segment ...... 5 the head, dorsolateral setae on the thoracic segments, lateral – At least one of these setae distinctly shorter (Fig. 3) ...... 8 setae on abdominal segments 1–7 and 2 pairs of lateral setae 5 Subapical and apical setae on anal segment longer than lateral on the anal segment. Similar confi guration of setae is known setae ...... Xylopachygaster mamaevi Krivosheina only in two other pachygastrine genera, Eupachygaster and – All marginal setae of anal segment nearly equal in length .. 6 Zabrachia, distributed in the Nearctic and Palaearctic Regions 6 Three pairs of anterodorsal setae and two pairs of dorsal setae but also in almost all pachygastrine larvae described from on thoracic segment 1 ...... Zabrachia tenella (Jaennicke) South America. However, the elongate sensilla which is – Two pairs of anterodorsal setae and 3 pairs of dorsal setae on developed lateral to the apical antennal segment seems to be thoracic segment 1 ...... 7 7 Dorsal setae on abdominal segments gradually shortened toward unique among the known pachygastrine larvae. On the other lateral margin, i.e. D1 longest ...... hand, a similar slender antennal sensilla is well developed in ...... Zabrachia stackelbergi Krivosheina & Rozkošný all the known aquatic larvae of Odontomyia, Oxycera and – D2 seta on abdominal segments longer than D1 seta ...... Stratiomys from the subfamily Stratiomyinae and Nemotelus ...... Zabrachia minutissima (Zetterstedt) from the subfamily Nemotelinae. The very characteristic 8 Head unusually long, much more than twice as long as broad ornamentation on the body segments, especially the presence basally; marginal setae of anal segment short, barely ¼ as long of a long and slender, longitudinally oriented pair of plaques as abdominal segments ...... on the ventral surface of thoracic segment 2 and each of ...... Pachygaster piriventris Rozkošný & Kovac, 1998 abdominal segments 1–7 is probably autapomorphic. – Head at most twice as long as broad basally; at least some of marginal setae on anal segment longer ...... 9 9 Apical setae on anal segment conspicuously longer than Johannsen (1922) already noticed that the earlier instars subapical setae ...... Ornopyramis tener Krivosheina differ from the fi nal one in mouthparts, details of cuticular – Apical setae distinctly shorter than subapical setae ...... 10 structure and sometimes also in chaetotaxy. This characteristic

247 Bucánková et at.: Larva and Puparium of Pegadomyia pruinosa

10 Lateral setae on abdominal segments longer than length of James, M. T., 1967. A preliminary review of the Argentine genera relevant segment (Figs. 3, 4); antenna with slender sensilla and species of Stratiomyidae (Diptera). Part 2. Pachygasterinae. lateral to apical segment (Fig. 21) ...... Acta Zoológica Lilloana, 21: 95–121. Pegadomyia pruinosa Kertész James, M. T., 1981. Stratiomyidae. In: McAlpine, J. F., B. V. – Lateral setae on abdominal segments at most as long as relevant Peterson, G. E. Shewell, H. J. Teskey, J. R.. Vockeroth, & D. segments; antenna without sensilla ...... 11 M. Wood (eds.), Manual of Nearctic Diptera. Vol. 1. Research 11 Head with conspicuous postocular lobe on each side; subapical Branch Agriculture Canada, Ottawa. 674 pp. setae on anal segment longer than lateral setae ...... Camptopteromyia fractipennis de Meijere Johannsen, O. A., 1922. Stratiomyiid larvae and puparia of the – Head without postocular lobes; subapical setae on anal segment north eastern states. Journal of the New York Entomological shorter than lateral setae ...... 12 Society, 30(4): 141–153 + 2 pls. 12 Two approximated transverse rows of enlarged cuticular plaques, Kertész, K., 1916. Vorarbeiten zu einer Monographie der fi rst consisting of rhomboid and second of transversely oval Notacanthen. XXXVI–XXXVIII. Annales Historico-Naturales or polygonal structures, distinct on abdominal segments below Musei Nationalis Hungarici, 14(1): 123–218. dorsal setae ...... Cechorismenus fl avicornis Kertész Kraft, K. J. & E. F., Cook, 1961. A revision of the Pachygasterinae – Transverse rows of enlarged plaques on dorsal surface of (Diptera, Stratiomyidae) of America North of Mexico. abdominal segments absent ...... 13 Miscellaneous Publications of the Entomological Society of 13 Two intersegmental rows of darkened plaques between thoracic America, 3(1): 1–24. segments 2 and 3 on ventral surface separated by one row of small cuticular plates ...... Krivosheina, N. P., 1965. New data on the taxonomy of ...... Neopachygaster secernibilis Krivosheina dendrophilous chameleon fl ies (Diptera, Stratiomyidae) and of – Intersegmental rows of darkened plaques between thoracic their larvae. Entomologicheskoye obozreniye, 44(3): 652–664. segments 2 and 3 on ventral surface separated by 2 rows of In Russian, English summary. small cuticular plates ...... Krivosheina, N. P., 1975. Novye dannye o ksilofil´nykh ...... Neopachygaster stackelbergi Krivosheina dvukrylykh nasekomykh (Stratiomyidae, Pachygasterinae), razvivayushchikhsya v tugaynoy rastitel´nosti sredney Azii. /New data on xylophilous two-wingled insects (Stratiomyidae, ACKNOWLEDGEMENTS Pachygasterinae) developing in tugai growths of Middle Asia/. Nauchnye doklady vysshey shkoly, Biologicheskiye nauki, 10: This study was supported by the Ministry of Education of 11–17. In Russian. the Czech Republic and the Masaryk University in Brno Krivosheina, N. P., 1976. Xylophilous larvae of the genus (Programme MSM 0021622416). Neopachygaster (Diptera, Stratiomyidae), their relations and biology. Zoologicheskiy zhurnal, 55: 559–565. In Russian, English summary. LITERATURE CITED Krivosheina, N. P., 1977. Xylophilous larvae of the soldier-fl ies of the subfamily Pachygasterinae (Diptera, Stratiomyidae). Blanchard, E. E., 1923. Apuntes sobre dos dipteros argentinos. Entomologicheskoye obozreniye, 56(4): 873–887. In Russian, Physis, 6: 319–323. English summary. Brèthes, J., 1922. Himenópteros y Dípteros de varias precedensias. Krivosheina, N. P., 2002. Review of the xylophilous fl ies of the genus Anales de la Sociedad Cientifi ca Argentina, 93: 119–146. Wallacea (Diptera, Stratiomyidae). Zoologicheskiy Zhurnal, 81(5): 597–607. In Russian, English summary. Brindle, A., 1962. Taxonomic notes on the larvae of British Diptera 7. The genus Pachygaster Meigen (Stratiomyidae). Krivosheina, N. P., 2004. A review of xylobiontic fl ies of genera The Entomologist, March 1962: 77–82. Neopachygaster Austen, Eupachygster Kertész, and Pachygaster Meigen (Diptera, Stratiomyidae) from Russia and neighboring Courtney, G. W., J. B. Sinclair & R. Meier, 2000. Morphology countries. Entomological Review, 84(4): 492–506. and terminology of Diptera larvae. In: Papp, L. & B. Darvas (eds), Contributions to a Manual of Palaearctic Diptera (with Krivosheina, N. P. & A., Freidberg, 2004. New species of special reference to fl ies of economic importance). Science xylophilous soldier-fl ies (Diptera, Stratiomyidae) from Israel. Herald, Budapest. Pp. 85–161. Entomological Review, 84(9): 1036–1042. Dušek, J. & R., Rozkošný, 1975. Revision mitteleuropäischer Krivosheina, N. P. & R. Rozkošný, 1985. Additional notes on Arten der Familie Stratiomyidae (Diptera) mit besonderer Palaearctic Pachygasterinae (Diptera, Stratiomyidae). Acta Berücksichtigung der Fauna der SSR VI. Acta Entomologica Entomologica Bohemoslovaca, 82: 143–149. Bohemoslovaca, 72: 259–271. Krivosheina, N. P. & R. Rozkošný, 1990. Zabrachia stackelbergi James, M. T., 1950. A new Damaromyia, and the larva of D. sp.n., a new species of xylophilous soldier fl y from eastern Asia tasmanica Kertész. (Diptera, Stratiomyidae). Proceedings of the (Diptera, Stratiomyidae). Acta Entomologica Bohemoslovaca, Entomological Society od Washington, 52(6): 312–315. 87: 304–313. James, M. T., 1965. Contributions to our knowledge of the Nearctic Lopes, A. L. F. de, Xerez, R. de, Silva, R. R. da & J. R., Pujol-Luz, Pachygasterinae (Diptera: Stratiomyidae). Annals of the 2006. Descrição dos pupários de Manotes crassimanus James Entomological Society of America, 58(6): 902–908. e Pedinocera longicornis Kertész (Diptera, Stratiomyidae, Pachygastrinae) da Ilha da Marabaia, Mangaritiba, Rio de Janeiro, James, M. T., 1966. A new genus of Pachygastrine Stratiomyidae Brazil. Revista Brasileira de Zoologia, 23(3): 733–739. reared from Cactus (Diptera). Journal of the Kansas Entomological Society, 39: 109–112. Mamaev, B. M., Krivosheina, N. P. & V. A., Potockaya, 1977. Opredelitel´ lichinok khishchnykh nasekomykh – entomofagov

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stvolovykh vrediteley /Key to entomophagous insects feeding Rozkošný, R. & D. Kovac, 2008. A revision of Pegadomyia Kertész upon stem pests/. Nauka, Moskva. 392 pp. In Russian. with descriptions of a new genus and four new species (Diptera, McFadden, M. W., 1967. Soldier fl y larvae in America North of Stratiomyidae). Systematics & Evolution, 39: 171–187. Mexico. Proceedings of the United States National Museum, Rozkošný, R. & M. Kozánek, 2007. A review of the Oriental Culcua Washington, 121(3569): 1–72. with descriptions of seven new species (Diptera, Stratiomyidae). Puloj-Luz, J. R. & R. de Xerez, 1999. The larva of Chalcidomorphina Insect Systematics & Evolution, 38: 35–50. aurata Enderlein 1914 (Diptera: Stratiomyidae) from Ilha da Teskey, H. J., 1976. Diptera larvae associated with trees in North Marambaua, Rio de Janeiro, Brasil. Proceedings of the America. Memoires of the Entomological Society of Canada, Entomological Society of Washington, 101(2): 295–299. 100: 1–53. Rozkošný, R., 1982-1983. A Biosystematic Study of the European Woodley, N. E., 2001. A world catalog of the Stratiomyidae (Insecta: Stratiomyidae (Diptera). Vol. 1. and Vol. 2, Dr. W. Junk, The Diptera). Backhuys Publishers, Leiden, 473 pp. Hague. 401 + 431 pp. Woodley, N. E., 2008. Kerteszmyia, a new genus of Pachygastrinae Rozkošný, R., 1997. Family Stratiomyidae. In: Papp, L. & B. from the Neotropical region (Diptera: Stratiomyidae). Zootaxa, Darvas, (eds.), Contributions to a Manual of Palaearctic Diptera 1746: 39–45. (with specieal reference to of economic importance). Xeres, R. de & J. R., Puloj-Luz, 2001. Description of the larva of Vol. 2. Nematocera and Lower Brachycera. Science Herald, Vittiger schnusei Kertész, 1909 (Diptera: Stratiomyidae) from Budapest. 592 pp. Ilha da Marambaia, Rio de Janeiro, Brazil. Studia Dipterologica, Rozkošný, R. & M. Baez, 1986. Larvae of the Canary Islands 8: 337–341. Stratiomyidae (Diptera). Vieraea, 16: 341–349. Xeres, R. de, Puloj-Luz, J. R. & G. G., Viana, 2002. Descrição da Rozkošný, R. & D. Kovac, 1991. First description of the male and larva de Cosmariomyia argyrosticta Kertész e do pupário de the larva of Camptopteromyia fractipennis de Meijere from Dactylodeictes lopesi Lindner (Diptera, Stratiomyidae). Revista Malaysia (Diptera: Stratiomyidae). Entomologica Scandinavica, Brasileira de Zoologia, 19(3): 747–755. 22: 297–304. Xeres, R. de, Puloj-Luz, J. R. & G. G., Viana, 2003a. Descrição Rozkošný, R. & D. Kovac, 1998. A new species of Pachygaster da larva de Popanomyia femoralis Kertész, 1909 a do pupário (Diptera: Stratiomyidae, Pachygasterinae), from West Malaysia de Engicerus major Lindner, 1964 (Diptera, Stratiomyidae). and Thailand. Studia Dipterologica, 5: 3-12. Revista Brasileira de Entomologia, 47(3): 7474–755. Rozkošný, R. & D. Kovac, 2007. Palaearctic and Oriental species Xeres, R. de, Puloj-Luz, J. R. & G. G., Viana, 2003b. Description of Craspedometopon Kertész (Diptera, Stratiomyidae). of the larva of Psephiocera modesta (Lindner, 1949) (Diptera: Acta Zoologica Academiae Scientiarum Hungaricae, 53(3): Stratiomyidae: Pachygastrinae). Studia Dipterologica, 10: 203–218. 189–193.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 251–254 Date of Publication: 31 Aug.2009 © National University of Singapore

TWO NEW SPECIES OF THE GENUS TACHYDROMIA MEIGEN (DIPTERA: ) FROM MALAYSIA

Igor Shamshev All-Russian Institute of Plant Protection, shosse Podbel’skogo 3, 188620, St. Petersburg – Pushkin, Russia (temporarily at RBINS, Brussels) Email: [email protected]

Patrick Grootaert Department of Entomology, Royal Belgian Institute of Natural Sciences, Rue Vautier 29, B-1000, Brussels, Belgium Email: [email protected]

ABSTRACT. – First data on the genus Tachydromia from Malaysia are provided including two new species for science: T. malaysiensis, new species, T. pahangiensis, new species.

KEY WORDS. – Diptera, Hybotidae, Tachydromia, new species, Malaysia, Oriental.

INTRODUCTION for the antenna follows Stuckenberg (1999); and for the male terminalia follows Sinclair & Cumming (2006). To The present paper is a contribution to the world revision of facilitate observations, the terminalia were macerated in the genus Tachydromia Meigen that was recently initiated hot 10 % KOH and immersed in glycerine. Drawings of by the authors (Shamshev & Grootaert, 2008). The group morphological features were made with a camera lucida is almost worldwide in distribution and currently includes attached to a compound microscope. In description, right 110 species (Yang et al., 2006). Tachydromia radiated in and left side of the male terminalia are based on the the Palaearctic Region with about 73 species known so far unrotated position viewed posteriorly, such that in the (Yang et al., loc. cit). At the moment only 16 species are illustrations the right surstylus appears on the readers left known from the Oriental region (Grootaert & Shamshev, side and vice versa. In Hybotidae, the male genitalia are 2009; Saigusa & Yang, 2002; Shamshev & Grootaert, 2005, rotated to the right, but they are fi gured in their unrotated 2008; Yang & Grootaert, 2006) and all except one are position. present in mountain and submontainous areas mainly on the northern transition zone between the Oriental and Palaearctic regions. Tachydromia luang Shamshev & Grootaert, 2005 SYSTEMATIC ACCOUNT is the exception in that it occurs in mountains as well as tropical lowlands. It is the only Tachydromia known in Tachydromia malaysiensis, new species Singapore so far (Shamshev & Grootaert, 2008) where it is (Figs. 1–3) quite common in secondary forest as well as in mangrove. No Tachydromia species have been reported from Malaysia Material examined. – Holotype – male, MALAYSIA: Pahang, yet and that is why we describe the only two new species we Tanah Rata, 1,460 m, 7 Jan.1990, coll. J. R. Vockeroth [CNC]. could fi nd during our world revision of Tachydromia. They were taken from a mountain in the Cameron Highlands in Diagnosis. – Recognised by yellow body, small palpus Pahang province of Malaysia. bearing very long subapical seta, entirely tomentose thorax, almost entirely yellow legs, wings with faint bands and yellow halters. MATERIALS AND METHODS Description. – Male. Body about 1.6 mm, wing 1.8 mm. This study is based on material housed in the Canadian Head brown. Eyes extending beyond ocellar tubercle and National Collection of Insects, Ottawa, Ontario, Canada almost touching on vertex. Frons short, narrow, pollinose, [CNC]. Terms used for adult structures primarily follow almost parallel-sided. Ocellar tubercle pollinose, ocellars those of McAlpine (1981), although the terminology minute. Occiput entirely pollinose, bearing 2 short closely

251 Shamshev & Grootaert: Two new species of Tachydromia from Malaysia set brownish vertical setae, covered with scattered short Wing normally developed, with two very faint infuscate pale setae longer near mouth-opening. Antenna with broad bands separated throughout. Costal seta absent. Vein scape, pedicel and postpedicel yellow, stylus brown; R1 meeting costa near wing midway. Proximal section postpedicel short, subtriangular; stylus apical, very long, of vein R4+5 considerably longer than Rs. Veins R4+5 and short pubescent. Proboscis yellow. Palpus small, truncate, M1+2 parallel toward wing-apex. Crossveins r-m and bm- yellow, bearing very long black subapical seta, with cu separated. Cells br and bm extending to wing midway. scattered pale yellow setulae. Halter yellow.

Thorax almost entirely yellow, subshining, fi nely tomentose, Abdomen almost entirely yellow, subshining, mostly with prescutellar depression, scutellum and mediotergite short yellowish setulae, tergites broadly brownish yellow somewhat darker. Postpronotal lobe very large, lacking dorsally, sternite 8 with long posteromarginal setae. conspicuous setae. Mesonotum with 2 notopleurals (posterior seta much longer and stronger) and 2 short Terminalia (Figs. 1–3) large, brownish, subshining. Right closely set scutellars (shorter than posterior notopleural cercus with deep apical excision, bearing several moderately seta); acrostichal and dorsocentral setae minute, the former long unmodifi ed setae. Left cercus shorter than right cercus, arranged in 1–2 irregular rows, lacking on prescutellar slightly concave apically, with several unmodifi ed setae depression; the latter uniserial, 1 prescutellar pair somewhat of different lengths. Right epandrial lamella conical, with longer. several long unmodifi ed setae, bearing large subglobular ventral projection. Right surstylus differentiated from Legs long, slender, almost entirely yellow, hind femur epandrium, long, narrow, with several spines on inner face. brownish yellow apically, hind tibia with brown ring on Left epandrial lamella small, with several short unmodifi ed apical 1/6. Fore coxa subshining, with numerous unmodifi ed setae. Left surstylus differentiated from epandrium, with setae anteriorly. Fore femur thickened, with rows of several unmodifi ed subapical setae. short anteroventral and posteroventral yellowish setae. Fore tibia spindle-shaped. Mid femur rather slender, with Female. Unknown. rows of brownish yellow anteroventral and posteroventral spinule-like setae becoming longer basally, bearing 1 Etymology. – The new species is named after Malaysia. long posteroventral seta near base. Mid tibia with hardly prominent ventral spinules (more distinct subapically) but Distribution and seasonal occurrence. – Malaysia. Known with 2 black apical spinules. Hind leg unmodifi ed, without from a single locality in mountains of Pahang Province. The prominent setae. Tarsi of all legs unmodifi ed. record is from the beginning of January.

Figs. 1–3. Tachydromia malaysiensis, new species, male. 1, right epandrial lamella, lateral view, 2, hypopygium, dorsal view, 3, left epandrial lamella, lateral view. Scale 0.1 mm.

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Remarks. – The relationships of T. malaysiensis are unclear ventral spinules, lacking subapical projection. Hind leg very beyond inclusion within the T. luang species group. In the long and slender, without prominent setae. Mid and hind key to Tachydromia species of the Oriental Region the new basitarsi with unmodifi ed setation. species runs to T. luang, which is known from Singapore and Thailand (Shamshev & Grootaert, 2008). Besides distinctive Wing normally developed, almost uniformly brownish differences in the male terminalia T. malaysiensis can be infuscate, darker anteriorly, paler near base. Costal seta readily distinguished from T. luang by entirely yellow fore short. Vein R1 meeting costa somewhat beyond wing tibiae (vs. contrastingly black on apical third in T. luang). midway. Proximal section of vein R4+5 considerably longer

than Rs. Veins R4+5 and M1+2 parallel toward wing-apex. Crossveins r-m and bm-cu separated. Cells br and bm Tachydromia pahangiensis, new species extending to wing midway. Halter with yellowish knob and brownish stem. Material examined. – Holotype – female, MALAYSIA: Pahang, Brinchang, 24 Nov.–2 Dec. 1977, coll. B. Bendell [CNC]. Abdomen black, subshining, with scattered setae longer laterally. Cercus long, slender, brown. Diagnosis. – Recognised by silvery white fl attened setae on occiput, black body and legs, wings almost entirely Male. Unknown. uniformly brownish infuscate and halters with yellow knob. Etymology. – The epithet refers to the type locality, Pahang. Description. – Female. Body about 2.3 mm, wing 2.8 mm. Head black. Eyes extending beyond ocellar tubercle and Distribution and seasonal occurrence. – Malaysia. Known almost touching on vertex. Frons short, narrow, pollinose, from a single locality in Pahang Province. The record is almost parallel-sided. Ocellar tubercle pollinose, ocellars from the end of November to the beginning of December. minute. Occiput entirely pollinose, bearing 2 moderately long closely set black verticals, 2 similar setae and some Remarks. – The relationships of T. pahangiensis are unclear scattered dark setulae on upper part, covered with numerous beyond inclusion within the T. luang species group. In silvery white fl attened setae on lower part closer to neck having silvery white flattened setae on occiput, largely and mouth-opening. Antenna brown, postpedicel short, shining thorax, black legs, almost entirely uniformly subtriangular; stylus apical, very long, short pubescent. brownish infuscate wings and halters with yellow knob Proboscis brown. Palpus small, truncate, transparent, almost the new species can be readily distinguished from all other lacking pubescence, with 1 very long subapical seta and species of the T. luang group, which are currently known some pale yellow setulae. from the Orient (Shamshev & Grootaert, 2008).

Thorax black, prosternum and anterior margin of proepisternum finely greyish tomentose, antepronotum, ACKNOWLEDGEMENTS postpronotal lobe (except outer face), scutum, scutellum, mediotergite, meron (= hypopleuron) and laterotergite (= The authors are indebted to Jeffrey Cumming, Bradley metapleuron) fi nely brownish tomentose, otherwise thorax Sinclair and Scott Brooks (Agriculture and Agri-Food shining. Postpronotal lobe very large, lacking conspicuous Canada, Ottawa) for the loan of specimens used in their setae. Mesonotum with 2 subequally strong, moderately study. Jeff Cumming and Adrian Plant commented on the long black notopleurals and 4 scutellars (apical pair manuscript. shorter than notopleurals, lateral pair minute); acrostichal and dorsocentral setae minute, the former arranged in 3–4 irregular rows, lacking on prescutellar depression; the latter LITERATURE CITED uniserial. Grootaert, P. & I. Shamshev, 2009. First records on Tachydromia Legs long, slender, largely shining, almost entirely black, Meigen and Tachypeza Meigen (Diptera: Hybotidae) from knees of fore legs, hind tibiae broadly before middle (but Viet Nam, with descriptions of four new species. Zootaxa: except narrow space basally), fore and mid tarsomeres in press. 1–2, hind basitarsus (except apex) and most part of hind McAlpine, J. F., 1981. Morphology and terminology – Adults. tarsomere 2 (except apex) yellow. Fore coxa subshining, Pp. 9–63. In: McAlpine, J. F. et al. (eds.), Manual of Nearctic fi nely tomentose anteriorly, shining laterally, with numerous Diptera, Vol. 1, Agriculture Canada, Research Branch, unmodified dark setae anteriorly. Fore femur strongly Monograph 27, 674 pp; Ottawa. thickened, whitish pubescent ventrally, with several black Saigusa, T. & D. Yang, 2002. Empididae (Diptera) from Funiu anteroventral spinules on about basal half. Fore tibia Mountains, Henan, (I). Studia Dipterologica, 9: somewhat spindle-shaped, with row of ventral spinules. 519–543. Fore basitarsus with ventral spinules. Mid femur slender, Shamshev, I. & P. Grootaert, 2005. The genus Tachydromia with rows of black anteroventral and posteroventral setae Meigen (Diptera: Hybotidae) from South East Asia, with the becoming longer basally. Mid tibia with hardly prominent description of three new species. Studia Dipterologica, 12: 109–117.

253 Shamshev & Grootaert: Two new species of Tachydromia from Malaysia

Shamshev, I. & P. Grootaert, 2008. New and little-known species Yang D. & P. Grootaert, 2006. Notes on Tachydromia from of the genus Tachydromia Meigen (Diptera, Hybotidae) from China (Diptera: Hybotidae). Transactions of the American Thailand. Zootaxa, 1830: 21–36. Entomological Society, 132: 133–135. Sinclair, B.J. & J.M. Cumming, 2006. The morphology, higher- Yang D., Zhang K., Yao G. & Zhang J. (2007) World Catalog level phylogeny and classifi cation of the Empidoidea (Diptera). of Empididae (Insecta: Diptera). China Agricultural Zootaxa, 1180: 1–172. University Press, Beijing, 599 pp. Stuckenberg, B. R., 1999. Antennal evolution in the Brachycera (Diptera), with a reassessment of terminology relating to the fl agellum. Studia dipterologica, 6: 33–48.

254 THE RAFFLES BULLETIN OF ZOOLOGY 2009

THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 255Ð277 Date of Publication: 31 Aug.2009 © National University of Singapore

DIVERSITY OF CHELIPODA MACQUART, 1823 (DIPTERA: EMPIDIDAE: HEMERODROMIINAE) IN NORTHERN THAILAND WITH DISCUSSION OF A BIODIVERSITY ‘HOT SPOT’ AT DOI INTHANON

Adrian R. Plant Department of Biodiversity & Systematic Biology, National Museum of Wales, Cathays Park, Cardiff, CF10 3NP, UK

ABSTRACT. – Nine species of Chelipoda Macquart, 1823 (Diptera: Empididae) are described from northern Thailand: C. chaiamnata, new species; C. inthawichayanona, new species; C. kameawuta, new species; C. laisoma, new species; C. manggawna, new species; C. meenamluang, new species; C. nakladam, new species; C. nakropa, new species and C. thaosuranaria, new species. One species, C. macrosceles new species is described from Vietnam and also reported from Thailand. In total, fourteen species of Chelipoda are reported from northern Thailand and an identifi cation key provided. Descriptions of C. fl avida Bru- netti, 1913; C. guangxiensis Yang & Yang, 1986; C. hubeiensis Yang & Yang, 1990 and C. menglunana Grootaert, Yang & Saigusa, 2000 are augmented. Eleven species (including seven endemics) occurred on the mountain Doi Inthanon which was identifi ed as a ‘hotspot’ of Chelipoda diversity. Species richness and abundance increased with altitude and seasonal infl uences on adult phenology were greatest at lower elevations. The uplifting of Doi Inthanon coincided with development of seasonal monsoon patterns and orogenesis of mountain ranges connecting with the eastern Himalaya. It is hypothesised that: (a) seasonal relaxation at higher altitudes provided moist refugia into which Chelipoda and other ombrophilous fauna migrated vertically in response to the intensifi cation of seasonality at lower elevations. Subsequent uplift- ing of Doi Inthanon’s basement well above the present day surrounding area would have isolated these faunal elements and promoted speciation; (b) the mountain may have been colonised from the Himalaya via ‘Palaearctic corridors’ of suitable moist forest habitat along intervening mountain chains.

KEY WORDS. – Diptera, Empididae, Chelipoda, Thailand, new species.

INTRODUCTION terrestrial invertebrates in national parks of Thailand. Sampling effort was concentrated in the following mostly The empidid genus Chelipoda Macquart, 1823, contains 92 northern and north eastern parks (with numbers of Malaise described species distributed across all faunal realms except trap and pan trap samples respectively in parenthesis). the Afrotropical, but little is known of the Asian fauna apart ÐDoi Inthanon (265, 62), Nam Nao (106, 63), Thung from in China where 20 species have been reported (Yang & Salaeng Luang (108, 63), Phu Kradueng (72, 41), Phu Yang, 2004). The present work describes nine new species Ruea (132, 77), Pa Nin Ngam (133, 73), Phu Phan (132, of Chelipoda from northern Thailand, one species from 77), Tat Tone (141, 77), Pha Taem (126, 77) and Khao Vietnam which is also found in Thailand, supplements the Yai (140, 84) [a total of 1,355 Malaise trap and 694 pan descriptions of four previously known species and presents a trap samples were searched for Chelipoda species]. Two key to all the northern Thailand species. The mountain Doi specimens were also included from Khao Phu Ð Khao Inthanon was identifi ed as a hotspot of Chelipoda diversity Ya National Park, in Trang Province, southern Thailand. and aspects of the ecology, altitudinal zonation and origins A total of 923 Thai specimens of Chelipoda resulted. of the mountain’s fauna were investigated. Additionally, 50 specimens from Vietnam belonging to a species also found in the Thailand samples were studied. Repository institutions for material were: Ð IRSNB, MATERIALS AND METHODS Royal Belgian Institute of Natural Sciences, Brussels, Belgium; NMWC, National Museum of Wales, Cardiff, Material used in this study was collected during 2006 and UK; RMNH, Nationaal Natuurhistorisch Museum, Leiden, 2007 as part of a three year project (TIGERÐ Thailand Netherlands; QSBG, Queen Sirikit Botanical Garden, Insect Group for Entomological Research) sampling Chiang Mai, Thailand.

255 Plant: Diversity of Chelipoda in northern Thailand

Morphological terms are essentially those of McAlpine Ð Wing weakly pigmented; if darkened, never with distinct (1981) and Stuckenberg (1999). Interpretation of genitalic subterminal band ...... 2 homology follows Cumming et al. (1995) and Sinclair 2 Legs conspicuously slender; F1 8Ð9x long as wide (Fig. 26) (2000). Colour descriptions refer to ground colour (i.e. not with a single row of denticles between double rows of ventral colour due to pruinosity) unless stated otherwise. Orientation spines ...... C. macrosceles, new species Ð Legs stouter (Figs. 25, 27); F1 at most 6x long as wide, usually is denoted by pd, posterodorsal; pv, posteroventral. C1, C2 strongly infl ated (F1 3.4 Ð4.8x long as wide), a double row of and C3 refer to the front, mid and hind coxae respectively; F ÐF and T ÐT to the corresponding femora and tibiae. denticles between double rows of ventral spines (if only single 1 3 1 3 row of denticles present then F conspicuously infl ated) .. 3 Other abbreviations used are: Ð BP, before present; dc, 1 3 Ground colour of thorax yellow or brownish yellow at least dorsocentral setae; Epan, epandrium; Hypan, hypandrium; on pleura; scutum sometimes darkened or with darker stripes lpo, lower postocular setae; MYA, million years ago; npl, ...... 4 notopleural setae; ocl, ocellar setae; poped, postpedicel; sa, Ð Ground colour of thorax black, at most with propleuron supraalar setae; sct, scutellar setae; upo, upper postocular contrastingly yellowish ...... 12 setae; vtl, vertical setae. 4 Head yellow ...... 5 Ð Head black ...... 6 The front femur bears four rows of setae ventrally 5 Upper occiput, vertex and frons darkened; scutum yellow with comprising two rows of long setae between which is a dark median stripe (Fig. 21) ...... C. fl avida Brunetti double (occasionally single) row of much shorter peg- Ð Upper occiput, vertex and frons yellow; scutum yellow without like setae (Fig. 27). This study employs the term spine dark median stripe ...... C. manggawna, new species to describe setae of the outer rows and denticle to denote 6 Thoracic dorsum brownish or yellowish black ...... 7 the shorter setae between the rows. One or two spines Ð Thoracic dorsum yellow, sometimes with dark median stripe are often present basally and although these are actually ...... 9 a continuation of the av or pv series of spines, they are 7 Front coxa without distinct anterobasal spine. Antenna with regarded separately as ‘basal spines’ because they are basal segments dark reddish yellow, not contrasting strongly positioned basally to the major quadruple rows of setae. For with dark postpedicel ...... C. guangxiensis Yang & Yang those species having two rows of denticles placed between Ð Front coxa with distinct anterobasal spine. Antenna with basal two rows of spines, the femoral formula (Plant, 2007) is segments yellowish, contrasting with dark postpedicel ...... 8 employed to describe their position and abundance. This 8 Scutum diffusely edged paler brown laterally, not distinctly records the median number and statistical range of spines contrasting with darker brown central area (Fig. 23) ...... or denticles in each row starting from the most anterior ...... C. nakropa, new species (mid elevation morph) Ð Scutum sharply edged yellowish lateral to line of dorsocentrals, and working posteriorly. Thus a femoral formula of 5(4Ð the yellow margins contrasting with central broad, almost 5)/22(19Ð26)/14(12Ð18)/4(4Ð5) +1 indicates that there are blackish area (Fig. 22) ...... 5 (range 4Ð5) av spines, 22 (range 19Ð26) av denticles, 14 ...... C. nakropa, new species (high elevation morph) (range 12Ð18) pv denticles, 4 (range 4Ð5) pv spines and 9 Scutum more or less wholly yellow ...... 10 one basal spine. Ð Scutum yellow with dark median stripe ...... 11

10 Front coxa with distinct anterobasal spine. F1 with single row In addition to full locality / date / collector data, labels for of denticles. Front tarsomeres 2 and 3 distinctly spinose ...... material collected by the TIGER Project has a unique data ...... C. kameawuta, new species code (prefi xed ‘T’) which is quoted on the label and used Ð Front coxa without distinct anteroventral spine. F1 with double administratively within the TIGER Project. row of denticles. Front tarsomeres 2 and 3 not distinctly spinose ...... C. thaosuranaria, new species 11 Scutum with narrow dark median stripe (Fig. 24). A contrasting TAXOMOMY deep black mark between and behind front coxae on av margin of katepisternum ...... C. chaiamnata, new species Chelipoda Macquart, 1823 Ð Scutum with broader dark median stripe. Area between and behind front coxae yellow, not contrasting with surroundings Diagnosis. – A characteristic genus of the Empididae ...... Chelipoda species D subfamily Hemerodromiinae with raptorial forelegs 12 Propleuron blackish (at most faintly yellowish), not contrasting distinctly separated from the mid legs and fore femur with rest of pleura ...... 13 bearing distinct rows of setae ventrally (Figs. 25Ð27). Ð Propleuron yellowish or reddish, contrasting with rest of black Chelipoda is distinguished from other southeast Asian pleura ...... 14 13 Thoracic setae and spines on F dark. Male sternites 7 & 8 Hemerodromiinae by the combination of (1) Postpedicel 1 with sparse black setae ...... C. hubeiensis Yang & Yang longer than wide, stylus longer (2) Katatergital setae present Ð Thoracic setae and spines on F1 yellow. Male sternites 7 & 8 (3) Male genitalia strongly refl exed anteriorly (4) Cell dm with numerous yellow setae (Fig. 11) ...... closed (crossvein dm-cu present) (5) Anal vein (A2+CuA2) ...... C. meenamluang, new species present (6) Cell br usually longer than cell bm, crossveins 14 Front coxa without distinct anterobasal spine. Posterior dc (in closing them not closely aligned (Fig. 28). line with npl) about as strong as anterior dc ...... C. nakladam, new species Ð Front coxa with distinct anterobasal spine. Posterior dc (in line Key to species of Chelipoda from Northern Thailand with npl) minute, much smaller than anterior dc ...... 15 15 Male cercus with strong pointed ad process (Fig. 4). Female 1. Wing with strong black subterminal band commencing at apex basal antennal segments yellowish ..... C. inthawichayanona, of cell dm leaving apex of wing clear ...... new species ...... C. menglunana Grootaert, Yang & Saigusa Ð Male cercus with strong pointed ad process and lower less pointed lobe (Fig. 8) ...... C. laisoma, new species

256 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Chelipoda chaiamnata, new species Female. Similar to male; antenna with poped slightly (Figs 1, 24) longer, 2.8x long as wide.

Material examined. – Holotype. Male, THAILAND: Loei, Phu Legs similar to male, F1 slightly more infl ated; femoral Ruea National Park, Nature Trail, 17¡30.740'N 101¡20.650'E, formula 5(5Ð5)/22(20Ð24)/16.5(15Ð17)/5(4Ð5) +1Ð2, 1,353 m, Malaise trap, coll. N. Jaroenchai, 26 Sep.Ð2 Oct.2006 usually only one strong basal spine, other very weak. (QSBG, T834).

Paratypes. One male, same data as holotype (NMWC); Cercus yellow, slightly elongated. 1 male, 19Ð26 Sep.2006 (QSBG, T831): Chiang Mai, Doi Inthanon National Park, Campground Pond, 18¡32.657'N, Etymology. – The specifi c epithet derives from the Thai 98¡31.482'E, 1,200 m, Malaise trap, coll. Y. Areeluck, word, chai-am-nat (domineering), in reference to supposed 2 females, 2Ð10 Nov.2006 (QSBG & NMWC, T831). fi erce predatory behaviour inferred from the presence of strongly raptorial front legs in this species. Used as a noun Diagnosis. – Black head. Yellow thorax with narrow in apposition. median stripe on scutum and a contrastingly deep black marking between and behind front coxae. Remarks. – Known only from Loei and Chiang Mai provinces from rather dry seasonal forest biotopes between Description. – Male. Body length 3 mm. Head black with 1,200 and 1,353 m from September to November. paler dust; ocl, vtl and upper upo strong, yellowish brown; other upo blackish, small; lpo pale; a few pale hairs behind mouth. Antenna with basal segments yellow; poped black, Chelipoda fl avida Brunetti, 1913 2.5x long as wide; stylus black, rather more than 2x long (Fig. 2, 21) as poped. Mouthparts brownish, proboscis black. Phyllodromia fl avida Ð Brunetti, 1920: 368Ð369. Thorax clear yellow, narrow median stripe on scutum, broader stripe on mediotergite and base of scutellum dark Material examined. – THAILAND, Chiang Mai, Doi Inthanon brown (Fig. 24). Area between and behind front coxa on National Park, Campground Pond, 18¡32.40'N 98¡31.80'E, 1,200 av margin of katepisternum contrastingly deep black. Setae m, Malaise trap, coll. Y. Areeluck: 2 males, 26 Oct.Ð2 Nov.2006 (NMWC, T379); 5 females, 2Ð10 Nov.2006 (NMWC, T385); 4 yellow; two dc (including one level with npl) upper npl, sa males, 3 females, 10Ð17 Nov.2006 (NMWC, T1916); 7 males, and sct all strong; otherwise only minute hairs posteriorly 6 females, 17Ð24 Nov.2006 (NMWC, T1862); 1 male, 8Ð15 on scutum, pospronotum and lower notopleural area. Dec.2006 (QSBG, T1879); 1 female, 22Ð29 Dec.2006 (QSBG, T1889); 1 female, 29 Dec.2006Ð5 Jan.2007 (QSBG, T1895); 1

Legs yellow, tarsomeres 4Ð5 obscurely darker. C1 0.85x as male, 1 female, 5Ð12 Jan.2007 (QSBG, T1917): Check Point 2, long as thorax, anterior ciliation of small setulae yellow, no 18¡31.554'N 98¡29.940'E, 1,700 m, Malaise trap, coll. Y. Areeluck, 1 male, 2Ð8 Jul.2006 (QSBG, T56); 1 male, 4 females, 15Ð22 strong anterobasal seta. F1 slightly longer than C1, infl ated, 3.7Ð3.9x as long as wide, widest 0.3Ð0.4 from base; femoral Jul.2006 (QSBG, T73); 1 female, 9Ð16.Aug.2006 (QSBG, T180); formula approximately 5(5Ð5)/20.5(20Ð23)/17(15Ð17)/5(5Ð 3 males, 9 females, 16Ð24.Aug.2006 (NMWC, T187); 1 male, 2 females, 24Ð30 Aug.2006 (QSBG, T232); 6 females, 12Ð19 6) +2Ð4 (Table 1); usually only one strong basal spine, Oct.2006 (NMWC, T371); 4 females, 19Ð26 Oct.2006 (QSBG, others very weak and contiguous with av and pv series of T377); 6 females, 26 Oct. Ð2 Nov.2006 (QSBG, T383); 3 males, 4 spines; denticles black, spines yellow to yellowish black. females, 2Ð10 Nov.2006 (QSBG, T389); 1 female, 17Ð24 Nov.2006 (QSBG, T1864); 3 males, 9 females, 24 Nov.Ð1 Dec.2006 (QSBG, Abdomen black, yellowish ventrally; tergite 8 reduced, T1870); 1 male, 7 females, 15Ð22 Dec.2006 (NMWC, T1886); 6 strongly sclerotized; sternites 7 and 8 with distinct setae females, 22Ð29 Dec.2006 (QSBG, T1891); 2 males, 9 females, 29 on posterior margins and ventrally. Epan and Hypan fused Dec.2006Ð5 Jan.2007 5 females, 5Ð12 Jan.2007 (NMWC, T1913); 2 (Fig. 1), rather hemispherical in lateral view, brownish females, 2Ð9 Feb.2007 (QSBG, T1793); 1 female, 16Ð23 Feb.2007 yellow becoming darker ventrally and posteriorly, bearing (NMWC, T1805); 1 female, 23 Feb.Ð2 Mar.2007 (QSBG, T1775); 1 female, 29 Apr.Ð6 May.2007 (QSBG, T1857): Summit Marsh, distinct setae posteriorly; left and right lamellae narrowly 18¡35.361'N, 98¡29.157'E, 2,500 m, pan trap, coll. Y. Areeluck, 1 separated by unpigmented membrane. Cercus fused with female, 28 Feb.2007 (QSBG, T1767). Trang, Khao Phu Ð Khao Ya Epan, yellowish, somewhat darker basally with long National Park, 7¡33.038'N 99¡47.369'E, 75 m, Malaise trap, coll. anteriorly directed digitiform process bearing long erect M. Sharkey, 2 females, 5Ð7 Sep.2005 (NMWC, T1902). Loei, Phu setae above and somewhat shorter more decumbent setae Ruea National Park, Malaise trap, coll. N. Jaroenchai; Nature Trail, below. Subepandrial process greyish yellow, a minute 17¡30.740'N 101¡20.650'E, 1,353 m, 1 male, 26 Sep. Ð2 Oct.2006 upturned dorsal ‘tooth’ apically. Phallus yellow apically, (NMWC, T834); Sa Sawan, 17¡30.735'N 101¡20.601'E, 1,352 m, darker basally, reaching almost to apex of subepandrial 1 male, 26 Sep. Ð2 Oct.2006 (NMWC, T835). process; apicolaterally with four or fi ve minute tubercles each bearing a minute short spine-like seta. Diagnosis. – Yellow species with dark median stripe on scutum and rather slender legs. Head yellow, darker on Wing membrane faintly yellowish; veins yellowish. upper occiput, vertex and frons. Squamae with dark yellow fringes. Halter whitish yellow.

257 Plant: Diversity of Chelipoda in northern Thailand u. 1 16 1 6 1 1 12 16 1 6 1 11 1 11 1 13 1 17 1 13 2Ð4 12 2Ð4 12 4Ð6 7 1Ð2 13 1Ð2 10 1Ð2 13 1Ð2 1Ð2 17 13 1Ð2 10 1Ð2 14 basals n theses) and standard 5(4Ð5) pv spines 4(4Ð4) [0] 4(4Ð4) [0] 4(4Ð4) [0] 4(4Ð4) [0] 5(5Ð6) [0.34] 5(5Ð7) [0.69] 4(4Ð5) [0.41] 5(4Ð5) [0.53] 6(5Ð7) [0.73] 5(5Ð6) [0.47] 4(3Ð4) [0.41] 4(4Ð5) [0.31] 4(3Ð4) [0.48] 5(5Ð6) [0.50] 5(5Ð6) [0.48] 5(4Ð5) [0.49] 5(4Ð5) [0.51] 5(4Ð6) [0.55] 8(8Ð11) [1.01] viations: M, male; F, female; u., unknown. pv denticles 14(13Ð16) [1.03] av denticles 22(20Ð26) [2.0] 18(15Ð23) [2.31] 14(12Ð17) [1.60] 16(14Ð18) [1.11] 13(11Ð15) [1.09] 19(19Ð20) [0.52] 15(12Ð16) [1.38] 20(18Ð23) [1.60] 12(10Ð13) [1.11] 20(17Ð22) [1.44] 13.5(11Ð16) [1.42] 20(18Ð25) [2.45] 15(13Ð17) [1.32] 18(15Ð21) [1.97] 15(12Ð17) [1.76] 23(22Ð25) [1.09] 16.5(15Ð17) [0.82] 24(21Ð27) [2.23] 14(11Ð16) [1.37] 23(18Ð25) [2.18] 13(11Ð16) [1.58] 21(19Ð23) [1.12] 22(19Ð24) [1.53] 15(14Ð17) [1.05] 15(13Ð17) [1.15] 20(17Ð25) [2.76] 24(21Ð27) [1.76] 14(12Ð19) [1.97] 16(14Ð18) [1.45] 24(19Ð28) [2.48] 14(14Ð20) [1.83] 22(19Ð26) [2.13] 14(12Ð18) [1.86] 19(15Ð21) [1.75] 14(14Ð22) [2.39] 17(15Ð19) [1.12] 13(12Ð15) [1.07] av spines 5(5Ð5) [0] 5(5Ð5) [0] 5(5Ð5) [0] 5(5Ð5) [0] 5(5Ð5) [0] 5(5Ð6) [0.33] 5(5Ð6) [0.32] 5(4Ð5) [0.33] 5(4Ð5) [0.32] 5(5Ð6) [0.27] 21.5(20Ð24) [1.49] 15(14Ð18) [1.09] 6(6Ð7) [0.45] 5(5Ð6) [0.31] 5(4Ð5) [0.42] 6(6Ð7) [0.49] 6(5Ð6) [0.42] 5(4Ð6) [0.55] 5(5Ð6) [0.41] 5(4Ð5) [0.39] 5(5Ð6) [0.48] 7(5Ð8) [0.90] F F 4.5(4Ð5) 21.5(20Ð25) 14.5(14Ð16) 5(4Ð5) 4 2 F F F F 5(5Ð5) 23(23Ð23) 16(15Ð17) 4(4Ð4) 3 1 F 5(5Ð5) 22(20Ð24) 16.5(15Ð17) 5(4Ð5) 4 1Ð2 F F F F F M 5(4Ð5) 18(15Ð18) 14(14Ð15) 5(506) 2Ð4 3 M 5(4Ð5) 18(15Ð18) 14(14Ð15) 5(506) 2Ð4 M M M M M M 5(5Ð5) 20.5(20Ð23) 17(15Ð17) 5(5Ð6) 2Ð4 4 M 5(5Ð5) 20.5(20Ð23) 17(15Ð17) 5(5Ð6) 2Ð4 M M M M M M Sex F u. u. u. u. u. u. u. F

avida

Chelipoda thaosuranaria

Chelipoda meenamluang Chelipoda laisoma

Chelipoda nakladam Chelipoda inthawichayanona Chelipoda hubeiensis Chelipoda chaiamnata Chelipoda guangxiensis

Chelipoda manggawna (high elev. morph) (mid elev. morph) Chelipoda nakropa Chelipoda nakropa Chelipoda nakropa

Chelipoda fl

Chelipoda menglunana Table 1. Femoral formula of Chelipoda species having four rows setae on front femur. The median number in each series is followed by the range (in paren deviation [in brackets]; n = number of femora sampled. Standard was not calculated for values less than 6. Abbre Species

258 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Description. – Male. Body length 3.0Ð3.5mm. Head yellow reported from the north (Chiang Mai), north eastern ( Loei) becoming darker dorsally on upper occiput, vertex and and southern (Trang) provinces of Thailand. C. fl avida was frons, ocellar protuberance black; setae black, similar to abundant on Doi Inthanon, mostly in mid elevation forest C. manggawna new species. Antenna with basal segments from 1,200Ð1,700 m for most of the year with a major yellow; poped 2.5Ð3.0× long as wide, dark brown; stylus emergence peak from October Ð January and a lesser peak 2.0Ð2.5× long as poped, brown (yellowish white in some in July and August. lights). Mouthparts yellowish but labellum black.

Thorax (Fig. 21) yellow to brownish yellow, pleura paler; Chelipoda guangxiensis Yang & Yang, 1986 postpronotal area and mediotergite often darkened; scutum (Fig. 3) with dark median stripe (usually strongest anteriorly but very variable) and indications of sublateral stripes Material examined. – THAILAND, Loei, Phu Kradueng National posteriorly. Chaetotaxy similar to C. manggawna new Park, Malaise and pan traps, coll. Thanongsak Srisa-ad, savannah species, all setae black. in pine forest, 16¡53.092'N 101¡47.413'E, 1,257 m, 1 male, 29Ð30 Oct.2006 (QSBG, T1214); 1 male, 2Ð3 Jan.2007 (QSBG, T1218); 1 female, 9Ð16 Jan.2007 (QSBG, T1226). Loei, Phu Ruea National Legs yellow, tarsomeres 4Ð5 darker. C 0.95Ð1.0 as long as 1 × Park, pan trap, coll. P. Tumtip: Ma Kraow Ditch, 17¡29.652'N thorax; rather slender, 9.5x as long as wide, anterobasal setae 101¡21.020'E, 1,167 m, 1 female, 10Ð11 Nov.2006 (QSBG, not distinguished from regular row of yellowish anterior T1113): Pan Hin Khan Maak Ditch, 17¡30.042'N 101¡20.474'E, setulae. F1 slightly longer than C1, moderately slender, 6× as 1,219 m, pan traps, coll. P. Tumtip, 1 male, 5Ð6 Feb.2007 long as wide, rather evenly infl ated below, widest 0.4 from (NMWC, T1698); 1 female, 7Ð8 Feb.2007 (NMWC, T1700); 1 base; femoral formula 5(5Ð5)/22(19Ð26)/14(12Ð18)/4(4Ð4) male, 9Ð10 Feb.2007 (NMWC, T1702). Nakhon Nayok, Khao Yai +1 (Table 1), denticles black; spines yellowish or yellowish National Park, nature trail in secondary moist evergreen forest, black, rather evenly spaced, becoming rather longer basally; 14¡24.515'N 101¡22.432'E, 750 m, Malaise trap, coll. P. Sandao, 1 female, 26 Aug.Ð2 Sep.2006 (NMWC, T409). basal spine distinct. T1 short, less than 0.7× as long as F1. Diagnosis. – Thorax dark dorsally, yellowish on pleura. Abdomen brown, paler ventrally; tergites 7 and 8 reduced; Head black. C without distinct anterobasal setae. Antennae apical abdominal segments with only short setae. Epan and 1 with basal segments dark reddish yellow, not contrasting Hypan fused (Fig. 2), erect, narrowly subrectangular in strongly with poped. lateral view, yellowish brown, only small setae posteriorly, left and right lamellae very narrowly separated my Description. – Male. Body length 2.5 mm. Head black unpigmented membrane (hardly visible in unmacerated with paler dusting. Stronger setae black including ocl, vtl specimens). Cercus fused with Epan, brownish yellow, and upper upo; other upo and lpo fi ne and paler; a patch bilobed; upper lobe elongate digitiform, covered with of fi ne pile behind mouth. Basal antennal segments dark numerous distinct setae of which three in distal part rather reddish brown; poped greyish black, 2× long as wide; stronger and more erect, apically with rather dense ‘brush’ stylus brown to yellow (depending on light), 2.5Ð3.0× long of minute upswept setulae; lower lobe emerging from inner as poped. Mouthparts yellowish with greyish labellum and face, very slender and gradually curved, yellowish with darker proboscis. darker broader tip. Subepandrial process and postgonite slender, inconspicuous. Phallus broad, yellowish, sharply Thorax with pleura yellow including most of laterotergite; minutely upcurved apically with a small recurved dorsal scutum, scutellum and mediotergite dark yellowish black. ‘beak’ subapically. All setae black; anterior dc and upper npl strong; mid dc (in line with npl) and posterior dc (near posterior margin of Wing membrane faintly greyish, veins brown. Squamae scutum) very fi ne; lower npl very fi ne, hardly stronger than yellow. Halter pale brown. scattering of fi ne setulae behind postpronotum; sa small. Female. Similar to male; antenna with poped almost 3x Legs dark yellow, tarsomeres 4Ð5 darker, F rather brownish long as wide, stylus 2.0Ð2.5× as long. 1 at extreme apex. C1 0.90Ð0.95× as long as thorax; rather stout, 6× as long as wide, narrowing slightly apically; no F slightly stouter; femoral formula 5(4Ð5)/24(19Ð28)/16(14Ð 1 strong anterobasal seta. F slightly longer than C , distinctly 20)/4(4Ð4). 1 1 infl ated, 4× as long as wide, widest 0.3 from base; femoral formula 5(5Ð5)/23(22Ð25)/16.5(15Ð17)/4(3Ð4) +1 (Table Abdomen brown, yellowish ventrally with sternite 8 brown, 1), spines yellow, denticles black; basal spine distinct, more rather elongate. Cercus elongate. or less contiguous with series of av spines.T1 0.72Ð0.75× long as F . Remarks. – Thai specimens agree with the description 1 and habitus fi gure in Brunetti (1920) although the male Abdomen brown dorsally, paler ventrally; tergites 6 and genitalia have not previously been fi gured and it has not 7 with posterior margin concave; tergite 8 considerably been possible to examine the type material. The species is reduced, distinctly narrowed dorsally. Subterminal tergites known from north eastern , the western slopes of the and sternites lacking strong setae. Epan and Hypan (Fig. 3) Tenasserim Mountains in (Burma) and is here

259 Plant: Diversity of Chelipoda in northern Thailand

Figs. 1Ð6. Male genitalia of Chelipoda species in lateral view: 1. C. chaiamnata new species; 2. C. fl avida Brunetti; 3. C. guangxiensis Yang & Yang; 4. C. inthawichayanona new species: 5Ð6 C. hubeiensis Yang & Yang; 5. typical form; 6. variant (outline only).

260 THE RAFFLES BULLETIN OF ZOOLOGY 2009 fused, brown, elongate smoothly trapezoid in lateral view, Falls, 18¡32.311'N 98¡36.048'E, 700 m, Malaise trap, 2 females, left and right lamellae narrowly separated by unpigmented 6Ð13 Sep.2006 (QSBG, T242). Chaiyaphum, Tat Tone National membrane. Cercus fused with Epan, brown basally with Park; dry dipterocarp forest, 15¡59.037'N 102¡2.103'E, 250 m, single long broad yellowish lobe bearing series of fine Malaise trap, coll. M. Ngoychanse, 2 females, 21Ð28 Jun.2006 (NMWC, T24); Phu hang sing, 15¡58.723'N 102¡02.231'E, 290 strong setae dorsally. Subepandrial process yellowish, m, Malaise trap, coll. T. Jaruphan & O. Budsawong, 4 females apically blackish, rather broad with apex narrowed and (NMWC, T226). strongly upcurved. Phallus yellow, somewhat sinuous apically. Diagnosis. – Head and thorax black including propleuron.

Thoracic setae and spines on F1 dark. Wing membrane faintly brown, veins brown. Squamae with black fringes. Halter greyish brown. Description. – Male. Body length 2.5Ð3.0 mm. Head black with paler dusting; vt and ocl strong, black; upper upo distinct, Female. Head and thorax similar to male. Legs similar lower upo smaller and lpo virtually absent with very little fi ne to male, femoral formula approx. 5/23/16/4 +1. Cercus pile behind mouth. Basal antennal segments yellowish; poped elongated, yellow. dirty yellow, darker apically, about 1.8x long as wide, stylus 2.5× as long. Palp pale with strong dark terminal seta. Remarks. – Previously known only from Guangxi, China (Yang & Yang, 1986), this species is now reported from the Thorax black, extensively dusted; all setae black including sandstone mesa formations in Thailand’s Loei province at two dc, one npl and one sa all strong; otherwise with only Phu Kradueng and Phu Ruea and from Khao Yai in Nakhon small hair like setae on humeral and posthumeral area and Nayok. Adults were caught at elevations from 750Ð1,257 on scutum posteriorly m between late October and early February and again in August. Legs yellow, tarsomeres 5 darker. C1 0.8× as long as thorax, no distinct anterobasal seta, all setulae small becoming

longer on distal half and quite long anteroapically. F1 1.1× Chelipoda hubeiensis Yang & Yang, 1990 as long as C1, distinctly inflated, 3.8× as long as wide, (Figs. 5, 6, 28) widest 0.4 from base; femoral formula 6(6Ð7)/18(15Ð 21)/15(12Ð17)/6(5Ð7) +1Ð2 (Table 1), spines and denticles Material examined. – THAILAND, Phetchabun, Nam Nao National black, av and pv spines somewhat longer basally, regularly Park, helicopter landing ground, 16¡43.156'N 101¡35.118'E, 890 spaced with smaller basal spine contiguous with and m, pan trap, coll. N. Hongyothi: 1 male, 2 females, 4Ð5 Jul.2006 (QSBG, T262). Chiang Mai, Doi Inthanon National Park, coll. indistinguishable from av series. T1 0.75× as long as F1. Y Areeluck: Kew Mae Pan, 18¡33.163'N 98¡28.8'E, 2,200 m, Malaise trap, 9 females, 2 females, 24Ð30 Aug.2006 (QSBG, Abdomen blackish. Tergite 6 with a few strong dark T233); 1 male 13Ð21 Sep.2006 (NMWC,T251); 5 females, 21Ð27 seta dorsally on posterior margin. Tergite 8 very narrow. Sep.2006 (QSBG, T344); 4 females, 27 Sep. Ð5 Oct.2006 (QSBG, Genitalia blackish, darker on apex of subepandrial process T350); 13 females, 5Ð12 Oct.2006 (NMWC, T364); 12Ð19 and with externally visible part of phallus yellow. Epan and Oct.2006 (NMWC, T370); 1 male, 7 females, 19Ð26 Oct.2006 Hypan fused, rather rounded in lateral view (Fig. 5), bearing (QSBG, T376); 4 females, 26 Oct. Ð2 Nov.2006 (QSBG, T382); scattered dark setae posteriorly; left and right lamellae 6 females, 2Ð10 Nov.2006 (NMWC, T388): Kew Mae Pan Trail, broadly separated by unpigmented densely micropilose 18¡33.162'N 98¡28.810'E, 2,200 m, Malaise trap,1 female, 24 Nov.Ð1 Dec.2006 (QSBG, T1866); 1 female, 1Ð8 May.2007 membrane (in many specimens the membranous and (QSBG, T1824); 1 male, 2 females, 8Ð15 May.2007 (QSBG, less strongly sclerotized regions partially collapse and T1829): Summit Forest, 18¡35.361'N 98¡29.157'E, 2,500 m the genitalia appear more pointed apically in lateral Malaise trap, 1 male, 9Ð16 Aug.2006 (QSBG, T178); 2 males, view (Fig. 6)). Cercus fused with Epan+ Hypan, bluntly 1 female, 16Ð24 Aug.2006 (QSBG, T185);3 females, 24Ð30 pointed, irregularly triangular, a regular series of erect dark Aug.2006 (QSBG, T235); 1 female, 30 Aug. Ð6 Sep.2006 (QSBG, setae dorsally and numerous fi ne yellowish setae below. T241); 1 female 6Ð13 Sep.2006 (QSBG, T247); 1 male, 3 females, Subepandrial process sharply projected anteriorly, rather 13Ð21 Sep.2006 (NMWC & QSBG, T253); 2 females, 21Ð27 broad, sharply upwardly curved apically. Phallus sharply Sep.2006 (QSBG, T346); 5 females, 27 Sep.Ð5 Oct.2006 (NMWC, reflexed anteriorly, basal section of anterior loop lying T352); 2 females, 15Ð22 Apr.2007 (QSBG, T1844); 4 females, 17Ð18 Apr.2007 (NMWC, T1834): Summit Marsh, 18¡35.361'N beneath a triangular unpigmented membrane (an anterior 98¡29.157'E, 2,500 m, Malaise trap, 1 male, 2 females, 2Ð9 extension of the medial membrane separating the lateral Aug.2006 (QSBG, T124); 6 males, 3 females, 9Ð16 Aug.2006 lamellae), with a distal loop emerging near base of cercus; (NMWC, T177); 5 males, 7 females, 16Ð24 Aug.2006 (NMWC, apex tightly confi ned between subepandrial processes. T184); 4 males, 6 females, 24Ð30 Aug.2006 (NMWC, T234); 1 male, 7 females, 30 Aug.Ð6 Sep.2006 (NMWC, T240); 5 females, Wing membrane clear or faintly brownish; veins yellowish 13Ð21 Sep.2006 (QSBG, T252); 2 females, 21Ð27 Sep.2006 brown, paler basally (Fig. 28). Squamae with black fringes. (NMWC, T345); 1 male, 27 Sep. Ð5 Oct.2006 (QSBG, T351); Halter greyish white. 1 male, 16Ð23 Mar.2007, (QSBG, T1812); 1 male, 23 Mar.Ð1 May.2007 (QSBG, T1818); 1 male, 4 females, 15Ð22 Apr.2007 (QSBG, T1840); 2 males, 11 females, 22Ð29 Apr.2007 (QSBG, Female. Similar to male but antenna with stylus rather T1846); 6 males, 4 females, 1Ð8 May.2007 (NMWC, T1823); 3 longer than in male, almost 3× long as poped. Upper upo males, 4 females, 8Ð15 May.2007 (QSBG, T1828): Vachiratharn rather stronger. Thorax with hair like setae on humeral and

261 Plant: Diversity of Chelipoda in northern Thailand

posthumeral areas rather stronger though still very small. Legs yellow, tarsomeres 3 apically and 4Ð5 darker; F2, F3

and sometimes T2 and T3 obscurely infuscated. C1 as long

C1 with anterior setulae less strongly developed and F1 as thorax, 1Ð2 distinct short anterobasal setae clearly much slightly larger and stouter than in male, widest 0.4 from stronger than anterior ciliation of minute setulae. F1 1.2× base; femoral formula 5(5Ð6)/21.5(20Ð24)/15(14Ð18)/5(5Ð as long as C1, moderately infl ated, 4.8× as long as wide, 6) +1, basal spine usually weaker than in male. Cercus widest 0.3Ð0.4 from base; femoral formula 5(5Ð5)/20(17Ð moderately long. 22)/13.5(11Ð16)/4(4Ð4) +1 (Table 1), spines dark but basal

spine sometimes yellowish, denticles black. T1 0.65Ð0.7×

Remarks. – This species was described from Wudangshan as long as F1. Mountain, Hubei, China (Yang & Yang, 1990) and is here reported from Chiang Mai and Petchabun provinces Abdomen dark brown; genitalia with fused Hypan + Epan in Thailand. The male genitalia of Thai specimens agree (Fig. 4) black, rather yellowish black above, slightly with Fig. 1 in Yang & Yang (1990) although the thoracic produced and bluntly pointed posteroapically, bearing only setae are black rather than yellow and in the key of Yang short dark setae; posterior mid line rather less strongly & Yang (2004) Thai specimens run to C. lyneborgi Yang sclerotized. Cercus largely black with strong pointed ad & Yang, 1990 (described from a single female and hence process and much shorter, blunter av process; strong setae probably unrecognizable). However, the colour of thoracic dorsally and on inner lower surface. Subepandrial process setae is rather variable in many Chelipoda spp. and the black, narrow, anteriorly directed, upturned distally. Phallus determination of Thai specimens as C. hubeiensis is strongly narrow, yellowish, sharply refl exed anteriorly. supported by genitalic characters. In Thailand, this species was abundant on Doi Inthanon in the upper wet forest zone Wing membrane faintly brownish; veins brownish, from 2,200Ð2,500 m. There were two peaks of abundance becoming yellowish at extreme base. Squamae with dark in August to November and between April to May. fringes. Halter grey.

Female. Similar to male but antenna with poped shorter and Chelipoda inthawichayanona, new species broader than in male, 2.5× long as wide (Fig. 4)

Legs similar to male but sometimes rather darker; F1 Material examined. – Holotype. Male, THAILAND: Chiang slightly broader, 4.1× as long as wide, femoral formula 5(4Ð Mai, Doi Inthanon National Park, Summit Forest, 18¡35.361'N 5)/20(18Ð25)/15(13Ð17)/4(4Ð4) +1Ð2. Cercus elongate. 98¡29.157'E, 2,500 m, Malaise trap, coll. Y. Areeluck, 16Ð24 Aug.2006 (QSBG, T185). Etymology. – The specific epithet commemorates King Inthawichayanon, one of the last Lanna kings who was Paratypes. Same data as holotype, 1 male, 2 females (QSBG & NMWC, T185); 2 males, 2 females, 9Ð16 Aug.2006 (NMWC, concerned for forest conservation and whose remains were T178); 1 male, 3 females, 24Ð30 Aug.2006 (QSBG, T235); 1 male, placed on Doi Inthanon, the type locality of this species. 13Ð21 Sep.2006 (QSBG, T253); 1 male, 1 female, 21Ð27 Sep.2006 (QSBG, T346): Summit Marsh, 18¡35.361'N 98¡29.157'E, 2,500 Remarks. – This species is confi ned to moist hill evergreen m, 2 males, 2Ð9 Aug.2006 (QSBG, T124); 1 female, 9Ð16 forest on the summit of Doi Inthanon at 2,500 m. Adults Aug.2006 (QSBG, T177); 2 males, 16Ð24 Aug.2006 (NMWC, were captured from August to October at the end of the T184); 1 male, 13Ð21 Sep.2006 (NMWC, T252); 3 females, 5Ð12 wet season. Oct.2006 (NMWC, T362).

Diagnosis. – Head and thorax black, propleuron contrastingly Chelipoda kameawuta, new species yellowish. C with distinct anterobasal spine. Posterior dc 1 (Fig. 7) (in line with npl) minute. Male cercus with distinct pointed process (Fig. 4). Material examined. – Holotype. Male, THAILAND: Chiang Mai, Doi Inthanon National Park, Kew Ma Trail, 18¡33.162'N Description. – Male. Body length 2.0Ð2.5 mm. Head 98¡28.810'E, 2,200 m, Malaise trap, Y. Areeluck, 22Ð29 Apr.2007 blackish brown; strongly dusted; larger setae black; vt, (QSBG, T1847). ocl and upper upo equally strong; other upo smaller; lpo small, multiserial, pale. Antenna dark brown, stylus white; Paratype. 1 female, same data as holotype, 29 Apr. Ð6 May.2007 poped 3× long as wide, stylus 2× as long. Palpi yellowish (QSBG, T1853). brown. Diagnosis. – Species with black head and all yellow thorax. Thorax blackish; strongly dusted especially on scutum. F1 strongly infl ated with only a single row of denticles below Propleuron contrastingly yellowish with supraalar area and front tarsomeres 2 & 3 strongly spinose (especially in and scutum posteriorly often rather yellowish brown or female). The upper occiput is slightly concave as viewed yellowish black. Thoracic setae black including one npl, one from above. sa and pair of sct all strong; anterior dc strong, posterior dc (in line with npl) minute; small anterior postpronotal and Description. – Male. Body length 3.0 mm. Head black with posterior postpronotal setae usually present. paler dusting; ocl, vtl and upper upo black; lpo and very

262 THE RAFFLES BULLETIN OF ZOOLOGY 2009 conspicuous patch of fi ne setulae behind mouth yellowish. Remarks. – This species is only known from hill evergreen Vertical seta as strong as ocl; one weak and one strong forest at 2,200 m on Doi Inthanon from April to early upper upo adjacent to vtl, obviously stronger than rest of May. upo series. Upper occiput slightly concave behind (viewed from above), vtl originating from slight lateral prominences either side of vertex. Basal antennal segments yellowish; Chelipoda laisoma, new species poped yellowish brown, about 2.5× long as wide (stylus (Fig. 8) missing in holotype). Mouthparts yellow. Material examined. – Holotype. Male, THAILAND: Chiang Thorax clear yellowish orange, all setae black. Upper npl, Mai, Doi Inthanon National Park, Checkpoint 2, 18¡31.559'N sa and anterior dc strong; mid dc (in line with npl) and 98¡29.941'E, 1,700 m, Malaise trap, coll. Y. Areeluck, 2Ð10 posterior dc (near hind margin of scutum) much weaker Nov.2006 (QSBG, T389). but distinct; anterior postpronotal seta present but weak, Paratypes. Same data as holotype, 1 male (NMWC, T383); Kew no stronger than one or two fi ne setulae between it and the Mae Pan Trail, 18¡33.162'N 98¡28.810'E, 2,200 m, 1 male, 2Ð9 equally fi ne lower npl. Mar.2007 (QSBG, T1777); Kew Mae Pan, 18¡33.163'N 98¡28.8'E, 2,200 m 2 males, 8Ð15 Jul.2006 (QSBG & NMWC, T66).

Legs yellow, tarsomeres 4Ð5 darker. C1 as long as thorax, rather stout, 6.5× long as wide, 1Ð2 distinct short stout setae Diagnosis. – Similar to C inthawichayanona with head and near base anteriorly. F1 as long as C1, distinctly infl ated, 4x as thorax black, propleuron contrastingly dark yellowish; C1 long as wide, widest 0.25 from base; pv and av setae strong, with distinct anterobasal spine; posterior dc (in line with black, slightly inclined anteriorly with only single row of npl) minute. Male cercus with two pointed processes. black denticles between becoming more spine-like basally; 2Ð3 shorter basal spines contiguous with series of av spines. Description. – Male. Body length 2.5 mm. Head blackish

T1 0.72Ð0.75× long as F1. Front tarsomere 2 short, 0.3× length brown; strongly dusted; larger setae black; vt, ocl and of tarsomere 3, bearing distinct short black apical setae; upper upo equally strong; other upo smaller; lpo small, tarsomeres 3 with stout setae apically and dorsally. multiserial, pale. Antenna brown, stylus whitish distally; poped 2.5Ð2.8× long as wide, stylus 2.5× as long. Abdomen yellowish brown including genitalia, only subepandrial process black; thinly covered with rather Thorax brownish black; strongly dusted especially dorsally long fi ne setae; tergite 8 reduced. Epan and Hypan fused where indications of broad darker stripe on scutum; (fi g. 7), erect elongate oval in lateral view, left and right propleuron contrastingly dark yellowish or dark orange; all lamellae narrowly separated by unpigmented membrane setae dark including one npl, one sa and pair of sct all strong; at least dorsally. Cercus closely fused with Epan, weakly anterior dc strong, posterior dc (in line with npl) minute; sclerotized, cluster of short setae at dorsal apex and more small anterior postpronotal and posterior postpronotal setae sparse longer fi ner setae elsewhere. Subepandrial process usually present complex, clearly visible through epandrial lamellae, anterodorsal apex sharply upturned. Phallus narrow, Legs yellow, often noticeably darker on F2, F3 and emerging beyond tip of subepandrial process. tarsomeres 4Ð5. C1 0.9× as long as thorax, slightly infl ated basally; a distinct short dark anterobasal seta present, Wing membrane very faintly darkened, veins brown. clearly stronger than anterior ciliation of minute yellowish

Squamae with dark fringes. Halter light brown. setulae. F1 almost as long as C1, moderately infl ated, about 4x as long as wide, widest 0.4 from base. Femoral formula Female. Similar to male. Head with stylus 3x as long as 5(5Ð5)/19(19Ð20)/15(12Ð16)/4(4Ð5) +1 (Table 1), spines poped; patch of yellow pile behind mouth stronger than and denticles blackish. T1 0.7× as long as F1. in male with a few conspicuously longer fi ne setae also present. Abdomen brown; tergite 5 with strong dark seta dorsally on posterior margin; tergite 8 very narrow, inconspicuous. Epan Legs similar to male but apical and dorsal setae on front and Hypan fused, rather posteriorly pointed in lateral view tarsomeres 2 and 3 stronger. (Fig. 8), blackish but less strongly sclerotized and yellowish immediately posterior of cercus, bearing a few dark setae Abdomen with sternite 8 brown, contrasting with preceding posteriorly; left and right lamellae very narrowly separated sternites; cercus rather short, 2× long as wide, brown. by unpigmented densely micropilose membrane. Cercus dark brown, rather paler posteriorly and below; fused with Wing membrane more distinctly brown, especially about Epan + hypandrium; anteriorly directed, with a cluster of base. small setae dorsally; bilobed; upper lobe pointed bearing a few small subterminal setae; lower lobe slightly spathulate Etymology. – The specifi c epithet is a contraction of the distally with extreme apex weakly pointed upcurved, a Thai, kaa, meaning leg and mee a-wut, meaning armed; cluster of short setulae near base below. Subepandrial in reference to the presence of strong spines on the front process dark, closely parallel with and of similar length to femur.

263 Plant: Diversity of Chelipoda in northern Thailand

Figs. 7Ð11. Male genitalia of Chelipoda species in lateral view: 7. C. kameawuta new species; 8. C. laisoma new species; 9. C. macrosceles new species; 10. C. manggawna new species; 11. C. meenamluang new species.

264 THE RAFFLES BULLETIN OF ZOOLOGY 2009 inner surface of upper lobe of cercus, apically pointed and Paratypes. Same data as holotype, 14 males, 21 females (RMNH); upcurved. Phallus apically slender, yellowish. 3 males, 3 females (IRSNB); 4 males, 3 females (NMWC).

Wing membrane very faintly darkened, veins brown. Additional material. VIETNAM, Cat Cat, 1,550 m, Malaise trap, coll. C. Van Achterberg, 2 males, 1 female, 29 Oct.1999 (RMNH). Squamae with dark fringes. Halter with grey knob and THAILAND, Chiang Mai, Doi Inthanon National Park, Summit paler stem. Marsh, 18¡35.361'N 98¡29.157'E, 2,500 m, Malaise trap, coll. Y. Areeluck, 1 male, 29 Apr.Ð 6 May.2007 (QSBG, T1852); Kew Female. Similar to male. Antenna with basal segments Mae Pan Trail, 18¡33.162'N 98¡28.810'E, 2,200 m, 1 female, yellowish, poped paler brown than in male, stylus apparently 22Ð29 Dec.2006 (QSBG, T1888); 1 male, 16Ð23 Mar.2007 brownish (apical part missing). Legs similar to male but F2 (NMWC, T1813); 1 female, 29 Apr. Ð6 May 2007 (QSBG, T1853): Kew Mae Pan, 18¡33.163'N 98¡28.8'E, 1 female, 2Ð10 Nov.2006 and F3 rather lighter and all tibiae obscurely darker. Femoral formula 4.5(4Ð5)/21.5(20Ð25)/14.5(14Ð16)/5(4Ð5) +2; (NMGW, T388). spines yellowish, a small pv basal spine present in addition to a stronger av spine also present in male. Wing veins and Diagnosis. – Slender species with distinctive black and membrane slightly yellowish compared with male. Cercus yellow markings on thorax and elongate front femora with moderately long. only a single row of denticles beneath. The female abdomen is distinctly petiolate basally. Etymology. – The specifi c epithet is contraction of the Thai words for shoulder, lai, and the colour orange, see som, This Description. – Male. Body length 2.5Ð3.0 mm. Head black, is in reference to the dark orange colour of the propleuron lightly dusted, subshining on frons; face bright yellowish in this species. white. Eyes clearly separated (not almost touching) below antenna. All setae yellow; ocl and vtl strong; upper upo Remarks. – This species is only known from predominantly slightly shorter than vtl, other upo and lpo becoming hill evergreen forest at 1,700Ð2,200 m on Doi Inthanon progressively weaker ventrally; patch of pale setae behind during July, November and March. mouth conspicuous. Antenna yellow, stylus darker apically in some lights; poped very narrow apically, 3× long as wide; stylus 2× long as poped. Mouthparts yellow. Chelipoda macrosceles, new species (Figs. 9, 19, 20, 26) Thorax clear yellow, thinly dusted, subshining. Scutum (Fig. 19) with somewhat variable brown markings on Material examined. – Holotype. Male, VIETNAM, Viet Try, Sa notopleural area, narrow median stripe widening posteriorly, Pa, Sin Chay, 22¡20'N 103¡50'E, c1,900 m, Malaise trap, coll. R. scutellum, mediotergite and laterotergite (scutal stripe de Vries, 21 Oct. Ð11 Nov.1999 (RMNH). usually broadened at extreme anterior margin of scutum and

Figs. 12Ð13. Male genitalia of Chelipoda species in lateral view: 12. C. nakladam new species; 13. C. menglunana Grootaert, Yang & Saigusa. Abbreviations: lcer, lower lobe of cercus; subep, subepandrial process; ucer, upper lobe of cercus.

265 Plant: Diversity of Chelipoda in northern Thailand notopleural mark often extensive). Thoracic setae yellow; anteriorly yellow anterior dc and sa strong; mid dc (in line with npl) weak and usually two fi ne small dc immediately behind. Sct fi ne and Legs similar to male, perhaps even more slender and with rather widely spaced; anterior postpronotal very small. ventral denticles on F1 more numerous (15Ð19). Abdomen petiolate basally (Fig. 26); segments 2Ð7 subshining black,

Legs yellow. C1 as long or slightly longer than thorax, otherwise yellow; cercus very short, hardly longer than slender, 9Ð10× long as wide, ciliated anteriorly on distal 0.5 wide, yellow. with minute yellowish setulae. F1 slightly longer than C1, conspicuously slender, slightly infl ated, 8Ð9× long as wide; Etymology. – The specifi c epithet derives from the Greek, a single row of 13Ð15 minute av denticles (pv denticles macrosceles, meaning long-legged in reference to the absent) with 2Ð3 pv and 3 av yellow spines and usually a slender front femur of this species. single basal spine ventrally. T1 0.7× as long as F1, the row of minute denticles ventrally rather longer and more erect Remarks. – This species is currently known from moist than usual. montane forests between 1,550 and 1,900 m in the Hoang Lien Son Mountains in northern Vietnam and from similar Abdomen yellow with tergites 2Ð5 and sternites 2Ð3 dark biotopes at 2,200Ð2,500 m on Doi Inthanon, Thailand. brown, all setae rather short and sparse. Genitalia with fused Adults were caught between October and November and Hypan + Epan (Fig. 9) brownish yellow, darker dorsally again in March. and with rounded blackish patch laterally; rather quadrate, bearing a few short setae; fused lobes rather widely separated dorsally, the aperture between them with greyish Chelipoda manggawna, new species membrane covering in front of which is an opening through (Figs. 10, 25) which internal organs project anterodorsally. Cercus yellow, broadly spathulate apically, bearing distinct regularly Material examined. – Holotype. Male, THAILAND: Chiang spaced setae. Subepandrial process complex, consisting Mai, Doi Inthanon National Park, Checkpoint 2, 18¡31.554'N of twisted yellowish structure. Phallus, pale yellow, long, 98¡29.940'E, 1,700 m, Malaise trap, coll. Y. Areeluck, 16Ð23 projecting anteriorly. Mar.2007 (QSBG, T1817). Paratypes. Same data as holotype: 1 male, 30 Aug. Ð6 Sep.2006 Wing membrane clear; veins yellowish basally, blackish at (NMWC, T238); 1 male, 6Ð13 Sep.2006 (QSBG, T244); 1 male, level of apex of basal cells, dusky yellow distally. Squamae 1 female, 13Ð21 Sep.2006 (NMWC, T250); 1 female, 19Ð26 with pale fringes. Halter white. Oct.2006 (NMWC, T377); 2 females, 2Ð10 Nov.2006 (QSBG, T389); 1 male, 17Ð24 Nov.2006 (QSBG, T1846); 4 females, Female. Antenna with poped slightly shorter than male. 24 Nov. Ð1 Dec.2006 (NMWC, T1870); 1 male, 2Ð9 Feb.2007 Thorax (Fig. 20) reddish black, subshininng; postpronotal (QSBG, T1793); 1 female, 16Ð23 Feb.2007 (QSBG, T1805); 1 area, thoracic ‘collar’, propleuron and katepisternum male, 23 Feb. Ð2 Mar.2007 (NMWC, T1775); 3 males, 16Ð23

Figs. 14Ð17. Chelipoda nakropa new species: 14. male genitalia in lateral view: 15Ð17: variation in form of male cercus: 15Ð16 high elevation morph; 17. mid elevation morph.

266 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Mar.2007 (QSBG, T1817); 3 males, 16Ð23 Mar.2007 (NMWC, Female. Head with setae rather stronger than male. F1 T1817); 2 females, 15Ð22 Apr.2007 (QSBG, T1845); 1 female, slightly more infl ated, 4.3× long as wide, widest 0.3 from 29 Apr. Ð6 May.2007 (QSBG, T1857); 1 male, 1 female 1Ð8 base; femoral formula 5(5Ð6)/24(21Ð27)/14(11Ð16)/4(4Ð5) May.2007 (NMWC, T1827): Kew Mae Pan Trail, 18°33.162’N, +1 (Table 1); av and pv spines blackish or dark yellow. 98°28.810’E, 2,200 m, 1 female, 1–8 May.2007 (NMWC, T1824); Abdomen brownish dorsally, whitish yellow ventrally; 1 female, 2Ð9 Mar.2007 (QSBG, T1777): Campground Pond, 18¡32.40'N 98¡31.80'E, 1,200 m, 1 male, 5Ð12 Jan.2007 (QSBG, sternite 8 dark brown, subquadrate. Cercus elongate, T1917): Summit Marsh, 18¡35.361'N 98¡29.157'E, 2,500 m, pan yellow. trap, 1 male 28 Feb.2007 (NMWC, T1767). Etymology. – The specifi c epithet derives from the Thai Diagnosis. – Yellow species without dark median stripe on word for dragon, mang-gawn; a reference to supposed fi erce scutum and legs somewhat stouter than in C. fl avida. Head predatory behaviour inferred by the presence of raptorial yellow, only ocellar protuberance black. front legs.

Description. – Male. Body length 3.0mm. Head yellow, Remarks. – This species is known only from Thailand’s ocellar protuberance black. Setae blackish, strong, including Doi Inthanon between August and May from 1,200Ð2,500 one ocl, one vtl and one upper upo; one or two minute upo m (mostly 1,700 m). below upper upo but occiput otherwise lacking upo and lpo and only a few minute setulae behind mouth. Antenna with basal segments yellow; poped 2× long as wide, dark brown; Chelipoda meenamluang, new species stylus 4× long as poped, dark brown to yellowish brown. (Fig. 11) Mouthparts yellow. Material examined. – Holotype. Male, THAILAND: Chiang Thorax. Dorsum yellow, pleura pale yellow, lateral margins Mai, Doi Inthanon National Park, Checkpoint 2, 18¡31.554'N of scutum narrowly darkened. Setae blackish; anterior dc 98¡29.940'E, 1,700 m, Malaise trap, coll. Y. Areeluck, 24Ð30 and upper npl strong, posterior dc (in line with npl) much Aug.2006 (QSBG, T232). weaker and of similar size to sa and sct. Lower npl much Paratypes. Same data as holotype; 1 male, 1 female, 9Ð16 smaller, anterior postpronotal setulae minute with 2Ð4 rather Aug.2006 (QSBG, T180): 2 males, 3 females, 16Ð24 Aug.2006 longer setulae between it and notopleural area. (NMWC, T187); 3 males, 1 female, 29 Dec.2006Ð 5 Jan.2007 (QSBG, T1897); 2 males, 2Ð9 Feb.2007 (NMWC, T1793); 5

Legs yellow, tarsomeres 4Ð5 darker. C1 as long as thorax males, 3 females, 23 Feb. Ð2 Mar.2007 (NMWC, T1775); 1 male, 2 (Fig. 25), rather slender, 9.5× as long as wide, anterobasal females, 2Ð9 Mar.2007 (QSBG, T1781); 1 male, 15Ð22 Mar.2007 setae not distinguished from regular row of yellowish (QSBG, T1845); 5 females, 1Ð8 May.2007; Kew Ma Trail, 18¡33.162'N 98¡28.810'E, 2,200 m, 1 female, 16Ð23 Mar.2007 anterior setulae. F1 as long as C1, distinctly infl ated, 4.6× as long as wide, widest 0.4Ð0.5 from base; femoral formula (QSBG, T1813); 1 male, 23 Mar. Ð1 May.2007 [1 Apr.2007 ?]. (QSBG, T1819): Summit Marsh, 18¡35.361'N 98¡29.157'E, 2,500 5(4Ð5)/23(18Ð25)/13(11Ð16)/4(3Ð4) +1 (Table 1), spines m, pan trap, 1 male, 24Ð25 feb.2007 (QSBG, T1763). yellowish, denticles black, pv spines very weak distally; basal spine rather weak, more or less contiguous with series Diagnosis. – Similar to C. hubeiensis with head and thorax of av spines.T1 0.65× long as F1. black, including propleuron but thoracic setae and spines on

F1 yellow and male sternites 7 & 8 with numerous yellow Abdomen brownish yellow, paler ventrally; tergite 8 setae. reduced; sternite 8 with distinct but short setae. Epan and Hypan (Fig. 10) similar to C. fl avida, fused, erect, Description. – Male. Body length 2.5 mm. Head black, narrowly subrectangular in lateral view, yellowish, only extensively dusted; vt and ocl strong, yellow; upper upo small setae posteriorly, left and right lamellae distinctly weaker, darker; other upo and lpo much smaller, latter separated by unpigmented membrane. Cercus fused merging into sparse patch of pale pile behind mouth. Basal with Epan; a short digitiform yellow process bearing antennal segments yellowish; poped dark (vaguely paler strong yellow setae apically, apparently emerging from about base), slightly more than 3× long as wide; stylus the inner face of a somewhat darker rounded and rather dark, 2× long as poped. Palp greyish yellow with strong undifferentiated basal lobe which bears more numerous dark terminal seta. Proboscis dark. smaller setae. Subepandrial process blackish, short and robust, conspicuously bent at 0.5 from base, flattened Thorax black or reddish black, extensively dusted. All above apically but convex below. Postgonite narrow, setae yellow including two dc, one npl and one sa all apically upturned, black, basally yellowish and broader. strong, sct rather weaker; a few small setae on humeral and Phallus narrow, yellow, slightly upturned apically, posthumeral area and on scutum posteriorly reaching as far as apex of cercus.

Legs yellow, tarsomeres 4Ð5 darker. C1 0.8Ð0.85× as long Wing membrane faintly brownish, veins brown. Squamae as thorax, anterior setulae, yellow, inconspicuous, becoming with dark fringes. Halter greyish white, stems darker. slightly longer distally, no distinct anterobasal seta. F1 distinctly infl ated, 3.4× as long as wide, widest 0.35 from base; femoral formula 5(5Ð6)/16(14Ð18)/13(11Ð15)/5(5Ð7)

267 Plant: Diversity of Chelipoda in northern Thailand

+2Ð4 (Table 1), the basal spines consisting of 1Ð2 smaller Aug.2006 (QSBG, T521); 3 males, 7 females, 10Ð11 Aug.2006 setae in line with and basal to both av and pv series; spines (NMWC, T522); 1 male, 2 females, 11Ð12 Aug.2006 (QSBG, T523); 1 female, 12Ð19 Aug.2006 (QSBG, T528); 3 females, 26 yellow, denticles black. T1 0.7Ð0.75× as long as F1. Aug.Ð2 Sep.2006 (NMWC, T534). Abdomen dark brown; tergites 5 and 6 with some distinct Diagnosis. – A yellowish species with black head and setae dorsally on posterior margin; sternites 7 and 8 with distinctively a strongly marked dark subterminal band on numerous strong yellowish setae. Epan and Hypan fused, the wing. somewhat triangular in lateral view (Fig.11), brownish, less strongly sclerotized and yellowish immediately posterior of Description. – Male. Body length 2.5 mm. Head black with cercus, bearing dark setae posteriorly; left and right lamellae pale dust. All setae yellow or whitish; ocl and vtl strong, narrowly separated by unpigmented densely micropilose upo and lpo becoming progressively weaker ventrally; patch membrane. Cercus dark brown, rather paler posteriorly; of pale setae behind mouth conspicuous. Basal antennal fused with Epan + Hypan; three strong black inwardly segments yellow; poped yellowish basally, darker apically, curving dorsal setae; an anteriorly directed process rather almost 3 long as wide; stylus black, thickened, 2 long as club-shaped apically bearing a strong dorsal subapical seta. × × poped. Mouthparts whitish, proboscis black. Subepandrial process dark, narrow, situated close to inner surface of cercus. Phallus yellowish, slender, distal section Thorax yellow, scutellum and mediotergite brownish. Setae almost linear, reaching to end of cercus. yellowish; two dc (including one level with npl) upper npl, sa and sct all strong; otherwise only minute hairs posteriorly Wing with membrane clear and veins yellowish. Squamae on scutum, pospronotum and lower notopleural area. dark yellow. Halter yellowish white. Legs yellow, tarsomeres 4Ð5 darker, T narrowly dark Female. Antenna with poped more uniformly dark and 1 brown posteriorly. C 0.8Ð0.85 as long as thorax, slightly stylus slightly longer than in male 1 × infl ated, 6.1Ð6.2× as long as wide, widest 0.25 from base. F slightly longer than C , distinctly infl ated, 3.7 as long as Femoral formula 5(5Ð6)/18(15Ð23)/14(12Ð17)/5(5Ð6) +1, 1 1 × wide, widest 0.3 from base; femoral formula 7(5Ð8)/17(15Ð the small basal spine in line with av series and occasionally 19)/13(12Ð15)/8(8Ð11) +1Ð2 (Table 1), spines yellow, a much smaller one in line with pv series. Abdomen brown, denticles black; pv spines usually rather close together paler ventrally; cercus moderately long. basally; basal spine(s) rather weak. Mid and posterior femora and tibiae slender, lacking strong setae. Etymology. – The specifi c epithet is a contraction of the Thai words for spiny, mee ngaam, and the colour yellow, Abdomen brownish yellow; genitalia (Fig. 13) yellow with see luang, in reference to the yellow spines on the front only apex of phallus and sheath blackish yellow and extreme femur. apex of subepandrial process dark. Remarks. – The male genitalia superfi cially resemble C. Epan and Hypan fused, with lateral lobes completely fused nigraristata Yang, Grootaert & Horvat, 2004, from the posteroapically but slightly separated posteroventrally, Nanling Mountains in China, however in that species the with scattered short setae. Cercus fused with Epan+Hypan, cercus is broadly triangular (Fig. 3 in Yang et al. 2004), consisting of two roughly triangular parts connected by a lacking a dorsobasal rounded swelling. C. nigraristata also narrow intermediate part along dorsum of Epan+Hypan; apparently has pale rather than yellow setae on the head, posterior part narrowly triangular with rather erect short three pairs of dc and only a very weak npl. C. meenamluang setulae dorsally; anterior part free apically and bearing is so far known only from Doi Inthanon in Thailand with 2-3 stout black setae apically. Subepandrial process, erect, most records at 1,700 m in FebruaryÐMay, August and narrow with apical hook. Phallus strongly refl exed forward, December. rather broad but abruptly narrowed distally and terminating just anterior of anterior lobe of cercus; phallic sheath also broad and continuing forward beyond apex of phallus for a Chelipoda menglunana Grootaert, considerable distance. Yang & Saigusa, 2000 (Fig. 13) Wing veins yellowish basally, darker distally; membrane Material examined. – THAILAND, Loei, Phu Ruea National Park, faintly brownish yellow, a strong black subterminal band Huay Taey Ditch, 17¡30.042'N 101¡20.474'E, 1,233 m, Malaise commencing at apex of cell dm leaving apex of wing clear. trap, coll. N. Jaroenchai: 1 male, 19Ð26 Aug.2006 (QSBG, T532); Squamae with pale fringes. Halter whitish yellow. 2 females, 5Ð12.Aug.2006 (NMWC, T526): Nern Wibaak Ditch, 17¡29.907'N 101¡20.483'E, 1,196 m, Malaise trap, 1 female, 12Ð19 Female. Antenna with poped darker than in male. Aug.2006 (QSBG, T527): Pan Hin Khan Maak Ditch, 17¡30.042'N 101¡20.474'E, 1,219 m, Malaise and pan traps, 11 males, 1 female, Femoral formula (female) 5(5Ð6)/19(15Ð21)/17(14Ð 5Ð6 Aug.2006, (NMWC, T517); 2 males, 3 females, 6Ð7 Aug.2006 22)/5(4Ð6) +1Ð2, pv spines usually more evenly spaced (QSBG, T518); 5 males, 4 females, 7Ð8 Aug.2006 (QSBG, T519); basally. Cercus moderately long, yellowish 5 males, 8Ð9 Aug.2006 (QSBG, T520); 1 male, 3 females, 9Ð10

268 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Remarks. – Described originally from Yunnan, China anteriorly directed, bilobed; upper lobe short, bluntly (Grootaert et al., 2000), C. menglunana is here reported pointed, bearing 2Ð3 strong erect setae above; lower lobe from Loei Province in north eastern Thailand. Adults were elongate, apically broadened and somewhat anvil-shaped. collected for a short period of the wet season in August at Subepandrial process evenly decurved, reaching apex of around 1,200 m. lower lobe of cercus. Phallus sharply refl exed anteriorly; distal section narrow, almost linear.

Chelipoda nakladam, new species Wing membrane faintly yellowish; veins yellow basally (Fig. 12) becoming brownish yellow apically. Squamae with yellowish black fringes. Halter yellowish white. Material examined. – Holotype. Male, THAILAND: Chiang Mai, Doi Inthanon National Park, Summit Marsh, 18¡35.361'N Female. Antenna with poped somewhat more uniformly 98¡29.157'E, 2,500 m, Malaise trap, coll. Y. Areeluck, 2Ð8 darkened than in male. Jul.2006 (QSBG, T53). F slightly larger and stouter than in male; femoral formula Paratypes. Same date as holotype, 1 male, 3 females, 15Ð22 1 July.2006 (QSBG, T70); 1 male, 6 females, 2Ð9 Aug.2006 5(4Ð5)/22(20Ð26)/14(13Ð16)/5(4Ð5) +2Ð4; basal spines less (NMWC, T124); 1 female, 16Ð24 Aug.2006 (QSBG, T184): numerous and smaller than in male. Cercus moderately Summit Forest, 18¡35.361'N 98¡29.157'E, 2,500 m, 1 male, long. 5 females, 9Ð16 Aug.2006 (QSBG, T178): Kew Mae Pan, 18¡33.163'N 98¡28.8'E, 2,200 m, 4 females, 29 Jun. Ð2 Jul.2006 Etymology. – The specifi c epithet is a contraction of the Thai (QSBG, T38): Checkpoint 2, 18¡31.559'N 98¡29.941'E, 1,700 m, 1 words for hunter, nak-laa, and the colour black, see dam, female, 21Ð27 Sep.2006 (NMWC, T343); 1 female, 5Ð12 Oct.2006 in reference to the black colour and presumed predatory (QSBG, T365): Vachiratharn Falls, 18¡32.311'N 98¡36.048'E, 700 habits of this species. m, 1 female, 6Ð13 Sep.2006 (QSBG, T242).

Diagnosis. – Similar to C inthawichayanona with head and Remarks. – This species is mostly confi ned to the upper thorax black, propleuron contrastingly dark yellowish but slopes of Doi Inthanon, Thailand from 1,700Ð2,500 m with adults active during the wet season from June to October. C1 without distinct anterobasal spine; posterior dc (in line with npl) as strong as anterior dc.

Description. – Male. Body length 2.5 mm. Head black Chelipoda nakropa, new species with paler dusting; larger setae dark yellowish brown to (Figs. 14Ð17, 22, 23, 27) black; vt, ocl and upper upo equally strong; other upo and lpo smaller, pale pile behind mouth conspicuous but short. This species is known from two altitudinally segregated Antenna yellowish with poped dorsoapically and stylus morphs, one from mid elevation and the other from higher elevations. The species is described from the mid elevation entirely blackish; poped about 1.7× long as wide, stylus morph. 2.2Ð2.5× as long. Palp dirty white with distinct terminal seta. Proboscis black. Mid elevation morph Thorax brownish black, propleuron contrastingly yellowish; Material examined. – Holotype. Male, mid elevation morph, all setae dark yellowish including two dc, one npl, one sa THAILAND: Chiang Mai, Doi Inthanon National Park, Checkpoint and pair of sct all strong; minute anterior postpronotal and 2, 18¡31.554'N 98¡29.940'E, 1,700 m, Malaise trap, coll. Y. posterior postpronotal setae usually present Areeluck, 21Ð27 Sep.2006 (QSBG, T343).

Legs pale yellow, tarsomere 5 darker. C1 0.75Ð0.8× as long Paratypes. Mid elevation morph. Same data as holotype: 3 males, as thorax, slightly infl ated basally, no distinct anterobasal 3 females, 15Ð22 Jul.2006 (NMWC, T73); 1 male, 1 female, 9Ð16 Aug.2006 (QSBG, T180); 4 males, 7 females, 16Ð24 Aug.2006 seta. F1 1.2× as long as C1, moderately and evenly infl ated, widest 0.25Ð0.6 from base; Femoral formula 5(5Ð5)/20(18Ð (NMWC, T187); 2 males, 1 female, 6Ð13 Sep.2006 (NMWC & 23)/12(10Ð13)/5(4Ð5) +4Ð6 (Table 1); spines yellow, 2Ð3 QSBG, T244); 1 male, 2 females, 13Ð21 Sep.2006 (QSBG, T250); 1 male, 1 female, 21Ð27 Sep.2006 (QSBG, T343); 1 female, 5Ð12 basal spines contiguous and evenly spaced with both av and Oct.2006 (QSBG, T365); 3 males, 11 females, 12Ð19 Oct.2006 pv series of spines, continuing to base of limb; denticles (NMWG, T371) 4 males, 15 females, 19Ð26 Oct.2006 (NMWC & black. T1 0.75× as long as F1. QSBG, T377); 5 females, 26 Oct. Ð2 Nov.2006 (NMWC, T383); 2 females, 2Ð10 Nov.2006 (QSBG, T389); 3 females, 24 Nov. Abdomen blackish; tergite 6 with strong dark seta dorsally Ð1 Dec.2006 (NMWC, T1870); 1 male, 22Ð29 Dec.2006 (QSBG, on posterior margin; tergite 8 very narrow. Genitalia T1891); 2 females, 2Ð9 Feb.2007 (QSBG, T1793); 1 male, 23 Feb. blackish with cerci, subepandrial process and phallus paler. Ð2 Mar.2007 (QSBG, T1775); 1 female, 2Ð9 Mar.2007 (QSBG, Epan and Hypan fused, rather rounded in lateral view T1781); 2 females, 16Ð23 Mar.2007 (NMWC, T1817); 3 females, (Fig. 12), bearing a few dark setae posteriorly; left and 15Ð22 Apr.2007 (QSBG, T1845): Kew Mae Pan, 18¡33.163'N, 98¡28.8'E, 2,200 m, 1 male, 9Ð16 Aug.2006 (QSBG, T179): Kew right lamellae narrowly separated by unpigmented densely Mae Pan Trail, 18¡33.162'N, 98¡28.810'E, 2,200 m, 1 female, 1Ð8 micropilose membrane (when macerated, this membrane Mat.2007 (QSBG, T1824). appears much broader). Cercus fused with Epan + Hypan,

269 Plant: Diversity of Chelipoda in northern Thailand

Additional material. Mid elevation morph Ð Same data as 0.95× as long as thorax; rather stout, slightly narrowed holotype: 3 males, 1 female, 24Ð30 Aug.2006 (NMWC, T232); 2 distally, 6x as long as wide; 1Ð2 anterobasal setae, yellowish, females, 16Ð23 Feb.2007 (QSBG, T1805); 8 males, 1 female, 29 stout, not as long as C1 is deep, clearly differentiated from Apr. Ð6 May.2007 (NMWC, T1857): Summit Forest, 18¡35.361'N series of regularly spaced minute anterior setulae. F 98¡29.157'E, 2,500 m, 1 male, 15Ð22 Apr.2007. 1 slightly longer than C1, distinctly infl ated (Fig. 27), 4x as long as wide, widest 0.3Ð0.4 from base; femoral formula 5(4Ð6)/20(17Ð25)/14(12Ð19)/5(4Ð5) +1Ð2 (Table 1), High elevation morph spines yellowish often becoming darker on distal part of Paratypes. High Elevation Morph. Kew Mae Pan, 18¡33.163'N limb; denticles black; basal spine(s) distinct, more or less 98¡28.8'E, 2,200 m, 1 female, 2Ð10 Nov.2006 (QSBG, T388): contiguous with series of av spines.T1 0.70Ð0.74× long as Kew Mae Pan Trail, 18¡33.162'N 98¡28.810'E, 2,200 m, 5 males, F1. 2 females, 17Ð24 Nov.2006 (NMWC, T1860); 30 males, 10 females, 24 Nov.Ð1 Dec.2006 (QSBG, T1866); 7 males, 1 female, Abdomen brownish yellow, paler ventrally; tergite 8 1Ð8 Dec.2006 (NMWC & QSBG, T1872); 21 males, 2 females, reduced, very narrow dorsally, broader laterally, strongly 8Ð16 Dec.2006 (NMWC, T1878); 2 males, 7 females, 15Ð22 sclerotized. Epan and Hypan (Fig. 14) fused, rather pointed Dec.2006 (QSBG, T1882); 6 males, 9 females, 22Ð29 Dec.2006 posteroventrally, brownish yellow, a few distinct but (QSBG, T1888); 39 males, 19 females, 29 Dec.2006 Ð 5 Jan.2007 small setae posteriorly; left and right lamellae narrowly (NMWG, T1893); 4 males, 1 female, 5Ð12 Jan.2007 (QSBG, T1928); 9 males, 14 females, 9Ð16 Feb.2007 (NMWC, T1795); 3 separated by unpigmented membrane. Cercus fused with males, 6 females, 23 Feb.Ð2 Mar.2007 (QSBG, T1771); 15 males, Epan, broad and brownish basally; a short digitiform yellow 13 females, 2Ð9 Mar.2007 (QSBG, T1777); 7 males, 11 females, upper process bearing distinct yellowish setae (length and 16Ð23 Mar.2007 (NMWC, T1929); 5 females, 16Ð23 Mar.2007 breadth of process rather variable between individuals (NMWC, T1813); 3 males, 2 females, 23 Mar. Ð1 May.2007 [1 and even between left and right side; apically rather Apr.2007 ?] (QSBG, T1819); 3 males, 2 females, 22Ð29 Apr.2007 more pointed than in Figs. 14 & 17) in some individuals, (QSBG, T1847): Summit Forest, 18¡35.361'N, 98¡29.157'E, sometimes broader); lower process more rounded and 2,500 m, 1 female, 19Ð26 Oct.2006 (QSBG, T375); 1 male, 2Ð10 shorter. Subepandrial process blackish, broad in dorsal Nov.2006 (QSBG, T387). view, narrower with apex upcurved in lateral view. Phallus Additional material. High Elevation Morph Ð Same data as yellow apically, darker basally, reaching to just beyond tip holotype: Ð Campground Pond, 18¡32.40'N 98¡31.80'E, 1,200 m, of upper process of cercus. 1 female, 29 Dec.2006Ð5 Jan.2007 (NMWC, T1895). Wing membrane faintly darkened; veins brown, slightly Diagnosis. – Head black. Thoracic dorsum extensively yellowish basally. Squamae with black fringes. Halter darkened, pleura yellowish. Somewhat resembling C. greyish. guangxiensis but C1 with distinct anterobasal spine and basal antennal segments yellow. Two altitudinal forms are Female. Similar to male but antenna with stylus yellowish recognised. Ð a mid elevation morph in which the dark white; upo and lpo rather stronger. marking on the scutum is diffusely edged laterally and a high elevation form in which the scutum is darker and F1 with spines often darker yellowish, femoral formula 5(5Ð sharply edged yellowish lateral to line of dorsocentrals. 6)/24(21Ð27)/16(14Ð18)/5(4Ð5) +1Ð2 (Table 1). Abdomen dark above, paler below; sternite 8 dark brown, bluntly Description. – Mid elevation morph: Male. Body length pointed apically; cercus elongate, yellow. 2.5Ð3.0 mm. Head black, strongly dusted especially on upper occiput. Setae black, ocl and vtl strong, upper upo slightly shorter; other upo and lpo weak, conspicuous patch High elevation morph of pale pile behind mouth spreading onto lower occiput. Antenna with basal segments yellow; poped brown, 2× Scutum sharply edged yellowish lateral to line of dorsocentrals long as wide; stylus brown, 3× long as poped. Mouthparts (Fig. 22), the yellow margins contrasting with central broad yellowish. almost blackish area. Katepisternum and meron more

obscurely darkened ventrally. F1 with av and pv spines Thorax with pleura yellow; scutum, scutellum, mediotergite tending to be slightly stronger, more numerous and darker. and laterotergite brownish yellow; scutum diffusely edged Male femoral formula 6(6Ð7)/21(19Ð23)/15(14Ð17)/5(5Ð6) paler brown laterally (Fig. 23), not distinctly contrasting +1Ð2; female 6(5Ð6)/22(19Ð24)/15(13Ð17)/5(5Ð6) +1 with darker central area. All setae black; upper npl and (Table 1). Abdomen generally darker. anterior dc strong, mid dc (in line with npl) very weak, posterior dc (near posterior margin of scutum) fine but Male cercus with digitiform process broader (Figs. 15, 16); usually distinct; sct weak and sa weaker still; a few minute subepandrial process less distinctly upturned apically setulae about and behind postpronotum; lower npl very weak. Etymology. – The specifi c epithet derives from the Thai word, nakrop, meaning warrior, in reference to presumed fi erce

Legs yellow, tarsomeres 4Ð5 darker; F2 and F3 dorsoapically, predatory behaviour suggested by the raptorial front legs.

T2 and mid basal tarsomeres sometimes also brownish. C1

270 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Remarks. – Morphological differences between the high lamellae broadly separated by unpigmented membrane. and low elevation morphs were not judged suffi cient to Cercus fused with Epan, yellowish, bilobed; upper lobe warrant specifi c status for the two forms, both of which short, bluntly pointed, dorsally with numerous closely are confi ned to forests on Doi Inthanon. The high elevation set long setae curving anteriorly and inwardly; lower morph was mostly found at 2,200 m with peak adult activity lobe longer, narrowly digitiform with a few short setulae from November Ð March. The mid elevation morph was distally and more numerous and longer setae below basally. abundant lower down the mountain at 1,700 m with peak Subepandrial process brownish yellow, narrow, broadened adult activity from JulyÐNovember and again from March and anvil-shaped apically. Phallus yellowish, narrow, Ð May (Fig. 29). The two morphs may prove to be sibling gradually tapered apically. Postgonite (?) closely apposed species with allotopic populations isolated by altitudinal and with phallus, apically broader with lateral twisted ribbon- phenological factors. like process extending laterally to inner face of lower lobe of cercus.

Chelipoda thaosuranaria, new species Wing membrane faintly greyish yellow, veins brownish (Fig. 18) yellow. Squamae with dark fringes. Halter pale yellow.

Material examined. – Holotype. Male, THAILAND: Loei, Phu Female unknown. Ruea National Park, Nature Trail, 17¡30.740'N 101¡20.650'E, 1,353 m, Malaise trap, coll. N. Jaroenchai, 26 Sep.Ð2 Oct.2006 Etymology. – The specifi c name commemorates Mo Mo, (QSBG, T834). a woman from Korat who was honoured with the epithet Thao Suranari (‘brave woman’) by Thailand’s King Rama Paratype. One male, same data as holotype (NMWC). III in recognition of her bravery during a nineteenth century Diagnosis. – Superfi cially resembling C. thaosuranaria Laotian invasion of Thailand. with head black and all yellow thorax but F1 with usual double row of denticles beneath, front tarsomeres 2 & 3 Remarks. – This species is only known from 1,353 m on the sandstone mesa formations at Phu Ruea, Thailand in not distinctly spinose and C3 with strong black anteroapical seta. late September Ð early October.

Description. – Male. Body length 2.0Ð2.5 mm. Head black with paler dusting; ocl, vtl and upper upo strong, black; Chelipoda species D other upo and lpo minute or absent; only a few pale setulae behind mouth. Antenna yellowish with poped obscurely Material examined. – THAILAND: Chiang Mai, Doi Inthanon National Park, Checkpoint 2, 18¡31.554'N 98¡29.940'E, 1,700 darker, especially apically and stylus blackish; poped 2.2 × m, Malaise trap, coll. Y. Areeluck, 3 females , 2Ð8 July.2006 long as wide, stylus 2× as long. Mouthparts yellowish (NMWC, T56) 7 females, 15Ð22 Jul.2006 (NMWG, T73); brown, proboscis darker. Loei, Phu Ruea National Park, Ma Kraow Ditch, 17¡29.652'N 101¡21.020'E, 1,167 m, pan trap, coll. P. Tumtip, 1 female, 10Ð11 Thorax clear yellow, mediotergite medially and scutum Noc.2006 (NMWC, T1113); Khonkaen, Nam Pong National Park sublaterally obscurely darkened. Setae black; two dc Offi ce, 16¡37.341'N 102¡34.467'E, 324 m, Malaise trap, coll. K. (including one level with npl) upper npl, sa and sct all Jaidee, 1 female, 19Ð26 Jul.2006 (NMWC, T109). strong; otherwise only minute hairs posteriorly on scutum, pospronotum and lower notopleural area.

Legs yellow, tarsomeres 4Ð5 and T1 obscurely darker. C1 0.8× as long as thorax, 5.0Ð5.2× as long as wide, slightly broader basally; anterior ciliation of fi ne yellowish setae distinct and almost as long as limb is deep on distal 0.6, no stronger anterobasal seta. C3 with strong black anteroapical seta as long as limb is wide and 2Ð3 weaker dark setae anteriorly. Mid trochanter with short pointed prominence in inner face basally. F1 1.2× as long as C1, 4x as long as wide, widest 0.3 from base; femoral formula approximately 5(4Ð5)/18(15Ð18)/14(14Ð15)/5(5Ð6) +2Ð4 (Table 1), spines yellow, denticles black; basal spines small, contiguous with and forming basal extension of both av and pv spines. Fig. 18. Chelipoda thaosuranaria new species, male genitalia. Abdomen dark yellow; tergite 8 reduced, slightly more Abbreviations: Epan+Hypan, fused epandrium and hypandrium; strongly sclerotized than preceding tergites; sternite 7 with lcer, lower lobe of cercus; mem, median membrane separating left long yellowish setae posteroventrally. Epan and Hypan and right lobes of fused epandrium + hypandrium; ph, phallus; fused (Fig. 18), subspherical in lateral view, brownish pgt, postgonite; subep, subepandrial process; ucer, upper lobe of yellow with distinct setae posteriorly; left and right cercus.

271 Plant: Diversity of Chelipoda in northern Thailand

Diagnosis. – In the absence of male specimens, this species between and behind front coxae; scutum with strong rather will not be formally described in the present work and it broad median stripe (0.3× width of scutum), sometimes is included in the key and mentioned here only to prevent more diffuse and fading in prescutellar depression; anterior confusion with other species. Variation in antennal colour dc strong, three pairs of much smaller postior dc; sa minute; and intensity of markings on the scutum may indicate that postalar present, minute. F1 strongly infl ated, spines yellow, more than one species is involved. double row of denticles black. Abdomen dark above, whitish yellow below. Head black with paler dusting and antenna yellow to brown, poped 2.5× long as wide. Thorax yellow including area

Figs. 19Ð24. Thoracic dorsum of Chelipoda spp. showing schematic pattern of ground colour. 19Ð20. C. macrosceles new species: 19. male; 20. female: 21. C. fl avida Brunneti, male: 22Ð23. C. nakropa new species, male: 22. high elevation morph; 23. mid elevation morph: 24. C. chaiamnata new species, male.

272 THE RAFFLES BULLETIN OF ZOOLOGY 2009

DISCUSSION & Yang, 2004) and now northern Thailand have been recently studied. Despite this, a few provisional comments Systematics are appropriate. Of the 14 species reported here from Thailand, seven were apparently confi ned to Doi Inthanon The genus Chelipoda contains 92 described species (2,565 m), the highest peak of the Thanon Thongchai distributed across all faunal realms except the Afrotropical. Range. An additional species was found in Thailand only The genus is rather structurally diverse and some included on Doi Inthanon but also occurred on high mountains in species from the Neotropical (Plant, 2009a) and Australasian northern Vietnam. Five species were restricted to Loei (Plant, 2007) realms for example exhibit potentially Province with three of these also occurring at other sites important morphological differences from those in the elsewhere, especially along the western margins of the Isaan Palaearctic. However, all species treated in this work share Plateau in Thailand and southern provinces of China. It is a keel-like fusion of the epandrium and hypandrium, an possible that this group of species provides evidence of a important synapomorphy in a major clade of Chelipoda biogeographic division separating the eastern mountains sensu lato, which includes all known species from the from those in the west (the NÐS axial Tenasserim mountains Indo-Malayan (Oriental) and Palaearctic realms and most and their offshoot, the Thanon Thongchai) although species from the Nearctic (Plant, 2007; 2009b). Further ecological factors could equally well be determinant as work is ongoing to resolve the systematic relationships many of the Loei localities were highly seasonal Pinus / within Chelipoda sensu lato. savannah biotopes, much dryer than the higher elevation evergreen forest biotopes of Doi Inthanon. Chelipoda fl ava is apparently widely distributed in Asia ranging from India, Distribution the western slopes of the Tenasserim in Myanmar and their eastern slopes in Chaing Mai, the peninsular mountains in The faunistics of Chelipoda species in Asia is very Trang as well as in Loei. imperfectly understood and only southern China (Yang

Figs. 25Ð28. Chelipoda species: 25. C. manggawna new species, male; 26. C. macrosceles new species, female habitus; 27. C. nakropa new species, male, front femora showing chaetotaxy; 28. C. hubeiensis Yang & Yang, female, wing. Abbreviations: bm, cell bm; br, cell br; bs, basal spines; d, denticles; dm, cell dm; dm-cu, crossvein dm-cu; s, spines.

273 Plant: Diversity of Chelipoda in northern Thailand

Table 2. Variation in species richness with altitude on Doi Ericaceae and the forest becomes extremely moist with Inthanon. Species Richness = number of species; Abundance = no ombrogenic (rain-inducing) conditions ensuring a moist, of individuals of all species / sample; n = number of samples in humid environment under the canopy throughout the year. which Chelipoda were found (note- The total number of samples at each altitude is unknown). An analysis of seasonal phenology at different altitudes Altitude (m) Species Richness Abundance n (Fig. 31) indicated declines in species richness at the start of the wet season and at the end of the cool dry season. Above 0 Ð 500 n/a n/a 0 1,700 m, species richness was slightly greater during the dry 501 Ð 1,000 2 1.5 2 season compared with the wet season but the pattern was 1,001 Ð 1,500 4 3 12 reversed at lower altitudes. Although little is known of the 1,501 Ð 2,000 7 3.5 80 immature stages of Chelipoda, they are probably associated 2,001 Ð 2,500 10 5.3 99 with moist soils in shaded, humid biotopes (Plant, 2007). It is hypothesized that outside the wet season, the seasonal drought experienced by the lower slopes of Doi Inthanon results in conditions which are less suitable for Chelipoda Diversity and phenology on Doi Inthanon but that seasonality is relaxed on the upper slopes which maintain a suitable moist environment even in the dry Of 911 specimens named in this study 833 (91%) season. Interestingly, Grootaert & Kiatsoonthorn (2003) representing 11 species, were collected on Doi Inthanon also provided some evidence for increased activity of adult allowing meaningful analysis of distributions on the Empididae during the beginning of the wet season in a mountain. Species richness and abundance increased with strongly seasonal secondary mixed deciduous forest at Na altitude (Table 2) and were particularly high in the hill Haeo, north east Thailand. evergreen forest zone above 1,700 m with pronounced altitudinal zonation in some species (Figs, 29, 30). Three species (C. hubeiensis, Yang & Yang, C. inthawichayanona The Doi Inthanon biodiversity ‘hotspot’ new species & C. macrosceles new species) were entirely restricted to the upper moist hill evergreen (cloud forest) The mountains of northern Thailand are situated within the zone. Below 1,200 m mixed deciduous forest predominates Indo-Burma biodiversity hotspot identifi ed by Myers et al. becoming progressively wetter with increasing altitude and (2000) as being of global signifi cance. Furthermore, there merging into hill evergreen forest above 1,500 m where are indications from groups as diverse as mammals, birds, Fagaceae (e.g. Castanopsis, Lithocarpus & Quercus) are reptiles and plants (Birdlife International, 2007) that Doi prominent in the canopy. Above 2,000 m Fagaceae are Inthanon is a key biodiversity site within this area. This increasingly replaced by Magnoliaceae, Theaceae and study identifi ed a rich Chelipoda fauna from Doi Inthanon

Fig. 29. Altitudinal zonation of Chelipoda nakropa new species on Doi Inthanon. The abundance at each elevation and date is proportional to the area of the circles; high elevation morph (open circles); mid elevation morph (shaded circles).

274 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 30. Altitudinal zonation of Chelipoda species on Doi Inthanon. The abundance at each elevation and date is proportional to the area of the circles; C. hubeiensis Yang & Yang (open circles); C. fl avida Brunetti (shaded circles). with 91% of individuals representing 78% of the Thai Chelipoda species (including seven apparently endemic species) being found on the mountain. It is likely that the apparent importance of Doi Inthanon for Chelipoda may have been infl ated by under sampling of comparable high elevation evergreen forests at other sites in Thailand but the richness of the mountain’s fauna demands further explanation.

Doi Inthanon is a metamorphic core complex bounded by low-angle faults which has been uplifted (MacDonald et al., 1993; Dunning et al., 1995; Searle & Morley, 2009; M. Searle, pers. com.) and is now considerably higher than the surrounding mountains. Its large altitudinal variation supports a greater range of altitudinal succession zones than elsewhere in northern Thailand and present day availability of multiple moist forest biotopes at higher elevations may at least partially explain the richness of the Chelipoda fauna.

Orogenesis of Thailand’s N-S axial mountains occurred at varying rates during the Cenozoic following the collision of India with Eurasia c 50 MYA (Royden et al., 2008). Elevation of the Tibetan Plateau resulted in the onset of a seasonal monsoon climate, perhaps as early as 15-20 MYA (Harris, 2006) with profound biotic consequences. ’s climate was probably warmer during the Miocene (10Ð23 MYA) than at present with less seasonally dependant rainfall patterns and supported more extensive Fig. 31. Infl uence of altitude on seasonal abundance of Chelipoda tropical rain forests extending as far north as southern spp. on Doi Inthanon. Radial plot of species richness (number of China (Heaney, 1991; Zhu, 2008). In the Pleistocene, species) throughout the year. Approximate limits of the major tropical forests retreated southwards in response to seasons are indicated.

275 Plant: Diversity of Chelipoda in northern Thailand progressive general cooling and modifi ed rainfall patterns efforts of many national park staff in Thailand are and during the glacial maximum (18,000 BP) montane gratefully acknowledged. The TIGER Project is supported vegetation and savannah were more frequent (Heaney, by the USA NSF (grant no. DEB-0542846). The Vietnam 1991). Fossil evidence from large mammals (Tougard, material was made available thanks to a SYNTHESYS 2001) and coniferous trees (Werner, 1997), a palynological grant obtained by P. Grootaert. analysis from peat bogs (Penny, 2005) and a molecular phylogeographic reconstruction of the population history of Simulium tani Takaoka & Davies (Diptera, Simuliidae) LITERATURE CITED (Pramual et al., 2005) for example, provide evidence for migration of southeast Asian biota in response to climatic Birdlife International, 2007. Ecosystem Profile, Indo-Burma fl uctuations during this period. biodiversity hotspot, Indochina region. Birdlife International, Cambridge. 153 pp. (downloaded from http://birdlifeindochina. It is hypothesised that exceptional biodiversity on Doi org/birdlife/news/CEPF_EN_22Aug08.pdf, Jan.2009). Inthanon might have resulted from altitudinal migration Brunetti, E., 1913. New Indian Empididae. Records of the Indian in response to climatic fl uctuations. A range of altitudinal Museum, 9: 11Ð45. succession zones in close approximation on the mountains’ Brunetti, E., 1920. Diptera Brachycera 1. In: Shipley, A. E. & slopes would have facilitated dynamic vertical dispersal Marshall, A. K. The Fauna of British India including Ceylon into montane refugia as environmental and vegetation and Burma. Taylor & Francis, London. 401 pp. patterns changed, with populations subsequently becoming Dunning, G. R., MacDonald, A. S. & Barr, S. M., 1995. Zircon isolated on the mountain as orogenesis and climatic change and monazite U-Pb dating of the Doi Inthanon core complex, continued. Furthermore, uplifting of Doi Inthanon probably northern Thailand: implications for extension within the began 20 MYA (MacDonald et al., 1993; Dunning et al., Ondosinian orogen. Tectonophysics, 251: 197Ð213. 1995; Searle & Morley, 2009; M. Searle, pers. com.) Grootaert, P. & Kiatsoonthorn, V., 2003. Insects of Na Haeo: a coincident with the development of a seasonal monsoon. preliminary survey and seasonal dynamics of dolichopodid Although a pronounced dry season developed at lower and empidid fl ies. IN: Ampornpan, L. & Dhillion, S. S. (Eds.), altitudes it is likely that, as at the present time, seasonality The Environment of Na Haeo, Thailand, Biodiversity, non- timber products, land use and conservation. Craftsman Press, was relaxed at higher altitudes which probably experienced Bangkok. pp. 121Ð135. more even annual precipitation levels. Seasonal relaxation at higher altitudes would have provided buffering refugia for Grootaert, P., Yang, D. & Saigusa, T., 2000. Empididae (Diptera: Empidoidea) from Xishuangbanna, Yunnan (I): ombrophilous fauna such as Chelipoda which were unable Hemerodromiinae. Bulletin de L’Institute Royal des Sciences to tolerate seasonal dry conditions at lower elevations. Naturelles de Belgique, Entomologie, 70: 71Ð80. The summit slopes of Doi Inthanon share at least some Hara. M., Kanazaki, K., Mizuno, T., Noguchi, H., Sri- Ngernyuang, K., Teejuntuk, S., Sungapalee, C., Ohkubo, T. affi nities with the Palaearctic Realm admixed with tropical & Bunyavejchewin, J., (2002). The fl oristic composition of Indo-Malayan infl uences. For example, Hara et al. (2002) tropical montane forest in Doi Inthanon National Park, northern found 60% of tree species in one study plot common Thailand, with special reference to its phytogeographical with the eastern Himalaya. Plant (2009c) described two relation with montane forests in tropical Asia. Natural History species of Trichopeza Rondani (Diptera, Brachystomatidae) Research, 7(1): 1Ð17. apparently endemic to the summit area of Doi Inthanon and Harris, N., (2006). The elevation history of the Tibetan Plateau considered this essentially Palaearctic genus of possible and its implications for the Asian monsoon. Palaeogeography, Himalayan origin had penetrated the Indo-Malayan along Palaeoclimatology, Palaeoecology, 241(1): 4Ð15. ‘corridors’ of suitable cool moist forest on the easternmost Heaney, L. R., (1991). A synopsis of climatic and vegetational mountain folds of the Himalaya. As yet no phylogeographic change in southeast Asia. Climate Change, 19: 53Ð61. resolution of Palaearctic and Indo-Malayan elements MacDonald, A. S., Barr, S. M., Dunning, G. R. & Yaowanoiyothin, has been demonstrated in Chelipoda but the spread of W., 1993. The Doi Inthanon metamorphic core complex in NW Palaearctic elements along building mountain chains can not Thailand: age and tectonic signifi cance. Journal of Southeast be discounted. The subsequent uplifting of Doi Inthanon’s Asian Earth Sciences, 8: 117Ð125. basement well above the surrounding area would have Macquart, J., 1923. Monographie des insects diptères de la isolated these elements and promoted speciation. famille des empides, observes dans le nord-ouest de la France. Recueil des Travaux de la Société d’Amateurs des Sciences, de l’Agriculture et des Arts à Lille, 1822,137Ð165. ACKNOWLEDGEMENTS McAlpine, J. F., 1981. Morphology and terminology Ð Adults Chapter 2. In: McAlpine, J. F., Peterson, B. V., Shewell, I thank Christophe Daugeron, Patrick Grootaert, Igor G. E., Teskey, H. J., Vockeroth, J. R. & Wood, D.M. Shamshev and Ding Yang for comment, advice and loan (Coords.), Manual of Nearctic Diptera, 1. Agriculture Canada of specimens. Mike Searle kindly provided information Monograph, 27: 9Ð63. on the geology of Doi Inthanon. For access to TIGER Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. Project material and local expertise in Thailand I am A. B. & Kent, J., 2000. Biodiversity hotspots for conservation grateful to Michael Sharkey, Brian Brown, Chaweewan priorities. Nature, 403: 853Ð858. Hutacharern and Ratana Lukanawarakul. The collecting

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Penny, D., (2001). A 40,000 year palynological record from Stuckenberg, B. R., 1999. Antennal evolution in the Brachycera north-east Thailand; implications for biogeography and (Diptera), with a reassessment of terminology relating to the palaeo-environmental reconstruction. Palaeogeography, fl agellum. Studia dipterologica, 6: 33Ð48. Palaeoclimatology, Palaeoecology 171(3-4): 97Ð128. Tougard, C., 2001. Biogeography and migration routes of Plant, A. R., 2007. The Hemerodromiinae (Diptera, Empididae) of large mammal faunas in south-east Asia during the late New Zealand II. Chelipoda Macquart. Zootaxa, 1537: 1Ð88. middle Pleistocene: focus on the fossil and extant faunas Plant, A. R., 2009a. The genus Chelipoda Macquart, 1823 from Thailand. Palaeogeography, Palaeoclimatology, (Diptera, Empididae, Hemerodromiinae) in Chile. Deutsche Palaeoecology, 168 (3Ð4): 337-358. Entomologische Zeitschrift, 56(1): 57Ð71. Werner, W. L., 1997. Pines and other conifers in Thailand Plant, A. R., 2009b. Revision of the east Asian genus Achelipoda Ð a Quaternary relic? Journal of Quaternary Science, 12: Yang, Zhang & Zhang, 2007 (Diptera: Empididae: 451Ð454. Hemerodromiinae) including designation of a neotype for Yang, D. & Yang, C 2004. Diptera, Empididae, Hemerodromiinae, Achelipoda pictipennis (Bezzi, 1912) and descriptions of six Hybotinae. In: Fauna Sinica, Insecta 34. Science Press, new species. Zootaxa, 2020: 37Ð50. Beijing, 335 pp. Plant, A. R., 2009c. Two new species of Trichopeza Rondani Yang, D., Grootaert, P. & Horvat, B., 2004. A new species of (Diptera: Empidoidea: Brachystomatidae) from northern Chelipoda Macquart, with a key to the species from China Thailand with a revised key to world species, Studia (Diptera: Empididae). Aquatic Insects, 26(1): 69Ð74. dipterologica, 15: in press. Yang, D. & Yang, C., 1986. Fourteen new species of dance fl ies Pramual, P., Kuvangkadilok, C., Baimai, V. & Walton, C., 2005. from Fujian and Guangxi (Diptera: Empididae). Wuyi Science Phylogeography of the black Simulium tani (Diptera: Journal 6: 75Ð88. Simuliidae) from Thailand as inferred from mtDNA sequences. Yang, D. & Yang, C., 1990. Eight new species of the genus Chelipoda Molecular Ecology, 14(13): 3989Ð4001. from China (Diptera: Empididae). Acta Zootaxonomica Sinica, Royden, L. H., Burchfi eld, B. C. & van der Hilst, R. D., 2008. 15(4): 483Ð488. The geological evolution of the Tibetan Plateau. Science, 321: Zhu, H., 2008. The tropical fauna of southern Yunnan, China, and 1054Ð1058. its biogeographic affi nities. Annals of the Missouri Botanical Searle, M. P. & Morley, C. K., 2009. Tectonics and thermal Garden, 95: 661Ð680. evolution of Thailand in the regional context of South-East Asia. Geological Society London Memoir: in press.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 279Ð295 Date of Publication: 31 Aug.2009 © National University of Singapore

FIRST INVENTORY OF THE WATER BUGS (HETEROPTERA: NEPOMORPHA: GERROMORPHA) OF LANGKAWI ISLAND, KEDAH, MALAYSIA

Herbert Zettel Natural History Museum Vienna, International Research Institute of Entomology, Burgring 7, A-1010 Vienna, Austria, Email: [email protected]

A. D. Tran Department of Invertebrate Zoology, Faculty of Biology, Hanoi University of Science, 334 Nguyen Trai, Thanh Xuan, Hanoi, Vietnam Email: [email protected]

ABSTRACT. – The fi rst survey of the water bug fauna of Langkawi Island, Malaysia, yielded 55 species (fi ve of which were identifi ed only to the genus level) inhabiting various freshwater habitats, mangroves, and sea shores and belonging to 31 genera and eleven families; 17 species of ten genera from seven families belong to Nepomorpha, 38 species of 21 genera from four families to Gerromorpha. Three species are newly described here: Hydrotrephes langkawicus, new species (Helotrephidae), Strongylovelia narusei, new species, and Microvelia (Picaultia) minutissima, new species (both Veliidae). These new Veliidae have a more wide distribution than only in Langkawi Island: Strongylovelia narusei, new species is also known from Terengganu in peninsular Malaysia, and Microvelia (Picaultia) minutissima, new species is known from Selangor in peninsular Malaysia and from Singapore. Another nine species are recorded from Malaysia for the fi rst time.

KEY WORDS. – Heteroptera, Nepomorpha, Gerromorpha, check-list, Helotrephidae, Veliidae, Hydrotrephes, Strongylovelia, Microvelia, new species, fi rst records, Langkawi, Malaysia, Singapore.

INTRODUCTION The water bug fauna of the Malay Peninsula is relatively well known, but only three reliable species records from The island of Langkawi (Pulau Langkawi) is situated off Langkawi were found in the literature: Halobates hayanus the northwest coast of peninsular Malaysia in the southern White, 1883 (Herring, 1961), Haloveloides sundaensis Andaman Sea, located approximately at 6°20’N and 99°45’E Andersen, 1992 (Andersen, 1992) and Xenobates murphyi (The Times Atlas of the World, 1992). In 2003 and 2004 the Andersen, 2000 (Andersen, 2000). These records are University of Malaysia organized two scientifi c expeditions based on an old collection by R. Brown in 1934 and on to survey the natural resources of Langkawi Island (Hussin collections by D. Kovac in 1993. More specimens from et al., 2005). The results were subsequently published in a the latter expedition are housed in the Zoological Reference special issue of the Malaysian Journal of Sciences (2005, Collection, Singapore, and in the Senckenberg Museum, volume 24). As part of this survey, some groups of aquatic Frankfurt am Main, and were included in the present study. insects were studied for their use in a classifi cation of the In 2006, Dr. Tohru Naruse and the authors visited Langkawi island’s streams, especially Ephemeroptera, Plecoptera, and for three days to explore the species diversity of water bugs Trichoptera (Yap, 2005). The check-list presented by Yap and crabs. The intensive collections primarily focused on a (2005) included four genera of Gerromorpha (Amemboa diverse range of habitats in order to record as many species sp., Halobates sp., Pseudovelia sp., and Rhagovelia sp.). as possible. Pseudovelia could not be confirmed here because the material studied by Yap was unavailable for the present study. The record of the marine genus Halobates from the MATERIAL AND METHODS island’s centre also appears doubtful, thus the Gerromorpha data obtained by Yap (2005) were not included in the Collecting. – Field work was carried out from 20Ð22 present paper. November 2006. Samples were taken with hand nets from eleven sites throughout the island (Fig. 1). The following

279 Zettel & Tran: Water bugs from Langkawi, Malaysia alphabetical list of sampling localities (including those of Durian Perangin: waterfalls with large pools, leg. A.D. Tran, other workers) contains the collecting codes used also in H. Zettel & T. Naruse, 21 Nov.2006 (TAD0618, HZL5) the taxonomic section. & leg. Kovac, 14 Dec.1993 (KV2). Northwestern part of the island (Datai and Telagah Tujuh Gunung Raya: small stream on way to summit, leg. A.D. areas): Tran, H. Zettel & T. Naruse, 21 Nov.2006 (TAD0617, Datai, environment: leg. E. Heiss & Perner, 12 Mar.1995 HZL4a). (HP1). Stream near road linking Padang Gaong Rd to Makam Datai rain forest: leg. E. Heiss, 2Ð10 Nov.2002 (HE1). Mahsuri Rd: leg. A.D. Tran & H. Zettel, 22 Nov.2006 Datai Resort, pool: leg. E. Heiss, 12 Apr.2008 (HE3). (TAD0622, HZL9). Pantai Datai: 18 Dec.1993, leg. D. Kovac (KV5). Northeastern part of the island (Tanjung Rhu areas): Pantai Kok, near Kuala Teriang, coastal pool: 13 Dec.1993, Jalan Tanjung Rhu, fi sh pond: at road, with dense vegetation, leg. D. Kovac (KV1). leg. H. Zettel, 21 Nov.2006 (HZL7a). Pebble beach near Sungei Lengara: leg. A.D. Tran, H. Zettel Jalan Tanjung Rhu, mangroves: tidal channels and pools, & T. Naruse, 20 Nov.2006 (TAD0615, HZL3a). leg. A.D. Tran, H. Zettel & T. Naruse, 21 Nov.2006 Swamp next to road to Telaga Tujuh: large, open water, (TAD0619, HZL6). near beach, leg. A.D. Tran, H. Zettel & T. Naruse, 22 Jalan Tanjung Rhu, rocky shore: leg. A.D. Tran, H. Zettel Nov.2006 (TAD0621, HZL8). & T. Naruse, 21 Nov.2006 (TAD0620, HZL7b). Sungei Lengara: river mouth, leg. H. Zettel, 20 Nov.2006 Pantai Rhu: 16 Dec.1993, leg. D. Kovac (KV4). (HZL3b). Telaga Tujuh [= Seven Wells] Ð Air Telaga: streams & Repositories. – Voucher specimens are deposited in the waterfalls, leg. A.D. Tran, H. Zettel & T. Naruse, 20 Natural History Museum Vienna, Austria (NHMW), in Nov.2006 (TAD0613, HZL1a, HZL1b) & leg. D. Kovac, the Zoological Reference Collection, National University 19 Dec. 1993 (KV6) & leg. E. Heiss, 4 Nov.2002 of Singapore (ZRC) and in the Senckenberg Museum, (HE2). Frankfurt am Main, Germany (SMFD). Specimens collected Temurun Waterfalls [= Sungei Temurun, Air Temurun]: by the fi rst author and by Dr. Ernst Heiss were dry-mounted, stream and waterfall with deep pool, leg. A.D. Tran, H. those collected by the second author were kept in 70 % Zettel & T. Naruse, 20 Nov.2006 (HZL2, TAD0614), ethanol. Specimens collected by Dr. Damir Kovac and leg. D. Kovac, 15 Dec.1993 (KV3) & leg. E. Heiss, 15 deposited in ZRC and SMFD, as well as paratype specimens Apr. 2008 (HE4). from other parts of Malaysia and from Singapore in ZRC, Central part of the island (Gunung Raya and nearby were partly dry-mounted during this study, but another part areas): of the series was kept in 70 % ethanol. Air Tejun: small forest stream near Kampung Buku, leg. A.D. Tran, H. Zettel & T. Naruse, 22 Nov.2006 Identification. – The following literature was used (TAD0623, HZL10). for identification: Lansbury (1972, 1973) for Nepidae;

Fig. 1. Map of Langkawi with sampling localities. Filled squares and circles = freshwater habitats; Unfi lled squares and circles = marine habitats. Squares = collections by the authors; circles = other collections.

280 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Nieser (2000, 2002) for Micronectidae; Nieser (2004) Ranatra parmata Mayr, 1865 for Notonectidae and Pleidae; Yang & Zettel (2005) for Hydrometridae; Andersen (1989, 1992, 2000), Yang & Material examined. – (all macropterous): Air Tejun: 1 male, 1 Polhemus (1994), and Andersen et al. (2002) for Veliidae; female, HZL10; 2 females, TAD0623. Andersen (1975, 1980), Polhemus & Andersen (1984), Chen & Nieser (2002), Polhemus (1994, 2001), Cheng et Distribution. – From northern Thailand to the Lesser Sunda al. (2001), and Andersen & Cheng (2004) for Gerridae. Islands (Lansbury, 1972). Northern records possibly belong Taxa not included in these references were identifi ed by to R. lansburyi Chen, Nieser & Ho, 2004 described from comparison with specimens in ZRC or NHMW; comparison Yunnan and Chiang Mai (see Chen et al., 2004). First record was also used to confi rm the results of our identifi cations. from Malaysia.

Description of new taxa. – Type specimens were studied under binocular microscopes. Structures were measured BELOSTOMATIDAE using an ocular micrometer and illustrated (Figs. 7Ð23) using a camera lucida. Body length, which is strongly Diplonychus rusticus (Fabricius, 1871) depending on preparation of specimens, is measured in tenths of millimetres, other measurements in hundredths Material examined. – Stream near road linking Padang Gaong Rd of millimetres. Eye Index (in Helotrephidae) is minimum to Makam Mahsuri Rd: 1 female (macropterous), HZL9. eye distance : maximum eye width, both measured perpendicular to median line of head. Digital photographs Distribution. – From India to Japan and Australia (Andersen (Figs. 2Ð6) were taken with a Leica DFC camera attached to & Weir, 2004). a Leica MZ16 binocular microscope with the help of Image Manager IM50 and processed with Auto-Montage Pro and Adobe Photoshop 7.0 programs. MICRONECTIDAE Micronecta (sensu stricto) drepani Nieser, 2000 TAXONOMY Material examined. – Temurun Waterfalls: 6 males, 5 females (macropterous), HZL2. NEPIDAE Distribution. – Thailand (Nieser, 2000). First record from Cercotmetus brevipes Montandon, 1909 Malaysia. Material examined. – Stream near road linking Padang Gaong Rd to Makam Mahsuri Rd: 1 male (macropterous), HZL9. Micronecta (sensu stricto) haliploides Horváth, 1904 Distribution. – From northeastern India and southern Material examined. – Telaga Tujuh Ð Air Telaga: 1 female China to Java, , and the Philippines (Lansbury, (macropterous), HE2. 1973). Lansbury (1973) records this species from “Telaga Pabila” a place which we were unable to locate, but may Distribution. – From India and to , Java be in Malaysia. Otherwise, this is the first record from and Bali (Nieser, 2002). Malaysia.

Micronecta (sensu stricto) johorensis Fernando, 1964 Ranatra longipes thai Lansbury, 1972 Material examined. – (all brachypterous): Telaga Tujuh Ð Air Material examined. – Stream near road linking Padang Gaong Rd Telaga: 8 males, 4 females, HZL1a. Temurun Waterfalls: 15 males, to Makam Mahsuri Rd: 1 male, 1 female (macropterous), HZL9. 2 females, HZL2.

Remarks. – Because of the different paramere compared Distribution. – Johor in Western Malaysia and Singapore with the nominate form (see Lansbury, 1972), this taxon (Nieser, 2002). First record from Kedah, which to our should have the status of a distinct species. knowledge is the northernmost recorded distribution.

Distribution. – Thailand (Lansbury, 1972). Chen et al. (2005) list the Malay Peninsula with a question mark. First Micronecta (Mesonecta) polhemusi Nieser, 2000 record from Malaysia. Material examined. – (all macropterous): Telaga Tujuh Ð Air Telaga: 41 males, 29 females, HZL1a; 1 male, 1 female, HZL1b; 6 males, 7 females, TAD0613.

281 Zettel & Tran: Water bugs from Langkawi, Malaysia

Distribution. – Thailand, Vietnam, and Singapore (Nieser, Enithares metallica Brooks, 1948 2002). First record from Malaysia. Material examined. – (all macropterous): Temurun Waterfalls: 10 males, 5 females, HZL2; 2 males, 1 female, TAD0614, 3 males, Micronecta (Sigmonecta) quadristrigata Breddin, 1905 1 female, KV3. Air Tejun: 2 males, 2 females, L10HZ; 1 male, TAD0623. Material examined. – (all macropterous): Telaga Tujuh Ð Air Telaga: 1 male, 2 females, TAD0613; 11 females, HZL1a. Swamp Distribution. – Thailand, Vietnam, and West Malaysia on way to Telaga Tujuh: 1 male, HZL8. (Nieser, 1998).

Distribution. – Widespread from Iran to Australia (Nieser, 2002). PLEIDAE

Paraplea liturata (Fieber, 1844) NAUCORIDAE Material examined. – Swamp next to road to Telaga Tujuh: 1 Heleocoris sp. female (macropterous), HZL8.

Material examined. – Air Tejun: 1 nymph, TAD0623. Distribution. – From India to , New Caledonia; several records from West Malaysia (Nieser, 2004). Remarks. – The only species of Heleocoris thus far recorded from the Malay Peninsula is H. ovatus Montandon, 1897 (Chen et al., 2005); however, the genus needs revision, and HELOTREPHIDAE nymphs cannot be identifi ed to species at present. Idiotrephes chinai Lundblad, 1933

NOTONECTIDAE Material examined. – Telaga Tujuh Ð Air Telaga: 6 males, 1 female (brachypterous), KV6; 2 males (brachypterous), 5 males, 10 females (macropterous), HZL1a; 1 male, 1 female Anisops breddini Kirkaldy, 1901 (brachypterous), 5 males, 4 females (macropterous), HZL1b; 1 female (brachypterous), TAD0613. Material examined. – Datai Resort, pool: 1 female (macropterous), HE3. Distribution. – West Malaysia, Sumatra, and Borneo (Papá ek & Zettel, 2000), southern Thailand (Sites & Distribution. – From India and Sri Lanka to Java and Polhemus 2002). Sulawesi (Nieser, 2004).

Hydrotrephes langkawicus, new species Anisops kuroiwae Matsumura, 1915 (Figs. 2, 6-12) Material examined. – Telaga Tujuh Ð Air Telaga: 1 female Material examined. – Holotype (macropterous male) and (macropterous), HE2. paratypes (1 hindwing-micropterous female, 3 macropterous males, 2 macropterous females), HZL9, labeled “MALAYSIA, Distribution. – From India to Iriomote (off Japan), Taiwan, Kedah\ C-Langkawi, S slopes\ of Gn. Raya, lowland\ stream, the Philippines, and Singapore (Nieser, 2004). 22.11.2006\ leg. H. Zettel (HZL9)”, holotypes and paratypes in NHMW, 1 paratype male in ZRC.

Anisops tahitiensis Lundblad, 1934 Description of macropterous male. – Habitus: see Figure 2. Body size: length 1.9Ð2.0 mm, width 1.35Ð1.40 mm. Material examined. – Temurun Waterfalls: 1 male (macropterous), KV3. Datai Resort, pool: 1 female (macropterous), HE3. Colour: Yellow with extended dark brown markings on dorsum, especially on head (Figs. 2, 6). Venter mostly Distribution. – From the Andaman Islands and Vietnam brownish. Legs and antennae yellow; rostrum light brown. through Malesian region to Australia, Tahiti, Guadalcanal, and Okinawa (Nieser, 2004); with several records from Cephalonotum with lateral margins behind eyes slightly West Malaysia and Singapore (Kovac & Yang, 1995; concave in dorsal view; sharp margin of pronotal part Nieser, 2004). ending in short distance from posterolateral corner and there forming a small, rather blunt angulation; head with densely set small punctures, with very narrow interspaces, almost dull; disk of pronotum set with numerous very fi ne micropunctures, and with scattered, unequally distributed and

282 THE RAFFLES BULLETIN OF ZOOLOGY 2009 somewhat larger punctures becoming denser towards sides. Ventral carinae (Fig. 8): Prosternal carina with posterior Mesoscutellum 0.9 times as long as wide, with puncturation corner approximately rectangular, with posterior edge of similar size, but slightly denser than on disk of pronotum, slightly concave; apices of meso- and metasternal carina micropunctures medially obliterated. Hemelytron with thin-laminate, that on mesosternum strongly reduced; slightly stronger puncturation, interspaces shagreened and carina of sternite 3 with few small denticles, the proximal dull. Genal plate stout; pronotal plate (Fig. 7) with shallow one variably enlarged. Abdominal segments strongly incision, anteriorly relatively wide. Inner corner of propleural asymmetrical. plate broadly convex. Eye index: 2.1Ð2.2. Fourth rostral segment 2.3 times as long as segment 3. Aedeagus (Fig. 9) moderately slender, apically rather stout and slightly bent to right side; with narrow apical

Figs. 2Ð6. Habitus of (2) Hydrotrephes langkawicus, new species (macropterous male, paratype). (3) Strongylovelia narusei, new species (apterous female, paratype). (4) Microvelia (Picaultia) minutissima, new species (apterous female, paratype). (5) Microvelia (Picaultia) minutissima, new species (macropterous male, holotype, right forewing broken off). (6) Frontal view of cephalonotum of Hydrotrephes langkawicus, new species (macropterous male, paratype).

283 Zettel & Tran: Water bugs from Langkawi, Malaysia plate posteriorly extended into short spine. Right paramere on the islands of Borneo (fi ve species), Sumatra, Siberut, (Fig. 10) shorter than left paramere, slender-lanceolate, and Nias (one species each) (Zettel, 2004a; Papá ek & curved, apex minutely pointed. Left paramere (Fig. 11) Zettel, 2005). Hydrotrephes langkawicus, new species is moderately slender, distally evenly narrowed and slightly one of the smallest species of the genus; in the H. martini curved, apex narrowly rounded. group only H. nitidus Zettel, 2004, a strongly shiny species with deeply emarginate prosternal carina, is of similar Description of macropterous female. – Body size: length size. The genital structures of the male of H. langkawicus 2.1Ð2.2 mm, width 1.46Ð1.49 mm. Eye index: 2.1. Most are characteristic. Further, the combination of the weakly characteristics similar to that of male, except the following. emarginate prosternal carina, the reduced lamina on the Abdomen symmetrical. Sternite 6 with concave hind mesosternal carina, and the lobate subgenital plate of the margin. Subgenital plate (Fig. 12) with broad mediodistal female is unique. lobe with broadly convex hind margin; inner ridge strongly concave, almost semicircular. Ventral laterotergites 8 Distribution. – Only known from the type locality on slender. Langkawi Island.

Hindwing-micropterous female: body size: length 2.1 mm, width 1.42 mm; eye index: 2.6; pronotum with MESOVELIIDAE posterolateral corners less elevated and with angulation of lateral margin more blunt; hemelytron without embolar Mesovelia horvathi Lundblad, 1933 and claval sutures; other characteristics as in brachypterous female. Material examined. – Swamp next to road to Telaga Tujuh: 1 female (apterous), HZL8. Stream near road linking Padang Gaong Hindwing-micropterous male: unknown. Rd to Makam Mahsuri Rd: 2 females (apterous), HZL9.

Etymology. – Named after the island of type locality. The Distribution. – Widespread in Australasia from southern species epithet is a Latinized adjective. China to Australia, and in the southeastern Palaearctic (Japan) (Polhemus & Polhemus, 2001); recorded from Remarks. – This species belongs to the Hydrotrephes several localities in West Malaysia (Yang et al., 1999; martini group as defi ned by Zettel (2000a). Hitherto, this Polhemus & Polhemus, 2001). species group contained eight described species, distributed

Figs. 7Ð12. Hydrotrephes langkawicus, new species: 7, genal and pronotal plate; 8, ventromedian carina of thorax and abdomen, with variations of prosternal carina, mesosternal carina, and carinae of sternites 2 and 3; 9, aedeagus, right view; 10, right paramere, right view; 11, left paramere, right view; 12, sternite 7 of female, ventral view, pilosity omitted.

284 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Mesovelia vittigera Horváth, 1895 Hydrometra orientalis Lundblad, 1933

Material examined. – Swamp next to road to Telaga Tujuh: 4 Material examined. – Swamp on way to Telaga Tujuh: 2 males, 1 female (apterous), 3 males (macropterous), HZL8; 1 males, (macropterous), HZL8; 2 males (macropterous), 1 male (apterous), 1 female (brachypterous), 1 male (macropterous), female (brachypterous), TAD0621. Telaga Tujuh Ð Air Telaga: TAD6021. 1 female (macropterous), TAD0613. Stream near road linking Padang Gaong Rd to Makam Mahsuri Rd: 1 male, 1 female Distribution. – Except for some remote oceanic islands in (macropterous), TAD0622. all warm regions of the Old World (Polhemus & Polhemus, 2001); recorded earlier from West Malaysia by Yang et al. Distribution. – Widespread from southern China to (1999). Australia (Yang & Zettel, 2005).

Mesovelia sp. VELIIDAE

Material examined. – Swamp next to road to Telaga Tujuh: 1 Strongylovelia narusei, new species male, 1 female (apterous), HZL8. (Figs. 3, 13Ð16)

Remarks. – This probably undescribed species is similar Material examined. – Holotype (apterous female) and paratypes and closely related to M. horvathi, but differs in orange (4 apterous females, 3 apterous males, 1 macropterous-dealate brown ground colour of body with weakly marked dark male), HZL10, labeled “MALAYSIA, Kedah\ C-Langkawi, pattern, relatively long pronotum of apterous morph, short Air Tejun,\ nr Kampung Buku, small\ stream, 22.11.2006\ leg. H. Zettel (HZL10)”, holotypes and paratypes in NHMW, 1 tarsomeres 2, and short apex of parameres of males. Polhemus paratype female and 1 paratype male in ZRC. Ð Further paratypes & Polhemus (2001) regarded M. horvathi as a variable and from Malaysia: 1 apterous female, 1 apterous male “MAL, widespread species (see above) and synonymized it with M. Terengganu, Sekaya,\ Sg. Brang. HK Lua,\ 21-OCT-1998,\ japonica Miyamoto, 1964, from Japan. The species complex LHK040” (ZRC). certainly needs careful revision. Description of apterous female. – Measurements: Body length 1.31Ð1.42 mm (holotype 1.42 mm). Body width HYDROMETRIDAE 0.74Ð0.80 mm (holotype 0.79 mm). Relative lengths of antennomeres 1Ð4 (holotype): 0.9 : 1.0 : 1.8 : 1.4. Relative Hydrometra annamana Hungerford & Evans, 1934 lengths of leg segments (relative to mesofemur length = 100; holotype): profemur 45, protibia 44, protarsus Material examined. – Swamp next to road to Telaga Tujuh: 1 male 4+14, mesofemur 100, mesotibia 81, mesotarsus 36+23, (brachypterous), 2 females (macropterous), HZL8. metafemur 71, metatibia 56, metatarsus 9+14.

Distribution. – Thailand and Vietnam (Yang & Zettel, Body tear-shaped, sides of abdomen not strongly convergent 2005). Vitheepradit et al. (2005) recorded H. annamana (Fig. 3). Dorsal aspect black except some indistinct dark already from the most-southern part of Thailand (Satun, orange marks along dorsal eye margin and mesonotum Songkhla) close to the Malaysian border. First record from yellowish white except narrow lateral margins. In lateral Malaysia. aspect pro-, meso-, and metapleura yellowish white except narrow or broad stripe along dorsal margin of meso- and metapleura black, mesacetabula with or without dark mark, Hydrometra jaczewskii Lundblad, 1933 and metacetabula with narrow or broad dark stripe distally. Ventral aspect black, except prosternum and mesosternum Material examined. – (all brachypterous): Air Tejun: 1 male, 1 yellowish white with or without infuscated acetabula. female, HZL10. 1 male, 1 female, TAD0623. Antenna and legs black, except metatrochanter, profemur except apex, and basal half of metafemur whitish; coxae Distribution. – Southern China, West Malaysia, Sumatra, variably infuscated. Java, and Borneo (Yang & Zettel, 2005). Median pronotal length 0.35 times eye length. Dorsum of thorax with very short, decumbent pilosity. In lateral Hydrometra kelantan Polhemus & Polhemus, 1995 aspect, head and mesonotum with scattered black erect setae, those on mesonotum much shorter than those Material examined. – Temurun Waterfalls: 1 male (macropterous), HZL2. on head. Posterior corners of meso-metanotum slightly acute, apex without conspicuous long setae. Structures of Distribution. – Thailand and West Malaysia (Vitheepradit abdomen (Figs. 3, 13, 14) relatively simple: in dorsal et al., 2005; Yang & Zettel, 2005). view (Fig. 13), connexiva nearly evenly converging, slightly more on segments 5 and 6. Laterotergites directed

285 Zettel & Tran: Water bugs from Langkawi, Malaysia more or less dorsad, slightly laterodorsad anteriorly Description of macropterous male. – Body length and weakly mediodorsad posteriorly, so that all tergites 1.18 mm, body width 0.67 mm. Colour similar as in completely, and all sternites partly visible in dorsal view. apterous morph, but posterior half of pronotum with Each sternite laterally with 1Ð2 long, black setae beneath half-ovate yellowish mark, and metafemora yellowish dorsal margin; sternite 7 additionally with relatively long white in proximal three-fi fths. Pronotum very large, at pilosity at connexival corners. Laterotergites 2Ð4 and 7 midline about 2.0 times as long as eye, covering meso- and tergites 1Ð7 with short pilosity; laterotergites 5-6 with and metanotum, with distinct humeri. Wings of dealate conspicuous, mesad directed setae; tergite 7 with some specimen broken off at base, approximately at level of long black setae on its lateral portions. Suture between posterior apex of pronotum. All tergites almost fl at, tergite tergites 1, 2, and 3 weakly impressed, medially hardly 1 not longer than tergite 2. curved cephalad; all other sutures well developed and nearly straight. Tergites without median elevations, and Macropterous female: unknown. dull. Hind margin of tergite 7 slightly convex; tergite 8 medially with shallow impression, with hind margin Etymology. – This species is dedicated to Tohru Naruse, who bearing few long, black setae. In lateral view (Fig. 14), accompanied the authors for fi eld work in Langkawi. few long setae surpassing connexival margin; connexival corners acute, with black pilosity. Gonocoxa plate-like; Remarks. – This species belongs to the S. esakii group proctiger small, directed ventrocaudad. as defined by Lansbury & Zettel (1997). Within this group, two species complexes are recognized. The S. Description of apterous male. – Measurements: Body esakii complex includes S. esakii Lansbury & Zettel, 1997 length 1.06Ð1.11 mm. Body width 0.62Ð0.66 mm. from Borneo, S. palawanensis Lansbury & Zettel, 1997 from Palawan (Philippines), and some other undescribed Colour similar to that of female, except yellowish marks Bornean species. It can be distinguished by wide tergites on meso- and metanotum separated by narrow black line of the apterous female that are completely visible in and pronotum medially with small orange mark in one dorsal view as the laterotergites are directed laterad or specimen. Dorsum of thorax and abdomen shinier than laterodorsad, by tufts of hairs on sternite 2 of the female, in female. Median pronotal length 0.4 times eye length. and by a slender distal section of the parameres of the Black setae laterally on mesothorax and sternites similar males (see Lansbury & Zettel, 1997). The second complex, with those of female, longest setae on sternites ca. 0.10 the S. aberrans complex, contains S. aberrans Lansbury & mm long. Dorsum of body with very short pubescence, Zettel, 1997 from Borneo, S. setosa Zettel & Tran, 2005 but head and tergite 7 with some longer setae in addition. from Vietnam, S. narusei, and several other undescribed Suture between tergites 1 and 2 weak, other sutures between species from Borneo and southeast Asia. Species of this tergites well developed. Tergite 5 circa 8 times as wide as complex can be recognized by the laterotergites of the long at midline. Paramere (Fig. 15, 16) moderately curved apterous female which are fl apped over the tergites to a at basal third, strongly twisted, relatively broad, subapically varying degree (at least slightly on segments 6 or 7), by a weakly widened (in caudal view), apex very acute. row of long setae on the sternites of the female (situated

Figs. 13Ð16. Strongylovelia narusei, new species. (13) Abdomen of apterous female (with corners of meso-metanotum), dorsal view. (14) Abdomen of apterous female, lateral view. (15) Paramere of male, lateral view. (16) Paramere of male, perpendicular view on apical part.

286 THE RAFFLES BULLETIN OF ZOOLOGY 2009 parallel with and beneath the connexival margin), by the Haloveloides (s. str.) sundaensis Andersen, 1992 absence of hair tufts on the female’s sternite 2, and by the subapically slightly widened paramere of the male Material examined. – (all apterous): Pantai Rhu: 16 males, (male of S. aberrans unknown). Additionally, the species 29 females, KV4. Jalan Tanjung Rhu, rocky shore: 1 female, have a similar colour pattern (but some variation in the HZL7b; 1 male, 1 female, TAD0620. extent of the yellow base of the metafemur) and agree in Former record from Langkawi: 1 male (paratype) Langkawi Is., 6.IV.1934, leg. R. Brown, in Coll. J.T. Polhemus (ANDERSEN the general structures of meso-metanotum and abdomen. 1992). For comparison, the authors used the type series of S. setosa and the holotype (female) of S. aberrans. Beside Distribution. – Widely distributed along the coasts of the specimens from Langkawi, only two specimens from the Sunda Shelf area; recorded from southern Thailand, Terengganu match the diagnostic characters of S. narusei Malaysia (peninsular, P. Tioman, Sarawak), Indonesia and were included in the type series. Numerous specimens (Pulau Batam, Java), and Vietnam (Andersen, 1992; Yang were studied from other parts of peninsular Malaysia et al., 1999; Zettel & Tran, 2006). (Johore), from Singapore, from the Indonesian islands of Batam and Bintan, and from Sarawak on Borneo (all in ZRC), but it was concluded that they either belong Xenobates argentatus Andersen, 2000 to additional undescribed species or that at least the differences are too big to include them in the type series Material examined. – Jalan Tanjung Rhu, mangroves: 1 female of S. narusei without a more detailed revision of the whole (apterous), HZL6. complex. Strongylovelia narusei differs from S. aberrans and S. setosa (and from most other material studied, Distribution. – Described from southern Thailand, Borneo except one population from Johore which is eventually (Sarawak), and southern Philippines (Andersen, 2000), conspecifi c with S. narusei) in a rather conspicuous long but records from Borneo and Philippines belong to pilosity on laterotergites 5 and 6 of the apterous female, undescribed, closely-related species (unpublished data). and from S. setosa in the more slender apex of the Confi rmed record from Malaysia. paramere of the male. The ratio of antennomeres 2 and 3 of females is 1.9Ð2.0 in S. aberrans, 1.7Ð1.8 in S. setosa and S. narusei. The posterior corners of the meso-metanotum Xenobates mandai Andersen, 2000 of apterous females bear a dense group of long black setae in S. narusei, which is absent or inconspicuous in other Material examined. – Jalan Tanjung Rhu, mangroves: 12 males, species. An important characteristic to separate species of 21 females (apterous), HZL6. the S. aberrans complex might be the presence or absence of long setae on tergite 7 of apterous females, which either Distribution. – Described from Singapore (Andersen, occur in small numbers on its lateral areas or in a more 2000) and recorded from Vietnam (Zettel & Tran, 2006). or less transverse row close to the tergite’s hind margin. First record from Malaysia. Unfortunately, these setae tend to break off, so that in some cases either only their base is visible or they cannot be seen at all. Such setae could be observed on the lateral Xenobates murphyi Andersen, 2000 parts of tergite 7 of S. narusei and S. aberrans, but not in S. setosa. The apterous female of S. setosa differs also Material examined. – Pantai Rhu: 2 females (apterous), KV4. from both species in a deeper, more elongate depression of the tergite 8. Former record for Langkawi: 1 male, 3 females (paratypes), same locality data (Andersen, 2000). Distribution. – Malaysia: Langkawi, Terengganu. Distribution. – West Malaysia, Singapore, Borneo, and Philippines (Andersen, 2000). Halovelia malaya Esaki, 1930

Material examined. – (all apterous): Pantai Datai: 1 male, 2 Microvelia (Picaultia) douglasi Scott, 1874 females, KV5. Pebble beach near Sungei Lengara: 2 males, 2 females, HZL3a; 3 males, 2 females, TAD0615. Jalan Tanjung Material examined. – Telaga Tujuh Ð Air Telaga: 1 male Rhu, rocky shore: 9 males, 5 females, HZL7b; 3 males, 5 females, (apterous), 2 females (macropterous), HZ1a; 1 male, 1 female TAD0620. (macropterous), TAD0613. Jalan Tanjung Rhu, fi sh pond: 1 male, 1 female (apterous), 2 females (macropterous), HZL7a. Swamp Distribution. – West coast of the Malay Peninsula, with on way to Telaga Tujuh: 4 males, 2 females (apterous), 2 males, 6 females (macropterous), HZL8. records from southern Thailand (Phang Nga, Phuket) and West Malaysia (Negeri Sembilan, Pulau Angsa) (Andersen, Distribution. – From India to Japan and Australia 1989). One male from Vietnam was preliminarily identifi ed (Andersen & Weir, 2004). as this species (Zettel & Tran, 2006).

287 Zettel & Tran: Water bugs from Langkawi, Malaysia

Microvelia (Picaultia) minutissima, new species 1 male (apterous), 1 female (apterous) “Nature Reserves Survey\ (Figs. 3, 4, 17-23) Chestnut Dr., NS 138B\ Singapore\ 19 May 1994” (ZRCS); 1 male, 1 female (apterous) “stm #H, Mac Ritchie\ Forest, 2.2.1994\\ Material examined. – Holotype (macropterous male) and paratypes NS124F” (ZRCS); 1 female (apterous) “Nature Reserves Survey\ (2 apterous females, 1 macropterous male, 5 macropterous MacRitchie, NS 161D\ Singapore\ 13 June 1994” (ZRCS); 2 females), HZL1b, labeled “MALAYSIA, Kedah\ W-Langkawi, females (apterous) “Nature Reserves Survey\ MacRitchie, NS Telaga Tujuh\ stream, 20.11.2006\ leg. H. Zettel (HZL1b)”, 161B\ Singapore, 17 June 1994” (ZRCS); 1 male (apterous), 1 holotype and paratypes in NHMW, 1 paratype macropterous female (apterous) “Nature Reserves Survey\ Nee Soon Swamp female in ZRC. Ð Further paratypes from Malaysia: 1 male Forest\ NS 158B, Singapore\ 13 June 1994” (ZRCS); 1 female (macropterous), 1 female (macropterous) “MAL- Selangor, Ulu\ (apterous) “SIN- Nee Soon\ swamp forest;\ 12-JUN-1995\ HK Lua Gombak;\ 06-MAY-1996\ HK Lua et al.\ LHK0305” (ZRCS). et al.\ NS0187A” (ZRCS); 1 female (apterous) “SIN- Nee Soon\ Ð Further paratypes from Singapore: 7 males, 5 females (apterous) KL Yeo\ 06-MAY-1992\ YKL0794A” (ZRCS); 1 male, 2 females “SIN- Bt. Timah NR\ HK Lua et al.\ 08-DEC-1995\ NS0209” (apterous) “ZRC Nee Soon Swamp Forest\ NS126A upstream #23\ (ZRCS, NHMW); 2 females (apterous) “ZRC Chestnut Drive\ 28 April 1994” (ZRCS). NS 128A\ 5th May 1994” (ZRCS); 3 males (apterous) “SIN- Chestnut Dr.,\ Seletar Reservoir,\ 26-MAY-1994\ HK Lua et Description of macropterous male. – Body length 1.28Ð al.\ NS0142C” (ZRCS, NHMW); 3 females (apterous) “SIN, 1.32 mm (holotype: 1.31). Pronotal width 0.56Ð0.58 mm Chestnut Dr.,\ Seletar Reservoir,\ “Ua2” side stream; HK Lua et (holotype: 0.58). Length of second antennomere of holotype al.\ 26-V-1994, NS142G” (ZRCS); 2 females (apterous) “Nature 0.11 mm. Length of metatibia of holotype 0.42 mm. Reserves Survey\ Chestnut Dr., NS 142C\ 26 May 1994” (ZRCS);

Figs. 17Ð23. Microvelia (Picaultia) minutissima, new species: 17, fore tibia and tarsus of male; 18, middle tibia and tarsus of male; 19, abdomen of macropterous male, lateralview; 20, abdomen of macropterous male, ventral view; 21, right paramere of male, lateral view; 22, abdomen of apterous female, dorsal view; 23, abdomen of apterous female, lateral view.

288 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Colour (Fig. 3): Head and pronotum brownish, humeri, and laterotergites 4Ð5 also browly infuscated. Tergites 1Ð3 anterior and posterior margin of pronotum yellowish orange (Ð4) more or less frosted. to different extend. Sides and venter mainly dark brown, connexival margins, segments 7 and 8, and genitalia yellow Pilosity as in macropterous morph. or light orange. Antennae brown, except base yellow. Legs yellow, but apices of femora and tibiae, and all tarsi Legs, abdomen, and genitalia as in macropterous morph. brownish. Fore wings pale brown, base and two weakly Pronotum much smaller, but long compared with some delimited spots whitish. other species of the genus, medianly ca. 0.8 times as long as head and almost completely covering metanotum, hind Pilosity: Generally short, except lateral hind margin of margin convex. Sides of abdomen anteriorly subparallel, sternite 7 set with long setae. laterotergites moderately raised throughout. Tergite 7 much larger than preceding tergites, ca. 0.8 times as long as wide Dorsum without large black impressions. Head width ca. and slightly longer than tergites 5 and 6 combined. 1.2 times head length. Relative lengths of antennomeres 1Ð4 (holotype): 1.0 : 1.0 : 1.2 : 2.5. Relative lengths of leg Description of apterous female. – Body length 1.17Ð1.31 segments (relative to metatibia length = 100; holotype): mm. Pronotal width 0.48Ð0.57 mm. profemur 66, protibia 54, protarsus 32, mesofemur 74, mesotibia 66, mesotarsus 11+28, metafemur 85, metatibia Colour dorsally similar to that of apterous male, but in some 100, metatarsus 12+30. Profemur slender. Protibia straight, specimens dark parts more pronounced and giving a more distally widened, apically with long slender process set in distinct pattern. Tergites (1Ð) 2Ð3 frosted, 4Ð8 not frosted. blunt angle with tibia axis and bearing apically a minute Venter and sides as in macropterous female. grasping comb (Fig. 17). Mesotibia with short process bearing minute grasping comb (Fig. 18). Abdomen slender Pronotum as in apterous male. Abdomen (Figs. 22, 23) (Fig. 20). Sternite 6 without modifications. Sternite 7 usually very narrow, with sides anteriorly constricted, anteromedially slightly swollen, posteriorly with strong, narrowest at segment 3, slightly convex at segments 5-6 transverse impression, distinctly concave in lateral view (Fig. and then again narrowed at segment 7. In such specimens 19); hind margin medially slightly emarginated. Segment 8 laterotergites almost vertical throughout. In specimens and genital capsule small. Pygophore and proctiger slightly with more swollen abdomen (probably fi lled with eggs), asymmetrical. Left paramere reduced. Right paramere (Fig. laterotergites directed more laterad or even totally flat, 21) elongate, curved, distally slender. giving the abdomen a broader appearance. Tergite 7 ca. 0.7 times as long as broad at anterior margin and ca. 1.5 Description of macropterous female. – Body length 1.37Ð times as long as tergite 6; its sides strongly convergent 1.49 mm. Pronotal width 0.60Ð0.67 mm. posteriad. Tergite 8 almost as long as tergite 7, slightly longer than wide, and shallowly concave. Terminalia as in Colour as in male, except sternite 7 ventrally brown; in some macropterous morph. specimens, dorsum more infuscated. Etymology. – From Latin minutissimus; referring to the Pilosity: generally short, but laterotergites 2 with few longer species’ extremely small size. setae, sternite 7 at connexival corner with tuft of long setae and laterotergites 8 and complete posterior edge of tergite Remarks. – The presence of a mesotibial comb of the 8 with dense brush of long setae. male (Fig. 18) and the asymmetrical genitalia of the male with a long right (Fig. 21) and a reduced left paramere Legs simple. Abdomen slender, anteriorly without place M. minutissima in the subgenus Picaultia Distant, modifi cations. Tergite 8 forming a sharp edge, dorsal and 1913. The new species is one of the smallest in the genus posterior face forming a right angle; posterior face ca. and has a slender body (Figs. 4, 5). Apterous specimens 2.5 times as wide as long. Proctiger forming a prominent, have the dorsum usually orange to light brownish with ventrocaudad directed knob. Most of gonocoxa 1 concealed variably infuscated pronotum and abdomen. The male can by sternite 7. be recognized by the concave outline of sternite 7 in lateral view (Fig. 19), by the small genital capsule (Fig. 20), and by Description of apterous male. – Body length 1.16Ð1.23 the shape of the slender and curved right paramere (Fig. 21). mm. Pronotal width 0.45Ð0.48 mm. The female can be easily distinguished from other Picaultia species by characteristics of the abdomen: The tergite 8 Colour: Similar to macropterous morph. Head usually possesses a dense brush of equally long setae all along its orange. Pronotum brown with broad orange margin posterior edge which are more than half as long as the tergite anteriorly, posterior margin rarely with narrow yellow length (Fig. 22); in the apterous female, tergite 1 is usually margin. Tergites and laterotergites variably brownly completely frosted, tergites 2Ð3 discretely, but completely infuscated. Most commonly, laterotergites, tergite 7, frosted and tergites 4Ð8 usually not frosted at all. segment 8, and medial areas of tergites 1Ð3 orange, tergites 4Ð5 brown, in other specimens tergites 3Ð6 to 1Ð6 brown Distribution. – Malaysia (Langkawi, Selangor) and Singapore.

289 Zettel & Tran: Water bugs from Langkawi, Malaysia

Microvelia sp. female (macropterous), HZL2. Air Tejun: 1 male (macropterous), 1 female (apterous), HZL10; 1 male, 2 females (apterous), Material examined. – Telaga Tujuh Ð Air Telaga: 2 females TAD0623. (macropterous), TAD0613. Distribution. – Southwestern China, Thailand, Vietnam, Remarks. – The two females possibly belong to an and West Malaysia (Andersen, 1995, Zettel & Chen, 1996; undescribed species. Males are required for subgeneric both sub Limnometra matsudai). classifi cation and identifi cation.

Neogerris assimilis Andersen, 1975 Perittopus asiaticus Zettel, 2001 Material examined. – Temurun Waterfalls: 1 male (macropterous), Material examined. – Dati rain forest: 4 males, 1 female HZL2. (macropterous), HE1; Temurun Waterfalls: 2 males, 1 female (apterous), KV3; 5 males, 7 females (macropterous), TAD0614; Distribution. – Thailand, Singapore, Sumatra, Borneo 10 males, 10 females, HZL2. Gunung Raja: 36 males, 25 (Andersen, 1995, Chen & Zettel, 1998). First record from females (macropterous), HZL4a; 1 male (apterous), 2 males, 4 West Malaysia. females (macropterous), TAD0617. Durian Perangin: 2 females (macropterous), TAD0618. Neogerris parvulus (Stål, 1859) Distribution. – Southwestern China, Thailand, and West Malaysia (Zettel, 2001). Material examined. – Swamp on way to Telaga Tujuh: 1 male, 1 female (macropterous), 1 female (apterous), HZL8.

Rhagovelia sumatrensis Lundblad, 1933 Distribution. – Widespread in the southeastern Palaearctic and Oriental Region, eastwards to New Guinea and the Material examined. – Telaga Tujuh Ð Air Telaga: 2 females (Andersen, 1995); records from the (macropterous), HZL1a; 1 male, 1 female (macropterous), HZL1b. Philippines partly refer to N. philippinensis Zettel, 2004 and Temurun Waterfalls: 1 female (apterous), KV3. Durian Perangin: 6 males, 3 females (macropterous), HZL5. Stream near road linking all material east of the Wallace Line should be re-examined Padang Gaong Rd to Makam Mahsuri Rd: 1 female (apterous), for conspecifi city (Zettel, 2004b). HZL9.

Distribution. – From India to southeastern China and Limnogonus (s. str.) fossarum fossarum Lombok in Indonesia (Zettel, 2000b). (Fabricius, 1775)

Material examined. – Sungei Lengara: 1 male (macropterous), Rhagovelia singaporensis Yang & Polhemus, 1994 HZL3b. Swamp on way to Telaga Tujuh: 1 male, 1 female (macropterous), HZL8; 2 males (macropterous), 1 female (apterous), TAD0621. Material examined. – Gunung Raya: 1 male (macropterous), HZL4a. Telaga Tujuh Ð Air Telaga: 1 female (macropterous), HZL1a; 1 female (apterous), HZL1b. Durian Perangin: 1 female Distribution. – The typical subspecies from India to (macropterous), KV2; 1 female (macropterous), HZL5. Air Tejun: Japan, Philippines, Borneo, and Sumatra; other subspecies 8 males, 12 females (apterous), 2 males, 1 female (macropterous), eastwards to Australia and Vanuatu (Andersen, 1975). HZL6; 5 males, 10 females (apterous), 1 male (macropterous), TAD0623. Limnogonus (s. str.) nitidus (Mayr, 1865) Distribution. – Described from Singapore (Yang & Polhemus, 1994) and later recorded from the Malay Material examined. – (all macropterous): Sungei Lengara: 2 Peninsula and some Indonesian islands (Anambas, Natuna, males, 1 female, HZL3b. Telaga Tujuh Ð Air Telaga: 1 male Bintan, Java) by Tran & Yang (2004). (macropterous), KV6; 2 males, HZ1a; 1 female, TAD0613. Temurun Waterfalls: 1 female, HZL2. Stream near road linking Padang Gaong Rd to Makam Mahsuri Rd: 1 male, 2 females, HZL9; 1 male, TAD0622. Jalan Tanjung Rhu, mangroves: 1 male, GERRIDAE TAD0619. Swamp on way to Telaga Tujuh: 1 male, 2 females, TAD0621. Tenagogonus matsudai Miyamoto, 1967 Distribution. – From India to southern China, Philippines, Material examined. Ð Telaga Tujuh Ð Air Telaga: 2 females Sulawesi, and the Lesser Sunda Islands (Chen et al., (macropterous), KV6; 1 female (apterous), 2 females (macropterous), HZ1b; 1 male, 1 female (apterous), 1 male, 1 2005). female (macropterous), TAD0613. Temurun Waterfalls: 3 males, 1

290 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Limnogonus (Limnogonoides) pectoralis (Mayr, 1865) Rheumatogonus intermedius Hungerford, 1933

Material examined. – Jalan Tanjung Rhu, mangroves: 1 male, Material examined. – (all apterous): Datei environment: 1 female, 1 female (macropterous), HZL6; 2 males, 1 female (apterous), HP1; Air Tejun: 3 males, 2 females, HZL10; 5 males, 4 females, TAD0619. TAD0623.

Distribution. – Sri Lanka, eastern India, Myanmar, and Distribution. – Southern Thailand, West Malaysia, and southern Thailand (Andersen, 1975; Hecher & Zettel, 1996; Sumatra (Chen & Nieser, 2002). Buzzetti et al., 2006). First record from Malaysia.

Asclepios annadalei Distant, 1915 Amemboa incurvata Polhemus & Andersen, 1984 Material examined. – (all apterous): Pantai Rhu: 7 males, 5 females, KV4. Jalan Tanjung Rhu, mangroves: 5 males, 3 females, Material examined. – Air Tejun: 1 male, 1 female (apterous), HZL6. HZL10; 3 males, 2 females (apterous), TAD0623. Distribution. – From India to the Malay Peninsula (Chen Distribution. – West Malaysia and Sumatra (Polhemus & et al., 2005). Andersen, 1984).

Halobates (sensu stricto) esakii Miyamoto, 1967 Onychotrechus esakii Andersen, 1980 Material examined. – (all apterous): Pantai Rhu: 1 male, 2 Material examined. – Datai environment: 1 female (macropterous), females, KV4. Pantai Datai: 1 female, KV5. HP1; Telaga Tujuh Ð Air Telaga: 1 male, 1 female (apterous), HZL1a; 1 male (apterous), HZL1b; 4 males, 3 females (apterous), Distribution. – From the Malay Peninsula (west coast) to TAD0613. Temurun Waterfalls: 1 female (apterous), HZL2; the Philippines and Halmahera in Indonesia (Andersen & 3 males, 5 females (apterous), 3 males, 5 females (apterous) Cheng, 2004, Zettel, 2005). 2 males (macropterous), TAD0614. Durian Perangin: 1 male (macropterous), TAD0618. Halobates (sensu stricto) hayanus White, 1883 Distribution. – Thailand, Vietnam, and West Malaysia (Andersen, 1980; Polhemus & Andersen, 1984). Material examined. – (all apterous): Jalan Tanjung Rhu, rocky shore: 5 males, 3 females, HZL7b, 3 males, 3 females, TAD0620. Cylindrostethus malayensis Polhemus, 1994 Former record from Langkawi: 1 male, “Langkawi Is., 4.IV.1934, Material examined. Ð Stream near road linking Padang Gaong leg. R. Birch”, in the Natural History Museum, London (HERRING Rd to Makam Mahsuri Rd: 3 males, 4 females (apterous), 1961). HZL9; 2 males, 2 females (apterous), TAD0622. Distribution. – Indo-West Pacifi c, from the Red Sea to Distribution. Ð West Malaysia, Singapore, and Sumatra Australia (Andersen & Cheng, 2004). (Polhemus, 1994), populations from southern Thailand need revision. Halobates (sensu stricto) proavus White, 1883

Ptilomera (sensu stricto) tigrina Uhler, 1860 Material examined. – (all apterous): Pantai Kok: 1 female, KV1. Pantai Datai: 40 males, 34 females, KV5. Material examined. – Temurun Waterfalls: 2 males (apterous), HZL2, 2 males, 1 female (apterous), HE4. Durian Perangin: 1 Distribution. – From the Nicobar Islands and southern male, 1 female (apterous), 1 male, 1 female (macropterous), HZL5. Thailand until Vanuatu (Andersen & Cheng, 2004). Stream near road linking Padang Gaong Rd to Makam Mahsuri Rd: 2 females (apterous), HZL9. Telaga Tujuh Ð Air Telaga: 1 male (apterous), 1 male (macropterous), HZL1a; 1 male (apterous), Halobates (sensu stricto) sexualis Distant, 1903 TAD0613. Gunung Raya: 2 males (apterous), TAD0617. Air Tejun: 1 female (apterous), 1 female (macropterous), HZL10. Material examined. – Pantai Rhu: 3 males, 4 females (apterous), KV4. Material examined. – From Myanmar and southern China to the Malay Peninsula; in West Malaysia a common species Distribution. – Malay Peninsula and Sri Lanka (Andersen (Polhemus, 2001). & Cheng, 2004).

291 Zettel & Tran: Water bugs from Langkawi, Malaysia

Metrocoris nigrofascioides Chen & Nieser, 1993 ping Chen. Using the key characters in Chen & Nieser (1993), male specimens might be identifi ed as M. nigrofasciatus Material examined. – Datai rain forest: 1 male, 2 females Distant, 1903 due to the fact that the subapical tooth on the (apterous), HE1; Telaga Tujuh Ð Air Telaga: 1 male, 4 females fore femur is of variable shape and often reduced in small (apterous), 2 females (macropterous), HZ1b; 2 males, 2 females apterous and in all macropterous specimens. Distinction of (apterous), TAD0613. Sungei Lengara: 1 male (apterous), these two species should be based on genitalia, especially HZL3b. Air Tejun: 1 male, 3 females (apterous), HZL10; 3 M. squamifer males, 2 females (macropterous), KV6; 1 female (apterous), on the shape of the paramere. The paramere of TAD0623. Durian Perangis: 1 male (apterous), 2 males, 5 has a distinct ventral angle Ð although rarely so strongly females (macropterous), KV2. Gunung Raya: 2 males, 3 females pronounced as in the fi gure by Chen & Nieser (1993) Ð but (macropterous), TAD0617. the parameres of M. nigrofasciatus and M. nigrofascioides are evenly rounded. Although sorting males of M. squamifer Remarks. – See M. squamifer. and M. nigrofascioides is easy by the absence or presence of a notch on the fore femur, females can be distinguished Distribution. – Originally described from Myanmar and only by colour, M. squamifer being on average lighter than Thailand (Chen & Nieser, 1993), later recorded from M. nigrofascioides. The key character for females of M. Vietnam (Zettel & Chen, 1996) and West Malaysia (Yang squamifer given in Chen & Nieser (1993) is the colour & Kovac, 1995; Yang et al., 1999; Cheng et al., 2001). pattern of tergite 8, but it could not conclusively separate the Langkawi specimens because apterous females from Langkawi have a black base of tergite 8. However, if tergite Metrocoris squamifer Lundblad, 1933 8 is partly retracted into tergite 7, in some M. squamifer females a colour pattern appears which corresponds with Material examined. – Datai environment: 1 male (apterous), the key character. Usually the yellow colour on tergite 8 is HP1; Datai rain forest: 1 male, 1 female (apterous), 1 male reduced to a small circular spot in M. nigrofascioides, but (macropterous), HE1; Telaga Tujuh Ð Air Telaga: 1 male, 2 females more extended in M. squamifer. For separation of females, (apterous), HZ1a. Temurun Waterfalls: 3 males (macropterous), 3 authors used the extension of the mesopleural stripe female (apterous), HZL2. Gunung Raya: 1 male (macropterous), (reaching further posteriad in M. nigrofascioides than in M. HZL4a. Durian Perangin: 1 male, 1 female (apterous), L5HZ. Air squamifer Tejun: 1 male (apterous), HZL10. ), and the result agreed well with the identifi cation of males from the same samples. Macropterous females are Remarks. – Identifi cation of the species of the Metrocoris generally lighter than apterous females of the same species, nigrofasciatus group is diffi cult. Identity of M. squamifer and this morph of M. nigrofascioides was assigned to the specimens from Langkawi has been confi rmed by comparison males from the same sample. with Malaysian specimens in NHMW identifi ed by Dr. Ping-

Fig. 24. Comparison of species richness of selected families of Nepomorpha and Gerromorpha of Malaysian islands with those of mainland Malaysia.

292 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Distribution. – Southern Thailand, West Malaysia, Sumatra, described from Tioman were also recorded from the and Java (Chen & Nieser, 1993). Malaysian mainland, in some cases more recently. The only endemic water bug described from Pulau Tioman is Limnometra tiomanensis Zettel, Yang & Tran, 2009. Ventidius sp.

Material examined. – Stream near road linking Padang Gaong Rd ACKNOWLEDGEMENTS to Makam Mahsuri Rd: 1 nymph, TAD0622. Both authors acknowledge the very kind support of Prof. Remarks. – Chen & Zettel (1999) record fi ve species of Peter K.L. Ng, Ms. Lua Hui Kheng, Mrs. Yang Chang Man Ventidius from West Malaysia and Singapore. Nymphs (Raffl es Museum of Biological Diversity Research, National cannot be identifi ed at present. University of Singapore) for access to collections and support for fi eldwork and travel. Thanks are also due to Prof. Dr. Ernst Heiss (Innsbruck, Austria) and Dr. Damir Kovac DISCUSSION (Senckenberg Museum, Frankfurt am Main, Germany) for making available collection specimens under their care; to Species diversity. – Here we recorded species from eleven Dr. Tohru Naruse for his enthusiasm in helping us during the families on the island of Langkawi. Most of the species fi eld trip; and to Dr. Michael T. Monaghan (Leibniz - IGB, belong to two families, the Gerridae (19 species; 35 %) Berlin) for a linguistic review of the manuscript. We thank and the Veliidae (12 species; 22 %), while the remaining Dr. Robert W. Sites (University of Missouri, Columbia) nine families together contain only 24 species. This agrees and an anonymous reviewer for reviewing our manuscript. proportionally with the species numbers known from the Malay Peninsula (Fig. 24). Species of some families, not yet collected, are expected to occur on Langkawi, particularly LITERATURE CITED representatives of the Ochteridae and the Hebridae. Andersen, N.M., 1975. The Limnogonus and Neogerris of the Old A total of 55 species (50 identifi ed) belonging to 31 genera World with character analysis and a reclassifi cation of the was recorded from Langkawi. A similar study based on Gerrinae (Hemiptera: Gerridae). Entomologica scandinavica, similar collection efforts was published by Yang et al. Suppl. 7: 1Ð96. (1999) on the island of Tioman; it contains somewhat Andersen, N.M., 1980. Hygropetric water striders of the genus smaller numbers of taxa: 33 species (25 identified) in Onychotrechus Kirkaldy with description of a related genus 25 genera. Both studies show that the island faunas are (Insecta, Hemiptera, Gerridae). Steenstrupia, 6: 113Ð146. composed of only a fraction of the diversity of the mainland Andersen, N.M., 1989. The coral bugs, genus Halovelia Bergroth fauna, although it can be expected that a more detailed (Hemiptera, Veliidae). II. Taxonomy of the H. malaya-group, survey would yield some additional species. cladistics, ecology, biology, and biogeography. Entomologica scandinavica, 20: 179Ð227. For Veliidae, Chen et al. (2005) listed 25 species of Veliidae Andersen, N.M., 1995. Cladistics, historical biogeography, and a for the Malaysian faunal region (south of the Isthmus of check list of gerrine water striders (Hemiptera, Gerridae) of Kra), and the total number of described species known the World. Steenstrupia, 21: 93Ð123. from that region is presently 31 (including species newly Andersen, N.M., 2000. The marine Haloveliinae (Hemiptera: described in this paper). Eleven identifi ed species (35 %) Veliidae) of Singapore, Malaysia and Thailand, with six new are recorded from Langkawi, and six (19 %) from Tioman species of Xenobates Esaki. Raffl es Bulletin of Zoology, 48(2): (Yang et al., 1999; Andersen, 2000). For Gerridae, Chen et 273Ð292. al. (2005) list 53 species for the Malaysian fauna, and 55 Andersen, N.M. & L. Cheng, 2004. The marine insect Halobates described species are presently known. The Langkawi fauna (Heteroptera: Gerridae): biology, adaptations, distribution, and contains 19 species (36 %), the Tioman fauna 12 species phylogeny. Oceanography and Marine Biology: An Annual (23 %) (Yang et al., 1999). Review, 4: 119Ð179. Andersen, N.M. & T. Weir, 2004. Australian Water Bugs. Endemism. – Our survey of Pulau Langkawi includes Their Biology and Identification (Hemiptera-Heteroptera, descriptions of three new species. One of them, Hydrotrephes Gerromorpha & Nepomorpha). Entomonograph, 14. CSIRO langkawicus, is unknown from anywhere else. However, it Publishing. 344 pp. is doubtful that this species is an island endemic, and we Andersen, N.M., C.M. Yang & H. Zettel, 2002. Guide to the expect that it will be recorded from the mainland in the aquatic Heteroptera of Singapore and Peninsular Malaysia. Ð 2. future, when more collections of Helotrephidae become Veliidae. Raffl es Bulletin of Zoology, 50(1): 231Ð249. available. Buzzetti, F.M., N. Nieser & J. Damgaard, 2006. Notes on water bugs from Southeast Asia and Australia (Heteroptera: No new species were described by Yang et al. (1999), but Nepomorpha & Gerromorpha). Atti dell’Accademia Roveretana degli Agiati, series VIII, VI B: 31Ð45. several new species were later described from the same Tioman material by other authors (e.g., Andersen, 2000; Chen, P.-p. & N. Nieser, 1993. A taxonomic revision of the Zettel, 2001, 2004c; Zettel et al., 2009. Most species Oriental water strider genus Metrocoris Mayr (Hemiptera, Gerridae). Part I & II. Steenstrupia, 19(1): 1Ð43, 45Ð82.

293 Zettel & Tran: Water bugs from Langkawi, Malaysia

Chen, P.-p. & N. Nieser, 2002. Taxonomic characters of the male Polhemus, D.A., 1994. Taxonomy, phylogeny, and zoogeography endosomal structure in the genus Rheumatogonus Kirkaldy of the genus Cylindrostethus Fieber in the paleotropical region (Hemiptera: Gerridae), with descriptions of four new species (Heteroptera: Gerridae). Bishop Museum Occasional Papers, from Borneo and Sri Lanka. Zoologische mededelingen 38: 1Ð34. Leiden, 76(21): 371Ð409. Polhemus, D.A., 2001. A review of the genus Ptilomera Chen, P.-p. & N. Nieser & J.-Z. Ho, 2004. Review of Chinese (Heteroptera: Gerridae) in Indochina, with descriptions of two Ranatrinae (Hemiptera: Nepidae) with description of four new new species. Journal of the New York Entomological Society, species of Ranatra Fabricius. Tijdschrift voor Entomologie, 109(2): 214Ð234. 147: 81Ð102. Polhemus, J.T. & N.M. Andersen, 1984. A revision of Amemboa Chen, P.-p., N. Nieser & H. Zettel, 2005. The aquatic and semi- Esaki with notes on the phylogeny and ecological evolution aquatic bugs (Heteroptera: Nepomorpha & Gerromorpha) of eotrechine water striders (Insecta, Hemiptera, Gerridae). of Malesia. Fauna Malesiana Handbooks 5. Brill, Leiden Steenstrupia, 10(3): 65Ð111. Ð Boston, 546 pp. Polhemus, J.T. & D.A. Polhemus, 2001 [2000]. The genus Chen, P.-p. & H. Zettel, 1998. Key to the genera and subgenera Mesovelia Mulsant & Rey in New Guinea (Heteroptera: of Gerridae (Gerromorpha) of Thailand and adjacent countries, Mesoveliidae). Journal of the New York Entomological with a check-list of species known from Thailand. Amemboa, Society, 108(3Ð4): 205Ð230. 2: 24Ð41. Sites, R.W. & J.T. Polhemus, 2002. Distribution of Helotrephidae Chen, P.-p. & H. Zettel, 1999. A taxonomic revision of the (Heteroptera) in Thailand. Journal of the New York Oriental water strider genus Ventidius Distant (Hemiptera, Entomological Society, 109(3Ð4): 372Ð391. Gerromorpha, Gerridae). Tijdschrift voor Entomologie, 141: The Times Atlas of the World, 1992. 9th Ed. Times Books, London. 137Ð208. 222 pp., 123 pls. Cheng, L., C.M. Yang & N.M. Andersen, 2001. Guide to the Tran, A.D. & C.M. Yang, 2004. The aquatic bugs (Heteroptera) of aquatic Heteroptera of Singapore and Peninsular Malaysia. the Anambas and Natuna Islands, Indonesia. Raffl es Bulletin I. Gerridae and Hermatobatidae. Raffl es Bulletin of Zoology, of Zoology, Supplement No. 11: 55Ð59. 49(1): 129Ð148. Vitheepradit, A., R.W. Sites, H. Zettel, & C.M. Yang, 2005 [2003]. Hecher, C. & H. Zettel, 1996. Faunistical and morphological Review of the Hydrometridae (Heteroptera) of Thailand, with notes on Limnogonus subgenus Limnogonoides Poisson, 1965 distribution records. Natural History Bulletin of the Siam (Heteroptera: Gerridae). Linzer biologische Beiträge, 28(1): Society, 51(2): 197Ð223. 325Ð333. Yang, C.M. & D. Kovac, 1995. A collection of aquatic and Herring, J.L., 1961. The genus Halobates (Hemiptera: Gerridae). semi-aquatic bugs (Insecta: Hemiptera: Gerromorpha and Pacifi c Insects, 3(2Ð3): 223Ð305. Nepomorpha) from Temengor Forest Reserve, Hulu Perak, Hussin, A., C.V. Chong, Y. Musa, M.S. Azirun, R. Hashim & S.M. Malaysia. Malayan Nature Journal, 48: 287Ð295. Phang, 2005. University of Malaya’s Scientifi c Expedition to Yang, C.M. & D.A. Polhemus, 1994. Notes on Rhagovelia Mayr Langkawi, 4 Ð 10 April, 2004. An integrated ecosystem study (Hemiptera: Veliidae) from Singapore, with description of a on northeast Langkawi. Malaysian Journal of Science, 24: 1. new species. Raffl es Bulletin of Zoology, 42(4): 987Ð993. Lansbury, I., 1972. A review of the Oriental species of Ranatra Yang, C.M., T.C.M. Wong, H.K. Lua & L.M. Koh, 1999. A Fabricius (Hemiptera - Heteroptera): Nepidae). Transactions of checklist of aquatic and semi-aquatic bugs (Insecta: Hemiptera: the Royal Entomological Society of London, 124: 287Ð341. Heteroptera) from Pulau Tioman, Peninsular Malaysia. Raffl es Lansbury, I., 1973. A review of the genus Cercotmetus Amyot & Bulletin of Zoology, Supplement No. 6: 277Ð288. Serville, 1843 (Hemiptera-Heteroptera: Nepidae). Tijdschrift Yang, C.M. & H. Zettel, 2005. Guide to the aquatic Heteroptera of voor Entomologie, 116: 83Ð106. Singapore and Peninsular Malaysia: 5. Family Hydrometridae. Nieser, N., 1998. Introduction to the Notonectidae (Nepomorpha) The Raffl es Bulletin of Zoology, 53(1): 79Ð97. of Thailand. Amemboa, 2: 10Ð14. Yap, S.Y., 2005. A preliminary classifi cation of Langkawi Island Nieser, N., 2000 [1999]. Three new species of Micronecta from streams using biotic index criteria. Malaysian Journal of Thailand with a key to SE Asian species (Heteroptera: Science, 24: 15Ð23. Corixidae). Journal of the New York Entomological Society, Zettel, H., 2000a. The Helotrephidae (Heteroptera) of Borneo. 107(2Ð3): 277Ð288. Entomological Problems, 31(1): 1Ð22. Nieser, N., 2002. Guide to the aquatic Heteroptera of Singapore Zettel, H., 2000b. Rhagovelia inexpectata sp.nov., a sibling species and Peninsular Malaysia. IV. Corixoidea. Raffl es Bulletin of of R. sumatrensis from Southeast Asia (Heteroptera: Veliidae). Zoology, 50(1): 263Ð274. Entomological Problems, 31(2): 175Ð178. Nieser, N., 2004. Guide to the aquatic Heteroptera of Singapore Zettel, H., 2001. Five new species of Perittopus FIEBER, 1861 and Peninsular Malaysia. III. Pleidae and Notonectidae. Raffl es (Hemiptera: Veliidae) from Southeast Asia. Raffl es Bulletin Bulletin of Zoology, 52(1): 79Ð96. of Zoology, 49(1): 109Ð119. Papá ek, M. & H. Zettel, 2000. Revision of the Oriental genus Zettel, H., 2004a. Weitere neue Helotrephini (Heteroptera: Idiotrephes (Heteroptera: Nepomorpha: Helotrephidae). Helotrephidae) aus China, Indonesien und Malaysien sowie European Journal of Entomology, 97: 201Ð211. von den Philippinen. Linzer Biologische Beiträge, 36(2): Papá ek, M. & H. Zettel, 2005 [2004]: Helotrephidae of the 1359Ð1382. World (Hemiptera: Heteroptera: Nepomorpha): checklist and Zettel, H., 2004b. Neue Wasserläufer (Insecta: Heteroptera: bibliography. Acta Societatis Zoologicae Bohemicae, 68: Gerridae) von den Philippinen. Annalen des Naturhistorischen 99Ð108. Museums in Wien, 105B: 361Ð387.

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Zettel, H., 2004c. Revision of the Timasius chinai species group Zettel, H. & A.D. Tran, 2006. New species and new records of (Insecta: Heteroptera: Hebridae), with descriptions of ten new Haloveliinae (Insecta: Heteroptera: Veliidae) from Vietnam. species. Insect Systematics and Evolution, 35: 241Ð260. Annalen des Naturhistorischen Museums in Wien, 107B: Zettel, H., 2005. A new sea-skater from the southern Philippines, 71Ð90. with a key to the Philippine species of Halobates (Heteroptera: Zettel H., C.M. Yang & A.D. Tran, 2009. Descriptions of two Gerridae). Entomofauna, 26(24): 409Ð420. large water striders of the genus Limnometra Mayr, 1865 Zettel, H. & P.-p. Chen, 1996. Beitrag zur Taxonomie und (Insecta: Heteroptera: Gerridae) from the Philippines and Faunistik der Gerridae mit Neubeschreibungen Malaysia. Annalen des Naturhistorischen Museums in Wien, der Gattung Andersenius gen.nov. aus der Unterfamilie 110B: 21Ð31. Ptilomerinae und weiterer Arten (Insecta: Heteroptera: Gerridae). Entomologische Abhandlungen Staatliches Museum für Tierkunde Dresden, 57(6): 149Ð182.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 297–303 Date of Publication: 31 Aug.2009 © National University of Singapore

FOUR NEW SPECIES OF HORAEOMORPHUS SCHAUFUSS FROM THE ORIENTAL REGION (COLEOPTERA: STAPHYLINIDAE, SCYDMAENINAE)

P. Jałoszy ski Os. Wichrowe Wzgórze 22/13, 61-678 Pozna , Poland Email: [email protected]

ABSTRACT. – Four new species of the genus Horaeomorphus Schaufuss (Coleoptera: Scydmaenidae: Scydmaeninae) are described: H. imitator new species and H. minor new species from Mindanao, Philippines; H. fakfakensis new species from Irian Jaya, Indonesia; and H. samosirensis new species from Sumatra, Indonesia. Habitus and important diagnostic characters of the new taxa, including aedeagi, are illustrated.

KEY WORDS. – Coleoptera, Staphylinoidea, Staphylinidae, Scydmaenidae, Scydmaeninae, Cyrtoscydmini, Horaeomorphus, new species, Oriental, Indonesia, Sumatra, New Guinea, Philippines.

INTRODUCTION of Horaeomorphus. Four species from Indonesia (Sumatra and New Guinea) and the Philippines turned out to differ Thirty species of the genus Horaeomorphus Schaufuss from all other members of the genus, and they are described (Coleoptera: Staphylinidae, Scydmaeninae: Cyrtoscydmini) below as new taxa. have been reported so far to occur in the Oriental Region and areas forming a transient zone between the Oriental to the East Palearctic Regions. The majority of species MATERIALS AND METHODS inhabit the Malay Peninsula and the Sunda Islands (20 species); most of them were revised by Jałoszy Dry-mounted specimens were handled in a standard way, ski (2006), and later three more species were described i.e., relaxed with warm water and dissected; aedeagi are (Jałoszy ski et al., 2007; Jałoszy ski & Nomura, 2008). preserved as Canada balsam mounts on pins under card with Within the Malay Subregion, Horaeomorphus is known specimens. Illustrations of aedeagi were prepared by free- to occur in the peninsular Malaysia (Kedah, Pahang, hand drawing. Habitus photos were taken as multiple shots Kuala Terengganu), Singapore, Tioman Is., Penang Is., at different depths of focus with Olympus C-750 camera and Borneo (Sabah, Sarawak, Kalimantan, Brunei Derussalam), Raynox macro lenses, fi nal pictures were assembled with Sumatra, and Siberut Is. In addition, one species is CombineZ freeware. The measurement convention applied known from Thailand (Franz, 1985), one from Vietnam herein follows that of Jałoszy ski (2006). All studied (Jałoszy ski & Nomura, 2004), one from Taiwan (Jałoszy specimens are deposited at: SMNS – Staatliches Museum ski, 2003), one from the Philippines (Jałoszy ski, 2004), für Naturkunde, Stuttgart, Germany. one from mainland China (Franz, 1985), four from Nepal (Franz, 1973; 1974; Vit, 2004), and one from Japan (Jałoszy ski, 2002). Members of this morphologically TAXONOMY diverse genus are not uncommon in hot and humid forests of SE Asia; they are usually encountered in leaf litter, rotten Horaeomorphus imitator, new species wood and under bark of trees. Most effi cient collecting (Figs. 1a, 2a, b, 4a) methods are sifting appropriate substrates and flight intercept traps. Material examined. – Holotype. Male, two labels: “MINDANAO, 1-3. May \ MISAMIS OCC., 1700 m \ DON VICTORIANO Thanks to kindness of Dr. Wolfgang Schawaller, I had an \ Bolm lgt., 1996” [yellow, printed], “HORAEOMORPHUS \ opportunity to examine several undetermined specimens imitator m. \ HOLOTYPUS \ det. P. JAŁOSZY SKI, ‘08” [red, printed] (SMNS).

297 Jałoszy ski: Four new Oriental Horaeomorphus

Diagnosis. – The following set of characters is unique for subtrapezoidal; internal sac symmetrical, with complicated, this species: body nearly as long as 3 mm, brown, slender; bell-shaped central complex; parameres slender, slightly pronotum strongly elongate, with three small ante-basal exceeding apex of median lobe, each with four apical pits located in deep groove; metatrochanters in males setae. strongly modifi ed, each forming very long, slightly curved rod-like projection with rounded apex; aedeagus with very Female. – Unknown. complicated, symmetrical internal armature composed of generally bell-shaped central complex, and each paramere Etymology. – The specifi c epithet imitator refers to the with numerous apical setae, without subapical setae. overall resemblance of the new species to H. blattnyi, another Horaeomorphus known to occur in the Philippines. Male. – Body (Fig. 1a) large (length 2.93 mm), slender, very convex, moderately dark brown, vestiture slightly Distribution. – Philippines: Misamis Occidental Prov: lighter than cuticle. Mindanao Is.

Head broadest at moderately large, strongly convex eyes, Remarks. – Horaeomorphus imitator is very similar to H. length 0.45 mm, width 0.60 mm; tempora slightly longer blattnyi Jałoszy ski, 2004, known to occur on Luzon. These than eye in dorsal view, arcuate; vertex weakly convex, two species share a very similar body shape, highly modifi ed with pair of small but deep pits located near posterior metatrochanters, and the structures of the aedeagus. A major margins of supraantennal tubercles; frons weakly convex; differences are the body length (>3.3 mm in H. blattnyi vs. supraantennal tubercles very distinct, strongly raised, well <3 mm in H. imitator), the internal sac of the aedeagus delimited from frons but indistinctly delimited from vertex. (much more complicated in H. imitator), and the parameres Punctures on vertex and frons very fine, shallow and (with several setae distributed between middle and apex in sparse, unevenly distributed, separated by spaces 2-4x as H. blattnyi, and with only apical setae in H. imitator). long as puncture diameters; setae moderately long, sparse, suberect to erect. Antennae moderately slender, shorter than half length of body, length 1.20 mm; relative lengths of Horaeomorphus minor, new species antennomeres (shortest antennomere II as 1): 1.67; 1; 1.67; (Figs. 1b, 2c,d) 1.5; 1.33; 1.17; 1.17; 1.33; 1.5; 1.67; 2. Material examined. – Holotype. Male, two labels: “MINDANAO, Pronotum oval, elongate, broadest between anterior 30km NW of \ MARAMAG, 13.-17. MAY \ BAGONGSILANG, third and fourth, length 0.93 mm, width at base 0.45 1700 m \ Bolm lgt., 1996” [yellow, printed], “HORAEOMORPHUS mm, maximum width 0.73 mm; discal part moderately \ minor m. \ HOLOTYPUS \ det. P. JAŁOSZY SKI, ‘08” [red, printed] (SMNS). Paratypes. 1 male, same data as for holotype strongly narrowing posteriorly to sharply marked posterior (SMNS); 1 male, “MINDANAO, 1-3. May \ MISAMIS OCC., constriction separating narrow basal collar; hind angles 1700 m \ DON VICTORIANO \ Bolm lgt., 1996” [yellow, printed] obtuse and blunt; posterior margin arcuate; posterior collar (SMNS); paratypes additionally provided with identifi cation labels delimited from disc by transverse dorsal row of three small analogous to that on the holotype, but yellow and annotated but deep pits located in narrow and deep groove. Punctures “PARATYPUS”. on disc very fi ne and shallow, unevenly distributed, those in middle are separated by spaces 2-5x as long as puncture Diagnosis. – This is one of the smallest species of diameters; vestiture sparse, moderately long, suberect. Horaeomorphus, remarkable by not reaching 2 mm in length; it differs from all congeners also in the following Elytra strongly elongate, oval, more convex than pronotum, combination of characters: lateral margins of pronotum broadest near anterior third, length 1.55 mm, width 0.98 slightly, but distinctly raised in posterior part to form mm, EI 1.59. Humeral calli weakly marked, delimited rounded lateral longitudinal carinae; base of pronotum from adsutural region by very short and shallow, broad without groove, with two large lateral pits and very small basal impressions; basal foveae indiscernible; apices of median pit; elytra broadest near anterior third and very elytra separately rounded. Punctures in anterior 2/3 of strongly narrowing from broadest place toward apices; elytra much more distinct than those on pronotum, large legs in males non-modified; aedeagus with strongly but shallow and slightly diffused; in median part of each asymmetrical, massive internal sac. elytron separated by spaces slightly longer than puncture diameters, punctures are gradually smaller and shallower Male. – Body (Fig. 1b) very small (length 1.78-1.93 mm, toward apices and lateral margins of elytra. Vestiture similar mean 1.87 mm), slender, fl attened, moderately dark brown, to that on pronotum but slightly longer and slightly more vestiture slightly lighter than cuticle; setae on pronotum suberect. Metathoracic wings not studied. slightly darker than those on elytra.

Metatrochanters strongly modifi ed, as in Fig. 4a. Head broadest at moderately large, moderately convex eyes, length 0.25-0.28 mm (mean 0.27 mm), width 0.35-0.38 Aedeagus (Figs. 2a, b) 0.65 mm in length; with moderately mm (mean 0.37 mm); tempora as long as eye in dorsal slender median lobe, apical part strongly narrowed, view, regularly, weakly rounded up to posterior 3/4, where

298 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 1. Dorsal habitus of holotype males: a, Horaeomorphus imitator, new species; b, Horaeomorphus minor, new species; c, Horaeomorphus fakfakensis, new species; d, Horaeomorphus samosirensis, new species (d). Scale bar = 0.5 mm.

Fig. 2. Aedeagus in ventral (a, c) and lateral (b, d) views: a, b, Horaeomorphus imitator, new species; c, d, Horaeomorphus minor, new species. Scale bar = 0.2 mm.

299 Jałoszy ski: Four new Oriental Horaeomorphus they are strongly bent toward occipital constriction; vertex 1.08 mm), width 0.60–0.65 mm (mean 0.63 mm), EI 1.69– weakly convex, with pair of small but deep pits located near 1.73. Base of elytra arcuate so that humeri are projected posterior margins of supraantennal tubercles; frons weakly anteriorly, humeral calli weakly marked, delimited from convex; supraantennal tubercles very distinct, strongly adsutural region by short and shallow, very broad basal raised, well delimited from frons but indistinctly delimited impressions; basal foveae indiscernible; apices of elytra from vertex. Punctures on vertex very fi ne, barely noticeable separately rounded. Punctures in anterior 2/3 of elytra under magnifi cation 80×; median part of frons bears dense, much more distinct than those on pronotum, large, deep moderately large, distinct punctures unevenly distributed and relatively sharply marked; in median part of each and separated by spaces 1–3× puncture diameters; setae elytron separated by spaces distinctly shorter than puncture moderately long, sparse, suberect to erect. Antennae diameters, punctures are gradually smaller and shallower moderately slender, shorter than half length of body, toward apices and lateral margins of elytra. Vestiture length 1.75–0.80 mm (mean 0.78 mm); relative lengths of slightly longer and distinctly more suberect than that on antennomeres (shortest antennomere II as 1): 0.83; 1; 1.07; pronotum. Metathoracic wings long, functional. 0.93; 0.8; 0.77; 0.73; 0.70; 0.97; 0.83; 1.5. Legs non-modifi ed. Pronotum inversely subtrapezoidal, elongate, broadest at anterior third, length 0.50–0.53 mm (mean 0.52 mm), width Aedeagus (Figs. 2c, d) 0.45 mm in length; median lobe at base 0.33 mm, maximum width 0.43–0.45 mm (mean moderately slender, with subtrapezoidal apical part; 0.43 mm); anterior margin rounded; lateral margins rounded internal sac strongly asymmetrical, darkly sclerotized and near broadest place, then nearly straight up to indistinct complicated; parameres slender, not exceeding apex of subbasal constriction separating short posterior collar; median lobe, each with 4–5 apical and subapical setae. lateral margins in posterior third to half raised, forming low and rounded lateral carinae; hind angles blunt, obtuse; Female. – Unknown. posterior margin weakly arcuate; base of pronotum with pair of large lateral pits and very small, indistinct median Etymology. – The name minor refers to the small body of pit. Punctures very small, moderately sharply marked, but this species. well visible under magnifi cation 40×, unevenly distributed, those on median part of disc are separated by spaces 1–3× Distribution. – Philippines: Provinces Bukidnon and as long as puncture diameters; setation moderately dense Misamis Occidental: Mindanao Island. and long, suberect. Remarks. – This small, slender and fl attened species can Elytra strongly elongate, drop-shaped, about as convex be easily distinguished from any other congeners by the as pronotum, broadest near anterior third and strongly asymmetrical and very large internal sac of the aedeagus. narrowing toward apices, length 1.03–1.13 mm (mean The only other species with asymmetrical internal sacs are

Fig. 3. Aedeagus in ventral (a, c) and lateral (b, d) views: a, b, Horaeomorphus fakfakensis, new species, c, d, Horaeomorphus samosirensis, new species. Scale bar = 0.2 mm.

300 THE RAFFLES BULLETIN OF ZOOLOGY 2009

H. deformatus Jałoszy ski, 2006 from W Malaysia (Kuala Head broadest at large, strongly convex eyes, length Terengganu), and H. pseudosabahensis Jałoszy ski, 2006 0.33 mm, width 0.43 mm; tempora slightly shorter than from Sabah and Sarawak. The latter species has distinctly eye in dorsal view, weakly and regularly rounded up to different body form (much larger and strongly convex). posterior 2/3, where they are strongly bent toward occipital Horaeomorphus deformatus is relatively similar to H. minor constriction; vertex weakly convex, with pair of small and in general body shape, but it can be easily distinguished shallow pits located near posterior margins of supraantennal on the basis of strongly modified metatrochanters and tubercles; frons weakly convex; supraantennal tubercles metafemora in males. very distinct, strongly raised, well delimited from frons but indistinctly delimited from vertex. Punctures on vertex and frons very fi ne but sharply marked, very sparse, unevenly Horaeomorphus fakfakensis, new species distributed, separated by spaces 4–6× as long as puncture (Figs. 1c, 3a, b) diameters; setae moderately long, sparse, suberect to erect. Antennae moderately slender, shorter than half length of Material examined. – Holotype. Male, two labels “IRIAN body, length 0.90 mm; relative lengths of antennomeres JAYA:Fakfak \ Kokas Insel Ogar \ 13.VIII.1996 \ leg. SCHÜLE/ (shortest antennomere VII as 1): 1.59; 1.36; 1.36; 1.36; 1.36; STÜBEN” [pale blue, printed], “HORAEOMORPHUS \ fakfakensis 1.27; 1; 1.36; 1.36; 1.36; 2.27. m. \ HOLOTYPUS \ det. P. JAŁOSZY SKI, ‘08” [red, printed] (SMNS). Pronotum very broad and nearly circular, broadest between middle and anterior third, length 0.68 mm, width at base 0.43 Diagnosis. – This moderately large Horaeomorphus can mm, maximum width 0.65 mm; anterior and lateral margins be distinguished from all other species of the genus on rounded together; subbasal constriction barely marked; hind the basis of the following set of characters: pronotum very angles obtuse and blunt; posterior margin nearly straight; broad, disc nearly circular, with relatively small oval median posterior collar very short, delimited from disc by transverse part covered with large, deep and dense punctures while dorsal row of fi ve pits; median pit moderately large, deep, remaining surface bears small and very shallow punctures; two lateral pairs composed of smaller and shallower pits, base of pronotum with fi ve pits, without groove; legs non- external ones are shifted anteriorly. Disc with median oval modifi ed. area densely covered with large and deep, oval or slightly irregular in shape punctures separated by spaces 1–2× Male. – Body (Fig. 1c) moderately large (length 2.08 as long as puncture diameters; remaining surface of disc mm), pronotum and elytra very broad, moderately strongly with similarly dense, but much smaller and very shallow convex, dark brown, vestiture slightly lighter than cuticle. punctures; vestiture moderately dense and long, suberect.

Elytra oval, very broad and relatively short, as convex as pronotum, broadest near anterior fourth, length 1.08 mm, width 0.73 mm, EI 1.48. Base of elytra arcuate, so that humeri are projecting anteriorly; humeral calli moderately distinct, delimited from adsutural region by short and deep, broad basal impressions; basal foveae indiscernible; apices of elytra separately rounded. Punctures in anterior 2/3 of elytra much more distinct than those on sides of pronotum, but much smaller than those on median part of pronotal disc, separated by spaces about equal to puncture diameters; punctures become gradually smaller and shallower toward apices and lateral margins of elytra. Vestiture similar to that on pronotum but slightly longer and slightly more suberect. Metathoracic wings not studied.

Legs non-modifi ed.

Aedeagus (Figs. 3a, b) 0.30 mm in length; relatively stout; median lobe with subtrapezoidal apical part distinctly projected in middle; internal sac relatively simple and lightly sclerotized, with small central complex; parameres slender, with apices reaching apex of median lobe, each with three very short apical setae.

Female. – Unknown. Fig. 4. Hind trochanter and femur (a), and hind trochanter, femur and tibia (b). Horaeomorphus imitator new species (a), Etymology. – Locotypical, after the type locality, Indonesian Horaeomorphus samosirensis new species (b). Scale bar = 0.2 mm. district Fakfak.

301 Jałoszy ski: Four new Oriental Horaeomorphus

Distribution. – Indonesia (New Guinea): Irian Jaya Barat. indistinctly separated from disc by very shallow constriction and dorsal row of three very small and shallow pits located Remarks. – This species is most similar to H. sarawakensis in narrow and deep groove, median pit prolonged anteriorly Franz, 1992 (from W Malaysia and Borneo), H. by short longitudinal groove; hind angles of pronotum valdepunctatus Franz, 1984 (W Malaysia), H. punctatissimus blunt, obtuse; posterior margin weakly arcuate. Punctures Franz, 1992 (Borneo, Sumatra and Siberut Is.), and H. on disc small and shallow but distinct, unevenly distributed, samosirensis described below. Together with H. fakfakensis, those in middle are separated by spaces 1.5–4× as long as these taxa share a similar body form, with very broad, puncture diameters; punctures become gradually smaller nearly circular pronotum, and stout elytra. Horaeomorphus and shallower toward margins of disc; vestiture sparse, fakfakensis can be distinguished from H. sarawakensis, H. moderately long, suberect. punctatissimus and H. samosirensis on the basis of nearly straight metatibiae, while those in the three species are Elytra very broad, oval, as convex as pronotum, broadest strongly bent. Horaeomorphus valdepunctatus, in turn, between middle and anterior third, length 1.08 mm, width has only slightly curved metatibiae, but metatrochanters 0.85 mm, EI 1.26. Base of elytra arcuate, so that humeri are in males are strongly modifi ed, forming a long projection; projected anteriorly; humeral calli weakly marked, delimited metatrochanters in H. fakfakensis are non-modifi ed. This from adsutural region by short, broad and relatively deep species is the fi rst member of the genus known to occur in basal impressions; basal foveae indiscernible; each elytron New Guinea. is slightly impressed near suture in anterior third; apices of elytra separately rounded. Punctures in anterior 2/3 of elytra much larger, deeper and denser than those on median part Horaeomorphus samosirensis, new species of pronotum, those on adsutural impression are separated by (Figs.1d, 3c, d, 4b) spaces distinctly shorter than puncture diameters; punctures are gradually smaller and shallower toward apices and Material examined. – Holotype. Male, three labels: “NORD- lateral margins of elytra. Vestiture slightly longer and more SUMATRA : \ Umg. Partungkoan \ Samosir, 28.8.91” [white, erect than that on pronotum. Metathoracic wings long, printed], “1600m, Urwald, \ unt. Pinus-Rinde \ ERBER” [white, functional. printed, middle line handwritten in black], “HORAEOMORPHUS \ samosirensis m. \ HOLOTYPUS \ det. P. JAŁOSZY SKI, ‘08” Hind legs strongly modifi ed, as in Fig. 4b. [red, printed] (SMNS).

Diagnosis. – This stout and moderately large species Aedeagus (Figs. 3c, d) 0.28 mm in length; median lobe is unique in having a hook-like ventral projection on relatively slender, with short, subtriangular apical part; metafemora and strongly bent metatibiae of males. internal sac simple and lightly sclerotized; parameres slender, distinctly exceeding apex of median lobe, each with Male. – Body (Fig. 1d) moderately large (length 2.20 mm), three short apical and subapical setae. with pronotum and elytra very broad and slightly fl attened, Female. – dark brown, vestiture slightly lighter than cuticle. Unknown. Etymology. – Head broadest at moderately large, strongly convex eyes, Locotypical, after the type locality, Samosir length 0.38 mm, width 0.48 mm; tempora much longer than Is. on Sumatra. eye in dorsal view, very weakly arcuate up to posterior 4/5, Distribution. – where they rapidly bend toward occipital constriction; vertex Indonesia (Sumatra), North Sumatra Prov.: weakly convex, with pair of small and very shallow pits Samosir Is. located near posterior margins of supraantennal tubercles; Remarks. – posterior part of frons flattened, anterior part convex; The only species of the genus with hook-like H. heissi supraantennal tubercles very distinct, strongly raised, well projections on the metafemora known so far was delimited from frons but indistinctly delimited from vertex. Franz, 1985 from W Malaysia (Pahang) and Indonesia Punctures on vertex and frons very fi ne, shallow and sparse, (Sumatra). The latter species is distinctly different in the unevenly distributed, separated by spaces 2-4x as long as general body form, it is smaller, more slender and distinctly H. samosirensis puncture diameters; setae moderately long, sparse, suberect fl atter than ; it also has only slightly bent H. samosirensis to erect. Antennae moderately slender, distinctly shorter metafemora, whereas those in are strongly Horaeomorphus than half length of body, length 0.88 mm; relative lengths bent. This new species is the fi rst reported of antennomeres (shortest antennomere VIII as 1): 1.4; 1.2; to occur in an island located on a lake. 1.24; 1.2; 1.16; 1.04; 1.04; 1; 1.2; 1.6; 2. ACKNOWLEDGMENTS Pronotum very broad, nearly circular, broadest between middle and anterior third, length 0.75 mm, width at base 0.38 mm, maximum width 0.73 mm; anterior and lateral I express my thanks to Dr. Wolfgang Schawaller (SMNS) margins rounded together; posterior collar extremely short, who kindly lent me materials for study.

302 THE RAFFLES BULLETIN OF ZOOLOGY 2009

LITERATURE CITED Jałoszy ski, P., 2003. Taxonomical notes on Southeast Asiatic species of Horaeomorphus Schaufuss (Coleoptera, Franz, H., 1973 (1971). Die auf meinen Forschungsreisen nach Scydmaenidae), with description of a new species from Nepal in den Jahren 1970 und 1971 gesammelten Scydmaeniden Taiwan. Bulletin of National Science Museum Tokyo, Ser. A, und einige nordindische Vertreter dieser Familie (Coleoptera, 29(2): 107–117. Scydmaenidae). Zeitschrift der Arbeitsgemeinschaft Jałoszy ski, P., 2004. The first record of Horaeomorphus Österreichischer Entomologen, 23: 113–156. Schaufuss (Coleoptera, Scydmaenidae) from the Philippines, Franz, H., 1974. Die Scydmaeniden des Raumes von Jumla in with description of H. blattnyi sp. nov. Revue suisse de WestNepal und aus dem Therai (Col.). Koleopterologische Zoologie, 111(4): 785–789. Rundschau, 51: 86–104. Jałoszy ski, P. 2006. Revision of Horaeomorphus Schaufuss Franz, H., 1984. Beitrag zur Kenntnis der Scydmaeniden von (Coleoptera, Scydmaenidae) of East [sic!] Malaysia, Singapore Sumatra und benachbarter Gebiete. Sitzungsberichte der and Sunda Islands. Genus, 17(1): 19–66. Österreichischen Akademie der Wissenschaften, Mathematisch- Jałoszy ski, P., & S. Nomura, 2004. A new species of Naturwissenschaftliche Klasse, Abt. I, 193: 89–142. Horaeomorphus Schaufuss (Coleoptera, Scydmaenidae) from Franz H., 1985. Neue und ungenügend bekannte Scydmaeniden Vietnam. Elytra, 32(1): 65–70. (Coleoptera) aus Taiwan, Fukien und Thailand. Mitteilungen der Jałoszy ski, P., & S. Nomura, 2008. Two new species of Münchner Entomologische Gesellschaft, 74: 91–128. Horaeomorphus Schaufuss (Coleoptera, Scydmaenidae) from Franz, H., 1992, Scydmaeniden aus Malaysia und Sulawesi Sabah, Borneo. Elytra, 36(1): 159–166. (Coleoptera: Scydmaenidae). Koleopterologische Rundschau, Jałoszy ski, P., Nomura, S., & A. G. Idris, 2007. A new 62: 69–76. Horaeomorphus from the Malay Peninsula. Elytra, 35(1): Jałoszy ski, P., 2002. First record of the genus Horaeomorphus 307–311. Schaufuss (Coleoptera, Scydmaenidae) from Japan, with Vit., S., 2004. Notes on Horaeomorphus occurring in Nepal description of a new species. Bulletin of National Science (Coleoptera: Scydmaenidae). Acta Societas Zoologicae Museum Tokyo, Ser. A, 28(4): 223–232. Bohemicae, 68: 287–299.

303 THE RAFFLES BULLETIN OF ZOOLOGY 2009

THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 305 Ð322 Date of Publication: 31 Aug.2009 © National University of Singapore

A CHECKLIST OF (ARACHNIDA: ARANEAE) FROM PENINSULAR MALAYSIA INCLUSIVE OF TWENTY NEW RECORDS

Y. Norma-Rashid Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia Email: [email protected] (Corresponding author)

Daiqin Li Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Republic of Singapore

ABSTRACT. – literature exclusive to Peninsular Malaysia is lacking and this work fi lls that gap with an annotated checklist of 425 species in 42 families and 238 genera. Twenty species are here listed as new records for Peninsular Malaysia.

KEY WORDS. – Araneae, species list, new records, diversity, Malaysia.

INTRODUCTION Such fi ndings are evident of many more potential unknowns lurking in the Peninsular awaiting discovery. It is therefore The spider fauna of South East Asia is relatively well our hope and primary objective that this compilation would known but that of Peninsular Malaysia is much less known provide baseline information to encourage interest in local in contrast to neighboring Singapore. Little work has been Arachnology. done on spiders and inventories exclusively on Peninsular Malaysia. This would hamper research and needless to say has important ramifi cations in terms of assessing the local MATERIAL AND METHODS biodiversity. Such implications are further aggravated when of late fundamental and baseline research are attracting less Specimens examined were collected from Peninsular fi nancial aid causing researchers to divert and concentrate Malaysia and deposited in the Raffles Museum of on biotechnology work. Biodiversity Research, National University of Singapore (RMBR, NUS) by various Arachnologists and other workers In theory and had been enhanced through many fi ndings and by reviewing available literature which had included that spiders have the applied potential, for example to Malaysian spiders primarily, Koh (1989), Murphy & increase agricultural productivity in taking the role as Murphy (2000), Song et al. (2002) and Platnick (2006). pest control and able to limit pest densities (Barrion & The museum collections that were inspected included Litsinger, 1995). Local possibilities, to name a few are from very old materials dated back in the 1920s, for example the family Araneidae; Cyclosa bifi da and C. mulmeinensis the species Lampropelma violaceopedes Abraham, 1924 that predates on rice leafhoppers, Hasarius adansoni and (Family: Theraphosidae) was collected from Johore in Plexippus petersi from family Salticidae also benefi cial as Nov.1923 and also from Langkawi and Kedah, Malaysia biocontrol in ricefi elds. on 23 Apr.1928.

Taxonomically, spiders are an important group globally The annotated checklist is presented in alphabetical comprised of more than 40,000 species under 106 families order of family in a format according to the sequence of: and 3,000 genera (Platnick, 2008). The Salticidae are the RMBR catalogue numbers for the museum collections most diverse family recorded accounting for many recent that were examined are labeled as ZRC.ARA followed by discoveries and new species. This is no exception for numerical series. A small number of specimens are yet to Peninsular Malaysia spider fauna where salticid new genus be catalogued, thus unnumbered. and species were made by Zhang et al. (2006) in addition to six new species and one new record from Singapore and Malaysia (Zhang et al., 2003).

305 Norma-Rashid & Li: Checklist of spiders from Peninsular Malaysia

RESULTS AND DISCUSSIONS ARANEIDAE Simon, 1895

Diversity of spiders Anepsion depressum (Thorell, 1877)

Together with old records (Table 1) and current new 4 females, 1 male, Juara track, Pulau Tioman, Pahang, det. records (Table 2), this work showed that the spider fauna D.X. Song, coll. D. Q. Li, 24 Jun.1999. for Malaysia includes 425 species, belonging to 42 family groups and 238 genera. From a global perspective this is small as taxonomists currently recognize more than 40,000 Cyclosa bifi da (Doleschall, 1859) species under 106 families and more than 3,000 genera (Platnick, 2008). Workman (1896) compiled a total of 203 3 females, ZRC.ARA.82, Juara track, Pulau Tioman, species in his book which had a majority of the illustrations Pahang, det. D.X. Song, coll. D. Li, 24 Jun.1999. done from specimens collected from Singapore and Penang and a smaller number representatives from Celebes, East India, Java and New Guinea. More interestingly, Song et C. insulana (Costa, 1834), new record al.(2002) summarized in his work where it was claimed that Malaysia is home to 463 species of spiders from 42 1 female, 1 male, ZRC.1994.66-67, garden in Genting, families and 181 genera. This discrepancy from the current Pahang, coll. J.A and F. Murphy, 1-15 Feb.1988. report, can be explained by the fact that species from Sabah and Sarawak were included in the list count. Murphy and Murphy (2000) had a total of 284 species from Malaysia Cyrtophora moluccensis (Doleschall, 1857), new record and this observation is in accordance with that of Platnick (2006) which had 276 species. 1 male, ZRC.ARA.90, Paya mangrove, Pulau Tioman, det. D.X. Song, coll. D. Li, 26 Jun.1999. In terms of numerical dominance, salticids topped the list with 107 species, some 24.9% of the total number of species in Peninsular Malaysia. The presence of a substantial Gea spinipes C. L. Koch, 1843 species number makes Peninsular Malaysia of considerable species richness. This is further supported by the existence 1 female, ZRC.ARA.130, Genting, coll. J.A and F. Murphy, of local endemics, it is worthy to note that the greatest 1Ð15 Feb.1988. number of endemics belonged to the families Liphistidae (all 15 species) and Tetrablemmidae (10 of 11 species). Interestingly also the so called hot spots are mainly from CLUBIONIDAE Wagner, 1887 areas of Batu Caves, National Park (Taman Negara) and the highland resorts within Pahang state. It should be noted Clubiona meraukensis Chrysanthus, 1967, new record that the level of endemism be regarded with caution as the 1 female, ZRC.ARA.64, Paya mangrove, Pulau Tioman, checklist produced here may not be through an exhaustive det. D.X. Song, coll. D.Q. Li, 26 Jun.1990. sampling. Green (1999) cautioned that for a comprehensive sampling, various techniques should be utilized also to include day and night catches to ensure nocturnal spider CORINNIDAE Karsch, 1880 families are represented in such studies. Attention should be drawn to the fact that although spiders maybe abundant Oedignatha mogamoga Marples, 1995 in Peninsular Malaysia but their presence had been poorly documented. 1 male, 2 females, loop trail near Sg. Kanchin, pitfall, Rompin, Pahang, det. Murphy, 20 Jul.1990. Admittedly, the checklist here is not exhaustive and may be inadequate to reveal the true diversity of Peninsular Malaysian spiders. Nevertheless, this work constitutes an LIOCRANIDAE Simon, 1897 effort which should be regarded as an attempt to spark interest to study the local spider fauna. Teutamus politus Thorell, 1890

Checklist on the new records and the available species 1 female, pitfall, loop trail near Sg. Kinchin, Rompin, for Peninsular Malaysia examined in the RMBR, NUS. It Pahang, det. Murphy, 20 June 1990. should be noted that the primary references for each species are as indicated in Table 1, where Murphy & Murphy (2000), Platnick (2006) and Song et. al.(2002) are cited. Remarks for new records are given in Table 2.

306 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. The spider species list belonging to Peninsular Malaysia (PM) / Malaysia (MAL) and other country distributions compiled from references as indicated in columns 2 and 3. Other countries where abbreviated are as follows: AU=Australia, BO=Borneo, CB=Cambodia, CH=China, HK=, IND=India, Indon=Indonesia, JA=Java, JP=Japan, MY=Myanmar,NG=New Guinea, PH=Philipines, PK=Pakistan, SB=Sabah, SL=Sri Lanka, SP=Singapore, SR=Sarawak, SU=Sumatra, SUL=Sulawesi, TL=Thailand, TW=Taiwan, VN=Vietnam.

Country Distributions From Sources Species List Murphy & Murphy (2000) N. Platnick (2006) Song et al. (2002)

LIPHISTIIDAE Liphistius batuensis Abraham, 1923 Bcaves MAL L. desultor Schiodte, 1849 Penang MAL L. endau Sedgwick, Platnick, 1987 Endau MAL L. johore Platnick, Sedgwick, 1984 Johore MAL L. kanthan Platnick, 1977 Ð MAL L. laruticus Schwendinger, 1977 Ð MAL L. langkawi Platnick, Sedgwick, 1984 Langkawi MAL L. malayanus Abraham, 1923 Gunong Angsi MAL L. m. cameroni Haupt, 1983 CHighlands MAL L. murphyorum Platnick, Sedgwick, Penang MAL 1984 L. panching Platnick, Sedgwick, 1984 Gua Panching MAL L. rufi pes Schwendinger, 1995 PM MAL L. tempurung Platnick, 1997 Ð MAL L. tioman Platnick, Sedgwick, 1984 Tioman MAL L. yangae Platnick, Sedgwick, 1984 Perlis MAL

FAMILY: BARYCHELIDAE Idioctis littoralis Abraham, 1924 PM, S-Kranji river SP MAL, SP Rhianodes atratus (Thorell, 1890) Penang MAL Sipalolasma aedifi catrix Abraham, 1924 PM, SP MAL MAL, PH, SP S. ophiriensis Abraham, 1924 Johore, Mt Ophir MAL MAL, SP

FAMILY: CTENIZIDAE Latouchia batuensis Roewer, 1962 Batu Caves MAL

FAMILY: HEXATHELIDAE Macrothele segmentata Simon, 1892 Penang MAL

FAMILY: NEMISIIDAE Damarchus cavernicola Abraham, 1924 Bcaves MAL D. montanus (Thorell, 1890) PM SU D. workmani Thorell, 1891 PM, SP SP MAL, SP

FAMILY: THERAPHOSIDAE andersoni (Pocock, 1895) PM MAL Coremiocnemis cunicularia (Simon, Penang MAL 1892) C. valida Pocock, 1895 * Penang, SP syn. C. validus Smith, 1987 MAL, SP Cyriopagopus schioedtei (Thorell, 1891) Penang MAL C. thorelli (Simon, 1901) Perak MAL Haplopelma doriae (Thorell, 1890) PM, SR BO H. minax (Thorell, 1897) PM MY, TL H. salangensis (Strand, 1907) Malacca MAL Lampropelma violaceopes Abraham, Penang, SP MAL MAL, SP 1924 Lyrognathus liewi West, 1991 Cameron Highlands MAL L. robustus Smith, 1988 Cameron Highlands MAL

307 Norma-Rashid & Li: Checklist of spiders from Peninsular Malaysia

Table 1. Continued.

Country Distributions From Sources Species List Murphy & Murphy (2000) N. Platnick (2006) Song et al. (2002)

Phlogiellus inermis (Aussere, 1871) PM, SP MAL MAL, SP Poecilotheria striata Pocock, 1895 Penang IND javanensis (Walckenaer, PM, SP MAL MAL, Indon, SP 1837) S. tahanensis Abraham, 1924 Gunung Tahan MAL

FAMILY: ANAPIDAE Crassignatha haeneli Wunderlich, 1995 Frasers Hill Ð Pseudanapis parocula (Simon, 1899) PM MAL

FAMILY: ARANEIDAE Actinacantha globulata (Walckenaer, PM, JA, SU SU, JA 1842) Acusilas coccineus Simon, 1895 JA, SC, SP, TW MAL, Indon, SP A. gentingensis Murphy & Murphy, Ð MAL 1983 A. malaccensis Murphy & Murphy, Ð MAL, SU 1983 Anepsion depressum (Thorell, 1877) PM, MY, SC, SP, SU, TW CH, MY to SUL Tioman, Indon, MY, SP A. fuscolimbatum (Simon, 1901) Ð MAL Arachnura melanura Simon, 1867 PM, CH, IND, JA, SU, TW IND, JP, SUL Araneus papulatus (Thorell, 1887) PM, MY MAL A. virgunculus (Thorell, 1890) PM, SU SU A. reinwardti (Doleschall, 1859) all? MAL to NG Argiope aemula (Walckenaer, 1842) SUL, probably all Indon to PH MAL, Indon, PH, SP, TL, VN Cyclosa bifi da (Doleschall, 1859) Indon, all Indon to PH, NG Tioman, Indon, MY, SP, VN C. camelodes (Thorell, 1878) PM NG C. confraga (Thorell, 1892) PM, SP, VN MAL, IND C. mulmeinensis (Thorell, 1887)*** all? Africa to JP, PH SP, PH Cyrtarachne conica O.P.-Cambridge, Ð MAL SP 1901 Cyrtophora beccarii (Thorell, 1878) Ð MAL to NG MAL, Indon, SP C. eczematica (Thorell, 1892) PM, JA, MY, SP MAL, JA, NG, SUL SP, Indon Gasteracantha arcuata (Fabricius, 1793) all? MAL, Indon, MY, SP, TL G. audouini Guerin, 1838 PM, BO, PH, SU PH, SU, Timor G. cuspidata Koch, CL, 1837 PM, JA MAL, JA, Nicobar Is G. diardi (Lucas, 1835) PM, CH, JA, SU, TL MAL, CH, TL MAL, Indon, SP, TL G. doriae Simon, 1877 SR, BO, SP, SU MAL, Indon, SP G. hesselti C. L. Koch, 1837 JA, probably all IND, CH to Moluccas MAL, Indon, MY, SP G. fornicata (Fabricius, 1775) PM, AU, BO, JA, SU Quensland G. geminata (Fabricius, 1798) PM, MY IND, SUL G. mengei Keyserling, 1864 PM, BO, SP, SU MAL, BO, SUL Gea spinipes C. L. Koch, 1843 E. Indies, probably all IND, CH, TW, Borneo MAL, Indon, MY, SP, VN G. spinipes nigrifrons Simon, 1901 Ð MAL G. subramata Thorell, 1890 SR, all IND, PH, NG MAL, MY, SP, PH Mangora hemicraera (Thorell, 1890) Penang MAL Milonia albula O. P.-Cambridge, 1899 PM, SP-Botanic G SP MAL, SP Neogea egregia (Kulczynski, 1911) PM, MY, SP NG MAL, MY, SP N. nocticolor (Thorell, 1887) PM, MY, SP IND to SU SB, Indon, SP Ordgarius sexspinosus (Thorell, 1894) PM, MY, SP IND to JP, Indon MAL, MY, SP Perilla teres Thorell, 1895 Ð MAL, MY, VN

308 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Continued.

Country Distributions From Sources Species List Murphy & Murphy (2000) N. Platnick (2006) Song et al. (2002)

Pitharatus junghuhni (Doleschall, 1859) Ð MAL, JA, SUL Poltys apiculatus Thorell, 1898 PM, SP SP MAL, SP P. dubius (Walckenaer, 1842) PM, JA, SU VN P. illepidus C. L. Koch, 1843 SP, all? Indon to PH, AU MAL, Indon, SP, PH Pronous affi nis Simon, 1901 Ð MAL Thelacantha brevispina (Doleschall, all? AU, IND to PH, Madagascar MAL, Indon, MY, SP, PH 1857) Zygiella calyptrata (Thorell, 1895) PM, CH, MY, SP Ð Z. calyptrata (Workman & Workman, Ð MAL, CH, MY MAL, MY, SP 1894)

FAMILY: CLUBIONIDAE Clubiona damirkovaci Deeleman- Ð MAL Reinhold, 2001 Malamatidia vethi Deeleman-Reinhold, Ð MAL, BO 2001 Matidia trinotata Thorell, 1890 Penang SP MAL MAL, SP Nusatidia aeria (Simon, 1897) PM, PH MAL Pristidia prima Deeleman-Reinhold, Ð MAL, JA, SU 2001 Pteroneta saltans Deeleman-Reinhold, Ð MAL, BO, SUL, Sunda Is 2001

FAMILY: CORINNIDAE Castoponera ciliata (Deeleman- PM, SU MAL Reinhold, 1993) Corinnomma harmandi Simon, 1886 PM, MY, SP, TL IND to CH, PH, SUL C. severum (Thorell, 1877) Ð MAL MAL,CB,Indon,MY,PH,SP,TL Oedignatha mogamoga Marples, 1995 Ð MAL, BO O. scrobiculata Thorell, 1881 Penang, JA, SP IND, TW to PH MAL, Indon, SP Pranburia mehannopi Deeleman- Ð MAL, CB, TL Reinhold, 1993

FAMILY: CRYPTOTHELIDAE Cryptothele sundaica Thorell, 1890 Penang, JA, SP, SU JA, SP, SUL MAL, Indon, SP Acantheis longiventris Simon, 1897 Ð MAL, Indon A. oreus (Simon, 1901) Ð MAL

FAMILY: CTENIDAE Ctenus corniger F. O. P.-Cambridge, PM, SP S.Africa MAL, SP 1898 C. fl oweri F. O. P.-Cambridge, 1897 Penang MAL C. fungifer Thorell, 1890 Penang MAL C. valvularis (Hasselt, 1882) PM, JA, SU JA, SU

FAMILY: DEINOPIDAE Deinopis kollari Doleschall, 1859 PM, MY MAL, MY

FAMILY: DESIDAE Badumna exilis Thorell, 1890 PM, JA JA B. hirsuta Thorell, 1890 PM, JA JA Desis martensi C. L. Koch, 1872 PM, SP MAL MAL, SP

FAMILY: DICTYNIDAE Penangodyna tibialis Wunderlich, 1995 Penang MAL

309 Norma-Rashid & Li: Checklist of spiders from Peninsular Malaysia

Table 1. Continued.

Country Distributions From Sources Species List Murphy & Murphy (2000) N. Platnick (2006) Song et al. (2002)

FAMILY: GNAPHOSIDAE Drassodes brachythelis (Thorell, 1890) PM, SU SU D. russulus (Thorell, 1890) PM, JA JA

FAMILY: HERSILIDAE Hersilia sumatrana (Thorell, 1890) PM, BO, SU MAL, BO, IND, SU

FAMILY: SPARASSIDAE Gnathopalystes crucifer (Simon, 1880) PM, JA MAL to JA G. kochi (Simon, 1880) PM, JA, MY, SP, SU MAL, BO, IND, JA, MY, MAL, Indon, MY, SP SU Heteropoda boiei (Doleschall, 1859) MAL, JA, SU H. furva Thorell, 1890 Penang MAL H. imbecilla Thorell, 1892 Ð MAL, SU H. leprosa Simon, 1884 MY, PM MAL, IND, MY H. nebulosa Thorell, 1890 Penang MAL H. parva Jager, 2000 MAL H. sexpunctata Simon, 1885 MY, PM MAL, IND Olios annandalei (Simon, 1901) Ð MAL O. cursor (Thorell, 1894) PM, SP MAL MAL, SP Pandercetes malleator Thorell, 1890 Penang Rhitymna pinangensis (Thorell, 1891) Penang MAL R. xanthopus Simon, 1901 Kelantan MAL Sinopoda microphthalmus (Fage, 1929) B Caves MAL Spariolenus tigris Simon, 1880 India, PM MAL, IND, PK Stasina planithorax Simon, 1897 Ð MAL Thelcticopis goramensis (Thorell, 1881) PM, NG MAL T. modesta Thorell, 1890 Penang, SP MAL MAL, SP T. pennata (Simon, 1901) Kelantan MAL

FAMILY: Batueta voluta Locket, 1982 Ð MAL MAL, SP Ceratinopsis blesti Locket, 1982 Batu Caves area, TL MAL MAL, SP C. orientalis Locket, 1982 Frasers Hill MAL Erigone bifurcata Locket, 1982 Frasers Hill, JA, PH MAL, PH, Karakatau Johorea decorata Locket, 1982 Ð MAL MAL, SP Kaestneria minima Locket, 1982 Batu caves MAL Knischatiria tuberosa Wunderlich, 1995 Cameron Highlands MAL Kuala versa Locket, 1982 Frasers Hill MAL Nasoona chrysanthusi Locket, 1982 Frasers Hill, SP MAL MAL, SP N. prominula Locket, 1982 Batu Caves area, TL MAL Nematogmus dentimanus Simon, 1886 PM, JA, TL MAL to SL, JA Neriene macella (Thorell, 1898) PM, SB, MY, TL MAL, CH, TL, MY Parameioneta spicata Locket, 1982 Frasers Hill, PH MAL Plectembolus trifl ectus Millidge, Kuala Lumpur MAL R-Smith, 1992 Pseudomicrocentria simplex Locket, Ð MAL MAL, SP 1982 Tapinopa vara Locket, 1982 Frasers Hill MAL Theoa tricaudata (Locket, 1982) Batu Caves area MAL, Seychelles

310 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Continued.

Country Distributions From Sources Species List Murphy & Murphy (2000) N. Platnick (2006) Song et al. (2002)

FAMILY: LIOCRANIDAE Sesieutes emanapatus Deeleman- 1 Ð MAL Reinhold, 200 Sphingius thecatus Thorell, 1890 Penang MAL Teutamus politus Thorell, 1890 Penang MAL, TL

FAMILY: LYCOSIDAE Lysania pygmaea Thorell, 1890 Penang MAL Pardosa heterophthalmus (Simon, 1898) PM, JA, SU IND to JA P. irretita Simon, 1886 PM, BO, TL MAL, BO, JA P. laidlawi Simon, 1901 Perak MAL P. pinangensis (Thorell, 1890) Penang, SU MAL, SU P. pusiola (Thorell, 1891) PM, SR, JA, MY, AU IND to CH, JA P. rabulana (Thorell, 1890) PM, JA, SP, SU MAL, JA, SU MAL, Indon, SP P. semicana Simon 1885 Malacca MAL, CH, SL Passiena spinicrus Thorell, 1890 Penang, HK, SU MAL, BO Venonia coruscans Thorell, 1894 SP MAL, SP, TL Zoica parvula (Thorell, 1895) PM, MY, TL MAL, TL, MY, SL

FAMILY: MIMETIDAE Mimetus margaritifer Simon, 1901 Kelantan MAL

FAMILY: MYSMENIDAE Crassignatna haeneli Wunderlich, 1995 Frasers Hill MAL

FAMILY: NEPHILIDAE Herennia ornatissima (Doleschall, SB, Indon, all syn. H. multipunta MAL, MY, SP, TL, VT 1859) * (Doleschall, 1859) Nephila pilipes (Fabricius, 1793) * all? syn N. maculata SP, MY, PH Roewer, 1942 Nephilengys malabarensis Genting & Kinabalu Park-SB syn N.andamanensis Indon, MY, SP, TL (Walckenaer, 1842) * (Tikader, 1977)

FAMILY: NESTICIDAE Nesticella connectens Wunderlich, 1995 Cameron Highlands MAL

FAMILY: OCHYROCERATIDAE Merizocera crinata (Fage, 1929) Batu Caves area MAL Speocera stellafera Deeleman-Reinhold, Kuala Lumpur, TL MAL, TL 1995

FAMILY: OONOPIDAE Gamasomorpha maschwitzi Wunderlich, Kuala Lumpur MAL 1995 Xyphinus xelo Deeleman-Reinhold, Kuala Lumpur MAL 1987

FAMILY: OXYOPIDAE Oxyopes birmanicus Thorell, 1887 PM, MY, SC, SP, SU CH to SU, IND Tioman, Indon, MY, SP O. gemellus Thorell 1891 PM MAL, Nicobar Is O. imbellis Thorell 1890 Penang MAL O. javanus Thorell, 1887 SP, probably all IN, CH to JA, PH MAL, MY, SP, TL O. keyserlingi Thorell, 1881 PM, NG NG O. lineatipes (C. L. Koch, 1847) SP, all? CH to PH, JA, SU MAL, MY, SP, TL O. patalongensis Simon, 1901 MAL

311 Norma-Rashid & Li: Checklist of spiders from Peninsular Malaysia

Table 1. Continued.

Country Distributions From Sources Species List Murphy & Murphy (2000) N. Platnick (2006) Song et al. (2002)

FAMILY: PALPIMANIDAE Boagrius pumilus Simon, 1893 MAL, SU MAL, Indon, SP Sarascelis raffrayi Simon, 1893 MAL, IND MAL, SP

FAMILY: Belisana bohorok Huber, 2005 MAL, BO, SU B. fraser Huber, 2005 MAL B. leuser Huber, 2005 MAL, BO, TL, SU B. nomis Huber, 2005 MAL, SP B. sandakan Huber, 2005 MAL, BO, SU B. strinatii Huber, 2005 MAL Calapnita phyllicola Deeleman- PM, KM, SU MAL, BO, SU Reinhold, 1986 C. vermiformis Simon, 1892 PM, JA,PH,SU MAL to SUL Holocneminus multiguttatus (Simon, all MAL to SL, SUL 1905) Mystes oonopiformis Bristowe, 1938 Parit Buntar MAL Pholcus diopsis Simon, 1901 Ð MAL P. vesculus Simon 1901 Perak MAL Physocyclus globusus (Taczanowski, PM, SP, VN Cosmopolitan Cosmopolitan 1873) Savarna tesselata (Simon, 1901) Ð MAL Spermophora miser Bristowe, 1952 Batu Caves MAL Uthina atrigularis Simon, 1901 PM, SP SP MAL

FAMILY: PISAURIDAE Denrolycosa fusca Doleschall, 1859 PM, JA JA Dolomedes femoralis Hasselt, 1882 PM,SU SU D. poroculus Simon, 1901 Ð MAL Eurychoera quadrimaculata Thorell, PM,SP MAL, SP 1897 Hygropoda longimana (Stoliczka, PM, India MAL, IND 1869) H. prognatha Thorell, 1894 PM, SP SP MAL, SP Polyboea vulpina Thorell, 1895 PM, MY, SP MAL, MY, SP, TL MAL, MY, SP

FAMILY: PSECHRIDAE Fecenia macilenta (Simon, 1885) Malacca, SP? MAL Psechrus argentatus (Doleschall, 1857) PM, SB, SP MAL to Queensland MAL, SP P. singaporensis Thorell, 1894 PM, JA, SP, SU MAL, CH, JA, SU MAL, Indon, SP P. torvus O.P.-Cambridge, 1869 PM, SL or IND, SP, TW? C, IND, TW, SL

FAMILY: SALTICIDAE Agorius constrictus Simon 1901 PM, SP SP MAL, SP A. graculipes Thorell, 1877 PM, SUL SUL Anarrhotus fossulatus Simon, 1902 PM, SP MAL MAL, SP Asemonea pinangensis Wanless, 1980 Penang MAL Augustaea formicaria Szombathy, 1915 PM, SP SP Bathippus pahang Zhang, Song & Li, 2003 Ð MAL (Endau, Pahang) B. schalleri Simon 1902 Penang Bavia aericeps Simon, 1877 PM, PH, SP, SU MAL to AU MAL, PH, SP B. capistrata (C. L. Koch, 1846) Ð MAL 312 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Continued.

Country Distributions From Sources Species List Murphy & Murphy (2000) N. Platnick (2006) Song et al. (2002)

B. sexpunctata (Doleschall, 1859) JA, SP, SU MAL, Indon, SP Bianor diversipes Simon 1901 Kelantan MAL Bristowia heterospina Reimoser, 1934 PM, SC, SP, VN IND, JP MAL, SP, VN Canama forceps (Doleschall, 1859) PM, JA NG C. lacerans (Thorell, 1881) Ð MAL Capocrossa politiventris Simon, 1901 Perak MAL Carrhotus coronatus (Simon, 1885) PM, JA, MY, SU, SC, VN CH, VN to JA C. malayanus Proszynski 1992 Kuala Lumpur MAL C. sannio (Thorell, 1877) PM, JA, MY, SC, SU, VN IND to SUL C. viduus (C. L. Koch, 1846) PM, JA, MY, SC, SP, SU IND to CH, JA MAL, Indon, MY, SP Chrysilla delicata Thorell, 1892 PM, MY, SC, SU MY C. doriai Thorell, 1890 PM, SU SU Colyttus bilineatus Thorell, 1891 Penang, SU SU, Moluccas Cosmophasis thalassina (C. L. Koch, PM, JA, SU MAL to AU MAL, Indon, SP 1846) C. umbratica Simon, 1903 PM, SP, SU IND to SU C. viridifasciata (Doleschall, 1859) PM, JA, SU SU to NG Cytaea sinuata (Doleschall, 1859) PM, Indon, PH, SU PH to AU Diplocanthopoda marina Abraham, Port Dickson MAL 1925 D. plocanthopoda (Thorell, 1881) Ð MAL to NG Echeclus concinnus Thorell, 1890 Penang MAL Emathis coprea (Thorell, 1890) PM, SU SU Epocilla aurantiaca (Simon, 1885) PM, IND, MY MAL, IND E. praetextata Thorell, 1887 PM, JA, MY, SP, SU MY to JA MAL, Indon, MY, SP Euophrys kulczynskii Thorell, 1890 Penang Ð Evarcha fl avocincta (C L. Koch, 1846) PM, Indon, JA, SC, SP, VN CH to JA MAL, Indon, SP, VN Gelotia syringopalpis Wanless, 1984 Kuala Lumpur, SR, SC, SP MAL, BO, CH MAL, SP Harmochirus brachiatus (Thorell, 1877) SU, probably all Bhutan to TW, IND, Indon MAL, MY, SP Hasarius adansoni (Audouin, 1826) all? Cosmopolitan MAL, SP Hyllus diardi (Walckanaer, 1837) all? MY, CH to JA MAL,Indon, MY, SP, TL, VN H. janthinus (C. L. Koch, 1846) PM, JA, MY, SU MY to JA H. lacertosus (C. L. Koch, 1846) PM, JA, SP, SU, VN VN to JA MAL, Indon, SP, VN H. pudicus Thorell, 1895 PM, MY IND to MY Icius glaucochirus (Thorell, 1890) PM, SU SU Idastrandia orientalis (Szombathy, 1915) PM, SP MAL Indon, SP, VN Irura pygaea (Thorell, 1891) Penang MAL Laufeia perakensis (Simon, 1901) Perak, JA MAL to JA Leikung kinabaluensis Benjamin, 2004 MAL, BO L. porosa (Wanless, 1978) Fraser’s Hill MAL, SU Ligurra aheneola (Simon, 1885) MAL L. latidens (Doleschall, 1859) PM to PH, JA MAL to IND PH, SP Mantius russatus Thorell, 1891 Penang MAL Marpissa elata Thorell 1881 PM, NG Ð Mintonia silvicola Wanless, 1987 Taman Negara MAL Myrmarachne albicrurata Badcock, PM, TL syn M. ramosa Badcock 1918 1918 * M. annandalei Simon, 1901 Kelantan MAL

313 Norma-Rashid & Li: Checklist of spiders from Peninsular Malaysia

Table 1. Continued.

Country Distributions From Sources Species List Murphy & Murphy (2000) N. Platnick (2006) Song et al. (2002)

M. aureonigra Edmunds & Prozyn’ski, MAL, SP 2003 M. biseratensis Badcock, 1918 MAL M. clavigera (Thorell, 1877) PM, SUL SU M. cornuta Badcock, 1918 PM-Bukit Besar MAL, SP M. cuneata Badcock, 1918 Bukit Besar, Talun, Ged MAL M. gedongensis Badcock, 1918 PM-Gedong, B Besar M.grossa Edmunds & Prosyn’ski, 2003 MAL M. hirsutipalpi Edmunds & Prosyn’ski, 2003 MAL M. hispidacoxa Edmunds & Prosyn’ski, 2003 MAL M. kochi Reimoser, 1925 MAL, SU, Indon M. malayana Edmunds & Prosyn’ski, MAL 2003 M. manducator (Westwood, 1841) MAL, IND, MY, SU MAL, Indon, MY, SP M. maxillosa (Koch CL, 1846) PM, JA, MY, SC, SP, SU MY to CH, PH, SUL MAL, Indon, MY, PH, SP M. wanlessi Edmunds & Prosyn’ski, MAL 2003 M. turriformis Badcock, 1918 PM-Bukit Besar, Talum MAL Neobrettus sumatranus Logunov, 1998 MAL, Indon, NG N. tibialis (Proszynski, 1978) PM, Bhutan MAL, BO Orsima ichneumon (Simon, 1901) PM, SR, SU MAL, BO, SU Pancorius protervus (Simon, 1902) MAL MAL, SP Panysinus nitens Simon, 1901 PM, SU MAL, SU Paracyrba wanlessi Zabka, Kovac, Selangor MAL 1996 malayensis Wanless, 1981 PM, SP, SU MAL, SP, SU MAL, Indon, SP Phidippus severus (Thorell, 1891) Penang Ð P. suavis (Simon, 1885) PM, SC, VN Nepal to MAL Phintella versicolor (C. L. Koch, 1846) all? CH, Korea, Hawaii, JP, MAL, Indon, MY, SP, VN SU, TW P. vittata (C. L. Koch, 1846) all? Indon to PH MAL, Indon, PH, SP, VN Plexippus malayensis Simon, 1864 Malacca nomina dubia* assamensis Wanless, 1978 PM, Assam, MY IND to MAL P. carassipalpis Peckham, Peckham, PM, Kucing, SP, SR BO, SP MAL, Indon, SP 1907 P. labiata (Thorell, 1887) MY, all? SL to PH MAL, Indon, MY, PH, SP, TL Pseudamycus albomaculatus (Hasselt, PM, JA, SU MAL to JA 1882) Pseudicius decemnotatus Simon 1885 PM, SP SP MAL, SP P. maureri Proszynski, 1992 Batu Caves MAL Pystira ephippigera (Simon, 1885) PM, BO, SP, SU SU Rhene albigera (C. L. Koch, 1848) PM, Indon, SC, SU IND to Korea, SU R. bufo (Doleschall, 1859) PM, Indon, MY, SU MY to SU R. fl avigera (C. L. Koch, 1848) PM, SB, SC, SP, SU, VN CH, VN, SU R. hirsuta (Thorell, 1877) PM, Indon, SUL SUL R. nigrita (C. L. Koch, 1846) PM, SU, Indon Indon R. rubrigera (Thorell, 1887) PM, MY, SC, SU, VN IND to CH, SU, Hawaii Siler pulcher Simon, 1901 Kelantan MAL

314 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Continued.

Country Distributions From Sources Species List Murphy & Murphy (2000) N. Platnick (2006) Song et al. (2002)

Sparbambus gombakensis (Zhang, **** Woon & Li) Spartaeus spinimanus (Thorell, 1878) PM, SR, JA, SP, SU SL to BO MAL, Indon, SP S. wildtracki Wanless, 1987 Taman Negara MAL Stagetillus semiostrinus (Simon, 1901) MAL Taraxella hillyardi Wanless, 1987 PM-Gunung Jerai MAL Telemonia festiva Thorell, 1887 MY, all? MY to JA MAL, Indon, MY, SP, VN T. luteocincta (Thorell, 1891) MAL Thiania bhamoensis Thorell, 1887 MY, all? MY to SU MAL, MY, SP T. pulcherrima C. L. Koch, 1846 PM, IC, JA, SU MAL, SL, SUL, VN T. sinuata Thorell, 1890 Penang MAL T. subserena Simon, 1901 Perak MAL Thorelliola ensifera (Thorell, 1877) SUL, all MAL to SUL, Hawaii Indon, SP, South Pacifi c Is.

FAMILY: SCYTODIDAE Scytodes cavernarum Roewer, 1962 Batu Caves MAL S. magna Bristowe, 1952 Batu Caves MAL S. pallida Doleschall, 1859 * Genting & Frasers, Indon, SP syn. S. pallidus Wang, 1994 Indon, SP, PH Stedocys leopoldi (Giltay, 1935) Frasers Hill MAL

FAMILY: SELENOPIDAE Selenops aculeatus Simon, 1901 Perak MAL

FAMILY: STENOCHILIDAE Colopea malayana Lehtinen, 1982 PM, SP, TL MAL, SP, TL MAL, SP, TL C. pusilla (Simon, 1893) PM, PH, SP MAL, PH MAL, PH, SP

FAMILY: SYMPHYTOGNATHIDAE Anapistula jerai Harvey 1998 MAL, BO, Kalimantan

FAMILY: TELEMIDAE Apneumonella jacobsoni Brignoli, 1977 PM, SU MAL, SU

FAMILY: TETRABLEMMIDAE Ablemma gombakense Wunderlich, 1995 Kuala Lumpur MAL Brignoliella michaeli Lehtinen, 1981 Penang MAL MAL, SP Lamania kraui (Shear, 1978) Pahang-Krau Reserve MAL Paculla cameronensis Shear, 1978 Cameron Highlands MAL P. negara Shear, 1978 Taman Negara MAL P. sulaimani Lehtinen, 1981 Taman Negara MAL Pahanga centenialis Lehtinen, 1981 Kuala Lumpur MAL P. dura Shear, 1979 Frasers Hill MAL Perania cerastes Schwendinger, 1994 Maxwell Hill 1200m MAL P. coryne Schwendinger, 1994 Cameron Highlands MAL Sulaimania vigelandi Lehtinen, 1981 PM-Kota Tinggi MAL

FAMILY: TETRAGNATHIDAE Leucauge argentina (Hasselt, 1882) PH, SP, SU MAL, Indon, SP, PH L. argentina nigriceps Thorell, 1890 Penang MAL MAL, Indon, PH, SP L. celebesiana (Walckenaer, 1841) PM, PH, SC, SP, SU IND to CH, JP, NG, SUL Indon, SP L. granulata (Walckenaer, 1841) JA, PM, SU Sunda Is to AU L. quadrifasciata (Thorell, 1890) PM, SU MAL, Nias IS L. tessellata (Thorell, 1887) * PM, MY, VN syn. L. lygisma Wang, 1991

315 Norma-Rashid & Li: Checklist of spiders from Peninsular Malaysia

Table 1. Continued.

Country Distributions From Sources Species List Murphy & Murphy (2000) N. Platnick (2006) Song et al. (2002)

Mesida gemmea (Hasselt, 1882) PM, JA, MY, SP, SU MY to JA, TW MAL, Indon, MY, SP Opadometa grata (Guerin, 1838) PM, NG, SP SU Indon, NG,Solomon Is Indon, MY, SP Orsinome phrygiana Simon, 1901 PM, JA, SU MAL O. vethi (Hasselt, 1882) PM, JA, SU MAL, CH, JA, SU Tetragnatha chauliodus (Thorell, 1890) Penang, all MY to NG, JP MAL, MY, SP T. hasselti Thorell, 1890 PM, JA, MY, SU, TL IND, SUL T. isidis (Simon, 1880) PM, SU Europe to SU T. lineata Roewer, 1942 MAL T. mandibulata Walckenaer, 1842 Mariana Is, all? Africa, AU, PH Tioman, Indon, MY, SP, TL T. maxillosa Thorell, 1895 * PM, JA, MY, PH, SC, SP, syn. T listeri Gravely, 1921 MAL, MY, PH, SP, TL, VN TL & VN T. serra Doleschall, 1857 Indon, HK, JA, SC, SP, SU, TL T. virescens Okuma, 1979 PM, IND, PH, TL IND, SL to Indon, PH Tylorida stellimicans (Simon, 1885) MAL T. ventralis (Thorell, 1877) SUL, all IND to TW, JP, NG MAL, Indon, MY, SP

FAMILY: Achaearanea mundula (C. L. Koch, PM, AU, MY, SC, SP IND to Caledonia MAL, Indon, MY,SP 1872) Argyrodes fasciatus Thorell, 1892 MAL, SP MAL, SP A. fi ssifrons O.P. -Cambridge, 1869 Tioman-MAL, Indon, MY, SP, TL A. fragilis Thorell 1877 PM, SUL SUL A. kualensis Hogg, 1927 Kuala Lumpur MAL A. miniaceus (Doleschall, 1857) PM, Indon, SC, SP Korea, JP, AU MAL, Indon, SP Anelosimus agnar Agnarsson, 2006 MAL A. kohi Yoshida, 1993 MAL, SP SP Coleosoma blandum O.P. Cambridge, Johore, Sri Lanka and all Cosmopolitan MY, SP, Cosmopolitan 1882 Episinus rhomboidalis (Simon, 1895) PM, SP, MY Cameroon MAL, MY, SP Molione triacantha Thorell, 1892 PM ,SC, SP, TW MAL, SP, TW MAL, SP M. uniacantha Wunderlich, 1995 PM, SU MAL, SU Phoroncidia lygeana (Walckenaer, 1841) JA, SU, all? MAL, SU Steatoda parakensis Simon, 1901 Perak MAL Theridion labeculosum Workman, 1900 PM, SP Ð MAL, SP T. ludus Simon, 1880 MAL to AU, Caledonia T. perpusillum Simon, 1885 Malacca MAL T. subradiatum Simon, 1901 MAL

FAMILY: THERIDIOSOMATIDAE Andasta cyclosina Simon, 1901 MAL Theridiosoma cyclosina (Simon, 1901) Perak T. nebulosum Simon, 1901 MAL

FAMILY: Alcimochthes limbatus Simon 1885 Malacca, SC, SP, SU, TW, CH, JP, SP, TW, VN MAL, MY, SP, VN VN Amyciaea forticeps (P.-Cambridge, O, PM, SL, JA, MY, SC, SP MAL,JA,MY,SL MAL, Indon, MY, SP 1873) Angaeus rhombifer Thorell, 1890 PM, SP, SU MAL, SU MAL, Indon, MY, SP Cebrenninus annulatus (Thorell, 1890) PM, SU SU

316 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Continued.

Country Distributions From Sources Species List Murphy & Murphy (2000) N. Platnick (2006) Song et al. (2002)

Hedana morgani (Simon, 1885) Malacca MAL Loxobates ornatus Thorell, 1891 Penang MAL Misumenops nepenthicola (Pocock, SB, SP, SU MAL, SP 1898) Oxytate virens (Thorell, 1891) Nicobar Is, SP, VN MAL, SP, VN Pharta bimaculata Thorell, 1891 PM, Nicobar Is MAL Philodamia hilaris Thorell, 1894 PM, SP SP MAL, SP P. variata Thorell, 1894 PM, SP SP MAL, SP Smodicinodes kovaci Ono, 1993 Selangor MAL Strigoplus albostriatus Simon, 1885 PM, JA, MY, VN MAL, Bhuttan Tmarus loriae Thorell, 1890 Penang MAL Zygometis cristulata Simon, 1901 Perak

FAMILY: ULOBORIDAE Philoponella quadrituberculata PM, JA, SP JA, Moluccas MAL, Indon, SP (Thorell, 1892) P. raffrayi (Simon, 1891) PM, JA, SP JA, Moluccas Uloborus oculatus Kulczynski, 1908 PM, SP SP MAL, SP U. spelaeus Bristowe, 1952 Batu Caves MAL U. undulatus Thorell, 1878 PM, Indon, JA, SP MAL, Indon, SP U. indicus Kulczynski, 1908 MAL to Pantropical MAL, SP Zosis geniculata (Olivier, 1789) C America, all MAL MAL, MY, SP, TL

FAMILY: ZODARIIDAE Heradion damrongi Damkittipakul & MAL Jocque, 2004 H. luctator Dankittipakul & Jocque, MAL 2004 H. pernix Dankittipakul & Jocque, 2004 MAL Mallinella cinctipes (Simon, 1893) PM, MY, SP MAL, Andaman, MY, SP MAL, Indon, MY, SP M. obnubila Simon, 1901 Perak MAL M. sciophana Simon, 1901 Perak MAL, SU

Species Total 405 284 276 112

* notes as indicated within the table synonymous (syn.) species given or other information. ** due to unknown specifi c areas, distributions stated as “all” or “cosmopolitan” are not considered unless supported by another reference *** presence of species as reported in J.K.H. Koh (1991) **** presence of species as fi rst described in Zhang et al (2006)

317 Norma-Rashid & Li: Checklist of spiders from Peninsular Malaysia

Table 2. New records of spiders for Peninsular Malaysia with some added notes .

Family / Species List Notes on aspects of taxonomy and/or Other related notes e.g descriptions, country distribution habitat and natural history

FAMILY: ARANEIDAE 1. Cyclosa insulana (Costa, 1834) Type locality Italy; have been recorded Characteristic feature of the species web is from Indonesia, Myanmar, Singapore, the presence of stabilimentum. Thailand and Vietnam. 2. Cyrtophora moluccensis (Doleschall, Type locality Indonesia; ranging from Webs normally located in shrubs. 1857) China, Indonesia to Japan and Australia.

FAMILY: CLUBIONIDAE 3. Clubiona meraukensis Chrysanthus, Previously known only in New Guinea. Can be found in shrubs seeking shelter in 1967 leaves that may be dead or alive.

FAMILY: LYCOSIDAE 4. Pardosa sumatrana (Thorell, 1890) Type locality Sumatra of wide distribution; Ground living spiders living in grassy areas, Hong Kong, India, Indonesia, Japan, Nepal, actively hunting down preys. Male shows Philippines, Sri Lanka, South China, courtship displays by up and down Sumatra. movements of the palps. 5. P. zhanjiangensis Yin, Wang, Peng Type locality Guangdong, China. Able to thrive in swampy areas. & Zie, 1995

FAMILY: PISAURIDAE 6. Dolomedes mizhoanus Kishida, 1936 Type locality Japan; also found in Taiwan Exploit waterside habitats and able to prey and little information on South East Asian on small fi shes. species.

FAMILY: SALTICIDAE 7. Epeus fl avobilineatus (Doleschall, Type locality Java, also found in Singapore Found in forests including mangroves and 1859) gardens 8. E. glorius Zabka, 1985 Type locality Vietnam; also found in A brightly coloured species roaming on Singapore and South China. garden or forest foliage. 9. Myrmarachne elongata Szombathy, Type Uganda (Africa), also found in These species are good ant mimics 1915 Myanmar and Vietnam. wander above ground. 10. Plexippus paykulli (Audouin, 1826) Type locality Egypt; wide ranging patterns; Versatile lifestyle; living in mangroves, near Africa, China, Indonesia, Japan, New water and agriculture land feasting on Guinea, Philippines, Singapore and Vietnam. agricultural pests such as armyworm. 11. Portia fi mbriata (Doleschall, 1859) Type locality from Ambon, Indonesia with Very rough overall appearance with a a wide distribution in Australia, Nepal, Sri characteristic leg segments suitable for Lanka and Taiwan. stealthy movements on prey’s web. This species is a spider eater and can be found in or near other spider’s web. 12. Stagetillus opaeiceps Simon, 1885 Species only known from type locality i.e Typically long and narrow abdominal Sumatra. shape. 13. Thianitara spectrum Simon, 1903 Known from type locality, Sumatra. Males seemed to resemble the more common congener, T. bhamoensis.

FAMILY: TETRAGNATHIDAE 14. Leucauge decorata (Blackwall, 1864) Type locality East Indies and distributional Build large webs in areas of grasses, shrubs regions are Hong Kong, Taiwan and to tall trees. Males are distinctly much Paleotropical. smaller than females. 15. L. tessellata (Thorell, 1887) Type locality Yunan, China Dorsal abdomen with dark patches. synonymous to L. lygisma Wang, 1991 16. Tetragnatha josephi Okuma, 1988 Previously known only from type locality, Characteristic long features from forward Singapore projecting fangs to abdomen and legs. Build webs in grasses to tall trees or near water, even in water tanks. 17. Tylorida striata (Thorell, 1877) Type locality Sumatra. Also found in Commonly found in grassy areas of gardens Australia, China, Japan, Philippines, and forest fringes. Has been recorded in Singapore, Taiwan. ricefi elds.

318 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 2. New records of spiders for Peninsular Malaysia with some added notes .

Family / Species List Notes on aspects of taxonomy and/or Other related notes e.g descriptions, country distribution habitat and natural history

FAMILY: THERIDIIDAE 18. Achaearanea t-notatum (Thorell, Type locality Myanmar, reported present in Abdomen with a characteristic shape in 1895) Singapore. profi le. Can be found in gardens and mangroves. 19. Moneta mirabilis (Bösenverg & Type locality Japan, also found in Taiwan In plan view the abdomen has a characteristic Strand, 1906) and Singapore. triangular shape.

FAMILY: THOMISIDAE 20. Phrynarachne decipiens (Forbes, Type locality Java, also found in Sumatra. Ability to camoufl age well in taking 1883) appearance of bird excrement.

LINYPHIIDAE Blackwall, 1859 1989; 2 females, 2 males, Pulau Tioman, coll. D.Q. Li, 27 June 1999. Nasoona prominula Locket, 1982

1 female, 1 male, ZRC.1994.51-52, leaf litter, Genting, FAMILY: OXYOPIDAE Thorell, 1870 Pahang, col. J.A & F. Murphy, 26 Nov.1990. Oxyopes birmanicus Thorell, 1887

Neriene macella (Thorell, 1898) 1 male, ZRC.ARA.249, Juara track, Pulau Timan, det. Song, coll. D.Q. Li, 24 June 1999; 2 females, ZRC.ARA.247, Sg. 5 males, Taiping Hills, 3,000 to 4,000 feet, det. N. Scharff; Mapor, Johore, coll. H.K.Lua; 1 male, waterfall, Fraser’s 1 male, Fraser’s Hill, Pahang, det. N. Scharff, coll. H.K. Hill, Pahang, coll. H.K.Lua, 31 Dec 1989; 1 female, swamp Lua, 30 Dec.1989. forest, North Selangor, 17 June 1991.

Parameioneta spicata Locket, 1982 FAMILY: PISAURIDAE Simon, 1890

1 female, 1 male, ZRC.1994.49-50, leaf litter, Genting, Dolomedes mizhoanus Kishida, 1936, new record Pahang, coll. J.A. Murphy, 30 Nov. 1990. 1 male, ZRC.ARA.107, Sg. Paya. Tioman, coll. D.Q. Li, 26 June 1999. LYCOSIDAE Sundevall, 1833

Pardosa sumatrana (Thorell, 1890), new record Eurychoera quadrimaculata Thorell, 1897

1 male, ZRC.ARA.275, Sg. Paya, Pulau Tioman, 26 June 1 female, Genting, Pahang, 1-15 Feb 1988; 3 females, 1999. Gunung Panti area, logging track, Johore, coll. C.M Yang, 20 Sept 1990; 1 male, 2 females, Trengganu rocky waterfall, coll. H.K. Lua, 18 March 1992; 2 females, peat swamp P. zhanjiangensis Yin, Wang, Peng & Zie, 1995, forest, North Selangor, coll. H.K. Lua, 19 June 1991, new record

1 female, 3 males, ZRC.ARA.277-278, Paya mangrove, Polyboea vulpina Thorell, 1895 Pulau Tioman, det. Song, coll. D.Q. Li, 26 June 1990. 1 male, 1 female, ZRC.ARA.293 / ZRC.ARA.1994-35-36, Genting, Pahang, 18-22 Aug. 1979. FAMILY: NEPHILIDAE Simon, 1894

Nephilengys malabarensis (Walckenaer, 1842)

6 females, 6 males, ZRC.ARA.236-233, on walls Gap Rest House, Selangor, det. D.H. Murphy, 16 Aug 1967; 3 females, Frasers Hill, Pahang, coll. H.K. Lua, 31 Dec

319 Norma-Rashid & Li: Checklist of spiders from Peninsular Malaysia

FAMILY: PHOLCIDAE C. L. Koch, 1850 Myrmarachne elongata Szombathy, 1915, new record

Uthina atrigularis Simon, 1901 1 female, 1 male, ZRC.1996.202-203, remnant forest, Layang-layang, Johore, det. J.A. Murphy, 27 July 1979, 1 female, 1 male, ZRC.ARA.393, Genting, 1-15 Feb 1988. Neobrettus tibialis (Proszynski, 1978)

FAMILY: PSECHRIDAE Simon, 1890 1 female, 1 male, banana trunks, Pahang, Genting, det. J.A. Murphy, 29 Nov 1990.

Fecenia macilenta (Simon, 1885) Plexippus paykulli (Audouin, 1826), new record 1 female, ZRC.ARA.126, Genting, Pahang, det. D.X. Song, 26 Nov. 1990. 1 female, ZRC.1996.195, garden, Genting, Pahang, det. J.A. Murphy, 1-15 Feb 1988. Psechrus singaporensis Thorell, 1894

1 male, Call. No. 1982.1.18.26, dark caves, Batu Caves, det. Portia fi mbriata (Doleschall, 1859), new record Walter C. Sedgwick, coll. E. Seimund, 19 Dec 1928. 1 female, 1 male, ZRC.1996-154, garden, Genting, Pahang, det. J.A. Murphy, 1-7 Feb 1988. FAMILY: SALTICIDAE Blackwall, 1841

Bristowia heterospina Reimoser, 1934 P. labiata (Thorell, 1887)

1 female, 1 male, ZRC.1996-168-169, leaf litter, Banting, 1 male, ZRC.1996.192, remnant forest, Layang-layang, Selangor, det. J.A. Murphy, 16 May 1981. Johore, det. J.A. Murphy, 27 July 1979.

Carrhotus sannio (Thorell, 1877) Rhene fl avigera (C. L. Koch, 1848)

1 female, ZRC1996-154, garden, Layang-layang, Johore, 1 female, 1 male, ZRC.1996.194-195, garden, Genting, det. J.A. Murphy, 21-23 Jul 1979. Pahang, det. J.A. Murphy, 26 Nov 1990.

Cosmophasis umbratica Simon, 1903 Stagetillus opaeiceps Simon, 1885, new record

1 female, 1 male, ZRC.1996.155-156, garden, Layang- 1 female, ZRC.1996.165, garden, Genting, Pahang, det. J.A. layang, Johore, det. J.A. Murphy, 21-23 July 1979. Murphy, 18 Aug 1979.

Epeus fl avobilineatus (Doleschall, 1859), new record Thiania bhamoensis Thorell, 1887

1 female, 1 male, ZRC.1996.180-181, garden, Layang- 1 female, 1 male, ZRC.1996.163-164, bushes, Pinang, det. layang, Johore, det. J.A. Murphy, 21-23 July 1979. J.A. Murphy, 16-17 Feb 1979.

E. glorius Zabka, 1985, new record Thianitara spectrum Simon, 1903, new record

1 female, 1 male, ZRC.1996.177-178, remnant forest, 1 female, 1 male, ZRC.1996.166-167, garden, Genting, Layang-layang, Johore, det. J.A. Murphy, 27 July 1979. Pahang, det. J.A. Murphy, 20 Aug 1979.

FAMILY: SCYTODIDAE Blackwall, 1864 Harmochirus brachiatus (Thorell, 1877) Scytodes pallida Doleschall, 1859 2 males, ZRC.ARA.137, on bushes, Genting, Pahang, det. J.A. Murphy, 26 Nov 1990. 1 female, 1 male, ZRC.1994.32-33 garden, Genting, Pahang, det. J.A. Murphy, 27 Nov. 1990.

320 THE RAFFLES BULLETIN OF ZOOLOGY 2009

FAMILY: TETRAGNATHIDAE Menge, 1866 Lampropelma violaceopes Abraham, 1924

Leucauge celebesiana (Walckenaer, 1841) 1 male, ZRC.ARA.178, Kuala Lipis, Pahang, det. H.C. Abraham, 30 June 1929. 4 females, ZRC.ARA.184, Pulau Tioman, Pahang, D.X. Song, coll. D.Q. Li, 24 June 1999; 1 female, 1 male, ZRC. ARA.234, Paya mangrove, Tioman, 26 June 1999. Selenocosmia javanensis (Walckenaer, 1837)

1 female, ZRC.ARA.332, Bukit Cerakah, H.C. Abraham, Leucauge decorata (Blackwall, 1864), new record 26 July 1921; 1 female, 1 male, ZRC.ARA.334, Selangor, Kuala Lumpur, H.M. Pendlebury, Feb 1924. 1 female, ZRC.ARA.185, Genting, Pahang, 1-14 Feb 1988. FAMILY: THERIDIIDAE Sundevall, 1833

L. tessellata (Thorell, 1887), new record Achaearanea mundula (C. L. Koch, 1872)

In synonymy: L. lygisma Wang, 1991 2 females, ZRC.ARA.18, Genting, H.K.Lua, 30 Dec. 1 male, ZRC.188, Tioman, det. D.X. Song, coll. D.Q. Li. 1989. 26 June 1999.

A. t-notatum (Thorell, 1895), new record Tetragnatha josephi Okuma, 1988, new record 1 female, 1 male, ZRC.1994-63-64, garden, Genting, 1 male, ZRC.ARA.365, Tioman, coll. D.Q. Li, 26 June Pahang, det. J.A.Murphy, coll. J.A & F. Murphy, 1 Feb 1999. 1998.

Tetragnatha mandibulata Walckenaer, 1842 A. fi ssifrons O.P. -Cambridge, 1869

1 male, ZRC.ARA.336, Sg Paya, Tioman, coll. D.Q. Li, 2 females, 2 males, ZRC.ARA.41, Paya mangrove, Pulau 26 June 1999. Tioman, coll. D.Q.Li, 26 June 1990.

Tylorida striata (Thorell, 1877), new record Coleosoma blandum O.P. -Cambridge, 1882

1 female, 1 male, ZRC.ARA.390, Pahang, 14 Feb 1988. 1 female, 1 male, ZRC.ARA.66, Genting, 26 Nov. 1990; 1 female, 1 male, ZRC.1994.56-57, garden, Genting, Pahang; coll. J.A & F. Murphy, 26 Nov 1990.

FAMILY: THERAPHOSIDAE Thorell, 1869 Moneta mirabilis (Bösenberg & Strand, 1906), new record Coremiocnemis valida Pocock, 1895 1 female, 1 male, Fraser’s Hill, Pahang, det. I. Agnarsson, 1 male, ZRC.ARA.177, Johore, Nov 1923; 1 female, ZRC. coll. H.K. Lua, 31 Dec 1989. ARA.418, Langkawi, Kedah, 23 April 1928; 3 females, ZRC.ARA.67, Fraser’s Hill, Pahang, coll. H.M. Pendlebury, 1 Feb 1929; 2 females, ZRC.ARA.68, Penang; 1 female, Phoroncidia bukolana Barrion & Litsinger, 1995, ZRC.ARA.179, Renggam, Johor, det. D.X. Song, 3 Aug new record 1938; 1 male, ZRC.ARA. 181, Kuala Tahan, Pahang, coll. C.S. Ogilvia, 1948; 1 female, ZRC.ARA.07, Kota Tinggi, 1 male, Fraser’s Hill, Pahang, coll. H.K.Lua, 31 Dec Johore, coll. Tan Kiou Nee, 11 Jan 1971. 1989.

C. cunicularia (Simon, 1892) P. lygeana (Walckenaer, 1841) 1 female, Fraser’s Hill, height of 4,000 feet, inhabits silk 1 female, 1 male, ZRC.ARA.1994.60-61, garden, Genting, lined burrows on earth banks, det. B.F. Striffl er, col. E. Loh Pahang, det. J.A. Murphy, 1-15 Feb 1988. & K. Lim, 2 June 1990.

321 Norma-Rashid & Li: Checklist of spiders from Peninsular Malaysia

FAMILY: THOMISIDAE Sundevall, 1833 LITERATURE CITED

Phrynarachne decipiens (Forbes, 1883), new record Barrion, A. T. & J. A. Litsinger, 1995. Riceland spiders of South 1 female, 1 male, ZRC.ARA.284, Ulu Gombak, 7 Nov & Southeast Asia. CAB Int. & Int. Rice Research Institute. 1969. Cambridge, United Kingdom. 700 pp. Green, J. 1999. Sampling method and time determines composition of spider collections. Journal of Arachnology. 27: 176Ð182. FAMILY: ULOBORIDAE Thorell, 1869 Koh, J. K. H., 1991. Spiders of the family Araneidae in Singapore mangroves. The Raffl es Bulletin of Zoology. 39(1): 169-182. Zosis geniculata (Olivier, 1789) Murphy, F.M & J. A. Murphy, 2000. An Introduction to the Spiders of South East Asia. Malayan Nature Society, Kuala 1 female, 1 male, ZRC.1994.10-11, garden, Genting, Lumpur. 625 pp. Pahang, coll. J.A & F. Murphy, 18-21 Aug 1979. Platnick, N.I., 2008. The world spider catalog, version 8.5. FAMILY: ZODARIDAE Thorell, 1881 American Museum of Natural History, online at http:// research.amnh.otg/entomology/spiders/catalog/index.html Platnick, N.I., 2006. The world spider catalog, version 7.0. Mallinella cinctipes (Simon, 1893) American Museum of Natural History, online at http:// research.amnh.otg/entomology/spiders/catalog/index.html 2 females, ZRC.1994.3-4, pitfall, loop trail, Ulu Kinchin, Song, D. X., J. X. Zhang & D. Li., 2002. A checklist of spiders Pahang, coll. H.K. Lua et al., 20 June 1990. from Singapore (Arachnida: Araneae). Raffles Bulletin of Zoology. 50(2): 359Ð388. Workman, T. 1896. Spiders: Malaysian Spiders. Belfast. 104 pp. CONCLUSION Zhang, J.X., D.X. Song & D. Li. 2003. Six new and one newly recorded species of Salticidae (Arachnida: Araneae) from The current compilation on spiders from Peninsular Singapore and Malaysia. Raffl es Bulletin of Zoology, 51(2): Malaysia although with an impressive total species number 187Ð195. of 425 species, in our opinion is far from complete. This Zhang J. X., J. R. W.Woon & D. Li, 2006. A new genus and work had indicated that the collections were rather skewed species of jumping spiders (Araneae: Salticidae: ) towards specifi c localities, for example tourist resorts (Batu from Malaysia. Raffl es Bulletin of Zoology, 54(2): 241Ð244. Caves, Tioman Island, Fraser’s Hill and Genting Highlands) and National Parks. It is imperative therefore to conduct a comprehensive sampling throughout Peninsular Malaysia to reveal the actual species numbers, accurate distribution patterns, state of endemism and current species status. We see this as our vital role and subsequent work to be focusing on so as to perhaps outrun the existing and forthcoming anthropogenic development.

ACKNOWLEDGEMENTS

There are many parties who have made this work possible. The fi rst author wishes to acknowledge: NUS, especially her host and members of the Spider Lab for the sabbatical attachment; RMBR headed by Prof Peter Ng and his many helpful staff members in which Ms H.K. Lua needs a special mention. Not forgetting our outmost gratitude to D.H. Murphy, C.M. Yang and H.K. Lua for the collections, D.X. Song for identifi cations and 2 anonymous reviewers helped to improve the manuscript.

322 THE RAFFLES BULLETIN OF ZOOLOGY 2009

THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 323 –342 Date of Publication: 31 Aug.2009 © National University of Singapore

SIX NEW SPIDERS FROM CAVES OF NORTHERN VIETNAM (ARANEAE: TETRABLEMMIDAE: OCHYROCERATIDAE: TELEMIDAE: SYMPHYTOGNATHIDAE)

Yucheng Lin Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, P. R. China Graduate University of Chinese Academy of Sciences, Beijing 100039, P. R. China

Dinh-Sac Pham Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, P. R. China Graduate University of Chinese Academy of Sciences, Beijing 100039, P. R. China

Shuqiang Li Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, P. R. China Email: [email protected] (Corresponding author)

ABSTRACT. – Six new species, collected from caves of Cuc Phuong and Cat Ba National Parks, Northern Vietnam, are diagnosed, described and illustrated: Lehtinenia bisulcus (male, female) (Tetrablemmidae), Speocera bulbiformis (male, female) (Ochyroceratidae), Telema cucphongensis (male, female), T. exiloculata (male, female) (Telemidae), Anapistula orbisterna (female) and Patu bispina (male, female) (Symphytognathidae). The families Ochyroceratidae, Telemidae and Symphytignathidae are reported from Vietnam for the fi rst time. All type specimens are deposited in the Institute of Zoology, Chinese Academy of Sciences in Beijing (IZCAS).

KEY WORDS. – Taxonomy, troglobiont, cosmotropical regions, diagnosis, description.

INTRODUCTION species live under leaf litter or beneath stones in caves. A total of 30 genera and 133 species have been described Early studies on the spiders of Vietnam were undertaken (Brignoli, 1972-1980; Shear, 1978, 1979; Bourne, 1980, by Simon (1886, 1903, 1904, 1909) and Hogg (1922), who 1981; Deeleman-Reinhold, 1980, 1993; Lehtinen, 1981; described species of the families Agelenidae, Araneidae, Schwendinger, 1989, 1994; Wunderlich, 1995; Burger, Ctenidae, Deinopidae, Hexathelidae, Liocranidae, Lycosidae, 2005; Tong & Li, 2008a; Platnick, 2009). Two subfamilies Mimetidae, Oonopidae, Philodromidae, Pholcidae, Pisauridae, are recognized, the Pacullinae (medium sized species) and Salticidae, Scytodidae, Sparassidae, Tetragnathidae, Tetrablemminae (minute to small species). Three species Theridiidae, Thomisidae, Uloboridae and Zodariidae. Later, were reported from Vietnam by Lehtinen (1981), i.e. Lehtinen (1981) described three new tetrablemmids and Singaporemma adjacens, S. halongense and Tetrablemma Zabka (1985) reported 100 Salticidae species, including 8 vietnamense. new genera and 51 new species. Recent work on spiders of Vietnam were done by Grismado & Ramírez (2004), The family Ochyroceratidae was erected by Fage in Jäger (2003), Jäger & Vedel (2005), Tu & Li (2004, 2006), 1912 and is distributed mostly in cosmotropical regions. Wang, Li & Xu (2008), Wang & Jäger (2008) on families Ochyroceratids are very small (total length 0.6-3.0 mm) and Amaurobiidae, Zodariidae, Sparassidae, and Linyphiidae. A web-spinning haplogyne spiders. Most of species are found total of 32 spider families, 159 genera and 320 species are in leave litter from the tropics or living as troglobites in the recorded from Vietnam (Pham, Xu & Li, 2007). caves (Saaristo, 1998; Baptista, 2003). Deeleman-Reinhold (1995) studied ochyroceratids from the Indo-Pacifi c region. The family Tetrablemmidae, erected by O. Pickard- Dumitrescu and Georgescu (1992) reported three species Cambridge in 1873 and distributed mostly in tropical from Cuba. Tong and Li (2007) described one new genus or subtropical regions, is known as “armoured spiders” and eight species of ochyroceratids from tropical Hainan because of the presence of abdominal scutum. Most of Island, China. As far, a total of 14 genera and 156 species are recorded worldwide (Platnick, 2009). 323 Lin & Li: Cave spiders from Vietnam

The family Telemidae, erected by Fage in 1913, is measurements are shown as: total length (femur, patella, distributed from tropical Africa, Europe, East and South tibia, metatarsus, tarsus). The following abbreviations are East Asia to North and Central America (Brignoli, 1977). used in the text and fi gures: ALE-anterior lateral eye; AME- Telemids are cryptozoa and live in moist and dark habitats, anterior median eye; AP-apical process; CA-copulatory such as in leaf litter, under stones and especially abundant antrum; CB-cymbium; CD-copulatory duct; E-embolus; in caves. In recent years, several telemid species were ED-ejaculatory duct; EF-epiginal fold; EP-epiginal pit; FD- described from Yunnan-Guizhou Plateau (Song & Zhu, fertilization duct; IVP-inner vulval plate; LH-lateral horn; 1994; Wang & Ran, 1998; Zhu & Chen, 2002; Tong & Li, PA-preanal plate; PLE-posterior lateral eye; PME-posterior 2008b) and tropical regions in southern China (Tong & Li, median eye; POG-postgenital plate; S-spermatheca; SR- 2008c; Lin & Li, 2008). The family Telemidae contains 7 seminal receptaculum; TS-tracheal spiracle; VP-ventral genera and 31 species worldwide (Platnick, 2009). plate; VS-vulval stem.

The family Symphytognathidae was established by Hickman in 1931 and redefi ned by Forster and Platnick TAXONOMY in 1977. Symphytognathids mostly occur in the tropics of Central and South America, the Oceania and the Africa. Tetrablemmidae O. Pickard-Cambridge 1873 Symphytonathids are the smallest spiders in the world. Male Patu digua from Colombia has a length of only 0.37 Lehtinenia Tong & Li 2008 mm (Forster & Platnick, 1977). Baert and Jocqué (1993) described a smallest female symphytonathid from Ivory Lehtinenia bisulcus new species Coast, i.e. Anapistula caecula. If it was found, male of A. (Figs. 1A−B; 2A−F) caecula may be smaller than male of P. digua. According to Platnick (2009), the Symphytognathidae includes 6 genera Material examined. – Holotype - Male (IZCAS), Prehistoric Man and 45 species. Three Anapistula species are reported from Cave (20°18'N, 105°40'E; Alt: 256 m), Cuc Phuong National Park, Asia (Ono, 2002; Tong & Li, 2006; Harvey, 1998). Patu Vietnam, coll. S. Li, 19 July 2008. occurs in Colombia, Oceania and Seychelles Islands of Paratypes – 4 females (IZCAS), same data as holotype. Africa. An undescribed species of the genus Patu is found in Japan with report on its web structure and web-building Diagnosis. – The new specie is similar to L. bicornis behavior (Hiramatsu & Shinkai, 1993; Ono, 1996). from Hainan Island, China (Tong & Li, 2008), but can be distinguished by the proximally wider and distally narrower Spiders from subterraneous habitats in Vietnam are poorly palpal bulb, the distally furcate embolus, the swollen palpal studied. During an exploration of four caves in Cuc Phuong femur, and the elevated ocular area in males; and the arcuate and Cat Ba National Parks, some tiny spiders were collected epiginal pit, the short and broad inner vulval plate, and the and six new species are recognized. They belong to the presence of translucent center process in frontal of inner families Tetrablemmidae, Ochyroceratidae, Telemidae and vulval plate in females. Symphytognathidae, and the last three families are newly recorded from Vietnam. Etymology. – The specifi c name comes from Latin bisulcus = forked, in reference to the shape of the distal end of embolus. MATERIALS AND METHODS Description. – Holotype male. Body orange. Total length Specimens were examined using a Leica M250 C 1.14. Carapace 0.50 long, 0.40 wide; Carapace 0.32 high. stereomicroscope. Further details were studied under an Abdomen 0.72 wide, 0.52 long. Clypeus 0.23 high. Sternum Olympus BX51 compound microscope. All drawings were 0.32 long, 0.30 wide. Carapace diamond-shaped, highest made using a drawing apparatus attached to the compound anteriorly at the eye group, slightly sloping backwards and microscope. Male palpi and female genitalia were examined sharply down forwards, with fi nely reticulate modifi cation. and illustrated after dissection. Vulvae of females were Six eyes in one group, with black ring, and a blunt, short removed and treated in lactic acid before illustration. process behind them. Ocular and cephalic areas bear hairs. Male palpi and female vulva were illustrated after being ALE>PLE>PME. Posterior eyes row recurved. Cheliceral embedded in Hoyer’s Solution and illuminated with incident promargin with a large tooth and lamina, frontal-middle light against a white background. All type specimens are with a condyle, another in inside base, fang short and preserved in 80% ethanol solution and deposited in the strong, basal boss large. Sternum with reticular ornaments, Institute of Zoology, Chinese Academy of Sciences in marginally rugose. Femora, tibiae, metatarsi and tarsi Beijing (IZCAS). Type specimen photos of the species with obviously modifi ed granula and serrate hairs. Tibia included in this paper can be viewed from website “Endemic bears three trichobothria, and one on metatarsus. Leg Spiders in China” which was created and maintained by measurements: I 1.23 (0.42, 0.08, 0.31, 0.20, 0.22); II 1.09 Shu-Qiang Li and Xin-Ping Wang (Li & Wang, 2009). (0.36, 0.08, 0.26, 0.19, 0.20); III 0.96 (0.30, 0.07, 0.21, 0.19, 0.19); IV 1.33 (0.41, 0.11, 0.34, 0.24, 0.23). Leg formula: All measurements were made under an Olympus BX51 4 1 2 3. Abdominal dorsal scutum long, oval, with smooth compound microscope and given in millimeters. Leg

324 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 1. Lehtinenia bisulcus new species: A. Male left palp, retrolateral view; B. Male left palp, prolateral view. Scale bars: 0.1 mm.

325 Lin & Li: Cave spiders from Vietnam

Fig. 2. Lehtinenia bisulcus new species: A. Female epiginal area and cleared vulva, ventral view; B. Female carapace, dorsal view; C. Ditto, lateral view; D. Female abdomen, ventral view; E. Male carapace and right palp, lateral view; F. Male chelicerae, frontal view. Scale bars: 0.1 mm.

326 THE RAFFLES BULLETIN OF ZOOLOGY 2009 surface. Lateral scutum I long, reaching the posterior margin Etymology. – The specific name comes from Latin of pulmonary plate. One pair of perigenital plates. bulbiformis = globose, in reference to the shape of male Male palpal bulbus proximally swollen, pear-shaped, palpal bulb. distally continued by a narrow extension; embolus relatively wide, strongly sclerotized, with distal end forming an Description. – Holotype male. Total length 1.12. Carapace asymmetric furcation; tibia longer than femur, swollen, 0.49 long, 0.41 wide; abdomen 0.57 long, 0.44 wide; nearly two times larger than femur, with one dorsal clypeus 0.09 high; sternum 0.30 long, 0.30 wide. Carapace trichobothrium on distal tibia (Fig. 1 A, B). pear-shaped, smooth, pale yellow, with modifi ed pigmental spots on thoracic margins. Ocular area dark. Six eye in Female. Color as in male. Total length 1.24. Carapace 0.54 a group, with black rings, anterior eyes row straight, long, 0.42 wide. Carapace 0.27 high. Abdomen 0.82 long, PLE>ALE=AME. Chelicerae pale yellow, with broad 0.63 long. Clypeus 0.12 high. Sternum 0.31 long, 0.31 lamina, six promarginal and two retromarginal teeth. wide. Carapace and sternum reticular ornaments same as in Chelicerae laterally slightly excavated, modifi ed with veins. male. Ocular area unmodifi ed. Six eyes in one group, eyes Sternum pale yellow, smooth, without markings. Legs smaller than corresponding eyes of male. ALE>PLE>PME. measurements: I 1.98 (0.63, 0.13, 0.60, 0.36, 0.26); II 1.76 Cheliceral surface without modified process. Legs with (0.54, 0.12, 0.51, 0.34, 0.25); III 1.46 (0.45, 0.12, 0.37, 0.32, granules. Ttrichobothria on legs same as in male. Leg 0.20); IV 2.11 (0.62, 0.14, 0.58, 0.47, 0.30). Leg formula: measurements: I 1.19 (0.40, 0.08, 0.29, 0.20, 0.22); II 1.11 4 1 2 3. Palp measurements: 0.71 (0.22, 0.10, 0.18, 0.21), (0.37, 0.08, 0.26, 0.19, 0.21); III 0.98 (0.30, 0.07, 0.21, 0.20, bulb 0.14 long, 0.18 wide. Abdomen pale, ovoid. Booklung 0.20); IV 1.37 (0.42, 0.13, 0.34, 0.24, 0.24). Leg formula: 4 invisible. One spiracle located ventrally at one third position 1 2 3. Preanal plate larger than that of male, with a pair of to spinnerets. sclerotized fl akes on the posterolateral corners. Postgenital plate subequal to preanal plate in width, postgenital plate Palpal femur narrower and longer than tibia and tarsus; scale-shaped. tibia slightly swollen, shorter than tarsus, with three dorsal trichobothria. Tarsus obtuse. Bulb compressed, globose, Epiginal pit transversely crescent, with vulval stem with a small hooked appendage (Fig. 3 A-C). connected via a pair of long, laterally extending, strongly sclerotized horns; lateral horns with procurved distal tip Female. Total length 1.14. Carapace 0.53 long, 0.43 wide; connected to the spermathecae; center process with length abdomen 0.64 long, 0.43 wide. clypeus 0.07 high; sternum subequal to the inner vulval plate, rugose membrane; inner 0.32 long, 0.32 wide. Pattern of carapace same as in male. vulval plate weakly sclerotized, with a broad base. Epiginal Sternum with modifi ed pigmental markins. Chelicerae as fold distinct, almost reaching the margin of epiginal shield in male. Leg measurements: I 1.76 (0.52, 0.14, 0.50, 0.37, (Fig. 2 A). 0.23); II 1.64 (0.50, 0.14, 0.46, 0.33, 0.21); III 1.36 (0.44, 0.12, 0.31, 0.29, 0.20); IV 1.90 (0.55, 0.15, 0.54, 0.40, 0.26). Distribution. – Known only from the type locality (Fig. Leg formula: 4 1 2 3. Palp measurements: 0.54 (0.18, 0.09, 13). 0.13, 0.14).

Vulval structure simple, a pair of asymmetrical spermathecae Ochyroceratidae Fage 1912 connected with “L”-shaped copulatory ducts, copulatory opening widely spaced with spermathecae, locating at Speocera Berland 1914 bilateral genital area, chitinous ducts relatively short, converged on the median line (Fig. 4 E). Speocera bulbiformis new species (Figs. 3A−C, 4A−E) Distribution. – Known only from the type locality (Fig. 13). Material examined. – Holotype – Male (IZCAS), Palace Cave (Dong Thien Cung) (20°18'N, 105°40'E; Alt: 256 m), Cuc Phuong National Park, Vietnam, coll. S. Li, 21 July 2008. Telemidae Fage 1913 Paratypes – 4 males and 10 females (IZCAS), same data as Telema Simon 1882 holotype.

Diagnosis. – The new species is similar to S. transleuser Telema cucphongensis new species from Sumatra (Deeleman-Reinhold, 1995), but can be (Figs. 5A−E, 6A−I) distinguished by the spiral course of ejaculatory duct in Material examined. – Holotype - Male (IZCAS), Prehistoric Man bulb, the detailed structure of apical appendage on bulb, Cave (20°18'N, 105°40'E; Alt: 256 m), Cuc Phuong National Park, the absence of modifi ed process on cheliceral surface and Vietnam, coll. S. Li, 19 July 2008. the asymmetrical “L” shape of paired chitinous ducts that connected to the spermathecae. Paratypes – 19 males and 28 females (IZCAS), same data as holotype.

327 Lin & Li: Cave spiders from Vietnam

Fig. 3. Speocera bulbiformis new species: A. Male left palp, prolateral view; B. Ditto, retrolateral view; C. Ditto, ventral view. Scale bars: 0.1 mm.

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Diagnosis. – The new species is similar to T. oculata (Tong 0.30 wide; abdomen 0.82 long, 0.68 wide. Carapace, legs, & Li, 2008), but can be distinguished by the large and labium, endites and chelicerae brown-yellow. Sternum elliptical palpal bulb (male unknown in T. oculata), the dark. Carapace pear-shaped, with a pair of setae on clypeus presence of four plumose setae at distal palpal tarsus, the behind eyes, with a large dark spot at middle thoracic area, annular and sclerotized pedicel in male, the short, distally margin dark and middle light brown, with distinctly radial swollen spermatheca in female. Both sexes of this new stripes. Ocular area dark. Six eyes with black rings, anterior species have the modifi ed pattern on carapace and purple- eye row nearly straight, separated from each by about ½ blue abdomen. of AME diameter, lateral eyes contiguous. Chelicerae with a pigmental strip in the frontal midline area. Promargin Etymology. – The specifi c epithet derives from the name of fang furrow with two large teeth, three small granular of the type locality. teeth and eleven plumose hairs, retromargin with four barely visible denticles. Legs with a dorsal spine at the Description. – Holotype male. Total length 1.32. Carapace distal patella and middle tibia. Leg measurements: I 3.14 0.50 long, 0.48 wide; clypeus 0.14 high; sternum 0.30 long, (0.94, 0.18, 0.92, 0.60, 0.50); II 2.60 (0.82, 0.16, 0.74, 0.50,

Fig. 4. Speocera bulbiformis new species: A. Male carapace, dorsal view; B. Female abdomen, ventral view; C. Ditto, lateral view; D. Male chelicerae, frontal view; E. Female vulva, dorsal view. Scale bars: 0.1 mm for A-D; 0.05 mm for E.

329 Lin & Li: Cave spiders from Vietnam

Fig. 5. Telema cucphongensis new species: A. Male left palp, prolateral view; B. Ditto, retrolateral view; C. Ditto (treated in lactic acid), retrolateral view; D. Male palpal bulb, apical view. Scale bars: 0.1 mm.

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Fig. 6. Telema cucphongensis new species: A. Male chelicerae, frontal view; B. Female colulus and spinnerets, ventral view; C. Epiginal area, ventral view; D-F. Cleared spermatheca, anterior (D), posterior (E) and lateral view (F); G-I. Male abdominal pedicel, anterior (G), dorsal (H) and lateral view (I). Scale bars: 0.1 mm.

331 Lin & Li: Cave spiders from Vietnam

0.42); III 1.95 (0.60, 0.15, 0.52, 0.36, 0.32); IV 2.58 (0.82, fovea. Reduced six eyes remaining in white eyespots, almost 0.16, 0.72, 0.50, 0.38). Leg formula: I-II-IV-III. Abdominal same size, anterior eye row slightly recurved, separated dorsum blue, venter darkish. Pedicel with a trianglular and a from each other by about 1.5 times their diameter, lateral rhombic anterodorsal sclerotized plates. Colulus pentagonal eyes contiguous. Cheliceral fang furrow with three large and dark. Spinnerets pale. teeth, three barely visible granulous denticles and eleven plumose hairs on promargin, three barely visible denticles Palp with a prolateral cymbial apophysis and a trichobothrium on retromargin. Legs with a dorsal spine at distal patella, 1 near distal /3 position of tibia. Femur, patella, tibia and three row of short spines on prolateral femur I. Tibia I-IV tarsus modifi ed by pigmental speckles. Distal tarsus with bear spines. Leg measurements: I 2.76 (0.85, 0.11, 0.86, three prolateral plumose spines. Palpal bulb oval, apex with 0.59, 0.35); II 2.33 (0.73, 0.11, 0.70, 0.48, 0.31); III 1.70 one broad embolus. The course of bulbous inner ejaculatory (0.56, 0.09, 0.49, 0.32, 0.24); IV 2.08 (0.70, 0.10, 0.61, duct relatively complex (Fig. 5 A-D). 0.41, 0.26). Leg formula: I-II-IV-III. Abdomen pale yellow, almost globose, with sparse long hairs. Colulus pale and Female. Total length 1.22. Carapace 0.52 long, 0.48 wide; pentagonal, spinnerets pale, the anterior largest, the middle clypeus 0.14 high; sternum 0.32 long, 0.30 wide; abdomen smallest. 0.78 long, 0.66 wide. Coloration and modifi ed pattern of body and legs same as in male. Leg measurements: I 2.82 Palp with a prolateral cymbial apophysis, elliptic bulb with (0.86, 0.16, 0.82, 0.52, 0.46); II 2.51 (0.80, 0.15, 0.72, 0.48, a simple trigonal embolus that basally broad and distally 0.36); III 1.94 (0.58, 0.14, 0.58, 0.34, 0.30); IV.2.46 (0.76, bent (Fig. 7 A-C). 0.16, 0.68, 0.46, 0.40). Leg formula: I-II-IV-III. Female. Total length 1.56. Carapace 0.66 long, 0.58 wide; Genital area with one row of hairs, postmargin recurved. clypeus 0.16 high; sternum 0.38 long, 0.34 wide; abdomen Vulval structure simple, spermatheca basally narrowed and 1.04 long, 0.94 wide. Eyes and chelicerae as in male. Leg distally swollen (Fig. 6 C-F). measurements: I 2.66 (0.82, 0.11, 0.83, 0.55, 0.35); II 2.23 (0.70, 0.10, 0.68, 0.45, 0.30); III 1.67 (0.54, 0.09, 0.49, 0.31, Distribution. – Known only from the type locality (Fig. 0.24); IV 2.07 (0.69, 0.10, 0.61, 0.41, 0.26). Leg formula: 13). I-II-IV-III.

Telema exiloculata new species Genital area covered with long hairs on genital plate. A (Figs. 7A−F, 8A−G) row of short spines present posterior epigastric furrow. Posterior margin of genital area straight, bilaterally slightly Material examined. – Holotype - Male (IZCAS), Trung Trang sclerotized. Spermatheca relatively large, with distinct Cave (20°48'N, 106°59'E; Alt: 256 m), Cat Ba National Park, shape, distorted two times medially, swollen distally, Vietnam, coll. S. Li, G. Zheng & D.S. Pham, 16 July 2008. attaching to a distal-lateral vesicle (Fig. 8 C-G). Paratypes – 15 males and 43 females (IZCAS), same data as Distribution. – Known only from the type locality (Fig. holotype. 13). Diagnosis. – The new species resembles to T. spina from China (Tong & Li, 2008) in having the similar palp, but can be distinguished by the underdeveloped eyespot, the lack of Symphytognathidae Hickman 1931 modifi ed pigmentation in both sexes, the small and elliptic palpal bulb, the presence of seven plumose setae at distal Patu Marples 1951 palpal tarsus in male, the asymmetrical, distally swollen and basally narrowed spermatheca (female unknown in T. Patu bispina new species spina). T. exiloculata is similar to T. cucphongensis in the (Figs. 9A−E, 10A−F and 11A−F) body size and the shape of palp, but different by the reduced Material examined. – Holotype - Male (IZCAS), Mat Cave eyespot, the narrower embolus, the longer and asymmetrical (20°21´N, 105°42´E; Alt: 18 m), Cuc Phuong National Park, spermatheca. Vietnam, coll. S. Li, 22 July 2008.

Etymology. – The specifi c name is from Latin exil- = tiny, Paratypes – 13 males and 20 females (IZCAS), same data as small and oculata = ocular, in reference to the vestigial holotype. eyespots on carapace of both sexes. Diagnosis. – This new species is similar to Patu silho from Description. – Holotype male. Total length 1.30. Carapace Seychelles (Saaristo, 1996) and Patu vitiensis from Fiji 0.60 long, 0.54 wide; clypeus 0.16 high; sternum 0.38 long, (Marples, 1951), but can be distinguished by the presence of 0.34 wide; abdomen 0.76 long, 0.66 wide. Carapace, legs, two large spurs on distal-ventral tibia II in male, the absence sternum, labium, endites and chelicerae yellow. Abdomen of a posterior protuberance on the globular abdomen, the pale yellow. Carapace smooth, without unmodifi ed pattern, modifi ed spines and different shapes of palpal cymbium, the with paired of setae at clypeus, behind eyes and at thoracic short and robust of embolus, the coiled copulatory ducts,

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Fig. 7. Telema exiloculata new species: A. Male left palp, prolateral view; B. Ditto, retrolateral view; C. Ditto (treated in lactic acid), retrolateral view; D. Male carapace, dorsal view; E. Male abdominal pedicel, dorsal view; F. Ditto, lateral view. Scale bars: 0.1 mm.view; C-F. Male leg I-IV, prolateral view. Scale bars: 0.05 mm for A, B; 0.2 mm for C-F.

333 Lin & Li: Cave spiders from Vietnam

Fig. 8. Telema exiloculata new species: A. Male chelicerae, frontal view; B. Female colulus and spinnerets, ventral view; C. Female epiginal area, ventral view; D-G. Cleared spermatheca, ventral (D), anterior (E); posterior (F) and lateral view (G). Scale bars: 0.1 mm.

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Fig. 9. Patu bispina new species: A. Male left palp, prolateral view; B. Palpal bulb, prolateral view; C. Palpal cymbium, dorsal view; D. Male body, dorsal view; E. Ditto, lateral view. Scale bars: 0.05 mm for A-C; 0.1 mm for D, E.view; C-F. Male leg I-IV, prolateral view. Scale bars: 0.05 mm for A, B; 0.2 mm for C-F.

335 Lin & Li: Cave spiders from Vietnam

Fig. 10. Patu bispina new species: A. Male left palp, retrolateral view; B. Palpal bulb, retrolateral view; C-F. Male leg I-IV, prolateral view. Scale bars: 0.05 mm for A, B; 0.2 mm for C-F.

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Fig. 11. Patu bispina new species: A. Female epigine, ventral view; B. Cleared vulva, ventral view; C. Ditto, dorsal view; D. Female body, dorsal view; E. Ditto, lateral view; F. Male chelicerae, frontal view. Scale bars: 0.05 mm for A, B, C and F; 0.1 mm for D and E.

337 Lin & Li: Cave spiders from Vietnam the presence of a ventral plate, and the epigine with a wide Epigine surface smooth, bears three pairs of long hairs, lobe on posterior margin. with a broad, short lobe. Vulva complex. Fertilization ducts straight, short and thin, spermathecae widely spaced, Etymology. – The specific epithet of the new species globose, strongly sclerotized. Copulatory ducts long, derives from Latin bi- = two, spina = spine, in reference coiled, with broad distal ends. Ventral plate rhombic, to the presence of two strong spines on ventrally tibia II smooth, membranous, covered partially fertilization ducts of male. and end of copulatory ducts (Fig. 11 A-C).

Description. – Holotype male. Total length 0.67. Carapace Distribution. – Known only from the type locality (Fig. 0.30 long, 0.30 wide, 0.21 high. Sternum 0.22 long, 0.23 13). wide. Abdomen 0.44 long, 0.44 wide, 0.55 high. body pale yellow, without markings. Carapace bears two setae at the ocular area and thoracic area separately, with smooth Anapistula Gertsch 1941 margin. Six eyes in three diads; ALE diameter subequal to PLE’s, smaller than PME’s. Posterior eye row slightly Anapistula orbisterna new species recurved. Ocular area distinctly elevated. Clypeus width (Figs. 12A−F) equal to three times ALE diameter. Chelicerae slender, fused at midline pars, shorter than endites, promargin with Holotype. – Female (IZCAS), Mat Cave (20°21'N, 105°42'E; a pair of adnate teeth. Labium wider than long (length/ Alt: 18 m), Cuc Phuong National Park, Vietnam, coll. S. Li, 22 width 0.29). Sternum wider than long (length/width 0.96), July 2008. plump, bears tenuous hairs. Legs pale yellow, clothed with setae and bristles. Tibia II bears two strongly ventral spurs Diagnosis. – This new species resembles Anapistula secreta at distal end. Each tibia with three dorsal trichobothria. from Panama (Gertsch, 1941), but can be distinguished Legs measurement: I 1.31 (0.41, 0.12, 0.32, 0.19, 0.27); by the globose spermathecae, the broad median epiginal II 1.09 (0.33, 0.12, 0.25, 0.15, 0.24); III 0.87 (0.25, 0.10, median ducts and the long fertilization ducts. 0.18, 0.13, 0.21); IV 1.01 (0.33, 0.11, 0.23, 0.13, 0.21). Leg formula: I-II-IV-III. Abdomen high (height/length Etymology. – The specifi c name derives from Greek orbi- = 1.25), sparsely covered with long hairs, globular in dorsal orbicular and stern- = sternum, referring to the nearly round view, posterior rear extended beyond spinnerets. Book sternum in female. lung absent. Anterior spinnerets larger than posterior ones, median spinnerets smallest; colulus absent. Description. – Holotype female. Total length 0.66. Carapace 0.28 long, 0.27 wide, 0.21 high. Sternum 0.21 Palp large. Femur, patella and tibia without any process. long, 0.21 wide. Abdomen 0.36 long, 0.32 wide, 0.40 Tibia bears four short spines. Thin sclerotized cymbium high. Carapace pale yellow, fl at, smooth, with paired long with two outspread processes, two long hairs present on hairs at ocular and thoracic areas respectively, without apex of a large process. Palpal bulb large, almost ovate. pigmental pattern. Four eyes in two diads, subequal in Radix haematodocha swollen with rugous membrane. size, ovoid and white. Anterior margin of clypeus without Tegulum nearly rectangular and distinctly sclerotized. short setae. Clypeus width subequal to 2.5 times ALE Embolus long, coiled and strongly sclerotized, intertwisted diameter. Palp absent. Chelicerae yellow, fused at midline with conductor. Proximal conductor and most of embolus pars, each with two sharp adnate teeth. Labium wider embedded in the radix haematodocha. Terminal apophysis than long (length/width 0.45). Sternum length and width large, smooth and sclerotized. Embolus arising from subeuqal (length/width 1.00). Legs clothed with setae and bottom of terminal apophysis (Fig. 9 A-C; 10 A, B). bristles. Each tibia bears a mesial-dorsal spine and three proximal trichobothria. Legs measurement: I 1.10 (0.34, Female. Total length 0.75. Carapace 0.32 long, 0.31 wide, 0.12, 0.24, 0.14, 0.26); II 1.02 (0.32, 0.12, 0.22, 0.14, 0.22); 0.16 high. Sternum 0.23 long, 0.24 wide. Abdomen 0.45 III 0.79 (0.24, 0.10, 0.14, 0.11, 0.20); IV 0.95 (0.29, 0.11, long, 0.46 wide, 0.58 high. Coloration and modifi cation 0.19, 0.12, 0.24). Leg formula: I-II-IV-III. Abdomen pale, of body and legs same as in male. Palp absent. Ocular covered with long hairs, globular, slightly longer than wide area upheaved. Posterior median eye smaller than in male. (length/width 1.13), relatively high (height/length 1.11), Posterior eyes row straight. Clypeus lower than in male. and posterior rear expanded beyond spinnerets. Anterior Legs measurement: I 1.24 (0.39, 0.12, 0.31, 0.17, 0.25); spinnerets slightly larger than posterior ones; median II 1.05 (0.33, 0.12, 0.23, 0.14, 0.23); III 0.90 (0.26, 0.10, spinnerets smallest; colulus absent. Book lung absent. Two 0.19, 0.13, 0.22); IV 1.01 (0.32, 0.11, 0.22, 0.13, 0.23). pairs of spiracles. Leg formula: I-II-IV-III. Abdomen covered with long hairs, globular, slightly longer than wide (length/width Epigine relatively small, unsclerotized, surface smooth, bears 0.98), very high (height/length 1.29) and posterior rear sparse long hairs. Vulva relatively simple. Spermathecae extending beyond spinnerets. Book lung absent. A pair of widely spaced, globose, distinctly sclerotized. Fertilization spiracles near epiginal furrow. Colulus absent. ducts long, thin, derived from ventral spermathecae. Epiginal median ducts wide, with broad base and cupped

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Fig. 12. Anapistula orbisterna new species: A. Female body, dorsal view; B. Sternum, coax, labium and maxillae, ventral view; C. Female chelicerae, frontal view; D. Epigine, ventral view; E. Cleared vulva, dorsal view; F. Cleared vulva and tracheal system, ventral view. Scale bars: 0.1 mm for A and B; 0.05 mm for C, D and F; 0.025 mm for E.

339 Lin & Li: Cave spiders from Vietnam top. Bilateral branches short, directly connected to the Bourne, J. D., 1981. Two new armoured spiders of the genus spermathecae. Ventral plate absent (Fig. 12 D-F). Paculla Simon, 1887 from Sarawak (Araneae: Pacullidae). Bulletin of the British Arachnological Society, 5: 217-220. Male. Unknown. Brignoli, P. M., 1972a. Some cavernicolous spiders from Mexico (Araneae), in “Subterranean fauna of Mexico, Part I”. Distribution. – Known only from the type locality (Fig. Quaderna Accademia Nazionale dei Lincei, 171: 129–155. 13). Brignoli, P. M., 1972b. Spinnen aus Nepal, I. Paculla martensi n. sp. (Arachnida: Araneae: Pacullidae). Senckenbergiana biologica, 53: 95-100. ACKNOWLEDGEMENTS Brignoli, P. M., 1973. Ragni della Melanesia, I. Un nuovo Tetrablemma di Guadalcanal (Isole Salomone) (Araneae The manuscript benefited greatly from comments by Tetrablemmidae). Memorie della Societa Entomologica Xinping Wang (University of Florida, USA) and Yanfeng Italiana, 52: 79-88. Tong (Shenyang Normal University, China). The field Brignoli, P. M., 1974. Tetrablemmidae (Araneae) dell’Angola e work was kindly supported by Le Xuan Canh, Vu Xuan della Zaire. Publicações culturais da Companhia de Diamantes Manh (Vietnamese Academy of Science and Technology, de Angola, 88: 177-196. Vietnam), and Luu van Hien (Cuc Phuong National Park). Brignoli, P. M., 1975. Über die Gruppe der Haplogynae (Araneae). This study was supported by the National Natural Sciences Proceedings of the 6th International Arachnology. Congress, Foundation of China (NSFC-30499341/30670239/30870 33-38. 271/30770268/30870473), by the National Science Fund Brignoli, P. M., 1976. On some recent papers about Indian spiders. for Fostering Talents in Basic Research (Special Subjects Bulletin of the British Arachnological Society, 3: 211-213. in Taxonomy, NSFC-J0630964/J0109), by the Brignoli, P. M., 1977. Two new spiders from Sumatra (Araneae, Knowledge Innovation Program of the Chinese Academy Telemidae and Ochyroceratidae). Zoologische Mededelingen of Sciences (KSCX2-YW-Z-008/KSCX3-IOZ-0811), by Leiden, 50: 221-229. the Ministry of Science and Technology of the People’s Brignoli, P. M., 1978a. Contributions à l’étude de la faune terrestre Republic of China (MOST grant no. 2006FY120100/ des îles granitiques de l’archipel des Séchelles (Mission 2006FY110500), and partly also by the Beijing Natural P.L.G. Benoit - J.J. Van Mol 1972). Araneae Tetrablemmidae. Science Foundation (5082013). Revue de Zoologie Africaine, 92: 431-435. Brignoli, P. M., 1978b. Spinnen aus Brasilien IV. Zwei neue blinde Bodenspinnen aus Amazonien (Arachnida, Araneae). Beiträge naturkundliche Forschungen Südwest-Deutschlands, LITERATURE CITED 37: 143-147. Brignoli, P. M., 1978c. A few notes on a remarkable South Baert, L. & R. Jocqué, 1993. Anapistula caecula n. sp., the smallest African troglobitic spider, Cangoderces lewisi Harington, known female spider (Araneae, Symphytognathidae). Journal 1951 (Araneae: Telemidae). Revue Suisse de zoologie, 85: of African Zoology, 107: 187-189. 111-114. Baptista, R. L. C., 2003. Speocera eleonorae sp. n., the first Brignoli, P. M., 1980. Ricerche nell’Asia sudorientale dell’Istituto troglomorphic spider from Brazilian caves (Araneae: di Zoologia de L’Aquila. I. Due nuovi ragni di Celebes Ochyroceratidae). Revista Ibérica de Aracnolofía, 7: 221- (Araneae: Pacullidae, Mimetidae). Bollettino della Societa 224. Entomologica Italiana, 112: 162-166. Bourne, J. D., 1980. New armored spiders of the family Burger, M., 2005. The spider genus Indicoblemma Bourne, with Tetrablemmidae from New Ireland and northern India description of a new species (Araneae: Tetrablemmidae). (Araneae). Revue suisse de Zoologie, 87: 301-317. Bulletin of the British Arachnological Society, 13: 97-111. Deeleman-Reinhold, C. L., 1980. Contribution to the knowledge of the southeast Asian spiders of the families Pacullidae and Tetrablemmidae. Zoologische Mededelingen Leiden, 56: 65-82. Deeleman-Reinhold, C. L., 1993. A remarkable troglobitic tetrablemmid spider from a cave in Thailand (Arachnida: Araneae: Tetrablemmidae). Natural Historial Bulletin of the Siam Society, 41: 99-103. Deeleman-Reinhold, C. L., 1995. The Ochyroceratidae of the Indo-Pacifi c region (Araneae). The Raffl es Bulletin of Zoology, (suppl), 2: 1-103. Dumitrescu, M. & M. Georgescu, 1992. Ochyroceratides de Cuba (Araneae). Mémoires de Biospéologie, 19:143-153. Fage, L. 1912. Etudes sur les Araignées cavernicoles. I. Revision des Ochyroceratidae (n. fam.). Biospelogica, XXV, Archives de Zoologie Expérimentale et Generale, 10(5): 97–162.

Fig. 13. Locality records of cave spiders in Vietnam.

340 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fage L. 1913. Etudes sur les Araignées cavernicoles. II. Revision Pham, D. S, X. Xu & S. Q. Li, 2007. A preliminary note on spider des Leptonetidae. Biospelogica, XXIX, Archives de Zoologie fauna of Vietnam (Arachnida: Araneae). Acta Arachnologica Expérimentale et Generale, 10(5): 479-576. Sinica, 16(2): 121-128. Forster, R. R., 1958. Spiders of the family Symphytognathidae Platnick, N. I., 2009. The world spider catalog, version 9.5. from North and South America. American Museum Novitates, American Museum of Natural History, online at http:// 1885: 1-14. research.amnh.org/entomology/spiders/catalog/index.html Forster, R. R. & N. I. Platnick, 1977. A review of the spider (accessed: 28 January, 2009). family Symphytognathidae (Arachnida, Araneae). American Saaristo, M. I., 1996. Symphytognathidae (Arachnida, Araneae), Museum Novitates, 2619: 1-29. a new spider family for the granitic islands of Seychelles. Gertsch, W. J., 1941. Report on some from Barro Phelsuma, 4: 53-56. Colorado Island, Canal Zone. American Museum Novitates, Saaristo, M. I., 1998. Ochyroceratid spiders of the granitic 1146: 1-14. islands of Seychelles (Araneae, Ochyroceratidae). Phelsuma, Gertsch, W. J., 1973. A report on cave spiders from Mexico and 6: 20-26. Central America. Bulletin of Association for Mexican Cave Schwendinger, P. J., 1989. On three new armoured spiders Studies, 5: 141-163. (Araneae: Tetrablemmidae, Pacullinae) from Indonesia and Grismado, C. J. and M. J. Ramírez, 2004. A new species of Thailand. Revue suisse de Zoologie, 96: 571-582. the genus Storenomorpha Simon from Vietnam (Araneae: Schwendinger, P. J., 1994. Four new Perania (Araneae: Zodariidae). Zootaxa, 453: 1-7. Tetrablemmidae, Pacullinae) from Thailand and Malaysia. Harington, J. S., 1951. A new leptonetid spider, Cangoderces Revue suisse de Zoologie, 101: 447-464. lewisi, n. gen., n. sp., from the Cango Caves, Oudtshoorn. Shear, W. A., 1978. Taxomomic notes on the armored spiders Annals of the Natal Museum, 12: 81-90. of the families Tetrablemmidae and Pacullidae. American Harvey, M. S., 1998. A review of the Australasian species of Museum Novitates, 2650: 1-46. Anapistula Gertsch (Araneae: Symphytognathidae). Records Shear, W. A., 1979. Pahanga, a new tetrablemmid spider genus of the Western Australian Museum, 19: 111-120. from Malaysia (Araneae, Tetrablemmidae). Bulletin of the Hickman, V. V., 1931. A new family of spiders. Proceedings of British Arachnological Society, 4: 294-295. the Zoological Society of London (B), 1931: 1321-1328. Simon, E., 1886. Arachnides recuellis par M. A. Pavie (sous chef Hiramatsu, T. & A. Shinkai, 1993. Web structure and web- du service des postes au Cambodge) dans le royaume de Siam, building behavior of Patu sp. (Araneae: Symphytognathidae). au Cambodge et en Cochinchine. Actes de la Société linnéenne Acta Arachnologica, 42: 181-185. de Bordeaux, 40: 137-166. Hogg, H. R., 1922. Some spiders from south Annam. Proceeding Simon, E., 1903. Etudes arachnologiques 33e Mémoire. of the Zoological Society of London, 285-312. LIII. Arachnides recueillis à Phuc-Son (Annam) par M. H. Fruhstorfer (nov-dec. 1899). Annales de la Societe Jäger, P., 2003. Rhitymna Simon 1897: an Asian, not an African Entomologica des France, 71: 725-736. spider genus. Generic limits and descriptions of new species (Arachnida, Araneae, Sparassidae). Senckenbergiana Simon, E., 1904. Arachnides recueillis par M. A. Pavie en biologica, 82: 99-125. Indochine. In Mission Pavie en Indochine 1879-1895. III. Recherches sur l’histoire naturells de l’Indochine Orientale. Jäger, P. & V. Vedel, 2005. Pseudopoda fi ssa sp. nov. – fi rst Paris, Pp. 270-295. recode of the genus from Vietnam (Araneae, Sparassidae). Zootaxa, 837: 1-5. Simon, E., 1909. Etude sur les arachnides du Tonkin (lre partie). Bulletin Scientifique de la France et de la Belgique, 42: Lehtinen, P. T., 1981. Spiders of the Oriental-Australian region. 69-147. III . Tetrablemmidae, with a world revision. Acta Zoologica Fennica, 162: 1-151. Song, D. & M. Zhu, 1994. On some species of cave arachnids of China. In: Du X. H. (ed.), Collected Papers on Zoology in Li, S. & X. Wang 2009. Endemic spiders in China. Online at Celebration of the Sixtieth Anniversary of the Founding of the http://www.ChineseSpecies.com & http://www.amaurobiidae. Zoological Society of China and in Honor of the Centenary com/araneae/ (accessed: 7 March, 2009). of the Birth of Professor Zhen Chen. Zoological Society of Lin, Y. & S. Li, 2008. A new species of the family Telemidae China, Beijing, pp. 35-46. (Arachnida, Araneae) from Xishuangbanna rainforest, China. Tong, Y. & S. Li, 2006. Symphytognathidae (Araneae), a spider Acta Zootaxonomica Sinica, 33: 650-653. family newly recorded from China. Zootaxa, 1259: 33-38. Marples, B. J., 1951. Pacifi c symphytognathid spiders. Pacifi c Tong, Y. & S. Li, 2007. First records of the family Ochyroceratidae Science, 5: 47-51. (Arachnida: Araneae) from China, with descriptions of a new O. Pickard-Cambridge., 1873. On some new genera and species genus and eight new species. The Raffl es Bulletin of Zoology, of Araneida. Procceeding of the Zoological Society of London, 55: 63-76. 1873: 112-129. Tong Y. & S. Li, 2008a. Tetrablemmidae (Araneae), a new Ono, H., 1996. A list of spider families of Japan. In Ishii, M., record family from China. Organisms Diversity & Evolution, T. Ohtani & Y. Johki (eds.): The Encyclopaedia of 8: 84-98. of Japan, 8 (Insects I): 25-27. Heibonsha, Tokyo. (In Tong Y. & S. Li, 2008b. Four new cave-dwelling Telema Japanese.) spiders (Araneae, telemidae) from Guizhou Province, China. Ono, H., 2002. First record of the genus Anapistula (Araneae, Zoosystema, 30(2), 1-10. Symphytognathidae) from Asia. Bulletin of tne National Tong, Y. & S. Li, 2008c. The spiders of the genus Telema Science Museum: Tokyo (A), 28: 61-64. (Araneae: Telemidae) from Hainan Island, China. The Raffl es Bulletin of Zoology, 56(1): 59-66.

341 Lin & Li: Cave spiders from Vietnam

Tu, L. & S. Li, 2004. A preliminary study of erigonine spiders Wunderlich, J., 1995. Beschreibung bisher unbekannter (Linyphiidae: Erigoninae) from Vietnam. The Raffl es Bulletin Spinnenarten und -Gattungen aus Malaysia und Indonesien of Zoology, 52: 419-433. (Arachnida: Araneae: Oonopidae, Tetrablemmidae, Tu, L. & S. Li, 2006. Three new and four newly recorded Telemidae, Pholcidae, Linyphiidae, Nesticidae, Theridiidae species of Linyphiinae and Micronetinae spiders (Araneae: und Dictynidae). Beiträge zur Araneologie. 4: 559-579. Linyphiidae) from Northern Vietnam. The Raffl es Bulletin of Zabka, M., 1985. Systematic and zoogeographic study on the Zoology, 54: 117-131. family Salticidae (Araneae) from Vietnam. Annales Zoologici, Wang, X. & J. Ran, 1998. A new cave spider of the genus Telema Warszawa, 39: 197-485 (Araneae: Telemidae) from China. Acta Zoologica Taiwanica, Zhu, M. & H. Chen, 2002. A new cave spider of the genus Telema 9: 93-96. from China (Araneae: Telemidae). Acta Zootaxonomica Sinica, 27: 82-84.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 343–452 Date of Publication: 31 Aug.2009 © National University of Singapore

RADIATION OF ENDEMIC SPECIES FLOCKS IN ANCIENT LAKES: SYSTEMATIC REVISION OF THE FRESHWATER SHRIMP H. MILNE EDWARDS, 1837 (CRUSTACEA: DECAPODA: ) FROM THE ANCIENT LAKES OF SULAWESI, INDONESIA, WITH THE DESCRIPTION OF EIGHT NEW SPECIES

Kristina von Rintelen Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung an der Humboldt-Universität zu Berlin, Invalidenstrasse 43, D- 10115 Berlin, Germany Email: [email protected] (Corresponding author)

Yixiong Cai National Biodiversity Centre, National Parks Board, 1 Cluny Road, Singapore 259569, Republic of Singapore Email: [email protected]

ABSTRACT. – The ancient lakes of the Indonesian island Sulawesi harbour two endemic species fl ocks of the freshwater shrimp genus Caridina (Crustacea: Decapoda: Atyidae). One of them forms the largest radiation within the genus. Species from both lake systems evolved under similar extrinsic conditions and show some parallel patterns, e.g. the development of unusual and fl amboyant colour patterns. After extensive sampling and fi eld observations over several years, we here present the fi rst comprehensive revision of all ancient lakes species from both lake systems. We describe eight new and synonymize one previously described species. Besides standard morphology-based species descriptions of alcohol preserved material, we also provide ecological and behavioural data as well as colour patterns of living animals whenever available. We further use a molecular phylogeny, based on the mitochondrial genes 16S and COI, to support our morphology-based species descriptions. The revision reveals that the total number of species (21) is almost twice as high as previously described. However, there is a considerably lower number of species in Lake Poso than in the Malili lakes, which might be explained by an age difference between the two species fl ocks or the less pronounced geographical structure of Lake Poso. The molecular phylogeny further suggests the existence of several cryptic species. Last but not least, we hint at conservation priorities, not only for the beautiful shrimps we present in this study, but also for all other organisms endemic to the ancient lakes of Sulawesi that are threatened with extinction by human impact.

KEY WORDS. – Sulawesi, Atyidae, Caridina, radiation, biodiversity, taxonomy.

CONTENTS C. lingkonae ...... 373 C. loehoe ...... 377 Introduction ...... 344 C. mahalona ...... 381 Material and Methods ...... 346 C. masapi ...... 387 Revision of Caridina from the ancient lakes of Sulawesi .... 347 C. parvula, new species ...... 392 Identifi cation keys to species from the ancient lakes of C. profundicola, new species ...... 396 Sulawesi ...... 347 C. spinata ...... 401 Morphological key ...... 347 C. spongicola ...... 405 Key to living animals in the fi eld ...... 352 C. striata, new species ...... 410 Malili lake system ...... 352 C. tenuirostris ...... 415 Lake Poso and its river system ...... 354 C. woltereckae ...... 420 Taxonomy ...... 355 Species from Lake Poso (Indonesia, Central Sulawesi) ...... 424 Species from the Malili lake system Caridina acutirostris ...... 424 (Indonesia, South Sulawesi) ...... 355 C. caerulea, new species ...... 428 Caridina dennerli, new species ...... 355 C. ensifera ...... 432 C. glaubrechti, new species ...... 359 C. longidigita ...... 436 C. holthuisi, new species ...... 364 C. sarasinorum ...... 439 C. lanceolata ...... 369 C. schenkeli, new species ...... 442

343 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Discussion ...... 446 224 µS). However, the concentration of dissolved oxygen is Radiation, ecology, and species diversity of freshwater not maintained with depth (Crowe et al., 2008). shrimps in the ancient lakes of Sulawesi ...... 446 Conservation implications for the ancient lake species of The ancient lakes of Sulawesi are fertile grounds for the Sulawesi ...... 450 adaptive radiation of several and largely endemic species Acknowledgements ...... 450 Literature cited ...... 450 fl ocks of vertebrates and invertebrates (fi shes: e.g. Herder et al., 2006, 2008; snails: e.g. von Rintelen et al., 2004, 2007c; crabs: e.g. Schubart & Ng, 2008; Schubart et al., 2008). INTRODUCTION This paper reports on two endemic species fl ocks of atyid freshwater shrimps (Crustacea, Decapoda, Caridina) that Ancient lakes, with their often highly diverse and speciose represent two of the larger radiations within these lakes. The endemic fauna, are natural laboratories for the study of Malili radiation forms the largest radiation within the genus species and speciation. Recently, two ancient lake systems in Caridina (von Rintelen et al., in review). The majority of the central highlands of the Indonesian island Sulawesi (Fig. the species have evolved as the result of adaptive radiations, 1) have been discovered as promising new model systems: and their ecological adaptations seem to have played a major both are not only older, larger and deeper than other lakes role in speciation (von Rintelen et al. 2007a, in review). on the island, e.g. Lake Lindu in Central Sulawesi or Lake According to these authors, several substrate specialists have Tondano in North Sulawesi, but their biodiversity is also evolved in the two lake systems. In contrast, only a few extraordinarily high due to the spectacular radiations of unspecialized species (generalists) today exist. A number of their inhabitants. the lacustrine species exhibit unusual and fl amboyant colour patterns that are species-specifi c (Zitzler & Cai, 2006; von The Malili lake system and Lake Poso (Fig. 1B–C) are Rintelen et al. 2007a; in review), and likewise might have completely isolated from each other. Age estimates range driven intralacustrine diversifi cation (von Rintelen et al., from more than one million years (Brooks, 1950; Haffner in review). In consequence of the lake radiations, the two et al., 2001) to a maximum of fi ve million years (Robert species fl ocks comprise a high number of largely endemic Hall, pers. comm. 2007). The solitary Lake Poso is drained species: 14 are currently described, four from Lake Poso and by the Poso River towards the north into Tomini Bay (Fig. ten from the Malili lake system (Tables 2-3). 1B). The Malili lake system consists of fi ve connected lakes that are drained by the Larona River (Fig. 1C) towards the The first to mention atyid shrimps from the two lake west into Bone Bay. The northernmost Lake Matano is systems was Schenkel (1902), who described three species connected to Lake Mahalona via Petea River and further to from Lake Poso and its drainage based on a collection by via Tominanga River. The two satellite lakes the Swiss naturalists F. and P. Sarasin (Sarasin & Sarasin, Lontoa [Wawontoa] and Masapi are not directly connected 1905). Schenkel’s species were later mentioned by Bouvier to the three major lakes. Lake Lontoa is indirectly connected (1925), Roux (1904), and Woltereck (1937a, b). The majority to Tominanga River and Lake Masapi to Larona River. of the Malili species were described by Woltereck (1937a, The longitudinal shape of Lake Poso and Lake Matano, the b) based on her father’s collection from 1932 (Woltereck, northernmost lake of the Malili system, may resemble typical 1933a, b). The riverine species Caridina opaensis Roux, graben lakes (compare Haffner et al., 2001 for Lake Matano) 1904, originally described from Southeast Sulawesi, was like Lake Baikal or , but today, they are reported as the only non-endemic shrimp from the Malili generally not regarded as such. Lake Poso (323 km2) has lakes (Woltereck, 1937a, b). Then, for almost 70 years the only one deep basin with a depth of 450 m (Abendanon, state-of-the-art remained unchanged. Brooks (1950) and 1915; Haffner et al., 2001), whereas Lake Matano and Lake Chace (1997) mentioned the species from the lakes, but Towuti each have two deeper basins. With a depth of almost basically referred to Schenkel (1902) and Woltereck (1937a, 600 m, Lake Matano represents the eight deepest lake in the b). Only in 2006, another new species, C. spongicola, was world (the deepest in Southeast Asia). With 203 m in depth, described by Zitzler & Cai from Lake Towuti, the largest Lake Towuti is distinctly shallower, but with 560 km2 more of the Malili lakes. Roy et al (2006) published a small-scale than three times as large as Lake Matano and represents study on C. lanceolata Woltereck, 1937a from the Malili the second largest lake in Indonesia (Giesen, 1994). The lakes. Cai & Wowor (2007) revised the Poso species fl ock depth of the three smaller Malili lakes is approx. 2-4 m and described one new species. Recently, Cai et al. (2009) (Lakes Lontoa and Masapi) and 73 m (Lake Mahalona). described two new species from the Malili lake system and Further, both are ultra-oligotrophic, meaning a high water redescribed four. Based on morphological and genetic data, transparency (approx. 11 m in Lake Poso and more than von Rintelen et al. (2007a, b) suggested a high number of 20 m in L. Towuti and L. Matano) and an extremely low yet undescribed species in both lake systems, which we nutrient and organic content (Giesen et al., 1991; Giesen, here describe. Unfortunately, Woltereck’s type specimens 1994; Haffner et al., 2001). This may play an important role could not be traced (KvR & YC, personal observation) in the regulation of species abundance and diversity (Haffner and have probably been lost during the Second World War et al., 2006). Temperatures in Lakes Matano, Mahalona, as has some of the fi sh type material in the most likely and Towuti vary between 27 and 31°C, a stable thermo- or depository, the Zoologische Staatssammlung München, chemocline is basically missing (isothermal mixing; also Germany, from the ancient lakes (Kottelat 1990a, b). The constant with depth in Lake Matano: pH 7.4 and conductivity collections of the museums in Berlin, Frankfurt, Hamburg,

344 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 1. The ancient lakes of Sulawesi. A. The two ancient lake systems on the Indonesian island Sulawesi. B. Overview of Caridina collecting sites from Lake Poso. C. Overview of Caridina collecting sites from the Malili lake system.

345 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi and Leipzig were checked as well. Cai et al. (2009) also as SEM material (mounted on specimen stubs). Voucher mentioned that Woltereck’s types are no longer extant and specimens are deposited in three museums: all holotypes, half hence designated neotypes for four species they redescribed. of the paratype series, and approximately half of the non-type Following this approach, and to complete the redescription material at the Division of Zoology, Research Center for of all of Woltereck’s species, we here redescribe and Biology, Indonesian Institute of Sciences (formerly Museum designate neotypes for C. lingkonae Woltereck, 1937a and Zoologicum Bogoriense, MZB); approximately half of the C. tenuirostris Woltereck, 1937a that have not been examined paratype series and the remaining material at the Museum für by Cai et al. (2009). Naturkunde Berlin (formerly Zoologisches Museum Berlin, ZMB), and some paratypes at the Zoological Reference Here, we revise all species from both ancient lake systems Collection of the Raffl es Museum for Biodiversity Research, of Sulawesi in order to update and expand the knowledge National University of Singapore, Singapore (ZRC). In of freshwater shrimp biodiversity in these lakes. In addition, addition, we re-examined type specimens from the Natural we provide the first identification keys for the ancient History Museum Basel, Basel, Switzerland, (NHMB). lake species of Sulawesi, which are separated into one standard morphological key and two keys for the quick pre- Digital photographs of the majority of living species from the identifi cation of living specimens from each lake system. With ancient lakes where taken in a small fi sh tank directly after the combination of morphological and molecular data, we capture. The description of colour patterns is based on fi eld further discuss the morphology-based species descriptions. notes and colour pictures taken from different angles (e.g. dorsal and lateral). Additional notes on substrate, behaviour, and ecology were taken whenever possible (rocks in shallow MATERIAL AND METHODS water generally refer to a depth above 3 m, rocks in deeper water to a depth below 3 m, if not otherwise indicated). A The study is based on material collected during several fi eld morphological overview with standard characters examined is trips to the ancient lakes of Sulawesi from 2002 to 2005 provided in Fig. 2. Specimens and their qualitative characters (Fig. 1C) by the authors, but also by M. Glaubrecht and T. were studied with a Leica MZ12 stereo microscope and a von Rintelen (for collecting details compare the respective Zeiss Axioskop 20 light microscope in 75-95% ethanol. material examined section of each species). Species from Some specimens of each species fi xed in 95% ethanol were the lakes were caught by hand net or with plastic containers dehydrated in 100% ethanol for 30 minutes and afterwards while snorkelling or scuba diving; the riverine taxa only critical point dried with a BAL-TEC CPD 030, mounted on with hand nets. For scanning electron microscopy (SEM), aluminium specimen stubs with standard adhesive pads, and specimens were fi xed in 95% ethanol. All other specimens coated with gold-palladium using a Polaron SC7 640 Sputter are preserved in 75% ethanol, if not otherwise indicated Coater. SEM pictures were taken on a LEO 1450VP Scanning

Fig. 2. General morphology of Caridina (modifi ed from Holthuis, 1955: 3; shrimp drawing modifi ed from Woltereck, 1937a: 215).

346 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Electron Microscope (software: 32 V02.03) at 10 kV and Identifi cation keys to species from the ancient lakes of later processed with Adobe Photoshop CS2. Morphometric Sulawesi. Ð Woltereck (1937a, b) mentioned the rostrum as a measurements (for details and abbreviations see Fig. 3) good character to delimit the different species she described were taken using a Leica MZ12 stereo microscope with an from the Malili lakes: “…the rostrum varies in length, but the ocular micrometer. Standard descriptive statistical parameters type does not change.” (Woltereck, 1937a: 228). Schenkel (sample size, range, mean, and standard deviation (SD), (1902) provided a detailed description of the rostrum in median) were calculated using Microsoft Excel 2000. In species from Lake Poso and included an elaborate table of species descriptions, mean and median were included. The rostral characters from one species. The recent examination median was considered as more meaningful in interspecifi c of specimens from both lake systems confi rmed that shape comparisons, because it relativizes outliers and thus better and denticulation of the rostrum are constant in the majority represents the average population parameter than the mean. of the species. Therefore, the following morphological key Therefore, in the taxonomic remarks, the range and the is mainly based on rostral characters from adult specimens median are compared between species, although in most cases of both sexes (although it has to be mentioned that females mean and median were identical. Standard parameters have are generally larger than males). It is not appropriate for the been taken as shown in Fig. 3. The width of the dactyli of the identifi cation of most juveniles, though. third and fi fth pereiopod were measured without the spines on the fl exor margin, because these were sometimes broken; During sampling in the lakes, most species could easily the terminal spines were included in the measurements, but be told apart (juveniles included) based on colour pattern, not in the spine counts. Drawings of dissected specimens substrate, collecting site, or behaviour. Thus, an additional were either made with a camera lucida mounted on the key for each lake system is provided for the quick pre- stereo microscope or a light microscope (for fragile body identifi cation of living animals in the fi eld. Because each appendages, e.g. pleopods), or from SEM pictures (e.g. species fl ock is endemic to its respective lake system and uropodal diaeresis, telson). Drawings were then digitized and both lake systems are completely isolated from each other, processed with Adobe Photoshop and Illustrator CS2. the key to living animals in the fi eld is subdivided into species from the Malili lake system and from Lake Poso The connecting rivers within the Malili lake system, e.g. (and its river system). Tominanga River (Fig. 1C) are rather an extension of the lakes themselves (aleit with currents). Thus, in the material All keys provided here are only applicable to species of examined section, specimens of lake species found in the Caridina from the ancient lakes of Sulawesi. Petea and Tominanga rivers as well as specimens from Larona River close to the outlet bay of Lake Towuti (fi gure 1C) have been assigned to the lake into which the respective MORPHOLOGICAL river is draining: Petea = Lake Matano; Tominanga = Lake KEY TO ALL ANCIENT LAKE SPECIES Mahalona; Larona = Lake Towuti (compare von Rintelen et al., in review). For this study, over 4,600 adults (plus 1 Rostrum distinctly shorter than scaphocerite and antennular several juveniles) were examined. We thus abandoned to peduncle (maximal reaching to end of second segment) ... 2 list the sex for the majority of specimens in the material examined section.

The molecular phylogeny (tree topology) of species of Caridina from the ancient lakes (and other species from Sulawesi and Java shown in Figs. 63-64 that are not part of this taxonomic revision) was taken from von Rintelen et al., (in review). However, species names were updated for – Rostrum longer (overreaching second segment of antennular this study, and here, the molecular results for each species peduncle), reaching near to or beyond end of scaphocerite or are discussed in the respective taxonomic remark section antennular peduncle ...... 5 following each species description (for technical details and sequence accession numbers see von Rintelen et al., in review).

REVISION OF CARIDINA FROM THE ANCIENT LAKES OF SULAWESI

In this revision, 21 species are recognized from the ancient lakes of Sulawesi, 15 (including eight new taxa) from the Malili lakes and six (including two new taxa) from Lake Poso (Tables 2-3); details of each species are provided below.

347 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 3. Standard morphometric characters in Caridina. A. Cephalothorax and abdomen (shrimp drawing modifi ed from Woltereck, 1937a: 215). B. Rostrum and cephalic appendages. C. First and second pereiopod. D. Tailfan (telson and uropods). E. Third and fi fth pereiopod. Abbreviations. antp (length of antennular peduncle), cl (carapace length), rl (rostrum length), abds5 (length of fi fth abdominal somite), abds6 (length of sixth abdominal somite), h tel (length/height of telson), w tel (width of telson), h ch1 (length/height of chela of fi rst pereiopod), w ch1 (width of chela of fi rst pereiopod), h ca1 (length/height of carpus of fi rst pereiopod), w ca1 (width of carpus of fi rst pereiopod), h ch2 (length/height of chela of second pereiopod), w ch2 (width of chela of second pereiopod), h ca2 (length/height of carpus of second pereiopod), w ca2 (width of carpus of second pereiopod), n spines p3 (number of spines on the dactylus of the third pereiopod), n spines p5 (number of spines on the dactylus of the fi fth pereiopod).

348 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Current taxonomy of species from the ancient lakes of Sulawesi based on this revision (in alphabetical order).

Taxon Lake system State of endemism Remarks C. acutirostris Schenkel, 1902 Poso endemic riverine (generalist?) C. caerulea, new species Poso endemic lacustrine (specialist?) C. dennerli, new species Malili endemic lacustrine specialist C. ensifera Schenkel, 1902 Poso endemic lacustrine generalist C. glaubrechti, new species Malili endemic lacustrine specialist C. holthuisi, new species Malili endemic lacustrine specialist C. lanceolata Woltereck, 1937a Malili endemic lacustrine generalist C. lingkonae Woltereck, 1937a Malili endemic lacustrine specialist C. loehae Woltereck, 1937a Malili endemic lacustrine specialist C. longidigita Cai & Wowor, 2007 Poso endemic lacustrine specialist C. mahalona Cai et al., 2009 Malili and Tomori area non-endemic riverine generalist C. masapi Woltereck, 1937a Malili endemic riverine generalist C. parvula, new species Malili endemic lacustrine specialist C. profundicola, new species Malili endemic lacustrine specialist C. sarasinorum Schenkel, 1902 Poso endemic lacustrine (specialist?) C. schenkeli, new species Poso endemic riverine generalist C. spinata Woltereck, 1937a Malili endemic lacustrine specialist C. spongicola Zitzler & Cai, 2006 Malili endemic lacustrine specialist C. striata, new species Malili endemic lacustrine specialist C. tenuirostris Woltereck, 1937a Malili endemic lacustrine specialist C. woltereckae Cai et al., 2009 Malili endemic lacustrine specialist

Table 2. Comparison of species diversity in both lake systems after a taxonomic revision.

Lake system n species before revision n species after revision Poso system 4 6 Malili lake system 10* 15 Total 14 21

*including Caridina towutensis Woltereck, 1937a.

2 Rostrum slender and appearing fragile, body small (carapace 3 Body usually small (mean carapace length < 3.0 mm), rostrum length < 3.0 mm), number of spines on the dactylus of the fi fth never reaching to end of second segment of antennular peduncle, pereiopod < 20 ...... C. loehae without a conspicuous gap on the dorsal margin, preanal carina rounded, without a spine ...... C. parvula

– Rostrum appearing rather broad and robust, teeth usually pronounced, number of spines on the dactylus of the fi fth pereiopod > 30 ...... 3

349 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

– Body usually large (mean carapace length > 4 mm), rostrum – Proximal part of rostrum not conspicuously triangular, with can reach second segment of antennular peduncle, with a or without unarmed gap on dorsal margin, fi rst and second conspicuous unarmed gap on the dorsal margin, preanal carina pereiopod stout to slender (if very slender, then rostrum slender with a spine ...... 4 throughout) ...... 8

7 Rostrum very long, reaching far beyond end of scaphocerite (ratio rostrum length/carapace length 1.4-2.8), distal part very slender ...... C. profundicola 4 Rostrum reaching near or to end of second segment of antennular peduncle, scaphocerite rather stout (3.0–3.6 times as long as wide), carpus of fi rst and second pereiopod stouter (2.0–2.7 and 4.5–5.9 times as long as wide), Poso riverine species ...... C. acutirostris

– Rostrum length variable, reaching to end of second segment of antennular peduncle or distinctly shorter, scaphocerite rather – Rostrum reaching beyond end of scaphocerite (ratio rostrum slender (3.5–4.1 times as long as wide), carpus of fi rst and length/carapace length 1.0-1.6), but not very far, generally second pereiopod more slender (2.5–3.3 and 5.6–7.0 times as broader and stouter ...... C. lingkonae long as wide), Malili riverine species ...... C. mahalona 5 Chelae of fi rst and second pereiopod uniformly long and slender, bearing very long fingers (setae), about as long as chelae ...... C. longidigita

8 Rostrum with a conspicuous unarmed gap on the dorsal margin, distally completely unarmed or with few widely spaced teeth, with or without subapical teeth ...... 9

– Chelae of fi rst and second pereiopod not uniformly long and slender, fi ngers rather short ...... 6

6 Proximal part of rostrum conspicuously triangular (best visible – Dorsal margin of rostrum without a conspicuous unarmed gap, transilluminated), otherwise more slender, dorsal denticulation denticulation throughout, although sometimes distally less without unarmed gap, first and second pereiopod very densely spaced ...... 15 slender ...... 7

350 THE RAFFLES BULLETIN OF ZOOLOGY 2009

9 Rostrum reaching well beyond end of scaphocerite (ratio rostrum 12 Rostrum not extremely long and slender (ratio rostrum length/ length/carapace length >1.1) ...... 10 carapace length 1.0–1.2), number of ventral teeth 8–14 ...... C. sarasinorum

– Rostrum reaching near to or slightly beyond end of scaphocerite (ratio rostrum length/carapace length <1.1) ...... 14 – Rostrum extremely long and slender (ratio rostrum length/ carapace length >1.4), 16-48 ventral teeth ...... 13

10 Rostrum strongly upturned, usually with 1-4 subapical teeth, ventral teeth prominent and widely spaced, sixth abdominal somite long (0.8-1.1 times length of carapace) ...... C. lanceolata

13 Rostrum with distinctly less teeth (dorsal 9–15, ventral 16–29) and shorter compared to carapace length (1.4–2.3), uropodal diaeresis with 9–11 spines, 6–9 spines on the dactylus of the third and 51–57 spines on the dactylus of the fi fth pereiopod ...... C. ensifera

– Rostrum straight to upturned (if strongly upturned ventral teeth densely spaced), but always without subapical teeth, sixth abdominal somite shorter (max. 0.8-0.9 times length of carapace) ...... 11 – Rostrum with distinctly more teeth (dorsal 11–20, ventral 26–48) 11 Rostrum very slender, body small and slender (carapace length and longer compared to carapace length (1.9–2.6), uropodal 2.4–3.3 mm), about 3 spines on the dactylus of the third and diaeresis with 11–14 spines, 4–5 spines on the dactylus of the 11–15 spines on the dactylus of the fi fth pereiopod, Malili third and 27–49 spines on the dactylus of the fi fth pereiopod species ...... C. tenuirostris ...... C. caerulea

– Rostrum broad to slender, body usually distinctly larger or more robust (carapace length 2.6–5.3 mm), about 4–9 spines on the dactylus of the third and >30 spines on the dactylus of the fi fth pereiopod, Poso species ...... 12 14 Malili (typical riverine) species ..... C. masapi, C. Mahalona – Poso (typical riverine) species .. C. acutirostris, C. schenkeli

351 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

15 Preanal carina rounded, without a spine ...... 16 KEY TO LIVING ANIMALS IN THE FIELD (MALILI LAKE SYSTEM)

1 Body reddish or yellowish, but mainly translucent ...... 2 – Body colour red or brown, often with white or beige markings ...... 3 2 Rostrum longer than scaphocerite and strongly upturned, with – Preanal carina with a spine ...... 17 prominent teeth and a conspicuous unarmed gap on dorsal margin, without a triangular shape, body yellowish to reddish, movements in all directions, from lakes or rivers ...... C. lanceolata

16 Rostrum not overreaching scaphocerite or antennular peduncle, body small (carapace length 1.8–2.8 mm) ...... C. spongicola

– Rostrum reaching (slightly) beyond end of scaphocerite and – Proximal part of rostrum conspicuously triangular, fi rst and antennular peduncle, carapace length 2.8 mm or more ...... second pereiopod extremely slender, from Lake Towuti or ...... C. striata, C. glaubrechti, C. woltereckae Lake Mahalona ...... 4 17 Rostrum long, reaching beyond end of scaphocerite, fi rst and second pereiopod conspicuously slender ...... C. spinata

3 Collected from Lake Masapi or Lake Lontoa ...... C. masapi – Collected from other localities ...... 5 – Rostrum reaching near or slightly beyond end of scaphocerite, 4 Rostrum very long, reaching far beyond end of scaphocerite, fi rst and second pereiopod not conspicuously slender ..... 18 body large and yellowish, abdomen with few yellow stripes, 18 Rostrum completely lacking a dorsal gap, slightly falciform, sometimes a kind of green saddle visible, eggs of ovigerous about 2 spines on the dactylus of the third and 25–30 spines females green, keeps rather still when disturbed, movements on the dactylus of the fi fth pereiopod, Lake Matano species side- or downwards, usually between large boulders below 3 ...... C. dennerli m, juveniles also on other substrate, only from Lake Towuti ...... C. profundicola

– Rostrum often with an inconspicuous unarmed gap on dorsal margin (less than ¼ of total length), the shape rather straight or angular, 3–6 spines on the dactylus of the third and 27–39 spines on the dactylus of the fi fth pereiopod ..... C. holthuisi

352 THE RAFFLES BULLETIN OF ZOOLOGY 2009

– Rostrum distinctly shorter, can overreach scaphocerite, but 8 Body mainly brown and white (harlequin-like), on in not very far, body usually reddish, pelagic or on substrate, but the outlet bay of Lake Towuti (fi ts in the sponges’ cavities) usually in shallow water, movements in all directions, in Lake ...... C. spongicola Towuti or Lake Mahalona ...... C. lingkonae

– Body either with a similar pattern, but then larger and mainly on rocks, or with a different colour pattern ...... 10 5 Body crimson to deep red with orange or yellow appendages, 9 Body red with white bands, tips of uropods white, rostrum often with two to three yellow or orange transversal stripes and slender ...... C. loehae a few same coloured dots on various body parts, antennules white, colours appearing bright and vivid, on rocks, often between boulders below 3 m, only from Lake Towuti ...... C. spinata

– Body only red, rostrum stouter ...... C. parvula

– Body not red or if dark red, then without a conspicuous combination of yellow or orange, usually not between boulders below 3 m ...... 6 6 Body bright to dark red, colour vivid, either without white markings, with white dots or dorsally with small transversal stripes, but without conspicuous stripes, on rocks ...... 7 – Body usually not unicoloured, but with conspicuous bands or 10 Body red, lateral with several longitudinal white stripes, fi rst longitudinal stripes ...... 8 and second pereiopod partly conspicuously white, on rocks in 7 Body always red covered with white dots, one distinct dot on Lake Towuti or Lake Mahalona ...... C. striata the dorsodistal part of the abdomen, chela and carpus of the fi rst and second pereiopod bright white, antenna, antennules and scaphocerite white, only in Lake Matano .... C. dennerli

– Body colouration with a different pattern ...... 11

– Body red, but without conspicuous white dots, on rocks in shallow water ...... 9

353 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

11 Body large, with the harlequin pattern similar to C. spongicola, 15 Body usually larger and more robust, rostrum highly variable, on rocks, only in Lake Towuti ...... C. woltereckae only occurring in rivers ...... C. mahalona – Body usually smaller and less robust, rostrum reaching to or slightly beyond end of scaphocerite, occurring in rivers and lakes ...... C. masapi

– Body colouration with a different pattern ...... 12 KEY TO LIVING ANIMALS IN THE FIELD 12 Body mainly brown with several white bands, on rocks, only (LAKE POSO AND ITS RIVER SYSTEM) in Lake Towuti ...... 13 – Body colouration with a different pattern ...... 14 1 Rostrum conspicuously long and slender (reaching far beyond 13 Rostrum without a conspicuous gap on dorsal margin, only in end of scaphocerite), body also slender and mainly transparent, Lake Towuti, collected from rocks ...... C. glaubrechti appendages bluish or reddish, uropods with clearly visible red or blue spots, often in huge swarms or attached to a substrate, collected from the lake ...... 2

– Rostrum with a conspicuous gap on dorsal margin, in Lake Towuti, Lake Mahalona and Tominanga River, collected from wood ...... C. tenuirostris – Rostrum short to long, but not conspicuously long, body usually more robust and less transparent, usually attached to any kind of substrate, collected from the lake or rivers ...... 3 2 Main colour of appendages bluish, tailfan with two conspicuous blue patches on each uropods ...... C. caerulea

14 Body dark brown, colour vivid, either completely without or with white-beige markings, rostrum straight and broad usually under leaf litter, mainly in the lakes ...... C. holthuisi

– Body less vivid brown or otherwise coloured, rostrum usually more slender and slightly curved, occurring in rivers or lakes ...... 15

354 THE RAFFLES BULLETIN OF ZOOLOGY 2009

– Main colour of appendages reddish, not bluish, tailfan with SPECIES FROM THE MALILI LAKE SYSTEM two conspicuous red patches on distal part of each uropods (INDONESIA, SOUTH SULAWESI) ...... C. ensifera Caridina dennerli, new species (Figs. 4-6; Table 3)

Material examined. Ð Holotype: ovigerous female (cl 3.1 mm)(MZB Cru 1540), Lake Matano, east shore, just at entrance to outlet bay, 02°31.54'S, 121°27.00'E, loc. 43-03, on gravel in shallow water, coll. K. & T. von Rintelen, 18 Sep.2003.

Paratypes (all Lake Matano) – 24 ex. (MZB Cru 1542, n=10; ZMB 29024, n=14, some SEM material), south shore, Soroako, Salonsa, INCO boat house, 02°30.71'S, 121°20.45'E, loc. 19-03, on gravel in shallow water, coll. K. & T. von Rintelen, 19 Sep.2003; 24 ex. 3 First and second pereiopod with conspicuously long chelae (MZB Cru 1541, n=14 and ZMB 29049, n=10, some SEM material), and fi ngers (setae), fi ngers partly orange, body brownish to east shore, just at entrance to outlet bay, 02°31.54'S, 121°27.00'E, greenish, usually on rocks or wood (hard substrate), rostrum loc. 43-03, on gravel in shallow water, coll. K. & T. von Rintelen, longer than scaphocerite, collected from the lake ...... 18 Sep.2003; 9 ex. (MZB Cru 1548, n=4; ZMB 29050, n=5, some ...... C. longidigita SEM material), north shore, 02°27.28'S, 121°21.21'E, loc. 98-03, on gravel, coll. K. & T. von Rintelen, 1 Oct.2003; 25 ex. (MZB Cru 1544, n=13; ZMB 29051, n=12, some SEM material), northwest corner, 02°27.71'S, 121°13.03'E, loc. 102-03, on boulders in deeper water, coll. K. & T. von Rintelen, 1 Oct.2003; 9 ex. (MZB Cru 1546, n=5; ZMB 29103, n=4, some SEM material), east shore, south bay, 02°32.77'S, 121°26.71'E, loc. 45-03, on gravel, coll. K. & T. von Rintelen, 1 Oct.2003; 10 ex. (MZB Cru 1547, n=5; ZMB 29104, n=5 and few juveniles, some SEM material), southwest shore, Cape Nikomene, 02°32.24'S, 121°24.76'E, loc. 46-03, on gravel, coll. K. & T. von Rintelen, 1 Oct.2003; 3 ex. (ZMB 29153, n=3 and few juveniles), south shore, near cave entrance, 02°29.85'S, 121°18.66'E, loc. 60-03, on boulders in deeper water, coll. K. & T. von Rintelen, 24 Sep.2003; 3 ex. (ZMB 29155),south shore, 02°27.84'S, 121°13.88'E, loc. 63-03, on gravel, coll. K. & – First and second pereiopod without conspicuously long fi ngers, T. von Rintelen, 24 Sep.2003; 3 ex. (ZMB 29156, some SEM collected from the lake or from rivers ...... 4 material),north shore, 02°25.67'S, 121°16.54'E, loc. 65-03, on gravel, 4 Rostrum reaching well beyond end of scaphocerite, fi rst and coll. K. & T. von Rintelen, 25 Sep.2003; 4 ex. (ZMB 29157), second pereiopod rather stout, collected from the lake ...... north shore, 02°26.36'S, 121°19.03'E, loc. 84-03, on gravel, coll...... C. sarasinorum K. & T. von Rintelen, 1 Oct.2003; 14 ex. (MZB Cru 1545, n=7; ZMB 29326, n=7, some SEM material), south shore, 02°27.85'S, 121°13.87'E, loc. 125-04, on boulders in deeper water, coll. P. Koller & K. von Rintelen, 1 Aug.2004; 1 ex. (ZMB 29327), south shore, canal between island and mainland, 02°28.46'S, 121°15.83'E, loc. 62-03, on gravel, coll. K. & T. von Rintelen, 1 Oct.2003; 3 ex. (ZMB 29328), north shore, 02°26.274'S, 121°18.83'E, loc. 133-04, on gravel, coll. K. & T. von Rintelen, 22 Jul.2004; 1 ex. (ZMB 29329), west shore, 02°26.828'S, 121°12.988'E, loc. 135-04, on gravel, coll. K. & T. von Rintelen, 23 Jul.2004; 3 ex. (ZMB 29330), north shore, 02°27.311'S, 121°21.047'E, loc. 09-05, on gravel in – Rostrum shorter, reaching slightly beyond end of scaphocerite, shallow water, coll. K. & T. von Rintelen, 7 Jan.2005; 4 ex. (MZB first and second pereiopod not conspicuously stout, from Cru 1543), Lake Matano (no details given), loc. F2-02, substrate rivers ...... C. acutirostris, C. schenkeli unknown, coll. F. Herder & A. Nolte, 1 Dec.2002.

Description. – Carapace length 1.5-3.4 mm (n=53). Rostrum TAXONOMY (Fig. 5A; Table 3) reaching near or to end of scaphocerite, slightly sickle-shaped, 0.9-1.3 times as long as carapace ATYIDAE de Haan, 1849 (n=39), armed dorsally with 15-25 teeth (including 3-7 teeth posterior to orbital margin), anterior less densely spaced, Caridina H. Milne Edwards, 1837 armed ventrally with 5-11 teeth. Antennal spine situated below inferior orbital angle. Pterygostomial angle broadly Caridina H. Milne Edwards, 1837: 362. rounded. Eyes well developed, anterior end 0.5 times length Type species. – Caridina typus H. Milne Edwards, 1837: 363 (type of basal segment of antennular peduncle (n=5). Antennular locality unknown, gender feminine), by monotypy. peduncle 1.0-1.3 times as long as carapace (n=5), second segment 2.0-2.2 times length of third segment, third segment

355 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

0.3-0.4 times length of basal segment. Stylocerite reaching maxillula (Fig. 6B) broadly rounded, upper lacinia elongate, 0.8-0.9 times length of basal segment of antennular peduncle with numerous distinct teeth and setae on inner margin, palp (n=5). Scaphocerite (Fig. 5D) 4.3-5.7 times as long as wide slender. Upper endites of maxilla (Fig. 6C) subdivided, palp (n=5). elongated, scaphognathite tapering posteriorly with numerous long, curved setae at posterior end. Distal end of palp of Sixth abdominal somite 0.5-0.7 times length of carapace fi rst maxilliped (Fig. 6F) triangular, with a long fi nger-like (n=35), 1.4-2.0 times as long as fi fth somite (n=32), 0.8-1.0 projection; fl agellum of the exopod very elongated, endopod times length of telson (n=24). Telson (Fig. 5C,H) 3.1-3.3 high, reaching to half the fl agellum of exopod in length. times as long as wide (n=5), distal margin rounded, without Second maxilliped (Fig. 6D) typical. Third maxilliped (Fig. projection, with 3-4 pairs of spinules and 1 pair of dorsolateral 6E) with ultimate segment slightly shorter than penultimate spinules; distal end with 3-4 pairs of spines, lateral pair segment. distinctly longer than intermediate pairs, median pair shortest. Preanal carina (Fig. 5E) with a spine. Uropodal diaeresis First and second pereiopod very slender, chela and carpus (Fig. 5B) with 12-13 movable spinules (n=5). of fi rst pereiopod distinctly stouter and broader than chela and carpus of second pereiopod (Fig. 5M-P); chela of fi rst 5 pairs of pleurobranchs well developed; 3 pairs of pereiopod 2.4-3.8 times as long as wide (n=35), 0.9-1.1 times arthrobranchs, 2 on third maxillipeds, with second pair length of carpus (n=39); tips of fi ngers rounded, without strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair hooks; dactylus 1.7-2.4 times as long as palm (n=6); carpus of podobranchs on second maxilliped reduced strongly to a 3.3-4.6 times as long as wide (n=35), 1.4-1.8 times length laminate form. Epipod present on fi rst pereiopod, but reduced. of merus (n=5). Chela of second pereiopod 2.8-3.7 times as Incisor process of mandible (Fig. 6A) ending in a row of long as wide (n=35), 0.6-0.7 times length of carpus (n=39); 3-4 small teeth, molar process truncated. Lower lacinia of tips of fi ngers rounded, without hooks, dactylus 1.6-2.1 times

Fig. 4. Caridina dennerli from the Malili lake system. A. Distribution. B.-C. Colour pattern of living animals (not to scale). Pictures courtesy of Chris Lukhaup.

356 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 5. Caridina dennerli from the Malili lake system. A. Cephalothorax and cephalic appendages, female (ZMB 29049); B. Uropodal diaeresis, male (ZMB 29051); C. Telson, male (ZMB 29156); D. Scaphocerite, male (ZMB 29051); E. Preanal carina, F. Third pereiopod, female (ZMB 29326); G. Fifth pereiopod; H. Distal end of telson male (ZMB 29156); I. Dactylus of third pereiopod female (ZMB 29326); J. Dactylus of fi fth pereiopod; K. Endopod of male fi rst pleopod (ZMB 29051); L. Appendix masculina of male second pleopod; M. First pereiopod, male (ZMB 29156); N. Second pereiopod; O. SEM image of anterior part of chela, male (ZMB 29104); P. SEM image of chela and carpus of fi rst and second pereiopods, female (ZMB 29024). Scale bars: A, D = 1.0 mm; C, E-G, K-P = 0.5 mm; B, H-J = 0.1 mm.

357 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Table 3. Summary of standard morphometric parameters for Caridina dennerli. parameter range mean ± SD median n cl (mm) 2.3-3.8 2.8 ± 0.4 2.7 29 rl / cl 0.6-1.2 0.9 ± 0.1 0.9 32 n dorsal rostral teeth 14-28 20 ± 3 20 32 n ventral rostral teeth 3-7 5 ± 1 5 32 abds6 / cl 0.5-0.7 0.6 ± 0.1 0.6 15 abds6 / abds5 1.4-1.8 1.6 ± 0.1 1.6 15 abds6 / h tel 0.9-1.0 0.9 ± 0.0 0.9 10 h tel / w tel 2.9-3.5 3.3 ± 0.2 3.4 6 n spines uropodal diaeresis 12-13 13 ± 1 13 5 h ch1 / w ch1 1.8-2.3 2.1 ± 0.2 2.1 18 h ch1 / h ca1 1.1-1.4 1.2 ± 0.1 1.2 17 h ca1 / w ca1 2.0-3.1 2.7 ± 0.3 2.7 13 h ch2 / w ch2 2.3-3.5 2.8 ± 0.3 2.8 18 h ch2 / h ca2 0.7-0.9 0.8 ± 0.1 0.7 22 h ca2 / w ca2 4.3-7.0 5.7 ± 0.9 5.7 18 n spines p3 3-6 4 ± 1 4 5 n spines p5 27-39 34 ± 5 33 5 as long as palm (n=6); carpus 6.9-8.5 times as long as wide Biology and ecology. – C. dennerli is a hard substrate (n=35), 1.4-1.9 times as long as merus (n=5). dweller (rocks) occurring in different water depths (from shallow water to approx. –10 m), on or under small rocks, Third pereiopod (Fig. 5F,I) slender, dactylus 3.8-5.3 times and between boulders. When disturbed, it tries to escape side- as long as wide (terminal spine included, without spines of or downwards rather than in other directions, but frequently fl exor margin; n=5), terminating in one large claw with 2 stays attached to a rock when it is uplifted. accessory spines on fl exor margin; propodus 14.7-24.2 times as long as wide, 4.9-6.2 times as long as dactylus; carpus Colour pattern. – C. dennerli has one of the most conspicuous 7.5-9.2 times as long as wide, 0.6-0.7 times as long as colour patterns among the ancient lake species (Fig. 4B-C). propodus, 0.5-0.6 times as long as merus; merus 11.0-12.4 Body and most appendages are primarily dark red to purple; times as long as wide, bearing 3-4 strong, movable spines body covered with several white conspicuous spots and one on posterior margin of outer surface. distinct white dot on the dorsodistal part of the abdomen. Chela and carpus of the fi rst and second pereiopod bright Fifth pereiopod slender (Fig. 5G,J), dactylus 3.0-5.1 times white and distinctly contrasting the otherwise red colour. as long as wide (terminal spine included, without spines of Antenna, antenulla, and scaphocerite also white. When fl exor margin; n=5), terminating in one large claw with 25- feeding, the white chelipeds were observed to be always 30 accessory spines on fl exor margin; propodus 17.3-24.2 clearly visible, whereas the rest of the (dark coloured) times as long as wide, 4.4-7.0 times as long as dactylus; body was more or less camoufl aged; eggs are also dark red. carpus 6.6-9.0 times as long as wide, 0.5 times as long Under stress, red body colour can change to blue, but only as propodus, 0.6 times as long as merus; merus 9.4-13.8 temporarily. This change of colour was only observed in a times as long as wide, bearing 1-3 strong, movable spines small water tank minutes after being caught. on posterior margin of outer surface. Etymology. – Caridina dennerli, new species, is dedicated Endopod of male fi rst pleopod (Fig. 5K) elongated triangular, to the German company Dennerle GmbH, which kindly 1.7-2.3 times as long as proximally wide (n=5), without supported the authors’ shrimp project on the ancient lake appendix interna. Appendix interna of male second pleopod species of Sulawesi. (Fig. 5L) 0.8-0,9 times length of appendix masculina (n=5). Taxonomic remarks. – The slightly falciform rostrum is a more constant character in C. dennerli than in other species. Ovigerous females with 8-14 eggs (n=7 females); egg size Thus, it is already distinguishable in most cases at fi rst sight. 1.0-1.2 x 0.5-0.7 mm (n=88, eggs with and without eyes). With regard to the rostrum, C. dennerli mainly resembles C. holthuisi, but also other species from Lake Towuti, e.g. the Distribution. – C. dennerli is endemic to Lake Matano and broad rostrum morph of C. striata, although it is more slender widely distributed within the lake (Fig. 4A). than in C. holthuisi and usually broader and shorter than in C. striata (reaching near or to end of scaphocerite vs. longer

358 THE RAFFLES BULLETIN OF ZOOLOGY 2009 than in C. striata). It differs from C. holthuisi not only in Caridina glaubrechti, new species its substrate preference (rocks vs. leaf litter in C. holthuisi) (Figs. 7-9; Table 4) and colour pattern (compare respective description), but also by a different number of ventral teeth on the rostrum (5-11, Caridina sp.1 – von Rintelen et al., 2007b: 262, fi g. 2b. median 9 vs. 3-7, median 5 in C. holthuisi) and distinctly more slender pereiopods in C. dennerli (for example chela Material examined. – Holotype: female (cl 2.7 mm)(MZB Cru of fi rst pereiopod 2.4-3.8, median 2.7 vs. 1.8-2.3, median 2122), Lake Towuti, west shore, south of Cape Timbalo, 02°42.91'S, 121°26.78'E, loc. 94-03, coll. K. & T. von Rintelen, 4 Oct.2003. 2.1 in C. holthuisi). Paratypes (all Lake Towuti) – 5 ex. (ZMB 29053, some SEM In the molecular phylogeny (Figs. 63-64), C. dennerli material), south shore, approx. 2 km east of Cape Mea, 02°55.8'S, is genetically distinct form the other species mentioned 121°26.92'E, loc. 74-03, coll. K. & T. von Rintelen, 28 Sep.2003; above. 2 ex. (ZMB 29074, some SEM material), north shore, bay east of

Fig. 6. Caridina dennerli from the Malili lake system. A. Mandible (ZMB 29024); B. Maxillula; C. Maxilla; D. second maxilliped; E. third maxilliped; F. fi rst maxilliped. Scale bars: A-F = 1mm.

359 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Cape Bintu, 02°39.48'S, 121°33.25'E, loc. 68-03, coll. K. & T. well developed, anterior end 0.6-0.8 times length of basal von Rintelen, 26 Sep.2003; 26 ex. (MZB Cru 1825, n=11; ZMB segment of antennular peduncle (n=5). Antennular peduncle 29077, n=15), west shore, south of Cape Timbalo, 02°42.91'S, 1.0 times as long as carapace (n=5), second segment 1.8-2.1 121°26.78'E, loc. 94-03, coll. K. & T. von Rintelen, 4 Oct.2003; 1 times length of third segment, third segment 0.3 times length ex. (ZMB 29086, some SEM material), Larona River, 02°45.06'S, of basal segment. Stylocerite reaching 0.9 times length of 121°20.12’E, loc. 50-03, coll. K. & T. von Rintelen, 21 Sep.2003; 12 ex. (MZB Cru 1826, n=6; ZMB 29109, n=6), west shore, north basal segment of antennular peduncle (n=5). Scaphocerite of Cape Wasupute, 02°46.9'S, 121°27.94'E, loc. 78-03, coll. K. & (Fig. 8D) 4.0-5.7 times as long as wide (n=5). T. von Rintelen, 26 Jul.2004; 7 ex. (ZMB 29301), west shore, west of Cape Timbalo, 02°42.631'S, 121°26.389'E, loc. 145-04, coll. K. Sixth abdominal somite 0.5-0.8 times length of carapace & T. von Rintelen, 26 Jul.2004; 3 ex. (ZMB 29335), northwest (n=10), 1.6-2.0 times as long as fi fth somite (n=5), 0.8-1.2 shore, 02°40.897'S, 121°25.015'E, loc. 143-04, coll. K. & T. von times length of telson (n=11). Telson (Fig. 8F-G,M-N) Rintelen, 25 Jul.2004; 2 ex. (MZB Cru 1827), west shore, Cape 3.2-3.4 times as long as wide (n=5), distal margin rounded, Bakara, 02°40.771'S, 121°26.11'E, loc. 144-04, on rocks in deeper without projection, with 3-4 pairs of spinules and 1 pair of water, coll. K. & T. von Rintelen, 26 Jul.2004. dorsolateral spinules; distal end with 3-4 pairs of spines, lateral pair distinctly longer than intermediate spines, Description. – Carapace length 2.3-3.4 mm (n=11). Rostrum median pair or median spine shortest. Preanal carina (Fig. (Fig. 8A; Table 4) long, reaching beyond end of scaphocerite, 8B) rounded, without a spine. Uropodal diaeresis (Fig. 8C) 0.9-1.7 times as long as carapace (n=12), armed dorsally with 11-14 movable spinules (n=5). with 11-17 teeth (including 2-5 teeth posterior to orbital margin), anterior less densely spaced, armed ventrally with 5 pairs of pleurobranchs well developed; 3 pairs of 5-16 teeth (n=9). Antennal spine situated below inferior arthrobranchs, 2 on third maxillipeds, with second pair orbital angle. Pterygostomial angle broadly rounded. Eyes strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair

Fig. 7. Caridina glaubrechti from the Malili lake system. A. Distribution. B. Colour pattern of living animal (not to scale). Picture courtesy of Chris Lukhaup.

360 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 4. Summary of standard morphometric parameters for Caridina glaubrechti. parameter range mean ± SD median n cl (mm) 2.3-3.4 2.9 ± 0.3 2.9 11 rl / cl 0.9-1.7 1.2 ± 0.3 1.1 12 n dorsal rostral teeth 11-17 15 ± 2 15 9 n ventral rostral teeth 5-16 9 ± 4 8 9 abds6 / cl 0.5-0.8 0.7 ± 0.1 0.7 10 abds6 / abds5 1.6-2.0 1.8 ± 0.2 1.8 5 abds6 / h tel 0.8-1.2 1.0 ± 0.1 1.0 11 h tel / w tel 3.2-3.4 3.3 ± 0.1 3.3 5 n spines uropodal diaeresis 11-14 13 ± 1 12 5 h ch1 / w ch1 2.0-2.4 2.2 ± 0.2 2.2 8 h ch1 / h ca1 1.1-1.4 1.2 ± 0.1 1.2 12 h ca1 / w ca1 1.9-3.4 2.6 ± 0.5 2.6 8 h ch2 / w ch2 2.3-3.2 2.8 ± 0.3 2.9 8 h ch2 / h ca2 0.7-0.8 0.8 ± 0.0 0.8 11 h ca2 / w ca2 4.8-6.7 5.7 ± 0.7 5.7 8 n spines p3 2-5 4 ± 1 4 4 n spines p5 14-35 26 ± 9 28 4 of podobranchs on second maxilliped reduced strongly to times as long as wide, bearing 2-3 strong, movable spines a laminate form. Epipod reduced or totally absent from the on posterior margin of outer surface. fi rst pereiopod. Incisor process of mandible (Fig. 9A) ending in a row of 4-5 small teeth, molar process truncated. Lower Fifth pereiopod slender (Fig. 8I-J), dactylus 3.8-4.5 times lacinia of maxillula (Fig. 9B) broadly rounded, upper lacinia as long as wide (terminal spine included, without spines of elongate, with numerous distinct teeth and setae on inner fl exor margin; n=4), terminating in one large claw with 14- margin, palp slender. Upper endites of maxilla (Fig. 9C) 35 accessory spines on fl exor margin; propodus 14.0-21.8 subdivided, palp short, scaphognathite tapering posteriorly times as long as wide, 4.1-6.5 times as long as dactylus; with numerous long, curved setae at posterior end. Distal carpus 5.0-7.2 times as long as wide, 0.5-0.6 times as long end of palp of first maxilliped (Fig. 9F) triangular, not as propodus, 0.6-0.7 times as long as merus; merus 8.5-12.0 ending with a fi nger-like projection; fl agellum of the exopod times as long as wide, bearing 2-3 strong, movable spines very elongated, endopod high, not exceeding the fl agellum on posterior margin of outer surface. of exopod in length. Second maxilliped (Fig. 9D) typical. Third maxilliped (Fig. 9E) with ultimate segment as long Endopod of male fi rst pleopod (Fig. 8K) elongated triangular, as penultimate segment. 1.8-2.7 times as long as proximally wide (n=5), without appendix interna. Appendix interna of male second pleopod Chela and carpus of fi rst pereiopod distinctly stouter and (Fig. 39L) 0.8-0.9 times length of appendix masculina broader than chela and carpus of second pereiopod (Fig. (n=5). 8O-Q); chela of fi rst pereiopod 2.0-2.4 times as long as wide (n=8), 1.1-1.4 times length of carpus (n=12); tips of Ovigerous females with 20 eggs (n=2 females); egg size fi ngers rounded, without hooks; dactylus 1.1-1.3 times as 0.8-1.0 x 0.5-0.6 mm (n=40, eggs with and without eyes). long as palm (n=5); carpus 1.9-3.4 times as long as wide (n=8), 1.1-1.4 times length of merus (n=5). Chela of second Distribution. – C. glaubrechti is endemic to Lake Towuti pereiopod 2.3-3.2 times as long as wide (n=8), 0.7-0.8 times and was mainly found in the western part of the lake (Fig. length of carpus (n=11); tips of fi ngers rounded, without 7A). hooks, dactylus 1.2-1.5 times as long as palm (n=5); carpus 4.8-6.7 times as long as wide (n=8), 1.4 times as long as Biology and ecology. – C. glaubrechti is a hard substrate merus (n=5). dweller on rocks and was mainly found in shallow water regions on smaller rocks, but also in deeper water zones Third pereiopod (Fig. 8H,E) slender, dactylus 3.6-4.2 times (below 3 m) on larger rocks (boulders). When disturbed, as long as wide (terminal spine included, without spines it tries to escape side- or downwards rather than in other of fl exor margin; n=4), terminating in one large claw with directions. This is a behaviour also typical for other rock 2-5 accessory spines on fl exor margin; propodus 11.4-15.0 dwellers (KvR, pers. observ.). C. glaubrechti is often found times as long as wide, 4.2-5.5 times as long as dactylus; in syntopy with other rock dwellers in Lake Towuti, such as carpus 5.8-7.5 times as long as wide, 0.6-0.7 times as long C. profundicola and C. spinata, but particularly C. striata as propodus, 0.5 times as long as merus; merus 9.0-11.3 and C. woltereckae.

361 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 8. Caridina glaubrechti from the Malili lake system. A. Cephalothorax and cephalic appendages, female (ZMB 29053); B. Preanal carina, male (ZMB 29109); C. Uropodal diaeresis, female (ZMB 29053); D. Scaphocerite, male (ZMB 29109); E. Dactylus of third pereiopod, female (ZMB 29074), F. Telson, female (ZMB 29053); G. Telson, another female (ZMB 29053); H. Third pereiopod, female (ZMB 29074); I. Dactylus of fi fth pereiopod; J. Fifth pereiopod; K. Endopod of male fi rst pleopod (ZMB 29109); L. Appendix masculina of male second pleopod; M. Distal end of telson, female (ZMB 29053); N. Distal end of telson, another female (ZMB 29053); O. First pereiopod, female (ZMB 29053); P. Second pereiopod; Q. SEM image of chela and carpus of fi rst and second pereiopods, female (ZMB 29053). Scale bars: A, D = 1.0 mm; B, F-H, J-L, O-Q = 0.5 mm; C, E, I, M-N = 0.1 mm.

362 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Colour pattern. – The primary colour of C. glaubrechti is both species not only differ in their substrate preference brown with several white bands or patches all over the body (rocks vs. wood in C. tenuirostris), but by the continuous (including pereiopods and uropods; Fig. 7B). A conspicuous dorsal denticulation of the rostrum (vs. anterior dorsal part white band is visible at the distal part of the abdomen. always completely unarmed in C. tenuirostris), a different Appendages are transparent or partly brownish. Eggs are number of spines on the uropodal diaeresis (11-14, median brown. This colour pattern remains visible even if the shrimp 12 vs. 7-8, median 8 in C. tenuirostris), and on the dactylus is under stress; the intensity of the colour merely fades. of the fi fth pereiopod (14-35, median 28 vs. 11-15, median 14 in C. tenuirostris). Etymology. – Caridina glaubrechti, new species, is dedicated to Matthias Glaubrecht, who initiated the current research on As alcohol bleached material, C. glaubrechti is almost endemic species fl ocks from the ancient lakes of Sulawesi, identical with C. striata and C. woltereckae, although and who also collected several shrimp specimens. the colour pattern in living specimens always allows an unambiguous separation. It slightly differs from C. Taxonomic remarks. – The colour pattern of C. glaubrechti woltereckae by a higher number of spines on the dactylus of closely resembles the colour pattern of C. tenuirostris, but the fi fth pereiopod (14-35, median 28 vs. 13-22, median 20 in

Fig. 9. Caridina glaubrechti from the Malili lake system. A. Mandible (ZMB 29053); B. Maxillula; C. Maxilla; D. second maxilliped; E. third maxilliped; F. fi rst maxilliped. Scale bars: A-F = 1mm.

363 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

C. woltereckae). Also, the dimorphic character of the rostrum at mouth of Petea River, 02°34.54'S, 121°30.48'E, loc. 55-03, on in C. striata could not be observed in C. glaubrechti. leaf litter, coll. K. & T. von Rintelen, 23 Sep.2003; 11 ex. (MZB Cru 1796, n=5; ZMB 29324, n=6), east shore, estuary of Ponsoa In the molecular phylogeny (Figs. 63-64), C. glaubrechti River, 02°35.101'S, 121°30.681'E, loc. 146-04, on Ottelia, coll. P. Koller, K. & T. von Rintelen, 3 Aug.2004. forms a single clade with the other rock dwellers C. striata and C. woltereckae, and the dweller C. spongicola, but Paratypes (Lake Towuti) – 33 ex. (MZB Cru 1797, n=15; ZMB their relationship is not resolved within this clade (compare 29036, n=18), southwest shore, west of Cape Tetetu, 02°54.13'S, von Rintelen et al., 2007b; for further details see taxonomic 121°23.78'E, loc. 76-03, on leaf litter, coll. K. & T. von Rintelen, 28 remarks on C. striata). Sep.2003; 3 ex. (ZMB 29078, some SEM material), west shore, at entrance to outlet bay, Cape Larona, 02°48.43'S, 121°24.75'E, loc. 73-03, on leaf litter, coll. K. & T. von Rintelen, 27 Sep.2003; 21 Caridina holthuisi, new species ex. (MZB Cru 1798, n=11; ZMB 29228, n=10 and some juveniles), (Figs. 10-12, Table 5) east shore, 02°40.84'S, 121°41.32'E, loc. 87-03, on leaf litter, coll. K. & T. von Rintelen, 2 Oct.2003; 4 ex. (ZMB 29303, some SEM material), northeast shore, at Lengkona, 02°40.483'S, 121°41.382'E, Caridina opaensis – Woltereck, 1937a: 222, fig. I.4, pls. 3,6 loc. 116-04, on leaf litter, coll. K. & T. von Rintelen, 28 Jul.2004; (locality: Matanno [Matano], Soroako). 3 ex. (MZB Cru 1799), west shore, west of Cape Timbalo, Cardina opaensis – Brooks, 1950: 168 (erroneous spelling). 02°42.631'S, 121°26.389'E, loc. 145-04, on mixed substrate, coll. K. & T. von Rintelen, 26 Jul.2004; 2 ex. (MZB Cru 1800), northwest Material examined. – Holotype – ovigerous female (cl 3.2 shore, south of Timampu, 02°39.466'S, 121°25.859'E, loc. 140-04, mm)(MZB Cru 2125), Lake Matano, south shore, canal between on macrophytes, coll. K. & T. von Rintelen, 25 Jul.2004. island and mainland, 02°28.46'S, 121°15.83'E, loc. 62-03, on leaf litter, coll. K. & T. von Rintelen, 1 Oct.2003. Comparative material examined. – Caridina opaensis Roux, 1904: 547, pl. 9, Figs. 8-10 (type locality: Southeast Sulawesi, Lake Opa, Paratypes (Lake Matano) – 7 ex. (ZMB 29272), south shore, 30 m above sealevel). 02°27.85'S, 121°13.87'E, loc. 125-04, on leaf litter, coll. K. & T. von Rintelen, 1 Aug.2004; 5 ex. (ZMB 29065, some SEM material), Syntypes – 2 females (cl 2.9-3.3 mm) (NHMB 9a), Southeast south shore, 02°27.84'S, 121°13.88'E, loc. 63-03, on leaf litter, coll. Sulawesi, Opa, Sulawesi, Indonesia, coll. Sarasin, 1904. K. & T. von Rintelen, 24 Sep.2003; 4 ex. (ZMB 29073), south shore, at small islands, 02°28.461'S, 121°15.591'E, loc. 137-04, on Others (all Southeast Sulawesi): 1 ex. (ZMB 29008), Benua macrophytes, coll. K. & T. von Rintelen, 24 Jul.2004; 44 ex. (MZB River, northern arm, 04°13.388'S, 122°6.397'E, loc. 85-05, coll. Cru 1790, n=22; ZMB 29075, n=22, some SEM material), south M. Glaubrecht, K. & T. von Rintelen, 31 May 2005; 1 ex. (ZMB shore, canal between island and mainland, 02°28.46'S, 121°15.83'E, 29010), stream at road Kendari – Lapuko, near Mulyasari, 04°7.34'S, loc. 62-03, on leaf litter, coll. K. & T. von Rintelen, 1 Oct.2003; 122°36.82'E, loc. 103-05, coll. K. & T. von Rintelen, 1 Jun.2005; 24 ex. (MZB Cru 1791, n=11; ZMB 29105, n=13, some SEM 1 ex. (ZMB 29018), stream at Labeala, east of Pundihaha, road material), north shore, 02°26.36'S, 121°19.03'E, loc. 84-03, on leaf Kendari – Kolaka, 03°57.987'S, 122°20.739'E, loc. 77-05, coll. M. litter, coll. K. & T. von Rintelen, 1 Oct.2003; 6 ex. (ZMB 29107, Glaubrecht, K. & T. von Rintelen, 30 May 2005; 1 ex. (ZMB 29338), some SEM material), south shore, Soroako, Salonsa, Pantai Ide, stream in Pruiala, north of Aopa area, 04°3.67'S, 122°6.845'E, 02°30.89'S, 121°20.53'E, loc. 40-03, on mixed substrate, coll. K. loc. 83-05, coll. M. Glaubrecht, K. & T. von Rintelen, 31 May & T. von Rintelen, 17 Sep.2003; 1 ex. (ZMB 29139), north shore, 2005; 1 ex. (ZMB 29339), Simbune River, approx. 1 km northeast 02°29.75'S, 121°25.81'E, loc. 42-03, on rocks, coll. K. & T. von of Raterate, road Kendari – Kolaka, 04°2.326'S, 121°54.204'E, Rintelen, 17 Sept. 2003; 4 ex. (ZMB 29140), south shore, 02°28.5'S, loc. 79-05, coll. M. Glaubrecht, K. & T. von Rintelen, 30 May 121°15.55'E, loc. 139-04, on mixed substrate, coll. K. & T. von 2005; 1 ex. (ZMB 29340), Humbuti River, northwest of Abuki, Rintelen, 24 Jul.2004; 16 ex. (MZB Cru 1792, n=8; ZMB 29189, 03°38.91'S, 121°52.38'E, loc. 78-05, coll. M. Glaubrecht, K. & T. n=8), at small islands, 02°28.458'S, 121°15.57'E, loc. F4-02, on mixed substrate, coll. F. Herder, 2 Nov.2002; 1 ex. (ZMB 29225), von Rintelen, 30 May 2005. north shore, 02°27.28'S, 121°21.21'E, loc. 98-03, on leaf litter, coll. K. & T. von Rintelen, 5 Oct.2003; 4 ex. (ZMB 29227), south Description. – Carapace length 2.3-3.8 mm (n=29). Rostrum shore, 02°27.84'S, 121°13.88'E, loc. 01-05, on macrophytes, coll. (Fig. 11A-E; Table 5) usually broad, reaching near or K. & T. von Rintelen, 1 Jan.2005; 1 ex. (ZMB 29231), south shore, slightly beyond end of scaphocerite, 0.6-1.2 times as long as Soroako, Salonsa, INCO boat house, 02°30.71'S, 121°20.45'E, loc. carapace (n=32), armed dorsally with 14-28 teeth (including 19-03, on rocks, coll. K. & T. von Rintelen, 19 Sep.2003; 6 ex. 4-8 teeth posterior to orbital margin), armed ventrally with (ZMB 29232, n=6 and some juveniles), north shore, 02°28.42'S, 3-7 teeth. Antennal spine situated below inferior orbital 121°24.21'E, loc. 41-03, on leaf litter, coll. K. & T. von Rintelen, angle. Pterygostomial angle broadly rounded. Eyes well 17 Sep.2003; 9 ex. (MZB Cru 1793, n=4; ZMB 29286, n=5, some SEM material), northwest shore, 02°25.742'S, 121°13.797'E, loc. developed, anterior end 0.5-0.6 times length of basal segment 134-04, on leaf litter, coll. K. & T. von Rintelen, 23 Jul.2004; 11 of antennular peduncle (n=6). Antennular peduncle 0.8-1.0 ex. (MZB Cru 1794, n=5; ZMB 29185, n=6), Matano catchment, times as long as carapace (n=6), second segment 1.6-2.1 times river, near mouth at northwest corner of Lake Matano, 02°25.88'S, length of third segment, third segment 0.3-0.4 times length 121°13.08'E, loc. 24-03, on leaf litter, coll. K. & T. von Rintelen, of basal segment. Stylocerite reaching 0.9-1.0 times length 13 Sep.2003. of basal segment of antennular peduncle (n=6). Scaphocerite (Fig. 11H) 3.8-4.8 times as long as wide (n=5). Paratypes (Lake Mahalona) –12 ex. (MZB Cru 1795, n=6; ZMB 29059, n=6), Lake Mahalona (no further details given), loc. F3-02, Sixth abdominal somite 0.5-0.7 times length of carapace substrate unknown, coll. J. Frommen, 1 Nov.2002; 9 ex. (ZMB 29063, n=9 and some juveniles, some SEM material), east shore, (n=15), 1.4-1.8 times as long as fi fth somite (n=15), 0.9-1.0

364 THE RAFFLES BULLETIN OF ZOOLOGY 2009 times length of telson (n=10). Telson (Fig. 11J-K) 2.9-3.5 Incisor process of mandible (Fig. 12A) ending in a row times as long as wide (n=6), distal margin rounded, without of 3-4 small teeth, molar process truncated. Lower lacinia projection, with 3-4 pairs of spinules and 1 pair of dorsolateral of maxillula (Fig. 12B) broadly rounded, upper lacinia spinules; distal end with 3-4 pairs of spines, lateral pair longer elongate, with numerous distinct teeth and setae on inner than intermediate pairs, median pair shortest. Preanal carina margin, palp slender. Upper endites of maxilla (Fig. 12C) (Fig. 11I) with a spine. Uropodal diaeresis (Fig. 11L) with subdivided, palp short, scaphognathite tapering posteriorly 12-13 movable spinules (n=5). with numerous long, curved setae at posterior end. Distal end of palp of fi rst maxilliped (Fig. 12F) triangular, with 5 pairs of pleurobranchs well developed; 3 pairs of a finger-like projection; flagellum of the exopod very arthrobranchs, 2 on third maxillipeds, with second pair elongated, endopod high, not exceeding the fl agellum of strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair exopod in length. Second maxilliped (Fig. 12E) typical. of podobranchs on second maxilliped reduced strongly to Third maxilliped (Fig. 12D) with ultimate segment distinctly a laminate form. Epipod present on fi rst two pereiopods. shorter than penultimate segment.

Fig. 10. Caridina holthuisi from the Malili lake system. A. Distribution (the equal sign roughly marks the geographic boundary between the two genetic clades; compare taxonomic remarks). B. Colour pattern of living animal (not to scale). Pictures courtesy of Chris Lukhaup.

365 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Table 5. Summary of standard morphometric parameters for Caridina holthuisi. parameter range mean ± SD median n cl (mm) 2.3-3.8 2.8 ± 0.4 2.7 29 rl / cl 0.6-1.2 0.9 ± 0.1 0.9 32 n dorsal rostral teeth 14-28 20 ± 3 20 32 n ventral rostral teeth 3-7 5 ± 1 5 32 abds6 / cl 0.5-0.7 0.6 ± 0.1 0.6 15 abds6 / abds5 1.4-1.8 1.6 ± 0.1 1.6 15 abds6 / h tel 0.9-1.0 0.9 ± 0.0 0.9 10 h tel / w tel 2.9-3.5 3.3 ± 0.2 3.4 6 n spines uropodal diaeresis 12-13 13 ± 1 13 5 h ch1 / w ch1 1.8-2.3 2.1 ± 0.2 2.1 18 h ch1 / h ca1 1.1-1.4 1.2 ± 0.1 1.2 17 h ca1 / w ca1 2.0-3.1 2.7 ± 0.3 2.7 13 h ch2 / w ch2 2.3-3.5 2.8 ± 0.3 2.8 18 h ch2 / h ca2 0.7-0.9 0.8 ± 0.1 0.7 22 h ca2 / w ca2 4.3-7.0 5.7 ± 0.9 5.7 18 n spines p3 3-6 4 ± 1 4 5 n spines p5 27-39 34 ± 5 33 5

Chela and carpus of fi rst pereiopod distinctly stouter and pleopod (Fig. 11R) 0.8-0.9 times length of appendix broader than chela and carpus of second pereiopod (Fig. masculina (n=5). 11S-T); chela of fi rst pereiopod 1.8-2.3 times as long as wide (n=18), 1.1-1.4 times length of carpus (n=17); tips of Ovigerous females with 19-25 eggs (n=2 females); egg size fi ngers rounded, without hooks; dactylus 0.9-1.3 times as 0.8-1.0 x 0.5-0.6 mm (n=38, eggs with and without eyes). long as palm (n=9); carpus 2.0-3.1 times as long as wide (n=13), 1.1-1.3 times length of merus (n=9). Chela of second Distribution. – Endemic to the Malili lake system; occurring pereiopod 2.3-3.5 times as long as wide (n=18), 0.7-0.9 times in all three major lakes and in Petea River, widely distributed length of carpus (n=22); tips of fi ngers rounded, without within each lake (Fig. 10B). hooks, dactylus 1.0-1.4 times as long as palm (n=9); carpus 4.3-7.0 times as long as wide (n=18), 1.2-1.5 times as long Biology and ecology. – C. holthuisi is a soft substrate as merus (n=10). dweller, mainly found under dead leaves (leaf litter), but also sporadically on macrophytes. Its colour pattern is similar to Third pereiopod (Fig. 11M,O) slender, dactylus 4.2-5.0 times its substrate, the usually dark brown leaves that can be found as long as wide (terminal spine included, without spines covering the shallow bottom in various shore areas. When of fl exor margin; n=5), terminating in one large claw with disturbed, C. holthuisi rather tries to escape downwards than 3-6 accessory spines on fl exor margin; propodus 8.8-13.5 in other directions to hide under its substrate. When a pile times as long as wide, 2.8-3.8 times as long as dactylus; of dead leaves is sampled with a dip net, specimens usually carpus 4.8-5.6 times as long as wide, 0.6-0.7 times as long accumulate at the bottom of the net. as propodus, 0.5-0.6 times as long as merus; merus 7.2-8.8 times as long as wide, bearing 3-4 strong, movable spines Colour pattern. Ð The body, and often also the appendages on posterior margin of outer surface. too, show a vivid dark brown colour similarly to the brown colour of the species’ leaf substrate (Fig. 10A). Various Fifth pereiopod slender (Fig. 11N,P), dactylus 3.7-6.3 times white-beige markings (usually transversal stripes or a as long as wide (terminal spine included, without spines of dorsal longitudinal stripe) are possible. Eggs are also dark fl exor margin; n=5), terminating in one large claw with 27- brown. 39 accessory spines on fl exor margin; propodus 11.0-15.0 times as long as wide, 2.7-3.1 times as long as dactylus; Etymology. Ð Caridina holthuisi, new species, is named carpus 4.6-5.5 times as long as wide, 0.5 times as long as in honour of L.B. Holthuis as one of the well-known propodus, 0.6-0.7 times as long as merus; merus 6.5-8.5 carcinologist of our time, who also contributed greatly to times as long as wide, bearing 2-3 strong, movable spines our knowledge of the shrimp genus Caridina. on posterior margin of outer surface. Taxonomic remarks. Ð Woltereck (1937a, b) described Endopod of male first pleopod (Fig. 11Q) elongated some specimens from Lake Matano as Caridina opaensis triangular, 1.8-2.5 times as long as proximally wide (n=5), Roux, 1904, and thus mentioned it as the only non-endemic without appendix interna. Appendix interna of male second species in the Malili lake system. Brooks (1950: 169) even

366 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 11. Caridina holthuisi from the Malili lake system and C. opaensis from SE Sulawesi. Cephalothorax and cephalic appendages from: A. Female, MT (ZMB 29286); B. Male, MT (ZMB 29286); C. Woltereck’s drawing of the rostrum (modifi ed from 1937a); D. Female, MT (ZMB 29107); E. Female, TW (ZMB 29303); F. Female, SE Sul (ZMB 29338); G. Female, SE Sul (ZMB 29339). H. Scaphocerite, male, MT (ZMB 29232); I. Preanal carina; J. Telson, female, MT (ZMB 29105); K. Distal end of telson; L. Uropodal diaeresis; M. Third pereiopod, female MT (ZMB 29075); N. Fifth pereiopod; O. Dactylus of third pereiopod; P. Dactylus of fi fth pereiopod; Q. Endopod of male fi rst pleopod, MT (ZMB 29232); R. Appendix masculina of male second pleopod; S. SEM image of chela and carpus of fi rst and second pereiopods, female, MT (ZMB 29286); T. First pereiopod, female (ZMB 29075); U. Second pereiopod. Scale bars: A-B, D-H = 1.0 mm; I-J, M-N, Q-U= 0.5 mm; K-L, O-P = 0.1 mm; C = no scale available.

367 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi discussed the origin of Lake Matano’s fauna based on the n=6, in C. opaensis), and a lower number of accessory spines presumed non-endemism of this species. However, albeit on fl exor margin of dactylus of the third and fi fth pereiopod some fi rst glance similarities between the true C. opaensis (3-6 and 31-39 vs. 6 and 54-64, n=3 in C. opaensis). Roux, 1904 from Southeast Sulawesi and Woltereck’s C. opaensis, i.e. C. holthuisi, new species (Fig. 29F-G), both C. holthuisi slightly resembles C. dennerli, but differs not are morphologically distinct species and Woltereck’s ‘C. only in its substrate preference (leaf litter vs. rocks in C. opaensis’ is here considered as to be C. holthuisi, new dennerli), or colour pattern (compare respective description), species. C. holthuisi can be distinguished from C. opaensis but also by a broader rostrum, a different number of ventral by its generally smaller size (cl 2.3-3.8, mean 2.8 vs. 2.9-4.9, teeth on the rostrum (5-11, median 9 vs. 3-7, median 5), and mean 4.0, n=23 in C. opaensis), a generally longer rostrum distinctly stouter pereiopods in C. holthuisi (for example compared to the carapace length (0.6-1.2, mean 0.9, vs. chela of fi rst pereiopod 1.8-2.3, median 2.1 vs. 2.4-3.8, 0.40.8, mean 0.7, n=25 in C. opaensis), a lower number of median 2.7 in C. dennerli). movable spinules on the uropodal diaeresis (12-13 vs. 14-19,

Fig. 12. Caridina holthuisi from the Malili lake system. A. Mandible (ZMB 29286); B. Maxillula; C. Maxilla; D. third maxilliped; E. second maxilliped; F. fi rst maxilliped. Scale bars: A-F = 1mm.

368 THE RAFFLES BULLETIN OF ZOOLOGY 2009

C. holthuisi can resemble C. masapi, but the rostrum in C. [Mahalona], Lake Matanno [Matano] at Bonti, Lake Matanno masapi usually differs by a more or less dense denticulation at Soroako). on the dorsal margin, and a straighter and broader shape (vs. Caridina lanceolata – Woltereck, 1937b: 307, fi g. 11; Chace, 1997: usually with a conspicuous unarmed gap on the dorsal margin 12; Fernandez-Leborans et al., 2006a: 1, fi g. 24; 2006b: 1985, Table I; Roy et al., 2006: 1090; von Rintelen et al., 2007b: and a more slender and cambered shape in C. masapi). 262, fi g. 2b; 2007b: 4, fi g. 2, 2008: 2244, Figs. 1, 4, Tables 1, 2; Cai et al., 2009: 15, Figs. 1-2 (type locality of neotype: Besides the morphological differences, C. holthuisi is Lake Matano, Mengonuwai). genetically distinct from C. opaensis (Fig. 63). All sequenced Cardina lanceolata Ð Brooks, 1950: 168 (erroneous spelling). specimens of C. opaensis from and around the type locality are not closely related to any of the ancient lake species Material examined. Ð Lake Matano: 10 ex. (ZMB 29021, some (compare von Rintelen et al., in review). On the other hand, SEM material), north shore, 02°29.75'S, 121°25.81'E, loc. 42- all specimens of C. holthuisi appear within the Malili clade. 03, coll. K. & T. von Rintelen, 17 Sep.2003; 112 ex. (MZB Cru Therefore, they must be regarded as truly endemic to the 1738, n=55; ZMB 29070, n=57), south shore, at small islands, 02°28.458'S, 121°15.57'E, loc. F4-02, mixed substrate, coll. lakes. However, within the Malili clade, C. holthuisi is not F. Herder, 2 Nov.2002; 5 ex. (ZMB 29082), northwest corner, monophyletic, but appears in two allopatric clades (Figs. 02°27.71'S, 121°13.03'E, loc. 102-03, on rocks in deeper water, 10B, 63-64). The existence of two cryptic species is therefore coll. K. & T. von Rintelen, 7 Oct.2003; north shore, 02°26.36'S, possible despite the fact that morphological differences have 121°19.03'E, loc. 84-03, on wood (ZMB 29090, n=3), coll. K. not been observed so far. & T. von Rintelen, 1 Oct.2003; 21 ex. (MZB Cru 1739, n=10, ZMB 29110; n=11), south shore, near cave entrance, 02°29.85'S, 121°18.66'E, loc. 60-03, on rocks in deeper water, coll. K. & T. von Caridina lanceolata Woltereck, 1937a Rintelen, 24 Sep.2003; 31 ex. (MZB Cru 1740, n=14, ZMB 29111, (Figs. 13-14, Table 6) n=17), south shore, west of small islands, 02°28.5'S, 121°15.55'E, loc. 82-03, on macrophytes, coll. K. & T. von Rintelen, 1 Oct.2003; 129 ex. (MZB Cru 1741a, n=35; ZMB 29120a, n=10 and MZB Caridina lanceolata Woltereck, 1937a: 224, Figs. I.7a-c, pls. Cru 1742b, n=50 ; ZMB 29120b, n=34, some SEM material), north 3,6 (type locality: Lake Towuti at Lingkona, Lake Mahalone

Fig. 13. Caridina lanceolata from the Malili lake system. A. Distribution. B. Colour pattern of living animal (not to scale). Picture courtesy of Chris Lukhaup.

369 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Table 6. Summary of standard morphometric parameters for Caridina lanceolata. parameter range mean ± SD median n cl (mm) 2.2-4.0 3.0 ± 0.4 3.1 129 rl / cl 1.5-2.3 1.9 ± 0.2 1.9 120 n dorsal rostral teeth 8-19 14 ± 2 13 124 n ventral rostral teeth 4-13 7 ± 2 7 124 abds6 / cl 0.8-1.1 0.9 ± 0.0 1.0 129 abds6 / abds5 1.4-2.3 2.0 ± 0.1 2.0 33 abds6 / h tel 1.0-1.9 1.3 ± 0.1 1.3 101 h tel / w tel 3.3-3.7 3.5 ± 0.1 3.5 6 n spines uropodal diaeresis 7-9 8 ± 1 8 5 h ch1 / w ch1 1.9-3.5 2.6 ± 0.4 2.6 35 h ch1 / h ca1 0.8-1.4 1.1 ± 0.1 1.1 127 h ca1 / w ca1 2.4-5.3 3.6 ± 0.7 3.7 35 h ch2 / w ch2 2.1-6.7 3.7 ± 0.8 3.7 35 h ch2 / h ca2 0.5-1.6 0.7 ± 0.1 0.6 127 h ca2 / w ca2 5.4-9.9 8.3 ± 1.2 8.6 35 n spines p3 4-6 5 ± 1 6 5 n spines p5 28-35 31 ± 3 31 5 shore, 02°28.42'S, 121°24.21'E, loc. 41-03, (a) on wood, (b) on east shore, 02°34.54'S, 121°30.48'E, loc. 55-03, on Ottelia, coll. macrophytes, coll. K. & T. von Rintelen, 17 Sep.2003; 2 ex. (ZMB K. & T. von Rintelen, 23 Sep.2003; 12 ex. (MZB Cru 1750, n=6; 29160), west shore, 02°26.828'S, 121°12.988'E., loc. 135-04, on ZMB 29042, n=6, some SEM material), south shore, 02°36.93'S, wood, coll. K. & T. von Rintelen & A. Wessel, 23 Jul.2004; 20 ex. 121°30.02'E, loc. 57-03, on Ottelia, coll. K. & T. von Rintelen, (MZB Cru 1743, n=11; ZMB 29162, n=9), south shore, 02°27.84'S, 23 Sep.2003; 18 ex. (MZB Cru 1751, n=9; ZMB 29236; n=9, 121°13.88'E, loc. 63-03, on mixed substrate, coll. K. & T. von some SEM material), east shore, 02°34.217'S, 121°30.681'E, loc. Rintelen, 24 Sep.2003; 26 ex. (MZB Cru 1744, n=13; ZMB 29164, 147-04, on macrophytes, coll. K. & T. von Rintelen, 3 Aug.2004; n=13, some SEM material), east shore, outlet bay, at Petea outlet, 31 ex. (MZB Cru 1752, n=15; ZMB 29250, n=16), south shore, 02°32.11'S, 121°28.69'E, loc. 44-03, on macrophytes, coll. K. & 02°36.982'S, 121°30.078'E, loc. 45-04, on wood, coll. M. Glaubrecht T. von Rintelen, 18 Sep.2003; 40 ex. (MZB Cru 1745, n=20; ZMB & T. von Rintelen, 26 Mar.2004; 1 ex. (ZMB 29336), north shore, 29190, n=20), north shore, 02°27.28'S, 121°21.21'E, loc. 98-03, on at cape, 02°34.71'S, 121°29.144'E, loc. 148-04, on mixed substrate, mixed substrate, coll. K. & T. von Rintelen, 5 Oct.2003; 2 ex. (ZMB coll. K. & T. von Rintelen, 3 Aug.2004; 15 ex. (MZB Cru 1753), 29193), east shore, just south of entrance to outlet bay, 02°31.54'S, east shore, estuary of Ponsoa River, 02°35.101'S, 121°30.681'E, 121°27.0'E, loc. 43-03, on rocks in shallow water, coll. K. & T. loc. 146-04, on Ottelia, coll. P. Koller, K. & T. von Rintelen, 3 von Rintelen, 18 Sep.2003; 2 ex. (ZMB 29194), southwest shore, Aug.2004; 8 ex. (ZMB 29115), Tominanga River, approx. 2.2 at Cape Nikomene, 02°32.24'S, 121°24.76'E, loc. 46-03, on rocks, km north of Lake Towuti, 02°36.5'S, 121°31.78'E, loc. 58-03, on coll. K. & T. von Rintelen, 18 Sep.2003; 7 ex. (ZMB 29237), north macrophytes, coll. K. & T. von Rintelen, 23 Sep.2003. shore, 02°25.67'S, 121°16.54'E, loc. 65-03, on leaf litter, coll. K. & T. von Rintelen, 25 Sep.2003; 18 ex. (ZMB 29249), south shore, Lake Towuti – 69 ex. (MZB Cru 1754, n=59; ZMB 29029, canal between island and mainland, 02°28.46'S, 121°15.83'E, loc. n=10, some SEM material), south shore, approx. 100 m offshore, 62-03, on mixed substrate, coll. K. & T. von Rintelen, 1 Oct.2003; 02°56.27'S, 121°23.67'E, loc. 75-03, on Ottelia, coll. K. & T. 14 ex. (ZMB 29321), south shore, 02°28.461'S, 121°15.591'E, loc. von Rintelen, 28 Sep.2003; 2 ex. (ZMB 29030), west shore, 137-04, on macrophytes, coll. K. & T. von Rintelen, 24 Sep.2004; 02°48.526'S, 121°25.044'E, loc. 120-04, on wood, coll. K. & T. 2 ex. (ZMB 29322), south shore, at small islands, 02°28.476'S, von Rintelen & A. Wessel, 29 Jul.2004; 141 ex. (MZB Cru 1755, 121°15.64'E, loc. 138-04, on wood, coll. K. & T. von Rintelen & A. n=123; ZMB 29032, n=18, some SEM material), west shore, outlet Wessel, 24 Jul.2004; 9 ex. (ZMB 29323), south shore, 02°27.85'S, bay, east of Cape Kombe, 02°48.08'S, 121°23.05'E, loc. 53-03, on 121°13.87'E., loc. 125-04, on rocks in deeper water, coll. P. Koller mixed substrate, coll. K. & T. von Rintelen, 21 Sep.2003; 34 ex. & K. von Rintelen, 1 Aug.2004; 1 ex. (MZB Cru 1746), east shore, (MZB Cru 1756, n=24; ZMB 29033a, n=8 and ZMB 29033b, n=2, south bay, 02°32.77'S, 121°26.71'E, loc. 45-03, on rocks, coll. K. some SEM material), southwest shore, Cape Sioloya, 02°50.7'S, & T. von Rintelen, 18 Sep.2003; 1 ex. (ZMB 29188), Petea River, 121°26.32'E, loc. 77-03, (MZB and ZMB a) pelagic, (b) on wood, 02°32.64'S, 121°29.51'E, loc. 101-03, on leaf litter, coll. K. & T. coll. K. & T. von Rintelen, 28 Sep.2003; 3 ex. (ZMB 29081), east von Rintelen, 6 Oct.2003; 15 ex. (MZB Cru 1762, n=8; ZMB shore, south of Cape Tomeraka, 02°44.47'S, 121°37.53'E, loc. 29279, n=7), Petea River, 02°32.672'S, 121°30.137'E, loc. F4-04, 70-03, on rocks, coll. K. & T. von Rintelen, 9 Oct.2003; 206 ex. substrate unknown, coll. F. Herder, 25 Mar.2004. (MZB Cru 1757a, n=22; ZMB 29093a, n=11 and MZB Cru 1758b, n=92; ZMB 29093b, n=81, some SEM material), southwest shore, Lake Mahalona – 41 ex. (MZB Cru 1747a, n=2; ZMB 29022a, west of Cape Tetetu, 02°454.13'S, 121°23.78'E, loc. 76-03, (a) on n=21 and MZB Cru 1748b, n=9; ZMB 29022b, n=9, some SEM wood, (b) pelagic, coll. K. & T. von Rintelen, 28 Sep.2003; 10 ex. material), northwest shore, 02°34.72'S, 121°29.12'E, loc. 56-03, (ZMB 29094, some SEM material), northeast shore, at Cape Noote, on (a) on wood, (b) on macrophytes, coll. K. & T. von Rintelen, 02°39.751'S, 121°39.195'E, loc. 117-04, on wood, coll. K. & T. 23 Sep.2003; 22 ex. (MZB Cru 1749, n= 11; ZMB 29041, n=11), von Rintelen, 28 Jul.2004; 7 ex. (ZMB 29112), Loeha Island, south

370 THE RAFFLES BULLETIN OF ZOOLOGY 2009 shore, 02°46.85'S, 121°32.86'E, loc. 96-03, on macrophytes, coll. 3.3-3.7 times as long as wide (n=6), distal margin rounded, K. & T. von Rintelen, 4 Oct.2003; 9 ex. (ZMB 29113), east shore, without projection, with 3-5 pairs of spinules and 1 pair of off Beau village, 02°48.99'S, 121°33.64'E, loc. 71-03, on Ottelia, dorsolateral spinules; distal end with 4 pairs of spines, lateral coll. K. & T. von Rintelen, 27 Sep.2003; 55 ex. (MZB Cru 1759, pair distinctly longer than intermediate pairs, median pair n=27; ZMB 29114, n=28), west shore, outlet bay, west of Cape shortest. Preanal carina (Fig. 14E) with a spine. Uropodal Tokaluku, 02°47.32'S, 121°23.38'E, loc. 52-03, on macrophytes, coll. K. & T. von Rintelen, 21 Sep.2003; 1 ex. (ZMB 29128), diaeresis (Fig. 14D) with 7-9 movable spinules (n=5). west shore, at entrance to outlet bay, Cape Larona, 02°48.43'S, 121°24.75'E, loc. 73-03, on wood, coll. K. & T. von Rintelen, 27 5 pairs of pleurobranchs well developed; 3 pairs of Sep.2003; (ZMB 29158, few juveniles), north shore, west of Cape arthrobranchs, 2 on third maxillipeds, with second pair Manu, 02°41.67'S, 121°36.85'E, loc. 69-03, on macrophytes, coll. strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair K. & T. von Rintelen, 27 Sep.2003; 4 ex. (ZMB 29161), Larona of podobranchs on second arthrobrach maxillipeds reduced River, close to outlet bay, 02°45.8'S, 121°20.8'E, loc. 51-03, on strongly to a laminate form. Epipods only present on fi rst two macrophytes, coll. K. & T. von Rintelen, 21 Sep.2003; 13 ex. (MZB pereiopods. Mouthparts as described by Cai et al. (2009). Cru 1761, n=6; ZMB 29163, n=7), Larona River, close to outlet bay, 02°45.6'S, 121°20.12'E, loc. 50-03, on macrophytes, coll. K. & T. von Rintelen, 20 Sep.2003; (ZMB 29166, few juveniles), east Chela and carpus of fi rst pereiopod distinctly stouter and shore, 02°52.79'S, 121°31.18'E, loc. 72-03, on Ottelia, coll. K. & broader than chela and carpus of second pereiopod (Fig. T. von Rintelen, 27 Sep.2003; 7 ex. (ZMB 29167), Loeha Island, 14M-O); chela of fi rst pereiopod 1.9-3.5 times as long as south shore, 02°47.22'S, 121°33.68'E, loc. 91-03, on Ottelia, coll. wide (n=35), 0.8-1.4 times length of carpus (n=127); tips K. & T. von Rintelen, 2 Oct.2003; 12 ex. (ZMB 29181), Loeha of fi ngers rounded, without hooks; dactylus 1.2-1.5 times Island, west shore, 02°45.5'S, 121°31.06'E, loc. 95-03, on rocks, as long as palm (n=7); carpus 2.4-5.3 times as long as wide coll. K. & T. von Rintelen, 4 Oct.2003; 23 ex. (ZMB 29182, some (n=35), 1.2-1.4 times length of merus (n=5). Chela of second SEM material), north shore, bay east of Cape Bintu, 02°39.48'S, pereiopod 2.1-6.7 times as long as wide (n=35), 0.5-1.6 times 121°33.25'E, loc. 68-03, on rocks, coll. K. & T. von Rintelen, 26 length of carpus (n=127); tips of fi ngers rounded, without Sep.2003; (ZMB 29183, few juveniles) west shore, north of Cape Wasupute, 02°46.9'S, 121°27.94'E, loc. 78-03, on rocks, coll. K. hooks, dactylus 1.2-1.7 times as long as palm (n=7); carpus & T. von Rintelen, 28 Sep.2003; 4 ex. (ZMB 29314), west shore, 5.4-9.9 times as long as wide (n=35), 1.5-1.6 times as long outlet bay, 02°47.142'S, 121°23.63'E, loc. 11-05, on mixed substrate, as merus (n=5). coll. K. & T. von Rintelen, 9 Jan.2005; 4 ex. (ZMB 29315), west shore, Cape Bakara, 02°40.771'S, 121°26.11'E, loc. 144-04, on Third pereiopod (Fig. 14H,K) slender, dactylus 4.5-5.4 times mixed substrate, coll. K. & T. von Rintelen, 26 Jul.2004; 12 ex. as long as wide (terminal spine included, without spines of (ZMB 29317), west shore, west of Cape Timbalo, 02°42.631'S, fl exor margin; n=5), terminating in one large claw with 4-6 121°26.389'E, loc. 145-04, on wood, coll. K. & T. von Rintelen, 26 accessory spines on fl exor margin; propodus 12.3-18.8 times Jul.2004; 4 ex. (ZMB 29318), northwest shore, south of Timampu, as long as wide, 3.4-4.5 times as long as dactylus; carpus 02°39.466'S, 121°25.859'E, loc. 140-04, on macrophytes, coll. K. & T. von Rintelen, 25 Jul.2004; 43 ex. (MZB Cru 1760, n= 28; 5.8-6.8 times as long as wide, 0.5 times as long as propodus, ZMB 29319, n=15), outlet bay, at Cape Kombe, 02°48.083'S, 0.5 times as long as merus; merus 10.5-11.4 times as long 121°23.049'E, loc. 118-04, (MZB) on macrophytes, (ZMB) on as wide, bearing 3-4 strong, movable spines on posterior wood, coll. K. & T. von Rintelen, 29 Jul.2004; 8 ex. (ZMB 29320), margin of outer surface. northwest shore, 02°40.897'S, 121°25.015'E, loc. 143-04, on wood (Pandanus), coll. K. & T. von Rintelen, 25 Jul.2004. Fifth pereiopod slender (Fig. 14I,L), dactylus 4.0-6.2 times as long as wide (terminal spine included, without spines of Description. Ð Carapace length 2.2-4.0 mm (n=129). Rostrum fl exor margin; n=5), terminating in one large claw with 28-35 (Fig. 14A-C; Table 6) very long, slender and always strongly accessory spines on fl exor margin; propodus 11.3-21.3 times upturned, reaching far beyond end of scaphocerite, 1.5-2.3 as long as wide (n=5), 3.3-5.3 times as long as dactylus; times as long as carapace (n=120), armed dorsally with 8- carpus 5.0-6.3 times as long as wide, 0.5 times as long as 19 teeth (including 1-3 teeth posterior to orbital margin), propodus, 0.5-0.6 times as long as merus; merus 8.3-11.5 approx. anterior third to half unarmed, usually with 1-4 times as long as wide, bearing 2-3 strong, movable spines subapical teeth, sometimes subapical teeth absent, armed on posterior margin of outer surface. ventrally with 4-13 teeth (n=124). Antennal spine situated below inferior orbital angle. Pterygostomial angle broadly Endopod of male fi rst pleopod (Fig. 14P) elongated triangular, rounded. Eyes well developed, anterior end 0.6-0.7 times 1.4-2.5 times as long as proximally wide (n=5), without length of basal segment of antennular peduncle (n=5). appendix interna. Appendix interna of male second pleopod Antennular peduncle 0.9-1.0 times as long as carapace (n=5), (Fig. 14Q) 0.9-1.0 times length of appendix masculina second segment 2.0-2.4 times length of third segment, third (n=5). segment 0.2-0.3 times length of basal segment. Stylocerite reaching 0.87-0.9 times length of basal segment of antennular Ovigerous females with 15-69 eggs (n=27 females); egg peduncle (n=5). Scaphocerite (Fig. 14F) 4.8-5.4 times as size 0.6-0.9 x 0.4-0.6 mm (n=701, eggs with and without long as wide (n=5). eyes).

Sixth abdominal somite 0.8-1.1 times length of carapace Distribution. Ð Endemic to the Malili lake system, widely (n=129), 1.4-2.3 times as long as fi fth somite (n=33), 1.0- distributed and abundant in Lake Matano, Lake Mahalona, 1.9 times length of telson (n=101). Telson (Fig. 14G,J) Lake Towuti, and connecting rivers, i.e. Larona (close to the

371 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 14. Caridina lanceolata from the Malili lake system. A. Cephalothorax and cephalic appendages, female (ZMB 29032); B. Rostrum variability (ZMB 29033a); C. Woltereck’s drawings of the rostrum, from several lakes (modifi ed from 1937a); D. Uropodal diaeresis, female (ZMB 29032); E. Preanal carina, male (ZMB 29093a), F. Scaphocerite; G. Telson, female (ZMB 29032); H. Third pereiopod, female (ZMB 29093b); I. Fifth pereiopod; J. Distal end of telson, female (ZMB 29032); K. Dactylus of third pereiopod, female (ZMB 29093b); L. Dactylus of fi fth; M. fi rst pereiopod, female (ZMB 29032); N. Second pereiopod; O. SEM image of chela and carpus of fi rst and second pereiopods; P. Endopod of male fi rst pleopod (ZMB 29093a); Q. Appendix masculina of male second pleopod. Scale bars: A-B, F = 1.0 mm; E, G-I, M-Q = 0.5 mm; D, J-L = 0.1 mm; C = no scale available.

372 THE RAFFLES BULLETIN OF ZOOLOGY 2009 outlet of Lake Towuti), Petea, and Tominanga (Fig. 13A). As Caridina lingkonae Woltereck, 1937a these rivers are rather an extension of the lakes themselves (Figs. 15-17, Table 7) (albeit with currents), C. lanceolata is regarded here, in contrast to C. masapi, as a typical lacustrine species. Caridina Lingkonae Woltereck, 1937a: 218, fig. I.1, pls. 3,6 (type locality: Lake Towuti at Loéha Island and at Lingkona Biology and ecology. Ð C. lanceolata occurs on various [Lengkona]). kinds of substrates, except sponges, that are available in Caridina lingkonae – Woltereck, 1937b: 299, fi g. 6; Chace, 1997: 13; von Rintelen et al., 2008: 2244, Table 1. the Malili lakes (rocks from gravel to boulders, wood, leaf Cardina lingkonae – Brooks, 1950: 168 (erroneous spelling). litter, different kinds of macrophytes, and in pelagic swarms), Caridina linkonae – Fernandez-Leborans et al., 2006b: 1985, Table and down to a depth of approx. 10 m. When disturbed, I (erroneous spelling). C. lanceolata makes characteristic abrupt movements in all directions or simply keeps still in midwater. It often Material examined. Ð Neotype: ovigerous female (cl. 4.1 mm)(MZB occurs syntopically, i.e. on the same substrate, with other Cru. 1554), Lake Towuti, west shore, at entrance to outlet bay, species, for example with C. tenuirostris on wood in Lake Cape Larona, 02°48.43'S, 121°24.75'E, loc. 73-03, pelagic, coll. Towuti and Lake Mahalona. It is the only wood dweller in K. & T. von Rintelen, 27 Sep.2003. Lake Matano and often the only shrimp on macrophytes Others from Lake Towuti: 184 ex. (MZB Cru 1763, n=149; ZMB surrounded by sand or mud, e.g. on the basal parts of the 29076, n=35, some SEM material), west shore, at entrance to outlet water plant Ottelia. bay, Cape Larona, 02°48.43'S, 121°24.75'E, loc. 73-03, pelagic, coll. K. & T. von Rintelen, 27 Sep.2003; 18 ex. (MZB Cru 1764, Colour pattern. Ð Body and appendages are transparent n=9; ZMB 29235, n=9), southwest shore, west of Cape Tetetu, throughout, with a reddish pigmentation caused by several 02°54.13'S, 121°23.78'E, loc. 76-03, pelagic, coll. K. & T. von red, sometimes yellowish-greenish, dots or spots (Fig. 13B). Rintelen, 28 Sep.2003; 1 ex. (ZMB 29239), east shore, south of Ovigerous females were observed to bear green eggs. Cape Tomeraka, 02°44.47'S, 121°37.53'E, loc. 70-03, on rocks, coll. K. & T. von Rintelen, 9 Oct.2003; 1 ex. (ZMB 29282), west shore, Taxonomic remarks. Ð Cai et al. (2009: 19) designated a Cape Larona, 02°48.526'S, 121°25.044'E, loc. 120-04, boulders in deeper water, coll. K. & T. von Rintelen, 29 Jul.2004; 3 ex. neotpye for C. lanceolata: “Specimens of Woltereck (1937a, (ZMB 29283), west shore, west of Cape Timbalo, 02°42.631'S, b) are no longer extant […]. As all new species described 121°26.389'E, loc. 145-04, on mixed substrate, coll. K. & T. von by Woltereck are morphologically close to each other and Rintelen, 26 Jul.2004; 1 ex. (ZMB 29287), outlet bay, at Cape to stabilize the taxonomic status of those species, neotypes Kombe, 02°48.083'S, 121°23.049'E, loc. 118-04, on boulders in are designated if specimens are available from the recent deeper water, coll. K. & T. von Rintelen, 29 Jul.2004; 15 ex. (MZB collections. A neotype from Lake Towuti is designated here Cru 1765, n=7; ZMB 29302, n=8), northeast shore, at Lengkona, (1 male, cl 2.9 mm, ZRC, Lake Matano, south coast)”. 02°40.483'S, 121°41.382'E, loc. 116-04, on mixed substrate, coll. K. & T. von Rintelen, 28 Jul.2004; 3 ex. (ZMB 29304), Loeha Island, C. lanceolata can easily be distinguished from all other ancient west shore, 02°45.5'S, 121°31.06'E, loc. 951-03, on rocks, coll. K. & T. von Rintelen, 4 Oct.2003; 1 ex. (ZMB 29316) , northeast shore, lake species by the characteristic shape and denticulation of at Cape Noote, 02°39.751'S, 121°39.195'E, loc. 117-04, pelagic, the rostrum, which is already visible in juveniles: strongly coll. K. & T. von Rintelen, 28 Jul.2004; 3 ex. (MZB Cru 1766), upturned with approximately anterior third to half unarmed west shore, outlet bay, 02°46.277'S, 121°21.83'E, loc. 02-05, on and usually with 1-4 subapical teeth. The arrangement of sponge, coll. K. & T. von Rintelen, 3 Jan.2005; 7 ex. (MZB Cru rostral teeth slightly resembles C. tenuirostris, but this species 1767), east shore, off Beau village, 02°48.99'S, 121°33.64'E, loc. has a distinctly more slender rostrum, a higher number of 71-03, on Ottelia, coll. K. & T. von Rintelen, 27 Sep.2003. ventral teeth (10-24, median 15 vs. 4-13, median 7 in C. lanceolata), and subapical teeth are always absent. Also, C. Others from Lake Mahalona: 1 ex. (ZMB 29208), east shore, at lanceolata differs from all other species by a distinctly longer mouth of Petea River, 02°34.54'S, 121°30.48'E, loc. 55-03, on leaf litter, coll. K. & T. von Rintelen, 23 Sep.2003. sixth abdominal somite compared to the carapace length (0.8-1.1, median 1.0 vs. shorter in all other species). Description. Ð Carapace length 2.3-4.5 mm (n=46). Rostrum (Fig. 16A-B; Table 7) long, reaching beyond end of Roy et al. (2006) hint at the possibility that C. lanceolata scaphocerite, proximal part typically triangular, 1.0-1.6 times might comprise cryptic species, but a recent study by von as long as carapace (n=46), armed dorsally with 17-29 teeth Rintelen et al. (in review) does not support this hypothesis. (including 3-5 teeth posterior to orbital margin), anteriorly Although there are genetic differences between allopatric less densely spaced, armed ventrally with 7-18 teeth. Antennal populations from the three major lakes of the Malili system, spine situated below inferior orbital angle. Pterygostomial C. lanceolata is here regarded as a valid taxon without angle broadly rounded. Eyes well developed, anterior the need of further taxonomic subdivision. C. lanceolata end 0.6-0.7 times length of basal segment of antennular is genetically distinct from all other ancient lakes species peduncle (n=5). Antennular peduncle 0.9-1.2 times as long (Figs. 63-64), and the clade only consisting of C. lanceolata as carapace (n=5), second segment 1.7-2.0 times length of specimens even represents a single colonization event of the third segment, third segment 0.3-0.4 times length of basal Malili lakes (Fig. 63). segment. Stylocerite reaching 0.8-0.9 times length of basal segment of antennular peduncle (n=5). Scaphocerite (Fig. 16F) 4.1-5.3 times as long as wide (n=5).

373 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Sixth abdominal somite 0.7-0.9 times length of carapace fl agellum of the exopod very short, endopod high, distinctly (n=46), 1.6-1.9 times as long as fi fth somite (n=20), 1.0- exceed the fl agellum of exopod in length. Second maxilliped 1.3 times length of telson (n=26). Telson (Fig. 16D,K) (Fig. 17E) typical. Third maxilliped (Fig. 17D) with ultimate 3.4-3.6 times as long as wide (n=5), distal margin rounded, segment distinctly shorter than penultimate segment. without projection, with 3-4 pairs of spinules and 1 pair of dorsolateral spinules; distal end with 4 pairs of spines, lateral First and second pereiopod very slender, chela and carpus pair distinctly longer than intermediate pairs, median pair of fi rst pereiopod distinctly stouter and broader than chela shortest. Preanal carina (Fig. 16E) with a spine. Uropodal and carpus of second pereiopod (Fig. 16N-P); chela of fi rst diaeresis (Fig. 16C) with 9-11 movable spinules (n=5). pereiopod 3.0-4.1 times as long as wide (n=20), 0.9-1.1 times length of carpus (n=46); tips of fi ngers rounded, without 5 pairs of pleurobranchs well developed; 3 pairs of hooks; dactylus 1.7-1.9 times as long as palm (n=5); carpus arthrobranchs, 2 on third maxillipeds, with second pair 4.4-5.0 times as long as wide (n=20), 1.3-1.4 times length strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair of merus (n=5). Chela of second pereiopod 4.2-5.6 times as of podobranchs on second maxilliped reduced strongly to a long as wide (n=20), 0.6-0.8 times length of carpus (n=46); laminate form. Epipod reduced or absent from fi rst pereiopod. tips of fi ngers rounded, without hooks, dactylus 1.4-1.6 times Incisor process of mandible (Fig. 17A) ending in a row as long as palm (n=5); carpus 7.9-10.7 times as long as wide of small teeth, molar process truncated. Lower lacinia of (n=20), 1.6-1.7 times as long as merus (n=5). maxillula (Fig. 17B) broadly rounded, upper lacinia elongate, with numerous distinct teeth on inner margin, palp slender. Third pereiopod (Fig. 16G,I) slender, dactylus 4.3-5.5 times Upper endites of maxilla (Fig. 17C) subdivided, palp short, as long as wide (terminal spine included, without spines scaphognathite tapering posteriorly with numerous long, of fl exor margin; n=5), terminating in one large claw with curved setae at posterior end. Distal end of palp of fi rst 1-3 accessory spines on fl exor margin; propodus 13.2-17.0 maxilliped (Fig. 17F) triangular, with a fi nger-like projection; times as long as wide, 3.9-4.9 times as long as dactylus;

Fig. 15. Caridina lingkonae from the Malili lake system. A. Distribution. B. Colour pattern of living animal (not to scale). Picture courtesy of Chris Lukhaup.

374 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 7. Summary of standard morphometric parameters for Caridina lingkonae. parameter range mean ± SD median n cl (mm) 2.3-4.5 3.5 ± 0.6 3.6 46 rl / cl 1.0-1.6 1.3 ± 0.1 1.2 46 n dorsal rostral teeth 17-29 22 ± 3 22 46 n ventral rostral teeth 7-18 12 ± 2 12 46 abds6 / cl 0.7-0.9 0.8 ± 0.1 0.8 46 abds6 / abds5 1.6-1.9 1.8 ± 0.1 1.8 20 abds6 / h tel 1.0-1.3 1.1-0.1 1.1 26 h tel / w tel 3.4-3.6 3.5 ± 0.1 3.5 5 n spines uropodal diaeresis 9-11 10 ± 1 10 5 h ch1 / w ch1 3.0-4.1 3.5 ± 0.3 3.5 20 h ch1 / h ca1 0.9-1.1 1.0 ± 0.1 1 .0 46 h ca1 / w ca1 4.4-5.0 4.7-0.2 4.7 20 h ch2 / w ch2 4.2-5.6 4.8 ± 0.3 4.8 20 h ch2 / h ca2 0.6-0.8 0.7 ± 0.0 0.7 46 h ca2 / w ca2 7.9-10.7 9.6 ± 0.7 9.6 20 n spines p3 1-3 2 ±1 1 5 n spines p5 17-42 33 ±10 36 5 carpus 5.3-5.9 times as long as wide, 0.5 times as long as lanceolata was also found in occasionally pelagic swarms, propodus, 0.4-0.5 times as long as merus; merus 10.5-12.2 but the majority of specimens of that species occurred in times as long as wide, bearing 3-4 strong, movable spines the littoral on various kind of substrate. When disturbed, it on posterior margin of outer surface. tries to escape in all directions.

Fifth pereiopod slender (Fig. 16H,J), dactylus 3.5-5.6 times Colour pattern. Ð C. lingkonae has a translucent reddish as long as wide (terminal spine included, without spines of body colouration throughout, similarly to C. lanceolata, fl exor margin; n=5), terminating in one large claw with 17- but more pronounced (Fig. 15B). Ovigerous females bear 42 accessory spines on fl exor margin; propodus 14.0-19.3 green eggs. times as long as wide, 4.3-5.5 times as long as dactylus; carpus 5.3-6.1 times as long as wide, 0.4-0.6 times as long Taxonomic remarks. Ð C. lingkonae might be confused with as propodus, 0.5-0.6 times as long as merus; merus 10.0-12.4 C. lanceolata in the fi eld, especially when occurring as a times as long as wide, bearing 2-5 strong, movable spines pelagic swarm, but a generally stouter body and the typical on posterior margin of outer surface. triangular shape of the rostrum (vs. not triangular, but longer and more slender in C. lanceolata) are characteristic for this Endopod of male fi rst pleopod (Fig. 16L) elongated triangular, species. C. lingkonae can further be distinguished by the 2.0-2.5 times as long as proximally wide (n=5), without dorsal denticulation of the rostrum (17-29 continuous teeth appendix interna. Appendix interna of male second pleopod vs. 8-19 teeth including an unarmed gap in C. lanceolata) and (Fig. 16M) 0.8-0.9 times length of appendix masculina a shorter sixth abdominal segment compared to the carapace (n=5). length (0.7-0.9, median 0.8 vs. 0.8-1.1, median 1.0 in C. lanceolata). The typical triangular shape of the proximal Ovigerous females with 30-32 eggs (n=3 females); egg size part of the rostrum (best visible transilluminated), and its 0.7-1.0 x 0.4-0.6 mm (n=90, eggs with and without eyes). dense dorsal and ventral denticulation in C. lingkonae, has already been mentioned by Woltereck (1937a: 218,b: 299). A Distribution. Ð Endemic to the Malili lakes, widely distributed similarly triangular shape is pronounced in C. profundicola, in Lake Towuti, a single specimen was caught in Lake but this species differs from C. lingkonae by a distinctly Mahalona (Fig. 15A). more slender and also longer rostrum compared to carapace length (1.4-2.8, median 1.9 vs. 1.0-1.6, median 1.2 in C. Biology and ecology. Ð Caridina lingkonae was already lingkonae) and a higher number of ventral teeth (13-24, mentioned as littoral and pelagic by Woltereck (1937a: 229) median 20 vs. 7-18, median 12 in C. lingkonae). C. lingkonae and Brooks (1950: 168). The majority of the specimens has similarly slender pereiopods than C. profundicola and caught between 2003 and 2004 were found in huge pelagic C. spinata that further distinguish C. lingkonae from all swarms similarly to those of C. ensifera from Lake Poso. other species. Furthermore, C. lingkonae differs from C. Although it was likewise found sporadically on other spinata by the shape of the rostrum and less spines on the substrates (e.g. rocks or leaf litter), C. lingkonae is here uropodal diaeresis; 9-11, median 10 vs. 12-16, median 14 regarded as a typical pelagic species. In comparison, C. in C. spinata).

375 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 16. Caridina lingkonae from the Malili lake system. A. Cephalothorax and cephalic appendages, female (ZMB 29076); B. Woltereck’s drawings of the rostrum, Lake Towuti (modifi ed from 1937a); C. Uropodal diaeresis, female (ZMB 29076); D. Telson; E. Preanal carina, male (ZMB 29076), F. Scaphocerite; G. Third pereiopod, female (ZMB 29076); H. Fifth pereiopod; I. Dactylus of third pereiopod; J. Dactylus of fi fth pereiopod; K. Distal end of telson; L. Endopod of male fi rst pleopod (ZMB 29076); M. Appendix masculina of male second pleopod; N. SEM image of chela and carpus of fi rst and second pereiopods; O. First pereiopod; P. Second pereiopod. Scale bars: A, F = 1.0 mm; D-E, G-H, L-P = 0.5 mm; C, I-K = 0.1 mm; B = no scale available.

376 THE RAFFLES BULLETIN OF ZOOLOGY 2009

In the molecular phylogeny (Figs. 63-64), C. lingkonae is Caridina loéhae – Woltereck, 1937b: 304, fig. 9; Fernandez- genetically distinct from all ancient lake species. Leborans et al., 2006b: 1985, Table I (partly as C. loeha, erroneous spelling). Caridina loehae – Chace, 1997: 13; von Rintelen et al., 2008: 2244, Table 1; Cai et al., 2009: 27, Fig. 7 (type locality of Caridina loehae Woltereck, 1937a neotype: Lake Towuti, about 3 km south of Timampu, estuary (Figs. 18-19, Table 8) of Sungei [River] Batuopa). Cardina loéhae – Brooks, 1950: 168 (erroneous spelling). Caridina Loéhae Woltereck, 1937a: 222, Figs. I.5a-d, pls. 3,6 (type locality: Matanno [Matano] islands, Lake Towuti XX, Lake Material examined. Ð Lake Matano: 8 ex. (ZMB 29062, n=8), Towuti at Loéha Island and at Lingkona). north shore, 02°26.36'S, 121°19.03'E, loc. 84-03, on rocks, coll.

Fig. 17. Caridina lingkonae from the Malili lake system. A. Mandible (ZMB 29076); B. Maxillula; C. Maxilla; D. third maxilliped; E. second maxilliped; F. fi rst maxilliped. Scale bars: A-F = 1mm.

377 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

K. & T. von Rintelen, 1 Oct.2003; 20 ex. (MZB Cru 1768, n=10; coll. K. & T. von Rintelen, 17 Sep.2003; 10 ex. (MZB Cru 1771, ZMB 29066, n=10, some SEM material), north shore, 02°27.28'S, n=5; ZMB 29168, n=5), north shore, 02°26.274'S, 121°18.83'E, loc. 121°21.21'E, loc. 98-03, on rocks, coll. K. & T. von Rintelen, 5 133-04, on rocks, coll. K. & T. von Rintelen, 22 Jul.2004; 15 ex. Oct.2003; 3 ex. (ZMB 29079, and few juveniles), south shore, (MZB Cru 1772, n=7; ZMB 29223, n=6), north shore, 02°27.311'S, Soroako, Salonsa, INCO boat house, 02°30.71'S, 121°20.45'E, loc. 121°21.047'E, loc. 09-05, on rocks in shallow water, coll. K. & 04-05, on rocks, coll. K. & T. von Rintelen, 3 Jan.2005; 42 ex. T. von Rintelen, 7 Jan.2005; 2 ex. (ZMB 29241), north shore, (MZB Cru 1769, n=30, ZMB 29080, n=12, some SEM material), 02°25.67'S, 121°16.54'E, loc. 65-03, on mixed substrate, coll. K. south shore, Soroako, Salonsa, INCO boat house, 02°30.71'S, & T. von Rintelen, 25 Sep.2003; 1 ex. (ZMB 29447), south shore, 121°20.45'E, loc. 19-03, on rocks, coll. K. & T. von Rintelen, 19 02°27.84'S, 121°13.88'E, loc. 63-03, on rocks, coll. K. & T. von Sep.2003; 15 ex. (MZB Cru 1770, n=7; ZMB 29118, n=8, some SEM Rintelen, 24 Sep.2003; 1 ex. (MZB Cru 1773), south shore, at small material), south shore, east of Soroako, just west of Cape Patipuoho, islands, 02°28.476'S, 121°15.64'E, loc. 138-04, on rocks, coll. K. & 02°31.57'S, 121°23.41'E, loc. 99-03, on rocks, coll. K. & T. von T. von Rintelen, 24 Jul.2004; 2 ex. (MZB Cru 1774), north shore, Rintelen, 5 Oct.2003; 4 ex. (ZMB 29233, some SEM material), 02°27.418'S, 121°21.533'E, loc. 10-05, on mixed substrate, coll. southwest shore, Cape Nikomene, 02°32.24'S, 121°24.76'E, loc. 46- K. & T. von Rintelen, 7 Jan.2005; 1 ex. (MZB Cru 1775), south 03, on rocks, coll. K. & T. von Rintelen, 18 Sep.2003; 3 ex. (ZMB shore, canal between island and mainland, 02°28.46'S, 121°15.83'E, 29244), north shore, 02°29.75'S, 121°25.81'E, loc. 42-03, on rocks, loc. 62-03, on rocks, coll. K. & T. von Rintelen, 1 Oct.2003; 1

Fig. 18. Caridina loehae from the Malili lake system. A. Distribution. B. Colour pattern of living animals (not to scale). Pictures courtesy of Chris Lukhaup.

378 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 8. Summary of standard morphometric parameters for Caridina loehae. parameter range mean ± SD median n cl (mm) 2.2-2.9 2.6 ± 0.2 2.6 27 rl / cl 0.5-1.3 0.8 ± 0.1 0.8 29 n dorsal rostral teeth 14-20 17 ± 2 17 29 n ventral rostral teeth 1-8 4 ± 2 4 29 abds6 / cl 0.5-0.8 0.6 ± 0.0 0.7 27 abds6 / abds5 1.5-2.1 1.8 ± 0.2 1.9 20 abds6 / h tel 0.9-1.7 1.0 ± 0.2 1.0 20 h tel / w tel 3.1-3.5 3.3 ± 0.2 3.3 6 n spines uropodal diaeresis 9-14 12 ± 2 11 5 h ch1 / w ch1 1.9-2.7 2.1 ± 0.2 2.1 27 h ch1 / h ca1 0.9-1.8 1.1 ± 0.2 1.0 30 h ca1 / w ca1 2.5-4.7 3.2 ± 0.5 3.3 26 h ch2 / w ch2 2.3-3.1 2.7 ± 0.2 2.6 26 h ch2 / h ca2 0.6-1.0 0.7 ± 0.1 0.6 30 h ca2 / w ca2 5.4-8.1 6.7 ± 0.7 6.7 27 n spines p3 2-6 3 ± 2 3 5 n spines p5 12-16 15 ± 2 16 5 ex. (MZB Cru 1776), south shore, 02°27.85'S, 121°13.87'E, loc. 19C) rounded, without a spine. Uropodal diaeresis (Fig. 19E) 125-04, on rocks, coll. P. Koller & K. von Rintelen, 1 Aug.2004; with 9-14 movable spinules (n=5). 36 ex. (MZB Cru 1780, n=14; ZMB 29084, n=22), Petea River, 02°32.64'S, 121°29.51'E, loc. 101-03, on rocks, coll. K. & T. von 5 pairs of pleurobranchs well developed; 3 pairs of Rintelen, 6 Oct.2003; 27 ex. (MZB Cru 1781, n=13; ZMB 29460, arthrobranchs, 2 on third maxillipeds, with second pair n=14). 02°32.672'S, 121°30.137'E, loc. F4-04, substrate unknown, coll. F. Herder, 25 Mar.2004. strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair of podobranchs on second maxilliped reduced strongly to a Lake Towuti – 1 ex. (MZB Cru 17771), outlet bay, at Cape Kombe, laminate form. Epipods only present on fi rst two pereiopods. 02°48.083'S, 121°23.049'E, loc. 118-04, on mixed substrate, coll Mouthparts as described by Cai et al. (2009). K. & T. von Rintelen, 29 Jul.2004; 8 ex. (MZB Cru 1779), Larona River, close to outlet bay, 02°45.06'S, 121°20.12'E, loc. 50-03, on Chela and carpus of fi rst pereiopod distinctly stouter and rocks, coll. K. & T. von Rintelen, 21 Sep.2003. broader than chela and carpus of second pereiopod (Fig. 19N-P); chela of fi rst pereiopod 1.9-2.7 times as long as Description. Ð Carapace length 2.2-2.9 mm (n=27). Rostrum wide (n=27), 0.9-1.8 times length of carpus (n=30); tips of (Fig. 19A,B; Table 8) short, reaching near or to end of second fi ngers rounded, without hooks; dactylus 1.4-1.6 times as segment of antennular peduncle, 0.5-1.3 times as long as long as palm (n=6); carpus 2.5-4.7 times as long as wide carapace (n=29), armed dorsally with 14-20 teeth (including (n=26), 1.2-1.3 times length of merus (n=5). Chela of second 3-5 teeth posterior to orbital margin), armed ventrally with pereiopod 2.3-3.1 times as long as wide (n=26), 0.6-1.0 times 1-8 teeth. Antennal spine situated below inferior orbital length of carpus (n=30); tips of fi ngers rounded, without angle. Pterygostomial angle broadly rounded. Eyes well hooks, dactylus 1.6-2.1 times as long as palm (n=6); carpus developed, anterior end 0.5-0.7 times length of basal segment 5.4-8.1 times as long as wide (n=27), 1.3-1.5 times as long of antennular peduncle (n=5). Antennular peduncle 0.8-1.1 as merus (n=6). times as long as carapace (n=5), second segment 1.6-1.8 times length of third segment, third segment 0.3-0.4 times length Third pereiopod (Fig. 19G,H) slender, dactylus 2.7-3.6 times of basal segment. Stylocerite reaching 0.9-1.0 times length as long as wide (terminal spine included, without spines of basal segment of antennular peduncle (n=5). Scaphocerite of fl exor margin; n=5), terminating in one large claw with (Fig. 19D) 3.7-4.7 times as long as wide (n=5). 2-6 accessory spines on fl exor margin; propodus 10.2-17.2 times as long as wide, 3.7-7.3 times as long as dactylus; Sixth abdominal somite 0.5-0.8 times length of carapace carpus 4.6-6.1 times as long as wide, 0.6-0.7 times as long (n=27), 1.5-2.1 times as long as fi fth somite (n=20), 0.9-1.7 as propodus, 0.5-0.7 times as long as merus; merus 6.8-9.6 times length of telson (n=20). Telson (Fig. 19F,K) 3.1-3.5 times as long as wide, bearing 1-4 strong, movable spines times as long as wide (n=6), distal margin rounded, without on posterior margin of outer surface. projection, with 3-4 pairs of spinules and 1 pair of dorsolateral spinules; distal end with 3-4 pairs of spines, lateral pair Fifth pereiopod slender (Fig. 19I,J), dactylus 3.2-4.0 times distinctly longer than intermediate pairs. Preanal carina (Fig. as long as wide (terminal spine included, without spines of

379 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 19. Caridina loehae from the Malili lake system. A. Cephalothorax and cephalic appendages, female (ZMB 29066); B. Woltereck’s drawings of the rostrum, from two lakes (modifi ed from 1937a); C. Preanal carina; D. Scaphocerite; E. Uropodal diaeresis, F. Telson, female (ZMB 29080); G. Dactylus of third pereiopod, female (ZMB 29118); H. Third pereiopod; I. Dactylus of fi fth pereiopod; J. Fifth pereiopod; K. Distal end of telson, female (ZMB 29080); L. Endopod of male fi rst pleopod (ZMB 29066); M. Appendix masculina of male second pleopod; N. SEM image of chela and carpus of fi rst and second pereiopods, female (ZMB 29233); O. First pereiopod; P. Second pereiopod. Scale bars: A, D = 1.0 mm; C, F, H, J, L-P = 0.5 mm; E, G, I, K = 0.1 mm; B = no scale available.

380 THE RAFFLES BULLETIN OF ZOOLOGY 2009

fl exor margin; n=5), terminating in one large claw with 12- C. parvula). With regard to the rostrum, it also resembles C. 16 accessory spines on fl exor margin; propodus 12.8-20.3 masapi. However, C. loehae is generally smaller (vs. 2.1-4.6 times as long aswide, 5.2-8.1 times as long as dactylus; mm, median 3.1 mm in C. masapi), has a shorter rostrum carpus 5.8-7.8 times as long as wide, 0.5-0.6 times as long (not overreaching end of second segment of antennular as propodus, 0.5-0.7 times as long as merus; merus 7.9-12.6 peduncle vs. longer in C. masapi), and a lower number of times as long as wide, bearing 2-3 strong, movable spines spines on the dactylus of the fi fth pereiopod (vs. 30-44, on posterior margin of outer surface. median 33 in C. masapi).

Endopod of male fi rst pleopod (Fig. 19L) elongated triangular, In the molecular phylogeny (Figs. 63-64), C. loehae is 1.8-2.3 times as long as proximally wide (n=5), without genetically distinct from all other ancient lake species. appendix interna. Appendix interna of male second pleopod (Fig. 19M) 0.8-0.9 times length of appendix masculina (n=5). Caridina mahalona Cai, Wowor & Choy, 2009 (Figs. 20–23; Table 9) Ovigerous females with 10-19 eggs (n=4 females); egg size 0.8-1.1 x 0.5-0.7 mm (n=60, eggs with and without eyes). Caridina mahalona Cai et al., 2009: 29, Figs. 8-9 (type locality: Lake Mahalona at southwest coast). Distribution. Ð C. loehae is endemic to the Malili lake system. There, however, widely distributed in Lake Matano and in Material examined. Ð Lake Mahalona catchment: 1 ex. (ZMB 29466, some SEM material), Ponsoa River, 02°32.243'S, 121°31.818'E, Petea River, but was only found in the outlet bay area of loc. F1-02, substrate unknown, coll. F. Herder, 7 Nov.2002. Lake Towuti (Fig. 18A). Woltereck mentioned the occurrence of C. loehae at three other localities in Lake Towuti, e.g. Lake Matano catchment – 44 ex. (MZB Cru 1835, n=22; ZMB at Loeha Island, therefore the distribution shown here may 29069, n=22, some SEM material), Lawa River, near mouth at not be complete. northwest shore of Lake Matano, 02°25.75'S, 121°13.27'E, loc. 25-03, on leaf litter, coll. K. & T. von Rintelen, 13 Sep.2003; 20 Biology and ecology. Ð C. loehae is a typical hard substrate ex. (MZB Cru 1836, n=10; ZMB 29096, n=10), river, near mouth dweller, mainly occurring on and under smaller rocks, and at northwest corner of Lake Matano, 02°25.88'S, 121°13.08'E, on gravel in shallow water (above 5 m), where it is often loc. 24-03, on mixed substrate, coll. K. & T. von Rintelen, 13 Sep.2003; 5 ex. (ZMB 29295, some SEM material), small stream collected with other rock dwellers such as C. parvula and northwest of Lake Matano, 02°25.846'S, 121°13.097'E, loc. 126-04, C. dennerli. When disturbed, it tries to escape side- or on macrophytes, coll. T. von Rintelen, 1 Aug.2004. downwards and often stays attached to rocks. The red colour can turn blue in stressed animals. Lake Towuti catchment – 19 ex. (MZB Cru 1840, n=9; ZMB 29067, n=10, some SEM material), Lengkona River, 02°40.82'S, Colour pattern. Ð Body colouration (including appendages) of 121°41.77'E, loc. 86-03, on leaf litter, coll. K. & T. von Rintelen, C. loehae varies from light to dark red with three conspicuous 2 Oct.2003; 1 ex. (ZMB 29192), Kondube River, at road north of white transversal stripes in regular intervals on the posterior Matompi, near Timampu, 02°38.36'S, 121°24.98'E, loc. 37-03, on part of the carapace and the abdomen, a scattering of small roots, coll. K. & T. von Rintelen, 15 Sep.2003; 36 ex. (MZB Cru 1841, n=18; ZMB 29210, n=18, some SEM material), Bombongan white spots covering the whole body and uropods with white River, 02°52.38'S, 121°22.54'E, loc. 49-03, on leaf litter, coll. K. & tips (Fig. 18B), although the white colour is not always T. von Rintelen, 20 Sep.2003; 17 ex. (MZB Cru 1842, n=9; ZMB strongly pronounced. Eggs were observed to be red. 29212, n=8), stream, tributary of Bombongan River, 02°51.59'S, 121°21.61'E, loc. 48-03, on leaf litter, coll. K. & T. von Rintelen, Taxonomic remarks. Ð Cai et al. (2009: 19) stated: “Specimens 20 Sep.2003. of Woltereck (1937a, b) are no longer extant […]. As all new species described by Woltereck are morphologically close Patingko River (Malili lake system) – 35 ex. (MZB Cru 1838, n= to each other and to stabilize the taxonomic status of those 17; ZMB 29085, n=18, some SEM material), at road Tabarano, off species, neotypes are designated if specimens are available road Malili-Soroako north of Balambano, 02°38.222'S, 121°14.56'E, loc. 14-03, on mixed substrate, coll. K. & T. von Rintelen, 15 from the recent collections”. Consequently, they designated a Sep.2003; 1 ex. (ZMB 29184, n=1), Kondara River (tributary neotype for C. loehae from Lake Towuti (ovigerous female, of Patingko River), at road Malili-Soroako, east of Leduledu, cl 2.6 mm, ZRC) (2009: 27). 02°35.11'S, 121°17.34'E, loc. 36-03, on leaf litter, coll. K. & T. von Rintelen, 15 Sep.2003; 14 ex. (MZB Cru 1839, n=7; ZMB With regard to its small size (carapace length 2.2-2.9 mm, 29196, n=7), south of road Malili-Soroako, 02°37.17'S, 121°14.95'E, median 2.6 mm), C. loehae is one of the smallest species loc. 33-03, on rocks, coll. K. & T. von Rintelen, 15 Sep.2003; 14 in the Malili lake system, similar to C. spongicola and C. ex. (ZMB 29197, some SEM material), at road Malili-Soroako, in parvula. It differs from both by the generally more slender Togo village, 02°36.53'S, 121°15.56'E, loc. 34-03, on leaf litter, and fragile rostrum, a different rostrum length (reaching coll. K. & T. von Rintelen, 15 Sep.2003. near or to end of second segment of antennular peduncle Tomori (north of the Malili lake system) – 10 ex. (MZB Cru 1837, vs. longer in C. spongicola), and a lower number of spines n=5; ZMB 29061, n=5, some SEM material), Momonsi River; at on the dactylus of the fi fth pereiopod (12-16, median 16 vs. road Nuha-Beteleme, 02°25.36'S, 121°21.43'E, loc. 64-03, on leaf 21-31, median 27 in C. spongicola and 34-39, median 37 in litter, coll. K. & T. von Rintelen, 25 Sep.2003.

381 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Description. – Carapace length 2.8-5.2 mm (n=17). Rostrum length of third segment, third segment 0.3-0.4 times length (Fig. 21A-E; Table 9) length variable, short to long, of basal segment. Stylocerite reaching 0.9-1.0 times length sometimes reaching slightly beyond end of scaphocerite, of basal segment of antennular peduncle (n=5). Scaphocerite sometimes distinctly shorter, 0.5-1.0 times as long as (Fig. 21F,K,P) 3.5-4.1 times as long as wide (n=5). carapace (n=21), armed dorsally with 7-21 teeth (including 1-6 teeth posterior to orbital margin), approx. anterior 1/4 to Sixth abdominal somite 0.5-0.7 times length of carapace 2/3 unarmed, without subapical teeth armed ventrally with (n=17), 1.7-1.9 times as long as fi fth somite (n=5), 0.9-1.0 2-9 teeth. Antennal spine situated below inferior orbital times length of telson (n=17). Telson (Fig. 21G,J,L,O,Q,T) angle. Pterygostomial angle broadly rounded. Eyes well 2.9-3.3 times as long as wide (n=6), distal margin rounded, developed, anterior end 0.6-0.7 times length of basal segment without projection, with 3-4 pairs of spinules and 1 pair of of antennular peduncle (n=5). Antennular peduncle 0.7-0.9 dorsolateral spinules; distal end with 3-4 pairs of spines, times as long as carapace (n=5), second segment 1.5-1.8 times lateral pair distinctly stronger but not always longer than

Fig. 20. Distribution of Caridina mahalona in the Malili lake system and the Tomori area.

382 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 9. Summary of standard morphometric parameters for Caridina mahalona. parameter range mean ± SD median n cl (mm) 2.8-5.2 4.5 ± 0.7 4.4 17 rl / cl 0.5-1.0 0.7 ± 0.2 0.7 21 n dorsal rostral teeth 7-21 13 ± 3 14 20 n ventral rostral teeth 2-9 5 ± 2 4 20 abds6 / cl 0.5-0.7 0.6 ± 0.0 0.6 17 abds6 / abds5 1.7-1.9 1.8 ± 0.1 1.8 5 abds6 / h tel 0.9-1.0 0.9 ± 0.1 0.9 17 h tel / w tel 2.9-3.3 3.2 ± 0.2 3.2 6 n spines uropodal diaeresis 12-15 13 ± 1 13 6 h ch1 / w ch1 2.0-2.5 2.3 ± 0.2 2.4 9 h ch1 / h ca1 0.7-1.4 1.2 ± 0.1 1.2 24 h ca1 / w ca1 2.5-3.3 2.9 ± 0.3 2.8 9 h ch2 / w ch2 2.6-3.4 2.9 ± 0.2 2.8 9 h ch2 / h ca2 0.7-1.3 0.8 ± 0.1 0.7 23 h ca2 / w ca2 5.6-7.0 6.3 ± 0.5 6.2 9 n spines p3 5-6 5 ± 1 5 6 n spines p5 39-57 51 ± 6 52 6 intermediate pairs. Preanal carina (Fig. 21H,M,R) with a Third pereiopod (Fig. 22A-B,I-J,Q-R) slender, dactylus 3.0- spine. Uropodal diaeresis (Fig. 21I,N,S) with 12-15 movable 4.4 times as long as wide (terminal spine included, without spinules (n=6). spines of fl exor margin; n=6), terminating in one large claw with 5-6 accessory spines on fl exor margin; propodus 9.0- 5 pairs of pleurobranchs well developed; 3 pairs of 13.0 times as long as wide, 3.6-4.5 times as long as dactylus; arthrobranchs, 2 on third maxillipeds, with second pair carpus 4.9-5.8 times as long as wide, 0.6-0.7 times as long strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair as propodus, 0.5-0.6 times as long as merus; merus 7.1-10.0 of podobranchs on second maxilliped reduced strongly to times as long as wide, bearing 2-3 strong, movable spines a laminate form. Epipod present on fi rst pereiopod. Incisor on posterior margin of outer surface. process of mandible (Fig. 23A) ending in a row of 4-5 small teeth, molar process truncated. Lower lacinia of maxillula Fifth pereiopod slender (Fig. 22C-D,K-L,S-T), dactylus 3.9- (Fig. 23B) broadly rounded, upper lacinia elongate, with 5.4 times as long as wide (terminal spine included, without numerous distinct teeth and setae on inner margin, palp spines of fl exor margin; n=6), terminating in one large claw slender. Upper endites of maxilla (Fig. 23C) subdivided, with 39-57 accessory spines on fl exor margin; propodus 9.6- palp short, scaphognathite tapering posteriorly with numerous 14.9 times as long as wide, 2.8-3.7 times as long as dactylus; long, curved setae at posterior end. Distal end of palp of fi rst carpus 4.7-5.7 times as long as wide, 0.5-0.6 times as long maxilliped (Fig. 23D) triangular, ending with a fi nger-like as propodus, 0.6-0.7 times as long as merus; merus 6.1-8.5 projection; fl agellum of the exopod very elongated, endopod times as long as wide, bearing 2-3 strong, movable spines high, not exceeding the fl agellum of exopod in length. Second on posterior margin of outer surface. maxilliped (Fig. 23F) typical. Third maxilliped (Fig. 23E) with ultimate segment distinctly shorter than penultimate Endopod of male fi rst pleopod (Fig. 22G,O,W) elongated segment. triangular, 1.7-2.7 times as long as proximally wide (n=5), without appendix interna. Appendix interna of male second Chela and carpus of fi rst pereiopod distinctly stouter and pleopod (Fig. 22H,P,X) 0.7-0.9 times length of appendix broader than chela and carpus of second pereiopod (Fig. masculina (n=5). 22E-F,M-N,U-V); chela of fi rst pereiopod 2.0-2.5 times as long as wide (n=9), 0.7-1.4 times length of carpus (n=24); Ovigerous females with 10-24 eggs (n=3 females); egg size tips of fi ngers rounded, without hooks; dactylus 1.1-1.4 1.0-1-2 x 0.6-0.8 mm (n=28, eggs with and without eyes). times as long as palm (n=9); carpus 2.5-3.3 times as long as wide (n=9), 1.1-1.4 times length of merus (n=8). Chela of Distribution. – C. mahalona mainly occurs in rivers within second pereiopod 2.6-3.4 times as long as wide (n=9), 0.7- the Malili lakes’ catchment (Fig. 20), but was also found at 1.3 times length of carpus (n=23); tips of fi ngers rounded, one locality north of Lake Matano (Tomori area), outside without hooks, dactylus 1.1-1.5 times as long as palm (n=9); of the system. Therefore, it is the only non-endemic species carpus 5.6-7.0 times as long as wide (n=9), 1.3-1.5 times as occurring in the Malili system. long as merus (n=8).

383 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 21. Caridina mahalona from the Malili lake system (each of the three columns shows a representative of a different genetic clade; compare remarks for details). Cephalothorax and cephalic appendages from: A. Male (ZMB 29069); B. Female (ZMB 29061); C. Female (ZMB 29085); D. Male (ZMB 29210); E. Female (ZMB 29067). F. Scaphocerite, female (ZMB 29061); G. Telson, male (ZMB 29069); H. Preanal carina, female (ZMB 29061); I. Uropodal diaeresis, male (ZMB 29069); J. Distal end of telson; K. Scaphocerite, male (ZMB 29210); L. Telson; M. Preanal carina; N. Uropodal diaeresis; O. Distal end of telson; P. Scaphocerite, female (ZMB 29085); Q. Telson, female (ZMB 29197); R. Preanal carina, female (ZMB 29085); S. Uropodal diaeresis, female (ZMB 29197); T. Distal end of telson, female (ZMB 29197). Scale bars: A-F, J, O = 1.0 mm; G-H, J, L-M, O, Q-R, T = 0.5 mm; I, N, S = 0.1 mm.

384 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 22. Caridina mahalona from the Malili lake system (each of the three columns shows a representative of a different genetic clade; compare remarks for details). A. Third pereiopod, female (ZMB 29069); B. Dactylus of third pereiopod; C. Fifth pereiopod; D. Dactylus of fi fth pereiopod; E. First pereiopod, female (ZMB 29295), F. Second pereiopod; G. Endopod of male fi rst pleopod (ZMB 29061); H. Appendix masculina of male second pleopod; I. Third pereiopod, male (ZMB 29210); J. Dactylus of third pereiopod; K. Fifth pereiopod; L. Dactylus of fi fth pereiopod; M. First pereiopod; N. Second pereiopod; O. Endopod of male fi rst pleopod; P. Appendix masculina of male second pleopod; Q. Third pereiopod, female (ZMB 29197); R. Dactylus of third pereiopod; S. Fifth pereiopod; T. Dactylus of fi fth pereiopod; U. First pereiopod; V. Second pereiopod; W. Endopod of male fi rst pleopod (ZMB 29085); X. Appendix masculina of male second pleopod. Scale bars: A, C, E-I, K, M-Q, S, U-X = 0.5 mm; B, D, J, L, R, T = 0.1 mm.

385 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Biology and ecology. – C. mahalona is an exclusively Taxonomic remarks. – C. mahalona mostly resembles C. riverine species, dwelling on various kinds of substrate (leaf masapi, but both species were never found together at any litter, riverine vegetation, roots, dead wood). Except for one locality. C. mahalona is generally larger than C. masapi riverine locality very close to Lake Matano (loc. 24-03), (carapace length 2.8-5.2, median 4.4 vs. 2.1-4.6, median where it occurred together with C. holthuisi, C. mahalona 3.1 in C. masapi), its rostrum displays a higher degree of was never found in sympatry with any other species (not variability than in C. masapi, and differs by the number of even the other riverine species of the Malili lake system, teeth on the dactylus of the fi fth pereiopod (39-57, median C. masapi). 52 vs. 30-44, median 33 in C. masapi). In specimens with a short rostrum, C. mahalona can resemble C. acutirostris from Colour pattern. – Without any species specifi c pattern. Body Lake Poso, although the scaphocerite usually is more slender colouration transparently yellowish or brownish, similar to C. (3.5-4.1 times as long as wide vs. 3.0-3.6 times as long as masapi, C. acutirostris, C. schenkeli, and many other riverine wide in C. acutirostris); the same applies to the carpus of the species from all over Sulawesi. Large (often ovigerous) fi rst and second pereiopod (2.5-3.3 and 5.6-7.0 times as long females usually appear darker than smaller specimens. as wide vs. 2.0-2.7 and 4.5-5.9 times as long as wide in C.

Fig. 23. Caridina mahalona from the Malili lake system. A. Mandible (ZMB 29067); B. Maxillula; C. Maxilla; D. fi rst maxilliped; E. third maxilliped; F. second maxilliped. Scale bars: A-F = 1mm.

386 THE RAFFLES BULLETIN OF ZOOLOGY 2009 acutirostris). The general range of parameters (for example 02°40.647'S, 121°24.915'E, loc. 142-04, on leaf litter, coll. K. & the number of rostral teeth) is usually higher in C. mahalona T. von Rintelen, 25 Jul.2004; 7 ex. (ZMB 29285), west shore, than in C. acutirostris (compare Tables 10,19). Cape Bakara, 02°40.771'S, 121°26.11'E, loc. 144-04, on mixed substrate, coll. K. & T. von Rintelen, 26 Jul.2004; 3 ex. (MZB Cru 1696), west shore, at entrance to outlet bay, Cape Larona, In the molecular phylogeny (Figs. 63-64), C. mahalona 02°48.43'S, 121°24.75'E, loc. 73-03, on leaf litter, coll. K. & T. appears in three allopatric clades (drawings of representatives von Rintelen, 27 Sep.2003; 1 ex. (MZB Cru 1697), southwest of each clade are shown in Figs. 21-22). The high degree of shore, Cape Sioloya, 02°50.7'S, 121°26.32'E, loc. 77-03, on leaf rostrum variability partly occurs within populations, and no litter, coll. K. & T. von Rintelen, 28 Sep.2003; 39 ex. (MZB Cru signifi cant morphological differences where found between 1699, n=39), Larona River, close to outlet bay of Lake Towuti, members of the different clades. However, the geographic 02°45.8'S, 121°20.8'E, loc. 51-03, on macrophytes, coll. K. & T. von pattern might suggest the existence of cryptic species Rintelen, 21 Sep.2003; 54 ex. (MZB Cru 1701, n=27; ZMB 29195, (compare von Rintelen et al., in review). n=27), Towuti catchment, stream at road Wawondula-Timampu, 02°38.47'S, 121°22.76'E, loc. 39-03, on mixed substrate, coll. K. & T. von Rintelen, 16 Sep.2003; 4 ex. (ZMB 29448), Lemolemo River, 02°42.62'S, 121°40.99'E, loc. 85-03, on leaf litter, coll. K. Caridina masapi Woltereck, 1937a & T. von Rintelen, 2 Oct.2003. (Figs. 24–26; Table 10) Lampesue River (Malili lake system) – 44 ex. (MZB Cru 1698, Caridina Masapi Woltereck, 1937a: 223, Figs. I.6a-h, pls. 3,6 n=22; ZMB 29047, n=22), 02°35.4'S, 121°39.85'E, loc. 79-03, on (type locality: Matanno [Matano] islands, Lake Towuti , Lake leaf litter, coll. K. & T. von Rintelen, 29 Sep.2003. Mahalone [Mahalona], Lake Wawontoa [Lontoa], Lake Masapi, small stream between Lake Matanno and Lake Mahalone). Tominanga River (Lake Mahalona) – 3 ex. (ZMB 29072), approx. Caridina masapi – Woltereck, 1937b: 306, fi g. 10; Chace, 1997: 16; 1.5 km east of Lake Mahalona, 02°38.73'S, 121°31.95'E, loc. 59- Fernandez-Leborans et al., 2006b: 1985, Table I; von Rintelen 03, on leaf litter, coll. K. & T. von Rintelen, 23 Sep.2003; 3 ex. et al., 2008: 2244, Table 1; Cai et al., 2009: 21, Figs. 4-5 (type (ZMB 29209), approx. 2.2 km north of Lake Towuti, 02°36.5'S, locality of neotype: southern shore of Lake Masapi). 121°31.78'E, loc. 58-03, on leaf litter, coll. K. & T. von Rintelen, Cardina masapi – Brooks, 1950: 168 (erroneous spelling). 23 Sep.2003.

Material examined. – Lake Lontoa: 74 ex. (MZB Cru 1689, Description. – Carapace length 2.1-4.6 mm (n=56). Rostrum n=37; ZMB 29038, n=37, some SEM material), southeast shore, (Fig. 25A-C, Table 10) shorter than antennular peduncle to 02°40.4'S, 121°43.35'E, loc. 92-03, on mixed substrate, coll. K. & T. von Rintelen, 3 Oct.2003; 16 ex. (MZB Cru 1690, n=8; ZMB slightly reaching beyond end of scaphocerite, 0.6-1.3 times 29045, n=8, some SEM material), southwest shore, 02°40.48'S, as long as carapace (n=56), armed dorsally with 7-21 teeth 121°43.06'E, loc. 93-03, on macrophytes, coll. K. & T. von (including 2-5 teeth posterior to orbital margin), approx. Rintelen, 3 Oct.2003. anterior third unarmed or with few teeth widely spaced, armed ventrally with 3-10 teeth. Antennal spine situated Lake Matano – 13 ex. (MZB Cru 1692), south shore, near cave below inferior orbital angle. Pterygostomial angle broadly entrance, 02°29.85'S, 121°18.66'E, loc. 60-03, on mixed substrate, rounded. Eyes well developed, anterior end 0.6-0.7 times coll. K. & T. von Rintelen, 24 Sep.2003; 5 ex. (ZMB 29083, n=5 and length of basal segment of antennular peduncle (n=5). few juveniles), Petea River, approx. 400 m east of Lake Mahalona, Antennular peduncle 0.8-1.0 times as long as carapace 02°34.41'S, 121°30.63'E, loc. 54-03, on mixed substrate, coll. K. & T. von Rintelen, 23 Sep.2003; 27 ex. (MZB Cru 1702, n=14; (n=5), second segment 1.7-2.4 times length of third segment, ZMB 29276, n=13), Petea River, approx. 1.8 km north of Lake third segment 0.3 times length of basal segment. Stylocerite Mahalona, 02°34.15'S, 121°31.4'E, loc. F2-04, substrate unknown, reaching 0.9-1.0 times length of basal segment of antennular coll. F. Herder, 31 Mar.2004; 9 ex. (MZB Cru 1703, n=4; ZMB peduncle (n=5). Scaphocerite (Fig. 25E) 3.2-4.5 times as 29280, n=5), Petea River, 02°34.17'S, 121°31.21'E, loc. F3-04, long as wide (n=5). substrate unknown, coll. F. Herder, 31 Mar.2004. Sixth abdominal somite 0.4-0.7 times length of carapace Lake Masapi – 170 ex. (MZB Cru 1693, n=70; ZMB 29035, n=100, (n=56), 1.4-2.1 times as long as fi fth somite (n=21), 0.8-1.1 some SEM material), south shore, 02°50.84'S, 121°21.09'E, loc. times length of telson (n=37). Telson (Fig. 25I,L) 2.9-3.6 47-03, on mixed substrate, coll. K. & T. von Rintelen, 20 Sep.2003; 81 ex. (MZB Cru 1694, n=62; ZMB 29277, n=19, some SEM times as long as wide (n=6), distal margin rounded, without material), south shore, 02°50.837'S, 121°21.116'E, loc. F5-04, on projection, with 3-5 pairs of spinules and 1 pair of dorsolateral mixed substrate, coll. F. Herder, 15 Apr.2004. spinules; distal end with 3-5 pairs of spines, sometimes with one median spine, lateral pair distinctly longer than Lake Towuti – 1 ex. (ZMB 29031, n=1 and some juveniles), east intermediate spines, median spine or pair of spines usually shore, 02°40.84'S, 121°41.32'E, loc. 87-03, on Ottelia, coll. K. & shortest. Preanal carina (Fig. 25D) with a spine. Uropodal T. von Rintelen, 2 Oct.2003; 14 ex. (MZB Cru 1695, n=7; ZMB diaeresis (Fig. 25F) with 10-14 movable spinules (n=6). 29046, n=7, some SEM material), north shore, at cape, 02°39.38’S, 121°29.73'E, loc. 67-03, on rocks in shallow water, coll. K. & T. 5 pairs of pleurobranchs well developed; 3 pairs of von Rintelen, 26 Sep.2003; 1 ex. (ZMB 29117), west shore, south of Cape Timbalo, 02°42.91'S, 121°26.78'E, loc. 94-03, on rocks arthrobranchs, 2 on third maxillipeds, with second pair in shallow water, coll. K. & T. von Rintelen, 3 Mar.2003; 2 ex. strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair (ZMB 29281), west shore, west of Cape Timbalo, 02°42.631'S, of podobranchs on second maxilliped reduced strongly to 121°26.389'E, loc. 145-04, on mixed substrate, coll. K. & T. a laminate form. Epipod present on fi rst pereiopod. Incisor von Rintelen, 26 Jul.2004; 2 ex. (ZMB 29284), northwest shore, process of mandible (Fig. 26A) ending in a row of 7-8 small

387 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi teeth, molar process truncated. Lower lacinia of maxillula Chela and carpus of fi rst pereiopod distinctly stouter and (Fig. 26B) broadly rounded, upper lacinia elongate, with broader than chela and carpus of second pereiopod (Fig. numerous distinct teeth and setae on inner margin, palp 25M-O); chela of fi rst pereiopod 1.9-2.9 times as long as slender. Upper endites of maxilla (Fig. 26C) subdivided, wide (n=25), 0.9-1.3 times length of carpus (n=56); tips of palp slender, short, scaphognathite tapering posteriorly with fi ngers rounded, without hooks; dactylus 1.1-1.3 times as numerous long, curved setae at posterior end. Distal end of long as palm (n=12); carpus 2.1-4.6 times as long as wide palp of fi rst maxilliped (Fig. 26F) triangular, with a fi nger-like (n=25), 1.1-1.3 times length of merus (n=5). Chela of second projection; fl agellum of the exopod very stout, endopod high, pereiopod 2.4-3.9 times as long as wide (n=25), 0.6-1.6 times but not exceed the fl agellum of exopod in length. Second length of carpus (n=55); tips of fi ngers rounded, without maxilliped (Fig. 26E) typical. Third maxilliped (Fig. 26D) hooks, dactylus 1.2-1.5 times as long as palm (n=12); carpus with ultimate segment as long as penultimate segment. 5.0-8.1 times as long as wide (n=25), 1.4-1.6 times as long as merus (n=5).

Fig. 24. Distribution of Caridina masapi in the Malili lake system.

388 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 10. Summary of standard morphometric parameters for Caridina masapi. parameter range mean ± SD median n cl (mm) 2.1-4.6 3.1 ± 0.6 3.1 56 rl / cl 0.6-1.3 0.8 ± 0.1 0.8 56 n dorsal rostral teeth 7-21 13 ± 2 13 56 n ventral rostral teeth 3-10 6 ± 2 6 56 abds6 / cl 0.4-0.7 0.6 ± 0.1 0.6 56 abds6 / abds5 1.4-2.1 1.8 ± 0.1 1.9 21 abds6 / h tel 0.8-1.1 1.0 ± 0.1 1.0 37 h tel / w tel 2.9-3.6 3.3 ± 0.3 3.3 6 n spines uropodal diaeresis 10-14 12 ± 2 12 6 h ch1 / w ch1 1.9-2.9 2.3 ± 0.2 2.3 25 h ch1 / h ca1 0.9-1.3 1.2 ± 0.1 1.2 56 h ca1 / w ca1 2.1-4.6 2.7 ± 0.6 2.5 25 h ch2 / w ch2 2.4-3.9 3.1 ± 0.4 3.1 25 h ch2 / h ca2 0.6-1.6 0.7 ± 0.1 0.7 55 h ca2 / w ca2 5.0-8.1 6.4 ± 0.9 6.5 25 n spines p3 3-7 6 ± 2 6 5 n spines p5 30-44 35 ± 5 33 5

Third pereiopod (Fig. 25G-H) slender, dactylus 3.5-5.9 times Mahalona. So far, it is the only shrimp species occurring in as long as wide (terminal spine included, without spines Lake Masapi and Lake Lontoa. of fl exor margin; n=5), terminating in one large claw with 3-7 accessory spines on fl exor margin; propodus 12.6-14.8 Biology and ecology. – C. masapi, similarly to C. lanceolata, times as long as wide, 2.9-5.0 times as long as dactylus; was found on various kinds of often mixed, but mainly soft carpus 5.4-6.9 times as long as wide, 0.5-0.6 times as long substrate (e.g. macrophytes and leaf litter). Thus, it seems as propodus, 0.5-0.6 times as long as merus; merus 8.1-11.0 rather to be a generalist with a respective feeding strategy times as long as wide, bearing 3-4 strong, movable spines (compare von Rintelen et al., in review). The cheliped on posterior margin of outer surface. morphology does not show any conspicuity, unlike in most other species from the Malili lakes (for example the Fifth pereiopod slender (Fig. 25J-K), dactylus 5.7-7.0 times unusually slender pereiopods in C. lingkonae, C. spinata, as long as wide (terminal spine included, without spines of and C. profundicola). fl exor margin; n=5), terminating in one large claw with 30- 44 accessory spines on fl exor margin; propodus 11.6-15.3 Colour pattern. – Yellowish or brownish to transparent, often times as long as wide, 2.6-3.3 times as long as dactylus; with transversal dark or light bands, but without an always carpus 5.0-5.9 times as long as wide, 0.5 times as long as equally pronounced pattern. The colouration resembles that propodus, 0.6 times as long as merus; merus 9.0-9.8 times as of many riverine Caridina species from Sulawesi, which long as wide, bearing 3 strong, movable spines on posterior are either dark (brownish) or lightly (yellowish-transparent) margin of outer surface. coloured. Large (often ovigerous) females usually appear darker than smaller specimens. Endopod of male first pleopod (Fig. 25Q) elongated triangular, 2.0-2.7 times as long as proximally wide (n=5), Taxonomic remarks. – Cai et al. (2009: 19) stated: “Specimens without appendix interna. Appendix interna of male second of Woltereck (1937a, b) are no longer extant […]. As all new pleopod (Fig. 25R) 0.8-0.9 times as long as appendix species described by Woltereck are morphologically close masculina (n=5). to each other and to stabilize the taxonomic status of those species, neotypes are designated if specimens are available Ovigerous females with 15-41 eggs (n=3 females); egg size from the recent collections”. Consequently, they designated 0.7-1.2 x 0.5-0.7 mm (n=54, eggs with and without eyes). a neotype for C. masapi from Lake Masapi (male, cl 2.9 mm, ZRC) (2009: 21). Distribution. – C. masapi is endemic to the Malili system, where it is widely distributed in the lakes and rivers (Fig. Here, C. masapi is regarded as a riverine species (that also 24). Although there is only a single collecting site from Lake enters the lakes) rather than a typical lacustrine species, Matano, and none directly from Lake Mahalona, Woltereck because of its occurrence in all fi ve lakes and the surrounding (1937a: 223,b: 306) reports this species from another locality rivers. C. lanceolata is also widely distributed in the lakes in Lake Matano (“Matanno islands”), which are further west (excluding Lake Masapi and Lake Lontoa), but does not of the current collecting site on the south coast) and Lake occur in any tributary to the lakes. Thus, we here regard it

389 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 25. Caridina masapi from the Malili lake system. A. Cephalothorax and cephalic appendages, female (ZMB 29038); B. Cephalothorax and cephalic appendages, male (ZMB 29277); C. Woltereck’s drawings of the rostrum, from all Malili lakes (modifi ed from 1937a); D. Preanal carina, female (ZMB 29277); E. Scaphocerite, F. Uropodal diaeresis, male (ZMB 29277); G. third pereiopod, female (ZMB 29277); H. Dactylus of third pereiopod; I. Telson, male (ZMB 29277); J. fi fth pereiopod, female (ZMB 29277); K. Dactylus of fi fth pereiopod; L. Distal end of telson, male (ZMB 29277); M. First pereiopod; N. Second pereiopod; O. SEM image of chela and carpus of fi rst and second pereiopods; P. Endopod of male fi rst pleopod; Q. Appendix masculina of male second pleopod. Scale bars: A-B, E = 1.0 mm; D, G, I-J, M-Q = 0.5 mm; F, H, K-L = 0.1 mm; C = no scale available.

390 THE RAFFLES BULLETIN OF ZOOLOGY 2009 as a lacustrine species. The rostrum superfi cially resembles riverine species of the Malili lake system, but the rostrum C. loehae, but it appears less fragile and longer (usually is not as variable as in C. mahalona and the anterior dorsal overreaching end of second segment of antennular peduncle part is not always unarmed. It is generally smaller than C. vs. not overreaching in C. loehae). Furthermore, both species mahalona (carapace length 2.1-4.6 mm, median 3.1 mm vs. show a different number of spines on the dactylus of the 2.8-5.2 mm, median 4.4 mm in C. mahalona) and differs by fi fth pereiopod (30-44, median 33 vs. 12-16, median 16 in C. the number of teeth on the dactylus of the fi fth pereiopod loehae). Also, C. masapi is similar to C. mahalona, the other (vs. 39-57, median 52 in C. mahalona). C. masapi can

Fig. 26. Caridina masapi from the Malili lake system. A. Mandible (ZMB 29277); B. Maxillula; C. Maxilla; D. third maxilliped; E. second maxilliped; F. fi rst maxilliped. Scale bars: A-F = 1mm.

391 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi resemble C. holthuisi, but the rostrum in C. masapi usually Caridina parvula, new species differs by a conspicuous unarmed gap on the dorsal margin (Figs. 27–29; Table 11) (sometimes with few teeth widely spaced) and a more slender and cambered shape (vs. usually straight and broader with a Material examined. – Holotype: ovigerous female (cl 3.2 mm)(MZB more or less thorough denticulation in C. holthuisi). Cru 2127), Lake Towuti, southwest shore, Cape Sioloya, 02°50.7'S, 121°26.32'E, loc. 77-03, on rocks, coll. K. & T. von Rintelen, 28 C. masapi is genetically distinct from C. loehae and C. Sep.2003. mahalona (Figs. 63-64). C. masapi appears in two allopatric Paratypes (Lake Matano) – 2 ex. (ZMB 29221), north shore, clades. One is restricted to Lake Masapi (MS; Fig. 64), the 02°27.418'S, 121°21.533'E, loc. 10-05, on mixed substrate, coll. other one to several lakes and rivers. This might hint at the K. & T. von Rintelen, 7 Jan.2005; 1 ex. (ZMB 29229), east shore, existence of cryptic species (compare von Rintelen et al., just south of entrance to outlet bay, 02°31.54'S, 121°27.0'E, loc. in review). 43-03, on rocks in shallow water, coll. K. & T. von Rintelen, 18

Fig. 27. Distribution of Caridina parvula in the Malili lake system.

392 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 11. Summary of standard morphometric parameters for Caridina parvula. parameter range mean ± SD median n cl (mm) 2.1-3.0 2.6 ± 0.3 2.6 15 rl / cl 0.4-0.8 0.5 ± 0.1 0.5 15 n dorsal rostral teeth 11-18 15 ± 2 14 15 n ventral rostral teeth 2-6 4 ± 1 4 15 abds6 / cl 0.5-0.6 0.6 ± 0.0 0.6 14 abds6 / abds5 1.4-1.9 1.6 ± 0.2 1.6 7 abds6 / h tel 0.9-1.0 0.9 ± 0.0 0.9 13 h tel / w tel 2.8-3.4 3.1 ± 0.2 3.1 5 n spines uropodal diaeresis 12-18 16 ± 2 16 5 h ch1 / w ch1 2.2-2.5 2.4 ± 0.1 2.4 10 h ch1 / h ca1 0.9-1.6 1.1 ± 0.2 1.0 14 h ca1 / w ca1 3.3-4.1 3.8 ± 0.2 3.8 10 h ch2 / w ch2 2.5-3.4 3.1 ± 0.2 3.1 10 h ch2 / h ca2 0.5-1.2 0.7 ± 0.2 0.6 14 h ca2 / w ca2 4.3-9.8 7.8 ± 1.6 8.0 10 n spines p3 2-3 3 ± 1 3 4 n spines p5 34-39 37 ± 2 37 4

Sep.2003; 1 ex. (ZMB 29242), north shore, 02°25.67'S, 121°16.54'E, 121°37.53'E, loc. 70-03, on rocks, coll. K. & T. von Rintelen, loc. 65-03, on mixed substrate, coll. K. & T. von Rintelen, 25 27 Sep.2003; 10 ex. (MZB Cru 1808, n=5; ZMB 29116, n=5), Sep.2003; 17 ex. (MZB Cru 1801, n=8; ZMB 29243, n=9, some west shore, at entrance to outlet bay, Cape Larona, 02°48.43'S, SEM material), west shore, north of Lake Matano, 02°26.91'S, 121°24.75'E, loc. 73-03, on leaf litter, coll. K. & T. von Rintelen, 27 121°13.01'E, loc. 83-03, on rocks, coll. K. & T. von Rintelen, 1 Sep.2003; 3 ex. (ZMB 29119, some SEM material), Loeha Island, Oct.2003; 2 ex. (ZMB 29247), south shore, east of Soroako, just west shore, 02°45.5'S, 121°31.06'E, loc. 95-03, on rocks, coll. K. west of Cape Patipuoho, 02°31.57'S, 121°23.41'E, loc. 99-03, on & T. von Rintelen, 4 Oct.2003; 1 ex. (ZMB 29226), east shore, rocks, coll. K. & T. von Rintelen, 5 Oct.2003; 2 ex. (MZB Cru 02°52.79'S, 121°31.18'E, loc. 72-03, on rocks, coll. K. & T. von 1802), north shore, 02°26.274'S, 121°18.83'E, loc. 133-04, on rocks, Rintelen, 27 Sep.2003; 6 ex. (ZMB 29263, some SEM material), coll. K. & T. von Rintelen, 22 Jul.2004; 2 ex. (MZB Cru 1803), west shore, west of Cape Timbalo, 02°42.631'S, 121°26.389'E, south shore, 02°27.85'S, 121°13.87'E, loc. 125-04, on rocks, coll. loc. 145-04, on mixed substrate, coll. K. & T. von Rintelen, 26 P. Koller & K. von Rintelen, 1 Aug.2004; 2 ex. (MZB Cru 1805), Jul.2004; 1 ex. (MZB Cru 1809), northeast shore, at Lengkona, south shore, Soroako, INCO boat house, 02°30.71'S, 121°20.45'E, 02°40.483'S, 121°41.382'E, loc. 116-04, on mixed substrate, coll. K. loc. 19-03, on rocks, coll. K. & T. von Rintelen, 19 Sep.2003; & T. von Rintelen, 28 Jul.2004; 1 ex. (MZB Cru 1810, ovigerous 3 ex. (MZB Cru 1806), south shore, canal between island and female with freshly hatched juveniles), west shore, north of Cape mainland, 02°28.46'S, 121°15.83'E, loc. 62-03, on rocks, coll. K. Sioloya, 02°50.389'S, 121°26.026'E, loc. 03-05, on rocks, coll. Y. & T. von Rintelen, 24 Jul.2004; 1 ex. (MZB Cru 1807), north Cai, K. & T. von Rintelen, 3 Jan.2005; 4 ex. (MZB Cru 1811), shore, 02°26.36'S, 121°19.03'E, loc. 84-03, on rocks, coll. K. & west shore, Cape Bakara, 02°40.771'S, 121°26.11'E, loc. 144-04, T. von Rintelen, 1 Oct.2003; 1 ex. (ZMB 29437), Petea River, on mixed substrate, coll. K. & T. von Rintelen, 26 Jul.2004; 4 ex. 02°32.672'S, 121°30.137'E, loc. F4-04, substrate unknown, coll. (MZB Cru 1812), west shore, north of Cape Wasupute, 02°46.9'S, F. Herder, 25 Mar.2004; 1 ex. (MZB Cru 1813), Petea River, 121°27.94'E, loc. 78-03, on rocks, coll. K. & T. von Rintelen, 28 02°32.64'S, 121°29.51'E, loc. 101-03, on rocks, coll. K. & T. von Sep.2003; Towuti catchment, Lemolemo River, 3 ex. (ZMB 29028, Rintelen, 6 Oct.2003. some SEM material), 02°42.62'S, 121°40.99'E, loc. 85-03, on rocks, coll. K. & T. von Rintelen, 2 Oct.2003. Paratypes (Lake Mahalona) – 3 ex. (MZB Cru 1814), Tominanga River, approx. 1.5 km east of Lake Mahalona, 02°38.73'S, Description. – Carapace length 2.1-3.0 mm (n=15). Rostrum 121°31.95'E, loc. 59-03, on rocks, coll. K. & T. von Rintelen, (Fig. 28A; Table 11) short, not reaching to end of second 23 Sep.2003. segment of antennular peduncle, 0.4-0.8 times as long as carapace (n=15), armed dorsally with 11-18 teeth (including Paratypes (Lake Towuti) – 1 ex. (ZMB 29020), south shore, approx. 2 km east of Cape Mea, 02°55.8'S, 121°26.92'E, loc. 74-03, 2-7 teeth posterior to orbital margin), anterior less densely on rocks, coll. K. & T. von Rintelen, 28 Sep.2003; 7 ex. (ZMB spaced, armed ventrally with 2-6 teeth. Antennal spine 29064), southwest shore, Cape Sioloya, 02°50.7'S, 121°26.32'E, situated below inferior orbital angle. Pterygostomial angle loc. 77-03, on rocks, coll. K. & T. von Rintelen, 28 Sep.2003; 5 broadly rounded. Eyes well developed, anterior end 0.5-0.6 ex. (ZMB 29097), northwest shore, 02°40.647'S, 121°24.915'E, times length of basal segment of antennular peduncle (n=5). loc. 142-04, on mixed substrate, coll. K. & T. von Rintelen, 25 Antennular peduncle 0.7-0.9 times as long as carapace (n=5), Jul.2004; 1 ex. (ZMB 29098), west shore, south of Cape Timbalo, second segment 1.5-1.7 times length of third segment, third 02°42.91'S, 121°26.78'E, loc. 94-03, on rocks in shallow water, segment 0.3-0.4 times length of basal segment. Stylocerite coll. K. & T. von Rintelen, 4 Oct.2003; 2 ex. (ZMB 29108, some reaching 0.9-1.0 times length of basal segment of antennular SEM material), east shore, south of Cape Tomeraka, 02°44.47'S,

393 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 28. Caridina parvula from the Malili lake system. A. Cephalothorax and cephalic appendages, female (ZMB 29263); B. Preanal carina; C. Uropodal diaeresis, female (ZMB 29028); D. Telson; E. Scaphocerite, F. Dactylus of third pereiopod; G. Third pereiopod; H. Dactylus of fi fth pereiopod; I. Distal end of telson; J. Fifth pereiopod; K. First pereiopod, female (ZMB 29243); L. second pereiopod; M. Endopod of male fi rst pleopod (ZMB 29243); N. Appendix masculina of male second pleopod; O. SEM image of chela and carpus of fi rst and second pereiopods, female (ZMB 29119). Scale bars: A, E = 1.0 mm; B, D, G, J-O = 0.5 mm; C, F, H-I = 0.1 mm.

394 THE RAFFLES BULLETIN OF ZOOLOGY 2009 peduncle (n=5). Scaphocerite (Fig. 28E) 3.3-5.4 times as spinules; distal end with 3-5 pairs of spines, lateral pair long as wide (n=5). longer than intermediate pairs, median pair usually shortest. Preanal carina (Fig. 28B) rounded, without a spine. Uropodal Sixth abdominal somite 0.5-0.6 times length of carapace diaeresis (Fig. 28C) with 12-18 movable spinules (n=5). (n=14), 1.4-1.9 times as long as fi fth somite (n=7), 0.9-1.0 times length of telson (n=13). Telson (Fig. 28D,I) 2.8-3.4 5 pairs of pleurobranchs well developed; 3 pairs of times as long as wide (n=5), distal margin rounded, without arthrobranchs, 2 on third maxillipeds, with second pair projection, with 3-5 pairs of spinules and 1 pair of dorsolateral strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair

Fig. 29. Caridina parvula from the Malili lake system. A. Mandible (ZMB 29064); B. Maxillula; C. Maxilla; D. third maxilliped; E. second maxilliped; F. fi rst maxilliped. Scale bars: A-F = 1mm.

395 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi of podobranchs on second maxilliped reduced strongly to specimens were found in Petea and Tominanga rivers, but a laminate form. Epipod present on fi rst two pereiopods. none in Lake Mahalona (Fig. 27). Incisor process of mandible (Fig. 29A) ending in a row of 3-5 small teeth, molar process truncated. Lower lacinia Biology and ecology. – This small and rather inconspicuous of maxillula (Fig. 29B) broadly rounded, upper lacinia species often lives in sympatry with other rock dwellers, for elongate, with numerous distinct teeth and setae on inner example C. loehae, under small rocks as its primary substrate margin, palp slender. Upper endites of maxilla (Fig. 29C) in shallow water regions. subdivided, palp short, scaphognathite tapering posteriorly with numerous long, curved setae at posterior end. Distal Colour pattern. – The colour pattern of C. parvula is rather end of palp of fi rst maxilliped (Fig. 29F) triangular, not inconspicuous compared to other species from the Malili ending with a distinct fi nger-like projection; fl agellum of lakes. The body usually shows a light red colouration, which the exopod stout, endopod high, not exceeding the fl agellum can turn completely blue when under stress, with a few faint of exopod in length. Second maxilliped (Fig. 29E) typical. white transversal stripes. Body appendages are transparent. Third maxilliped (Fig. 29D) with ultimate segment as long Eggs are the same colour as the body. as penultimate segment. Etymology. – Caridina parvula refers to the small size of First and second pereiopod very slender, chela and carpus this new species (the Latin word parvus means little). of fi rst pereiopod distinctly stouter and broader than chela and carpus of second pereiopod (Fig. 28K-L,O); chela of Taxonomic remarks. – C. parvula (carapace length 2.1-3.0 fi rst pereiopod 2.2-2.5 times as long as wide (n=10), 0.9-1.6 mm, median 2.6 mm) is one of the smallest species in the times length of carpus (n=14); tips of fi ngers rounded, without Malili lakes, similarly to C. loehae and C. spongicola, but hooks; dactylus 1.4-2.0 times as long as palm (n=5); carpus differs from C. spongicola by a shorter rostrum (not reaching 3.3-4.1 times as long as wide (n=10), 1.2-1.3 times length to end of second segment of antennular peduncle vs. longer of merus (n=5). Chela of second pereiopod 2.5-3.4 times as in C. spongicola), by a higher number of spines on the long as wide (n=10), 0.5-1.2 times length of carpus (n=14); uropodal diaeresis (12-18, median 16 vs. 10-12, median tips of fi ngers rounded, without hooks, dactylus 1.5-1.8 times 11 in C. spongicola), and by a lower number of spines on as long as palm (n=5); carpus 4.3-9.8 times as long as wide the dactylus of the fi fth pereiopod (34-39, median 37 vs. (n=10), 1.3-1.4 times as long as merus (n=5). 21-31, median 27 in C. spongicola). The very short and broad rostrum is characteristic for C. parvula. The length Third pereiopod (Fig. 28F-G) slender, dactylus 3.2-5.0 times of the rostrum only resembles C. loehae, but is distinctly as long as wide (terminal spine included, without spines broader. Both species further differ by a different number of of fl exor margin; n=4), terminating in one large claw with spines on the uropodal diaeresis (vs. 9-14, median 11 in C. 2-3 accessory spines on fl exor margin; propodus 8.8-14.3 loehae) and on the dactylus of the fi fth pereiopod (vs. 12-16, times as long as wide, 2.8-4.6 times as long as dactylus; median 16 in C. loehae). However, both species often occur carpus 4.8-7.4 times as long as wide, 0.6-0.7 times as long in syntopy (on rocks in shallow water) and have a similar as propodus, 0.5-0.6 times as long as merus; merus 7.2-10.6 colour pattern, although the white markings in C. loehae are times as long as wide, bearing 3-4 strong, movable spines often more pronounced than in C. parvula. on posterior margin of outer surface. In the molecular phylogeny(Figs. 63-64), C. parvula is Fifth pereiopod slender (Fig. 28H,J), dactylus 4.0-5.0 times genetically distinct from all other ancient lake species. as long as wide (terminal spine included, without spines of fl exor margin; n=4), terminating in one large claw with 34- 39 accessory spines on fl exor margin; propodus 11.3-16.7 Caridina profundicola, new species times as long as wide, 3.0-4.0 times as long as dactylus; (Figs.30–32; Table 12) carpus 3.4-6.6 times as long as wide, 0.5-0.6 times as long as propodus, 0.5-0.7 times as long as merus; merus 7.3-10.6 Material examined. – Holotype: male (cl 3.5 mm)(MZB Cru times as long as wide, bearing 1-2 strong, movable spines 1549), Lake Towuti, Loeha Island, southwest shore, 02°45.58'S, on posterior margin of outer surface. 121°31.14'E, loc. 149-04, on boulders in deeper water, coll. K. & T. von Rintelen, 5 Aug.2004.

Endopod of male first pleopod (Fig. 28M) elongated Paratypes (Lake Towuti) – 7 ex. (MZB Cru 1552, n=3; ZMB 29025, triangular, 1.8-2.4 times as long as proximally wide (n=5), n=4, some SEM material), east shore, south of Cape Tomeraka, without appendix interna. Appendix interna of male second 02°44.47'S, 121°37.53'E, loc. 70-03, on boulders in deeper water, pleopod (Fig. 28N) 0.8-0.9 times length of appendix coll. K. & T. von Rintelen, 9 Oct.2003; 6 ex. (ZMB 29054a, n=3; masculina (n=5). some SEM material; ZMB 29054b, n=3), west shore, at entrance to outlet bay, Cape Larona, 02°48.43'S, 121°24.75'E, loc. 73-03, Ovigerous females with 12-15 eggs (n=3 females); egg size (a) on boulders in deeper water, (b) on leaf litter, coll. K. & T. von 0.8-0.9 x 0.5-0.6 mm (n=37, eggs with and without eyes). Rintelen, 8 Oct.2003; 6 ex. (MZB Cru. 1553, n=3; ZMB 29055, n=3, some SEM material), Loeha Island, north shore, 02°45.64'S, 121°34.32'E, loc. 97-03, on boulders in deeper water, coll. K. & T. Distribution. – Endemic to the Malili lake system. There, von Rintelen, 4 Oct.2003; 1 ex. (ZMB 29305), west shore, Cape widely distributed in Lake Matano and Lake Towuti, some Larona, 02°48.526'S, 121°25.044'E, loc. 120-04, on boulders in

396 THE RAFFLES BULLETIN OF ZOOLOGY 2009 deeper water, coll. K. & T. von Rintelen, 29 Jul.2004; 5 ex. (ZMB length of antennular peduncle (n=5). Scaphocerite (Fig. 31E) 29435, some SEM material), Loeha Island, north shore, 02°45.324'S, 3.4-5.1 times as long as wide (n=22). 121°32.019'E, loc. 226-05, on boulders in deeper water, coll. K. & T. von Rintelen, 23 Oct.2005; 9 ex. (MZB Cru. 1550), Loeha Sixth abdominal somite 0.7-1.0 times length of carapace Island, southwest shore, 02°45.58'S, 121°31.14'E, loc. 149-04, on (n=35), 1.5-2.1 times as long as fi fth somite (n=22), 0.9-1.1 boulders in deeper water, coll. K. & T. von Rintelen, 5 Aug.2004; 2 ex. (MZB Cru. 1551), northeast shore, at Cape Noote, 02°39.751'S, times length of telson (n=30). Telson (Fig. 31F,K) 3.4-4.0 121°39.195'E, loc. 117-04, on boulders in deeper water, coll. K. times as long as wide (n=5), distal margin rounded, without & T. von Rintelen, 28 Jul.2004. projection, with 2-4 pairs of spinules and 1 pair of dorsolateral spinules (n=22); distal end with 4 pairs of spines, lateral pair Description. – Carapace length 2.7-4.9 mm (n=35). Rostrum distinctly longer than intermediate pairs, median pair shortest. (Fig. 31A-C; Table 12) very long and slender, proximal part Preanal carina (Fig. 31G) with a spine. Uropodal diaeresis triangular widened, equally pronounced in male and female, (Fig. 31D) with 9-11 movable spinules (n=9). reaching far beyond scaphocerite; 1.4-2.8 times as long as carapace (n=34), armed dorsally with 16-25 teeth, including 5 pairs of pleurobranchs well developed; 3 pairs of 2-3 posterior to orbital margin, dorsal teeth throughout less arthrobranchs, 2 on third maxillipeds, with second pair densely spaced than ventral teeth, armed ventrally with strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair 13-24 teeth. Antennal spine situated below inferior orbital of podobranchs on second maxilliped reduced strongly to a angle. Pterygostomial angle broadly rounded. Eyes well laminate form. Epipod absent from all pereiopods. Incisor developed, anterior end 0.6-0.7 times length of basal segment process of mandible (Fig. 32A) ending in a row of 2-3 small of antennular peduncle (n=5). Antennular peduncle 0.8-1.1 teeth, molar process truncated. Lower lacinia of maxillula times as long as carapace (n=5), second segment 1.8-2.0 (Fig. 32B) broadly rounded, upper lacinia elongate, with times length of third segment, third segment 0.2-0.3 times numerous distinct teeth and setae on inner margin, palp length of basal segment. Stylocerite reaching 0.9-1.0 times slender. Upper endites of maxilla (Fig. 32C) subdivided,

Fig. 30. Caridina profundicola from the Malili lake system. A. Distribution. B. Colour pattern of living animal (not to scale). Picture courtesy of Rainer Masche.

397 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Table 12. Summary of standard morphometric parameters for Caridina profundicola. parameter range mean ± SD median n cl (mm) 2.7-4.9 3.9 ± 0.7 4.0 35 rl / cl 1.4-2.8 1.9 ± 0.3 1.9 34 n dorsal rostral teeth 16-25 20 ± 2 19 34 n ventral rostral teeth 13-24 20 ± 3 20 34 abds6 / cl 0.7-1.0 0.8 ± 0.1 0.8 35 abds6 / abds5 1.5-2.1 1.8 ± 0.1 1.8 22 abds6 / h tel 0.9-1.1 1.1 ± 0.1 1.1 30 h tel / w tel 3.4-4.0 3.7 ± 0.2 3.8 5 n spines uropodal diaeresis 9-11 10 ± 1 10 9 h ch1 / w ch1 2.9-4.4 3.5 ± 0.4 3.5 20 h ch1 / h ca1 0.8-1.1 0.9 ± 0.0 0.9 34 h ca1 / w ca1 4.2-5.6 5.1 ± 0.4 5.3 20 h ch2 / w ch2 4.3-6.1 5.1 ± 0.5 5.1 20 h ch2 / h ca2 0.6-0.7 0.6 ± 0.0 0.6 34 h ca2 / w ca2 8.8-12.2 10.8 ± 0.9 10.8 20 n spines p3 1-2 1 ± 0 1 16 n spines p5 34-44 39 ± 4 39 7 palp very slender, scaphognathite tapering posteriorly with 20.4-22.8 times as long as wide (n=5), 3.6-4.6 times as long numerous long, curved setae at posterior end. Distal end as dactylus; carpus 6.6-9.3 times as long as wide, 0.5 times of palp of fi rst maxilliped (Fig. 32D) triangular, with a as long as propodus, 0.5-0.6 times as long as merus; merus long fi nger-like projection; fl agellum of the exopod very 10.7-14.3 times as long as wide, bearing 3 strong, movable elongated, endopod high, reaching half the fl agellum of spines on posterior margin of outer surface (n=2). exopod in length. Second maxilliped (Fig. 32F) typical. Third maxilliped (Fig. 32E) with ultimate segment distinctly Endopod of male fi rst pleopod (Fig. 31P) elongated triangular, shorter than penultimate segment. 1.8-2,2 times as long as proximally wide (n=5), without appendix interna. Appendix interna of male second pleopod First and second pereiopod very slender, chela and carpus (Fig. 31Q) 0.8-1.0 times length of appendix masculina of fi rst pereiopod distinctly stouter and broader than chela (n=5). and carpus of second pereiopod (Fig. 31M-O); chela of fi rst pereiopod 2.9-4.4 times as long as wide (n=20), 0.8-1.1 times Ovigerous females with 41-80 eggs (n=9 females); egg length of carpus (n=34); tips of fi ngers rounded, without size 0.7-0.9 x 0.4-0.6 mm (n=202, eggs with and without hooks; dactylus 1.0-1.3 times as long as palm (n=6); carpus eyes). 4.2-5.6 times as long as wide (n=20), 1.3-1.5 times length of merus (n=5). Chela of second pereiopod 4.3-6.1 times as Distribution. – Endemic to Lake Towuti (Fig. 30A). long as wide (n=20), 0.6-0.7 times length of carpus (n=34); tips of fi ngers rounded, without hooks, dactylus 1.1-1.2 times Biology and ecology. – C. profundicola is a hard substrate as long as palm (n=6); carpus 8.8-12.2 times as long as wide dweller. Adult specimens of this species were exclusively (n=20), 1.3-1.6 times as long as merus (n=5). found in deeper water regions, approx. below 3 m, although two juveniles were collected among leaf litter in shallow Third pereiopod (Fig. 31I,L) slender, dactylus 5.8-7.8 times water. The majority of species was found between large rocks as long as wide (terminal spine included, without spines of (boulders), often together with C. spinata. C. profundicola fl exor margin; n=5), terminating in one large claw with 1-2 is a rather inactive species, which keeps still when disturbed accessory spines on fl exor margin (n=16); propodus 14.0- (KvR pers. observation), although it is capable of very fast 19.0 times as long as wide (n=5), 3.2-4.1 times as long as movements if necessary. dactylus; carpus 6.9-8.2 times as long as wide, 0.6 times as long as propodus, 0.4-0,5 times as long as merus; merus Colour pattern. – Body and appendages yellowish- 11.5-15.7 times as long as wide, bearing 3-4 strong, movable transparent, sometimes slightly red, usually with two spines on posterior margin of outer surface. conspicuous yellow transversal stripes on the abdomen (Fig. 30B). Eggs green, contrasting the body colour. The yellow Fifth pereiopod slender (Fig. 31H,J), dactylus 6.2-8.3 times stripes are also already distinctive in juveniles. as long as wide (terminal spine included, without spines of fl exor margin; n=5), terminating in one large claw with Etymology. – Caridina profundicola refers to the unusually 34-44 (n=7) accessory spines on fl exor margin; propodus deep occurrence of this new species in the Malili lake system.

398 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 31. Caridina profundicola from the Malili lake system. A. Cephalothorax and cephalic appendages, female (ZMB 29025); B. Rostrum, other female (ZMB 29025); C. Rostrum, female (ZMB 29054a); D. Uropodal diaeresis, female (ZMB 29025); E. Scaphocerite, male (ZMB 29025), F. Telson, female (ZMB 29025); G. Preanal carina; H. Fifth pereiopod; I. Third pereiopod; J. Dactylus of fi fth pereiopod; K. Distal end of telson; L. Dactylus of third pereiopod; M. First pereiopod, female (ZMB 29054a); N. Second pereiopod; O. SEM image of chela and carpus of fi rst and second pereiopods, female (ZMB 29025); P. Endopod of male fi rst pleopod (ZMB 29025); Q. Appendix masculina of male second pleopod. Scale bars: A-C, E = 1.0 mm; F-I, M-Q = 0.5 mm; D, J-L = 0.1 mm.

399 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

The name is a combination of the Latin words profundus slender pereiopods and often occur on the same substrate (depths) and collere (to inhabit). (usually boulders in deeper water) at the same locality, but differ in the shape of the rostrum (proximal part triangular Taxonomic remarks. – C. profundicola differs from all Malili while distal part distinctly slender vs. not triangular, but rather species by the characteristic triangular shape of the proximal uniformly slender in C. spinata), a longer rostrum compared part of the otherwise very slender rostrum. A similar triangular to the carapace length (1.4-2.8, median 1.9 vs. 0.9-1.7, shape is only pronounced in C. lingkonae, but differs by a median 1.2 in C. spinata), a larger number of ventral teeth distinctly more slender and also longer rostrum compared on the rostrum (13-24, median 20 vs. 5-12, median 9 in C. to carapace length (1.4-2.8, median 1.9 vs. 1.0-1.6, median spinata) and on the dactylus of the fi fth pereiopod (34-44, 1.2 in C. lingkonae), and a higher number of ventral teeth median 39 vs. 25-31, median 29 in C. spinata), respectively, (13-24, median 20 vs. 7-18, median 12 in C. lingkonae). and a lower number of spines on the uropodal diaeresis (9- 11, median 10 vs. 12-16, median 14 in C. spinata). Both C. profundicola (2.7-4.9 mm, median 4.0 mm) and C. spinata species differ in their behaviour: C. profundicola is distinctly (carapace length 3.0-5.0 mm, median 4.2 mm) are the largest more inactive and can almost be caught by hand, while C. lacustrine species in the Malili system. Both show similar spinata always appears rather active. With its extremely long

Fig. 32. Caridina profundicola from the Malili lake system. A. Mandible (MZB Cru 1552); B. Maxillula; C. Maxilla; D. fi rst maxilliped; E. third maxilliped; F. second maxilliped. Scale bars: A-F = 1mm.

400 THE RAFFLES BULLETIN OF ZOOLOGY 2009 and slender rostrum, C. profundicola further resembles C. Material examined. – Lake Towuti: 19 ex. (MZB Cru 1555, n=10 ensifera and C. caerulea from Lake Poso, but differs in the and ZMB 29026, n=9, some SEM material), west shore, at entrance triangular shape and the constant denticulation (vs. always to outlet bay, Cape Larona, 02°48.43'S, 121°24.75'E, loc. 73-03, with an unarmed gap in both Poso species). coll. K. & T. von Rintelen, 8 Oct.2003; 1 ex. (ZMB 29056, n=1 and few juveniles, some SEM material), east shore, south of Cape Tomeraka, 02°44.47'S, 121°37.53'E, loc. 70-03, coll. K. & T. von In the molecular phylogeny (Figs. 63–64), C. profundicola Rintelen, 27 Sep.2003; 1 ex. (ZMB 29057, n=1 and few juveniles), is genetically distinct from all other ancient lake species. southwest shore, west of Cape Tetetu, 02°54.13'S, 121°23.78'E, loc. 76-03, coll. K. & T. von Rintelen, 28 Sep.2003; 1 ex. (ZMB 29058, some SEM material), Loeha Island, north shore, 02°45.64'S, Caridina spinata Woltereck, 1937a 121°34.32'E, loc. 97-03, coll. K. & T. von Rintelen, 4 Oct.2003; (Figs. 33–35; Table 13) (ZMB 29141, n=few juveniles), south shore, approx. 2 km east of Cape Mea, 02°55.8'S, 121°26.92'E, loc. 74-03, coll. K. & T. von Caridina spinata Woltereck, 1937a: 221, fi g. I.3, pls. 3,6 (type Rintelen, 28 Sep.2003; (ZMB 29142, n=few juveniles), north shore, locality: Lake Towuti, Lake Matanno [Matano]). bay east of Cape Bintu, 02°39.48'S, 121°33.25'E, loc. 68-03, coll. Caridina spinata – Woltereck, 1937b: 302, fi g. 8; Chace, 1997: K. & T. von Rintelen, 26 Sep.2003; 1 ex. (ZMB 29154), Larona 20; von Rintelen et al., 2008: 2244, Table 1; Cai et al., 2009: River, close to outlet bay, 02°45.8'S, 121°20.8'E, loc. 51-03, coll. 25, Fig. 6 (type locality of neotype: Lake Towuti, about 3 km K. & T. von Rintelen, 28 Jul.2004; 2 ex. (ZMB 29434), Loeha south of Timampu, estuary of Sungei [River] Batuopa). Island, north shore, 02°45.324'S, 121°32.019'E, loc. 226-05, coll. K. Cardina spinata – Brooks, 1950: 168 (erroneous spelling). & T. von Rintelen, 23 Oct.2005; 6 ex. (MZB Cru 1556), northeast Not: Caridina spinata – von Rintelen et al., 2007b: 262, fi g. 2b. shore, at Cape Noote, 02°39.751'S, 121°39.195'E, loc. 117-04, coll.

Fig. 33. Caridina spinata from the Malili lake system. A. distribution. B,C. colour pattern of living animals (not to scale). Picture B. courtesy of Chris Lukhaup.

401 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Table 13. Summary of standard morphometric parameters for Caridina spinata. parameter range mean ± SD median n cl (mm) 3.0-5.0 4.1 ± 0.6 4.2 17 rl / cl 0.9-1.7 1.3 ± 0.2 1.2 16 n dorsal rostra teeth 14-24 17 ± 3 17 16 n ventral rostral teeth 5-12 8 ± 2 9 16 abds6 / cl 0.5-0.7 0.6 ± 0.0 0.6 18 abds6 / abds5 1.5-1.9 1.7 ± 0.1 1.7 11 abds6 / h tel 0.8-1.0 0.9 ± 0.0 0.9 12 h tel / w tel 3.2-3.6 3.3 ± 0.1 3.3 6 n spines uropodal diaeresis 12-16 14 ± 1 14 6 h ch1 / w ch1 2.0-3.6 2.8 ± 0.6 3.0 13 h ch1 / h ca1 0.9-1.4 1.1 ± 0.2 1.0 18 h ca1 / w ca1 2.1-5.2 3.7 ± 1.3 4.5 12 h ch2 / w ch2 2.3-5.5 3.8 ± 1.1 4.3 13 h ch2 / h ca2 0.5-0.8 0.6 ± 0.1 0.6 17 h ca2 / w ca2 4.8-11.9 8.4 ± 2.6 9.6 13 n spines p3 2-3 2 ± 0 2 5 n spines p5 25-31 29 ± 2 29 5

K. & T. von Rintelen, 28 Jul.2004; 1 ex. (MZB Cru 1557), Loeha of podobranchs on second maxilliped reduced strongly to Island, southwest shore, 02°45.58'S, 121°31.14'E, loc. 149-04, coll. a laminate form. Epipod present on fi rst pereiopod. Incisor K. & T. von Rintelen, 5 Aug.2004; 2 ex. (MZB Cru 1558, n=2 process of mandible (Fig. 35A) ending in a row of 3-4 small juveniles), Loeha Island, west shore, 02°45.5'S, 121°31.06'E, loc. teeth, molar process truncated. Lower lacinia of maxillula 95-03, coll. K. & T. von Rintelen, 5 Aug.2004. (Fig. 35B) broadly rounded, upper lacinia elongated, with numerous distinct teeth and setae on inner margin, palp Description. – Carapace length 3.0-5.0 mm (n=17). Rostrum slender. Upper endites of maxilla (Fig. 35C) subdivided, (Fig. 34A-B, Table 13) long, reaching beyond or far beyond palp short, scaphognathite tapering posteriorly with numerous end of scaphocerite, 0.9-1.7 times as long as carapace long, curved setae at posterior end. Distal end of palp of (n=16), armed dorsally with 14-24 teeth (including 3-5 teeth first maxilliped (Fig. 35F) triangular, with a finger-like posterior to orbital margin), anterior less densely spaced, projection; fl agellum of the exopod very elongated, endopod armed ventrally with 5-12 teeth. Antennal spine situated high, reaching half the fl agellum of exopod in length. Second below inferior orbital angle. Pterygostomial angle broadly maxilliped (Fig. 35E) typical. Third maxilliped (Fig. 35D) rounded. Eyes well developed, anterior end 0.6 times length with ultimate segment distinctly shorter than penultimate of basal segment of antennular peduncle (n=5). Antennular segment. peduncle 0.9-1.0 times as long as carapace (n=5), second segment 1.4-2.0 times length of third segment, third segment Chela and carpus of fi rst pereiopod distinctly stouter and 0.3-0.4 times length of basal segment. Stylocerite reaching broader than chela and carpus of second pereiopod (Fig. 0.9-1.0 times length of basal segment of antennular peduncle 34N-P); chela of fi rst pereiopod 2.0-3.6 times as long as (n=5). Scaphocerite (Fig. 34F) 3.3-5.4 times as long as wide (n=13), 0.9-1.4 times length of carpus (n=18); tips of wide (n=5). fi ngers rounded, without hooks; dactylus 1.3-1.5 times as long as palm (n=5); carpus 2.1-5.2 times as long as wide Sixth abdominal somite 0.5-0.7 times length of carapace (n=12), 1.2-1.5 times length of merus (n=5). Chela of second (n=18), 1.5-1.9 times as long as fi fth somite (n=11), 0.8- pereiopod 2.3-5.5 times as long as wide (n=13), 0.5-0.8 times 1.0 times length of telson (n=12). Telson (Fig. 34E,I) 3.2- length of carpus (n=17); tips of fi ngers rounded, without 3.6 times as long as wide (n=6), distal margin rounded, hooks, dactylus 1.3-1.6 times as long as palm (n=5); carpus without projection, with 3-4 pairs of spinules and 1 pair of 4.8-11.9 times as long as wide (n=13), 1.4-1.6 times as long dorsolateral spinules; distal end with 3 pairs of spines, lateral as merus (n=5). pair distinctly longer than intermediate pairs, median pair or median spine shortest. Preanal carina (Fig. 34C) with a Third pereiopod (Fig. 34G,K) slender, dactylus 2.8-4.0 times spine. Uropodal diaeresis (Fig. 34D) with 12-16 movable as long as wide (terminal spine included, without spines spinules (n=6). of fl exor margin; n=5), terminating in one large claw with 2-3 accessory spines on fl exor margin; propodus 17.0-23.0 5 pairs of pleurobranchs well developed; 3 pairs of times as long as wide, 7.0-7.8 times as long as dactylus; arthrobranchs, 2 on third maxillipeds, with second pair carpus 6.8-8.9 times as long as wide, 0.5-0.6 times as long strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair as propodus, 0.5-0.6 times as long as merus; merus 10.0-13.4

402 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 34. Caridina spinata from the Malili lake system. A. Cephalothorax and cephalic appendages, male (ZMB 29026); B. Woltereck’s drawing of the rostrum (modifi ed from 1937a); C. Preanal carina, male (MZB Cru. 1556); D. Uropodal diaeresis, male (ZMB 29026); E. telson; F. Scaphocerite, male (MZB Cru. 1556); G. Third pereiopod, female (ZMB 29026); H. Fifth pereiopod; I. Distal end of telson, male (ZMB 29026); J. Dactylus of fi fth pereiopod, female (ZMB 29026); K. Dactylus of third pereiopod; L. Endopod of male fi rst pleopod (MZB Cru. 1556); M. Appendix masculina of male second pleopod; N. SEM image of chela and carpus of fi rst and second pereiopods, female (ZMB 29058); O. First pereiopod, male (ZMB 29026); P. Second pereiopod. Scale bars: A, F = 1.0 mm; C, E, G-I, L-P = 0.5 mm; D, J-K = 0.1 mm; B = no scale available.

403 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi times as long as wide, bearing 3-4 strong, movable spines as propodus, 0.6-0.7 times as long as merus; merus 9.2-11.8 on posterior margin of outer surface. times as long as wide, bearing 2-3 strong, movable spines on posterior margin of outer surface. Fifth pereiopod slender (Fig. 34H,J), dactylus 3.6-5.4 times as long as wide (terminal spine included, without spines of Endopod of male first pleopod (Fig. 34L) elongated fl exor margin; n=5), terminating in one large claw with 25- triangularly, 1.8-1.9 times as long as proximally wide 31 accessory spines on fl exor margin; propodus 18.7-26.3 (n=5), without appendix interna. Appendix interna of male times as long as wide, 3.9-7.6 times as long as dactylus; second pleopod (Fig. 34.M) 0.7-0.9 times length of appendix carpus 6.9-8.7 times as long as wide, 0.5-0.6 times as long masculina (n=5).

Fig. 35. Caridina spinata from the Malili lake system. A. Mandible (MZB Cru 1555); B. Maxillula; C. Maxilla; D. third maxilliped; E. second maxilliped; F. fi rst maxilliped. Scale bars: A-F = 1mm.

404 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Ovigerous females with 17-31 eggs (n=3 females); egg size larger size (carapace length up to 5.0 mm vs. not larger than 1.0-1.1 x 0.6-0.7 mm (n=37, eggs with and without eyes). 3.4-3.8 mm in the other species).

Distribution. – Endemic to Lake Towuti and widely In the molecular phylogeny (Figs. 63-64), C. spinata is distributed within the lake (Fig. 33A). genetically distinct from all other ancient lake species.

Biology and ecology. – C. spinata is a hard substrate dweller on rocks. Whereas juveniles were also frequently observed Caridina spongicola Zitzler & Cai, 2006 in shallow water zones (above approx. 3-5 m), adults seem (Figs. 36–38; Table 14) to prefer boulders in deeper water zones, where they often occur in syntopy with C. profundicola and sometimes with Caridina spongicola Zitzler & Cai, 2006: 271, Figs. 1-3. (type other rock dwellers from Lake Towuti. When disturbed, C. locality: outlet bay of Lake Towuti) spinata tries to hide in nearby gaps between rocks (usually Caridina spongicola – von Rintelen et al., 2007b: 262, Figs. 1, boulders). Like in other typical rock dwellers from the 2008: 2244, Table 1. Malili lakes it rather escapes side- or downwards than in Material examined. – Holotype: ovigerous female (eggs without other directions. eyes), cl 2.4 mm (MZB Cru 1559), Lake Towuti, west shore, outlet bay, west of Cape Tokaluku, 02°47.261'S, 121°23.17'E, loc. 119-04, Colour pattern. – Body and appendages mainly crimson to on sponge, coll. K. & T. von Rintelen, 29 Jul.2004. deep red (Fig. 33B-C), often with two to three bright yellow or orange transversal stripes at the end of the carapace and Paratypes (Lake Towuti) – 3 females (cl 2.0-2.4 mm) (MZB Cru the abdomen and a few dots of the same colour on various 1560); 2 ovigerous females (cl 2.4-2.8 mm) (MZB Cru 1560), same body parts or body appendages, e.g. tips of the uropods. data as holotpye; 5 males (cl 1.8-2.3 mm)(MZB Cru 1560), same Chelae and uropods can be completely yellow or orange. This data as holotype; 11 females (cl 1.9-2.6 mm)(ZMB 29027, some SEM material), 2 ovigerous females (cl 2.4 mm)(ZMB 29027, some combination of red-crimson and yellow or orange is unique SEM material), Lake Towuti, west shore, outlet bay, west of Cape in the ancient lake species, although a red body colouration Tokaluku, 02°47.32'S 121°23.38'E, loc. 52-03, on sponge, coll. K. is common in rock dwellers. Antennules usually transparently & T. von Rintelen, 21 Sep.2003; 4 males (cl 1.9-2.1 mm)(ZMB white. Eggs coloured as body. This colour pattern remains 29027, some SEM material), same data as previous sample; 9 males visible even if the shrimp is under stress, the intensity of (cl 2.1-2.4 mm), 12 females (cl 2.2-2.6 mm), 6 ovigerous females the colour might fade. (cl 2.4-2.6 mm)(ZRC 2006.0114), Lake Towuti, west shore, outlet bay, west of Cape Tokaluku, 02°46.277'S 121°21.83'E, loc. 02-05, Taxonomic remarks. – Cai et al. (2009: 19) stated: “Specimens on sponge, coll. Y. Cai, K. & T. von Rintelen, 3 Jan.2005. of Woltereck (1937a, b) are no longer extant […]. As all new Others (Lake Towuti) ) – 170 ex. (MZB Cru 1845, n=75 ;ZMB species described by Woltereck are morphologically close 29125, n=95 and several juveniles), same data as paratypes of to each other and to stabilize the taxonomic status of those ZRC 2006.0114, loc. 02-05, on sponge; 23 ex. (ZMB 29313, species, neotypes are designated if specimens are available n=23 and several juveniles), west shore, outlet bay, 02°47.345'S, from the recent collections”. Consequently, they designated a 121°23.356'E, loc. 14-05, on sponge, coll. K. & T. von Rintelen, neotype for C. spinata from Lake Towuti (ovigerous female, 9 Jan.2005; 12 ex. (ZMB 29129, n=12 and several juveniles), west cl 4.3 mm, ZRC) (2009: 25). shore, outlet bay, 02°47.623'S, 121°22.724'E, loc. 13-05, on sponge, coll. K. & T. von Rintelen, 9 Jan.2005; (ZMB 29294, several In living animals the colour pattern of C. spinata always juveniles), same data as holotype, loc. 119-04, on sponge. distinguishes it from all other species. C. spinata (carapace length 3.0-5.0 mm, median 4.2 mm) and C. profundicola (2.7- Description. – Carapace length 1.8-2.8 mm (n=48). Rostrum 4.9 mm, median 4.0 mm) are the largest lacustrine species (Figs. 36B, 37.A, 38.A; Table 14) short, straight and slender, in the Malili lakes. Both have similarly slender pereiopods anterior third slightly upturned, reaching to or slightly beyond and often occur on the same substrate (usually boulders in third segment of antennular peduncle, 0.7-3.0 times as long as deeper water) at the same locality. They differ in the shape carapace (n=48), armed dorsally with 14-25 teeth (including of the rostrum (not triangular, but rather uniformly slender 3-5 teeth posterior to orbital margin), anterior less densely vs. proximal part triangular while distal part distinctly spaced, armed ventrally with 3-15 teeth. Antennal spine slender in C. profundicola), a shorter rostrum compared to situated below inferior orbital angle. Pterygostomial angle the carapace length (0.9-1.7, median 1.2 vs. 1.4-2.8, median broadly rounded. Eyes well developed, anterior end reaching 1.9 in C. profundicola), a smaller number of ventral teeth to or beyond half length of basal segment of antennular on the rostrum (5-12, median 9 vs. 13-24, median 20 in C. peduncle. Antennular peduncle 0.8-1.2 times as long as profundicola) and on the dactylus of the fi fth pereiopod (25- carapace (n=10), second segment 2.0-2.3 times length of 31, median 29 vs. 34-44, median 39 in C. profundicola), as third segment, third segment 0.2-0.3 times length of basal well as a higher number of spines on the uropodal diaeresis segment (n=5). Stylocerite reaching 0.8-0.9 length of basal (12-16, median 14 vs. 9-11, median 10 in C. profundicola). segment of antennular peduncle (n=5). Scaphocerite (Fig. With regard to the rostrum, C. spinata resembles C. striata, 37C) slender, 3.5-5.0 times as long as wide (n=8). C. glaubrechti and C. woltereckae, but it differs in the slender form of the fi rst and second pereiopods and the generally Sixth abdominal somite 0.5-0.7 times length of carapace (n=48), 1.2-2.3 times as long as fi fth somite (n=21), 0.7-

405 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 36. Caridina spongicola from the Malili lake system. A. Distribution. B. Rostrum variability (ZMB 29027). C.-D. Colour pattern of living animals (not to scale). Figure from Zitzler & Cai (2006), i.e. by the same authors.

406 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 14. Summary of standard morphometric parameters for Caridina spongicola. parameter range mean ± SD median n cl (mm) 1.8-2.8 2.3 ± 0.3 2.4 48 rl / cl 0.7-3.0 1.6 ± 0.8 1.2 48 n dorsal rostral teeth 14-25 20 ± 2 20 48 n ventral rostral teeth 3-15 6 ± 2 6 48 abds6 / cl 0.5-0.7 0.6 ± 0.1 0.6 48 abds6 / abds5 1.2-2.3 1.9 ± 0.3 1.9 21 abds6 / h tel 0.7-1.0 0.9 ± 0.1 0.9 28 h tel / w tel 2.8-4.1 3.4 ± 0.3 3.4 13 n spines uropodal diaeresis 10-12 11 ± 1 11 12 h ch1 / w ch1 2.3-2.9 2.6 ± 0.2 2.7 20 h ch1 / h ca1 0.8-1.4 1.2 ± 0.1 1.2 48 h ca1 / w ca1 2.5-3.5 2.9 ± 0.3 3.0 20 h ch2 / w ch2 3.0-4.0 3.4 ± 0.3 3.3 20 h ch2 / h ca2 0.7-0.8 0.8 ± 0.0 0.8 46 h ca2 / w ca2 5.9-7.9 6.6 ± 0.5 6.6 20 n spines p3 1-3 2 ± 1 2 7 n spines p5 21-31 26 ±4 27 7

1.0 times length of telson (n=28). Telson (Fig. 37D,F) 2.8- fl exor margin; n=5), terminating in one large claw with 1-3 4.1 times as long as wide (n=13), distal margin rounded, accessory spines on fl exor margin (n=7); propodus 11.1-15.0 without projection, with 3-4 pairs of spinules and 1 pair times as long as wide, 3.3-5.3 times as long as dactylus; of dorsolateral spinules; distal end with 4 pairs of spines, carpus 5.0-6.1 times as long as wide, 0.5-0.7 times as long lateral pair distinctly longer than intermediate pairs, median as propodus, 0.5 times as long as merus; merus 8.1-10.0 pair shortest. Preanal carina (Fig. 37B) rounded, without times as long as wide, bearing 2-4 strong, movable spines spine. Uropodal diaeresis (Fig. 37E) with 10-12 movable on posterior margin of outer surface. spinules (n=12). Fifth pereiopod slender (Fig. 37I-J), dactylus 3.5-4.4 times Incisor process of mandible (Fig. 38B) ending in irregular as long as wide (terminal spine included, without spines teeth, molar process truncated. Lower lacinia of maxillule of fl exor margin; n=5), terminating in one large claw with (Fig. 38C) broadly rounded, upper lacinia elongated, with a 21-31 accessory spines on fl exor margin (n=7); propodus number of distinct teeth on inner margin, palp slender. Upper 13.1-15.0 times as long as wide, 3.6-4.5 times as long as endites of maxilla (Fig. 38G) subdivided, palp elongate, dactylus; carpus 4.6-5.9 times as long as wide, 0.4-0.5 times scaphognathite tapering posteriorly. Palp of fi rst maxilliped as long as propodus, 0.6 times as long as merus; merus 7.1- (Fig. 38D) truncate, ending in triangular shape. Podobranchs 9.0 times as long as wide, bearing 2 strong, movable spines of second maxilliped (Fig. 38F) reduced to small lamina. on posterior margin of outer surface. Third maxilliped (Fig. 38E) with ultimate segment slightly shorter than penultimate segment. Endopod of male fi rst pleopod (Fig.38H) elongated triangular, 2.0-2.8 times as long as proximally wide (n=5), without Chela and carpus of fi rst pereiopod distinctly stouter and appendix interna, appendix interna of male second pleopod broader than chela and carpus of second pereiopod (Fig. (Fig. 38I) not reaching end of appendix masculina. 37K-M); chela of fi rst pereiopod 2.3-2.9 times as long as wide (n=20), 0.8-1.4 times length of carpus (n=48); tips of Ovigerous females with 12-18 eggs (n=4 females); egg size fi ngers rounded, without hooks; dactylus 1.2-1.5 times as 0.8-0.9 x 0.4-0.6 mm (n=53, eggs with and without eyes). long as palm (n=5); carpus 2.5-3.5 times as long as wide (n=20), 1.2-1.5 times length of merus (n=5). Chela of second Distribution. – Caridina spongicola is endemic to Lake pereiopod 3.0-4.0 times as long as wide (n=20), 0.7-0.8 times Towuti and so far only known from the outlet bay, where length of carpus (n=46); tips of fi ngers rounded, without its sponge host occurs (Fig. 36A; Zitzler & Cai, 2006). hooks, dactylus 1.3-1.7 times as long as palm (n=5); carpus 5.9-7.9 times as long as wide (n=20), 1.4-1.6 times as long Biology and ecology. – During an extensive substrate as merus (n=5). specifi c sampling in the Malili lake system in 2003, 2004, and 2005, Caridina spongicola was exclusively found on Third pereiopod (Fig. 37G-H) slender, dactylus 3.0-5.8 times a currently undescribed freshwater sponge of the suborder as long as wide (terminal spine included, without spines of Spongillina. It grows in the outlet of lake Towuti at depths

407 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 37. Caridina spongicola from the Malili lake system. A. Cephalothorax and cephalic appendages, female (ZMB 29027); B. Preanal carina; C. Scaphocerite,female (ZMB 29125); D. telson, female (ZMB 29027); E. Uropodal diaeresis; F. Distal end of telson; G. Third pereiopod; H. Dactylus of third pereiopod; I. Fifth pereiopod; J. Dactylus of fi fth pereiopod; K. First pereiopod; L. Second pereiopod; M. SEM image of chela and carpus of fi rst and second pereiopods. Scale bars: A, C = 1.0 mm; B, D, F-G, I, K-M = 0.5 mm; E, H, J = 0.1 mm. Figure modifi ed from Zitzler & Cai (2006).

408 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 38. Caridina spongicola from the Malili lake system. A. Cephalothorax and cephalic appendages, female (ZMB 29027); B. Mandible; C. Maxillule; D. First maxilliped; E. Third maxilliped; F. Second maxilliped; G. Maxilla; H. Endopod of male fi rst pleopod (ZMB 29027); I. Appendix masculina of male second pleopod fi fth pereiopod. Scale bars: A = 1.0 mm; B-G = 0.5 mm; H-I = 0.2 mm. Figure from Zitzler & Cai (2006), i.e. by the same authors.

409 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi of 2-5 (-10)m. The shrimps either occur on the sponge or distinctly stouter in C. parvula), and a different number of dwell inside its oscula (Zitzler & Cai, 2006; von Rintelen spines on the dactylus of the fi fth pereiopod (21-31, median et al., 2007b). 27 vs. 12-16, median 16 in C. loehae vs. 34-39, median 37 in C. parvula). A preliminary gut content analysis was carried out to investigate the shrimp’s diet (Zitzler & Cai, 2006). According In the molecular phylogeny (Figs. 63-64), C. spongicola to these authors, none of the six dissected guts contained appears within an unresolved clade of the rock dwellers C. traces of poriferean spicules. The spicules are presumably too striata, C. glaubrechti, and C. woltereckae (compare von big (0.2-0.3 mm) to be consumed by the shrimp. On the other Rintelen et al., 2007b), although C. spongicola differs in hand, a variety of diatoms, which possibly accumulate on or morphology and choice of habitat (sponge) from the other within the sponge, were found in the guts. These fi ndings species (for example its generally smaller size and a shorter suggest that the shrimp does not feed on sponge tissue and rostrum vs. rostrum reaching beyond end of scaphocerite in thus does not parasitize its host. Instead, it appears to be a the rock dwellers). commensal using the sponge’s cavities as shelter and the inherent accumulation of diatoms as a food supply (Zitzler & Cai, 2006). Caridina striata, new species (Figs. 39–41; Table 15) Colour pattern. – Carapace with three transversal dark brown bands (Fig.36C-D), first two usually joined at Caridina spinata – von Rintelen et al., 2007b: 262, fi g. 2b. dorsal surface to form a n-shaped band in lateral view. Anterior part of cephalothorax, antennular peduncle, bases Material examined. – Holotype: ovigerous female, cl 3.5 mm (MZB of antennae and posterior rostrum similarly pigmented, Cru 2121), Indonesia, Sulawesi Selatan, Lake Towuti, north shore, 02°38.56'S, 121°27.82'E, loc. 66-03, on rocks, coll. K. & T. von whereas anterior rostrum, antennae and distal antennules Rintelen, 26 Sep.2003. mostly unpigmented. First and second pereiopods white with brown bands, abdomen with a conspicuous white Paratypes (Lake Towuti) – 7 ex. (ZMB 29023, some SEM material), stripe expanding laterally along each side, dorsally densely north shore, bay east of Cape Bintu, 02°39.48'S, 121°33.25'E, loc. covered with dark brown bands except for a white patch on 68-03, on rocks, coll. K. & T. von Rintelen, 26 Sep.2003; 6 ex. third sternum, ventrally uniformly brown. Uropods with a (ZMB 29048, n=6, some SEM material), south shore, approx. 2 km characteristic brown band on distal endopods, endopods and east of Cape Mea, 02°55.8'S, 121°26.92'E, loc. 74-03, on rocks, coll. exopods with white-pigmented tips, respectively. Pleopods K. & T. von Rintelen, 28 Sep.2003; 11 ex. (MZB Cru 1815, n=5; and telson colourless. Eggs usually dark brown. This colour ZMB 29095, n=6, some SEM material), Loeha Island, north shore, 02°45.64'S, 121°34.32'E, loc. 97-03, on rocks, coll. K. & T. von pattern remains visible even if the shrimp is under stress, Rintelen, 4 Oct.2003; 2 ex. (ZMB 29169, n=2, some SEM material), the intensity of the colour merely fades (compare Zitzler & west shore, north of Cape Wasupute, 02°46.9'S, 121°27.94'E, loc. Cai, 2006; von Rintelen et al., 2007b). In a few specimens, 78-03, on rocks, coll. K. & T. von Rintelen, 28 Sep.2003; 4 ex. the colour pattern resembled C. glaubrechti, but the majority (ZMB 29170, n=4), north shore, west of Cape Manu, 02°41.67'S, was observed to be as mentioned above. 121°36.85'E, loc. 69-03, on boulders in deeper water, coll. K. & T. von Rintelen, 27 Sep.2003; 15 ex. (MZB Cru 1816, n=7; ZMB Taxonomic remarks. – The rostrum of C. spongicola displays 29171, n=8), north shore, at cape, 02°39.38'S, 121°29.73'E, loc. a high degree of variation within the populations (Fig. 36B; 67-03, on rocks in deeper water, coll. K. & T. von Rintelen, 26 compare Zitzler & Cai, 2006), similarly to many other Sep.2003; 40 ex. (MZB Cru 1817, n=25; ZMB 29172, n=15), north shore, 02°38.56'S, 121°27.82'E, loc. 66-03, on rocks, coll. K. & species from the Malili lakes. However, certain qualitative T. von Rintelen, 26 Sep.2003; 13 ex. (MZB Cru 1818, n=6; ZMB characters, i.e. the general shape or the arrangement of the 29173, n=7), southwest shore, west of Cape Tetetu, 02°54.13'S, rostral teeth, are constant not only in C. spongicola, but in 121°23.78'E, loc. 76-03, on rocks, coll. K. & T. von Rintelen, 28 all other ancient lake species (e.g. Schenkel, 1902; Woltereck Sep.2003; 13 ex. (MZB Cru 1819, n=6; ZMB 29174, n=7), west 1937a, b; Cai & Wowor, 2007). shore, south of Cape Timbalo, 02°42.91'S, 121°26.78'E, loc. 94-03, The colour morph of the majority of living specimens on rocks, coll. K. & T. von Rintelen, 4 Oct.2003; 16 ex. (MZB Cru closely resembles C. woltereckae, and both species can 1820, n=8; ZMB 29175, n=8), Loeha Island, west shore, 02°45.5'S, easily be confused in the fi eld, although C. woltereckae is 121°31.06'E, loc. 95-03, on rocks, coll. K. & T. von Rintelen, 4 a typical rock dweller and has a much wider distribution. Oct.2003; 9 ex. (MZB Cru 1821, n=4; ZMB 29176, n=5), east shore, 02°52.79'S, 121°31.18'E, loc. 72-03, on rocks, coll. K. & C. spongicola is generally smaller (carapace length 1.8- T. von Rintelen, 27 Sep.2003; 7 ex. (ZMB 29177), west shore, 2.8, median 2.4 vs. 2.4-3.8, median 2.8 in C. woltereckae) at entrance to outlet bay, Cape Larona, 02°48.43'S, 121°24.75'E, and has a shorter rostrum (reaching to or slightly beyond loc. 73-03, on rocks, coll. K. & T. von Rintelen, 8 Oct.2003; 4 ex. third segment of antennular peduncle vs. reaching beyond (ZMB 29178), east shore, south of Cape Tomeraka, 02°44.47'S, end of scaphocerite in C. woltereckae). Its smaller size (cl 121°37.53'E, loc. 70-03, on rocks, coll. K. & T. von Rintelen, 27 1.8-2.8 mm, median 2.4) also distinguishes C. spongicola Sep.2003; 9 ex. (ZMB 29299, n=9 and few juveniles, some SEM from most of the other lake species apart from C. loehae material), west shore, Cape Bakara, 02°40.771'S, 121°26.11'E, and C. parvula. From these, it differs by a longer rostrum loc. 144-04, on rocks in deeper water, coll. K. & T. von Rintelen, (reaching to or slightly beyond third segment of antennular 26 Jul.2004; 1 ex. (ZMB 29337), Loeha Island, southwest shore, 02°45.58'S, 121°31.14'E, loc. 149-04, on rocks in deeper water, peduncle vs. shorter in the other species), a different shape coll. K. & T. von Rintelen, 5 Aug.2004; 5 ex. (MZB Cru 1822), of the rostrum (more slender and fragile in C. loehae and

410 THE RAFFLES BULLETIN OF ZOOLOGY 2009 west shore, outlet bay, 02°46.277'S, 121°21.83'E, loc. 02-05, on K. & T. von Rintelen, 23 Sep.2003; 5 ex. (ZMB 29102, n=5, some sponge, coll. K. & T. von Rintelen, 3 Jan.2005. SEM material), east shore, 02°34.217'S, 121°30.681'E, loc. 147-04, on rocks, coll. K. & T. von Rintelen, 3 Aug.2004; 17 ex. (MZB Paratypes (Lake Mahalona) – 44 ex. (MZB Cru 1823, n=22; ZMB Cru 1824, n=8; ZMB 29298, n=9), north shore, at cape, 02°34.71'S, 29039, n=22 and some juveniles, some SEM material), northwest 121°29.144'E, loc. 148-04, on mixed substrate, coll. K. & T. von shore, at cape, 02°34.72'S, 121°29.12'E, loc. 56-03, on rocks, coll. Rintelen, 3 Aug.2004.

Fig. 39. Caridina striata from the Malili lake system. A. Cephalothorax and cephalic appendages, female with short and stout rostrum (ZMB 29048); B. Cephalothorax and cephalic appendages, female with long and slender rostrum (ZMB 29169); C. Rostrum variability (ZMB 29023); D. Uropodal diaeresis, male (ZMB 29023); E. Preanal carina, F. Scaphocerite; G. Telson, female with short and stout rostrum (ZMB 29048); H. Telson, female with long and slender rostrum (ZMB 29169); I. Dactylus of third pereiopod, female (ZMB 29048); J. Dactylus of fi fth pereiopod; K. Distal end of telson (ZMB 29048); L. Distal end of telson (ZMB 29169); M. Third pereiopod, female (ZMB 29048); N. Fifth pereiopod; O. Endopod of male fi rst pleopod (ZMB 29023); P. Appendix masculina of male second pleopod; Q. First pereiopod, female (ZMB 29048); R. Second pereiopod; S. SEM image of chela and carpus of fi rst and second pereiopods, female (ZMB 29095). Scale bars: A-C, F = 1.0 mm; E, G-H, M-S = 0.5 mm; D, I-L = 0.1 mm.

411 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Table 15. Summary of standard morphometric parameters for Caridina striata. parameter range mean ± SD median n cl (mm) 1.7-3.8 3.0 ± 0.5 3.1 36 rl / cl 0.8-2.4 1.3 ± 0.4 1.1 36 n dorsal rostral teeth 3-25 12 ± 8 15 36 n ventral rostral teeth 4-28 9 ± 6 7 36 abds6 / cl 0.5-0.8 0.6 ± 0.1 0.6 36 abds6 / abds5 1.4-2.1 1.7 ± 0.2 1.7 20 abds6 / h tel 0.8-1.1 1.0 ± 0.1 1.0 14 h tel / w tel 2.9-3.7 3.4 ± 0.4 3.4 5 n spines uropodal diaeresis 11-14 13 ± 1 13 5 h ch1 / w ch1 2.2-3.0 2.4 ± 0.2 2.4 21 h ch1 / h ca1 1.1-1.3 1.2 ± 0.1 1.2 35 h ca1 / w ca1 2.5-3.5 2.9 ± 0.3 2.8 21 h ch2 / w ch2 2.7-4.0 3.1 ± 0.3 3.0 22 h ch2 / h ca2 0.7-1.0 0.7 ± 0.1 0.7 20 h ca2 / w ca2 5.5-7.5 6.3 ± 0.5 6.1 21 n spines p3 2-3 3 ± 0 3 5 n spines p5 24-35 31 ± 5 33 5

Description. – Carapace length 1.7-3.8 mm (n=36). Rostrum teeth, molar process truncated. Lower lacinia of maxillula (Fig. 40A-C; Table 15) generally long to very long, anterior (Fig. 41B) broadly rounded, upper lacinia elongated, with upturned, reaching beyond end of scaphocerite; rostrum numerous distinct teeth and setae on inner margin, palp dimorphic, either very long and slender, reaching far beyond slender. Upper endites of maxilla (Fig. 41C) subdivided, end of scaphocerite (Fig. 40B) or shorter and broader with palp short, scaphognathite tapering posteriorly with numerous less teeth, reaching beyond end of scaphocerite (Fig. 40A); long, curved setae at posterior end. Distal end of palp of 0.8-2.4 times as long as carapace (n=36), armed dorsally with first maxilliped (Fig. 41F) triangular, with a finger-like 3-25 teeth (including 3-5 teeth posterior to orbital margin), projection; fl agellum of the exopod very elongated, endopod anterior less densely spaced, armed ventrally with 4-28 high, reaching half the fl agellum of exopod in length. Second teeth. Antennal spine situated below inferior orbital angle. maxilliped (Fig. 41E) typical. Third maxilliped (Fig. 41D) Pterygostomial angle broadly rounded. Eyes well developed, with ultimate segment distinctly shorter than penultimate anterior end 0.6 times length of basal segment of antennular segment. peduncle (n=5). Antennular peduncle 1.0-1.1 times as long as carapace (n=5), second segment 1.8-2.8 times length of Chela and carpus of fi rst pereiopod distinctly stouter and third segment, third segment 0.2-0.4 times length of basal broader than chela and carpus of second pereiopod (Fig. segment. Stylocerite reaching 0.9-1.1 times length of basal 40Q-S); chela of fi rst pereiopod 2.2-3.0 times as long as segment of antennular peduncle (n=5). Scaphocerite (Fig. wide (n=21), 1.1-1.3 times length of carpus (n=35); tips of 40F) 5.0-5.7 times as long as wide (n=5). fi ngers rounded, without hooks; dactylus 1.0-1.3 times as long as palm (n=7); carpus 2.5-3.5 times as long as wide Sixth abdominal somite 0.5-0.8 times length of carapace (n=21), 1.2-1.4 times length of merus (n=5). Chela of second (n=36), 1.4-2.1 times as long as fi fth somite (n=20), 0.8-1.1 pereiopod 2.7-4.0 times as long as wide (n=22), 0.7-1.0 times times length of telson (n=14). Telson (Fig. 40G-H, K-L) length of carpus (n=20); tips of fi ngers rounded, without 2.9-3.7 times as long as wide (n=5), distal margin rounded, hooks, dactylus 1.1-1.4 times as long as palm (n=7); carpus without projection, with 3-4 pairs of spinules and 1 pair 5.5-7.5 times as long as wide (n=21), 1.3-1.5 times as long of dorsolateral spinules; distal end with 4 pairs of spines, as merus (n=5). lateral pair distinctly longer than intermediate pairs, median pair not always shortest. Preanal carina (Fig. 40E) rounded, Third pereiopod (Fig. 40I,M) slender, dactylus 4.4-5.4 times without a spine. Uropodal diaeresis (Fig. 40D) with 11-14 as long as wide (terminal spine included, without spines movable spinules (n=5). of fl exor margin; n=5), terminating in one large claw with 2-3 accessory spines on fl exor margin; propodus 11.8-12.7 5 pairs of pleurobranchs well developed; 3 pairs of times as long as wide, 3.1-3.6 times as long as dactylus; arthrobranchs, 2 on third maxillipeds, with second pair carpus 5.2-6.6 times as long as wide, 0.6-0.7 times as long strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair as propodus, 0.5 times as long as merus; merus 8.9-9.7 of podobranchs on second maxilliped reduced strongly to times as long as wide, bearing 3-4 strong, movable spines a laminate form. Epipod present on fi rst pereiopod. Incisor on posterior margin of outer surface. process of mandible (Fig. 41A) ending in a row of 3-4 small

412 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 40. Caridina striata from the Malili lake system. A. Colour pattern of living animals (not to scale). B. Distribution. Picture on the right courtesy of Chris Lukhaup.

413 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fifth pereiopod slender (Fig. 40J,N), dactylus 4.4-6.0 times Ovigerous females with 17-38 eggs (n=3 females); egg size as long as wide (terminal spine included, without spines of 0.8-0.9 x 0.5 mm (n=37, eggs with and without eyes). fl exor margin; n=5), terminating in one large claw with 24- 35 accessory spines on fl exor margin; propodus 13.1-17.6 Distribution. – C. striata is endemic to the Malili lake system. times as long as wide, 3.1-4.2 times as long as dactylus; There, widely distributed and often numerous in Lake Towuti, carpus 5.0-6.4 times as long as wide, 0.5 times as long as but was also found in Lake Mahalona (Fig. 39B). propodus, 0.5-0.6 times as long as merus; merus 9.1-9.7 times as long as wide, bearing 3-4 strong, movable spines Biology and ecology. – C. striata is a hard substrate dweller on posterior margin of outer surface. on rocks. It occurs both in shallow water regions on and under smaller rocks, and in deeper water zones (below 3 m) Endopod of male first pleopod (Fig. 40O) elongated between larger rocks (boulders). When disturbed, it tries to triangular, 1.6-2.1 times as long as proximally wide (n=5), escape side- or downwards rather than in other directions. without appendix interna. Appendix interna of male second C. striata is often found in syntopy with other rock dwellers pleopod (Fig. 40P) 0.8-1.0 times length of appendix masculina in Lake Towuti, such as C. profundicola and C. spinata, but (n=5). particularly C. glaubrechti and C. woltereckae.

Fig. 41. Caridina striata from the Malili lake system. A. Mandible (ZMB 29172); B. Maxillula; C. Maxilla; D. third maxilliped; E. second maxilliped; F. fi rst maxilliped. Scale bars: A-F = 1mm.

414 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Colour pattern. – Body red, laterally with characteristic the distinct colour patterns in all three species were found to white stripes, dorsally with some white spots (Fig. 39A). be stable over the years of sampling. While morphological The uropods sometimes bear red and white patches on the differences are largely lacking, they differ in behaviour and distal margin. Appendages either transparent or reddish- distribution (compare von Rintelen et al., 2007b, in review). transparent. First and second pereiopod usually conspicuously C. striata was observed to be generally more active and white. When animals are feeding, the white chelipeds were faster than the other two rock dwellers and usually tried to observed to be always clearly visible, whereas the rest of the escape sidewards instead of staying attached to a rock as (darker coloured) body was more or less camoufl aged. This observed in C. glaubrechti and C. woltereckae. C. striata colour pattern remains visible even if the shrimp is under also occurs in Lake Mahalona, whereas the others seem to stress, the intensity of the colour merely fades. be restricted to Lake Towuti.

Etymology. – The name Caridina striata, new species, refers to the characteristic colour pattern of red and white stripes Caridina tenuirostris Woltereck, 1937a (the Latin word striatus means striped). (Figs. 42–45; Table 16)

Taxonomic remarks. – As alcohol bleached material, Caridina tenuirostris Woltereck, 1937a: 224, fi g. I.8, pls. 3,6 (type C. striata is almost identical with C. glaubrechti and C. locality: Lake Towuti at Lingkona). woltereckae, although the colour pattern in living animals Caridina tenuirostris – Woltereck, 1937b: 309, fi g. 12; Chace 1997: allows an unambiguous separation. It slightly differs from C. 20; von Rintelen et al., 2008: 2244, Table 1. Cardina tenuirostris – Brooks, 1950: 168 (erroneous spelling). woltereckae by a higher number of spines on the dactylus of Caridina Towutensis – Woltereck, 1937a: 220, fi g. I.2, pls. 3,6 the fi fth pereiopod (24-35, median 33 vs. 13-22, median 20 (type locality: Lake Towuti, South). in C. woltereckae). The dimorphic character of the rostrum Caridina towutensis – Woltereck, 1937b: 301, fi g. 7 (type locality in C. striata was not observed in the other two species. further specifi ed as Lake Towuti, South, Cape Sirioga); Chace, 1997: 20; von Rintelen et al., 2008: 2244, Table 1. In the molecular phylogeny (Figs. 63-64), all three species Cardina towutensis – Brooks, 1950: 168 (erroneous spelling). form a single clade with the sponge dweller C. spongicola, but their relationship is not resolved within this clade Material examined. – Neotype: ovigerous female (cl. 2.8 mm), (compare von Rintelen et al., 2007b, in review). However, Lake Towuti, southwest shore, west of Cape Tetetu, 02°54.13'S,

Fig. 42. Caridina tenuirostris from the Malili lake system. A. Distribution. B. Colour pattern of living animal (not to scale). Picture courtesy of Rainer Masche.

415 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Table 16. Summary of standard morphometric parameters for Caridina tenuirostris. parameter range mean ± SD median n cl (mm) 2.4-3.3 2.9 ± 0.2 2.9 32 rl / cl 1.1-1.8 1.5 ± 0.2 1.4 32 n dorsal rostral teeth 9-18 14 ± 2 14 32 n ventral rostral teeth 10-24 14 ± 3 15 32 abds6 / cl 0.6-0.9 0.8 ± 0.0 0.8 32 abds6 / abds5 1.8-2.3 2.0 ± 0.1 1.9 20 abds6 / h tel 1.0-1.5 1.2 ± 0.1 1.3 12 h tel / w tel 2.8-5.7 3.6 ± 1.2 3.4 5 n spines uropodal diaeresis 7-8 8 ± 0 8 5 h ch1 / w ch1 1.7-2.3 1.9 ± 0.2 1.9 20 h ch1 / h ca1 1.3-1.7 1.5 ± 0.1 1.5 32 h ca1 / w ca1 1.5-2.4 1.8 ± 0.2 1.8 20 h ch2 / w ch2 1.9-3.1 2.4 ± 0.4 2.3 20 h ch2 / h ca2 0.8-1.0 0.9 ± 0.1 0.9 32 h ca2 / w ca2 3.1-5.0 4.0 ± 0.7 3.8 20 n spines p3 3 - - 6 n spines p5 11-15 13 ± 1.7 14 6

121°23.78'E, loc. 76-03, on wood (MZB Cru 2126), coll. K. & T. Others (Lake Mahalona) – 47 ex. (MZB Cru 1789, n=23 and some von Rintelen, 28 Sep.2003. juveniles; ZMB 29040, n=24, some SEM material), northwest shore, at cape, 02°34.72'S, 121°29.12'E, loc. 56-03, on wood, coll. K. Others (Lake Towuti) – 32 ex. (MZB Cru 1782, n=17; ZMB 29034, & T. von Rintelen, 23 Sep.2003; 3 ex. (ZMB 29224), east shore, n=15, some SEM material), east shore, south of Cape Tomeraka, 02°34.217'S, 121°30.681'E, loc. 147-04, on wood, coll. K. & T. 02°44.47'S, 121°37.53'E, loc. 70-03, on wood, coll. K. & T. von von Rintelen, 3 Aug.2004; 6 ex. (ZMB 29071), Tominanga River, Rintelen, 27 Sep.2003; 27 ex. (MZB Cru 1783, n=15; ZMB 29043, approx. 2.2 km north of Lake Towuti, 02°36.5'S, 121°31.78'E, loc. n=12), wet shore, at entrance to outlet bay, Cape Larona, 02°48.43'S, 58-03, on wood, coll. K. & T. von Rintelen, 23 Sep.2003. 121°24.75'E, loc. 73-03, on wood, coll. K. & T. von Rintelen, 27 Sep.2003; 30 ex. (MZB Cru 1784, n=15; ZMB 29122, n=15), north Description. – Carapace length 2.4-3.3 mm (n=32). Rostrum shore, bay east of Cape Bintu, 02°39.48'S, 121°33.25'E, loc. 68-03, (Fig. 43A-B; Table 16) long and throughout slender, reaching on wood, coll. K. & T. von Rintelen, 26 Sep.2003; 10 ex. (ZMB far beyond end of scaphocerite, 1.1-1.8 times as long as 29123), east shore, 02°52.79'S, 121°31.18'E, loc. 72-03, on wood, carapace (n=32), armed dorsally with 9-18 teeth (including coll. K. & T. von Rintelen, 27 Sep.2003; 12 ex. (ZMB 29124), Loeha Island, west shore, 02°45.5'S, 121°31.06'E, loc. 95-03, on 1-4 teeth posterior to orbital margin), approx. anterior 2/3 wood, coll. K. & T. von Rintelen, 4 Oct.2003; 35 ex. (MZB Cru to ½ unarmed, without subapical teeth, armed ventrally with 1785, n=12; ZMB 29127, n=23, some SEM material), north shore, 10-24 teeth. Antennal spine situated below inferior orbital at cape, 02°29.73'S, 121°29.73'E, loc. 67-03, on wood, coll. K. angle. Pterygostomial angle broadly rounded. Eyes well & T. von Rintelen, 26 Sep.2003; 6 ex. (ZMB 29132), southwest developed, anterior end 0.6-0.7 times length of basal segment shore, Cape Sioloya, 02°50.7'S, 121°26.32'E, loc. 77-03, on wood, of antennular peduncle (n=5). Antennular peduncle 0.9-1.0 coll. K. & T. von Rintelen, 28 Sep.2003; 34 ex. (MZB Cru 1786, times as long as carapace (n=5), second segment 1.9-2.2 times n=20; ZMB 29133, n=14), southwest shore, west of Cape Tetetu, length of third segment, third segment 0.3 times length of 02°54.13'S, 121°23.78'E, loc. 76-03, on wood, coll. K. & T. von basal segment. Stylocerite reaching 0.8-0.9 times length of Rintelen, 28 Sep.2003; 6 ex. (ZMB 29134), west shore, north of Cape Wasupute, 02°46.9'S, 121°27.94'E, loc. 78-03, on wood, coll. basal segment of antennular peduncle (n=5). Scaphocerite K. & T. von Rintelen, 28 Sep.2003; 26 ex. (MZB Cru 1787, n=9; (Fig. 43F) 4.3-5.4 times as long as wide (n=5). ZMB 29300, n=17), east shore, 02°43.82'S, 121°39.211'E, loc. 115-04, on wood, coll. K. & T. von Rintelen, 28 Jul.2004; 3 ex. Sixth abdominal somite 0.6-0.9 times length of carapace (ZMB 29311), west shore, west of Cape Timbalo, 02°42.631'S, (n=32), 1.8-2.3 times as long as fi fth somite (n=20), 1.0-1.5 121°26.389'E, loc. 145-04, on mixed substrate with wood, coll. K. times length of telson (n=12). Telson (Fig. 43E,K) 2.8-5.7 & T. von Rintelen, 26 Jul.2004; 7 ex. (MZB Cru 1788, n=4; ZMB times as long as wide (n=5), distal margin rounded, without 29312, n=3), west shore, Cape Bakara, 02°40.771'S, 121°26.11'E, projection, with 3-4 pairs of spinules and 1 pair of dorsolateral loc. 144-04, on mixed substrate with wood, coll. K. & T. von spinules; distal end with 3-5 pairs of spines, lateral pair Rintelen, 26 Jul.2004; 3 ex. (ZMB 29450), west shore, Cape Bakara, 02°40.876'S, 121°26.043'E, loc. 225-05, on wood, coll. distinctly longer than intermediate pairs, median pair shortest. K. & T. von Rintelen, 23 Oct.2005; 13 ex. (ZMB 29130, n=13 Preanal carina (Fig. 43C) with a spine. Uropodal diaeresis and some juveniles, some SEM material), Larona River, close to (Fig. 43D) with 7-8 movable spinules (n=5). outlet bay, 02°45.8'S, 121°20.8'E, loc. 51-03, on wood, coll. K. & T. von Rintelen, 21 Sep.2003.

416 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 43. Caridina tenuirostris from the Malili lake system. A. Cephalothorax and cephalic appendages, male (ZMB 29127); B. Woltereck’s drawing of the rostrum (modifi ed from 1937a); C. Preanal carina, male (ZMB 29127); D. Uropodal diaeresis; E. telson, female (ZMB 29127); F. Scaphocerite, male (ZMB 29127); G. Third pereiopod; H. Fifth pereiopod; I. Dactylus of third pereiopod; J. Dactylus of fi fth pereiopod; K. Distal end of telson, female (ZMB 29127); L. First pereiopod, male (ZMB 29127); M. Second pereiopod; N. SEM image of chela and carpus of fi rst and second pereiopods, female (ZMB 29071); O. Endopod of male fi rst pleopod (ZMB 29127); P Appendix masculina of male second pleopod. Scale bars: A, F = 1.0 mm; C, E, G-H, L-P = 0.5 mm; D, I-K = 0.1 mm; B = no scale available.

417 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

5 pairs of pleurobranchs well developed; 3 pairs of Chela and carpus of fi rst pereiopod distinctly stouter and arthrobranchs, 2 on third maxillipeds, with second pair broader than chela and carpus of second pereiopod (Fig. strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair 43L-N); chela of fi rst pereiopod 1.7-2.3 times as long as of podobranchs on second maxilliped reduced strongly to wide (n=20), 1.3-1.7 times length of carpus (n=32); tips of a laminate form. Epipod on fi rst pereiopod. Incisor process fi ngers rounded, without hooks; dactylus 1.0-1.6 times as of mandible (Fig. 44A) ending in a row of 3-4 small teeth, long as palm (n=5); carpus 1.5-2.4 times as long as wide molar process truncated. Lower lacinia of maxillula (Fig. (n=20), 1.0-1.6 times length of merus (n=5). Chela of second 44B) broadly rounded, upper lacinia elongate, with numerous pereiopod 1.9-3.1 times as long as wide (n=20), 0.8-1.0 times distinct teeth and setae on inner margin, palp slender. Upper length of carpus (n=32); tips of fi ngers rounded, without endites of maxilla (Fig. 44C) subdivided, palp elongated, hooks, dactylus 1.5-1.7 times as long as palm (n=5); carpus scaphognathite broadly tapering posteriorly with numerous 3.1-5.0 times as long as wide (n=20), 1.1-1.3 times as long long, curved setae at posterior end. Distal end of palp of fi rst as merus (n=5). maxilliped (Fig. 44F) triangular, ending with a fi nger-like projection; fl agellum of the exopod short, endopod high, not Third pereiopod (Fig. 43G,I) slender, dactylus 2.0-3.2 times exceed the fl agellum of exopod in length. Second maxilliped as long as wide (terminal spine included, without spines of (Fig. 44E) typical. Third maxilliped (Fig. 44D) ultimate fl exor margin; n=6), terminating in one large claw with 3 segment slightly shorter than penultimate segment. accessory spines on fl exor margin; propodus 8.6-12.2 times

Fig. 44. Caridina tenuirostris from the Malili lake system. A. Mandible (ZMB 29133); B. Maxillula; C. Maxilla; D. third maxilliped; E. second maxilliped; F. fi rst maxilliped. Scale bars: A-F = 1mm.

418 THE RAFFLES BULLETIN OF ZOOLOGY 2009 as long as wide, 4.3-6.8 times as long as dactylus; carpus times as long as wide, 4.8-6.4 times as long as dactylus; 3.6-5.2 times as long as wide, 0.5-0.6 times as long as carpus 3.9-4.6 times as long as wide, 0.5-0.6 times as long propodus, 0.5 times as long as merus; merus 6.8-8.3 times as propodus, 0.6 times as long as merus; merus 6.1-7.3 as long as wide, bearing 2-3 strong, movable spines on times as long as wide, bearing 2 strong, movable spines on posterior margin of outer surface. posterior margin of outer surface.

Fifth pereiopod slender (Fig. 43H,J), dactylus 2.5-3.3 times Endopod of male first pleopod (Fig. 43O) elongated as long as wide (terminal spine included, without spines of triangular, 1.6-2.3 times as long as proximally wide (n=5), fl exor margin; n=6), terminating in one large claw with 11- without appendix interna. Appendix interna of male second 15 accessory spines on fl exor margin; propodus 10.5-14.4 pleopod (Fig. 26P) 0.9-1.0 times as long as appendix masculina (n=5).

Fig. 45. Caridina towutensis sensu Woltereck (1937a, b). A. The presumed type locality in Lake Towuti. B. Woltereck’s drawing of the rostrum (modifi ed from 1937a).

419 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Ovigerous females with 11-22 eggs (n=3 females); egg size Woltereck’s descriptions. A rather more plausible explanation 0.8-0.9 x 0.5-0.6 mm (n=51, eggs with and without eyes). is the misinterpretation of C. towutensis as a distinct species. Woltereck examined only nine specimens and might have Distribution. – C. tenuirostris is endemic to the Malili lake incidentally described local variations of another species. system. It occurs in Lake Towuti, Lake Mahalona, and the Woltereck’s drawing of the rostrum (Fig. 45B) closely connecting Tominanga River as well as Larona River close resembles juveniles or small adults (usually males) of C. to the outlet bay of Lake Towuti (Fig. 42A; for localitiy tenuirostris, that have not developed full rostrum length names see Fig. 1.C). yet. Consequently, we here synonymize C. towutensis with C. tenuirostris. Biology and ecology. – With its rather stout first and second pereiopods, C. tenuirostris represents a typical hard- substrate dweller. The majority of specimens were collected Caridina woltereckae Cai, Wowor & Choy, 2009 from wood. It often occurs syntopically on wood with C. (Figs. 46–47; Table 17) lanceolata in Lake Towuti and Lake Mahalona, but whereas C. lanceolata occurs on various substrates, the occurrence Caridina woltereckae Cai et al., 2009: 19, Fig. 3 (type locality: of C. tenuirostis is mainly restricted to wood. Lake Towuti, Cape Larona, near Sungai [River] Larona outlet, rocky coast with white sand substrate). Colour pattern. – The primary colour of C. tenuirostris is Caridina sp.2 – von Rintelen et al., 2007b: 262, fi g. 2b. brown with several white transversal stripes all over the Material examined. – Lake Towuti: 28 ex. (MZB Cru 1828, body (Fig. 42B). A conspicuous white band is visible at the n=10 and few juveniles; ZMB 29037, n=18, some SEM material), distal part of the abdomen. Appendages are transparent or west shore, at entrance to outlet bay, Cape Larona, 02°48.43'S, partly brownish. This colour pattern remains visible even 121°24.75'E, loc. 73-03, (MZB) on mixed substrate, (ZMB) on if the shrimp is under stress, though the intensity of the rocks, coll. K. & T. von Rintelen, 8 Oct.2003; 24 ex. (MZB Cru colour merely fades. 1829, n=12; ZMB 29044, n=12, some SEM material), north shore, bay east of Cape Bintu, 02°39.48'S, 121°33.25'E, loc. 68-03, on Taxonomic remarks. – The arrangement of rostral teeth rocks, coll. K. & T. von Rintelen, 26 Sep.2003; 13 ex. (MZB Cru slightly resembles that in C. lanceolata, but C. tenuirostris has 1830, n=6; ZMB 29052, n=7, some SEM material), Loeha Island, west shore, 02°45.5'S, 121°31.06'E, loc. 95-03, on rocks, coll. K. a distinctly more slender rostrum, a higher number of ventral & T. von Rintelen, 4 Oct.2003; 13 ex. (MZB Cru 1831, n=7; ZMB teeth (10-24, median 15 vs. 4-13, median 7 in C. lanceolata), 29106, n=6, some SEM material), southwest shore, west of Cape always lacking subapical teeth, and a shorter sixth abdominal Tetetu, 02°54.13'S, 121°23.78'E, loc. 76-03, on rocks, coll. K. & T. somite compared to carapace length (0.6-0.9, median 0.8 vs. von Rintelen, 28 Sep.2003; 4 ex. (ZMB 29144), west shore, south 0.8-1.1, median 1.0 in C. lanceolata). The pereiopods are of Cape Timbalo, 02°42.91'S, 121°26.78'E, loc. 94-03, on rocks, further distinctively stouter than in C. lanceolata. The colour coll. K. & T. von Rintelen, 4 Oct.2003; 7 ex. (ZMB 29145), Loeha pattern of C. tenuirostris closely resembles C. glaubrechti, Island, north shore, 02°45.64'S, 121°34.32'E, loc. 97-03, on rocks, but both species not only differ in their substrate preference coll. K. & T. von Rintelen, 4 Oct.2003; 21 ex. (MZB Cru 1832, (wood vs. rocks in C. glaubrechti), but by the continuous n,=9; ZMB 29146, n=12), north shore, 02°38.56'S, 121°27.82'E, loc. 66-03, on rocks, coll. K. & T. von Rintelen, 26 Sep.2003; 13 dorsal denticulation of the rostrum (vs. anterior dorsal part ex. (MZB Cru 1833, n=6; ZMB 29147, n=7, some SEM material), always completely unarmed in C. tenuirostris), a different north shore, at cape, 02°39.38'S, 121°29.73'E, loc. 67-03, on rocks number of spines on the uropodal diaeresis (7-8, median 8 in deeper water, coll. K. & T. von Rintelen, 26 Sep.2003; 2 ex. vs. 11-14, median 12 in C. glaubrechti), and on the dactylus (ZMB 29148, n=2 and few juveniles, some SEM material), north of the fi fth pereiopod (11-15, median 14 vs. 14-35, median shore, west of Cape Manu, 02°41.67'S, 121°36.85'E, loc. 69-03, 28 in C. glaubrechti). on rocks in deeper water, coll. K. & T. von Rintelen, 27 Sep.2003; 1 ex. (ZMB 29149, n=1 and few juveniles), west shore, north of In the molecular phylogeny (Figs. 63-64), C. tenuirostris is Cape Wasupute, 02°46.9'S, 121°27.94'E, loc. 78-03, on rocks, genetically distinct from all other ancient lake species. coll. K. & T. von Rintelen, 28 Sep.2003; 3 ex. (ZMB 29151), east shore, south of Cape Tomeraka, 02°44.47'S, 121°37.53'E, loc. 70-03, on rocks, coll. K. & T. von Rintelen, 27 Sep.2003; 1 ex. Woltereck’s (1937a) species C. towutensis was never reported (ZMB 29310, n=1, some SEM material), west shore, north of Cape by any later collectors, e.g. neither by M. Kottelat nor C. Sioloya, 02°50.386'S, 121°26.026'E, loc. 03-05, on rocks, coll. Y. Schubart (see Cai et al., 2009), and was not found during Cai, K. & T. von Rintelen, 3 Jan.2005; 4 ex. (ZMB 29331), west fi eldwork for this study at the Malili lakes including an shore, northeast shore, at Cape Noote, 02°39.751'S, 121°39.195'E, exhaustive search at the (presumed) type locality at Cape loc. 117-04, on rocks in deeper water, coll. K. & T. von Rintelen, Sirioga [Sioloya], Lake Towuti, in 2005 (Fig. 45A; Yixiong 28 Jul.2004; 13 ex. (MZB Cru 1834, n=7; ZMB 29332, n=6), Cai, K. & T. von Rintelen, pers. fi eld observation). However, Cape Bakara, 02°40.771'S, 121°26.11'E, loc. 144-04, on rocks in at this locality (loc. 77-03) other species were found, i.e. deeper water, coll. K. & T. von Rintelen, 26 Jul.2004; 3 ex. (ZMB 29333), west shore, outlet bay, east of Cape Kombe, 02°48.08'S, C. lanceolata, C. parvula, C. masapi, and C. tenuirostris. 121°23.05'E, loc. 53-03, on rocks, coll. K. & T. von Rintelen, 21 A possible explanation could be the extinction of this tiny Sep.2003; 4 ex. (ZMB 29334), west shore, west of Cape Timbalo, species (“total length of largest specimen including the 02°42.631'S, 121°26.389'E, loc. 145-04, on rocks, coll. K. & T. rostrum 16 mm”; Woltereck, 1937b: 301), but this seems von Rintelen, 26 Jul.2004. unlikely for no other species has become extinct since

420 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Description. – Carapace length 2.4-3.8 mm (n=26). of dorsolateral spinules; distal end with 4 pairs of spines, Rostrum (Fig. 47A; Table 17) long, reaching beyond end of lateral pair distinctly longer than intermediate pairs, median scaphocerite, 1.0-1.6 times as long as carapace (n=20), armed pair not always shortest. Preanal carina (Fig. 47C) rounded, dorsally with 13-22 teeth (including 3-4 teeth posterior to without a spine. Uropodal diaeresis (Fig. 47D) with 11-13 orbital margin), anterior less densely spaced, armed ventrally movable spinules (n=5). with 3-13 teeth. Antennal spine situated below inferior orbital angle. Pterygostomial angle broadly rounded. Eyes well 5 pairs of pleurobranchs well developed; 3 pairs of developed, anterior end 0.5-0.6 times length of basal segment arthrobranchs, 2 on third maxillipeds, with second pair of antennular peduncle (n=5). Antennular peduncle 0.9-1.0 strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair times as long as carapace (n=5), second segment 2.0-2.3 times of podobranchs on second maxilliped reduced strongly to length of third segment, third segment 0.3 times length of a laminate form. Epipods only present on fi rst pereiopod. basal segment. Stylocerite reaching 0.9-1.0 times length of Mouthparts as described by Cai et al. (2009). basal segment of antennular peduncle (n=5). Scaphocerite (Fig. 47B) 4.7-5.6 times as long as wide (n=5). Chela and carpus of fi rst pereiopod distinctly stouter and broader than chela and carpus of second pereiopod (Fig. Sixth abdominal somite 0.6-0.9 times length of carapace 47M-O); chela of fi rst pereiopod 2.0-2.5 times as long as (n=26), 1.5-1.8 times as long as fi fth somite (n=20), 0.9 wide (n=20), 1.2-1.5 times length of carpus (n=26); tips of times length of telson (n=7). Telson (Fig. 47E,H) 3.3- fi ngers rounded, without hooks; dactylus 1.0-1.5 times as 3.9 times as long as wide (n=5), distal margin rounded, long as palm (n=6); carpus 2.1-2.9 times as long as wide without projection, with 3-4 pairs of spinules and 1 pair (n=20), 1.2-1.3 times length of merus (n=5). Chela of second

Fig. 46. Caridina woltereckae from the Malili lake system. A. Distribution. B.-C. Colour pattern of living animals (not to scale). Pictures courtesy of Chris Lukhaup.

421 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Table 17. Summary of standard morphometric parameters for Caridina woltereckae. parameter range mean ± SD median n cl (mm) 2.4-3.8 2.8 ± 0.3 2.8 26 rl / cl 1.0-1.6 1.3 ± 0.2 1.3 20 n dorsal rostral teeth 13-22 18 ± 2 19 26 n ventral rostral teeth 3-13 8 ± 2 7 26 abds6 / cl 0.6-0.9 0.6 ± 0.1 0.6 26 abds6 / abds5 1.5-1.8 1.6 ± 0.1 1.6 20 abds6 / h tel 0.9 - - 7 h tel / w tel 3.3-3.9 3.5 ± 0.3 3.4 5 n spines uropodal diaeresis 11-13 12 ± 1.0 13 5 h ch1 / w ch1 2.0-2.5 2.2 ± 0.1 2.3 20 h ch1 / h ca1 1.2-1.5 1.3 ± 0.1 1.3 26 h ca1 / w ca1 2.1-2.9 2.6 ± 0.2 2.6 20 h ch2 / w ch2 2.4-3.1 2.7 ± 0.2 2.7 20 h ch2 / h ca2 0.7-1.0 0.8 ± 0.0 0.8 25 h ca2 / w ca2 4.8-7.3 6.1 ± 0.7 6.1 20 n spines p3 1-2 2 ± 0 2 5 n spines p5 13-22 19 ± 4 20 5 pereiopod 2.4-3.1 times as long as wide (n=20), 0.7-1.0 times Distribution. – C. woltereckae is endemic to Lake Towuti, length of carpus (n=25); tips of fi ngers rounded, without where it is widely distributed (Fig. 46A). hooks, dactylus 1.3-1.6 times as long as palm (n=6); carpus 4.8-7.3 times as long as wide (n=20), 1.4-1.5 times as long Biology and ecology. – C. woltereckae is a hard substrate as merus (n=5). dweller on smaller rocks mainly in shallow water, but also in deeper water regions (below 3 m) between larger Third pereiopod (Fig. 47F-G) slender, dactylus 2.8-4.0 times rocks (boulders). When disturbed, in tries to escape side- as long as wide (terminal spine included, without spines or downwards rather than in other directions, but mainly of fl exor margin; n=5), terminating in one large claw with stays attached to rocks. C. woltereckae is often found in 1-2 accessory spines on fl exor margin; propodus 12.5-17.0 syntopy with other rock dwellers in Lake Towuti, such as times as long as wide, 4.8-6.5 times as long as dactylus; C. profundicola, C. spinata, C. striata, or C. glaubrechti. carpus 5.5-6.5 times as long as wide, 0.5-0.6 times as long as propodus, 0.5 times as long as merus; merus 9.2-9.9 Colour pattern. – Carapace with three transversal dark times as long as wide, bearing 2-3 strong, movable spines brown (sometimes reddish) bands (Fig. 46B-C), fi rst two on posterior margin of outer surface. usually joint at dorsal surface to form a n-shaped band in lateral view. Appendages are either transparent or slightly Fifth pereiopod slender (Fig. 47I-J), dactylus 3.4-4.5 times pigmented. Most parts of first and second pereiopods as long as wide (terminal spine included, without spines of usually bright white, abdomen with a conspicuous white fl exor margin; n=5), terminating in one large claw with 13- stripe expanding laterally along each side, dorsally densely 22 accessory spines on fl exor margin; propodus 16.0-22.0 covered with dark brown bands except for a white belt on times as long as wide, 4.4-5.8 times as long as dactylus; the posterior of the carapace. Uropods with white-pigmented carpus 4.9-6.5 times as long as wide, 0.5-0.6 times as long tips or unpigmented. Eggs usually dark brown. This colour as propodus, 0.6 times as long as merus; merus 9.1-10.0 pattern remains visible even if the shrimp is under stress, times as long as wide, bearing 2-3 strong, movable spines the intensity of the colour merely fades. When feeding, the on posterior margin of outer surface. white chelipeds were observed to be always clearly visible, whereas the rest of the (darker coloured) body was more or Endopod of male first pleopod (Fig. 47K) elongated less camoufl aged. triangular, 1.6-2.0 times as long as proximally wide (n=5), without appendix interna. Appendix interna of male second Taxonomic remarks. – The colour morph of living specimens pleopod (Fig. 47L) 0.8-0.9 times length of appendix closely resembles C. spongicola. Therefore, both species can masculina (n=5). easily be confused in the fi eld, although C. woltereckae is a typical rock dweller and has a much wider distribution Ovigerous females with 19-29 eggs (n=2 females); egg size (vs. sponge dweller and restricted to the outlet bay of Lake 0.8-1.0 x 0.5-0.6 mm (n=48, eggs with eyes). Towuti). It is generally also larger (carapace length 2.4-3.8, median 2.8 vs. in 1.8-2.8, median 2.4 in C. spongicola) and has a longer rostrum (reaching beyond end of scaphocerite

422 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 47. Caridina woltereckae from the Malili lake system. A. Cephalothorax and cephalic appendages, female (ZMB 29052); B. Scaphocerite, female (ZMB 29037); C. Preanal carina; D. Uropodal diaeresis, female (ZMB 29310); E. Telson, F. Third pereiopod, female (ZMB 29147); G. Dactylus of third pereiopod; H. Distal end of telson, female (ZMB 29310); I. Fifth pereiopod, female (ZMB 29147); J. Dactylus of fi fth pereiopod; K. Endopod of male fi rst pleopod (ZMB 29037); L. Appendix masculina of male second pleopod; M. SEM image of chela and carpus of fi rst and second pereiopods, female (ZMB 29052); N. First pereiopod, female (ZMB 29052); O.; P. Second pereiopod. Scale bars: A-B = 1.0 mm; C, E-F, I, K-O = 0.5 mm; D, G-H, J = 0.1 mm.

423 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi vs. reaching to or slightly beyond third segment of antennular Sixth abdominal somite 0.6 times length of carapace (n=9), peduncle in C. spongicola). As alcohol bleached material, 1.7-2.0 times as long as fi fth somite (n=5), 0.9-1.0 times length C. woltereckae is almost identical with C. striata and C. of telson (n=5). Telson (Fig. 49G,J) 3.0-3.3 times as long as glaubrechti, although the colour pattern in living specimens wide (n=5), distal margin rounded, without projection, with always allows an unambiguous separation. It slightly differs 4-5 pairs of spinules and 1 pair of dorsolateral spinules; distal from both by a lower number of spines on the dactylus of end with 4-5 pairs of spines. Preanal carina (Fig. 49E) with the fi fth pereiopod (13-22, median 20 vs. 14-35, median 28 a spine. Uropodal diaeresis (Fig. 49F) with 11-17 movable in C. glaubrechti and 24-35, median 33 in C. striata). Also spinules (n=5). the dimorphic character of the rostrum in C. striata could not be observed in C. woltereckae. 5 pairs of pleurobranchs well developed; 3 pairs of arthrobranchs, 2 on third maxillipeds, with second pair In the molecular phylogeny (Figs. 63-64), C. woltereckae strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair forms a single clade with the other rock dwellers C. striata of podobranchs on second maxilliped reduced strongly to and C. glaubrechti, and the sponge dweller C. spongicola, but a laminate form. Epipods present on fi rst two pereiopod, their relationship is not resolved within this clade (compare reduced or totally absent from third pereiopod. Incisor von Rintelen et al., 2007b; for further details see taxonomic process of mandible (Fig. 50A) ending in a row of 3- remarks on C. striata). 5 small teeth, molar process truncated. Lower lacinia of maxillula (Fig. 50B) broadly rounded, upper lacinia elongate, with numerous distinct teeth and setae on inner SPECIES FROM LAKE POSO (INDONESIA, margin, palp slender. Upper endites of maxilla (Fig. 50C) CENTRAL SULAWESI) subdivided, palp short, scaphognathite tapering posteriorly with numerous long, curved setae at posterior end. Distal Caridina acutirostris Schenkel, 1902 end of palp of fi rst maxilliped (Fig. 50F) triangular, ending (Figs. 48–50; Table 18) with a short fi nger-like projection; fl agellum of the exopod elongated, endopod high, not exceeding the fl agellum of Caridina acutirostris Schenkel, 1902: 496, pl. 8, Figs. 3a-c, 4b (type locality: area south of Lake Poso, approx. 600 m above sealevel). Caridina acutirostris – Roux, 1904: 551; Bouvier, 1905: 73, 1925: 166, Figs. 353-355; Chace, 1997: 6; Cai & Wowor, 2007: 314; von Rintelen et al., 2007a: 1033, fi g. 2; Tables 1-2, 2008: 2244, Table 1.

Material examined. – Holotype: female (cl 5.2mm) (NHMB 3a), area south of Lake Poso, approx. 600 m above sealevel, coll. Sarasin, 1907.

Lake Poso catchment: 14 ex. (MZB Cru 1843, n=7; ZMB 29439, n=7), Tonusu, approx. 3 km south of Tonusu towards Siuri, 01°48.95'S, 120°31.18'E, loc. 185-05, on macrophytes, coll. K. von Rintelen, 6 Oct.2005; 11 ex. (MZB Cru 1844, n=5; ZMB 29440, n=6 and some juveniles, some SEM material), stream south of Pendolo, 02°8.702'S, 120°43.854'E, loc. 196-05, on roots, coll. K. von Rintelen, 8 Oct.2005.

Description. – Carapace length 3.1-5.8 mm (n=11). Rostrum (Fig. 49A-C; Table 18) short, usually shorter than scaphocerite, reaching to or near distal end of second segment of antennular peduncle, in large females sometimes reaching near end of scaphocerite, 0.3-0.7 times as long as carapace (n=11), armed dorsally with 10-13 teeth (including 3-4 teeth posterior to orbital margin), about anterior third to half unarmed, without subapical teeth, armed ventrally with 4-9 teeth. Antennal spine situated below inferior orbital angle. Pterygostomial angle broadly rounded. Eyes well developed, anterior end 0.6-0.7 times length of basal segment of antennular peduncle (n=5). Antennular peduncle 0.7-1.1 times as long as carapace (n=5), second segment 1.4-1.8 times length of third segment, third segment 0.3-0.4 times length of basal segment. Stylocerite reaching 0.9-1.0 times length of basal segment of antennular peduncle (n=5). Scaphocerite Fig. 48. Distribution of Caridina acutirostris in the Poso (Fig. 49D) 3.0-3.6 times as long as wide (n=5). catchment.

424 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 18. Summary of standard morphometric parameters for Caridina acutirostris. parameter range mean ± SD median n cl (mm) 3.1-5.8 4.3 ± 0.7 4.1 11 rl / cl 0.3-0.7 0.5 ± 0.1 0.5 11 n dorsal rostral teeth 10-13 11 ± 1 11 11 n ventral rostral teeth 4-9 5 ± 2 4 11 abds6 / cl 0.6 - - 9 abds6 / abds5 1.7-2.0 1.8 ± 0.1 1.8 5 abds6 / h tel 0.9-1.0 1.0 ± 0.0 1.0 5 h tel / w tel 3.0-3.3 3.1 ± 0.1 3.1 5 n spines uropodal diaeresis 11-17 14 ± 2 13 5 h ch1 / w ch1 2.0-2.6 2.3 ± 0.2 2.2 8 h ch1 / h ca1 1.2-1.3 1.3 ± 0.0 1.3 8 h ca1 / w ca1 2.0-2.7 2.2 ± 0.3 2.1 8 h ch2 / w ch2 2.9-3.4 3.2 ± 0.2 3.2 8 h ch2 / h ca2 0.8-0.9 0.8 ± 0.0 0.8 8 h ca2 / w ca2 4.5-5.9 5.1 ± 0.5 4.9 8 n spines p3 4-9 6 ± 2 6 5 n spines p5 45-66 55 ± 7.6 55 5 exopod in length. Second maxilliped (Fig. 50D) typical. without appendix interna. Appendix interna of male second Third maxilliped (Fig. 50E) with ultimate segment slightly pleopod (Fig. 49N) 0.7-0.8 times length of appendix shorter than penultimate segment. masculina (n=4).

Chela and carpus of fi rst pereiopod distinctly stouter and Ovigerous females with 23-54 eggs (n=2 females); egg size broader than chela and carpus of second pereiopod (Fig. 1.1-1.3 x 0.7-0.8 mm (n=20, eggs with and without eyes). 49O-Q); chela of fi rst pereiopod 2.0-2.6 times as long as wide (n=8), 1.2-1.3 times length of carpus (n=8); tips of Distribution. – C. acutirostris is endemic to the Poso river fi ngers rounded, without hooks; dactylus 0.7-1.4 times as catchment occurring in streams around the lake (Fig. 48). long as palm (n=5); carpus 2.0-2.7 times as long as wide So far only known from two distant localities, the southern (n=8), 1.1-1.2 times length of merus (n=5). Chela of second one is the type locality “Salukuwa and other small streams, pereiopod 2.9-3.4 times as long as wide (n=8), 0.8-0.9 times drainage of Kodina River, south of Lake Poso”, where Fritz length of carpus (n=8); tips of fi ngers rounded, without and Paul Sarasin collected the specimens of C. acutirostris hooks, dactylus 1.0-1.4 times as long as palm (n=5); carpus (Sarasin & Sarasin, 1905: 238) later described by Schenkel 4.5-5.9 times as long as wide (n=8), 1.4-1.6 times as long (1902). as merus (n=5). Dactylus of third pereiopod (Fig. 49H,K) 3.2-3.9 times as In the molecular phylogeny (Figs. 63,65), two specimens long as wide (terminal spine included, without spines of referred to as C. cf. acutirostris from the Tomori region fl exor margin; n=5), terminating in one large claw with 4-9 cluster with specimens of C. acutirostris (compare von accessory spines on fl exor margin; propodus 8.6-11.1 times Rintelen et al., 2007a). These have not been included here as long as wide, 3.3-3.7 times as long as dactylus; carpus due to differences in morphology and their geographic origin. 4.6-5.7 times as long as wide, 0.6-0.7 times as long as Their taxonomic status awaits further investigation. propodus, 0.5 times as long as merus; merus 7.1-9.2 times as long as wide, bearing 2-3 strong, movable spines on posterior Biology and ecology. – C. acutirostris is an exclusively margin of outer surface. Dactylus of fi fth pereiopod (Fig. riverine species that was collected from vegetation (green 49I,L) 4.0-5.6 times as long as wide (terminal spine included, parts and roots). It was never found in sympatry with the without spines of fl exor margin; n=5), terminating in one other riverine species endemic to the Poso system (C. large claw with 45-66 accessory spines on fl exor margin; schenkeli). propodus 10.0-12.5 times as long as wide, 2.9-3.2 times as long as dactylus; carpus 4.1-5.5 times as long as wide, 0.5 Colour pattern. – Without any species specifi c pattern. times as long as propodus, 0.6 times as long as merus; merus Body colouration transparently yellowish or brownish, 6.7-7.9 times as long as wide, bearing 2-3 strong, movable typical for riverine species from all over Sulawesi. Large spines on posterior margin of outer surface. (often ovigerous) females usually appear darker than smaller specimens. Endopod of male first pleopod (Fig. 49M) elongated triangular, 2.1-2.4 times as long as proximally wide (n=4),

425 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 49. Caridina acutirostris from the Lake Poso catchment. A. Schenkel’s drawing of cephalothorax and cephalic appendages (modifi ed from 1902); B. Cephalothorax and cephalic appendages, male (ZMB 29440); C. Cephalothorax and cephalic appendages, another male (ZMB 29440); D. Scaphocerite, female (ZMB 29440); E. Preanal carina, F. Uropodal diaeresis, male (ZMB 29440); G. Telson; H. Third pereiopod; I. Fifth pereiopod; J. Distal end of telson; K. Dactylus of third pereiopod; L. Dactylus of fi fth pereiopod; M. Endopod of male fi rst pleopod; N. Appendix masculina of male second pleopod; O. First pereiopod; P. Second pereiopod; Q. SEM image of chela and carpus of fi rst and second pereiopods. Scale bars: B-D = 1.0 mm; E,G-I, M-Q = 0.5 mm; F, J-L = 0.1 mm; A = no scale available.

426 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Taxonomic remarks. – C. acutirostris differs from all Poso schenkeli). Further, C. acutirostris can resemble specimens species by the short rostrum (usually not reaching end of of C. mahalona (Malili lakes) with a short rostrum, although scaphocerite vs. longer in all other species) and the ratio the scaphocerite usually is stouter (3.0-3.6 times as long as of rostrum to carapace length (0.3-0.7, median 0.5 vs. over wide vs. 3.5-4.1 times as long as wide in C. mahalona). 0.7 in the other species). With regard to the rostrum and Further, the carpus of the fi rst and second pereiopod is body size, C. acutirostris mainly resembles C. schenkeli stouter (2.0-2.7 and 4.5-5.9 times as long as wide vs. 2.5- (carapace length in mm 3.1-5.8, median 4.1 and 3.6-5.1, 3.3 and 5.6-7.0 times as long as wide in C. mahalona). The median 4.2 in C. schenkeli), but differs by the length of the general range of parameters (for example the number of rostrum (shorter in C. acutirostris), and a lower number of rostral teeth) is usually higher in C. mahalona than in C. ventral rostral teeth (4-9, median 4 vs. 9-13, median 11 in C. acutirostris (Tables 10,19).

Fig. 50. Caridina acutirostris from the Lake Poso catchment. A. Mandible (ZMB 29440); B. Maxillula; C. Maxilla; D. second maxilliped; E. third maxilliped; F. fi rst maxilliped. Scale bars: A-F = 1mm.

427 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

In the molecular phylogeny (Figs. 63, 65) C. acutirostris Paratypes (Lake Poso) – 1 ex. (ZMB 29207), east shore, 01°59.867'S, is genetically distinct from all other Poso species, however 120°41.238'E, loc. 160-04, on mixed substrate, coll. K. & T. von appears within the Poso clade (for a detailed discussion see Rintelen, 16 Aug.2004; 17 ex. (MZB Cru 1718, n=9; ZMB 29251, von Rintelen et al., 2007a). n=8, some SEM material), south shore, Pendolo, beach at Hotel Mulia, 02°3.876'S, 120°41.587'E, loc. 50-04, on wood, coll. M. Glaubrecht & T. von Rintelen, 27 Mar.2004; 16 ex. (MZB Cru 1719, n=7; ZMB 29260, n=9, some SEM material), west shore, Cape Caridina caerulea, new species Bancea, 01°59.023'S, 120°35.108'E, loc. 59-04, on rocks in shallow (Figs. 51–53; Tables 19–20) water, coll. M. Glaubrecht & T. von Rintelen, 29 Mar.2004; 1 ex. (ZMB 29290, n=1 and some juveniles, some SEM material), south Caridina ensifera Schenkel, 1902 pro parte: 490, pl. 8, Figs. 1a-e, shore, Pendolo beach at Hotel Mulia, 02°3.928'S, 120°41.536'E, 4d (type locality: Lake Poso). loc. 157-04, on wood, coll. K. & T. von Rintelen, 15 Aug.2004; Caridina ensifera – Cai & Wowor, 2007 pro parte: 311, Figs. 8 ex. (ZMB 29292a, n=2; ZMB 29292b, n=6), east shore, south 1-2. of Cape Sinampada, 01°56.25'S, 120°40.443'E, loc. 159-04, (a) on Caridina ensifera “blue” – von Rintelen et al., 2007a: 1034, Figs. rocks in deeper water (approx. 13 m), (b) on macrophytes, coll. M. 1-2, Tables 1-2. Glaubrecht & T. von Rintelen, 29 Mar.2004; 5 ex. (ZMB 29306), east shore, Tando Bone, 01°50.0'S, 120°38.004'E, loc. 157-05, on Material examined. – Holotype –male (cl 4.4 mm)(MZB Cru 2123), wood, coll. K. von Rintelen, 3 Oct.2005; 13 ex. (MZB Cru 1720, n=6; Lake Poso, west shore, Cape Bancea, 01°59.023'S, 120°35.108'E, ZMB 29325, n=7), west shore, Siuri, 01°48.259'S, 120°31.667'E, loc. 59-04, on rocks in shallow water, coll. M. Glaubrecht & T. loc. 186-05, on mixed substrate, coll. K. von Rintelen, 6 Oct.2005; von Rintelen, 29 Mar.2004. 4 ex. (ZMB 29382), north shore, 01°47.162'S, 120°33.144'E, loc.

Fig. 51. Caridina caerulea from Lake Poso. A. Distribution. B-C. Colour pattern of living animals (not to scale). Picture B. courtesy of Chris Lukhaup.

428 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 19. Summary of standard morphometric parameters for Caridina caerulea.

cl (mm) 3.0-4.5 3.7 ± 0.4 3.7 40 rl / cl 1.9-2.6 2.2 ± 0.2 2.2 40 n dorsal rostral teeth 11-20 15 ± 2 16 40 n ventral rostral teeth 26-48 34 ± 5 34 40 abds6 / cl 0.4-0.8 0.7 ± 0.1 0.7 40 abds6 / abds5 1.0-2.5 2.0 ± 0.2 2.0 40 abds6 / h tel 0.9-1.0 0.9 ± 0.0 0.9 5 h tel / w tel 3.5-4.1 3.8 ± 0.3 3.9 5 n spines uropodal diaeresis 11-14 12 ± 1.1 12 5 h ch1 / w ch1 1.9-2.7 2.2 ± 0.2 2.2 40 h ch1 / h ca1 0.9-1.5 1.3 ± 0.1 1.3 40 h ca1 / w ca1 1.9-5.1 2.4 ± 0.5 2.4 40 h ch2 / w ch2 2.1-3.2 2.7 ± 0.2 2.7 40 h ch2 / h ca2 0.6-1.4 0.8 ± 0.1 0.8 40 h ca2 / w ca2 2.2-6.0 5.0 ± 0.6 5.0 40 n spines p3 4-5 5 ± 1 5 5 n spines p5 27-49 36 ± 9 35 5

Table 20. Comparison of the rostrum denticulation in Caridina ensifera based on the original description (modifi ed from Schenkel, 1902: tables on pages 493 and 495) and this study. parameter range mean ± SD median n Rostrum original description (Schenkel, 1902) n dorsal rostral teeth 9-20 14 ± 3 13 36 n ventral rostral teeth 8-26 17 ± 5 17 36 Rostrum C. ensifera this study n dorsal rostral teeth 9-15 12 ± 2 12 40 n ventral rostral teeth 16-29 22 ± 3 23 40 Rostrum C. caerulea, new species n dorsal rostral teeth 11-20 15 ± 2 16 40 n ventral rostral teeth 26-48 34 ± 5 34 40

187-05, on rocks, coll. K. von Rintelen, 6 Oct.2005; 6 ex. (ZMB 2-4 teeth posterior to orbital margin), approx. anterior 2/3 29385), west shore, 02°2.734'S, 120°37.368'E, loc. 178-05, on wood, unarmed, without subapical teeth, armed ventrally with coll. K. von Rintelen, 6 Oct.2005; 4 ex. (ZMB 29393), east shore, 26-48 teeth. Antennal spine situated below inferior orbital at road Tentena-Peura, 01°47.33'S, 120°38.079'E, loc. 160-05, on angle. Pterygostomial angle broadly rounded. Eyes well wood, coll. K. von Rintelen, 3 Oct.2005; 8 ex. (MZB Cru 1721, developed, anterior end 0.5-0.6 times length of basal segment n=4; ZMB 29394, n=4), west shore, 01°58.21'S, 120°34.316'E, loc. 181-05, on wood, coll. K. von Rintelen, 6 Oct.2005; 13 ex. of antennular peduncle (n=5). Antennular peduncle 0.9-1.1 (MZB Cru 1722, n=6; ZMB 29395, n=7, some SEM material), times as long as carapace (n=5), second segment 1.8-2.0 times east shore, bay at Cape Nceppo, 01°52.39'S, 120°38.974'E, loc. length of third segment, third segment 0.3 times length of 156-05, on mixed substrate, coll. K. von Rintelen, 3 Oct.2005; 7 basal segment. Stylocerite reaching 0.8-1.0 times length of ex. (MZB Cru 1723, n=3; ZMB 29400, n=4), east shore, shallow basal segment of antennular peduncle (n=5). Scaphocerite bay at Cape Songuo, 01°53.748'S, 120°39.939'E, loc. 155-05, on (Fig. 52D) 3.6-4.8 times as long as wide (n=5). mixed substrate, coll. R. Lamers & K. von Rintelen, 3 Oct.2005; 1 ex. (ZMB 29405), west shore, Taipa, 01°55.289'S, 120°32.77'E, Sixth abdominal somite 0.4-0.8 times length of carapace loc. 182-05, on wood, coll. K. von Rintelen, 6 Oct.2005. (n=40), 1.0-2.5 times as long as fi fth somite(n=40), 0.9-1.0

times length of telson (n=5). Telson (Fig. 52C,J) 3.5-4.1 Description. – Carapace length 3.0-4.5 mm (n=40). Rostrum times as long as wide (n=5), distal margin rounded, without (Fig. 52A; Tables 19-20) very long and slender, reaching projection, with 4-5 pairs of spinules and 1 pair of dorsolateral far beyond end of scaphocerite, 1.9-2.6 times as long as spinules; distal end with 2-3 pairs of spines, lateral pair carapace (n=40), armed dorsally with 11-20 teeth (including distinctly longer than intermediate pairs. Preanal carina (Fig.

429 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 52. Caridina caerulea from Lake Poso. A. Cephalothorax and cephalic appendages, male (ZMB 29251); B. Uropodal diaeresis; C. Telson, female (ZMB 29251); D. Scaphocerite, female (ZMB 29393); E. Preanal carina, F. Dactylus of third pereiopod, male (ZMB 29395); G. Dactylus of fi fth pereiopod; H. Third pereiopod; I. Fifth pereiopod; J. Distal end of telson, female (ZMB 29251); K. SEM image of chela and carpus of fi rst and second pereiopods, female (ZMB 29251); L. First pereiopod, male (ZMB 29260); M. Second pereiopod; N. Endopod of male fi rst pleopod (ZMB 29393); O. Appendix masculina of male second pleopod. Scale bars: A, D = 1.0 mm; C, E, H-I, K-O = 0.5 mm; B, F-G, J = 0.1 mm.

430 THE RAFFLES BULLETIN OF ZOOLOGY 2009

52E) with a spine. Uropodal diaeresis (Fig. 52B) with 11-14 with numerous long, curved setae at posterior end. Distal movable spinules (n=5). end of palp of fi rst maxilliped (Fig. 53F) triangular, ending with a short fi nger-like projection; fl agellum of the exopod 5 pairs of pleurobranchs well developed; 3 pairs of short and stout, endopod high, almost reaching end of the arthrobranchs, 2 on third maxillipeds, with second pair fl agellum of exopod. Second maxilliped (Fig. 53E) typical. strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair Third maxilliped (Fig. 53D) with ultimate segment as long of podobranchs on second maxilliped reduced strongly to as penultimate segment. a laminate form. Epipods present on fi rst two pereiopods. Incisor process of mandible (Fig. 53A) ending in a row Chela and carpus of fi rst pereiopod distinctly stouter and of 3-4 small teeth, molar process truncated. Lower lacinia broader than chela and carpus of second pereiopod (Fig. of maxillula (Fig. 53B) broadly rounded, upper lacinia 52K-M); chela of fi rst pereiopod 1.9-2.7 times as long as elongate, with numerous distinct teeth and setae on inner wide (n=40), 0.9-1.5 times length of carpus (n=40); tips of margin, palp slender. Upper endites of maxilla (Fig. 53C) fi ngers rounded, without hooks; dactylus 1.1-1.4 times as subdivided, palp short, scaphognathite tapering posteriorly long as palm (n=5); carpus 1.9-5.1 times as long as wide

Fig. 53. Caridina caerulea from the Lake Poso catchment. A. Mandible (ZMB 29260); B. Maxillula; C. Maxilla; D. third maxilliped; E. second maxilliped; F. fi rst maxilliped. Scale bars: A-F = 1mm.

431 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

(n=40), 1.1-1.3 times length of merus (n=5). Chela of second “red” in C. ensifera; compare von Rintelen et al. 2007a) pereiopod 2.1-3.2 times as long as wide (n=40), 0.6-1.4 times always allows an unambiguous separation, even in juveniles. length of carpus (n=40); tips of fi ngers rounded, without Additionally, they show different substrate preferences and hooks, dactylus 1.3-1.6 times as long as palm (n=5); carpus behaviour (rather stationary on hard substrate, i.e. rock and 2.2-6.0 times as long as wide (n=40), 1.3-1.6 times as long wood, vs. often pelagic on various kinds of substrate in C. as merus (n=5). ensifera). Although C. caerulea is almost identical with C. ensifera (excluding the always distinct colour pattern), it Third pereiopod (Fig. 52F,H) slender, dactylus 3.0-3.8 times can be distinguished by not only a generally higher number as long as wide (terminal spine included, without spines of rostral teeth (Table 20), but also by a higher number of fl exor margin; n=5), terminating in one large claw with of spines on the uropodal diaeresis (11-14, median 12 vs. 4-5 accessory spines on fl exor margin; propodus 12.9-16.3 9-11, median 10 in C. ensifera) and by a lower number of times as long as wide, 5.0-6.0 times as long as dactylus; spines on the third and fi fth pereiopod (4-5, median 5 and carpus 5.9-8.0 times as long as wide, 0.5-0.6 times as long 27-49, median 35 vs. 6-9, median 6 and 51-57, median 52 as propodus, 0.5 times as long as merus; merus 9.4-11.8 in C. ensifera). times as long as wide, bearing 3-5 strong, movable spines on posterior margin of outer surface. The morphological results are well supported by molecular data (Figs. 63,65), placing C. caerulea and C. ensifera in Fifth pereiopod slender (Fig. 52G,I), dactylus 3.6-5.0 times two separate clades that are not even sister groups (for a as long as wide (terminal spine included, without spines of detailed discussion see von Rintelen et al., 2007a). fl exor margin; n=5), terminating in one large claw with 27- 49 accessory spines on fl exor margin; propodus 15.8-22.3 times as long as wide, 4.3-6.0 times as long as dactylus; Caridina ensifera Schenkel, 1902 carpus 6.2-7.2 times as long as wide, 0.5-0.6 times as long (Figs. 54–55; Tables 20–21) as propodus, 0.5-0.6 times as long as merus; merus 8.5-11.3 times as long as wide, bearing 3-5 strong, movable spines Caridina ensifera Schenkel, 1902 pro parte: 490, pl. 8, Figs. 1a-e, on posterior margin of outer surface. 4d (type locality: Lake Poso). Caridina ensifera – Roux, 1904: 552; Bouvier, 1904: 131, 1905: Endopod of male first pleopod (Fig. 52N) elongated 73, 1912: 918, 1913a: 463; 1913b: 182, 1925: 163, Figs. 344-352; Chace, 1997: 9; Fernandez-Leborans & von Rintelen, 2007; Cai & triangular, 2.1-2.8 times as long as proximally wide (n=5), Wowor, 2007 pro parte: 311, Figs. 1-2; von Rintelen et al., 2007a: without appendix interna. Appendix interna of male second 1033, Figs. 1-2; Tables 1-2, 2008: 2244, Table 1. pleopod (Fig. 52O) 0.8-0.9 times length of appendix masculina (n=5). Material examined. Ð Lectotype: male (cl 3.9 mm) (NHMB 1a), Indonesia, Sulawesi, Lake Poso, coll. Sarasin, no date indicated. Ovigerous females with 16-32 eggs (n=2 females); egg size 0.9-1.1 x 0.6-0.7 mm (n=25, eggs with and without eyes). Paralectotypes – 5 males (cl 3.1-3.5 mm), 10 females (cl 3.0-5.3 mm) (NHMB 1a), same data as lectotype. Distribution. – Endemic to Lake Poso (excluding rivers) Others (Lake Poso): 16 ex. (MZB Cru 1709, n=8; ZMB 29248, n=8, and widely distributed within the lake (Fig. 51A), although some SEM material), south shore, Pendolo beach at Hotel Mulia, not as abundant as C. ensifera. 02°3.928'S, 120°41.536'E, loc. 157-04, on wood, coll. K. & T. von Rintelen, 15 Aug.2004; 10 ex. (MZB Cru 1710, n=5; ZMB 29253, Biology and ecology. – C. caerulea was mainly found on n=5, some SEM material), east shore, Cape Watulunto, 02°0.825'S, hard substrate (wood, rocks, but also sporadically on soft 120°42.007'E, loc. 63-04, on mixed substrate, coll. M. Glaubrecht substrate, for example macrophytes; compare von Rintelen & T. von Rintelen, 30 Mar.2004; 5 ex. (ZMB 29291), east shore, et al., 2007a). south of Cape Panti, 02°55.277'S, 120°40.289'E, loc. 158-04, on macrophytes, coll. K. & T. von Rintelen, 16 Aug.2004; 4 ex. (ZMB Colour pattern. – Body transparently yellowish or reddish, 29381), north shore, 01°47.162'S, 120°33.144'E, loc. 187-05, on rocks, coll. K. von Rintelen, 6 Oct.2005; 9 ex. (MZB Cru 1711, n=4; antennules reddish; legs and rostrum bluish (Fig. 51B). ZMB 29384, n=5), west shore, Siuri, 01°48.259'S, 120°31.667'E, The most conspicuous pattern is visible on the tailfan, each loc. 186-05, pelagic, coll. K. von Rintelen, 6 Oct.2005; 20 ex. endopod bearing an elongated blue patch (upside down V- (MZB Cru 1712, n=10; ZMB 29389, n=10, some SEM material), shape) on the distal part (Fig. 51C). east shore, bay at Cape Nceppo, 01°52.39'S, 120°38.974'E, loc. 156-05, on mixed substrate, coll. K. von Rintelen, 3 Oct.2005; Etymology. – The name Caridina caerulea refers to the 14 ex. (MZB Cru 1713, n=7; ZMB 29392, n=7), west shore, conspicuous colour pattern of this new species (the Latin 02°2.734'S, 120°37.368'E, loc. 178-05, on mixed substrate, coll. word caeruleus means blue). C. caerulea is the only ancient K. von Rintelen, 6 Oct.2005; 21 ex. (MZB Cru 1714, n=10; ZMB lake shrimp exhibiting a partly blue body colouration. 29396, n=11), west shore, 01°58.21'S, 120°34.316'E, loc. 181-05, on mixed substrate, coll. K. von Rintelen, 6 Oct.2005; 7 ex. (MZB Cru 1715, n=3; ZMB 29397, n=4), east shore, at road Tentena- Taxonomic remarks. – Of all Lake Poso species, C. Peura, 01°47.33'S, 120°38.079'E, loc. 160-05, on rocks, coll. K. caerulea closely resembles C. ensifera. Therefore, both von Rintelen, 3 Oct.2005; 8 ex. (MZB Cru 1716, n=4; ZMB 29399, taxa can easily be confused as alcohol bleached material, n=4 and some juveniles), east shore, shallow bay, 01°49.702'S, although in living specimens the colour pattern (“blue” vs. 120°38.161'E, loc. 159-05, on macrophytes, coll. K. von Rintelen,

432 THE RAFFLES BULLETIN OF ZOOLOGY 2009

3 Oct.2005; 17 ex. (MZB Cru 1717, n=8; ZMB 29404, n=9, some Sixth abdominal somite 0.4-0.9 times length of carapace SEM material), west shore, 01°52.205'S, 120°32.281'E, loc. 184-05, (n=40), 1.0-2.6 times as long as fi fth somite (n=40), 1.2-1.3 pelagic, coll. R. Lamers & K. von Rintelen, 6 Oct.2005. times length of telson (n=5). Telson (Fig. 55E,J) 3.6-4.1 times as long as wide (n=5), distal margin rounded, without Description. – Carapace length 3.5-5.3 mm (n=40). Rostrum projection, with 3-4 pairs of spinules and 1 pair of dorsolateral (Fig. 55A; Tables 20-21) very long and slender, reaching spinules; distal end with 2-3 pairs of spines, lateral pair far beyond end of scaphocerite, 1.4-2.3 times as long as distinctly longer than intermediate spines. Preanal carina carapace (n=40), armed dorsally with 9-15 teeth (including (Fig. 55C) with a spine. Uropodal diaeresis (Fig. 55D) with 1-3 teeth posterior to orbital margin), approx. anterior 2/3 9-11 movable spinules (n=5). unarmed, without subapical teeth, armed ventrally with 16-29 teeth. Antennal spine situated below inferior orbital 5 pairs of pleurobranchs well developed; 3 pairs of angle. Pterygostomial angle broadly rounded. Eyes well arthrobrachs, 2 on third maxillipeds, with second pair developed, anterior end 0.6-0.7 times length of basal segment strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair of antennular peduncle (n=5). Antennular peduncle 0.9-1.0 of podobranchs on second maxilliped reduced strongly to a times as long as carapace (n=5), second segment 1.8-2.2 times laminate form. Epipods only present on fi rst two pereiopods. length of third segment, third segment 0.3 times length of Mouthparts as described by Cai & Wowor (2007). basal segment. Stylocerite reaching 0.8-0.9 times length of basal segment of antennular peduncle (n=5). Scaphocerite Chela and carpus of fi rst pereiopod distinctly stouter and (Fig. 55B) 3.6-4.5 times as long as wide (n=5). broader than chela and carpus of second pereiopod (Fig.

Fig. 54. Caridina ensifera from Lake Poso. A. Distribution. B-C. Colour pattern of living animals (not to scale). Picture B. courtesy of Chris Lukhaup.

433 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Table 21. Summary of standard morphometric parameters for Caridina ensifera. parameter range mean ± SD median n cl (mm) 3.5-5.3 4.4 ± 0.4 4.4 40 rl / cl 1.4-2.3 2.1 ± 0.2 2.0 40 n dorsal rostral teeth 9-15 12 ± 2 12 40 n ventral rostral teeth 16-29 22 ± 3 23 40 abds6 / cl 0.4-0.9 0.9 ± 0.1 0.9 40 abds6 / abds5 1.0-2.6 2.2 ± 0.3 2.2 40 abds6 / h tel 1.2-1.3 1.2 ± 0.1 1.2 5 h tel / w tel 3.6-4.1 3.9 ± 0.2 3.9 5 n spines uropodal diaeresis 9-11 10 ± 1 10 5 h ch1 / w ch1 2.0-2.8 2.5 ± 0.2 2.5 40 h ch1 / h ca1 1.0-1.3 1.1 ± 0.1 1.1 40 h ca1 / w ca1 2.5-4.0 3.1 ± 0.4 3.2 40 h ch2 / w ch2 2.8-4.4 3.5 ± 0.3 3.4 40 h ch2 / h ca2 0.7-0.8 0.7 ± 0.0 0.7 40 h ca2 / w ca2 5.4-7.3 6.4 ± 0.5 6.4 40 n spines p3 6-9 7 ± 1 6 5 n spines p5 51-57 53 ± 3 52 5

55K-M); chela of fi rst pereiopod 2.0-2.8 times as long as Ovigerous females with 19-25 eggs (n=2 females); egg size wide (n=40), 1.0-1.3 times length of carpus (n=40); tips of 0.9-1.0 x 0.5-0.6 mm (n=20, eggs with and without eyes). fi ngers rounded, without hooks; dactylus 1.0-1.3 times as long as palm (n=5); carpus 2.5-4.0 times as long as wide Distribution. – Endemic to Lake Poso (excluding rivers) and (n=40), 1.0-1.3 times length of merus (n=5). Chela of second widely distributed within the lake (Fig. 54A). pereiopod 2.8-4.4 times as long as wide (n=40), 0.7-0.8 times length of carpus (n=40); tips of fi ngers rounded, without Biology & Ecology. – C. ensifera is a generalist often hooks, dactylus 1.2-1.4 times as long as palm (n=5); carpus found in pelagic swarms or sporadically on various kinds 5.4-7.3 times as long as wide (n=40), 1.3-1.6 times as long of substrate (rocks and wood or soft substrate, for example as merus (n=5). sand or macrophytes; compare von Rintelen et al., 2007a). It is the most abundant shrimp species in Lake Poso. Third pereiopod (Fig. 55F-G) slender, dactylus 5.0-5.4 times as long as wide (terminal spine included, without spines Colour pattern. – Body yellowish-transparent with few white of fl exor margin; n=5), terminating in one large claw with or darker dots, antennules reddish (Fig. 54B). The most 6-9 accessory spines on fl exor margin; propodus 10.0-13.0 conspicuous pattern is visible on the tailfan, each exopod times as long as wide, 3.1-3.7 times as long as dactylus; bearing a red spot on the distal part (Fig. 54C). carpus 4.7-6.1 times as long as wide, 0.5-0.7 times as long as propodus, 0.4-0.5 times as long as merus; merus 9.2-11.4 Taxonomic remarks. – C. ensifera very closely resembles C. times as long as wide, bearing 2-4 strong, movable spines caerulea, previously listed as C. ensifera by Cai & Wowor on posterior margin of outer surface. (2007), but discovered as a cryptic species by von Rintelen et al. (2007a). In their revision of the Lake Poso species, Fifth pereiopod slender (Fig. 55H-I), dactylus 5.4-7.0 times Cai & Wowor (2007: 314) describe the colour of C. ensifera as long as wide (terminal spine included, without spines of as “a single specimen from Lake Poso […] transparent fl exor margin; n=5), terminating in one large claw with 51- fi nely spectra, blue-red n-shape on brachiostegal region, 57 accessory spines on fl exor margin; propodus 11.1-20.7 blue spot on distal exopod of uropods-conspicuous”. Thus, times as long as wide, 2.5-3.0 times as long as dactylus; they describe the colour pattern of C. caerulea, although carpus 4.9-5.4 times as long as wide, 0.5 times as long as their data rather hint at C. ensifera sensu Schenkel (1902). propodus, 0.5-0.6 times as long as merus; merus 8.8-11.1 The reason to assign C. ensifera (this study) to the original times as long as wide, bearing 2-3 strong, movable spines description of C. ensifera, and to describe C. caerulea as a on posterior margin of outer surface. new species, is mainly based on the rostrum denticulation mentioned in Schenkel’s original description (see Table Endopod of male first pleopod (Fig. 55N) elongated 20). C. ensifera, as here describe, shows a high congruence triangular, 1.8-2.5 times as long as proximally wide (n=5), with Schenkel’s data (dorsally 9-15 and ventrally 16-29 vs. without appendix interna. Appendix interna of male second dorsally 9-20 and ventrally 8-26 in the original description), pleopod (Fig. 55O) 0.7-0.9 length of appendix masculina whereas in C. caerulea the number of ventral teeth (26-48) (n=5). does not really agree with Schenkel’s description, especially

434 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 55. Caridina ensifera from Lake Poso. A. Cephalothorax and cephalic appendages, female (ZMB 29389); B. Scaphocerite, male (ZMB 29404); C. Preanal carina; D. Uropodal diaeresis, female (ZMB 29389); E. Telson, female (ZMB 29248), F. Third pereiopod, female (ZMB 29389); G. Dactylus of third pereiopod; H. Fifth pereiopod; I. Dactylus of fi fth pereiopod; J. Distal end of telson, female (ZMB 29248); K. First pereiopod, male (ZMB 29404); L. Second pereiopod; M. SEM image of chela and carpus of fi rst and second pereiopods; N. Endopod of male fi rst pleopod; O. Appendix masculina of male second pleopod. Scale bars: A-B = 1.0 mm; C, E-F, H, J-O = 0.5 mm; D, G, I = 0.1 mm.

435 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi if the median is considered. Other parameters of Schenkel’s 01°58.21'S, 120°34.316'E, loc. 181-05, on wood, coll. K. von description either fi t both species (for example the number Rintelen, 6 Oct.2005. of spinules and spines of the telson) or are not comparable due to an obviously different technique of measurement (for Description. – Carapace length 2.9-4.1 mm (n=12). Rostrum example the carapace and rostrum length). Another aspect (Fig. 57A; Table 22) long with an anterior upturn, mostly to consider here is that C. ensifera generally has the highest reaching beyond end of scaphocerite, 0.9-1.4 times as density of all shrimps in Lake Poso and we thus assume it long as carapace (n=11), armed dorsally with 16-21 teeth more likely to be caught by the Sarasins than C. caerulea. (including 4-6 teeth posterior to orbital margin), approx. Although C. ensifera is almost identical with C. caerulea anterior third to half unarmed, without subapical teeth, (not counting the always distinct colour pattern), it can not armed ventrally with 13-23 teeth (n=8). Antennal spine only be distinguished by a generally lower number of rostral situated below inferior orbital angle. Pterygostomial angle teeth (Table 20), but also by a lower number of spines on the broadly rounded. Eyes well developed, anterior end 0.5-0.6 uropodal diaeresis (9-11 vs. 11-14 in C. caerulea) and by a times length of basal segment of antennular peduncle (n=5). higher number of spines on the third and fi fth pereiopod (6-9 Antennular peduncle 1.0-1.1 times as long as carapace (n=5), and 51-57 vs. 4-5 and 27-49 in C. caerulea). A disciminant second segment 1.5-0.2 times length of third segment, third analysis of several morphological characters separates both segment 0.3-0.4 times length of basal segment. Stylocerite species a hundred percent (von Rintelen et al. 2007a). reaching 0.9-1.0 times length of basal segment of antennular peduncle (n=5). Scaphocerite (Fig. 57D) 3.8-4.3 times as The morphological results are well supported by molecular long as wide (n=5). data (Figs. 63,65), placing C. ensifera and C. caerulea in two separate clades that are not even sister groups (for a Sixth abdominal somite 0.5-0.7 times length of carapace detailed discussion see von Rintelen et al., 2007a). (n=11), 1.7-1.9 times as long as fi fth somite (n=10), 1.0-1.1 times length of telson (n=6). Telson (Fig. 57C,H) 2.9-3.1 times as long as wide (n=5), distal margin broadly rounded, Caridina longidigita Cai & Wowor, 2007 without projection, with 3-4 pairs of spinules and 1 pair of (Figs. 56–57; Table 22) dorsolateral spinules; distal end with 4 pairs of spines, lateral pair longer than intermediate pairs, median pairs shortest. Caridina longidigita Cai & Wowor, 2007: 317, Figs. 4-5 (type Preanal carina (Fig. 57E) with a spine. Uropodal diaeresis locality: west coast of Lake Poso at Taipa area, Poso River (Fig. 57B) with 15-17 movable spinules (n=5). at the outlet of Lake Poso, east coast of Lake Poso at Besuna village). 5 pairs of pleurobranchs well developed; 3 pairs of Caridina longidigita – von Rintelen et al., 2008: 2244, Table 1. arthrobranchs, 2 on third maxillipeds, with second pair Caridina spec. A – von Rintelen et al., 2007a: 1035, fi g. 2, Tables strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair 1-2. of podobranchs on second maxilliped reduced strongly Material examined. – Lake Poso: 42 ex. (MZB Cru 1704a, n=5; to a laminate form. Epipods absent from all pereiopods. ZMB 29060a, n=6; MZB Cru 1705b, n=9; ZMB 29060b, n=12; Mouthparts as described by Cai & Wowor (2007). MZB Cru 1706c, n=5; ZMB 29060c, n=5, some SEM material), east shore, south of Cape Sinampada, 02°56.25'S, 120°40.443'E, Chela and carpus of fi rst pereiopod not distinctly stouter loc. 159-04, (a) on rocks in deeper water, (b) on wood, (c) on and broader than chela and carpus of second pereiopod rocks in shallow water, coll. K. & T. von Rintelen, 16 Aug.2004; (Fig. 57K-N); chela of fi rst pereiopod long and slender, 14 ex. (MZB Cru 1707, n=7; ZMB 29252, n=7, some SEM 4.6-6.5 times as long as wide (n=9), 0.7-1.0 times length of material), east shore, south of Cape Tolambu, 01°57.928'S, carpus (n=10); tips of fi ngers rounded, without hooks, but 120°40.536'E, loc. 65-04, on rocks, coll. M. Glaubrecht & T. von Rintelen, 30 Mar.2004; 4 ex. (ZMB 29258), west shore, Cape with extremely long fi ngers (about length of or longer than Bancea, 01°59.023'S, 120°35.108'E, loc. 59-04, on rocks, coll. M. chela); dactylus 3.6-4.6 times as long as palm (n=5); carpus Glaubrecht & T. von Rintelen, 29 Mar.2004; 7 ex. (ZMB 29289), 4.8-8.1 times as long as wide (n=8), 1.0-1.2 times length of east shore, 02°0.825'S, 120°42.007'E, loc. 161-04, on wood, coll. merus (n=5). Chela of second pereiopod 4.8-6.4 times as K. von Rintelen, 16 Aug.2004; (ZMB 29293, some juveniles), long as wide (n=9), 0.7-1.0 times length of carpus (n=10); east shore, 01°59.867'S, 120°41.238'E, loc. 160-04, on mixed tips of fi ngers rounded, without hooks, but with extremely substrate, coll. K. & T. von Rintelen, 16 Aug.2004; 1 ex. (ZMB long fi ngers (about length of or longer than chela); dactylus 29387), west shore, 02°2.734'S, 120°37.368'E, loc. 178-05, on 3.4-3.9 times as long as palm (n=5); carpus 5.2-7.9 times as wood, coll. K. von Rintelen, 6 Oct.2005; 22 ex. (MZB Cru 1708, long as wide (n=8), 1.0-1.3 times as long as merus (n=5). n=11; ZMB 29390, n=11, some SEM material), east shore, bay at Cape Nceppo, 01°52.39'S, 120°38.974'E, loc. 156-05, on mixed substrate, coll. K. von Rintelen, 3 Oct.2005; 8 ex. (ZMB 29391), Third pereiopod (Fig. 57F,I) slender, dactylus 3.1-3.6 times east shore, at road Tentena-Peura, 01°47.33'S, 120°38.079'E, loc. as long as wide (terminal spine included, without spines 160-05, on wood, coll. K. von Rintelen, 3 Oct.2005; 5 ex. (ZMB of fl exor margin; n=5), terminating in one large claw with 29398), east shore, shallow bay at Cape Songuo, 01°53.748'S, 4-5 accessory spines on fl exor margin; propodus 11.5-15.0 120°39.939'E, loc. 155-05, on mixed substrate, coll. R. Lamers times as long as wide, 4.7-6.5 times as long as dactylus; & K. von Rintelen, 3 Oct.2005; 3 ex. (ZMB 29401), west shore, carpus 6.4-8.5 times as long as wide, 0.7-0.8 times as long Taipa, 01°55.289'S, 120°32.77'E, loc. 182-05, on wood, coll. as propodus, 0.5-0.6 times as long as merus; merus 9.4-11.5 K. von Rintelen, 6 Oct.2005; 1 ex. (ZMB 29456), west shore,

436 THE RAFFLES BULLETIN OF ZOOLOGY 2009 times as long as wide, bearing 3-5 strong, movable spines Ovigerous females with 24-29 eggs (n=2 females); egg size on posterior margin of outer surface. 1.0-1.2 x 0.6-0.7 mm (n=20, eggs with and without eyes).

Fifth pereiopod slender (Fig. 57G,J), dactylus 2.9-3.9 times Distribution. – Endemic to Lake Poso (excluding rivers) as long as wide (terminal spine included, without spines of and widely distributed within the lake (Fig. 56A), although fl exor margin; n=5), terminating in one large claw with 26- less abundant than C. ensifera. 33 accessory spines on fl exor margin; propodus 12.9-20.0 times as long as wide, 4.6-6.7 times as long as dactylus; Biology and ecology. – Cai & Wowor (2007) already carpus 6.3-7.5 times as long as wide, 0.6 times as long mentioned the occurrence of C. longidigita on “rocky as propodus, 0.6 times as long as merus; merus 9.1-10.2 substrates”. This could not only be confi rmed in the fi eld, times as long as wide, bearing 2-4 strong, movable spines but also further differentiated in gravel from shallow water on posterior margin of outer surface. (above 3 m) and boulders in deeper water (below 3 m). Additional samples from wood show this species to be a Endopod of male first pleopod (Fig. 57O) elongated typical hard-substrate dweller. Further, C. longidigita shows triangular, 1.9-2.3 times as long as proximally wide (n=5), a unique feeding behaviour that has not been reported from without appendix interna. Appendix interna of male second any species of Caridina so far. Instead of the common feeding pleopod (Fig. 57P) 0.8-0.9 times length of appendix masculina behaviour described by Fryer (1960), C. longidigita makes (n=5). lateral sweeping movements with its extremely long fi ngers

Fig. 56. Caridina longidigita from Lake Poso. A. Distribution. B. Colour pattern of living animal (not to scale). Picture courtesy of Chris Lukhaup.

437 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 57. Caridina longidigita from Lake Poso. A. Cephalothorax and cephalic appendages, male (ZMB 29252); B. Uropodal diaeresis; C. Telson; D. Scaphocerite, male (ZMB 29390); E. Preanal carina, F. Third pereiopod, male (ZMB 29252); G. Fifth pereiopod; H. Distal end of telson; I. Dactylus of third pereiopod; J. Dactylus of fi fth pereiopod; K. First pereiopod, female (ZMB 29390); L. Second pereiopod; M. SEM image of anterior part of chelae (from top: lateral, ventral, setae), male (ZMB 29252); N. SEM image of chela and carpus of fi rst and second pereiopods, male (ZMB 29390); O. Endopod of male fi rst pleopod; P. Appendix masculina of male second pleopod. Scale bars: A, D = 1.0 mm; E-G, K-P = 0.5 mm; B, H-J = 0.1 mm.

438 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 22. Summary of standard morphometric parameters for Caridina longidigita. parameter range mean ± SD median n cl (mm) 2.9-4.1 3.5 ± 0.3 3.4 12 rl / cl 0.9-1.4 1.2 ± 0.2 1.3 11 n dorsal rostral teeth 16-21 18 ± 2 18 8 n ventral rostral teeth 13-23 16 ± 4 16 8 abds6 / cl 0.5-0.7 0.6 ± 0.1 0.6 11 abds6 / abds5 1.7-1.9 1.8 ± 0.1 1.7 10 abds6 / h tel 1.0-1.1 1.0 ± 0.0 1.0 6 h tel / w tel 2.9-3.1 3.0 ± 0.1 3.0 5 n spines uropodal diaeresis 15-17 16 ± 1 16 5 h ch1 / w ch1 4.6-6.5 5.6 ± 0.5 5.6 9 h ch1 / h ca1 0.7-1.0 0.9 ± 0.1 0.9 10 h ca1 / w ca1 4.8-8.1 6.6 ± 1.1 6.7 8 h ch2 / w ch2 4.8-6.4 5.5 ± 0.5 5.5 9 h ch2 / h ca2 0.7-1.0 0.9 ± 0.1 0.8 10 h ca2 / w ca2 5.2-7.9 6.7 ± 1.1 7.1 8 n spines p3 4-5 5 ± 1 5 5 n spines p5 26-33 30 ± 3 30 5

(M. Glaubrecht & T. von Rintelen, pers. fi eld observation Paralectotypes – 4 males (cl 2.6-2.9 mm), 6 females (cl 2.7-3.4 2007), while all other species lack this lateral component. mm) (NHMB 2a), data same as lectotype.

Colour pattern. – Body appearing transparently brownish Others: Lake Poso: 3 ex. (ZMB 29068), south shore, Pendolo beach at Hotel Mulia, 02°3.928'S, 120°41.536'E, loc. 157-04, on wood, to greenish (sometimes darker), with small dots covering coll. K. & T. von Rintelen, 15 Aug.2004; 2 ex. (ZMB 29137), east the whole body. Fingers of chelae orange, but without a shore, 01°59.867'S, 120°41.238'E, loc. 160-04, on mixed substrate, particular pattern (Fig. 56B). Eggs dark brown. coll. K. & T. von Rintelen, 16 Aug.2004; 12 ex. (ZMB 29201a, n=6; ZMB 29201b, n=1, and MZB Cru 1732, n=5), east shore, south Taxonomic remarks. – C. longidigita mostly resembles of Cape Sinampada, 02°56.25'S, 120°40.443'E, loc. 159-04, (ZMB C. sarasinorum, but can easily be distinguished by its a) on leaf litter, (ZMB b and MZB) on wood, coll. M. Glaubrecht extremely long fi ngers on the chela of the fi rst and second & T. von Rintelen, 30Mar.2004; 7 ex. (ZMB 29261, some SEM pereiopod (vs. short in C. sarasinorum) and by more slender material), east shore, Cape Watulunto, 02°0.825'S, 120°42.007'E, pereiopods. It differs further by a higher number of ventral loc. 63-04, on leaf litter, coll. M. Glaubrecht & T. von Rintelen, 30 Mar.2004; 17 ex. (MZB Cru 1733, n=9; ZMB 29288, n=8), east rostral teeth (13-23, median 16 vs. 8-14, median 13 in C. shore, 02°0.825'S, 120°42.007'E, loc. 161-04, on wood, coll. K. von sarasinorum). Rintelen, 16 Aug.2004; 13 ex. (MZB Cru 1734, n=6; ZMB 29383, n=7), west shore, Siuri, 01°48.259'S, 120°31.667'E, loc. 186-05, In the molecular phylogeny, C. longidigita does not appear on mixed substrate, coll. K. von Rintelen, 6 Oct.2005; 5 ex. (ZMB monophyletic (Figs. 63,65), but based on its distinctive 29386), west shore, 02°2.734'S, 120°37.368'E, loc. 178-05, on morphology it is regarded as a single valid species that wood, coll. K. von Rintelen, 6 Oct.2005; 11 ex. (MZB Cru 1735, might sometimes hybridize with other species (compare von n=6; ZMB 29388, n=5, some SEM material), east shore, at road Rintelen et al., 2007a). Tentena-Peura, 01°47.33'S, 120°38.079'E, loc. 160-05, on wood, coll. K. von Rintelen, 3 Oct.2005; 14 ex. (MZB Cru 1736, n=7; ZMB 29402, n=7, some SEM material), west shore, 01°52.205'S, 120°32.281'E, loc. 184-05, on macrophytes, coll. K. von Rintelen, Caridina sarasinorum Schenkel, 1902 6 Oct.2005; 15 ex. (MZB Cru 1737, n=8; ZMB 29403, n=7), (Figs. 58–59; Table 23) east shore, shallow bay, 01°49.702'S, 120°38.161'E, loc. 159-05, on macrophytes, coll. K. von Rintelen, 3 Oct.2005; 1 ex. (ZMB Caridina sarasinorum Schenkel, 1902: 492, pl. 8, Figs. 2a-e, 4a 29406), west shore, Taipa, 01°55.289'S, 120°32.77'E, loc. 182-05, (type locality: Lake Poso). on wood, coll. K. von Rintelen, 6 Oct.2005. Caridina sarasinorum – Chace, 1997: 19; Cai & Wowor, 2007: 315, fi g. 3; von Rintelen et al., 2007a: 1033, fi g. 2, Tables 1-2, Description. – Carapace length 2.6-3.6 mm (n=12). 2008: 2244, Table 1. Rostrum (Fig. 59A; Table 23) long, reaching beyond end Caridina Sarasinorum – Roux, 1904: 551; Bouvier, 1905: 73, 1913b: 182, 1925: 168, Figs. 356-359. of scaphocerite, 1.0-1.2 times as long as carapace (n=8), armed dorsally with 15-21 teeth (including 4-6 teeth Material examined. – Lectotype: ovigerous female (cl 3.1 mm) posterior to orbital margin), approx. anterior third to half (NHMB 2a), Indonesia, Sulawesi, Lake Poso, coll. Sarasin, no unarmed, without subapical teeth, armed ventrally with date indicated. 8-14 teeth. Antennal spine situated below inferior orbital

439 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Table 23. Summary of standard morphometric parameters for Caridina sarasinorum. parameter range mean ± SD median n cl (mm) 2.6-3.6 3.1 ± 0.3 3.1 12 rl / cl 1.0-1.2 1.1 ± 0.1 1.1 8 n dorsal rostral teeth 15-21 18 ± 2 17 8 n ventral rostral teeth 8-14 12 ± 2 13 8 abds6 / cl 0.6-0.8 0.7 ± 0.1 0.7 11 abds6 / abds5 1.7-2.0 1.9 ± 0.1 1.9 11 abds6 / h tel 0.9-1.0 0.9 ± 0.1 1.0 6 h tel / w tel 3.2-3.6 3.4 ± 0.2 3.3 5 n spines uropodal diaeresis 8-10 9 ± 1 9 5 h ch1 / w ch1 1.9-2.0 1.9 ± 0.1 1.9 8 h ch1 / h ca1 1.3-1.5 1.5 ± 0.1 1.5 9 h ca1 / w ca1 1.1-1.9 1.7 ± 0.3 1.7 8 h ch2 / w ch2 2.2-2.9 2.5 ± 0.2 2.6 8 h ch2 / h ca2 0.8-0.9 0.8 ± 0.1 0.8 9 h ca2 / w ca2 3.6-5.0 4.4 ± 0.5 4.6 8 n spines p3 6-7 7 ± 0 7 5 n spines p5 33-43 39 ± 4 39 5

angle. Pterygostomial angle broadly rounded. Eyes well developed, anterior end 0.5-0.6 times length of basal segment of antennular peduncle (n=5). Antennular peduncle 0.9-1.1 times as long as carapace (n=5), second segment 1.7-2.0 times length of third segment, third segment 0.3-0.4 times length of basal segment. Stylocerite reaching 0.9-1.0 times length of basal segment of antennular peduncle (n=5). Scaphocerite (Fig. 59D) 3.8-4.4 times as long as wide (n=5).

Sixth abdominal somite 0.6-0.8 times length of carapace (n=11), 1.7-2.0 times as long as fi fth somite (n=11), 0.9- 1.0 times length of telson (n=6). Telson (Fig. 59C,H,K) 3.2-3.6 times as long as wide (n=5), distal margin rounded, without projection, with 3-4 pairs of spinules and 1 pair of dorsolateral spinules; distal end with 3 pairs of spines, lateral pair sometimes but not always longer than intermediate pairs. Preanal carina (Fig. 59E) with a spine. Uropodal diaeresis (Fig. 59B) with 8-10 movable spinules (n=5).

5 pairs of pleurobranchs well developed; 3 pairs of arthrobranchs, 2 on third maxillipeds, with second pair strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair of podobranchs on second maxilliped reduced strongly to a laminate form. Epipods present on fi rst pereiopod, greatly reduced or absent from second pereiopod. Mouthparts as described by Cai & Wowor (2007).

Chela and carpus of fi rst pereiopod distinctly stouter and broader than chela and carpus of second pereiopod (Fig. 59L-N); chela of fi rst pereiopod 1.9-2.0 times as long as wide (n=8), 1.3-1.5 times length of carpus (n=9); tips of fi ngers rounded, without hooks; dactylus 0.9-1.1 times as long as palm (n=5); carpus 1.1-1.9 times as long as wide (n=8), 1.0-1.2 times length of merus (n=5). Chela of second pereiopod 2.2-2.9 times as long as wide (n=8), 0.8-0.9 times Fig. 58. Distribution of Caridina sarasinorum in Lake Poso.

440 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 59. Caridina sarasinorum from Lake Poso. A. Cephalothorax and cephalic appendages, female (ZMB 29388); B. Uropodal diaeresis, male (ZMB 29402); C. SEM image of telson and uropods, female (ZMB 29388); D. Scaphocerite, female (ZMB 29403); E. Preanal carina, F. Fifth pereiopod, female (ZMB 29388); G. Third pereiopod; H. Telson; I. Dactylus of third pereiopod; J. Dactylus of fi fth pereiopod; K. Distal end of telson; L. SEM image of chela and carpus of fi rst and second pereiopods; M. First pereiopod; N. Second pereiopod; O. Endopod of male fi rst pleopod (ZMB 29403); P. Appendix masculina of male second pleopod. Scale bars: A, D = 1.0 mm; C, E-H, L-P = 0.5 mm; B, I-K = 0.1 mm.

441 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi length of carpus (n=9); tips of fi ngers rounded, without Caridina schenkeli, new species hooks, dactylus 0.9-1.4 times as long as palm (n=5); carpus (Figs. 60–62; Table 24) 3.6-5.0 times as long as wide (n=8), 1.3-1.5 times as long as merus (n=5). Caridina spec. B – von Rintelen et al., 2007a: 1035, fi g. 2, Tables 1-2. Third pereiopod (Fig. 59G,I) slender, dactylus 3.3-4.5 times as long as wide (terminal spine included, without spines Material examined. – Holotype: female (cl 4.3 mm)(MZB Cru 2124), small stream, west of Lake Poso, 02°2.613'S, 120°37.311'E, of fl exor margin; n=5), terminating in one large claw with loc. 179-05, on macrophytes, coll. K. von Rintelen, 6 Oct.2005. 6-7 accessory spines on fl exor margin; propodus 9.3-11.7 times as long as wide, 2.9-4.1 times as long as dactylus; Paratypes (Lake Poso catchment) – 38 ex. (MZB Cru 1724, n=19; carpus 4.1-5.0 times as long as wide, 0.6-0.7 times as long ZMB 29159, n=19), Uebangke River, north of tributary of Lake as propodus, 0.5-0.6 times as long as merus; merus 6.8-8.9 Poso, 01°46.48'S, 120°35.61'E, loc. 188-05, on mixed substrate, times as long as wide, bearing 3-4 strong, movable spines coll. K. von Rintelen, 7 Oct.2005; 24 ex. (MZB Cru 1725, on posterior margin of outer surface. n=12; ZMB 29254, n=12), Sulewana, above rapids, 01°39.121'S, 120°39.742'E, loc. 52-04, on mixed substrate, coll. M. Glaubrecht Fifth pereiopod slender (Fig. 59F,J), dactylus 4.0-5.6 times & T. von Rintelen, 28 Mar.2004; 22 ex. (MZB Cru 1726, n=11; ZMB 29407, n=11), Njongi River, approx. 1 km east of Tentena, as long as wide (terminal spine included, without spines of 01°44.348'S, 120°40.102'E, loc. 163-05, on macrophytes, coll. K. fl exor margin; n=5), terminating in one large claw with 33- & T. von Rintelen, 3 Oct.2005; 10 ex. (ZMB 29441), small stream, 43 accessory spines on fl exor margin; propodus 10.0-16.0 west of Lake Poso, 01°53.816'S, 120°31.466'E, loc. 183-05, on times as long as wide, 2.6-3.2 times as long as dactylus; roots, coll. K. von Rintelen, 6 Oct.2005; 43 ex. (MZB Cru 1727, carpus 4.3-5.7 times as long as wide, 0.5-0.6 times as long n=22; ZMB 29442, n=21 and few juveniles, some SEM material), as propodus, 0.6 times as long as merus; merus 6.3-7.8 small stream, west of Lake Poso, 02°2.613'S, 120°37.311'E, loc. times as long as wide, bearing 2-3 strong, movable spines 179-05, on macrophytes, coll. K. von Rintelen, 6 Oct.2005; 11 ex. on posterior margin of outer surface. (MZB Cru 1728, n=5; ZMB 29443, n=6), stream, west of Lake Poso, 02°0.233'S, 120°35.765'E, loc. 180-05, mixed substrate, coll. K. von Rintelen, 6 Oct.2005; 25 ex. (MZB Cru 1729, n=12; ZMB Endopod of male first pleopod (Fig. 59O) elongated 29444, n=13), Salopa River, 01°46.333'S, 120°32.49'E, loc. 177-05, triangular, 1.9-2.5 times as long as proximally wide (n=5), without appendix interna. Appendix interna of male second pleopod (Fig. 59P) 0.8-0.9 times length of appendix masculina (n=5).

Ovigerous females with 19-23 eggs (n=2 females); egg size 0.9-1.0 x 0.5-0.6 mm (n=20, eggs with and without eyes).

Distribution. – Endemic to Lake Poso (excluding rivers), widely distributed within the lake (Fig. 58), although less abundant than C. ensifera.

Biology and ecology. – C. sarasinorum was found on various kinds of substrate (wood, leaf litter, macrophytes), particularly on weed and wood, often in large numbers at several localities.

Colour pattern. – Body transparently yellowish or greenish, lacking a particular pattern. However, further details are still unknown.

Taxonomic remarks. – C. sarasinorum resembles C. longidigita, but can easily be distinguished by its stouter pereiopods and the short fi ngers on the chela of the fi rst and second pereiopod (vs. distinctly more slender pereiopods and very long fi ngers in C. longidigita). It further differs by a lower number of ventral rostral teeth (8-14, median 13 vs. 13-23, median 16 in C. longidigita).

In the molecular phylogeny (Figs. 63,65), C. sarasinorum does not appear monophyletic, but based on its distinctive morphology it is here regarded as a single valid species that might sometimes hybridize with other species (compare von Fig. 60. Distribution of Caridina schenkeli in the Poso Rintelen et al., 2007a). catchment.

442 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 24. Summary of standard morphometric parameters for Caridina schenkeli. parameter range mean ± SD median n cl (mm) 3.6-5.1 4.2 ± 0.4 4.2 17 rl / cl 0.9-1.1 1.0 ± 0.1 0.9 10 n dorsal rostral teeth 9-16 13 ± 2 13 10 n ventral rostral teeth 9-13 11 ± 1 11 10 abds6 / cl 0.6-0.7 0.7 ± 0.0 0.7 17 abds6 / abds5 1.9-2.0 2.0 ± 0.1 2.0 6 abds6 / h tel 0.8-1.0 1.0 ± 0.1 1.0 8 h tel / w tel 3.0-3.6 3.4 ± 0.3 3.6 5 n spines uropodal diaeresis 10-11 10 ± 0 10 5 h ch1 / w ch1 1.9-3.2 2.4 ± 0.4 2.3 10 h ch1 / h ca1 1.1-1.4 1.3 ± 0.1 1.3 10 h ca1 / w ca1 2.1-3.2 2.5 ± 0.4 2.4 10 h ch2 / w ch2 2.5-4.4 3.3 ± 0.5 3.3 10 h ch2 / h ca2 0.7-0.9 0.8 ± 0.0 0.8 10 h ca2 / w ca2 4.5-6.5 5.5 ± 0.6 5.5 10 n spines p3 6-8 7 ± 1 7 5 n spines p5 57-64 59 ± 3 57 5 on mixed substrate, coll. K. & T. von Rintelen, 5 Oct.2005; 28 ex. 5 pairs of pleurobranchs well developed; 3 pairs of (MZB Cru 1730, n=14; ZMB 29445, n=14, some SEM material), arthrobranchs, 2 on third maxillipeds, with second pair Sulewana, above rapids, 01°39.121'S, 120°39.742'E, loc. 169-05, strongly reduced in size, 1 pair on fi rst pereiopod; 1 pair on mixed substrate, coll. K. & T. von Rintelen, 4 Oct.2005; 34 ex. of podobranchs on second maxilliped reduced strongly to (MZB Cru 1731, n=17; ZMB 29446, n=17), Poso outlet, Tentena, a laminate form. Epipod present on fi rst two pereiopods. 01°45.908'S, 120°38.366'E, loc. 195-05, on wood, coll. R. Lamers & K. von Rintelen, 7 Oct.2005; 4 ex. (ZMB 29457), Sulewana Incisor process of mandible (Fig. 62A) ending in a row of rapids, 02°38.871'S, 120°39.279'E, loc. 170-05, on macrophytes, 4-6 small teeth, molar process truncated. Lower lacinia of coll. K. & T. von Rintelen, 4 Oct.2005. maxillula (Fig. 62B) broadly rounded, upper lacinia elongate, with numerous distinct teeth and setae on inner margin, palp Description. –Carapace length 3.6-5.1 mm (n=17). slender. Upper endites of maxilla (Fig. 62C) subdivided, palp Rostrum (Fig. 61A; Table 24) reaching near or beyond short, scaphognathite tapering posteriorly with numerous end of scaphocerite, 0.9-1.1 times as long as carapace long, curved setae at posterior end. Distal end of palp of (n=10), armed dorsally with 9-16 teeth (including 2-5 teeth fi rst maxilliped (Fig. 62F) triangular, not ending with a posterior to orbital margin), approx. anterior third to half fi nger-like projection; fl agellum of the exopod short, endopod unarmed, without subapical teeth, armed ventrally with high, reaching near to end of fl agellum of exopod. Second 9-13 teeth. Antennal spine situated below inferior orbital maxilliped (Fig. 62E) typical. Third maxilliped (Fig. 62D) angle. Pterygostomial angle broadly rounded. Eyes well with ultimate segment as long as penultimate segment. developed, anterior end 0.4-0.6 times length of basal segment of antennular peduncle (n=5). Antennular peduncle 0.8-1.0 Chela and carpus of fi rst pereiopod distinctly stouter and times as long as carapace (n=5), second segment 1.6-2.0 times broader than chela and carpus of second pereiopod (Fig. length of third segment, third segment 0.3-0.4 times length 61M-O); chela of fi rst pereiopod 1.9-3.2 times as long as of basal segment. Stylocerite reaching 1.0 times length of wide (n=10), 1.1-1.4 times length of carpus (n=10); tips of basal segment of antennular peduncle (n=5). Scaphocerite fi ngers rounded, without hooks; dactylus 1.0-1.4 times as (Fig. 61D) 3.3-4.7 times as long as wide (n=5). long as palm (n=5); carpus 2.1-3.2 times as long as wide (n=10), 1.1-1.2 times length of merus (n=5). Chela of second Sixth abdominal somite 0.6-0.7 times length of carapace pereiopod 2.5-4.4 times as long as wide (n=10), 0.7-0.9 times (n=17), 1.9-2.0 times as long as fi fth somite (n=6), 0.8-1.0 length of carpus (n=10); tips of fi ngers rounded, without times length of telson (n=8). Telson (Fig. 61C,H) 3.0-3.6 hooks, dactylus 1.2-1.4 times as long as palm (n=5); carpus times as long as wide (n=5), distal margin rounded, without 4.5-6.5 times as long as wide (n=10), 1.3-1.4 times as long projection, with 3-6 pairs of spinules and 1 pair of dorsolateral as merus (n=5). spinules; distal end with 2-3 pairs of spines, lateral pair usually longer than intermediate pairs. Preanal carina (Fig. Dactylus of third pereiopod (Fig. 61F,I) 3.3-4.3 times as 61E) with a spine. Uropodal diaeresis (Fig. 61B) with 10-11 long as wide (terminal spine included, without spines of movable spinules (n=5). fl exor margin; n=5), terminating in one large claw with 6-8 accessory spines on fl exor margin; propodus 9.8-14.2

443 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 61. Caridina schenkeli from the Poso catchment. A. Cephalothorax and cephalic appendages, female (ZMB 29442); B. Uropodal diaeresis; C. Telson; D. Scaphocerite; E. Preanal carina, F. Third pereiopod; G. Fifth pereiopod; H. Distal end of telson; I. Dactylus of third pereiopod; J. Dactylus of fi fth pereiopod; K. Endopod of male fi rst pleopod (ZMB 29442); L. Appendix masculina of male second pleopod; M. First pereiopod, female (ZMB 29442); N. Second pereiopod; O. SEM image of chela and carpus of fi rst and second pereiopods. Scale bars: A, D = 1.0 mm; C, E-G, K-O = 0.5 mm; B, H-J = 0.1 mm.

444 THE RAFFLES BULLETIN OF ZOOLOGY 2009 times as long as wide, 3.4-4.8 times as long as dactylus; propodus, 0.6-0.7 times as long as merus; merus 7.2-9.3 carpus 5.0-6.0 times as long as wide, 0.5-0.7 times as long times as long as wide, bearing 2-3 strong, movable spines as propodus, 0.5 times as long as merus; merus 8.5-10.5 on posterior margin of outer surface. times as long as wide, bearing 3-4 strong, movable spines on posterior margin of outer surface. Endopod of male first pleopod (Fig. 61K) elongated triangular, 2.0-2.4 times as long as proximally wide (n=5), Dactylus of fi fth pereiopod (Fig. 61G,J) 3.7-4.8 times as without appendix interna. Appendix interna of male second long as wide (terminal spine included, without spines of pleopod (Fig. 56L) 0.7-0.8 times length of appendix fl exor margin; n=5), terminating in one large claw with 57- masculina (n=5). 64 accessory spines on fl exor margin; propodus 11.5-17.0 times as long as wide, 2.8-4.5 times as long as dactylus; Ovigerous females with 26-37 eggs (n=2 females); egg size carpus 4.5-7.0 times as long as wide, 0.5 times as long as 1.0-1.1 x 0.6-0.7 mm (n=30, eggs with and without eyes).

Fig. 62. Caridina schenkeli from the Poso catchment. A. Mandible (ZMB 29442); B. Maxillula; C. Maxilla; D. third maxilliped; E. second maxilliped; F. fi rst maxilliped. Scale bars: A-F = 1mm.

445 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Distribution. – C. schenkeli is endemic to the Poso catchment, conspicuously less species in Lake Poso than in the Malili but does not occur in the lake itself (Fig. 60). So far, this lakes. The considerably lower number of taxa in Lake Poso species has not been found in rivers east and south of Lake might be explained by several factors, e.g. differences in age Poso. of the lake species fl ocks or the less pronounced geographical structure of Lake Poso as a single lake. Although, these Biology and ecology. – C. schenkeli is an exclusively hypotheses would need testing. riverine species collected from various kinds of substrate (rocks, riverine vegetation, roots, dead wood). It was not The molecular phylogeny (Figs. 63-65) was used to discuss found in sympatry with the other riverine species endemic the morphology-based species description. Here, we discuss to the Poso system (C. acutirostris). the general results (compare von Rintelen et al., 2007a, b, in review): the majority of species (particularly the colourful Colour pattern. – Without any species specifi c pattern. Body specialists from the Malili lakes) appear monophyletic colouration transparently yellowish or brownish, typical for in the tree, but almost half of the morpho-species appear many other riverine species from all over Sulawesi. Large para- or polyphyletic. Based on our morphological results, (often ovigerous) females usually appear darker than smaller we regard those species that do not appear monophyletic specimens. in the tree as valid species. Nevertheless, the occasional mismatch of morphological and molecular data requires an Taxonomic remarks. – With regard to rostrum shape and explanation: Among the lacustrine generalists (Table 1), body size, C. schenkeli resembles C. acutirostris (carapace only Caridina lanceolata from the Malili lakes (Figs. 63- length in mm 3.6-5.1, median 4.2 and 3.1-5.8, median 4.1 64) and C. ensifera from Lake Poso (Fig. 65) are recovered in C. acutirostris), but differs by the ratio of rostrum to as monophyletic, while the riverine generalists C. masapi, carapace length (0.9-1.1, median 0.9 vs. 0.3-0.7, median 0.5 C. mahalona (Malili), and C. schenkeli (Poso) appear in in C. acutirostris), a generally longer rostrum (reaching near more than one clade (Figs. 64-65). In C. masapi and C. or beyond end of scaphocerite vs. shorter in C. acutirostris), mahalona, the existence of cryptic species seems most likely and a higher number of ventral rostral teeth (9-13, median as the different clades of both species form geographic 11 vs. 4-9, median 4 in C. acutirostris). clusters (allopatric distibution; compare von Rintelen et al., in review). Von Rintelen et al. (2007a) discussed the non- C. schenkeli is morphologically more variable than all other monophyly of C. schenkeli (there C. spec. B) as indicative Poso species. In the molecular phylogeny (Figs. 63,65), C. of introgressive hybridization, because the lack of distinctive schenkeli does not appear monophyletic, but based on its colour patterns might facilitate ‘mating errors’ in this taxon. distinctive morphology it is here regarded as a single valid A similar scenario was suggested by the same authors for the species that might sometimes hybridize with other species lacustrine species C. longidigita and C. sarasinorum from (compare von Rintelen et al., 2007a). Lake Poso. In contrast, the always distinctive and species- specifi c colour patterns of C. ensifera, C. caerulea (Poso), and of the majority of the colourful specialists from the DISCUSSION Malili lake system (Table 1) seem to prevent hybridization. The molecular phylogeny further shows that the specialized Radiation, ecology, and species diversity of freshwater lacustrine species C. holthuisi from the Malili lakes also shrimps in the ancient lakes of Sulawesi appears in two geographically distinct clades (Fig. 64) that are not sister groups to each other. Hence, the genetic data Von Rintelen et al. (in review) suggested at least three (albeit the current lack of morphological differences between independent colonization events for the ancient lakes of representatives of both clades) rather suggest the existence of Sulawesi, one for Lake Poso and two for the Malili lakes two cryptic species than hybridization or incomplete lineage (compare Fig. 63). However, only one of the Malili invasions sorting. The only genetically (and partly morphologically, if led to a subsequent radiation (von Rintelen et al., in review). the colour patterns in living animals is ignored) completely Contrary to Woltereck’s (1937a, b) assumption, all lacustrine unresoved clade of specialists from the Malili lakes comprises species in the Malili system are endemic. Beyond these, the sponge-dweller C. spongicola and the morphologically the entire Malili species fl ock (i.e. including the riverine almost indistinguishable rock-dwellers C. glaubrechti, C. species of the lakes’ catchment) is endemic to the Malili striata, and C. woltereckae (Fig. 64, compare von Rintelen system, except for C. mahalona. A single specimen of that et al. 2007b). This insuffi cient resolution, with basically no species was caught in the southernmost part of the Tomori geographical pattern, might be caused by incomplete lineage area just north of Lake Matano (Figs. 1C). Previous studies sorting due to very recent speciation events, introgression, on the ecology of the ancient lake species (Zitzler & Cai, or the misinterpretation of intraspecifi c polymorphism as 2006; von Rintelen et al. 2007a, b, in review) suggested different species. In the fi rst case, a better resolution might the existence of substrate specialists and generalists in both be gained with certain nuclear markers (e.g. AFLPs), species fl ocks. These results are confi rmed in this paper and which would also serve to test the other hypotheses. It is summarized for all species in Table 1. This revision, and here regarded as rather unlikely that the four taxa are just the results gained by von Rintelen et al. (2007a, in review), intraspecifi c colour variants, as they also exhibit considerable reveal that the total number of species is almost twice as high differences in behaviour, particularly the widespread C. than previously described (Table 2). In general, there are striata and C. woltereckae. These species also differ in their

446 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 63. Bayesian Inference phylogram (mtDNA, 16S and COI) of Caridina from the ancient lakes of Sulawesi (for other taxa compare von Rintelen et al., in review). Numbers on branches are, from top, Bayesian posterior probabilities, ML and MP bootstrap values. The scale bar indicates the number of substitutions per site. For each sequenced specimen museum accession numbers are provided. Locality abbreviations (compare Fig. 1): Lam (Lampesue River catchment), LT (Lake Lontoa), MHL (Lake Mahalona), MS (Lake Masapi), MT (Lake Matano), MTca (Lake Matano catchment), Pat (Patingko River), Pon (Ponsoa River), TW (Lake Towuti), TWca (Lake Towuti catchment), PS (Lake Poso), PSca (Lake Poso catchment), SSul (South Sulawesi), SESul (Southeast Sulawesi).

447 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

Fig. 64. Bayesian Inference phylogram (mtDNA, 16S and COI) showing taxa within the two Malili clades (for other taxa compare von Rintelen et al., 2009). For each sequenced specimen museum accession numbers are provided. Locality abbreviations (compare Fig. 1): Lam (Lampesue River catchment), LT (Lake Lontoa), MHL (Lake Mahalona), MS (Lake Masapi), MT (Lake Matano), MTca (Lake Matano catchment), Pat (Patingko River), Pon (Ponsoa River), TW (Lake Towuti), TWca (Lake Towuti catchment), SSul (South Sulawesi).

448 THE RAFFLES BULLETIN OF ZOOLOGY 2009 use of the same substrate, and C. spongicola is not a rock sponge), and only single specimens of two other species (C. dweller at all. In a certain sense, one can regard the three lingkonae and C. striata) were found on the sponges as well rock dwellers as morphologically and genetically (at least (von Rintelen et al., 2007b; KvR personal fi eld observation). with mtDNA) cryptic species. Moreover, the colour pattern The specimens from three populations of C. glaubrechti, of C. spongicola seems less fi xed than that of the other three which group with morphologically very different species, species and usually resembles that of C. woltereckae, in few show no apparent morphological differences to the remaining cases also C. glaubrechti. This might hint at a less species- populations. Again, introgressive hybridization could play specifi c and still variable colour pattern in C. spongicola, a role, but also the existence of cryptic species cannot be but besides minor morphological differences, the choice excluded as those populations form a coherent geographic of habitat of C. spongicola differs greatly from the rock cluster in Lake Towuti. The species boundaries of the three dwellers. In 15 dissected sponges a high number of C. rock dwellers may not yet be as fixed as in most other spongicola specimens were found (maximum 137 in a single Malili species, but this is probably just a question of time

Fig. 65. Bayesian Inference phylogram (mtDNA, 16S and COI) showing taxa within the Poso clade (tree topology from von Rintelen et al., in review). For each sequenced specimen museum accession numbers are provided. Locality abbreviations (compare Fig. 1): PS (Lake Poso), PSca (Lake Poso catchment).

449 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi since the colour pattern obviously seems to be an effective colourful ones, are highly endangered of becoming extinct. delimitation factor in the other taxa (compare von Rintelen Thus, sampling of living specimens should be sensibly et al., 2007a, b, in review). limited and other precautions are necessary to preserve the species diversity in the ancient lakes of Sulawesi also for In cases involving allopatric populations of a single species, future generations. the problem of species delimitation of allopatric taxa arises, e.g. the Towuti versus Mahalona populations in C. tenuirostris or the Matano versus Mahalona/Towuti populations in C. ACKNOWLEDGEMENTS lanceolata (Fig. 64), which form separate and genetically suffi ciently distant clades. Roy et al. (2006) discussed the Thomas von Rintelen and Matthias Glaubrecht (ZMB) possibility that C. lanceolata might comprise cryptic species, kindly helped collecting specimens and fi nanced part of the because they found larger sequence divergence between fi eldwork. We thank both for the great opportunity to work allopatric populations from Lake Matano and Mahalona. on the fauna of the fascinating lake systems of Sulawesi. Following their argument would mean to accept that C. Ristiyanti Marwoto and Daisy Wowor (MZB) greatly tenuirostris also comprises two species, since distances supported the fi eldwork in Indonesia and gave overall logistic between the two clades of that species are comparable to that support. PT. INCO in Soroako, Indonesia, provided logistic of C. lanceolata. However, the approach taken here is not support at the Malili lakes. to split morphologically and ecologically indistinguishable (allopatric) populations into separate species, particularly if Carsten Lüter (ZMB) fi nancially supported a fi eld trip in they are sister group to each other. 2004. The Advancement of Women (Frauenförderung, ZMB) supported the fi rst author of this study with two travel grants and the purchase of a graphic software suite for preparing Conservation implications for the ancient lake the fi gures. Chris Lukaup (Bittenfeld, Germany) provided species of Sulawesi most of the beautiful colour pictures presented in this study. Rainer Masche (Heidelberg, Germany) kindly provided the We found a higher number of species than previously colour pictures of Caridina tenuirostris and C. profundicola. described. This is by no means a rare phenomenon in endemic Many thanks to the following people for collecting some organisms from the ancient lakes of Sulawesi. The species specimens: Arne Nolte (University Cologne, Germany), Peter diversity in other groups was likewise much higher than Koller (University Regensburg, Germany), Fabian Herder expected, e.g. in snails (von Rintelen et al., 2007c). Several and Joachim Frommen (Museum Koenig, Bonn, Germany), authors discuss the possibility of the extinction of endemic Rebecca Lamers and Andreas Wessel (ZMB). We further species from Sulawesi and the ancient lakes (Whitten et al., thank two anonymous referees for their valuable comments 1987a, b; von Rintelen et al., 2007c, in review). They hint at and their stamina while reading the long manuscript. the various threats in these lakes posed by introduced predator fi sh (e.g. tilapia, snakeheads, and carp), the Canadian nickel mine P.T. INCO at Lake Matano, the quantities of waste LITERATURE CITED directed into the lakes from the rapidly expanding human population and the unlicensed export of native specimens. Abendanon, E. C., 1915. Midden-Celebes-Expeditie. Geologische Further, illegal logging around the lakes’ shoreline can cause en geographische doorkruisingen van Midden-Celebes (1909- 1910). E.J. Brill, Leiden. erosion and subsequent landslides. Recently, not only the colourful species of Caridina, but also snails, crabs, and Bouvier, E.-L., 1904. Crevettes de la famille des Atyidés: espèces qui font partie des collections du Muséum d’Histoire naturelle. fi shes from the lakes have caused a sensation in commercial Bulletin du Museum National d’Histoire Naturelle, 104: 129- aquarium trade and tens of thousands of specimens were 138. exported to various countries, especially to Germany (Chris Bouvier, E.-L., 1905. Observations nouvelles sur les Crevettes de Lukhaup, pers. comm. 2007). In addition, in standard aquatic la famille des Atyidés. Bulletin scientifi que de la France et de toxicity tests members of the shrimp genus Caridina from la Belgique, 39: 55-134. Java, Indonesia, showed a higher sensitivity for some Bouvier, E.-L., 1912. Sur la classifi cation du genre Caridina et chemicals than other freshwater (Sucahyo et al., les variations extraordinaires d’une espèce de ce genre, la 2008) and the species of Caridina from the ancient lakes Caridina brevirostris. Comptes Rendus de l’Académie des thus seem even more threatened by human impact. sciences, 154, 915-922. Bouvier, E.-L., 1913a. The Percy Sladen Trust Expedition, XXVIII. The shrimps’ diversity of colourful species is only one Les Caridines dees Seychelles.Transactions of the Linnean aspect of the fascinating fauna of Sulawesi’s ancient lakes. Society of London, 15, 447-472. They are also home to many rare and unusual species and Bouvier, E.-L., 1913b. Sur la classifi cationdes Crevettes de la communities, for example the fi rst shrimp-sponge association famille des Atyidés. Bulletin de la Société entomologique de described in freshwater organisms (von Rintelen et al., 2007b) France, 1913, 177-182. or the numerous endemic and often colourful fi shes, snails, Bouvier, E.-L., 1925. Recherches sur la morphologie, les variations, and crabs that make the lakes similarly worth of protection la distribution géographique des crevettes de la famille des as e.g. the Galapagos Islands. Some of the locally restricted Atyidés. Encyclopédie Entomologique, series A, 4: 1-370. species with partly very small populations, especially the

450 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Brooks, J. L., 1950. Speciation in ancient lakes. Quarterly Review Holthuis, L. B., 1955. The recent genera of the caridean and of Biology, 25: 131-176. stenopodidean shrimps (Class Crustacea, Order Decapoda, Cai, Y. & D. Wowor, 2007. Atyid shrimps from Lake Poso, Supersection Natantia) with keys for their determination. Central Sulawesi, Indonesia with description of a new species Zoologische Verhandelingen, 26: 1-157. (Crustacea: Decapoda: ). The Raffl es Bulletin of Zoology, Kottelat, M., 1990a. Sailfi n silversides (Pisces: Telmatherinidae) of 55: 311-230. Lakes Towuti, Mahalona and Wawontoa (Sulawesi, Indonesia) Cai, Y., D. Wowor & S. Choy, 2009. Partial revision of freshwater with descriptions of two new genera and two new species. shrimps from Central Sulawesi, Indonesia, with descriptions Ichthyological Explorations of Freshwaters, 1: 227-246. of two new species (Crustacea: Decapoda: Atyidae). Zootaxa, Kottelat, M., 1990b. The ricefishes (Oryziidae) of the Malili 2045: 15-32. Lakes, Sulawesi, Indonesia, with description o a new species. Chace, F. A., 1997. The Caridean Shrimps (Crustacea: Decapoda) Ichthyological Explorations of Freshwaters, 1: 151-166. of the Albatross Phillipine Expedition, 1907-1910, Part Milne Edwards, H., 1837. Histoire Naturelle des Crustacés, 7: Families Atyidae, Eugonatonotidae, Rhynchocinetidae, Comprenant l’Anatomie, la Physiologie et la Classifi cation de Bathypalaemonellidae, Processidae, and Hyppolytidae. ces Animaux. Libraire Encyclopedique de Roret, Paris. Smithsonian Contributions to Zoology, 587: 1-106. Roux, J., 1904. Décapodes d’eau douce de Célèbes. Revue Suisse Crowe, S. A., A. H. O’Neill, S. Katsev, P. Hehanussa, G. D. Haffner, de Zoologie, 12: 539-572. B. Sundby, A. Mucci & D. A. Fowle, 2008. The biogeochemistry Roy, D., D. W. Kelly, C. H. J. M. Fransen, D. D. Heath & G. D. of tropical lakes: A case study from Lake Matano, Indonesia. Haffner, 2006. Evidence of small-scale vicariance in Caridina Limnology and Oceanography, 53: 319-331. lanceolata (Decapoda, Atyidae) from the Malili Lakes, Sulawesi. Fernandez-Leborans, G. & K. von Rintelen, 2007. Epibiontic Evolutionary Ecology Research, 8: 1087-1099. communities on the freshwater shrimp Caridina ensifera Sarasin, P. & F. Sarasin, 1905. Reisen in Celebes ausgeführt in den (Crustacea, Decapoda, Atyidae) from Lake Poso (Sulawesi, Jahren 1893-1896 und 1902-1903. Kreidel, Wiesbaden. Indonesia). Journal of Natural History, 41: 2891-2917. Schenkel, E., 1902. Beitrag zur Kenntnis der Dekapodenfauna von Fernandez-Leborans, G., K. Zitzler & R. Gabilondo, 2006a. Epibiont Celebes. Verhandlungen der Naturforschenden Gesellschaft in protozoan communities on Caridina lanceolata (Crustacea, Basel, 13: 485-585. Decapoda) from the Malili lakes of Sulawesi (Indonesia). Zoologischer Anzeiger, 245: 167-191. Schubart, C. D. & P. K. L. Ng, 2008. A new molluscivore crab from Lake Poso confirms multiple colonisation of ancient Fernandez-Leborans, G., K. Zitzler & R. Gabilondo, 2006b. lakes in Sulawesi by freshwater crabs (Decapoda: Brachyura). Protozoan ciliate epibionts on the freshwater shrimp Caridina Zoological Journal of the Linnean Society, 154: 211-221. (Crustacea, Decapoda, Atyidae) from the Malili lake system on Sulawesi (Indonesia). Journal of Natural History, 40: Schubart, C. D., T. Santl & P. Koller, 2008. Mitochondrial patterns 1983-2000. of intra- and interspecific differentiation among endemic freshwater crabs of ancient lakes in Sulawesi. Contributions Fryer, G., 1960. The feeding mechanisms of some atyid prawns to Zoology, 77: 83-90. of the genus Caridina. Transactions of the Royal Society of Edinburgh, 64: 217-244. Sucahyo, D., N. M. van Straalen, A. Krave, C.A.M. van Gestel, 2008. Acute toxicity of pesticides to the tropical freshwater Giesen, W., 1994. Indonesia’s major freshwater lakes: a review shrimp Caridina laevis. Ecotoxicology and Environmental of current knowledge, development processes and threats. Safety, 69 :421-7. Mitteilungen des Internationalen Vereins für Limnologie, 24: 115-128. von Rintelen, K., T. von Rintelen, & M. Glaubrecht, 2007a. Molecular phylogeny and diversifi cation of freshwater shrimps Giesen, W., M. Baltzer & R. Baruadi, 1991. Integrating (Decapoda, Atyidae, Caridina) from ancient Lake Poso conservation with land-use development in wetlands of South (Sulawesi, Indonesia) - the importance of being colourful. Sulawesi. Directorate General of Forest Protection and Nature Molecular Phylogenetics and Evolution, 45: 1033-1041. Conservation, Bogor. von Rintelen, K., T. von Rintelen, M. Meixner, C. Lüter, Y. Cai & Haffner, G. D., P. E. Hehanussa & D. Hartoto, 2001. The biology M. Glaubrecht, 2007b. Freshwater shrimp-sponge association and physical processes of large lakes of Indonesia: Lakes Matano from an ancient lake. Biology Letters, 3: 262-264. and Towuti. In: Munawar, M. & R. E. Hecky (eds.). The Great Lakes of the World (GLOW): Food-web, health and integrity. von Rintelen, K., A. Karge, & W. Klotz, 2008. News from a small Backhuys Publishers, Leiden. Pp. 183-192. island – fi rst record of a freshwater shrimp (Decapoda, Atyidae, Caridina) from Peleng, Banggai Islands, Indonesia. Journal of Haffner, G. D., L. Sabo, A. Bramburger, P. Hamilton & P. Natural History, 42: 2243-2256. Hehanussa, 2006. Limnology and sediment dynamics in the Malili Lakes: What regulates biological reproduction? In: von Rintelen, K., M. Glaubrecht, C. D. Schubart & T. von Proceedings International Symposium Bogor, Indonesia 20-22 Rintelen, (in review). News from Wallace’s dreamponds: March 2006. PT INCO Tbk., Indonesian Institute of Science, adaptive radiation of colourful shrimps from the Malili lakes Research Centre for Limnology. P. 5. of Sulawesi. Proceedings of the Royal Society B: Biological Sciences, in review. Herder, F., A. W. Nolte, J. Pfaender, J. Schwarzer, R. K. Hadiaty & U. K. Schliewen, 2006. Adaptive radiation and hybridization von Rintelen, T., A. B. Wilson, A. Meyer & M. Glaubrecht, 2004. in Wallace’s Dreamponds: evidence from sailfi n silversides in Escalation and trophic specialization drive adaptive radiation of the Malili Lakes of Sulawesi. Proceedings of the Royal Society freshwater gastropods in ancient lakes on Sulawesi, Indonesia. B: Biological Sciences, 273: 2209-2217. Proceedings of the Royal Society B: Biological Sciences, 271: 2541-2549. Herder, F., J. Pfaender & U. K. Schliewen, 2008. Adaptive sympatric speciation of polychromatic „roundfi n“ sailfi n silverside fi sh in von Rintelen, T., P. Bouchet & M. Glaubrecht, 2007c. Ancient Lake Matano (Sulawesi). Evolution, 62: 2178-2195. lakes as hotspots of diversity: a morphological review of an

451 von Rintelen & Cai: Revision of Caridina from ancient lakes of Sulawesi

endemic species fl ock of Tylomelania (Gastropoda: Cerithioidea: Woltereck, E., 1937b. Zur Systematik und geographischen Pachychilidae) in the Malili lake system on Sulawesi, Indonesia. Verbreitung der Caridinen. Internationale Revue der gesamten Hydrobiologia, 592: 11-94. Hydrobiologie und Hydrographie, 34: 294-330. Whitten, A. J., K. D. Bishop, S. V. Nash & L. Clayton, 1987a. One Woltereck, R., 1933a. Meine Forschungsreise nach Amerika und or More Extinctions from Sulawesi, Indonesia? Conservation Ostasien zum Studium insulärer und lakustrischer Endemismen. Biology, 1: 42-48. Internationale Revue der gesamten Hydrobiologie und Whitten, T., G. S. Henderson & M. Mustafa, 1987b. The Ecology of Hydrographie, 28: 338–349. Sulawesi. The Ecology of Indonesia Series, Volume IV. Gadjah Woltereck, R., 1933b. Mitteilungen von der Wallacea-Expedition Mada University Press. Woltereck. Mitt. III. Das hauptsächliche Arbeitsgebiet. Woltereck, E., 1937a. Systematisch–variationsanalytische Zoologischer Anzeiger, 102: 319–326. Untersuchungen über die Rassen- und Artbildung bei Zitzler, K. & Y. Cai, 2006. Caridina spongicola, new species, a Süßwassergarnelen aus der Gattung Caridina (Decapoda, freshwater shrimp (Crustacea: Decapoda: Atyidae) from the Atyidae). Internationale Revue der gesamten Hydrobiologie ancient Malili lake system of Sulawesi, Indonesia. Raffl es und Hydrographie, 34: 208-262. Bulletin of Zoology, 54(2): 271–276.

452 THE RAFFLES BULLETIN OF ZOOLOGY 2009

THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 453–464 Date of Publication: 31 Aug.2009 © National University of Singapore

PERICLIMENAEUS NUFU, A NEW SPECIES OF SHRIMP (CRUSTACEA: DECAPODA: PONTONIINAE) FROM VIETNAM

Zdene ˇk Durišˇ Department of Biology and Ecology, Faculty of Natural Sciences, University of Ostrava, Chittussiho 10, 710 00 Ostrava, Czech Republic Email: [email protected]

Ivona Horká Department of Biology and Ecology, Faculty of Natural Sciences, University of Ostrava, Chittussiho 10, 710 00 Ostrava; and Department of Ecology, Faculty of Natural Sciences, Charles University, Vinic ˇná 7, 128 44 Prague, Czech Republic Email: [email protected]

Dao Tan Hoc Institute of Oceanography, Vietnamese Academy of Sciences and Technology, Nhatrang, Vietnam Email: [email protected]

ABSTRACT. – A new species of the commensal pontoniine shrimp genus Periclimenaeus, P. nufu, new species, was found in samples from dead coral habitats in shallow Vietnamese waters (Van Phong Bay) of the South China Sea. The new species is placed in the Periclimenaeus robustus species group, with a characteristic anteromedian rounded lobe on the fi rst abdominal tergite. It is readily distinguishable from most species of the genus by the unique shape of the widely ovate uropodal exopods; their distolateral margins and unusually rounded distolateral angles are distinctly serrate. Other remarkable features are the produced, movable anterovental angle of the carapace, ambulatory dactyli with long and slender unguis, and with a markedly reduced additional unguis. The true host of the single specimen available, assumed to be an encrusting sponge, is unknown. The new species is described and illustrated, and a key to distinguish related species is proposed.

KEY WORDS. – South China Sea, Pontoniinae, Periclimenaeus nufu, new species.

INTRODUCTION of many of these species remain unreported, most are known as associates of sponges or compound ascidians (Bruce, A Norwegian-Vietnamese research project devoted to 1976; Marin, 2007). The dead coral habitat is not typical studies on the biotic communities of dead coral rubble for shrimps of this genus; however, encrusting or boring habitats was held in 2003 and 2006, and included collecting sponges and colonial ascidia may often grow within dead expeditions at various sites of the Van Phong and Nhatrang bases of live corals and on blocks of coral rubble. Bays, Vietnam. Identification of symbiotic shrimps from these collections, deposited in the museum of the A single specimen of an as-yet undescribed species of the Oceanographic Institute, Vietnamese Academy of Sciences genus Periclimenaeus was found in a sample from rather and Technology, Nhatrang, yielded the discovery of one shallow water; the actual host is unknown. This new species, new species of the genus Periclimenaeus Borradaile, and described below, increases the number of congeners known also several new records of shrimps that will be published in Vietnamese waters of the South China Sea to ten. This in a separate report. number is evidently underestimated, and further records will surely follow. About 69 species of the pontoniine genus Periclimenaeus, the second most speciose genus of the palaemonid subfamily The following abbreviations are used: CL, postorbital Pontoniinae, are currently known, of which at least 56 are carapace length; RF, rostral formula; ION, Institute of distributed throughout the Indo-West Pacifi c area, including Oceanography, Academy of Sciences and Technology, exclusively symbiotic forms. Despite the fact that the hosts Nhatrang, Vietnam.

453 Durišˇ et al.: Periclimenaeus nufu, new species from Vietnam

SYSTEMATICS Abdomen smooth, fi rst segment tergite with low, anteriorly directed and fl attened median lobe on dorsal surface (Fig. Family Palaemonidae Rafi nesque, 1815 2E), pleura rounded, fourth and fi fth posteriorly produced, rounded, sixth segment median length subequal to fifth Subfamily Pontoniinae Kingsley, 1878 segment length, posterolateral and posteroventral angles produced, subacute. Genus Periclimenaeus Borradaile, 1915 Telson (Fig. 2F) about 1.4 times sixth abdominal segment Periclimenaeus nufu, new species length, 0.5 of CL, 1.7 times longer than anterior width; (Figs. 1–5) lateral margins feebly convex, posteriorly convergent; dorsal telson spines about 0.16-0.18 of telson length, Material examined. – Holotype: female (CL 1.9 mm, TL 6.5 situated at 0.2 and 0.5 of telson length; posterior margin mm), ION R.4254/E.54104, sample n. 10.D2, Bai Tré site, Lon broadly convex without median point, lateral posterior o o Island, 12 36'25"N, 109 19'58"E, Van Phong Bay, Vietnam, South spines half of dorsal spines length, situated in advance of China Sea, 28 Sep.2003, depth 5m, coral rubble, coll. ION staff intermediate and submedian spines, intermediate spines (Department of Marine Living Resources). subequal to dorsal spines, submedian spines 1.3 times longer than intermediate spines, stout, setulose. Diagnosis. – Rostral dentition 4/0; anteroventral angle of carapace produced, movable; telson with two pairs of large Eyes (Fig. 2A) with globular cornea situated obliquely on dorsal spines at 0.2 and 0.5 of telson length, posterior margin stalk, with small accessory pigmented spot dorsally on stalk with lateral spines situated anteriorly from remaining spines; close to posterior corneal margin; corneal diameter about fi rst abdominal segment tergite with anterior median lobe; 0.2 of postorbital CL; stalk short, swollen, medial length mandibular incisor process normal, distally dentate; fi rst about 1.5 of corneal diameter. pereiopod fi ngers with cutting edges entire, carpus longer than chela, coxa with distal lobe dorsally and unarmed Antennule (Figs. 2A,C) of normal form; basal peduncular ventrally; major second pereiopod with dactyl almost segment about 2.5 times as long as central width, stylocerite semicircular dorsally and with low plunger ventrally, elongate, subtriangular, distally acute and laterally rounded, palm looks granulate – covered by numerous soft papillae; lateral margin straight, slightly tapering distally, distolateral minor second pereiopod fi ngers with cutting edges simple, tooth stout, subtriangular, overreaching anterior margin, straight, shear-like fi ngers shorter than palm, palm papillose; reaching almost to distal end of intermediate segment, ambulatory dactyli biunguiculate, with slender unguis medial margin with minute ventromedial tooth at about subequal to corpus length and distoventral tooth feebly 0.4 of segment length; intermediate segment about 0.2 developed, ventral margin of corpus concave, denticulate of proximal segment length, distinctly wider than long, proximally; uropodal rami broadly ovate, distolateral angle distal segment slightly longer than preceding, length of exopod rounded, serrate. subequal to width; upper fl agellum biramous; four proximal segments fused, short ramus with three segments, 6 groups Etymology. – The abbreviation NUFU (Norwegian Program of aesthetascs; longer ramus slender, with about seven for Development, Research and Education) is adopted as segments, lower fl agellum similar, slender with about 10 the specifi c name for the new species, in reference to the segments. Vietnamese-Norwegian research project under which the type specimen was collected and examined. Antenna (Fig. 2D) of normal form; basicerite short, laterally and dorsally unarmed; carpocerite subcylindrical, reaching Description (based on the female holotype). – A small about 0.75 of scaphocerite length; scaphocerite about 2.5 sized pontoniine shrimp of subcylindrical form belonging times longer than broad, broadest at about 0.6 of length, to the Periclimenaeus robustus species group (Bruce, 2005) anterior margin rounded, lateral margin slightly concave, (Fig. 1). almost straight, with well developed distal tooth reaching level of distal margin of lamella. Rostrum (Fig. 2B) about 0.35 of CL, reaching distal end of basal segment of antennular peduncle, slightly arched Thoracic sternites narrow and unarmed. dorsally with four acute teeth, fi rst tooth well in advance of posterior orbital margin, with short interspersed setae, Mouthparts (Fig. 3) from left side dissected. Mandible (Fig. ventral lamina toothless, straight, upturned proximally. 3A,B) without palp; incisor process well developed, with four apical teeth, molar process tapering distally, with four Carapace (Figs 1; 2A,B) smooth, without epigastric, groups of subacute teeth. supraorbital or hepatic spines, with a low swollen tubercle in postorbital position; antennal spine well developed, Maxillula (Fig. 3C) with bilobed palp (Fig. 3D), lower marginal, inferior orbital angle obsolete, anteroventral lobe short, with small spinule; upper lacinia broad, dorsal margin of carapace produced, rounded, forming soft margin convex, distal margin with about eight strong movable plate. serrate spines and several slender serrulate setae; lower lacinia short, truncate, with a group of about eight slender

454 THE RAFFLES BULLETIN OF ZOOLOGY 2009 terminal and four subterminal setae, several long setae on features; coxa medially angulate with pair of setae; exopod ventral margin. normally developed with four plumose terminal setae; epipod elongate, reaching two-thirds of ischiobasal length, Maxilla (Fig. 3F) with simple palp, tapering, distally rounded distally, without podobranch. rounded, basally setose, slightly shorter than basal endite, basal endite deeply bilobed, upper lobe with about eight Third maxilliped (Fig. 3I) stout, with endopod slightly slender simple setae and single plumose distal seta, lower overreaching distal end of carpocerite; coxa with minute lobe slightly more than 3 times longer than central width, ventral tubercle, non-setose, lateral plate semicircular, anterior lobe about 1.5 times longer than basal width, arthrobranch absent; basis fused with ischiomerus, combined medial margin slightly angulate proximally, marginal setae ischio-basal segment about 3.5 times longer than basal plumose; posterior lobe well developed. width, with series of long and short spiniform setae ventrally and pair of short distolateral setae; penultimate segment First maxilliped (Fig. 3G) with elongate flattened palp, about 0.45 of ischio-basal segment length, 2.5 times longer about thrice longer than central width, not reaching anterior than wide, with ventrolateral and ventromedial rows of margin of basal endite, with single preterminal plumose long spiniform setae and pair of short distolateral setae - seta; basal endite with distal margin produced, rounded, one spiniform; terminal segment about 0.6 of penultimate medial margin straight with numerous slender setulose setae segment length, with pair of terminal spines longer than and one single seta; coxal endite divided from basal endite segment and scattered shorter spiniform setae ventrally and by shallow emargination, with several long setulose setae on sides of ventral margin; exopod normally developed, medially; exopod with normal fl agellum with four plumose subequal to ischio-basal segment, with four plumose terminal setae, caridean lobe large; produced, with lateral terminal setae. margin broadly rounded, marginal setae plumose; epipod well developed, deeply bilobed, lobes elongate, distally First pereiopods (Fig. 4A-B) stout, overreaching carpocerite rounded. by distal end of merus; chela with palm subcylindrical, compressed, 1.7 times longer than deep, fi ngers similar, Second maxilliped (Fig. 3H) with normally developed subequal to palm length, broad and high basally and tapering endopod, dactylar segment broad, about thrice longer distally, with groups of short stiff setae, subspatulate, with than maximum width, distomedial margin straight, with elongate unguis and small adjacent tooth distally (Fig. 4C), numerous serrulate spines; propodal segment normal, cutting edges medial, entire; carpus 1.2 times chela length, distomedial margin weakly convex with several simple thrice longer than distal width, tapering proximally; merus spines; carpus, merus and ischiobasis without special slightly longer than carpus and 5 times longer than central

Fig. 1. Periclimenaeus nufu, new species, female holotype. Scale bar = 1 mm.

455 Durišˇ et al.: Periclimenaeus nufu, new species from Vietnam

Fig. 2. Periclimenaeus nufu, new species, female holotype. A, anterior cephalothorax, eyes and antennae, dorsal . B, anterior carapace, lateral. C, antennule, dorsal. D, antenna, ventral. E, posterior carapace and anterior fi rst abdominal segment, dorsal. F, telson, dorsal. G, same, distal part. H, right uropod, dorsal. I, same, exopod, with distolateral margin enlarged. Scale bars = 0.5 mm.

456 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 3. Periclimenaeus nufu, new species, female holotype, mouthparts (from the left side). A, mandible. B, same, molar and incisor processes. C, maxillula. D, same, palp. E, same, laciniae. F, maxilla. G, fi rst maxilliped. H, second maxilliped. I, third maxilliped. Scale bars = 1 mm.

457 Durišˇ et al.: Periclimenaeus nufu, new species from Vietnam depth; ischium two thirds of merus length; basis without slightly proximally, ventral margin convex; with series special features; coxa simple ventrally but dorsally produced of long setae along ventral margin of palm and fixed to distinct lobe with rounded tip. fi nger; fi ngers about two thirds of palm length, dactylus compressed, slightly exceeding fi xed fi nger, about 2.4 times Major second pereiopod (Fig. 4D) well developed, length longer than maximal depth, dorsal margin convex, tip blunt, about twice CL, palm about twice longer than maximal cutting edge simple; fi xed fi nger basal width subequal to depth, slightly swollen proximally, oval in section, covered dactylus width, rather straight, tapering distally to upturned with small soft papillose tubercles (Fig. 4) dorsally and subacute tip, cutting edge grooved proximally; carpus short, ventrally, ventral tubercles aligned to transversal rows (Fig. less than 0.4 of palm length, stout, distally excavate, length 4F); fi ngers (Fig. 4E) 0.4 of palm length, sparsely setose; subequal to distal depth, ventral margin simple; merus short dactyl twice longer than maximal depth, dorsal margin and stout, slightly longer than both carpus length and half strongly convex, with stout obtuse hooked tip, cutting of palm length, about 1.7 times longer than central depth, edge with low elongate molar process proximally, distal ventral margin tuberculate; ischium subequal to merus cutting edge convex, entire; fi xed fi nger tapering distally, length, ventral margin with distomesial rounded lobe; basis tip hooked; carpus about 0.35 of palm length, narrow and coxa short, robust, without special features. proximally, broadly expanded distally, several tubercles ventrally; merus about 0.4 of palm length, robust, twice Ambulatory legs robust; third pereiopods (Fig. 5A, C) longer than central depth, tuberculate ventrally; ischium with dactyli (Fig. 5B, D) 0.4 of propod length, feebly 0.8 of meral length, twice longer than distal depth, tapering biunguiculate; unguis distinctly demarcated, slender, 5 proximally, without ventral denticles; basis and coxa times longer than basal width, slightly curved, corpus normal, without special features. compressed, about twice longer than proximal depth, tapering distally, dorsal margin slightly convex, ventral Minor second pereiopod (Fig. 4H) chela length subequal to margin sinuate, with minute but acute distal accessory tooth CL, with palm (Fig. 4I) tuberculate dorsally and ventrally, somewhat separated from base of unguis, three minute sharp oval in section, 1.5 times longer than central depth, tapering denticles proximally on corpus; propod about 0.55 of CL,

Fig. 4. Periclimenaeus nufu, new species, female holotype. A, right fi rst pereiopod, lateral. B, same, distal segments, lateral. C, same, tips of fi ngers. D, major second pereiopod, lateral. E, same, distal palm and fi ngers, mesial. F, same, ventral margin of palm. G, same, tubercle from ventral palm. H, minor second pereiopod, lateral. I, same, chela. Scale bars = 1 mm.

458 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 5. Periclimenaeus nufu, new species, female holotype. A, left third pereiopod, lateral. B, same, distal propodus and dactylus. C, right third pereiopod, lateral. D, same, distal propodus and dactylus. E, right fourth or fi fth pereiopod, lateral. F, same, distal propodus and dactylus. G, left fi fth pereiopod, lateral. H, same, distal propodus and dactylus, mesial. Scale bars: A, C, E-G = 1 mm; B, D, F, H = 0.1 mm.

459 Durišˇ et al.: Periclimenaeus nufu, new species from Vietnam

3.8 times longer than proximal width, tapering distally, and P. uropodialis Barnard, 1958. In both these species the distoventral angle armed with two stout spines about 0.5 margin is deeply serrate and the distolateral angle terminates of dorsal corpus length, three to four additional smaller in a row of four to six spines; these species also possess a single spines irregularly spaced on ventral margin, with supraorbital spine that is lacking in the present new species, proximal one smallest and close to preceding spine; carpus and differ also (see the key below) in the rostral armament, subequal and as stout as propod, about 3.5 times longer than dorsal and terminal telson spines, and ventral spination of distal width, tapering proximally, unarmed; merus subequal ambulatory propodi (Kubo, 1940; Barnard, 1958; Miyake to propod length but stouter, about 3 times longer than & Fujino, 1967). In other congeners, the lateral margin of proximal width, several sharp tubercles ventrally; ischium the uropodal exopod is straight or moderately convex and two thirds of propod length, slightly more slender than terminates with a more or less distinct tooth and a movable merus, tapering proximally; basis and coxa robust, without spine medially. This movable spine is also well developed special features. in the present species. A similar lobate distolateral angle of the uropodal exopod was described for all three species Fourth and fifth pereiopods (Fig. 5E, G, respectively) of the related genus Paraclimenaeus Bruce, P. fi mbriatus generally similar and subequal to third pereiopods, with (Borradaile, 1915), P. spinicauda (Bruce, 1969) and P. daclyli (Fig. 5F, H, respectively) gradually slightly slender seticauda (Bruce, 2008) but the marginal serration of these and longer than third dactylus; fourth dactylus with species is equipped with long spines (Bruce, 1969, 1988, accessory tooth vestigial, corpus with only single proximal 2009). In the present new species only inconspicuous denticle on ventral margin; fourth propodus with distoventral denticles are present on the distal serrations. Paraclimenaeus pair of spines short, 0.25 of dactylar corpus dorsal length; differs from Periclimenaeus in the specifi c setation of the fi fth dactylus with unguis unusually long, nine times longer fi rst chelae, in the sound-producing structure on the second than basal width, additional unguis inconspicuous, corpus pereiopods with the plunger situated on the fi xed fi nger and unarmed; additional ventral spines lacking; fi fth propod the fossa on dactyl, and other characters listed in the original totally unarmed. generic diagnosis (Bruce, 1988).

Uropods (Fig. 2H) with protopodite posterolaterally Another peculiar structure is the ‘movable’ anteroventral unarmed; exopod (Fig. 2I) broadly ovate, subequal to (pterygostomial) angle of the carapace. In the present telson length, 1.6 times longer than broad, lateral margin species, the angle, much softer than the remaining carapace, convex with distal half serrate, non-setose, distolateral is well produced and divided from the carapace by a angle produced to rounded serrate lobe, serration with distinct suture. It is possible that the latter is not unique, vestigial terminal denticles (Fig. 2I-detail), distolateral lobe but has just gone uncommented in previous reports. A medially with slender acute spine with incurved tip, spine similar anteroventral lobe, subdivided from the carapace, far exceeding distal end of lobe and reaching level of distal was illustrated by Bruce (1989: Fig. 3A) in his original end of exopod; endopod slightly shorter than exopod, ovate, description of Periclimenaeus storchi. A more or less 2.2 times longer than broad. pronounced anteroventral angle is known from some other Periclimenaeus species, e.g., P. ascidiarum Holthuis, 1951, Color. – Specimen preserved, no traces on color. as well as some other American species (Holthuis, 1951), and P. gorgonidarum, P. garthi Bruce, 1974a, P. serrula Host. – The specimen was collected during an examination Bruce & Coombes, 1995, or P. stylirostris Bruce, 1969, of coral rubble. No host animal was recorded. All species of among Indo-West Pacifi c congeners (Miyake & Fujino, Periclimenaeus, if their host is reported, live in association 1967; Bruce, 1972, 1974a; Bruce & Coombes,1995). This with host animals, sponges or compound ascidians. feature, however, needs confirmation in these species; basing on recently examined specimens, the pterygostomial Distribution. – Known only from the type locality, Van region of the carapace is not produced or articulated in P. Phong Bay, south of Nhatrang Bay, Vietnam (South China gorgonidarum (A.J. Bruce, pers. comm.). Sea). The carapace of the new species has a low swollen tubercle on the postorbital position which is similar, to some extent, DISCUSSION to that in another Vietnamese species, P. pachyspinosus Marin, 2007, and also in P. bidentatus Bruce, 1970, P. About 69 species of the pantropical genus Periclimenaeus nielbrucei Bruce, 2006, or P. tuamotae Bruce, 1969 (Bruce, are actually known, with 12 Atlantic species and the 1969, 1970, 2006; Marin, 2007). In these, however, the remaining majority of species distributed through the Indo- tubercles are more distinct, subacute, not broadly swollen. West Pacifi c and Western American areas. Periclimenaeus More feebly developed, obtusely rounded, supraorbital nufu, new species, is easily distinguishable from all other areas are described or fi gured in several other species, e.g., species of the genus by the unique shape of the broadly ovate P. leptodactylus Fujino & Miyake, 1968, P. rastrifer Bruce, uropodal exopod with a serrate distolateral lobe outside of a 1980, P. spinimanus Bruce, 1969, P. tchesunovi Duriš,ˇ 1990, single movable spine. A serrate lateral margin of uropodal P. tridentatus Bruce, 2002, or P. zarenkovi Duriš,ˇ 1990 exopod is known only in P. gorgonidarum (Balss, 1913) (Fujino & Miyake, 1968; Bruce, 1969, 1980, 2002; Duriš,ˇ

460 THE RAFFLES BULLETIN OF ZOOLOGY 2009

1990). The present new species differs from all these by the shape of the uropodal exopods noted above, and also by Periclimenaeus ardeae has 8-9 dorsal teeth on the laterally combination of characters on the fi rst and second chelae, and lanceolate rostrum, hooked tips of the fi rst pereiopod fi ngers, of the ventral armament of the ambulatory dactyli. and the chelae of the second pereiopods covered with long slender spinules on dorsomedial aspects (Bruce, 1970). The Periclimenaeus nufu, new species, belongs to the P. rostrum and fi rst pereiopod chelae of P. nufu, new species, robustus-group of species that now includes at least nine are different from those of the former species, but the second other species: P. ardeae Bruce, 1970, P. djiboutensis, P. pereiopod chelae are similarly covered by tubercles which gorgonidarum, P. lobiferus, Bruce 1978a, P. orontes, Bruce are soft and papillose in the new species. Spinulose chelae 1986, P. palauensis Miyake & Fujino, 1968, P. spinimanus, are widely reported in many Periclimenaeus species from P. robustus Borradaile, 1915, and P. uropodialis Barnard, all main tropical marine areas. Together with P. ardeae 1958 (Barnard, 1958; Bruce, 2005). These species have an and P. nufu, new species, that character is also present in abdomen with a semicircular anteromedian dorsal lobe on all known species of the P. robustus group (Bruce, 1974b, the fi rst abdominal tergite, usually fi tting beneath the fl at, 1978a,b, 1986, 2005), excluding P. palauensis (Miyake & shallow posteromedian depression dorsally on the carapace. Fujino, 1968). Dense spinulation of the upper surfaces of A key for distinguishing these species was provided by the second pereiopod chelae, with long slender spines, are Bruce (2005). especially developed in P. spinimanus (Bruce, 1969, 2005). We have also observed distinct subquadrate tubercles in Together with the unique uropodal exopod, the present an undescribed sponge-dwelling species from Caribbean new species also differs by a produced distodorsal lobe on waters ( Durišˇ et al., manuscript), not of P. robustus group. the fi rst pereiopod coxa, and an articulated anteroventral For scanning electron microscopy, we prepared a single angle of the carapace. Within this species group, a chela of another Caribbean species, possibly P. brucei produced anteroventral angle of the carapace is present Cardoso & Young, 2007. Curiously, the chela lost these in P. djiboutensis (Bruce, 1970, 1974b). That species has spinules, leaving only minute oval membranous fi elds at a distinct dorsolateral lobe on the antennal basicerite - a their positions after drying procedures. The function of these unique character among congeners; the palm of the fi rst soft spiniform structures remain unknown; we only can pereiopod chela is elongate, about thrice longer than fi ngers, suggest on a soft molting stage of the chelae covers in the the minor second pereiopod dactyl is distally bidentate, and described cases. The host remains unknown in P. lobiferus, the dorsal telson spines are all situated on the proximal fi fth P. nufu, new species, P. palauensis and P. spinimanus; all of the telson (Bruce, 1986). The fi rst pereiopod fi nger: palm other species of this group are sponge associates (Bruce, lengths ratio, similar to those of P. djiboutensis, is also 1970, 1981, 1986; Marin, 2007). close to that in P. spinimanus. Both the former species are generally quite similar; the latter species, however, differs In P. palauensis the palm and dactyl of the fi rst pereiopod in the normal shape of the antennal basicerite and the dorsal are compressed and expanded basally (Bruce, 1970, 2005), telson armament, and in the dense spinulation of the second characters not found in P. nufu, new species. The second pereiopod chelae (see below). pereiopod chelae are smooth in P. palauensis. The dorsal rostral armament of the latter species is similar to those Periclimenaeus lobiferus has a longer rostrum reaching of P. ardeae, P. djiboutensis, P. lobiferus, P. orontes and almost to the end of the antennular peduncle, and with nine, P. robustus, bearing 5-9 slender and well erected teeth on mostly long, slender and erect dorsal teeth. The mandibular the laterally lanceolate rostrum. Within the P. robustus incisor process is reduced (Bruce, 1978a). The new species group, P. nufu, new species, occupies an isolated position possess a short rostrum not overreaching the basal segment in possessing a rather styliform rostrum with 4 depressed of the antennular article, fi ve dorsal teeth, the incisor process dorsal teeth. is well developed, dentate distally. Periclimenaeus lobiferus is the only representative of the robustus group with a In most species of the group discussed, the dactyl of the denticulate ventral margin of the ambulatory dactyli that it minor second pereiopod is semicircular (unknown in P. shares with the present new species. The dactyli are long and palauensis), not elongate as in P. lobiferus and P. nufu, slender, however, with ungui subequal to the corpus, and new species. In P. orontes, and to some extent also in with an indistinct distoventral tooth, in P. nufu, new species. P. stylirostris, the dactyl has a distodorsal edge which is Periclimenaeus ardeae, a sponge associated shrimp, and P. produced into a sharp carina (Bruce, 1986, 2005; Bruce & palauensis, whose host remains unknown, bear a unique Coombes, 1995). The accessory tooth of the ambulatory (among pontoniines) tuft of long setae dorsally on the fi rst dactyli is minute in both P. orontes and P. nufu, new species, pereiopod dactyli (Miyake & Fujino, 1968; Bruce, 1970, but the dactyli are more robust and not spinulate ventrally 1978a). Periclimenaeus ardeae is similar to P. robustus and in P. orontes. Both pairs of dorsal telson spines are situated may prove to be synonymous with the latter (Bruce, 2005). on the anterior third of the telson in the latter species, a Nothing is still known about a host animal, or about the character shared only with P. djiboutensis. presence or absence of the tuft of setae in P. robustus. Well developed tufts, rather dorsolateral, are also present on the The Periclimenaeus robustus group now consists, together fi rst pereiopod fi ngers in P. djiboutensis and P. spinimanus with the present new species, of ten species. It is possible (Bruce, 1974b, 1978b). that some other previously-described Periclimenaeus species

461 Durišˇ et al.: Periclimenaeus nufu, new species from Vietnam will be added to this group after future revisions, since that 5 Basicerite with well developed dorsolateral lobe; anteroventral character may have been overlooked or uncommented angle of carapace produced; fi rst pereiopod fi ngers about 1/3 (Bruce, 1986). The actual species group, fi rst mentioned of palm length; RF 7-9/0 ...... P. djiboutensis Bruce, 1970 by Bruce (1986) but formally named by that author later [western Indian Ocean, Great Barrier Reef] – Basicerite without developed dorsolateral lobe; anterovenral (Bruce, 2005), is a rather heterogeneous assemblage of angle of carapace not produced; first pereiopod fingers small species with an irregular distribution of the main subequal to palm length; RF 6/0 ...... diagnostic characters for each species, but sharing only ...... P. orontes Bruce, 1986 [northern Australia] a single unique character – the anteromedian lobe on 6 Third and fourth pereiopods dactyls with corpus ventrally the fi rst abdominal tergite. The group is not regarded as denticulate; RF 9/0 ...... necessarily monophyletic, but rather more as a useful ...... P. lobiferus Bruce [western Indian Ocean] basket for sorting species (A.J. Bruce – pers. comm.). – Third and fourth pereiopods dactyls with corpus ventrally Molecular analyses would yield needed insight into the entire ...... 7 phylogenic relations within this group. However, all species 7 Second pereiopod chelae smooth, not spinulate or tuberculate; RF 7/0 ...... P. palauensis Miyake & Fujino [Philippine Sea] mentioned above are rare, and, except for P. ardeae, P. – Second pereiopod chelae spinulate or tuberculate ...... 8 djiboutensis, P. gorgonidarum and P. robustus, are known 8 Dorsal surfaces of second pereiopod chelae densely covered only from their unique type specimens. This constrains the with long slender spinules, including dorsal margin of possibilities of proceeding with adequate methods. The true dactylus; RF 9/1 ...... systematic relation of P. robustus to other congeners is also ...... P. spinimanus Bruce [western Indian Ocean] highly important since it is the type species of the genus – Dorsal surfaces of second pereiopod chelae with small short Periclimenaeus Borradaile (Bruce, 2005). acute tubercles ...... 9 9 Rostral midrib slender, lanceolate, dorsal carina shallow, tip Nine species of the genus Periclimenaeus are now known slenderly acute, ventral margin smoothly convex, RF 8-9/0 ...... P. ardeae Bruce [Great Barrier Reef] from the South China Sea (Bruce, 1979; Li et al., 2004). – Rostrum midrib robust, deep, tip broadly acute, ventral margin All of them, i.e., P. arabicus (Calman, 1939), P. djiboutensis straight, RF. 9/0 ...... Bruce, 1970, P. hecate (Nobili, 1904), P. pachyspinosus, P...... P. robustus Borradaile [western Indian Ocean] rastrifer Bruce, 1980, P. rhodope (Nobili, 1904), P. storchi Bruce, 1969, P. stylirostris Bruce, 1969, and P. tridentatus (Miers, 1884), are also reported from Vietnamese waters ACKNOWLEDGMENTS (Bruce, 1993; Marin, 2007; Marin & Savinkin, 2007). The present new species increases the number of Vietnamese This study was supported by the Vietnam-Norwegian Periclimenaeus species to ten. research project funded by the Norwegian Program for Development, Research and Education (NUFU). The Czech authors are very grateful to the management of the Institute KEY TO THE KNOWN INDO WEST-PACIFIC of Oceanography, Vietnamese Academy of Sciences SPECIES OF THE PERICLIMENAEUS and Technology, Nhatrang, for kindly providing us with ROBUSTUS GROUP facilities and material for our studies, especially to Mr. (after Bruce, 2005, modifi ed): Nguyen Van Long, the Vietnamese project manager, for ensuring our access to interesting NUFU specimens. The 1 Lateral margin of uropodal exopods serrate on distal half .... authors are also indebted to Dr. A.J. Bruce (Queensland ...... 2 Museum, South Brisbane), and to anonymous reviewers, for – Lateral margin of uropodal exopods entire ...... 4 2 Swollen supraorbital tubercles present, not spines; ventral reading the manuscript and valuable comments, and Mr. D. margin of 3rd and 4th pereiopod propodus feebly spinulate Hardekopf (Charles University, Prague) for fi nal language (not more than six spines including terminal pair); distolateral corrections. The study was partly supported by the Czech angle of uropodal exopod terminating with serrate lobe and a National Committee for cooperation with IOC UNESCO single spine on diaeresis; RF 4/0 ...... (DURIŠ),ˇ by the Moravian-Silesian Government from the P. nufu D ˇ uriš, Horká & Hoc, new species [South China Sea] program “Mobility of students and young researchers”, – Supraorbital spines present; ventral margin of 3rd and 4th projects VAV4/06 and VAV11/07 (IH), and by the NUFU pereiopod propodus heavily spinulate (about 12-20 spinules); project Marine Biodiversity within the framework of the distolateral angle of uropodal exopod with about 4 spines .... project “Aquaculture and Coastal Management in Vietnam: ...... 3 3 Dorsal telson spines all distinctly on anterior half of telson; Modeling – Biodiversity – Fish health”, 2003-2007 ambulatory dactyls with corpus and unguis ventrally entire; (DTH). RF 1+6/1 ...... P. gorgonidarum (Balss, 1913) [East Africa, Seychelles, Japan, Australia] – Posterior pair of dorsal telson spines distinctly on posterior half LITERATURE CITED of telson; ambulatory dactyls with corpus and unguis ventrally serrate; RF 1+6/3 ...... Balss, H., 1913. Diagnosen neuer ostasiatischer Macruren...... P. uropodialis Barnard, 1958 [western Indian Ocean] Zologischer Anzeiger, 42: 234–239. 4 Dorsal telson spines all distinctly on anterior half of telson .. Barnard, K. H., 1958. Further additions to the crustacean fauna-list ...... 5 of Portuguese East Africa. Memórias do Museu Dr. Álvaro de – Dorsal telson spines distinctly not all on anterior half of telson, Castro, 4: 3–23. second pair at about midlength of telson ...... 6

462 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Borradaile, L. A., 1915. Notes on Carides. Annals and Magazine Borradaile, 1915 (Crustacea: Decapoda: Pontoniinae). Cahiers of Natural History, series 8, 15: 205–213. de Biologie Marine, 46: 389–398. Bruce, A. J., 1969. Preliminary descriptions of ten new species Bruce, A.J., 2006. Periclimenaeus nielbrucei sp. nov. (Crustacea: of the genus Periclimenaeus Borradaile, 1915 (Crustacea, Decapoda: Pontoniinae), a new sponge associate from Decapoda, Natantia, Pontoniinae). Zoologische Mededelingen, the Capricorn Islands, Queensland, with notes on related Leiden, 44: 159–176. Periclimenaeus species. Zootaxa, 1224: 1–22. Bruce, A. J., 1970. Further preliminary descriptions of new species Bruce, A. J., 2008. Palaemonoid shrimps from the Australian North of the genus Periclimenaeus Borradaile, 1915 (Crustacea, West Shelf. Zootaxa, 1815: 1–24. Decapoda, Natantia, Pontoniinae). Zoologische Mededelingen, Bruce, A. J., 2009. Notes on some Indo-Pacific Pontoniinae, Leiden, 44: 305–315. XLVII. Re-evaluation of the genera Apopontonia Bruce, 1976, Bruce, A. J., 1972. A report on a small collection of pontoniid Paraclimenaeus Bruce, 1988 and Climeniperaeus Bruce, 1996. shrimps from Fiji, with the description of a new species Crustaceana, 82: 493–504. of Coralliocaris Stimpson (Crustacea, Decapoda, Natantia, Bruce, A. J. & K. E. Coombes, 1995. The palaemonoid shrimp Pontoniinae). Pacifi c Science, 26: 63–86. fauna (Crustacea: Decapoda: Caridea) of the Cobourg Bruce, A. J., 1974a. A report on a small collection of pontoniine Peninsula, Northern Territory. The Beagle, Records of the shrimps from the northern Indian Ocean. Journal of the Marine Museums and Art Galleries of the Northern Territory, 12: biological Association of India, 16: 437–454. 101–144. Bruce, A. J., 1974b. Observations upon some specimens of Calman, W. T., 1939. Crustacea: Caridea. Scientifi c Report of the the genus Periclimenaeus Borradaile (Decapoda Natantia, John Murray Expedition, 6 (4): 183–224. Pontoniinae) originally described by G. Nobili. Bulletin Cardoso, I. A. & P. S. Young, 2007. Caridea (Crustacea, Decapoda: du Muséum National d’Histoire Naturelle, Paris (3), 258: Disciadidae, Palaemonidae, Processidae, Rhynchocinetidae) 1557–1583. from Rocas Atoll including two new species of Periclimenaeus Bruce, A. J., 1976. Shrimps and prawns of coral reefs, with special Borradaile, 1915. Arquivos do Museu Nacional, Rio de reference to commensalism. In: Jones, O.A. & R. Endean (eds), Janeiro, 65: 277–337. Biology and Ecology of Coral Reefs, Vol 3. Academic Press, Duriš,ˇ Z., 1990. Two new species of the commensal shrimp genus New York. Pp. 37–94. Periclimenaeus Borradaile, 1915 (Decapoda, Palaemonidae) Bruce, A. J., 1978a. A report on a collection of pontoniine shrimps from the Maldive Islands. Journal of Natural History, 24: from Madagascar and adjacent Seas. Zoological Journal of the 615–625. Linnean Society, 62: 205–290. Duriš,ˇ Z., I. Horká & F. Sandford, submitted. Periclimenaeus Bruce, A. J., 1978b. Pontoniinid shrimps from the ninth cruise pectinidactylus n. sp. (Crustacea: Decapoda: Pontoniinae) from of R/V Anton Bruun, IIOE, 1964, II: The remaining genera. the Belizean Barrier Reef, Caribbean Sea. Zootaxa. Bulletin of Marine Science, 28: 18–136. Fujino, T. & S. Miyake, 1968. Description of two new species Bruce, A. J., 1979. Records of some pontoniine shrimps from the of pontoniid shrimps (Crustacea, Decapoda, Palaemonidae) South China Sea. Cahiers de l’Indo-Pacifi que, 1: 215–248. commensal with sponges. OHMU, 1 (3): 85–96. Bruce, A. J., 1980. On some pontoniine shrimps from Nouméa, Holthuis, L. B., 1951. A general revision of the Palaemonidae New Caledonia. Cahiers de l’Indo-Pacifi que, 2(10): 1–39. (Crustacea Decapoda Natantia) of the Americas. I. The Bruce, A. J., 1981. Pontoniine shrimps of Heron Island. Atoll subfamilies Euryrhynchinae and Pontoniinae. Allan Hancock Research Bulletin, 245: 1–33. Foundation, Occasional Paper, 11: 1–332, pls 1–63. Bruce, A. J., 1986. Three new species of commensal shrimps from Kingsley, J. S., 1878. List of the North American Crustacea Port Essington, Arnhem Land, Northern Australia (Crustacea: belonging to the sub-order Caridea. Bulletin of the Essex Decapoda: Palaemonidae). The Beagle, Occasional Papers Institute, 10: 53–71. of The Northern Territory Museum of Arts and Sciences, 3: Kubo, I., 1940. Studies on Japanese palaemonoid shrimps. II. 143–166. Pontoniinae. Journal of the Imperial Fisheries Institute, 34: Bruce, A. J., 1988. A redescription of Periclimenaeus fi mbriatus 31–75. Borradaile, 1915, with the designation of a new genus Li, X., A. J. Bruce & R. B. Manning, 2004. Some palaemonid (Crustacea: Decapoda: Palaemonidae). Zoological Journal of shrimps (Crustacea: Decapoda) from northern South China the Linnean Society, 94: 219–232. Sea, with descriptions of two new species. The Raffl es Bulletin Bruce, A. J., 1989. A report on some coral reef shrimps from the of Zoology, 52: 513–553. Philippine Islands. Asian Marine Biology, 6: 173–192. Marin, I., 2007. Pontoniine shrimps (Decapoda: Caridea: Bruce, A. J., 1993. Some coral reef pontoniine shrimps from Palaemonidae) inhabiting boring sponges (Porifera: Vietnam. Asian Marine Biology, 10: 55–75. Demospongia) from Nhatrang Bay, Vietnam, with description of three new species. Zoologische Mededelingen, Leiden, 81: Bruce, A. J., 2002. A redescription of Periclimenaeus tridentatus 217–240. (Miers, 1884), based on specimens from Port Essington, Northern Territory, and a note on P. hecate (Nobili, 1904) Marin, I. & O. Savinkin, 2007. Further records and preliminary (Crustacea: Decapoda: Pontoniinae), with a key for the list of pontoniine (Caridea: Palaemonidae: Pontoniinae) preliminary identifi cation of the tunicate-associated species and hymenocerid (Caridea: Hymenoceridae) shrimps from of Periclimenaeus Borradaile. Journal of Natural History, Nhatrang Bay. In: Britayev, T. & D. Pavlov (eds), Benthic 36: 565–584. Fauna of the Bay of Nhatrang, Southern Vietnam. IPEE, Moscow. Pp.176–208, Pls. 83–96. Bruce, A. J, 2005. A re-description of Periclimenaeus robustus Borradaile, the type species of the genus Periclimenaeus

463 Durišˇ et al.: Periclimenaeus nufu, new species from Vietnam

Miers, E. J. (1884) Crustacea. Report of the Zoological Collections Nobili, G., 1904. Diagnoses préliminaires de vingt-huit espèces made in the Indo-Pacifi c Ocean during the Voyage of H.M.S. nouvelles de Stomatopodes et Décapodes Macroures de la “Alert” 1881–2. Pp. 178–322, 513–575. Mer Rouge. Bulletin du Muséum d’Histoire naturelle, Paris, Miyake, S. & T. Fujino, 1967. On four species of Pontoniinae 10: 228–238. (Crustacea, Decapoda, Palaemonidae) found in Porifera Rafinesque, C. S., 1815. Analyse de la Nature ou Tableau de inhabiting the coast regions of Kyushu, Japan. Journal of the l’Univers et des Corps organisés. Palermo. 224 pp. Faculty of Agriculture, Kyushyu University, 14: 225–291, Pl. 3. Miyake, S. & T. Fujino, 1968. Pontoniinid shrimps from the Palau Islands (Crustacea, Decapoda, Palaemonidae). Journal of the Faculty of Agriculture, Kyushu Imperial University, 10: 339–431.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 465–473 Date of Publication: 31 Aug.2009 © National University of Singapore

A NEW SPECIES OF THALASSINA (CRUSTACEA: DECAPODA: THALASSINIDAE) FROM MALAYSIA

Moh H. H. and Chong V. C. Institute of Biological Sciences / Institute of Ocean & Earth Sciences, University of Malaya, 50603 Kuala Lumpur, Malaysia

ABSTRACT. – Thalassina kelanang, a new species of Thalassina from Malaysia is described, and compared to published descriptions and specimens of Thalassina anomala (from Malaysia), T. squamifera (from Australia) and T. gracilis (from Thailand and Malaysia). A number of morphological features of the carapace, rostrum, scaphocerite, chela, abdominal pleura and sternites, and petasma could be used to distinguish between the new species and T. anomala. Thalassina kelanang appears to be more similar to T. squamifera in general morphology, but can be distinguished from the latter by its distinctive rostrum and male copulatory organ (petasma). Thalassina kelanang has a rostrum with a characteristically deep median sulcus that extends behind the adrostral carina; the petasma has 3–4 strong proximal spines. These characters are not found in two other congeners as well.

KEY WORDS. – New species, Thalassina, mud lobsters, Malaysia.

INTRODUCTION from Australia and one from the Philippines. They further added that T. squamifera lacks the oblique tuberculate ridge The family Thalassinidae Latreille, 1831, contains the single starting near the base of the fi xed fi nger and running back on genus Thalassina Latreille, 1806, which had at one time the lateral surface of the large cheliped in T. anomala. This been considered monotypic (Glaessner, 1969), but Holthuis character was found to be most useful in separating fossil (1991) suggested that there may be more than one species. materials of the two species (Campbell & Woods, 1970). Thalassina anomala (Herbst, 1804) is the valid type species, fi rst described as Cancer (Astacus) anomalus Herbst, 1804, Thalassina emerii Bell, 1844, was fi rst described based based on a female type specimen collected from an unknown on a fossil specimen believed to be likely from the mouth locality. The species was subsequently redescribed under of the Daly River, Northern Territory, Australia, but its the following synonyms: Thalassina scorpionides Latreille, recognition in museum specimens from N.W. Australia 1806 (type locality: unknown); Thalassina scabra Leach, suggests that this species may be extant (see Davie, 2002, 1814 (type locality: unknown); Thalassina talpa White, p. 475). Another species, Thalassina chilensis Steenstrup 1847 (type locality: Philippines); Thalassina gracilis Dana, & Lütken, 1862, from the coast of Chile was believed to 1852 (type locality: Telegraph Island, near Singapore); and be distinct from T. anomala, but De Man (1928) suspected Thalassina maxima Hess, 1865 (type locality: New South that T. chilensis is likely T. gracilis Dana, 1852 which he Wales, Australia) (in Miers, 1880; De Man, 1928). thought was synonymous with T. anomala. Holthuis (1991) surmised that the type locality of T. chilensis is likely to be De Man (1928) described his specimens of T. anomala var. incorrect given that it has since never been found in Chile. squamifera (type locality: Karakelang-islands, Indonesia) Dworschak (1992) in personal communication with de Saint as quite different from the typical, widespread T. anomala, Laurent reported T. gracilis as likely a valid species. Thus in that the former had a small movable scaphocerite on far, world-wide there appears to be at least four extant its antennal peduncle while the typical anomala did not species of mud lobsters belonging to the genus Thalassina. have it. In addition, he also recognized that the shape of There is however a need to review the taxonomic status of the ridge between the second to fi fth pleopods is different all described species of thalassinid mud lobsters. Such a between the two varieties. Campbell & Woods (1970) review has been carried out by the late de Saint Laurent’s elevated T. anomala var. squamifera to species rank, hence co-worker, Dr. Ngoc-Ho of the National Museum of Natural T. squamifera De Man, 1915, after examination of the History, Paris, and has been published in a supplement of Australian specimens. Support for this assignment came this Journal after the acceptance of this paper. Ngoc-Ho & from Poore & Griffi n (1979) who examined 32 samples de Saint Laurent (2009) proposed three new species.

465 Moh & Chong: A new Thalassina from Malaysia

In Malaysia, Thalassina anomala was fi rst recorded from Percival, 26 Sep.1983; 1 male (146, 51.7 mm) (NSMAG, the states of Penang and Sarawak (in De Man, 1928), but Cr.000517), Ludmilla Creek, Darwin, N.T., Australia, the species appears quite widespread, appearing also in coll. J.R.Hanley, 12 Oct.1983; 1 male (139.6, 51.3 mm) the states of Selangor (Sasekumar, 1974) and Johor (Ng (NSMAG, Cr.001475), Ludmilla Creek, Darwin, N.T., & Kang, 1988). However, there has been no attempt to Australia, coll. D. Percival, 13 Oct. 1983; 1 female (113.0, examine closely these shy and diffi cult to catch creatures, 41.9 mm) (NSMAG, Cr.009965), near bridge Channel to see if there are more than one species. This paper Island, N.T., Australia; coll. M. Burke, 19 Feb. 1992; 1 describes two main species found in Selangor, Malaysia; female (70.3, 26.1mm) (NSMAG, Cr. 013891), Port Keats, one the typical T. anomala, and the other a new species. We N.T., Australia, coll. K. Metcalfe & party, undated. compared their morphology to specimens of T. squamifera obtained from Natural Sciences Museum & Art Gallery T. gracilis – 1 male (69.8, 25.8 mm) and 1 female (57.3, of the Northern Territory (NSMAG), Australia and T. 21.8 mm) (ZRC 2007.0512), Ranong mangroves, South gracilis from the Zoological Reference Collection (ZRC) Thailand, coll. P. Naiyanetr; 1 male (69.8, 25.5 mm) of the Raffl es Museum of Biodiversity Research, National (ZMUM), Carey Island, Kuala Langat [=District], Selangor, University of Singapore, and our collection. Our reasons Malaysia, coll. H.H.Moh, 19 Sep.2008. for a new species are as described below.

TAXONOMY MATERIAL AND METHODS Thalassina kelanang, new species Study sites. – Mud lobsters were sampled from two study (Figs. 1, 2A, 3A, 4A, 5A, 5B, 6A, 7A, 7B, 8A) sites at Kelanang Beach and Carey Island, Selangor, Malaysia. The mud lobster mounds were located inside or Material examined. – Holotype – male (150.0, 54.1 mm) (ZMUM), near to mangrove forests in the intertidal shore. The sandy- from mound in mangrove forest, Kelanang Beach, Kuala Langat, mud beach of Kelanang has a narrow (0.6 km) and degrading Selangor, Malaysia, coll. H.H. Moh, Apr.2007. fringe of mangrove forests where on the landward side a Paratypes – 1 female (141, 50.3 mm) (ZMUM), Kelanang Beach, coastal bund runs along the entire coastline. All specimens Kuala Langat, Selangor, Malaysia, coll. H.H.Moh, Oct. 2006; of the new species were sampled from Kelanang Beach. In 1 male, (140, 52.0 mm), 4 females (120, 44.6 mm), (162, 58.9 Carey Island, which is located just north of Kelanang, the mm), (167, 60.8 mm), (150, 55.4 mm), (ZMUM), Kelanang mud lobster mounds of only T. anomala are found on the Beach, Kuala Langat, Selangor, Malaysia, coll. H.H.Moh, Nov. landward side of perimeter bunds which are built around the 2006; 1 male, (114, 42.9 mm), 2 females (163, 58.4 mm), (140, entire island to protect the oil palm plantations that occupy 51.5 mm), (ZMUM), Kelanang Beach, Kuala Langat, Selangor, former mangrove forests from seawater intrusion. Malaysia, coll. H.H.Moh, Mac. 2007; 2 males (143, 51.9 mm), (133, 48.8 mm), 2 females (120, 43.7 mm), (119, 45.4 mm), Sampling. – Mud lobsters were trapped by using a 50 cm (ZMUM), Kelanang Beach, Kuala Langat, Selangor, Malaysia, coll. H.H.Moh, Apr. 2007; 1 female (161, 59.1 mm), (ZMUM), –long wire with a tethered piece of fi sh netting (1.5” or 2.5” Carey Island, Kuala Langat, Selangor, Malaysia, coll. H.H.Moh, mesh size) on one end and a T-handle at the opposite end. Oct. 2006; 1 male (183, 63.6 mm), (ZMUM), Carey Island, Kuala The wire was inserted into the burrow with the T-handle Langat, Selangor, Malaysia, coll. H.H.Moh, Nov. 2006. resting on top of the mound. The traps were laid during dusk and recovered after 15–18 hours. Trapped animals Description of holotype. – Carapace elongate oval in dorsal were entangled in the gill netting as they crawled up from aspect; sculptured by circular depressions or punctae, the the muddy bottom. The animals were also caught by digging largest pair (gastric pits) associated with post-cervical below their mounds using a spade. All specimens were groove; upper lateral sides heavily covered with short identifi ed and measured using a pair of digimatic calipers, anteriorly-directed spines; short posteriorly-directed spine with a precision of 0.01mm. Measurements provided are on dorsal median margin not reaching fi rst abdominal tergite of the total length (measured along the midline from tip of (Fig. 2A). Rostrum fl at, narrowly triangular and waisted rostrum to tip of telson) and the carapace length (measured along the midline from the tip of the rostrum to the posterior edge of the carapace). Identifi ed specimens are deposited in the Zoological Museum, University Malaya (ZMUM). Two specimens of the new species (male and female) are also deposited in ZRC, Singapore, and NSMAG, Australia.

Comparative material examined. – Thalassina anomala – 13 males and 5 females (TL; 114.6–241.1 mm) (ZMUM), Carey Island, Selangor, Malaysia, coll. H.H.Moh, Jun.– Sep.2006.

T. squamifera – 1 male (1325, 47.8 mm) (NSMAG, Fig. 1. Thalassina kelanang, new species, holotype-male, TL = 150 mm, Cr.004775), Micket Creek, Darwin, N.T., Australia, coll. D. CL = 54.1 mm (ZMUM).

466 THE RAFFLES BULLETIN OF ZOOLOGY 2009 near base (Fig. 3A), with lateral margins that continue rows, ventral surface with two serrated ridges. Dactyli posteriorly as short divergent ridges (adrostral carina) twice as long as fi xed fi nger, narrow and laterally fl attened, extending half length of gastro-orbital carina; median sulcus right dorsal margin armed with row of 13–15 spines and or groove deep, extending beyond adrostral carina; 3–11 numerous long fi ne setae, ventral surface with two serrated blunt marginal spinules or tubercles on adrostral carina. ridges and two rows of fi ne setae, a few punctae present Supra-orbital, antennal and branchiostegal spines strong along dorsal surface. and sharp; orbital and sub-orbital spines short; 4–8 sharp spines at curved anterior end of branchiocardiac groove. Pereopod 2 subchelate, smaller than pereopod 1; basi- Oblique groove with 10–14 spines on dorsal margin, ischium laterally flattened with ventral margin armed anterior-most spine largest, thinly setose. Anterior margin of with 6–9 strong spines and a row of setae; merus laterally antennal region armed with series of short spines. Numerous fl attened, dorsal margin with row of 4–6 strong decurved tubercles on anterior margin of branchiostegite. spines, ventral surface densely setose; carpus setose on dorsal and ventral margins, dorsal margin with 2–3 strong, Antenna with highly reduced antennal scale or scaphocerite decurved spines; propodal length slightly longer than width, on the outer side, scaphocerite large, setose on inner margin dorsal margin of fi xed fi nger armed with a longitudinal row (Fig. 4A). Antennal fl agellum when stretched backward of blunt teeth; dactylus with two rows of setae on dorsal reached fi rst or second abdominal somite, length more than margin, outer surface with medial longitudinal row of setae, fi ve times length of antennular fl agellum. ventral margin serrated with row of blunt teeth, postero- ventral margin setose. Pereopods 1 (chelipeds) asymmetrical and subchelate, left chela larger than right (but see Paratypes below). Meri Pereopod 3 narrow and fl attened laterally; coxa armed with large, fl attened laterally on dorsal surface, but broad or 4–6 spines on inner surface; ischium armed with 4–6 spines triangular on ventral surface; right merus with 17 dorsal on ventral margin; merus with row of 6–10 decurved spines spines, left with 18 dorsal spines, anterior-most 4 spines on dorsal margin, ventral margin serrated with two rows large and decurved, inner and outer ventral margins serrulate of 10–12 spines; carpus armed with 4–5 strong spines on with numerous subequal denticles on ventral surface. Carpi dorsal margin, ventral margin spineless; propodus small relatively small, inner dorsal margin with a row of 7–8 strong and laterally compressed, with setae on dorsal and ventral spines, outer ventral margin armed with a row of spines, surfaces; dactylus slender as long as propodus, ventral anterior-most being most prominent. Propodi granulated on margin with row of setae, dorsal margin with seven short entire surface, granules on the posterior half of inner ventral spines and row of setae. surface comparatively larger than those on anterior half, dorsal surface with two ridges: inner ridge armed with row Pereopod 4 similar but slightly smaller than pereopod 3; of 10 strong spines (Fig. 5A, 5B), outer ridge on proximal dactylus slender, longer than propodus. three-quarters distance, armed with row of small tubercles, outer surface with long fi ne setae occurring in tufts along Pereopod 5 smaller than pereopod 4, not compressed; coxae with gonopores facing each other on either side of mid- ventral line; outer margin armed with a row of spines.

Male abdomen elongate and narrow; somite width as wide as length; fi rst abdominal somite smallest and narrowest; third and fourth somites largest. Dorsal tergite of first abdominal somite raised as a distinct rectangular piece, with inverted Y groove (Fig. 6A).

Base of pleuron of second and third abdominal somites, each with two longitudinal, serrated ribs or carinae occupying anterior three-quarters distance to posterior end of segment (Fig. 7A). Abdominal sternite of second to fi fth somites with distinct bicuspid sternal ridge between opposite pleopods; each cusp bearing 3–6 teeth (Fig. 7B).

Mature male pleopod 1 uniramus, with opposing endopods modifi ed and united to form petasma or intromittent organ; distal end of petasma narrowly oval to pointed, setal row on outer and inner margins reaching or almost reaching tip; inner distal setae modifi ed to form fi ne interlocking hooks on disc-like, subterminal keel of petasma; outer proximal end of petasma armed with 3–4 strong spines (Fig. 8A). Pleopods 2–5 biramous; pleopods 3–5 of equal size, but Fig. 2. Dorsal view of carapace. A, Thalassina kelanang (holotype, 150.0, 54.1 mm); B, T. anomala-Male (151.4, 51.1 mm). Scale bar = 10 mm. shorter than pleopod 2. Uropods styliform.

467 Moh & Chong: A new Thalassina from Malaysia

Telson broadly triangular, about as long as previous the former type and 11 of the latter type. Merus of right somite. cheliped with 12–17 dorsal spines, left 15–18, anterior 3–5 spines large and decurved. In female, gonopores on inner Variation. – Although our holotype male has a larger right ventral surface of coxa of pereopod 3; pleopod 1 uniramus; cheliped than the left, the left cheliped can be larger than the pleopods 2–5 larger and biramous, bearing long setae which right for both male and female, but in some of our specimens are particularly well-developed for carrying eggs during the difference was not obvious. Our specimens had 14 of breeding season.

Fig. 3. Dorsal view of anterior region of cephalothorax. A, T. kelanang (holotype, 150.0, 54.1 mm); B, T. anomala-Male (151.4, 51.1 mm); C, T. squamifera- Male (132.5, 47.8 mm); D, T. gracilis-Male (69.8, 25.8 mm). Scale bar = 5 mm.

468 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 4. Dorsal view of right antennal peduncle showing movable scaphocerite. A, T. kelanang (holotype, 150.0, 54.1 mm); B, T. anomala, (absent)-Male (151.4, 51.1 mm); C, T. squamifera-Male (132.5, 47.8 mm). Scale bars: a–b = 20 mm; c = 10 mm.

Fig. 5. Right chela of pereopod 1. A–B, outer and inner aspects, T. kelanang (holotype, 150.0, 54.1 mm); C–D, outer and inner aspects, T. anomala-Male (151.4, 51.1 mm). Scale bar = 10 mm.

469 Moh & Chong: A new Thalassina from Malaysia

Etymology. – The species is named after its type locality, Kelanang Beach, while the animal inhabits the fringing Kelanang, in the district of Kuala Langat of the state of Rhizophora forest, there were more mounds on open sandy Selangor, Malaysia. The name is used as a noun. mud substrate without vegetation. In contrast, T. anomala were found in muddy substrate particularly in Carey Island, Colour. – Carapace orange to brown on dorsal aspect, although few T. kelanang were found on the island. Thus, becoming grey ventrolaterally. Abdomen red to orange the two species appear to occupy their own microhabitats in on dorsal aspect, pleura grey. Dorsal aspect of pereopods the same general area. Male T. kelanang, unlike T. anomala, brownish orange, ventral aspect grey. are very aggressive infl icting painful pinches on handlers; males often ended up with broken legs if placed together Biological notes. – Thalassina kelanang construct sandy in an aquarium. mud mounds of generally less than 0.5 m in height. At

Fig. 6. Dorsal view of fi rst abdominal somite. A, T. kelanang (holotype, 150.0, 54.1 mm); B, T. anomala-Male (151.4, 51.1 mm). Scale bar = 10 mm.

Fig. 7. Second abdominal somite. A–B, dorsal and ventral aspects, T. kelanang (holotype, 150.0, 54.1 mm); C–D, dorsal and ventral aspects, T. anomala- Male (151.4, 51.1 mm). Scale bar = 10 mm.

470 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Remarks. – Thalassina kelanang shows similarities with the anomala specimens in India, except for one female, sympatric species, T. anomala in terms of size, coloration generally did not have the scaphocerite. From a total of 65 and general morphology. However, their morphological specimens of T. anomala examined in this study, 29 of them differences warrant the separation of the two species. In have much reduced scaphocerites, while 36 specimens do all our 65 T. anomala specimens, the posterior median not have scaphocerites (Fig. 4B). In contrast, all specimens spine of the carapace, often decurved, always overhangs of T. kelanang have distinctly large, triangular scaphocerites the articulation with the fi rst abdominal tergite (Fig. 2B). with a row of long setae on their inner margin (see Fig. 4A). In contrast, the median spine of T. kelanang is short, blunt The fi ve specimens of T. squamifera also have scaphocerites and never overhangs the fi rst abdominal tergite. However, but only one specimen has a row of marginal setae on the this character is similar to that of Thalassina squamifera De right scaphocerite (Fig. 4C). Thalassina kelanang has a long Man. The oblique groove of the carapace of T. anomala is antennal fl agellum that when stretched backwards reached covered with a thick row of setae, whereas in T. kelanang more than half the length of the fi rst abdominal somite; the and T. squamifera it is sparsely covered by setae. The fl agellum of T. anomala is much shorter, reaching less than rostrum of Thalassina kelanang has an acute tip, proximal three quarters of the carapace length. While the examined waist and a deep median sulcus (groove) that extends up males of T. squamifera all had broken antennae, both to the posterior pair of dorsal punctae behind the posterior females bore antennal fl agella that reached the posterior end of the adrostrals; the latter reaches only the anterior margins of the carapace. half of the gastro-orbital carina (see Fig. 3A). In contrast, both T. anomala and T. squamifera have a triangular The merus of the cheliped in T. kelanang has a row of 3–5 rostrum with a shallow median sulcus that does not reach strong spines on its dorsal margin, whereas in T. anomala beyond the adrostrals; the latter extends to three-quarters there are only two strong spines. There are also two or three or full length of the gastro-orbital carina (Fig. 3B, 3C). In strong spines in T. squamifera. Three other distinguishing addition, both species have rather smooth or at the most features of T. kelanang are (i) the fi xed fi nger of its chela is three tubercles on their adrostral and gastro-orbital carinae, half the length of the movable fi nger, whereas in T. anomala posterior to the orbital margin. These features of the rostrum the fi xed fi nger is a quarter to a third the length of the appear to be important in separating the different species movable fi nger (Fig. 5C, D), (ii) 8–12 strong dorsal spines of Thalassina. In fact, the examined T. gracilis specimens on the inner dorsal ridge of the palm, whereas T. anomala show a distinctive depressed and more acute rostrum unlike has 14–20 blunt spines or tubercles, and (iii) lateral dorsal that of T. kelanang and others (Fig. 3D). ridge of outer surface of palm extends to three-quarters distance but not to distal end, whereas in T. anomala, the De Man (1928) pointed out the differences between T. ridge extends right up to the distal end (Fig. 5C). The same anomala and T. squamifera (as a variety of T. anomala), characters for T. squamifera are respectively fi xed fi nger in that only the latter has a scaphocerite on the antennal half the length of movable fi nger, 9–11 inner dorsal spines peduncle as well as a tuberculate ridge on the abdominal and a lateral dorsal ridge that extends between half to three sternites (see below). Sankolli (1970) reported that T. quarters of distance to distal end.

Fig. 8. Ventral view of petasma. A, T. kelanang (holotype, 150.0, 54.1 mm); B, T. anomala-Male (193, 61.4 mm); C, T. squamifera-Male (132.5, 47.8 mm); D, T. gracilis-Male (69.8, 25.8 mm). Scale bar = 5 mm.

471 Moh & Chong: A new Thalassina from Malaysia

Table 1: Comparative morphology of Thalassina anomala, T. squamifera and T. kelanang (new species).

T. anomala (Herbst, 1804) T. squamifera De Man, 1915 T. kelanang, new species

Dorsal median margin of carapace Dorsal median margin of carapace Similar to T. squamifera projected as long, hooked spine resting on projected as short spine not resting on the fi rst abdominal tergite. fi rst abdominal tergite. Rostrum triangular. Adrostral carina of Generally similar to T. anomala except Rostrum waisted. Adrostral carina extending carapace extending three quarters or entire rostrum more acute. to about half the distance of gastro-orbital distance of gastro-orbital carina, both carina, both carinae with 3–11 blunt carinae smooth or bearing maximum of tuber cles postorbitally. Median sulcus of three blunt tubercles postorbitally. rostrum deep, extending behind adrostrals. Median sulcus of rostrum shallow, not extending to behind adrostrals. Scaphocerite absent or if present, very Scaphocerite present, with or without Scaphocerite distinctly large, with marginal small. marginal setae. row of long setae. Oblique tuberculate ridge present on inner Oblique tuberculate ridge on fi rst cheliped Oblique tuberculate ridge on fi rst cheliped surface of fi rst cheliped propodus, starting propodus absent. propodus absent. near the base of the fi xed fi nger and running posteriorly. Pereopod 1 with a row of 13–20 blunt Pereopod 1 with a row of 9–11 blunt Pereopod 1 with a row of 8–12 strong spines or tubercles on the inner propodal spines or tubercles on the inner propodal dorsal spines on the inner propodal ridge. ridge. Lateral dorsal ridge extends the ridge. Lateral dorsal ridge extends to Lateral dorsal ridge extends to three quarters entire length of propodus. more than half but never three quarters or more of the propodal length. of the propodal length. Merus of pereopod 1 with 2 strong dorsal Merus of pereopod 1 with 2–3 large dorsal Merus of pereopod 1 with 3–5 large dorsal spines. spines. spines. Tergite of fi rst abdominal somite has two Tergite of fi rst abdominal somite raised up Similar to T. squamifera. petaloid depressions in the form of an as a distinct rectangular piece, with inverted inverted V. Y groove. Pleura of second to sixth abdominal Pleura of second and third abdominal Similar to T. squamifera somites with single longitudinal carina somites with two longitudinal, serrated occupying entire length of somite. carinae occupying anterior three quarters of somite length. Abdominal sternites of second to fi fth Abdominal sternites of second to fi fth Abdominal sternites of second to fi fth somites with only one median tubercle. somites with distinct bicuspid sternal ridge, somites with distinct bicuspid sternal ridge, each cusp bearing 3–5 teeth for male while each cusp bearing 3–6 teeth in both male adult female without any. and female. Petasma without proximal spines, tip Petasma without proximal spines; outer Petasma with 3–4 strong proximal spines broadly rounded without setae. and inner marginal setal rows extending on outer margins; outer and inner marginal almost to pointed tip. “Neck” behind keel setal rows extending to pointed tip. “Neck” broad, width half the length of inner keel behind keel slender, width one quarter the surface. length of inner keel surface.

Several distinctive differences between the three species distinguishing the two varieties of mud lobster (sensu de are also observed in the abdomen and its appendages. Man, 1928). Thalassina kelanang and T. squamifera have an inverted Y-groove on the dorsal tergite of the first abdominal Male holotype and paratypes of T. kelanang (see Fig. 8A) somite (see Fig. 6A), whereas T. anomala has two petaloid have a petasma or intromittent organ that is quite different depressions in the form of an inverted V (Fig. 6B). In T. from that of T. anomala in that both outer and inner marginal kelanang and T. squamifera, the longitudinal ‘three-quarters setal rows of T. kelanang are reaching its distal tip, whereas long’ carina runs across the base of the pleuron of the second the latter’s petasmal tip is broadly rounded without setae and third abdominal somites only, whereas in T. anomala (Fig. 8B). In T. squamifera, inner marginal setae but no the carina runs the entire somite length and is present on terminal setae are present on the petasmal tip (Fig. 8C). the second to sixth abdominal somites (Fig. 7C). A sternal Another important difference between the petasma of the ridge (second to fi fth somites) bearing two cusps each with three species is the presence of 3–4 proximal spines in T. 3–6 teeth/ tubercles is present in T. kelanang as well as in kelanang but which are absent in both T. anomala and T. T. squamifera, whereas in T. anomala, only one median squamifera. All our nine male specimens of T. kelanang tubercle is present (Fig. 7D). This is the other feature have these proximal spines. The petasma of T. squamifera is

472 THE RAFFLES BULLETIN OF ZOOLOGY 2009 stout compared to that of its congeners. We also examined Herbst, J. F. W., 1804. Versuch einer Naturgeschichte der Krabben the petasma of T. gracilis and this is distinctly different und Krebse nebst einer systematischen Beschreibung ihrer from the rest and also without proximal spines (Fig. 8D). verschiedenen Arten, 3(4): 1–49, pls. 59–62. Gotttlieb August Therefore, despite the close similarities between T. kelanang Lange, Berlin & Stralsund. and T. squamifera (Table 1), based on mainly differences Hess, W., 1865. BeitrSge zur Kenntnis der Decapoden-Krebse Ost- of their petasma and the rostrum, we conclude that they are Australiens. Archiv fi ir Naturgeschichte, 31: 127–173. two different species. Holthuis, L. B., 1991. FAO Species Catalogue, Vol. 13: Marine Lobsters of the World: An Annotated and Illustrated Catalogue The new species of T. kelanang is more similar to T. of Species of Interest to Fisheries Known To Date. FAO squamifera than to T. anomala in general morphology, Fisheries Synopsis, 125: 1–292. but can be distinguished from T. squamifera based on Latreille, P. A., 1806. Genera Crustaceorum et Insectorum the morphology of the petasma and rostrum. Thus, the secundum ordinem naturalem in familias disposita, iconibus characteristics of both rostrum and petasma are very useful exeplisque plurimis explicata. A. Koenig, Paris & Argentorati. in distinguishing the species of Thalassina. Pp. i–xviii + 302 p. Latreille, P. A., 1831. Cours d’entomologie ou de I’histoire naturelle des Crustaces, des Arachnides, des Myriopodes et ACKNOWLEDGEMENTS des Insectes. Exposition methodique des ordres, des families et des genres des trois premieres classes. A I’usage des eleves de I’ecole du Museum d’Histoire naturelle, Paris. Pp. i–xiii, We wish to thank Golden Hope Plantations (now Sime 1–568, Atlas: pls. 1–26. Darby Plantation Private Limited) for providing a research grant and field assistance, to support this study which Leach, W. E., 1814. Crustaceology. In Brewster, D. (ed.), The Edinburgh Encyclopaedia, Blackwood: Edinburgh, 7(2): forms part of a PhD thesis presently undertaken by the 383–437. first author. We thank the University of Malaya for providing research facilities. We are very grateful to the Man, J. G. de, 1915. Zur Fauna von Nord-Neuguinea. Nach den Sammlungen von Dr. P. N. van Kampen und K. Gjellerup in Natural Sciences, Museum and Art Gallery of the Northern den Jahren 1910–1911. Macrura. Zoologisches Jahrbücher Territory, Australia and Raffles Museum of Biological Abtheilung für Systematik, Jena, 38: 385–458, Pls. 27–29. Research, National University of Singapore, for loan of Man, J. G. de, 1928. The Decapoda of the Siboga-Expedition. their specimens. Part 7. The Thalassinidae and Callianassidae collected by the Siboga-Expedition with some remarks on the Laomediidae. Siboga Expéditie Monographie 39a: 1–187. LITERATURE CITED Miers, E. J., 1880. On a collection of Crustacea from the Malaysian region.—Part III. Crustacea Anomura and Macrura (except Bell, T., 1844. On the Thalasina Emerii, a fossil crustacean, Penaeidea). Annals and Magazine of Natural History (ser. 5), forwarded by Mr. W. S. MacLeay, from New Holland. 3: 370–384. Proceedings of the Geological Society of London, 4: 360– 362. Ng, P. K. L. & N. Kang, 1988. Thalassina: the mud lobster. Nature Malaysiana, 13 (4): 28–31. Campbell, B. M. & J. T. Woods, 1970. Quaternary crustaceans from northern Australia in the collections of the Bureau Ngoc-Ho, N. & M. de Saint Laurent, 2009. The genus Thalassina of Mineral Resources, Canberra. Bulletin of the Bureau of Latreille, 1806 (Crustacea: Thalassinidea: Thalassinidae). Mineral Resources, 108: 41–42. Raffl es Bulletin of Zoology, Supplement No. 20: 121–158. Dana, J. D., 1852. Crustacea. Part I. United States Exploring Poore, G. C. B., & D. J. G. Griffin, 1979. The Thalassinidea Expedition, during the years 1838, 1839, 1840, 1841, 1842, (Crustacea: Decapoda) of Australia. Records of the Australian under the command of Charles Wilkes, U.S.N, 13(2): i–viii, Museum, 32: 217–321. 1–685; Atlas (1855), C. Sherman, Philadelphia. Sankolli, K. N., 1970. The Thalassinoidea (Crustacea, Anomura) Davie, P.J.F., 2002. Crustacea: : Phyllocarida, of Maharashtra. Journal of the Bombay Natural History Hoplocarida, Eucarida (Part 1). In: Wells, A. & W. W. K. Society, 67: 235–249. Houston (eds), Zoological Catalogue of Australia. Vol. 19.3A. Sasekumar, A., 1974. Distribution of macrofauna on a Malayan CSIRO Publishing, Melbourne. Pp. i–xii + 1–551. mangrove shore. Journal of Animal Ecology, 43: 51–69. Dworschak, P. C., 1992. The Thalassinidea in the Museum of Steenstrup, J. & C. Lutken, 1862. Om Thalassina anomala Natural History, Vienna; with some remarks on the biology of (HERBST). Videnskabelige meddelelser fra dansk the species. Annalen des Naturhistorischen Museums in Wien. naturhistorisk foreningi Kobenhavn, 1861: 267–248, pls. Serie B, Botanik und Zoologie, 93: 189–238, fi gs. 1–18. 1–7. Glaessner, M. F., 1969. Decapoda: R400–532. In: Moore, R. White, A., 1847. List of the specimens of Crustacea in the C. (ed.), Treatise on invertebrate paleontology, Part R, collection of the British Museum. British Museum Natural Arthropoda 4(2). University of Kansas Press and Geological History, London. Pp. i–viii +1–143. Society of America, Inc., Boulder, Colorado.

473 THE RAFFLES BULLETIN OF ZOOLOGY 2009

THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 475–480 Date of Publication: 31 Aug.2009 © National University of Singapore

A NEW SPECIES OF MACROPHTHALMUS DESMAREST, 1823 (CRUSTACEA: DECAPODA: BRACHYURA: MACROPHTHALMIDAE) FROM BOHOL ISLAND, THE PHILIPPINES

Jose Christopher E. Mendoza Department of Biological Sciences, Faculty of Science, National University of Singapore, 14 Science Drive 4, Singapore 117543 Email: [email protected]

Tohru Naruse Department of Biological Sciences, Faculty of Science, National University of Singapore, 14 Science Drive 4, Singapore 117543 Current address: Transdisciplinary Research Organization for Subtropical and Island Studies, University of the Ryukyus, 870 Uehara, Taketomi, Okinawa 907-1541, Japan Email: [email protected]

ABSTRACT. – Many new taxa have already been described as a result of the PANGLAO 2004 Marine Biodiversity Project. We report a new species of the ocypodoid crab genus Macrophthalmus Desmarest from the Philippines. Macrophthalmus pentaodon, new species, can be distinguished from other species in the genus primarily by the presence of fi ve anterolateral teeth on the carapace, the greatest known so far in the genus, and by its steeply oblique upper orbital margins. It can be further distinguished from closely allied species by its smaller size and shorter ocular peduncles.

KEYWORDS. – Macrophthalmus pentaodon, Brachyura, Macrophthalmidae, Philippines, Bohol, PANGLAO 2004.

INTRODUCTION by Ward (1941). Macrophthalmus sandakani Rathbun, 1914 was reported from Cebu by Estampador (1959) stating that The brachyuran crab family Macrophthalmidae Dana, “These crabs inhabit muddy beaches, and are quite abundant 1851 has been recognized as separate from Ocypodidae in the mouths of streams. The author has seen them collected Rafinesque, 1815 on account of morphological and for food at the mouth of Mambaling River in Cebu”. Both molecular evidence (see Kitaura et al., 2002; Mendoza species have since been treated as junior synonyms of M. & Ng, 2007; Ng et al., 2008). It is largely represented latreillei (Desmarest, 1822) (cf. Barnes, 1977). by the genus Macrophthalmus Desmarest, 1823, which contains 8 subgenera and 54 valid species (Barnes, 1977; Among the decapod Crustacea collected in the central Mendoza & Ng, 2007; Barnes & Davie, 2008; Naruse & Philippines by the PANGLAO 2004 Marine Biodiversity Kosuge, 2008; Ng et al., 2008). There are currently eleven Project (see Bouchet et al., 2009) were some unusual species of Macrophthalmus known from the Philippines: macrophthalmid crabs. They differed suffi ciently from any M. barnesi Serène, 1971; M. convexus Stimpson, 1858; known species of Macrophthalmus, and were considered M. crinitus Rathbun, 1913; M. dagohoyi Mendoza & Ng, new to science. One species has since been described 2007; M. depressus Rüppell, 1830; M. defi nitus Adams & by Mendoza & Ng (2007), and a second new species is White, 1849; M. japonicus (De Haan, 1835); M. latreillei described in this paper. (Desmarest, 1822); M. philippinensis Serène, 1971; M. tomentosus Souleyet, 1841; and M. transversus (Latreille, 1817). Three of these, M. barnesi, M. dagohoyi and M. MATERIALS AND METHODS philippinensis, have their type localities in the Philippines (cf. Ward, 1941; Estampador, 1959; Barnes, 1967; Serène, Carapace size is expressed as CW (carapace width) by CL 1971; Manuel et al., 1991; Komai et al., 1995; Mendoza & (carapace length). The CW and the widths of the female Ng, 2007). Macrophthalmus granulosus De Man, 1904 was third and fi fth abdominal segments were measured at the reported from the Gulf of Davao in the southern Philippines widest level, while other measurements follow Komai et al.

475 Mendoza & Naruse: Macrophthalmus pentaodon, new species

(1995: Fig. 1). Extra-orbital ocular peduncle length (length upper margin with a single row of minute granules, lower of the ocular peduncle beyond the external orbital angle) margin with row of granules adjacent to it, extending as was calculated by subtracting orbital length (from the base a distinct ridge onto fi xed fi nger, proximal part on palm of the ocular peduncle to the tip of the external orbital angle) granular; fi ngers nearly fl at, dactylus about 1.2 times longer from ocular peduncle length. Specimens are deposited in than palm, slightly curved, cutting edge toothless, fi xed the National Museum of the Philippines, Manila (NMCR), fi nger slightly defl exed, cutting edge with a few minute Ryukyu University Museum, Fujukan, Okinawa, Japan teeth on the middle region. (RUMF), Wakayama Prefectural Museum of Natural History, Wakayama, Japan (WMNH), and the Zoological Second to fi fth pereiopods (Fig. 1a) relatively long; meri Reference Collection, Raffles Museum of Biodiversity of second to fi fth pereiopods with subdistal tooth, third Research, National University of Singapore (ZRC). and fourth pereiopods with wider meri; dactyli with subrhomboidal cross-section, rather compressed laterally, dactylus of fourth pereiopod about 0.8 times as long as TAXONOMIC ACCOUNT propodus, sparsely setose on fl exor surface.

MACROPHTHALMIDAE Dana, 1851 Abdomen (Fig. 1e) wide, fully expanded, lateral margins convex; telson 2.3 times as wide as long, proximal margin Macrophthalmus (Macrophthalmus) Desmarest, l823 straight, slightly narrower than and appearing embedded into distal margin of sixth segment; sixth segment 2.2 times Macrophthalmus (Macrophthalmus) pentaodon, wider than telson, distal margin concave; fi fth segment 1.1 new species times wider than third; fourth segment widest; fi rst segment Fig. 1 with a transverse ridge dividing it into upper and lower halves. Material Examined. – Holotype: female (5.0 by 3.5 mm) (NMCR 27012), Stn. S21, reef slope with silt, 4–12 m, 9°41.7'N Genital opening situated just posterior to distal margin 123°50.9'E, Manga, Bohol Island, Philippines, coll. by PANGLAO of thoracic sternite 6; operculum sub-ovate, directed 2004 Marine Biodiversity Project, 20 Jun.2004. medially.

Description of female holotype. – Carapace (Fig. 1a) Comparative Material. – Macrophthalmus (Macrophthalmus) rectangular, regions not well-defined; dorsal surface philippinensis Serène, 1971, holotype male (10.0 by 5.6 mm) naked, relatively smooth, with short transverse ridge on (ZRC.1969.12.12.1), paratype male (10.0 by 5.6 mm) (ZRC. metabranchial region; greatest width across external orbital 1969.12.12.2), Busuanga, Palawan, Philippines, coll. by Norton teeth, 1.4 times as wide as long. Front 0.2 times as wide as and Dayrit, 10–30 May.1933. carapace, with shallow median furrow, not constricted at bases of ocular peduncles; frontal margin thinly rimmed. Macrophthalmus (Macrophthalmus) ryukyuanus Naruse & Kosuge, Upper orbital border steeply divergent posteriorly, with wide 2008, holotype male (9.3 by 5.3 mm) (ZRC 2007.0524), paratype male (CL 3.5 mm) (RUMF-ZC-538) off mouth of Urauchi River, convexity on inner third, smooth, sub-cristate; lower orbital Iriomote Island, Ryukyu Islands, Japan (24˚24.98'N, 123˚46.04'E), border sub-cristate, terminating just anterior to anterior 19 m depth, coll. T. Kosuge and K. Higa, dredge, 16 Aug.2005. margin of chelipedal coxa, outer half sparsely lined with very low granules. Lateral margins of carapace subparallel, Macrophthalmus (Tasmanoplax) latifrons Haswell, 1882, 1 male armed with 5 anterolateral teeth (including external orbital (27.0 by 16.7 mm), 1 ovig. female (23.1 by 15.0 mm) (ZRC tooth), followed posteriorly by small tubercles; external 1965.7.20.43–44), Oxford, Tasmania, coll. by Anonymous, orbital tooth narrow, acute, exceeding all other subsequent 1941. teeth; tips of subsequent teeth more rounded, bases wider, third largest, fi fth smallest; third tooth separated from fourth Ilyoplax dentata Ward, 1933, 1 male (5.5 by 4.0 mm) (ZRC 1995.959), estuarine muddy bay, 10.44°S, 142.33°E, far north of by wide V-shaped incision. Posterior margin of epistome Queensland, Australia, coll. by J. Short, 26 Oct.1990. (Fig. 1b) convex medially, without endostomial ridge. Ilyoplax gangetica (Kemp, 1919), 1 male (7.0 by 4.5 mm) (ZRC Ocular peduncle (Fig. 1a, b) long and stout, margins slightly 2001.2339), Stn. KR(S)1, mud, Ranong, Thailand, coll. by P. sinuous, exceeding exernal orbital tooth by 11.5% of its total Clark, 11 Nov.2001. length and half length of cornea in frontal view. Ilyoplax obliqua Tweedie, 1935, 1 male (4.6 by 3.3 mm), 1 ovig. Third maxillipeds separated by median hiatus, not completely female (4.7 by 3.2 mm) (ZRC 1987.227–228), Lim Chu Kang, covering buccal cavern when closed; median length of Singapore, coll. by P.K.L. Ng, 19 Mar.1987. ischium about 1.5 times that of merus; merus and ischium Ilyoplax orientalis (De Man, 1888), 1 male (5.8 by 4.3 mm) (ZRC with setose inner margins; distal external margin of merus 1987.231–239), Lim Chu Kang, Singapore, coll. by P.K.L. Ng & rounded. Exopod narrow (Fig. 1c). S. Harminto, 3 Sep.1986.

Chelipeds (Fig. 1d) symmetrical, weak. Palm of chela Tmethypocoelis ceratophora (Koelbel, 1897), 1 male (6.4 by smooth on inner surface, outer surface sparsely granulated, 3.8 mm) (ZRC 1993.622–625), Horikawa reef fl at, Tamagusuku Village, Okinawa, Japan, coll. by P.K.L. Ng, Apr.1992.

476 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 1. Holotype of Macrophthalmus (Macrophthalmus) pentaodon, new species, NMCR 27012 (5.0 by 3.5 mm). a, habitus; b, frontal view showing eye, front, antenna, antennules & epistome; c, right third maxilliped; d, left chela, external view; e, telson and abdominal segments. Scales, 1 mm.

477 Mendoza & Naruse: Macrophthalmus pentaodon, new species

Habitat and Distribution. – The sole specimen of margin of the merus (vs. exopod shorter, reaching only to Macrophthalmus (Macrophthalmus) pentaodon, new mid-level of merus) (Fig. 1c); and 7) the relatively longer species, was found in muddy to silty bottoms at depths and more slender walking legs (vs. shorter and stouter) (Fig. ranging from 4 to 12 m. This species, collected by vacuum 1a) (cf. Barnes, 1966: pl. XXIV; Barnes, 1967: 241–244, suction of the bottom sediment, is reported, thus far, only fig.14, pl. IV). Macrophthalmus pentaodon can also be from the type locality, Bohol island, Philippines. easily distinguished from the monotypic genus Enigmaplax Davie, 1993, which contains E. littoralis Davie, 1993, by Etymology. – The specifi c epithet, pentaodon, is an arbitrary the following characters: 1) the more rectangular carapace combination from the Greek words penta (n., five) and outline, with the lateral margins divergent anteriorly (vs. odon (n., tooth), referring to the fi ve anterolateral teeth on more squarish, lateral margins subparallel to convergent in the carapace of this species. Used as a noun in apposition. E. littoralis) (Fig. 1a); 2) the relatively narrower front (vs. very wide front in E. littoralis) (Fig. 1a, b); 3) the steeply Remarks. – Macrophthalmus (Macrophthalmus) oblique upper orbital border (vs. horizontal in E. littoralis); pentaodon, new species, is morphologically unique in 4) the relatively longer ocular peduncles, which go just the Macrophthalmidae in its posteriorly divergent upper beyond the tip of the external orbital tooth (vs. short and orbital borders. The new species clearly belongs to stout, not reaching or just reaching the tip of the external Macrophthalminae, typically possessing the features of orbital tooth) (Fig. 1a); 5) the convex central portion of the the subfamily such as elongated eyestalks, a rectangular epistome posterior margin (vs. concave) (Fig. 1b); 6) and carapace, antennules that fold transversely or obliquely, a the rectangular aspect of the third maxilliped, without any narrow inter-antennulary septum, and external maxillipeds external or internal extensions in either merus or ischium that do not completely close the buccal cavern (Barnes, 1967; (vs. the sigmoidal aspect of the third maxilliped, due to an Sakai, 1976; Davie, 2002). It can easily be distinguished anterolateral extension in the merus and a posteromesial from Dotillidae Stimpson, 1858, and superfi cially similar extension in the ischium) (Fig. 1c) (cf. Davie, 1993: 5–9, genera such as Ilyoplax Stimpson, 1858 and Tmethypocoelis fi gs. 1, 2). Koelbel, 1897, by having a more rectangular carapace (Fig. 1a) (vs. more quadrate in dotillids); having rectangular At the subgeneric level, we believe that M. pentaodon merus of the third maxilliped about half the size of the belongs in the subgenus Macrophthalmus (see Barnes, 1967; ischium (Fig. 1c) (vs. merus oval, larger or as large as Komai et al., 1995) wherein the posteromedian margin of ischium in dotillids); having no tympani on the merus of the the epistome is protuberant, not concave, and the ocular walking legs (vs. present in some species of Ilyoplax); and peduncles are more than 0.5 times as long as the carapace having a distinct and acute subdistal spine on the anterior (Figs. 1a, b). It differs from the subgenus Tasmanoplax margin of the merus of the walking legs (vs. no subdistal Barnes, 1967, the only other subgenus with a protuberance spine) (Fig. 1a). (cf. Kemp, 1919; Serène & Lundoer, 1974; in the epistome’s posteromedian margin, in that the ischium Davie, 1990). Members of Camptandriidae Stimpson, 1858 of the third maxilliped is distinctly larger than the merus have various carapace shapes. Since the most discriminative (Fig. 1c), whereas in Tasmanoplax they are subequal (cf. character of the family is the strongly recurved G1 of the Barnes, 1967). Macrophthalmus pentaodon differs from all male, it is sometimes diffi cult to identify the familial place other species in the subgenus Macrophthalmus in having of female specimens. However, Macrophthalmus pentaodon fi ve anterolateral teeth, the greatest number for this genus, has relatively long ocular peduncles and a narrow front, and thus far. By contrast, other species of Macrophthalmus in this regard, this new species can be easily distinguished (Macrophthalmus) have either two or three (rarely four) from Camptandriidae. anterolateral teeth, including the external orbital angle (cf. Barnes, 1967; 1970; 1971; 1977). Species in the Within Macrophthalminae, M. pentaodon clearly falls under subgenus Macrophthalmus tend to have relatively thicker the genus Macrophthalmus primarily due to condition of ocular peduncles as juveniles, this was also observed in M. the third maxilliped, wherein the merus is wider than long pentaodon although the female holotype is clearly adult as and is much smaller than the ischium, which is longer than it already possesses a fully expanded abdomen (Fig. 1e). wide; the long ocular peduncles; and the anteriorly divergent In most other species the adults have thin ocular peduncles lateral carapace margins (cf. Barnes, 1967). It can easily be together with bulbuous corneas. The relatively thick ocular distinguished from Australoplax Barnes, 1966, under which peduncle and small cornea (Fig. 1a, b) of M. pentaodon there is only one species, A. tridentata (A. Milne-Edwards, can be also considered as a unique character of this small 1873) by 1) the more rectangular carapace outline (vs. species. more quadrate in A. tridentata) (Fig. 1a); 2) the straight frontal margin (vs. obtusely convex) (Fig. 1a, b); 3) having Macrophthalmus pentaodon, new species, is perhaps most 5 triangular anterolateral teeth (vs. having 3 quadrangular similar to M. ryukyuanus Naruse & Kosuge, 2008, in being anterolateral teeth) (Fig. 1a); 4) having long eyes that go relatively small in size and in having the ocular peduncle beyond the external orbital tooth (vs. short eyes that do not only weakly exceeding beyond the external orbital tooth. go beyond external orbital tooth) (Fig. 1a); 5) the merus of However, M. pentaodon differs from M. ryukyuanus in the third maxilliped which is half as large as the ischium the following features: (1) absence of a constriction on the (vs. merus and ischium subequal) (Fig. 1c); 6) having the front across the bases of the ocular peduncles (Fig. 1a) (vs. exopod of the third maxilliped reaching up to the anterior present in M. ryukyuanus), (2) steeply oblique upper orbital

478 THE RAFFLES BULLETIN OF ZOOLOGY 2009 border (Fig. 1a) (vs. moderately oblique in M. ryukyuanus), Barnes, R. S. K., 1970. The species of Macrophthalmus (Crustacea: (3) fi ve teeth on the anterolateral margin of the carapace Brachyura) in the collections of the British Museum (Natural (Fig. 1a) (vs. three teeth on the anterolateral margin of the History). Bulletin of the British Museum, Natural History, carapace in M. ryukyuanus), and (4) acicular dactylus of the Zoology, 20: 203–251. fourth ambulatory leg (vs. lanceolate dactylus of the fourth Barnes, R. S. K., 1971. Biological results of the Snellius ambulatory leg in M. ryukyuanus ) (cf. Naruse & Kosuge, Expedition. XXIII. The genus Macrophthalmus (Crustacea: 2008). In addition to this, M. pentaodon differs from M. Brachyura). Zoologische Verhandelingen, Leiden, 115: 1–40. ryukyuanus in the relative length of the ocular peduncle Barnes, R. S. K., 1977. Concluding contributions towards and in body size. The extent to which the ocular peduncles a revision of, and a key to, the genus Macrophthalmus exceed the length of the orbit in M. pentaodon is 11.5% of (Crustacea: Brachyura). Journal of Zoology (London), 182: its total length (holotype, CW 5.0 mm), whereas it is 21% 267–280. in M. ryukyuanus (holotype, CW 9.3 mm). Macrophthalmus Barnes, R. S. K. & P. J. F. Davie, 2008. A new species of the pentaodon is also superfi cially similar to M. philippinensis sentinel crab Macrophthalmus (Mareotis) Barnes, 1967 due to their small size and the general carapace outline. (Crustacea: Brachyura: Macrophthalmidae) from Western Australia. Zootaxa, 1807: 63–68. However, it can be distinguished from M. philippinensis by 1) the 5 anterolateral teeth on the carapace (vs. 3 Bouchet, P., P. K. L. Ng, D. Largo & S.-H. Tan. 2009. PANGLAO anterolateral teeth in M. philippinensis); 2) the absence of 2004 – Investigations of the marine species richness in the Philippines. Raffl es Bulletin of Zoology, Supplement No. 20: a constriction on the front across the bases of the ocular 1–19. peduncles (vs. present); and 3) the shorter, thicker ocular peduncles with small corneas (vs. longer ocular peduncles, Dana, J. D., 1851. Conspectus crustacearum quae in orbis terrarum half their length going beyond the tip of the external orbital circumnavigatione, Carolo Wilkes e classe Reipublicae Foederatae Duce, lexit et descriptsit J.D. Dana. Proceedings angle, with larger, bulbous corneas) (cf. Serène, 1971). of the Academy of Natural Sciences of Philadelphia, 5: 247–254. Davie, P. J. F., 1990. New and rare crabs of the subfamily ACKNOWLEDGEMENTS Dotillinae (Crustacea: Ocypodidae) from northern Australia and . Memoirs of the Queensland Museum, We thank the main organizers of the PANGLAO 2004 28(2): 463–473. Marine Biodiversity Project, Philippe Bouchet (Muséum Davie, P. J. F., 1993. A new genus of macrophthalmine crab national d’Histoire naturelle) and Danilo Largo (University (Crustacea: Decapoda: Ocypodidae) from eastern Australia. of San Carlos); the strong fi nancial support from the TOTAL Records of the Australian Museum, 45: 5–9. Foundation, as well as the support of the ASEAN Regional Davie, P. J. F., 2002. Crustacea: Malacostraca: Eucarida (Part 2): Centre for Biodiversity and Conservation (ARCBC), the Decapoda – Anomura, Brachyura. In: Wells, A. & Houston, Bureau of Fisheries and Aquatic Resources (BFAR), the W.W.K. (eds.), Zoological Catalogues of Australia. Vol. 19.3B. National Museum of the Philippines, Manila, the Muséum Melbourne: CSIRO Publishing, Australia. 641pp. national d’Histoire Naturelle, Paris, and the National Desmarest, A. G., 1822. Les Crustacés proprement dits. In: University of Singapore. The strong support provided by Histoire naturelle des Crustacés fossiles. Paris, F.G. Levrault. the University of San Carlos, Cebu is also acknowledged. pp. 67–154, Pls. 5–11 Our colleagues—Peter Ng, Marivene Manuel-Santos, S. H. Desmarest, A. G., 1823. Dictionnaire des Sciences Naturelles, vol. Tan and Joelle Lai—were responsible for the Brachyura 28. F.G. Levrault, Paris, Pp.138–425. collected during this expedition. We also thank Darren Yeo and two anonymous reviewers for their suggestions to Estampador, E. P., 1959. Revised checklist of Philippine crustacean decapods. Natural and Applied Science Bulletin, 17: 1–127. improve this paper. This study was supported by research grant R-154-000-334-112 from the National University of Haan, H. M. de, 1833–1849. Crustacea. In: P.F. von Siebold (ed.), Singapore. Fauna Japonica sine descriptio animalium, quae in itinere per Japoniam jussu et auspiciis superiorum, qui summum in India Batava Imperium tenent, suscepto, annis 1823–1830 collegit, notis, observationibus et adumbrationibus illustravit. LITERATURE CITED Amsterdam: J. Muller & Sons. i–xvii + i–xxxi + iix–xvi + 1–243, Pls. A–J, L–Q, 1–55, Circ. Table 2. Adams, A. & A. White, 1849. The Crustacea. In: Adams, A. Haswell, W. A., 1882. On some new Australian Brachyura. (ed.), The Zoology of the voyage of the H.M.S. Samarang, Proceedings of the Linnaean Society, New South Wales, 6: 1843–1846. London: Reeve, Benham & Reeve. 66 pp. 540–551. Barnes, R. S. K., 1966. The status of the genus Euplax H. Milne Kemp, S., 1919. Notes on the Crustacea Decapoda in the Indian Edwards, 1852; and a new genus Australoplax of the subfamily Museum. XII – Scopimerinae. Records of the Indian Museum, Macrophthalminae Dana, 1851. (Brachyura: Ocypodidae). 16(5): 305–348, Pl. 12. Australian Zoologist, 13: 370–376. Kitaura, J., K. Wada, & M. Nishida, 2002. Molecular phylogeny Barnes, R. S. K., 1967. The Macrophthalminae of Australasia; of grapsoid and ocypodoid crabs with special reference to the with a review of the evolution and morphological diversity genera Metaplax and Macrophthalmus. Journal of Crustacean of the type genus Macrophthalmus (Crustacea: Brachyura). Biology, 22: 682–693. Transactions of the Zoological Society of London, 31: 195–262.

479 Mendoza & Naruse: Macrophthalmus pentaodon, new species

Koelbel, K., 1897. Beschreibung der Krebse. In Die Rathbun, M. J., 1913. Descriptions of new species of crabs of the wissenschaftlichen Ergebnisse der Reise des Grafen Béla family Ocypodidae. Proceedings of the United States National Széchenyi in Ostasien. Bd. 2: 709–718, pl. 1. [not seen] Museum, 44: 615–620. Komai, T., S. Goshima & M. Murai, 1995. Crabs of the genus Rathbun, M. J. 1914. New species of crabs of the families Macrophthalmus of Phuket, Thailand (Crustacea: Decapoda: Grapsidae and Ocypodidae. Proceedings of the United States Ocypodidae). Bulletin of Marine Science, 56: 103–149. National Museum, 47: 69–85. Latreille P. A., 1817. Nouveau dictionnaire d’histoire naturelle: Rüppell, E. S., 1830. Beschreibung und Abbildung von 24 Arten appliquée aux arts, à l’agriculture, à l’économie rurale et kurzschwänzigen Krabben, als Beitrag zur Naturgeschichte domestique, à la médecine, etc. 2nd Ed., Vol. 13. Paris, des rothen Meeres. H.L. Brönner, Frankfurt. Pp. 1–28, pls Deterville. p. 295. 1–6. Man, J. G. de, 1887–1888. Report on the podophthalmous Sakai, T., 1976. Crabs of Japan and the Adjacent Seas. Kodansha Crustacea of the Mergui Archipelago, collected for the Ltd., Tokyo. 3 vols. xxix + 773 pp., 379 fi gs. (in English): Trustees of the Indian Museum, Calcutta, by Dr. John 1–461 (in Japanese): 1–16, Pls. 1–251. Anderson, F.R.S., Superintendent of the Museum. Journal of Serène, R., 1971. Observations préliminaires sur des brachyoures the Linnaean Society, Zoology, 22: 1–312, Pls. 1–19. nouveaux ou mal connus du Sud-est Asiatique (Crustacea Man, J. G. de, 1904. Beschreibung einiger brachyurer Krebse aus Decapoda). Bulletin du Muséum national d’Histoire naturelle, posttertiären Schichten der Minahassa, Celebes. Sammlungen 42(5): 903–918, Pls. 1–6. des Geologischen Reichsmuseums in Leiden, I te Serie, 7: Serène, R. & S. Lundoer, 1974. Observations on the male 254–278, Pls. 9, 10. pleopod of the species of Ilyoplax Stimpson with a key to the Manuel, M. R., P. C. Gonzales & L. Basmayor, 1991. Crustacean identifi cation of the species. Phuket Marine Biological Center fauna of Natunawan Cove in Tabaco, Albay, (Crustacea: Research Bulletin No. 3, Phuket, Pp. 3–10. Brachyura, Macrura and Stomatopoda). National Museum Souleyet, L. F. A., 1841. Crustacés. In: F. Eydoux & L.F.A. Papers, Manila, 2(1): 59–102. Souleyet (eds.), Voyage autour de monde exécuté pandant les Mendoza, J. C. E. & P. K. L. Ng, 2007. Macrophthalmus (Euplax) années 1836 et 1837 sur la corvette La Bonite, commandée H. Milne-Edwards, 1852, a valid subgenus of ocypodoid crab par M. Vaillant, Paris, 1: 219–244. (Decapoda: Brachyura: Macrophthalmidae), with description Stimpson, W., 1858. Crustacea Ocypodoidea: Prodromus of a new species from the Philippines. Journal of Crustacean descriptionis animalium evertebratorum, quae in Expeditione Biology, 27(4): 860–870. ad Oceanum Pacifi cum Septentrionalem, a Republica Federata Milne-Edwards, A., 1873. Recherches sur la faune carcinologique missa, Cadwaladaro Ringgold et Johanne Rodgers Ducibus, de la Nouvelle Calédonie. 2. Nouvelles archives du Muséum observatit et descripsit W. Stimpson. Pars V. Proceedings d’Histoire naturelle de Paris, 9: 155–332. of the Academy of Natural Sciences of Philadelphia, 10: Naruse, T. & T. Kosuge, 2008. A new species of Macrophthalmus 93–110. (Crustacea: Decapoda: Brachyura: Macrophthalmidae) from Tweedie, M. W. F., 1935. Notes on the genus Ilyoplax Stimpson Iriomote Island, Ryukyu Islands, Japan. Species Diversity, (Brachyura, Ocypodidae). Bulletin of the Raffl es Museum, 10: 13: 117–122. 53–61, Pls. 2–3. Ng, P. K. L., D. Guinot & P. J. F. Davie, 2008. Systema Ward, M., 1933. New genera and species of marine Decapoda Brachyurorum: Part I. An annotated checklist of the extant Brachyura. Australian Zoologist, 7: 377–394. brachyuran crabs of the world. Raffl es Bulletin of Zoology, Ward, M., 1941. New Brachyura from the Gulf of Davao, Mindanao, Supplement No. 17: 1–286. Philippine Islands. American Museum Novitiates, 1104: 1–15. Rafinesque, C. S., 1815. Analyse de la nature ou tableau de l’univers et des corps organisés. l’Imprimerie de Jean Barravechia, Palermo. 224 pp.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 481–494 Date of Publication: 31 Aug.2009 © National University of Singapore

OYSTERS (BIVALVIA: OSTREIDAE AND GRYPHAEIDAE) RECORDED FROM MALAYSIA AND SINGAPORE

Katherine Lam Hoi Ha Wan Marine Life Centre, Department of Biology and Chemistry, City University of Hong Kong, Kowloon Tong, Hong Kong Present address: Oceanway, Unit 3, No. 34, Tai Chung Hau Village, Sai Kung, Hong Kong. Email: [email protected]

Brian Morton Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom. Email: [email protected]

ABSTRACT. – Oysters recorded from Malaysia and Singapore are revised herein, based on six collected species with description of shell characters and other records from the literature. The collected oysters are Saccostrea cuccullata (Born, 1778), Saccostrea mordax (Gould, 1850), Crassostrea gigas (Thünberg, 1793), Planostrea pestigris (Hanley, 1846), Dendostrea folium (Linnaeus, 1758) and Hyotissa imbricata (Lamarck, 1819). Of these, Saccostrea mordax, Dendostrea folium and Hyotissa imbricata are new records. Including other species recorded in the literature, i.e., Alectryonella plicatula, Ostrea denselamellosa, Hyotissa hyotis and Parahyotissa numisma, there are now 10 species of oysters recorded from Malaysia and Singapore. An identifi cation key based on shell characters is included.

KEY WORDS. – Oyster, Ostreidae, Gryphaeidae.

INTRODUCTION from Malaysia and Singapore, comprises but six species. The literature (e.g., Mathias & Charles, 1978; Zulfi gar & Oysters appear to have a low species diversity in Tan, 1998), also identifi es ‘Crassostrea gigas’ as being Malaysia and Singapore. Morris & Purchon (1981), for introduced into Malaysia for mariculture purposes. Tan & example, recorded only fi ve species of Ostreidae and two Chou (2000) also identify C. gigas from Singapore. species of Gryphaeidae from the area. Species identifi ed were Alectryonella plicatula (Gmelin, 1791), ?Ostrea A recent collection of oysters from Pulau Langkawi on the denselamellosa Lischke, 1869, Ostrea palmipes Sowerby, west coast of Malaysian Peninsula, identifi es fi ve species of 1871, Saccostrea cuccullata (Born, 1778), Saccostrea native oysters that include three new records for the area. echinata (Quoy & Gaimard, 1835), Hyotissa hyotis A mariculture species, Crassostrea gigas, was collected (Linnaeus, 1758) and Hyotissa numisma (Lamarck, 1819) from Johor Strait, Malaysia. The specimen was grown from (now Parahyotissa (Numismoida) numisma [Lamprell spat fl own in from hatcheries in Australia. In this paper, a & Healy, 1998, fig. 324]). A recent expedition to the checklist of Malaysian and Singaporean oysters is given Anambas and Natuna Islands, located between the West and descriptions provided for native species including the Malaysian Peninsula and Borneo, identified no oysters new records. (Tan & Kastoro, 2004). Saccostrea cuccullata has been identifi ed from Malaysian rocky shores and West Malaysian mangroves by Berry (1964, 1972) and Sasekumar (1974) MATERIAL AND METHODS as either Crassostrea cuccullata or Ostrea cuccullata. Crassostrea cuccullata and an unidentified Ostrea sp. Sample collection. – Oysters were collected from intertidal occur on rocky intertidal surfaces in Singapore (Purchon habitats, such as mangroves, rocky shores and sandy & Enoch, 1954). All the rock oysters from Singapore were, beaches in Pulau Langkawi, West Malaysia. Those from however, later genetically identifi ed as S. cuccullata (Lam subtidal waters were obtained by trawling. The samples & Morton, 2006). Since S. cuccullata and S. echinata have were identifi ed using the following shell characters: (1), also been genetically identifi ed as synonymous (Lam & general size; (2), shape and surface sculpture; (3), hinge Morton, 2006), the list of native oysters hitherto recorded structure and ligament position and extent; (4), attachment

481 Lam & Morton: Oysters from Malaysia and Singapore area of the left valve; (5), presence and pattern of chomata; Ostrea cucullata – Born, 1780: 114, Pl. 6, Figs. 11, 12; Awati & (6), position, colour and relative size of the adductor muscle Rai, 1931: 1–107. scar and (7), external and internal shell colour. Details of Ostrea echinata Quoy & Gaimard, 1835: 455, Pl. 76, Figs. 13, habitat and biogeography were based mainly on the authors’ 14. Ostrea commercialis Iredale & Roughley, 1933: 278. observations, complemented by published information. Saccostrea cucullata – Stenzel, 1971: N1134–N1135, Fig. J106. Saccostrea cucullata – Morris, 1985: 125–128, Pl. 3, Fig. E, F, G; Abbreviations used in the text. – NHM, The Natural Lam, 2003: 110–112, Pls. 11–12. History Museum, London, United Kingdom; MNHN, Musèum National d’Histoire Naturelle, Paris, France; Material examined. – Born’s type is in Naturhistorisches Museum, USNM, National Museum of Natural History [formerly Vienna (Morris, 1985): data unknown. United States National Museum], Smithsonian Institution, Washington D. C., United States. RV, right valve; LV, left Specimens in this collection (all preserved in alcohol) - [NHM] valve. 20090286, “On big mangrove trees, Tanjong Rhu mangrove, Pulau Langkawi, Malaysa” (9) and “On mangrove rocks” (two clusters) coll. B. Morton, 3 & 5 Feb.2004. [NHM] 20090287, Pelangi RESULTS Beach rocks, low intertidal, Pulau Langkawi, Malaysia, coll. B. Morton, 3 & 5 Feb.2004 (33). [NHM] 20090288, intertidal, Pelangi Beach groyne, Pulau Langkawi, Malaysia, coll. B. Morton, 3 & Systematic list of Pulau Langkawi oysters collected 5 Feb.2004. [NHM] 20030507, Tanah Merah, Singapore, coll. in this study B. Morton, 9 Jul.2001 (2). [NHM] 20030508, Kallang River, Singapore, coll. B. Morton, 9 Jul.2001 (2). All the fi gured specimens have been deposited in the NHM under accession numbers 20090286–20090293. Description. – Shell size small to medium, up to ~ 70 mm in length and ~ 75 mm in height, ~5–20 mm in width, with Suborder Ostreina Férussac, 1822 an oval to subtriangular outline, depending upon substratum Superfamily Ostreoidea Rafi nesque, 1815 and available space. Hinge line straight, short, with the Family Ostreidae Rafi nesque, 1815 ligament occupying its total length. Ligamental area short. Subfamily Crassostreinae Torigoe, 1981 External surfaces of both left and right valves white, lilac to Genus Saccostrea Dollfus and Dautzenberg, purple with dark purple coloration at the shell margin. 1920 Saccostrea cuccullata (Born, 1778) Three main growth forms or ecotypes in terms of external Saccostrea mordax (Gould, 1850) shell characters were recorded. Genus Crassostrea Sacco, 1897 Crassostrea gigas (Thünberg, 1793) The fi rst ecotype occurs on mangrove trees and attaches to Genus Planostrea Harry, 1985 intertidal tree trunks as solitary individuals. Sizes are large, Planostrea pestigris (Hanley, 1846) up to ~70 mm in length, 75 mm in height and 7 mm in Genus Dendostrea Swainson, 1835 width. Attachment area of left valve almost complete with Dendostrea folium (Linnaeus, 1758) slightly raised shell margin. Flat left valves usually slightly larger than right valve, shallowly cupped and with slightly Family Gryphaeidae Vyalov, 1936 raised margins and dense growth squamae. Commissural Subfamily Pycnodonteinae Stenzel, 1959 shelf not obvious. Surface of the right valve in large Genus Hyotissa Stenzel, 1971 specimens eroded probably by acidic freshwaters, revealing Hyotissa imbricata (Lamarck, 1819) the alternate white calcareous and brown conchiolin layers of the shell. In smaller specimens, commarginal layers of purple, weak, fl aky growth squamae cover the right valves. TAXONOMY Ribs not raised but weak crenulations along the ventral shell margin identify the number of ribs present. A comparison of shell characters of the six species of Malaysian oysters treated herein is given in Table 1. The second ecotype occurs on low intertidal beach rocks as solitary individuals. Sizes are medium, up to ~45 mm Ostreidae Rafi nesque, 1815 in length, 50 mm in height and 8 mm in width. Flat left valve attached completely to the substratum without Crassostreinae Torigoe, 1981 raised margin. Commissural shelf not obvious. Flat left valves slightly smaller than right valve, which are slightly Saccostrea Dollfus & Dautzenberg, 1920 convex, covered with commarginal layers of dense, fl aky lamellar scales radiating from the ligament. Scales usually Saccostrea cuccullata (Born, 1778) eroded along the ligamental side, where commarginal Common name: Rock oyster (Spiny oyster for the growth squamae are revealed. These end as black or purple ‘echinata’ morphotype) (Fig. 1) conchiolin scales along the ventral shell margin. White or purple radiating stripes occur on the convex right valves of Ostrea cuccullata Born, 1778: 100. some specimens. Shell margin usually not crenulate or if it

482 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Comparison of shell characters of the six species of oysters herein recorded from Pulau Langkawi, West Malaysia.

Taxa Chomata Shape Sculpture Maximum Size 1

Saccostrea cuccullata Present Oval to subtriangular Right valve covered with growth squamae 70 × 75 × 7 with hyote spines Saccostrea mordax Present Triangular or elongate Parallel grooves run from hinge to ventral 47 × 30 × 6 D-shape margin Crasssotrea gigas Absent Spatulate to oval Both valves have radial ribs and right valve 30 × 25 × 15 covered with calcareous growth squamae Planostrea pestigris Present Oval Flat and smooth 50 × 40 × 4 Dendostrea folium Inconspicuous Orbicular to oval Smooth, covered by dichotomous ribs 55 ×30 ×10 Hyotissa imbricata Present Circular Dichotomous ribs, growth squamae and 45 × 50 × 15 ocassion hyote spines on both valves

1 Maximum size is listed here as height (mm) × length (mm) × width (mm) is, only weakly crenulate refl ecting the number and position Remarks. – The Saccostrea cuccullata collected from Pulau of the slightly raised radial ribs. Marginal plications weak, Langkawi illustrate the effect of substratum on the growth usually irregularly-spaced and shallowly-rounded. form, resulting in various ecotypes. For example, those growing on mangrove tree stems are laterally compressed, The third ecotype occurs in clusters on intertidal rocks on with the left valve possessing a great attachment surface beaches or small hard substrata, such as dead mollusc or and a raised left shell margin. Individuals occurring on low barnacle shells. Sizes are small, up to ~30 mm in length, 40 intertidal beach rocks have a similar growth form as the mm in height and 12 mm in width. Attachment area of the former except the right valve is convex and the whole of left valve usually ~ half the shell length. Left valve margin the left valve is attached to the substratum, without a raised raised and thus deeply cupped. Commissural shelf not margin. This prevents the animal from being dislodged by obvious. Surface of the left valve with up to about 15 ribs. wave action. S. cuccullata also occurs on intertidal rocky Commarginal layers of weak, fl aky growth squamae occur substrata. Individuals from this zone cluster together, on the left valve margin that is raised above the substratum. compete for attachment area and are of small size (~10 mm Fine crenulations along the ventral shell margin identify to 20 mm). The shell margins are plicate and left shell valves the number of ribs present, forming a fl aky shell margin have a raised margin and small attachment area. patterned black, purple and white. Flat to slightly convex right valve covered with comarginal layers of dense, fl aky lamellar scales radiating from the ligament. These scales are Saccostrea mordax (Gould, 1850) usually eroded along the ligamental side, where alternate Common name: Crenulate rock oyster (Fig. 2) white calcareous and brown conchiolin layers are revealed. They end as black conchiolin scales along the ventral shell Ostrea cucullata Lamarck ,1819: 200 [non Born, 1778] margin. Shell margin crenulate refl ecting the number and Ostraea mordax Gould, 1850: 346; Sowerby, 1871, Pl. 15, Fig. position of the radial ribs. Marginal plications small, usually 31a, b. regularly-spaced and sharply-rounded. Ostrea forskali var. mordax Lamy, 1929: 159. Ostrea amasa Iredale, 1939: 399, Pl. 17, Fig. 8. Crassostrea amasa Thomson, 1954: 154, Pl. 7, Figs. 1, 2. Interiors of both valves of all ecotypes usually either Crassostrea tuberculata Thomson, 1954: 157, Pl. 8, Fig. 3. iridescent bluish green or opalescent white with patches Saccostrea mordax – Torigoe, 1981: 328, Pl. 17. of bluish green, or olive to yellowish green. Adductor scar Saccostrea mordax – Qi & Choe, 2000: 138–139, Fig. 3C–E; Lam, large, D-shaped, and may have purple or yellow growth 2003: 112–113, Pl. 13. bands paralleling the width of the shell. Scars on the left Saccostrea cucullata – Morris, 1985: 125–128, Pl. 3, Fig. A, B, and right valves of the same specimen of same shape, size, C, D. and colour, positioned in the posterior ventral third of the shell interior. Chomata and gutters may be present in young Material examined. – Syntypes: [USNM] 5958, ‘‘Feejee Islands’’(Fiji), coll. United States Exploring Expedition, no date, individuals. These are well developed from the hinge region 3 dry shells. to the adductor muscle, but fade beyond. Voucher: [NHM] 20090289, Pelangi Beach rocks, low intertidal, Distribution and habitat. – Subtropical and tropical Indo- Pulau Langkawi, Malaysia, coll. B. Morton, 4 Feb.2004, two West Pacifi c, from southern Japan to Australia, as verifi ed individuals preserved in alcohol. by mitochondrial DNA markers (Lam and Morton, 2006). This oyster dominates the eulittoral zone of sheltered rocky Description. – Shell medium, up to 47 mm in height, 30 shores. mm in length and 6 mm in width. Outline either triangular or an elongate D-shaped depending upon the substratum.

483 Lam & Morton: Oysters from Malaysia and Singapore

Fig. 1. Saccostrea cuccullata (Born, 1778) from Pulau Langkawi, Malaysia, showing external and internal views of the right and left shell valves. A–D, ecotype occurring on mangrove trees (NHM20090286), E–H, ecotype occurring on low intertidal beach rocks (NHM20090287), I–L, ecotype occurring on intertidal rocks (NHM20090288).

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Left valve fl at and attached completely.The dorsal margin Distribution and habitat. – Saccostrea mordax occurs only very thin and easily broken when collected. Margin of on oceanic, exposed rocky shores as individuals among the left valve built up steeply along the anterior and posterior Septifer and Tetraclita zone on slopes or in pools frequently sides. Margins thick, with packed layers of growth squamae refreshed by strong waves (Lam & Morton, 2004). This running along the margin. Closely and evenly spaced ribs species is widely distributed in the Indo-West Pacifi c, for perpendicular to these end as marginal crenulations. In example, Japan, Korea, Taiwan, Hong Kong, South China most cases, where the oyster grows on unlimited fl at rock Sea, peninsular Malaysia, Singapore, Indonesia, New surfaces, the anterior margin is reduced so that the right Hebrides [now Vanuatu] and Australia (Lam & Morton, valve is in touch with the substratum. When viewed along 2006). the mouth-anus axis, the shape of the oyster is almost a right-angled triangle with height given by the height of the Remarks. – Saccostrea mordax has been identified posterior margin and base given by the left valve. Hinge previously as S. amasa and S. tuberculata (Thompson, line straight and short. Ligament area elongated to form an 1954). This species is often confused with S. cuccullata obvious left beak. because of similar shell characters. Lam & Morton (2006) suggest that S. mordax occurs only on exposed, wholly Right valve convex, thicker than the left valve and white marine rocky shores whereas the other Saccostrea lineages with purple patches on the less eroded ventral area. Shell occupy a wide range of habitats from brackish mangroves usually eroded with exposed conchiolin scales near the to somewhat less exposed marine shores. Un-eroded dorsal end. Parallel grooves extend from half way along Saccostrea mordax individuals are distinct from other the dorso-ventral axis to the ventral shell margin. These species of Saccostrea in terms of the regularly-spaced grooves reveal uneroded growth lines on the right valve. grooves radiating from the umbone to the ventral margin Evenly-spaced crenulations around the shell margin are of the right valve, its triangular shell shape and finely, more obvious anteriorly and posteriorly. regularly, m-shaped plicated valve margin.

Interior of the shell white with a shiny, pearly appearance. A band of dark green conchiolin usually occur near the Crassostrea Sacco, 1897 ventral margin of the right valve. This band may be absent in some specimens. It appears that the conchiolin and prismatic Crassostrea gigas (Thünberg 1793) calcite layers are deposited alternately at the right, inner, Common name: Giant Pacifi c oyster (Fig. 3) ventral shell surface. Adductor muscle scar relatively large and positioned in the posterior ventral half of the pallial Ostrea gigas Thünberg 1793: 140–142, Pl. 6, Figs. 1–3. area, circular to elongate-oval according to the growth form Ostrea gigas – Lischke 1869: 174. of the shell and mostly white, slightly stained with growth Ostrea laperousii Schrenck 1861: 92–93, Fig. 6. bands or purple. Chomata white, short, rod-shaped and Ostrea laperousii – Schrenck 1867: 475–482, Pl. 19, Figs. 1–6. Ostrea (Crassostrea) gigas – Hirase 1930: 45–49, Figs. 61–63. arranged in a single line around the inner margin. They are Ostrea (Crassostrea) lapérousei – Hirase 1930: 49–55. more prominent dorsally and fade as they extend towards Crassostrea gigas – Torigoe 1981: 304–305, 325, Pl. 2, Fig. 1, the ventral shell margin. Pl. 14.

Fig. 2. Saccostrea mordax (Gould, 1850) from Pulau Langkawi, Malaysia (NHM20090289). A, external view of the right shell valve, B, internal view of the right shell valve and C, internal view of the left shell valve.

485 Lam & Morton: Oysters from Malaysia and Singapore

Fig. 3. Crassostrea gigas (Thünberg, 1793) from Johor Strait, Malaysia (NHM20090290). A, external view of the right shell valve, B, external view of the left shell valve. C, internal view of the right shell valve D, internal view of the left shell valve.

486 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Material examined. – Type not studied. The type material is Description. – Shell of moderate size, up to 50 mm in height, probably in the University Museum, Uppsala, Sweden. 40 mm in length and 4 mm in width. Outline subquadrate, attenuated dorsally. Shell laterally compressed, generally Voucher: [NHM]20090290, Johor Strait, Malaysia, coll. K. S. Tan, in one plane. Right valve smaller and closely fi tting within Nov.2004, dry shells of three individuals. the margin of the left valve. Right valve smooth, with

the outer shell layer continuous and having few growth Description. – Shell height up to ~60 mm, outline variable increments. Little shell erosion and few encrustations. with usually spatulate to oval individuals. Attachment area Exterior cream to yellowish, usually with dark lavender of left valve depending on substratum type. Both valves irregular rays. Left valve usually either light or white, concave with left valve more deeply cupped and hence with between 6–10 low, widely-spaced ribs which may with a deep umbonal cavity. Both valves with dichotomous have obsolete hyote spines at some growth increments. radial ribs from the umbo; the tops of the ribs well-rounded, Attachment area small and restricted to near the left umbo. and radial ribs with growth squamae recognisable on Most specimens are attached to shells of other bivalves both valves. Older part of the right valve, i.e., the dorsal and gastropods. Some are unattached. Chomata small, surface, usually eroded. Wavy plications along the shell uniform, closely-spaced and in straight lines along the margins refl ect the positions and height of the ribs. No anterior and posterior margins near the hinge. Hinge line chomata. Adductor muscle scar reniform, antero-dorsal straight and short. Marginal commissural shelf on the left border concave and close to the postero-ventral shell margin valve wide and fl at with a well-defi ned inner edge. Interior from the valve centre. External coloration of both valves of the shell white with a pearly nacre. Chalky deposits is variable from white and light purple with deep purple prominent on the commissural shelf of the left valve only. lines radiating from the umbo. Internally, shell white with Adductor muscle scar white, large and elongate, positioned patches of chalky deposits and hollow chambers. Muscle approximately at the middle of the shell, slightly towards scar colourless with occasional purple growth lines. the posterior. Distribution and habitat. – Distribution of native Crasssotrea Distribution and habitat. – Indo-West Pacific, the gigas includes Japan, Korea, maritime districts of Russia Philippines, Taiwan, Thailand, North Borneo, South and and the Yellow Sea of China. Mariculture stocks occur in East China Seas, Yellow Sea, Shandong Province, China British Columbia to California, Hawaii, Guandong Province to Honshu, Japan, Townsville, Queensland, Australia, in China, Tasmania, New Zealand and Brazil (Inaba & Mauritius, Intertidal zone to -10 m on rocks and corals. Torigoe, 2004). Remarks. – Harry (1985) proposed a new genus, Planostrea, Remarks. – Morphological variations in shell form occur exclusively for Ostrea pestigris. This genus is described among individuals occupying different substrata. Growth as of moderate size (to 75 mm), very compressed in form of the shell can be cup-shaped with a deep umbonal one plane, being non-lamellose and with a continuous cavity, transversely fl attened with a large attachment area outer shell layer. Well-developed chomata line up along on the left valve or dorso-ventrally elongated in mud grown the dorsal margins near the hinge, with a wide and fl at individuals (Lam, 2003). marginal commissural shelf and a lavender outer surface with radial stripes. This species can be distinguished easily from other oysters because of the consistent shape Planostrea Harry, 1985 of a smooth, fl attened, circular disc. Unlike other oysters, it is usually free from encrustations and the influence Planostrea pestigris (Hanley, 1846) of the substratum to which it is attached. This species Common name: Flat oyster (Fig. 4) can be distinguished from Ostrea densellamellosa and Alectryonella plicatula by having a smooth and straight Ostrea pestigris Hanley, 1846: 106–107. Ostrea paulucciae Crosse, 1869: 188. shell margin. The latter two have crenulated shell margins. Ostrea palmipes Sowerby, 1871, sp. 56, Fig. a–c. It is also different from Hyotissa numisma in having a Planostrea pestigris – Harry, 1985: 143, Fig. 22. white interior instead of a violet one and in lacking the Ostrea pestigris – Morris, 1985: 129, Pl. 4A–D; Scott, 1994: 69, vesicular microstructure of gryphaeids. This species has Pl. 5B. been synonymised with Ostrea paulucciae Crosse, 1869, and Ostrea palmipes Sowerby, 1871, on the basis of Material examined. – Holotype: [USNM] 666809, ‘‘Isle of Luzon; similar shell characters (Tchang & Lou, 1956). Therefore, on rocks’’, coll. H. Cumming, no date, dry shell, height, 75 mm. the O. palmipes from Malaysia as identifi ed by Morris & Purchon (1981) is actually Planostrea pestigris. Syntype of Ostrea palmipes: [NHM] 1907.10.28.77 & 1907.12.30.10–11, one dry shell no other data.

Voucher – [NHM] 20090291, Pelangi Beach, intertidal sand, Pulau Langkawi, Malaysia, coll. B. Morton, 4 Feb.2004, one individual preserved in alcohol.

487 Lam & Morton: Oysters from Malaysia and Singapore

Dendostrea Swainson, 1835 Ostrea (Pretostrea) bresia Iredale, 1939: 396–397. Lopha folium – Stenzel, 1971: N1157, Fig. J47. Dendostrea folium (Linnaeus, 1758) Common name: Foliate oyster (Fig. 5) Material examined. – Type not studied. The type material is in the University Museum, Uppsala, Sweden. This species is not represented in the Linnaean collection of the Linnean Society of Ostrea folium Linnaeus, 1758: 699. London. Ostrea folium – Born, 1780: 112; Dodge, 1952: 190–191. Dendostrea glaucina Lamarck, 1819: 212. Voucher: [NHM] 20090292, “Dredged from off Pelangi Beach, Dendostrea folium – Swainson 1835: 39. ~2–3 m, Pulau Langkawi, Malaysia”, coll. B. Morton, 7 Feb.2004, Dendostrea folium – Sowerby 1839: 137: Fig. 181, Iredale, 1939: six individuals preserved in alcohol. 402, Pl. 7, Fig. 11; Torigoe 1981: 315–316, 336–337, Pl. 5, Fig. 2, Pl. 26; Harry, 1985: 137–138, Fig. 18; Carriker & Gaffney, 1996: 8; Lam, 2003: 113–114, Pl. 14. Description. – Shell of medium size, up to 55 mm in height, 30 in length and 10 in width. Outline oval, subequivalve.

Fig. 4. Planostrea pestigris (Hanley, 1846) from Pulau Langkawi, Malaysia (NHM20090291). A, external view of the right shell valve, B, external view of the left shell valve, C, internal view of the right shell valve and D, internal view of the left shellvalve.

488 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 5. Dendostrea folium (Linnaeus, 1758) from Pulau Langkawi, Malaysia (NHM20090292). A, external view of the right shell valve, B, external view of the left shell valve, C, anterior view of an individual, showing the “graspers” developed to hold on to a Modiolus micropterus shell, D, internal view of the right shell valve and E, internal view of the left shell valve.

489 Lam & Morton: Oysters from Malaysia and Singapore

Right valve lilac to dark purple externally, left valve white Hyotissa hyotis forma imbricata – Stenzel, 1971: N961 & N1026, with thin purple stripes. Both valves with dichotomous Fig. J5 & J49. ribs radiating from the umbones and ending ventrally as Hyotissa hyotis imbricata – Habe & Okutani, 1975: 195. either a zig-zagged or rounded undulating margin. Rib tops Parahyotissa imbricata – Harry, 1985: 130. rounded and bearing obsolete hyote spines at some growth Material examined. – Type not studied. Probably in the Geneva, increments. Reddish-purple streaks may radiate from the Switzerland Museum. umbones. Usually, growth squamae on both valves eroded and shell thus often smooth. Attachment area of the left Voucher: [NHM] 20090293, “Dredged from off Pelangi Beach, valve extending halfway from the umbo to the ventral ~2–3 m, Pulau Langkawi, Malaysia”, coll. B. Morton, 7 Feb.2004, margin. Right valve convex left valve attached to hard two individuals preserved in alcohol. substratum with “claspers”, which are shelly processes that clasp the twig-like substratum (Stenzel, 1971). Description. – Shell semicircular or orbicular, up to 45 mm in height, 50 mm in length and 15 mm in width, equivalve. Commissural shelf not developed. Umbonal cavity shallow, Hinge line long and straight and approximately equal to ligament short. Chomata usually either not present or shell length in smaller individuals. Shell relatively thin restricted to both sides of the ligament and to half the shell and light in smaller individuals but becoming thicker and height as small elongate tubercles and corresponding pits. heavier in larger ones. Both valves with dichotomous ribs Interior of the shell lustrous white with iridescent bluish bearing prominent growth squamae that increase in length green patches particularly along ridges formed by the ribs. to become hyote spines. In eroded individuals hyote spines Adductor muscle scar either reniform or crescentric and obsolete but growth squamae still prominent at the newly- the same colour as the interior of the shell. It is positioned grown ventral margin. Attachment area from small and posterior to the centre of the pallial region. limited at the umbones, to large and encompassing the entire left valve. Shell margins of both valves undulate, fi tting into Distribution and Habitat. – Indo-West Pacifi c, Australia, each other and, thus, refl ecting the positions of the radial the Philippines, South and East China Seas, Hainan, Taiwan ribs. External coloration of both valves from white to cream to Kii Penisula, Japan. Usually shallow, from the sublittoral in younger individuals to pink and purple with dark purple fringe to 8–10 m; it might extend to 50 m on rocks. bands in older ones. Shell interior white. Commissural shelf Attached to other living sessile bivalves. The specimens large, dull in texture because of the vesicular shell structure. collected were attached to the mussel Modiolus micropterus Ligament short, ligamental area usually not elongate. Deshayes, 1836 (Fig. 4). Umbonal cavity shallow, chomata absent. Adductor muscle scar large, white or pink, approximately circular and Remarks. – Sometimes, species of Hyotissa may be positioned postero-dorsally from the centre of the valve. confused with Dendostrea folium especially in terms of external shell characters. Internal shell characters are Distribution and habitat. – An Indo-West Pacifi c species, more reliable in distinguishing these two species. For occurring from the Philippines, Australia and South China example, the shape of the adductor muscle scar is the Sea to the Boso Peninsula, Japan. This subtidal species is most important feature for identifi cation: that of Hyotissa usually obtained by trawling and diving (Lam & Morton, is large and circular while that of Dendostrea folium is 2004). crescentric. Species of Hyotissa also have a well-developed commissural shelf and are whitish internally whereas Remarks. – Morris & Purchon (1981) recorded two Dendostrea does not have an obvious commissural shelf gryphaeids, Hyotissa hyotis (Linnaeus, 1758) and Hyotissa and internally the basal whiteness is always patterned with numisma (Lamarck, 1819) by trawling off the West coast dark yellowish green patches showing the position of radial of Malaysia. Our collected Hyotissa is distinguished from rays. The gryphaeid vesicular microstructure also readily these two in having an irregular and rounded shell margin, distinguishes Hyotissa. crenulations and a white shell interior. Hyotissa hyotis has regular, strong and acute shell margin crenulations and H. numisma has white shell exterior and slightly violet or Gryphaeidae Vyalov, 1936 largely white interior.

Pycnodonteinae Stenzel, 1959 DISCUSSION Hyotissa Stenzel, 1971 Several checklists of oysters are available for various areas Hyotissa imbricata (Lamarck, 1819) of South East Asia and Australia. Twenty-two species Common name: Imbricated oyster (Fig. 6) of Ostreidae and Gryphaeidae have been recorded from (subtropical) Japan (Torigoe, 1981), 13 from Korea (Qi Ostrea imbricata Lamarck, 1819: 213. & Choe, 2000), 12 from Hong Kong (Lam & Morton, Ostraea imbricata – Sowerby, 1871, sp. 36, Pl. 17, Fig. 36 a, b. 2004), nine from Thailand (Yoosukh & Duangdee, 1999) Dendostrea imbricata – Habe, 1951: 93. and 11 from Australia (Thomson, 1954). Tsi et al. (1983) Pretostrea imbricata – Habe & Kosuge, 1967: 138, Pl. 51, Fig. records a total of 17 oyster species from the South China 14.

490 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Sea but, conversely, Tomascik et al. (1997) identifi es only recorded from Malaysia and Singapore plus an introduced Crassostrea gigas as present in Indonesian mangroves, and, mariculture species typically identified as ‘Crassostrea as noted earlier, Tan & Kastoro (2004) identifi ed no oysters gigas’. The name Crassostrea gigas was commonly from the Anambas and Natuna Islands, located between given to the cultivated oyster in Hong Kong until Lam & the West Malaysian Peninsula and Borneo. This study Morton (2003) identifi ed it genetically as a new species identifi es nine species of oysters from peninsular Malaysia, – Crassostrea hongkongensis. It is therefore possible that although the two species of Hyotissa reported upon by the species of Crassostrea identifi ed from cultivation areas Morris & Purchon (1981) were actually collected from in Malaysia may not be C. gigas and this requires study. Phuket (Thailand) and from more northerly latitudes on the east coast of peninsular Malaysia (Table 2). Similarly, The number of species recorded in the present study is although Saccostrea cuccullata and its morphotype S. similar to that recorded from Thailand by Yoosukh & echinata plus the similarly rocky intertidal Alectryonella Duangdee (1999) except there is a difference in species plicata were recorded by Morris & Purchon (1981) from composition. Oysters present in Thailand but not in both coasts of peninsular Malaysia and Singapore, Ostrea Peninsula Malaysia include Crassostrea iredalei (Faustino, palmipes (= Planostrea pestigris) was only recorded 1932), Striostrea (Parastriostrea) mytiloides (Lamarck, from the west coast as reported herein. Similarly, we also 1819), Lopha cristagalli (Linnaeus, 1758) and the cultured herein identify Saccostrea mordax, Dendostrea folium and Crassostrea belcheri (Sowerby, 1871) (not C. gigas). The Hyotissa imbricata as new records from the west coast of so-called S. cuccullata fi gured as a second specimen in peninsular Malaysia. Thus, a total of nine oyster species are Yoosukh & Duangdee (1999, Fig. 6) is in fact Saccostrea

Fig. 6. Hyotissa imbricata (Lamarck, 1819) from Pulau Langkawi, Malaysia (NHM20090293). A, external view of the right shell valve, B, external view of the left shell valve, C, internal view of the right shell valve and D, internal view of the left shell valve.

491 Lam & Morton: Oysters from Malaysia and Singapore

Table 2. A list of oysters recorded from Malaysia and Singapore. Taxa in bold are treated in the present study.

Taxa Localities Recorded / Collected Reference Remarks (detailed as possible) by whom and when

Family Ostreidae

Saccostrea cuccullata East and West coast C. Nielson, 1976 Morris & Purchon, This species has been identifi ed from (Born, 1778) of Malaysia, and R. D. Purchon 1981 Malaysian rocky shores and West Singapore waters Malaysian mangroves by Berry Tanah Merah and B. Morton, Lam & Morton, (1964, 1972) and Sasekumar (1974) as Kallang River, 9 Jul.2001 2006 either Crassostrea cuccullata or Ostrea Singapore cuccullata. Crassostrea cuccullata and an unidentifi ed Ostrea sp. occur on rocky Pulau Langkawi, B. Morton, This study Enoch, 1954). Also regarded as S. echinata Malaysia 3 & 5 Feb.2004 by Morris and Purchon (1981).

Saccostrea mordax Pulau Langkawi, B. Morton This study (Gould, 1850) Malaysia 4 Feb.2004

Crassostrea gigas Malaysia Mathias & Charles, As introduced species to Malaysia (Thünberg, 1793) 1978 for mariculture Zulgigar & Tan, 1998 Johor Strait, Tan Koh Siang This study Grown-out from spat fl own from hatcheries Malaysia November 2005 in Australia Singapore Tan & Chou, 2000

Planostrea pestigris West coast of R. D. Purchon Morris & Purchon, This species was identifi ed as Ostrea (Hanley, 1846) Malaysia 1981 palmipes from Malaysia by Morris and Purchon (1981). Pulau Langkawi, B. Morton, This study Malaysia 4 Feb.2004

Dendostrea folium Pulau Langkawi, B. Morton, This study (Linnaeus, 1758) Malaysia 7 Feb.2004

Alectryonella East and West C. Nielson, 1976 Morris & Purchon, plicatula (Gmelin, coasts of Malaysia, and R. D. Purchon 1981 1791) Singapore

?Ostrea West coast of D. Broome Morris & denselamellosa Malaysia Purchon, 1981 Lischke, 1869

Family Gryphaeidae

Hyotissa imbricata Pulau Langkawi, B. Morton This study (Lamarck, 1819) Malaysia 7 Feb.2004

Hyotissa hyotis East and West C. Nielson, 1976 Morris & Purchon, (Linnaeus, 1758) coasts of Malaysia and R. D. Purchon 1981

Parahyotissa West coast of R. D. Purchon Morris & Purchon, This species was regarded as Hyotissa numisma Malaysia 1981 numisma (Lamarck, 1819)

mordax. The fi gured Saccostrea forskalii (Gmelin, 1791) coastal waters of Peninsula Malaysia (but including in the same paper also conforms to the description of southern Thailand) are thus now known to possess Saccostrea cuccullata. 13 species of oyster. These are: Crassostrea belcheri, Crassostrea iredalei, Crassostrea gigas, Saccostrea On the other hand, Alectryonella plicatula, Planostrea cuccullata, Striostrea mytiloides, Alectryonella plicatula, pestigris, Ostrea denselamellosa, Hyotissa are recorded Planostrea pestigris, Ostrea denselamellosa, Lopha from Malaysia but not Thailand. The intertidal and shallow cristagalli, Dendostrea folium, Hyotissa hyotis, Hyotissa

492 THE RAFFLES BULLETIN OF ZOOLOGY 2009 numisma and Hyotissa imbricata. However, the three Born, I., 1780. Testacea Musei Caesarei Vindobonensis. Sumptibus species of Crassostrea need closer study not only to Joannis Pauli Kraus, Vindobonae, Vienna. 458 pp. ascertain true identities and hence species numbers, but Carriker, M. R. & P. M. Gaffney, 1996. A catalogue of selected also to assist in the management genetics of maricultural species of living oysters (Ostreacea) of the world. In: Kennedy, stocks. Notwithstanding, species numbers recorded from V. S., R. I. E. Newell & A. F. Eble (eds.), The Eastern Oyster the West Malaysian Peninsula approximate those recorded Crassostrea virginica. Maryland Sea Grant College, Maryland. from elsewhere in Southeast Asia. Pp. 1–18. Crosse, H., 1869. Diagnoses molluscorum novorum. Journal de Conchyliologie, 17 (3e serie, Tome 9): 183–188. KEY FOR IDENTIFICATION OF OYSTERS Deshayes, G. P., 1836. Histoire naturelle des animaux sans FROM MALAYSIA AND SINGAPORE vertebras. Deuxiemme edition, revue et augmente des notes. Paris 11: 580 pp. 1. Shell smooth, outline subquadrate, laterally compressed in one Dodge, H., 1952. A historical review of the mollusks of Linnaeus, plane ...... Planostrea pestigris Part 1, The Classes Loricata and Pelecypoda. Bulletin of the – Not so ...... 2 American Museum of Natural History, 100: 1–264. 2. Fingerprint shell structure on the internal face of the valves Dollfus, G. F. & P. Dautzenberg, 1920. Conchyliogie du Miocène ...... Alectryonella plicatula moyen du bassin de la Loire, pt. 1: Pélécypodes (Suite et fi n). – Not so ...... 3 Paleontologie, 22: 379–500. 3. Alternative conchiolin and calcareous layers make up shell and presence of chomata ...... 4 Faustino, L. A., 1932. Recent and fossil shells from the Philippine – Not so ...... 5 Islands. The Philippine Journal of Science, 49: 543–551. 4. Radiating ridges on RV, evenly crenulated m-shaped ventral Férussac, A. E., 1822. Tableaux systématiques des animaux margin ...... Saccostrea cuccullata mollusques classés en familles naturelles. A. Bertrand, Paris. – Not so ...... Saccostrea mordax 184 pp. 5. Shell exterior dark purple, interior lustrous brown or green. LV sometimes with claspers ...... Dendostrea folium Gmelin, J. F., 1791. Caroli a Linné Systema naturae per regna – Not so ...... 6 tria naturae. Editio 13. Volume 1. Part 6. G. E. Beer, Leipzig. 6. Vesicular shell structure in shell interior ...... 7 Pp. 3021–3910. – Not so ...... 9 Gould, A. A., 1850. Shells of the United States Exploring 7. Shell margin with strong, acute plication ..... Hyotissa hyotis Expedition. Proceedings of the Boston Society of Natural – Not so ...... 8 History, 3: 343–348. 8. Tops of dichotomous radial ribs rounded or bear prominent Habe, T., 1951. Genera of Japanese Shells. Kairui-bunken- growth squamae which becomes hyote spines ...... kankokai, Kyoto, Japan. (S. 1–186, 1951; 187–278, 1952; ...... Hyotissa imbricata 281–326, 1953) [in Japanese]. – Not so ...... Parahyotissa numisma 9. RV covered concentrically by many dense layers of fragile Habe, T. & S. Kosuge, 1967. Shells of the world in colour, II The growth squamae, Shell margin fi nely crenulated ...... tropical Pacifi c. Hoikusha, Osaka. 194 pp...... Ostrea denselamellosa Habe, T. & T. Okutani, 1975. Mollusca II. Gakken, Tokyo. 294 – Not so ...... Crassostrea gigas pp. Hanley, S., 1846. A description of new species of Ostrea, in the collection of H. Cuming, Esq. Proceedings of the Zoological ACKNOWLEDGEMENTS Society of London, 13: 105–107. Harry, H. W., 1985. Synopsis of the supraspecifi c classifi cation We would like to thank Tan Koh Siang, Gustav Paulay, of living oysters (Bivalvia: Gryphaeidae and Ostreidae). The and anonymous reviewers for their comments on the drafts Veliger, 28: 121–158. of the manuscript. Tan Koh Siang is also thanked for the Hirase, S. 1930. On the classifi cation of Japanese oysters. Japanese collection of Crassostrea gigas specimens from Malaysia. Journal of Zoology, 3: 1–65. Inaba, A. & Torigoe, K. 2004. Oysters in the world. Part 2. Systematic description of the recent oysters. Bulletin of the LITERATURE CITED Nishinomiya Shell Museum, 3: 1–63.

Awati, P. R. & H. S. Rai, 1931. The Indian Zoological Memoirs Iredale, T., 1939. Mollusca. In: Iredale, T. (ed.), Great Barrier Reef on Indian Animal Types: III Ostrea cucullata (The Bombay Expedition 1928–1929, Scientifi c Reports 5(6), Part I. British Oyster). Methodist Publishing House, Lucknow. 107 pp. Museum (Natural History), London. Pp. 211–425. Berry, A. J., 1964. The natural history of the shore fauna of North Iredale, T. & T.C. Roughley, 1933. The scientifi c name of the Penang. Malayan Nature Journal, 18: 81–103. commercial oyster of New South Wales. Proceedings of the Linnean Society of New South Wales, 58: 278. Berry, A. J., 1972. The natural history of West Malaysian mangrove faunas. Malayan Nature Journal, 25: 135–162. Lam, K., 2003. Morphological variations in oyster shell form (Bivalvia: Ostreidae): phenotypic plasticity identified by Born, I., 1778. Index Rerum Naturalium Musei Caesarei genotypic analysis. In: Shin, P. (ed.), Turning the tides, a Vindobonensis, pars prima, Testacea. Ex Offi cina Krausiana, festschrift in honour of Professor Brian Morton. The Marine Vindobonae, Vienna. 442 pp. Biological Association of Hong Kong, Hong Kong. Pp. 103–133.

493 Lam & Morton: Oysters from Malaysia and Singapore

Lam, K. & B. Morton, 2003. Mitochondrial DNA and morphological Schrenck, L. von, 1867. Mollusken des AmurLandes und des identification of a new species of Crassostrea (Bivalvia: Nordjapanischen Meeres. Reisen ünd Forschungen im Amur- Ostreidae) cultured for centuries in the Pearl River Delta, Hong Lande in den Jahren 1854–1856, 2: 259–974. Kong, China. Aquaculture, 228: 1–13. Scott, P. V., 1994. Bivalve molluscs from the southeastern waters Lam, K. & B. Morton, 2004. The oysters of Hong Kong. (Bivalvia: of Hong Kong. In: Morton, B. (ed.), The malacofauna of Ostreidae and Gryphaeidae). The Raffl es Bulletin of Zoology, Hong Kong and Southern China III. Proceedings of the third 52(1): 11–28. international workshop on the malacofauna of Hong Kong and Lam, K & B. Morton, 2006. Morphological and mitochondrial- Southern China, Hong Kong 1992. Hong Kong University Press, DNA analysis of the Indo-West Pacifi c rock oysters (Ostreidae: Hong Kong. Pp. 55–100. Saccostrea species). Journal of Molluscan Studies, 72(3): Sowerby, G. B., 1839. A Conchological Manual. G. B. Sowerby, 235–245. London. 313 pp. Lamarck, J. B. P. de M., 1819. Histoire naturelle des animaux Sowerby, G. B., 1871. Conchologia Iconica. Volume 18. Ostrea. sans vertebres. Suite des conchiferes. Chez L’Auteur, Paris. L. Reeve & Co, London. 258 pp. Stenzel, H. B. 1959. Cretaceous oysters of southwestern North Lamprell, K. & J. Healy, 1998. Bivalves of Australia. Volume 2. America. International Geological Congress, Mexico City, Leiden: Backhuys Publishers. 1956. El Sistema Cretacico, 1: 15–37. Lamy, E., 1929. Revision des Ostrea vivants du Museum National Stenzel, H. B., 1971. Treatise on invertebrate paleontology. In: d’Histoire Naturelle de Paris. Journal de Conchyliologie, 7: Moore, R. C. & C. Teichert (eds.), Part N. Mollusca 6, Bivalvia. 1–46, 71–108, 133–168, 233–275. Volume 3(of 3) – Oysters. Geological Society of America Inc. Linnaeus, C., 1758. Systema Naturae per regna tria naturae, and the University of Kansas Press, Lawrence, Kansas. Pp. secundum classes, ordines, genera, species cum characteribus, N953–N1224. differentiis, synonymis, locis. Tomus I. editio 10, reformata. Swainson, W., 1835. The elements of modern conchology briefl y and Laurentii Salvii, Holmiae, Stockholm. 824 pp. plainly stated, for the use of students and travellers. Baldwin Lischke, C. E., 1869–1874. Japanische Meeres-Conchylien. Ein and Craddock, London. 62 pp. Beitrag zur Kenntnis der Mollusken mit besonderer Tan, K. S. & L. M. Chou, 2000. A Guide to Common Seashells of Rücksicht auf die geographische Verbreitung derselben. Vol. Singapore. Singapore Science Centre, Singapore. 168 pp. 1, 192 pp., 14 pls., 1869; Vol. 2, 184 pp., 14 pls., 1871; Vol. Tan, K. S. & W. W. Kastoro, 2004. A small collection of gastropods 3, 123 pp, 9 pls., 1874, Theodor Fischer, Kassel. and bivalves from the Anambas and Natuna Islands, South Mathias, J. A. & J. K. Charles, 1978. Mangroves, In: Chua, T. China Sea. The Raffl es Bulletin of Zoology, 11(Supplement): E. & J. A. Mathias (eds.), Coastal resources of West Sabah: 47–54. a preliminary investigation in relation to oil spill. Penerbit Tchang, S. & T. Lou, 1956. A study on Chinese oysters. Acta Universiti Sains Malaysia, Pulau Pinang. Pp. 259–261. Zoologica Sinica, 8(1): 65–94. Morris, S., 1985. Preliminary guide to the oysters of Hong Kong. Thomson, J. M., 1954. The genera of oysters and the Australian Asian Marine Biology, 2: 119–138. species. Australian Journal of Marine and Freshwater Research, Morris, S. & R. D. Purchon, 1981. The marine shelled Mollusca 5: 132–168. of West Malaysia and Singapore, Part 3, Bivalvia. Journal of Thünberg, C. P., 1793. Tekning och Beskifning pa en ostronsort Molluscan Studies, 47: 322–327. ifram Japon. Kongliga Svenska Vetenskaps Akademiens Nya Purchon, R. D. & I. Enoch 1954. Zonation of the marine fauna and Handlingar, 14: 140–142. fl ora on a rocky shore near Singapore. Bulletin of the Raffl es Tomascik, T., A. J. Mah, A Nontji & M. K. Moosa, 1997. The Museum, Singapore, 25: 47–65. Ecology of the Indonesian Seas. Periplus Editions, Hong Kong. Qi, H. & B. L. Choe, 2000. Five unrecorded ostreacean species 1388 pp. (Mollusca, Bivalvia) from Korean waters. The Korean Journal Torigoe, K., 1981. Oysters in Japan. Journal of Science-Hiroshima of Systematic Zoology, 16(2): 133–140. University Series B Division 1, 29: 291–481. Quoy, J. R. C. & J. P. Gaimard, 1835. Voyage de découvertes de Tsi, C. Y., X. T. Ma, Z. K. Lou & F. S. Zhang, 1983. Illustrations l’Astrolabe exècuté par ordre du Roi pendant les années 1826– of the fauna of China (Mollusca). Volume 2. Science Press, 1827–1828–1829, sous le commandment de M.J. Dumont Beijing. 274 pp. (In Chinese). D’Urville Zoologie. Tome 3 (part I). Tastu, Paris. Vyalov, P. O. S., 1936. Sur la classifi cation des huitres. Comptes Rafinesque, C. S., 1815. Analyse de la nature ou tableau de Rendus (Doklady) de l’Aadémie des Sciences de l’URSS, 4: l’univers et des corps organisés. Le nature es mon guide, et 17–20. Linnéus mon maître. Privately published, Palermo. 224 pp. Yoosukh, W. & T. Duangdee, 1999. Living oysters in Thailand. Sacco, F., 1897. Pelecypoda (Ostreidae, Anomiidae e Dimyidae) Phuket Marine Biological Center Special Publication, 19: of L. Bellardi & Federico Sacco, 1872–1904, I molluschi dei 363–370. terreni Terziarii de Piemonte e della Liguria. Carlo Clausen, Torino. 66 pp. Zulfi gar, Y. & S. H. A. Tan, 1998. A review of oyster culture in Malaysia. In: The 6th Asian Fisheries Forum. Asian Fisheries Sasekumar, A., 1974. Distribution of macrofauna on a Malayan Society. Pp. 168–170. mangrove shore. Journal of Animal Ecology, 43: 51–69. Schrenck, L. von, 1861. Vorläufige Dia gnosen einiger neuer Molluskenarten aus der Meerenge der Tartarei und dem Nordjapanischen Meere. Bulletin de l’Académie Imperiale des Sciences de St Pétersbourg, 4: 408–413.

494 THE RAFFLES BULLETIN OF ZOOLOGY 2009

THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 495–500 Date of Publication: 31 Aug.2009 © National University of Singapore

AITENG ATER, NEW GENUS, NEW SPECIES, AN AMPHIBIOUS AND INSECTIVOROUS SEA SLUG THAT IS DIFFICULT TO CLASSIFY [MOLLUSCA: GASTROPODA: OPISTHOBRANCHIA: SACOGLOSSA(?): AITENGIDAE, NEW FAMILY]

Cornelis (Kees) Swennen & Somsak Buatip Faculty of Science and Technology, Prince of Songkla University, Pattani 94000, Thailand Email: [email protected]

ABSTRACT. – Aiteng, new genus, shows characteristics of both Cephalaspidea and Acochlidea (pre- pharyngeal nerve ring) and Sacoglossa (pharynx, radula uniseriate, one tooth functional). As no family could be identifi ed, the Aitengidae, new family, has been erected. It is placed in the Sacoglossa with which it has most characters in common. The type species is Aiteng ater, new species, a small, inconspicuous, grey to blackish opisthobranchs without shell, rhinophores, gills or other protuberances. The large eyes are lateral in uncoloured fi elds. The notum has wide free borders along the sides and posterior part. The head is extending, but can largely be retracted under the notum. The pharynx is large and the radular ribbon has tens of uniserial teeth in both ascending and descending limbs with one functional tooth in front of the pharynx. The teeth are triangular with a wide base, a strong central cusp and small denticles along sides. The salivary ducts are vesicular, the salivary glands consist of several tens of separate follicles. The main branch of the digestive gland runs from the small stomach posteriorly via the upper part of body branching off laterally and covering a large area with pale vessels that have small grey follicles in the upper part of the body except over the renopericardium. Dorsal vessels run just under the skin between the renopericardium and the border of the notum. Tens of hermaphrodite follicles are in the posterior part of the body. The penis is slender, unarmed. The prostate around the internal vas deferens above the pharynx. The female opening is in the right side close to the anus. Aiteng ater, new species, occurs on the solid mud bottom of dense mangrove forests in the Pak Phanang Bay, Gulf of Thailand. The specimens live amphibiously in and around small pools high in the intertidal zone, only covered by the sea during spring high tides. The slugs reach a length of 8-12 mm and feed on insect larvae and pupae.

KEY WORDS. – Gastropoda, Opisthobranchia, Sacoglossa, Aitengidae new family, Aiteng new genus, Mangrove, Thailand.

INTRODUCTION MATERIALS AND METHODS

Blackish slugs with a wide body and a length of about 10 Details about locality, dates, and numbers are given in mm were discovered on the mud and in small pools in a Materials examined in the chapter Taxonomy. Specimens mangrove forest in the Pak Phanang Bay (Gulf of Thailand). were picked up with a small spoon from the mud. At the When noting that they had a notum with a wide free border, same time a part of the mud surface was taken up to a the slugs were believed to be young specimens of the family depth 20 mm and stored in a plastic box. Substrate and the Onchidiidae. That idea was rejected when the expanded slugs were transported to the lab. A number of individuals head showed no stalked eyes, but internal eyes like those of were narcotised with MgCl2 and stored in a formaldehyde the sacoglossan Limapontia spp. After leaving the mosquito seawater solution. Some were set aside and after a few saturated mangrove forest for taking a better view in the days transferred into 70% ethanol, and others were used lab, it appeared that the species could not be allocated to for dissection in a Petri dish with a black wax layer on the any family known to the authors. Therefore, the slugs were bottom. Dissections were done by hand with the help of fi ne studied in more detail. As no description of a family, genus, needles under a 4-64x stereo microscope. Notes, drawings, or species was found of which the characteristics fi t with and photos were made of details at different stages of our slugs, the family, genus, and species are described as dissection. Live specimens were kept for six months in their new in this paper. closed box of 200 x 300 mm with the substrate on which

495 Swennen & Buatip: Aiteng ater, new genus and species they were collected, but regularly provided with food. The Dozens of individuals of similar size were found at the same site mud surface remained irregular. In this way only a part of on 3 Oct.2007. Two individuals in the same size range and two the substrate was submerged like it was in the fi eld. The juveniles of 2.0 mm and 2.1 mm were found at the same site on slugs were frequently observed, on some days also at night. 13 Apr.2008, and about 50 specimens varying in length between Some feeding tests were conducted. 4 and 12 mm on 4 Oct.2008. The description is based on 17 specimens, eight of which were dissected. The holotype and three paratypes are deposited in the Zoological Reference Collection (ZRC) of the Raffl es Museum of Biodiversity Research, National TAXONOMY University of Singapore, and three paratypes in the Zoological Museum, University of Amsterdam (ZMA).

Aitengidae, new family Live colouration. – Dorsum grey to black, area around eyes not pigmented (Figs. 1B,C, 2A,C). Upper foot border, lateral None of the known families of the Cephalaspidea, Sacoglossa body sides, and underside notum rim grey. Foot sole grey and other opisthobranch orders fi t with the characters of or not pigmented. Aiteng, new genus, described below. Therefore, we create the monogeneric Aitengidae, new family, with the same External morphology. – Broad, smooth slugs, length 2.5 characters as the genus. to 3 times width in creeping specimens (Fig. 1B,C). Body covered by notum with wide free border overhanging foot, but without tentacles, rhinophores, gills, cerata, tubercles Aiteng, new genus or other protuberances (Figs. 1B,C,D, 2A,B,C). Head with velum and sideward directed eyes under low crests (Figs. Diagnosis. – Non-shelled opisthobranchs, body dorso- 1D, 2C). Head can be retracted under frontal notum border. ventrally flattened, notum with wide free border under Foot sole over whole length divided by deep groove, often which head can be retracted. Cerata, gills, rhinophores, and kept partly or wholly closed (Fig. 2B). Frontal foot corners tentacles lacking. Ganglionic nerve ring pre-pharyngeal. not extended, rounded, anterior border smoothly curved, Pharynx large, radula uniseriate, both ascending and posterior tip rounded, usually not passing notum border, but descending limbs with several tens of teeth, one functional notum can contract making foot border visible all around. tooth. Single major branch of digestive gland from simple Frontal borders of velum and foot rarely show slight notch. stomach to posterior part, widely branching off laterally. No clear renopericardial bulb. Renopore not located. Male Male aperture under right eye. Female opening on right aperture under right eye, female aperture opens besides anus body wall beside anus. in ventral side of notum rim against anterior right lateral body wall (Fig. 2C). Type species. – Aiteng ater, new species, described in this paper from Pak Phanang Bay, Gulf of Thailand. Gender: Internal characteristics. – Nervous system with four pre- masculine. pharyngeal ganglia. Eyes well developed, diameter 125–135 µm, length 180–220 µm, lens spherical (Fig. 1K). Eyes Etymology. – The name is derived from Ai Theng, which nearly sitting on cerebro pleural ganglion (Fig. 1E). Pharynx is the name of one of the popular puppets in shadow plays yellowish (length 900–1330 µm, height 780–875 µm in 8-11 (wayang) in the southern part of Thailand. It is a jolly, mm long specimens) voluminous ascus slightly diverging smooth, black, male, who plays in the night. Statues and left. Radula uniseriate, one functional tooth; 30–34 teeth in drawings of various famous puppets were seen along straight ascending limb, 29–33 teeth in curved descending the roads in the area during our visits. The smooth Ai limb, some small, broken teeth in ascus (Fig. 2F). Teeth Theng with his large lateral eyes did remind us of the just triangular (height 70–84 µm) with strong median cusp discovered slug (Fig. 1A). and 6–10 small denticles along lateral border (Figs.1M, 2H). Teeth in descending limb smaller, by clearly worn cusps. Two large, joined oral glands along ventral side of DISCUSSION AITENGIDAE AND AITENG pharynx. Salivary duct ampullar, curved, laterally entering pharynx (Fig. 2D). Salivary glands consisting of tens of The new family has been placed in the Sacoglossa, with loose, irregularly shaped follicles. (Fig. 1I). Oesophagus a question mark, based on several characters (see the short, dark-coloured, from posterior dorsal side of pharynx discussion of the species below). to simple stomach. Intestine dark pigmented, from anterior right side of stomach to anus. Major branch of digestive gland posteriorly from stomach, sending off side branches Aiteng ater, new species that branch several times forming fi ne network up into free (Figs. 1–2) border of notum; branches pale (Figs. 1F, 2D). Small, dark speckled, digestive follicles on dorsal side of branches Materials examined. – Seven individuals with lengths varying (Fig. 1G), covering whole notum under skin, absent above from 6 to 10 mm were found by the authors in the Pak Phanang pericardium. Renopericardium mid-frontal under dorsal skin Bay, in the mangrove forest west of the sand spit between bay and of notum. Transparent dorsal vessels run under skin from Gulf of Thailand (at 8°29'18"N, 100°10'55"E) on 29 Sep.2007. near notum border to reno-pericardium (Figs. 1G, 2E).

496 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 1. Aiteng ater, new species: A, photo of a wayang (shadow puppet) and of a statue of Ai Theng at a shop near Pak Phanang; B, creeping adult specimen length 9.0 mm in lab; C, creeping young slug length 2.0 mm; D, young slug curled up length 2.1 mm; E, nerve ring, width of photo 170 µm; F, digestive tubes in ventral view in posterior part of body, width of photo 2600 µm; G, posterior lateral side of notum in dorsal view with skin largely removed showing digestive follicles and dorsal vessels; H, prostate dorsal view, width photo 270 µm; I, parasites around salivary follicles, ventral view; J, ventral view of albumen gland, ampulla, and follicles; K, eye; L, penis; M, lateral view of radular teeth. Legend: ag − albumen gland; am − ampulla; dg − digestive follicles; dt − digestive tubes; dv − dorsal vessels; ey − eye; fb − foot border; fo − follicles of ovotestis; nb − notum border; pa − parasite; ph − pharynx; pr − prostate; sg − salivary follicles; sr − seminal receptacle; st − stomach; ve −velum.

497 Swennen & Buatip: Aiteng ater, new genus and species

Hermaphrodite follicles yellowish, numerous, length 120- supposed these were parasites, but they were not identifi ed 190 µm (Fig. 1J). Connecting ductules gradually unite or studied. into hermaphroditic duct continuing through black spotted ampulla (Fig. 1J). Postampullary hermaphroditic duct short; Habitat and behaviour. – All specimens were found in splits into short oviduct and vas deferens. Albumen duct a dense mangrove forest high in the intertidal zone, not from compound albumen gland (Figs. 1J, 2G) connects covered by the sea during neap high tides. The slugs were to short oviduct. Fertilisation region, capsule gland and usually along the water level of crab burrows, foot prints, and mucus gland very close, distal parts separate; large oviduct small pools in rather stiff mud with fallen twigs and leaves. could not precisely be traced in these glands. Oviduct and The salinity of the water varied between 18 and 37 S during vaginal duct partly united, connected with compact seminal our visits. The leaf cover of the mangrove trees Avicennia receptacle shortly before female aperture. Vas deferens runs marina (Forsk.) Vierh., Bruguiera cylindrica (L.) Blume, parallel with oviduct to right body wall and then anteriorly; and Rhizophora apiculata Blume, with an undergrowth of prostate surrounds part of vas deferens curving along and Acanthus ilicifolius L. and Acrostichum aureum L. shaded over pharynx (Figs 1H, 2G), continuing as thin vas deferens the substrate from direct sunlight. Specimens kept in the to penis sack. Penis thin, unarmed, on right side of head lab usually rested along the water’s edge, often partly in (Fig. 1L). the water, with a preference for small depressions in the mud, which is similar to the fi eld. When they were exposed Endoparasites. – White, cigar-shaped bodies of different to strong light, they moved until shade was found. Night sizes were found under the skin and loose on other observations showed that they were actively moving in the organs in some specimens during dissecting (Fig. 1I). We dark, but all movements were slow. Heart beats per 30 s

Fig. 2. Aiteng ater, new species: A, dorsal view of slug, length 9 mm, in rest; B, ventral view of slug in rest against glass; C, lateral view of creeping slug, length 11 mm; D, diagram of digestive system in dorsal view; E, dorsal vessels; F, pharynx, length 900 µm; G, diagram of the genital complex in dorsal view; H, radular teeth of two specimens. Legend: ag − albumen gland; al − ascending limb of radula; am − ampulla; as − ascus ;bw − body wall; cg − capsule gland; dg − digestive gland; dl − descending limb of radula; dv − dorsal vessels; (fa) − position of female aperture hidden under free notum border; fa − female aperture; fb − foot border; fg − foot groove; hd − hermaphrodite duct; in − intestine; ma − male aperture; mg − mucus gland; mo − mouth; nb − notum border; oe − oesophagus; pc − renopericardium; ph − pharynx; pr − prostate; ps − penis sack; sd − salivary duct; sg − area of salivary follicles; so − short oviduct; sr − seminal receptacle; st − stomach; vd − vas deferens; ve − velum.

498 THE RAFFLES BULLETIN OF ZOOLOGY 2009 in three moving specimens were 30, 32, and 35 at 32°C. The number of radular teeth in Aiteng ater, new species, Feeding tests showed that small green algae collected from is much higher than in most sacoglossans. Only species the site were neglected. However, pupae of insects of the of the shelled genus Cylindrobulla may have also 80 or orders Coleoptera and found in the mud were more teeth (Jensen, 1989). The affi nities of Cylindrobulla opened and emptied by the slugs kept in the laboratory. to other groups have long been disputed (Jensen, 1989, Further trials showed that also imagines of mosquitos and 1996b; Mikkelsen, 1998: table 1). Jensen (1996a) found ant larvae were eaten. Copulations and eggs were not seen that it belonged to a separate order in between Sacoglossa in the fi eld or laboratory. A few small slugs (length about 2 and Cephalaspidea for which she proposed the name mm) were discovered in the substrate samples taken to the Cylindrobullacea. Among the arguments indicated why lab in April 2008. This suggests that reproduction may occur Cylindrobulla would not belong to the Sacoglossa are: in the beginning of the year shortly after the rainy season. not associated with algae, which are the food for most sacoglossans; the possession of an atypical radula; atypical Etymology. – The specifi c name is according the colour that shape of the teeth; the lack of preradular teeth; doubt if the looks black on the mud of its habitat. ascus was a real ascus. Mikkelsen (1996, 1998), on the other hand, found that Cylindrobulla belongs to the Sacoglossa by using similar cladistical analyses. In Aiteng ater, new DISCUSSION species, the high number of teeth in the pharynx may be related to a high wear of the active tooth during feeding. Aiteng ater, new species, is a small, inconspicuous, grey Likely, making a hole is more diffi cult in an exoskeleton of to blackish opisthobranchs with a wide free notum border an insect than in the membrane of an algal cell. The used along its sides and posterior part, but without shell, teeth are clearly more worn than the teeth of algae eating rhinophores, gills or other protuberances. The absence of sacoglossans. It may be that for rasping open an exoskeleton protuberances may be related to its specialism of living successively new teeth have to be used. Therefore, it seems amphibiously high in the intertidal zone among mangroves. likely that Aiteng ater needs to have a larger number of It also seems extremely specialised by feeding on insects. teeth available for feeding than slugs feeding on foods with Striking internal features are the large pharynx with a softer covering. In a series of pharynxes studied, one numerous uniseriate teeth in an ascending and a descending showed a decline in teeth size towards the ascus (Fig. 2F) radular limb, the large oral and salivary glands, and the and the others had teeth of similar size in their ascending large area occupied by tubes of the digestive gland. These and descending limbs, except shorter median cusps by wear features are likely related to the diffi culty of ingesting and in the descending limb. There was always only a small digesting lipids and proteins of its insect foods. amount of broken teeth in the ascus. As there is no means of exit in the ascus of Aiteng ater, these observations may The external characters give no direct clues to indicate a family suggest that used teeth become resorbed in the ascus. This or higher order; the species appears unique. The internal would also explain the absence of preradular teeth in adult characters are somewhat confusing. The prepharyngeal specimens. A notum with a free margin such as in Aiteng ganglionic ring is characteristic for some families of ater, new species, is not found in other sacoglossans, but Cephalaspidea (Schmekel, 1985; Mikkelsen, 1996) and the lateral extension along the dorsal sides in Costasiella Acochlidea (Ev. Marcus, 1982, Jörger et al., 2008); in other coronata Swennen, 2007 and, although less pronounced, opisthobranch orders the ring is postpharyngeal (Schmekel, the wider notum of the bare-backed Limapontia depressa 1985; Jensen, 1996a). Acochlidea are very small interstitial Alder & Hancock, 1862 show some similarity and the slugs with a short foot and a large visceral hump, and the extensions in these species are also fi lled with branches of cephalaspid genera show besides a pre- or postpharyngeal the digestive gland. nerve ring, a shell, sperm-groove, Hancock’s organ, ciliated strips on the mantle margin, three gizzard plates, rachidian Nearly all characteristics of Aiteng ater , new species, point plus lateral teeth. Although some lack one or more of these to placing it in the Sacoglossa, but there are problems. characters (Mikkelsen, 1996), none of these is found in The prepharyngeal nerve ring suggests a connection of the Aiteng ater, new species. The presence of a well developed species with the Cephalaspidea (Schmekel, 1985; Jensen, pharynx with a uniserial radula on an ascending and a 1996a; Mikkelsen, 1996). Abnormal is also the food of descending limb, a posteroventral ascus in which the worn the species, nearly all known shelled and non-shelled teeth are stored instead of becoming lost during feeding sacoglossans feed on algae, a few are specialized on animal are specifi c characteristics of the Sacoglossa (Bergh, 1878; food (gastropod eggs), but up to now none on insects Schmekel, 1985). Characteristic for sacoglossans are also (Jensen, 1997). The place of the Aitengidae, new family, the dorsal, symmetrically arranged branches of the digestive within the Sacoglossa or in a new order may be determined gland, the reproductive system with numerous small after further study. hermaphrodyte follicles and a closed vas deferens (Sander- Esser, 1984; Gascoigne, 1985; Mikkelsen, 1996). The dorsal vessels under the skin of the notum that are connected with ACKNOWLEDGEMENTS the renopericardium show similarity with the dorsal vessels in sacoglossan genera such as Aplysiopsis, Bosellia, Cyerce, We like to thank Mrs. Narongrit Butmata and Ni-hasem Elysia and some others (Jensen, 1996a). Waesalae for their help in collecting the specimens, Kathe

499 Swennen & Buatip: Aiteng ater, new genus and species

Rose Jensen and Robert G. Moolenbeek for help with the Jensen, K. R., 1997. Evolution of the Sacoglossa (Mollusca, literature, discussing the placement, and comments on an Opisthobranchia) and the ecological associations with their earlier version of the draft, and two anonymous referees for food plants. Evolutionary Ecology, 11: 301–335. useful suggestions to improve the MS. Jörger, K. M., T. P. Neusser, G. Haszprunar, & M. Schrödl, 2008. Undersized and underestimated: 3D visualization of the Mediterranean interstitial acochlidian gastropod Pontohedyle milaschewitchii (Kowalevsky, 1901). Organisms Diversity & LITERATURE CITED Evolution, 8 (3): 194–214.

Bergh, L. S. R., 1878. Beiträge zur Kenntniss der Aeolidiaden, Marcus, Ev. 1982. Systematics of the genera of the order 6. Verhandlungen der Kaiserlich-Königlichen Zoologisch- Ascoglossa (Gastropoda). Journal of Molluscan studies, Botanische Gesellschaft, Wien, 28: 553–584. Supplement, 10: 1–31. Gascoigne, T., 1985. A provisional classifi cation of families of Mikkelsen, P. M.,1996. The evolutionary relationships of the order Ascoglossa (Gastropoda: Nudibranchiata). Journal Cephalaspidea s.l. (Gastropoda: Opisthobranchia): A of Molluscan Studies, 51: 8–22. phylogenetic analysis. Malacologia, 37: 375–442. Jensen, K. R., 1989. A new species of Cylindrobulla from Phuket, Mikkelsen, P. M.,1998. Cylindrobulla and Ascobulla in the western Thailand, with a discussion of the systematic affi liations of the Atlantic (Gastropoda, Opisthobranchia, Sacoglossa): systematic genus. Phuket Marine Biological Center Research Bulletin, review, description of a new species, and phylogenetic 52: 1–11. reanalysis. Zoologica Scripta, 27: 49–71. Jensen, K. R., 1996a. Phylogenetic systematics and classifi cation Sander-Esser, B. 1984. VergleichendeUntersuchungen zur of the Sacoglossa (Mollusca, Gastropoda, Opisthobranchia). Anatomie und Histologie der vorderen Genitalorgane Philosophical Transactions of the Royal Society of London, der Ascoglossa (Gastropoda, Euthyneura). Zoologische B 351: 91–122. Jahrbücher. Abteilung für Anatomie und Ontogenie der Tiere, 111: 195–243. Jensen, K. R., 1996b. The Diaphanidae as a possible sister group of the Sacoglossa (Gastropoda, Opisthobranchia). In: Taylor, Schmekel, L. 1985. Aspects of evolution within the opisthobranchs. J.D. (ed.), Origin and evolutionary radiation of the Mollusca. The Mollusca, 10: 221–267. Oxford University Press. Pp. 231–247.

500 THE RAFFLES BULLETIN OF ZOOLOGY 2009

THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 501–504 Date of Publication: 31 Aug.2009 © National University of Singapore

BETTA PARDALOTOS, A NEW SPECIES OF FIGHTING FISH (TELEOSTEI: OSPHRONEMIDAE) FROM SUMATRA, INDONESIA

Tan Heok Hui Raffl es Museum of Biodiversity Research, Department of Biological Sciences, National University of Singapore, Kent Ridge, Singapore 119260, Republic of Singapore Email: [email protected]

ABSTRACT. – A new species of Betta from the B. waseri group is described based on recent material. It is closely allied to B. chloropharynx from Pulau Banka. Betta pardalotos differs from B. chloropharynx in having a slightly different throat pattern; spotted opercle and throat (vs. unmarked); even sloping or convexity at area posterior to upper jaw to supra-orbital area (vs. slight concavity) and other characters. This brings to eight members in the B. waseri group.

KEY WORDS. – Betta, new species, Sumatra, peat swamp, biodiveristy.

INTRODUCTION the Zoological Reference Collection (ZRC) of the Raffl es Museum of Biodiversity Research, National University of The Betta waseri species group was fi rst proposed by Ng & Singapore; Research and Development Centre for Biology, Kottelat (1994). They redescribed B. waseri Krummenacher The Indonesian Institute of Sciences (LIPI, formerly the (1986) based on fresh material from Pahang (Malaysia) and Museum Zoologicum Bogoriense - MZB), Cibinong, described the following new species: B. hipposideros from Indonesia; and the collection of Maurice Kottelat (CMK) Selangor (Malaysia), B. tomi from Johor (Malaysia) and in Cornol, Switzerland. B. spilotogena from Pulau Bintan (Indonesia). Kottelat & Ng (1994) described B. chloropharynx from Pulau Banka Meristic and morphometric measurements follow that (Indonesia), but they treated it as part of the B. akarensis of Ng & Kottelat (1994) and Tan & Ng (2005a). All group. Tan & Kottelat (1998) transferred B. chloropharynx measurements are taken with a pair of digital Mitutoyo® into B. waseri group, with justifications. Tan (1998) calipers. Abbreviations used are SL - standard length, TL further described two species, viz. B. pi from Sungei - total length, HL - head length. Kolok (southern Thailand) and B. renata from central Sumatra (Indonesia). In 2005, Tan & Ng (2005b) covered the labyrinth fishes of Sumatra and associated islands, TAXONOMY listing down 32 species from three families (Anabantidae, Helostomatidae and Osphronemidae). At present, the B. Betta pardalotos, new species waseri group consists of seven species. (Figs. 1–5)

Recently, consignments of Betta were obtained from southern Material examined. – Holotype – MZB 10999 (53.3 mm SL), Sumatra. From initial examination of living material, they Indonesia, Sumatra: South Sumatra Province; Musi drainage; resembled B. chloropharynx. Upon acclimatization, there Palembang, Laut Kenten, Sungai Gelam; T. Sim, 11 Oct.2006. were distinct morphological and colour pattern differences. Paratypes – CMK, 2 ex., MZB 11000, 2 ex., ZRC 51837, 5 The southern Sumatran population is herein described as a ex. (48.6–61.2 mm SL), same locality data as holotype. — ZRC new species – B. pardalotos. 51838, 2 ex., (54.0–72.4 mm SL), same locality as holotype, 5 June 2006. — ZRC 51839, 1 ex. (55.4 mm SL), same locality as holotype, M. Kottelat & H. H. Ng, 14 May 2008. MATERIAL AND METHODS Diagnosis. – Betta pardalotos can be distinguished from Specimens obtained were initially fi xed in 10 % formalin other members of the B. waseri group in having the solution and then transferred to 70 % ethanol solution following combination of characters: two white rounded for long term storage. Material examined is deposited in patches on a black throat (Figs. 2, 3, 5); opercle with three

501 Tan: A new species of fi ghting fi sh from Sumatra

arched rows of black dots following opercle edge; black transverse bars on the dorsal and caudal fin interradial membranes; absence of a dark distal border on anal fi n; operculum without lower distal margin black. It is further differentiated from the closely allied B. chloropharynx

Fig. 1. Betta pardalotos, ZRC 51838, paratype, 72.4 mm SL. Fig. 4. Betta pardalotos, MZB 10999, holotype, 53.3 mm SL.

Fig. 2. Betta pardalotos, ZRC 51838, paratype, 72.4 mm SL, close-up of head.

Fig. 5. Betta pardalotos, ZRC 51837, paratype, 61.2 mm SL, close-up of head pattern, lateral and ventral views.

Fig. 3. Betta pardalotos, ZRC 51838, paratype, 72.4 mm SL, front view Fig. 6. Betta chloropharynx, ZRC 35166, 56.6 mm SL, holotype; of head showing lower jaw, throat and opercle pattern. Sumatra: Banka Island."

502 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Meristic and morphometric data of Betta pardalotos.

Holotype Paratypes (n=7) MZB 10999 Min. Max. mode Standard length (mm) 53.3 51.7 72.4 Anal fi n rays (total) 29 (II,27) 27 30 29 Dorsal fi n rays (total) 10 (I,9) 9 10 10 Pelvic fi n rays 1, 5 1, 5 Pectoral fi n rays 12 12 Subdorsal scales 7 7 7 ½ 7 Transverse scales 10 10 Lateral scales 33 33 34 34 Lateral scale below dorsal fi n origin 16 15 17 16 Lateral scale above anal fi n origin 6 6 7 6 Predorsal scales 24 23 26 24 Postdorsal scales 13 12 13 12 % standard length Min. Max. mean SD (±) Total length 167.1 135.7 167.1 144.1 9.77 Body length 67.0 65.9 69.8 68.2 1.32 Predorsal length 67.2 65.2 67.2 66.3 0.88 Postdorsal length 21.7 21.4 24.4 22.9 1.23 Caudal peduncle depth 21.7 18.4 21.7 20.1 0.94 Preanal length 46.3 41.5 57.8 45.3 5.44 Head length 35.6 32.5 35.8 34.1 1.13 Body depth 29.5 24.7 29.5 27.0 1.41 Pelvic fi n length 34.0 28.7 34.3 31.7 2.10 Anal fi n base length 55.9 53.7 58.9 56.7 1.77 Dorsal fi n base length 14.4 12.9 14.8 13.8 0.68 % head length Orbit diameter 25.5 23.2 28.8 26.6 1.76 Postorbital length 47.1 47.1 54.3 50.6 2.89 Interorbital width 39.2 37.3 41.8 39.1 1.44 Snout length 28.3 22.8 29.2 25.8 2.05

(Fig. 6) in having the following characters: heavily spotted pelvic fi n falcate with fi rst ray fi lamentous, relatively long opercle (vs. no spots); even sloping or convexity at area (pelvic fi n length 28.7–34.3% SL), reaching up to 12th posterior to upper jaw to supra-orbital area (vs. slight anal fi n ray; pectoral fi n rounded. Vertebral count: 11–12 concavity); body dusky with irregular blotches (vs. uniform + 19–21 (total 31–32, mode 32, n=10). body pattern); anal-fi n origin at lateral scale 6–7 (vs. 8); deeper caudal peduncle (18.4–21.7% SL, vs. 16.7–18.8); Live colouration. – See Figs. 1–3 for live colouration. longer head (32.5–35.8% SL, vs. 29.9–33.7); more lateral Head and body dorsum dark brown. Eye with unique scales (modally 34, vs. 33). colouration zones of the B. waseri group (as defi ned by Tan, 1998). Lower jaw with lower and upper lips black, Description. – General body form as in Figs. 1, 4; meristics throat with two white semi-circles (curved surface facing and morphometrics listed in Table 1. Body relatively long downwards; see Figs. 2, 3, 5), bordered below with black and stout (body depth at dorsal fi n origin 24.7–29.5% SL); chin bar. Lower half of opercle creamy white with light head stout with pointed snout and evenly sloping or slight greenish-gold iridescence, lower half of opercle distinctly convexity at supra-orbital area (head length 32.5–35.8% covered with three rows of fairly regularly spaced small SL); dorsal fin pointed, situated nearer to caudal fin black spots, arranged according to curvature of opercle (predorsal length 65.2–67.2% SL), dorsal fi n base short edge. Body yellowish-brown, with indistinct central dark (dorsal fi n base length 12.9–14.8% SL), covering 7–7 ½ brown stripe, with faint dark patches just above anal fi n subdorsal scales; caudal fin rounded with median rays sheath scales. Dorsal fi n brownish with up to 13 transverse elongate; anal fi n with posterior rays elongate, anal fi n base bars on interradial membrane. Caudal fi n brownish with more than half of SL (anal fi n base length 53.7–58.9% SL); up to 16 transverse bars on interradial membrane. Anal

503 Tan: A new species of fi ghting fi sh from Sumatra

fi n brownish, without distal dark border but with very thin in Southeast Asia), alluding to the spotted pattern on the white margin. Pelvic fi ns yellowish-brown with whitish opercle. interradial membrane, distal part of pelvic fi n fi lamentous ray iridescent whitish-green. Pectoral fi n hyaline with a Comparative material. – See Kottelat & Ng (1994), Ng black sub-basal bar. & Kottelat (1994), Tan (1998) and Tan & Ng (2005a and 2005b) for a list of comparative material. Preserved coloration. – Preserved coloration illustrated in Figs. 4–5. Colouration as above, except no iridescence Additional material. – Betta chloropharynx – ZRC 47248, present and opercle pattern indistinct on some specimens. 1 ex. (69.3 mm SL), Indonesia, Sumatra: Banka; D. Yong, Jul.2001. — ZRC 51825, 6 ex., (43.8–73.1 mm SL), Distribution. – Betta pardalotos is currently known only Indonesia, Sumatra: Banka; N. Takahashi, 30 Jul.2002. from the Musi basin in South Sumatra province in Sumatra, Indonesia (Fig. 7). ACKNOWLEDGEMENTS Field notes. – The type locality is a tributary of the lower part of Musi River, as such there are euryhaline Many thanks to the following: Gunawan Kasim, Patrick Yap, elements present, as seen in the presence of Nypa palms, Maurice Kottelat, H. H. Ng and Dennis Yong, for donation Hemibagrus hoevenii (a bagrid catfi sh known only from and collection of material; David Armitage, for pictures lower reaches of rivers), Zenarchopterus ectuntio and of B. chloropharynx for comparison work. Funding from various gobiid species. However, Betta pardalotos the Raffl es Museum of Biodiversity Research and research was obtained from smaller feeder streams, which were grant R-154-000-318-112 from the National University of freshwater. Syntopic osphronemids present include: Singapore is kindly acknowledged. Belontia hasseltii, Betta edithae, Luciocephalus pulcher and Trichopodus trichopterus. LITERATURE CITED Etymology. – From the Greek pardalis, of the feline leopard (Panthera pardalis, an inhabitant of the tropical rainforests Kottelat, M. & P. K. L. Ng, 1994. Diagnoses of fi ve new species of fi ghting fi shes from Banka and Borneo (Teleostei: Belontiidae). Ichthyological Exploration of Freshwaters, 5: 65–78. Krummenacher, R., 1986. Betta waseri spec. nov. Aquarien und Terrarien Eine Zeitschrift aus dem Kosmos-Verlag, 33: 177–181. Ng, P. K. L. & M. Kottelat, 1994. Revision of the Betta waseri group (Teleostei: Belontiidae). Raffl es Bulletin of Zoology, 42: 593–611. Schindler, I. & J. Schmidt, 2006. Review of the mouthbrooding Betta (Teleostei, Osphronemidae) from Thailand, with descriptions of two new species. Zeitschrift für Fischkunde, 8: 47–69. Tan, H. H., 1998. Two new species of the Betta waseri group (Teleostei: Osphronemidae) from central Sumatra and southern Thailand. Ichthyological Exploration of Freshwaters, 8: 281–287. Tan, H. H. & M. Kottelat, 1998. Two new species of Betta (Teleostei: Osphronemidae) from the Kapuas basin, Kalimantan Barat, Borneo. Raffl es Bulletin of Zoology, 46: 41–51. Tan, H. H. & K. K. P. Lim, 2004. Inland fi shes from the Anambas and Natuna Islands, South China Sea, with description of a new species of Betta (Teleostei: Osphronemidae). Raffl es Bulletin of Zoology, Supplement no. 11: 107–115. Tan, H. H. & P. K. L. Ng, 2005a. The fi ghting fi shes (Teleostei: Osphronemidae: genus Betta) of Singapore, Malaysia and Brunei. Eds. Yeo, D. C. J. & M. Kottelat, Southeast Asian Freshwater Fish Diversity. Raffles Bulletin of Zoology, Supplement no. 13: 43–99. Tan, H. H. & P. K. L. Ng, 2005b. The labyrinth fi shes (Teleostei: Anabantoidei, Channoidei) of Sumatra, Indonesia. Eds. Yeo, D. C. J. & M. Kottelat, Southeast Asian Freshwater Fish Diversity. Raffl es Bulletin of Zoology, Supplement no. 13: Fig. 7. Map of Sumatra showing location of Betta chloropharynx (square) 115–138. and B. pardalotos (circle).

504 THE RAFFLES BULLETIN OF ZOOLOGY 2009

THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 505–509 Date of Publication: 31 Aug.2009 © National University of Singapore

RASBORA PATRICKYAPI, A NEW SPECIES OF CYPRINID FISH FROM CENTRAL KALIMANTAN, BORNEO

Tan Heok Hui Raffl es Museum of Biodiversity Research, Department of Biological Sciences, National University of Singapore, Kent Ridge 119260, Republic of Singapore. E-mail: [email protected]

ABSTRACT. – Rasbora patrickyapi, new species, is described from the lowland blackwaters of Central Kalimantan, Borneo. It appears to be most closely related to R. kalochroma and R. einthovenii, from which it differs in having a different life colouration, a complete lateral line with 28 scales and presence of a supra-anal black blotch. It is apparently stenotopic to black water of peat swamp forests.

KEY WORDS. – Taxonomy, new species, peat swamp, Borneo, Rasbora.

INTRODUCTION to caudal fi n base). Last two rays of dorsal and anal fi ns articulate on the same pterygiophore and is counted as The lowland freshwater habitats of Central Kalimantan, two. Indonesian Borneo, are still poorly explored. Not surprisingly, a number of new fish species were Specimens examined are deposited in the Museum recently described from this area. They include – Zoologicum Bogoriense, Bogor (MZB); Collection of Cyprinidae: Eirmotus isthmus Tan & Kottelat (2008), Maurice Kottelat, Cornol, Switzerland (CMK); and the Paedocypris carbunculus Britz & Kottelat (2008); Zoological Reference Collection, Raffles Museum of Cobitidae: Kottelatlimia hipporhynchos Kottelat & Tan Biodiversity Research, National University of Singapore, (2008); Bagridae: Nanobagrus immaculatus Ng (2008a); Singapore (ZRC). Siluridae: Ompok supernus Ng (2008b); Osphronemidae: Betta uberis Tan & Ng (2006), Parosphromenus opallios Kottelat & Ng (2005). TAXONOMY

While examining shipments of Rasbora kalochroma from Rasbora patrickyapi, new species Central Kalimantan at an ornamental fi sh export facility (Figs. 1A–D) in Singapore, the author was alerted to an unusual species of Rasbora mixed with the R. kalochroma. This species Material examined. – Holotype: MZB 10707, 41.8 mm SL; Central resembles R. kalochroma in colour and size, but has a Kalimantan: Rungan-Kahayan basin, Sungei Rijak, km 84 along colour pattern that is reminiscent of R. einthovenii. Further road from Palangkaraya to Telakin (01°37.319'S 113°37.560'E, 54 examination confi rms it to be a new species of Rasbora, m asl); P. Yap et al., 18 Sep.2007. and it is herein described. Paratypes – ZRC 51748, 11 ex., MZB 10708, 4 ex., CMK 21508, 5 ex., 29.8–42.2 mm SL; same locality data as holotype. – ZRC 51749, 20 ex., 31.9–44.5 mm SL; Central Kalimantan: Rungan- MATERIAL AND METHODS Kahayan basin, from aquarium fi sh trade; P. Yap, 24 Jul.2007. – MZB 5334, 11 ex., paratypes, 23.6–57.0 mm SL; Central Specimens were collected with push nets, fi xed in 10 % Kalimantan: Katingan River basin, Kecamatan Katingan ilir, formalin and later transferred to 75 % ethanol for long Sungei Hampalit; A. Jaim, 18 Mar.1984. – ZRC 51750, 5 ex., term storage. Specimens were measured with Mitutoyo® 23.8–46.5 mm SL; Central Kalimantan: Katingan River basin, digital calipers on the left side according to Kottelat stream before Tumbang Samba; T. Idei, 2004. (1984), colour pattern terminology follows Brittan (1954). Abbreviations used: SL – standard length, HL – head Diagnosis. – Rasbora patrickyapi is differentiated from its length, BL – trunk length (from posterior edge of opercle congeners in the following combination of characters: in life, body with iridescent, black midlateral stripe bordered

505 Tan: New species of Rasbora from Borneo by a white stripe above it, reddish unpaired fins, sides placed relatively far back (54.0–56.6% SL and 68.7–70.8% of body with violet sheen, dorsum with golden sheen. SL respectively). Lateral line complete with 28 scales; distinct symphyseal knob; body depth at dorsal fin origin 23.9–26.1% SL; Dorsal fi n triangular, with 2 simple and 7 branched rays, predorsal scales 12–13 (modally 13); transverse scales 5.1.2; last two rays articulate on the same pterygiophore; origin circumpeduncular scales 15; predorsal length (54.0–56.6% above lateral line scale 7 or 8 (modally 8), behind origin SL). of pelvics. Caudal fi n forked, with upper lobe longer than lower lobe, ratio of length versus caudal peduncle depth Description. – General body shape and appearance as shown 1.54–1.66. Anal fi n triangular, with 2 simple and 5 branched in Fig. 1; meristics and morphometrics in Table 1. Head rays, last two rays articulate on the same pterygiophore; broadly pointed, relatively short (head length 27.8–29.0% origin below lateral line scale 13 or 14 (modally 13). Pelvic SL), relatively narrow (head width 47.8–49.1% HL) and fi n triangular, with 1 simple and 7 branched rays, adpressed deep (head depth 58.6–63.1% HL). Mouth terminal and fi n does not reach anal-fi n origin; origin below lateral line slightly upturned, symphyseal knob distinct; no tubercels scale 6 or 7 (modally 7); pelvic axillary scales present, just present. Orbit relatively large (27.7–30.4% HL), situated longer than base of pelvic fi n. Pectoral fi n triangular, with nearer to tip of snout than opercle edge. Interorbital width 1 simple and 12 branched rays, adpressed fi n not reaching large (33.3–37.2% HL), dorsal profi le a gentle slope to slight pelvic-fi n origin, axillary lobe present, about equal length concavity. Slope of nape gentle from head to body, body with pectoral-fi n base. Two scale rows between lateral line cylindrical, compressed laterally, relatively slender, deepest and pelvic-fi n origin. at dorsal fi n origin (23.9–26.1% SL), most slender at caudal peduncle (13.5–14.9% SL). Lateral line complete, running Predorsal scales 12–13 (modally 13), transverse scales diagonally from opercle edge towards pelvic fi n origin and at anus 5.1.2, transverse scales at dorsal-fi n origin 6.1.2, to just below the middle of caudal base. Dorsal and anal fi ns lateral scales 28 (+ 2 on caudal fi n), caudal peduncle scales 4.1.2.

Fig. 1. Rasbora patrickyapi, A, ZRC 51749, paratype, ca. 40 mm SL, life colouration; B, ZRC 51749, paratype, ca. 40 mm SL, life colouration; C, ZRC 51748, paratype, 41.4 mm SL, freshly preserved; D, MZB 10707, holotype, 41.8 mm SL, preserved material, Central Kalimantan: Rungan.

Fig. 2. Rasbora kalochroma. ZRC 51752, 37.9 mm SL; Central Fig. 3. Rasbora einthovenii. ZRC 50123, 32.1 mm SL; West Kalimantan: Kalimantan: Rungan. Sambas.

506 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Meristics and morphometric data of Rasbora patrickyapi.

Rasbora patrickyapi, new species Catalogue numbers MZB 10707 (holotype) Holotype + ZRC 51748 (paratypes) Sample size 1 5 Standard length (mm) 41.8 39.3–41.8 % Standard length Total length 130.1 129.6–133.2 Trunk length 72.2 71.5–73.6 Predorsal length 56.2 54.0–56.6 Preanal length 70.8 68.7–70.8 Prepelvic length 51.9 50.3–51.9 Head length 27.8 27.8–29.0 Body depth at dorsal fi n origin 23.9 23.9–26.1 Body depth at anus 20.3 20.3–21.5 Caudal peduncle depth 13.9 13.5–14.9 Caudal peduncle length 22.5 21.1–23.8 Dorsal fi n base length 12.2 11.6–12.2 Anal fi n base length 12.7 10.9–12.7 Pelvic fi n length 18.4 16.8–18.6 Pectoral fi n length 24.4 22.6–24.4 Upper caudal lobe length 31.8 31.4–36.4 Middle caudal length 20.6 16.8–20.6 Lower caudal lobe length 28.0 28.0–34.1 % Head length Head depth 58.6 58.6–63.1 Head width 48.3 47.8–49.1 Snout length 29.3 27.7–29.7 Orbital diameter 28.4 27.7–30.4 Interorbital width 37.1 33.3–7.2

Vertebral count: 17–18 + 15–16, total = 32–34 (mode 33, Distribution. – Rasbora patrickyapi is currently known n = 10). only from the lowland peat swamps and degraded heath forest of the Katingan and Kahayan river basins of Central Live coloration. – See Figs.1A–B. Dorsum of head and Kalimantan, Borneo (Fig. 4). body dark brown with gold sheen. Top of eye golden- orange. Black stripe running from lower jaw, through eye Field notes. – Rasbora patrickyapi inhabits shallow, to opercle edge, continuing onto midlateral black stripe slow-fl owing swampy areas next to the fl owing blackwater (margins are irregular) to caudal base and through to tips streams. At the type locality (Fig. 5), and is sympatric of middle caudal fi n rays; with green iridescence. A white with Rasbora kalochroma. Other fishes include: stripe above midlateral black stripe posterior to opercle Cyprinidae – Osteochilus pentalineatus, O. spilurus, edge to caudal base. A black suparanal blotch above anal O. bleekeri, Rasbora cephalotaenia, Sundadanio cf. fi n origin. Body with violet sheen throughout. All unpaired axelrodi, Systomus rhomboocellatus, S. johorensis, S. fi ns reddish, pelvic fi n reddish and pectoral fi n yellowish. trifasciatus; Cobitidae – Kottelatlimia hipporhynchos, Dorsal fi n anterior base to mid area with black pigments. K. pristes; Nemacheilidae – Nemacheilus sp.; Siluridae – Ompok supernus, Silurichthys phaiosoma; Clariidae – Coloration in preservative. – See Figs. 1C–D. Freshly Clarias leiacanthus; Hemiramphidae – Hemirhamphodon preserved specimens with colours as in life, but muted and chrysopunctatus; Nandidae – Nandus nebulosus; lacking iridescence and sheen (Fig. 1C). Specimens stored Osphronemidae – Betta anabatoides, B. foerschi, in ethanol were discoloured, with no red colouration (Fig. Luciocephalus pulcher, Sphaerichthys selatenensis; 1D). Body cream, with dark brown dorsum and black Channidae – Channa bankanensis; Mastacembelidae central stripe. The midlateral black stripe is broadest at – Macrognathus circumcinctus. The lowland swamplands the middle of the body, sometimes interrupted with cream around Palangkaraya have mainly been logged, and patches above the region between the pelvic and anal fi ns. the vegetation is secondary. The habitat is heath forest Mid-dorsal black stripe present, mid-ventral black stripe interspersed with peat swamp. The substrate are a mixture present on caudal peduncle. of peat and silica sand.

507 Tan: New species of Rasbora from Borneo

Etymology. – Named for Patrick Yap Boon Hiang, a slope (vs. more arched); presence of supra-anal black blotch long-time supporter of the museum and freshwater fish (vs. absence); more pelvic-fi n rays (1, 7, vs. 1, 6); more enthusiast and exporter, who has generously donated much lateral scales (28 +2, vs. 23–24 +2); more circumpeduncular fi sh material for the author’s research. scales (15 vs. 13); smaller predorsal length (54.0–56.6% SL, vs. 56.7–58.6); smaller pectoral fi n length (22.6–24.4% Remarks. – Rasbora patrickyapi belongs to the R. SL, vs. 24.3–26.4); smaller head width (47.8–49.1% HL, einthovenii group(as defi ned by Brittan, 1954) but displays vs. 49.5–54.3); smaller interorbital width (33.3–37.2% HL, characters of both R. eithovenii and R. kalochroma. vs. 40.7–46.0).

Brittan (1954) listed four species belonging to the Rasbora patrickyapi differs from its sympatric congener, R. R. einthovenii group, and these are R. einthovenii, R. kalochroma in the following characters: presence of black cephalotaenia, R. tubbi and R. jacobsoni. The basis for midlateral stripe (vs. absence of stripe, instead having two this species group is not very clearly defi ned, Brittan (1954) black rounded blotches, one above the pectoral fi n and the only listed the following characters: circumpeduncular other above the anal fi n, see Fig. 2); body with violet sheen in scale rows 12 (except for R. tubbi, with 14); and an life (vs. red); pectoral, pelvic and anal fi ns without distal tip overall morphological similarity. He also mentioned the of second ray extending beyond interradial membrane (vs. variable lateral line scale counts (R. einthovenii 29–32, tips of second ray extending beyond interradial membrane); R. cephalotaenia 32–34, R. tubbi 34–35, and R. jacobsoni presence of supra-anal black blotch (vs. absence); more 24–27). From the present study, the circumpeduncular scale pectoral-fi n rays (1, 12 vs. 1, 11); more tranverse scales at rows are counted based on a slightly different technique, dorsal-fi n origin (6.1.2 vs. 5.1.2); more circumpeduncular and R. einthovenii has 13 and R. patrickyapi has 15. The scales (15 vs. 12); dorsal, anal and pelvic fi ns placed more overall morphology of R. patrickyapi places it with the R. anterior in relation to lateral scale number (dorsal:7–8 vs. einthovenii group. 10; anal: 13–14, vs. 16–16½; pelvic: 6–7, vs. 8); smaller preanal length (68.7–70.8% SL, vs. 70.8–73.1); more Rasbora patrickyapi differs from R. einthovenii in the slender body (body depth 20.3–21.5 % SL vs. 21.9–23.0); following characters: body with violet sheen in life (vs. more slender caudal peduncle (its depth 13.5–14.9% SL vs. absence); reddish unpaired fi ns in life (vs. hyaline to pale 15.3–17.1; its length 21.1–23.8 % SL vs. 18.3–21.2); larger yellow); well demarcated broad white stripe above black ratio of length versus caudal peduncle depth (1.54–1.66 midlateral stripe (vs. weakly marked, see Fig. 3); absence of vs. 1.12–1.27); smaller pelvic fi n length (16.8–18.6% SL reticulate pattern on edge of body scales along dorso-lateral vs. 18.7–22.1); smaller pectoral fi n length (22.6–24.4% SL area above pectoral to pelvic fi n region (vs. presence); lower vs. 25.0–29.3); smaller head width (47.8–49.1% HL vs. margin of midlateral black stripe indistinct (vs. conspicuous 50.0–56.4); smaller interorbital width (33.3–37.2% HL vs. in lower half of body); dorsal and anal fi ns without marking 41.3–47.3). (vs. sub-distal black bars); dorsal profi le of body a gentle Rasbora patrickyapi can be differentiated from the rest of striped rasboras occurring in Borneo (namely R. agyrotaenia, R. cephalotaenia, R. dusonensis, R. gracilis, R. rutteni, R. sarawakensis, R. tornieri and R. trifasciata) by the following characters: it is a stenotopic inhabitant of peat swamps (vs. riverine habitat of R. agyrotaenia, R. dusonensis and R. tornieri; vs. hill stream habitat of R. rutteni, R. sarawakensis and R. trifasciata; vs. swamp forest habitat of R. cephalotaenia and R. gracilis), lateral scale count of

Fig. 4. Map of Borneo showing distribution of Rasbora patrickyapi (circle); type locality of Rasbora einthovenii (square); type locality of Rasbora kalochroma (triangle). Fig. 5. Type locality of Rasbora patrickyapi (March 2008).

508 THE RAFFLES BULLETIN OF ZOOLOGY 2009

28 (vs. 24–27 of R. sarawakensis and R. trifasciata; vs. LITERATURE CITED 29–35 of R. dusonensis, R. cephalotaenia, R. agyrotaenia, R. gracilis and R. tornieri), presence of black supra-anal Brittan, M. R., 1954. A revision of the Indo-Malayan freshwater blotch (vs. black supra-anal stripe of R. sarawakensis, R. fi sh genus Rasbora. Monograph of the Institute of Science and cephalotaenia, R. agyrotaenia, R. tornieri and R. gracilis; Technology, Manila 3: 1–224. vs. absence in R. dusonensis and R. rutteni) (data extracted Britz, R. & M. Kottelat, 2008. Paedocypris carbunculus, a from Brittan, 1954, and Kottelat et al., 1993). new species of miniature fish from Borneo (Teleostei: Cypriniformes: Cyprinidae). Raffl es Bulletin of Zoology, 56 Comparative material. – Rasbora einthovenii – ZRC 50123, (2): 415–422. 5 ex., 26.4–34.7 mm SL; West Kalimantan: Sambas [type Kottelat, M., 1984. A new Rasbora s.l. (Pisces: Cyprinidae) from locality] basin, Sungei Sinabar, blackwater tributary of northern Thailand. Revue Suisse de Zoologie, 91: 717–723. Sambas River (Fig. 3). Rasbora kalochroma – ZRC 51451, Kottelat, M., A. J. Whitten, S. N. Kartikasari & S. Wirjoatmodjo, 10 ex., 33.3–60.2 mm SL; Central Kalimantan: Kahayan 1993. Freshwater fi shes of Western Indonesia and Sulawesi. basin, Rungan River, aquarium trade. – ZRC 51751, 14 Periplus Editions, Hong Kong, 259 pp., 84 pls. ex., 37.8–52.5 mm SL; Central Kalimantan: Katingan basin, Kottelat, M. & P. K. L. Ng, 2005. Diagnoses of six new species Kasongan east area. – ZRC 51752, 4 ex., 25.7–39.7 mm SL; of Parosphromenus (Teleistei: Osphronemidae) from Malay Central Kalimantan: Rungan-Kahayan basin, Sungei Rijak, Peninsula and Borneo, with notes on other species. Raffl es km 84 along road from Palangkaraya to Telakin (Fig. 2). Bulletin of Zoology, supplement no. 13: 101–113. Kottelat, M. & H. H. Tan, 2008. Kottelatlimia hipporhynchos, a new species of loach from southern Borneo (Teleostei: ACKNOWLEDGEMENTS Cobitidae). Zootaxa, 1967: 63–72. Ng, H. H., 2008a. A new species of Nanobagrus (Teleostei: I am grateful to Patrick Yap, for generously providing Bagridae) from southern Borneo. Copeia, 2008 (1): 93–98. fish material over the years; Peter K. L. Ng, for his Ng, H. H., 2008b. Ompok supernus, a new catfi sh (Teleostei: continuous support through the years; Maurice Kottelat, Siluridae) from Borneo. Zootaxa, 1877: 59–68. for his encouragement and advice; Kelvin K. P. Lim, for Tan, H. H. & M. Kottelat, 2008. Revision of the cyprinid genus his comments and helpful suggestions; Hendra, for local Eirmotus, with description of three new species from Sumatra logistic support. This study has been partially supported by and Borneo. Raffl es Bulletin of Zoology, 56 (2): 423–433. the Raffl es Museum of Biodiversity Research and research Tan, H. H. & P. K. L. Ng, 2006. Six new species of Betta grant R–154–000–318–112 from the National University (Teleostei: Osphronemidae) from Borneo. Ichthyological of Singapore. Exploration of Freshwaters, 17 (2): 97–114.

509 THE RAFFLES BULLETIN OF ZOOLOGY 2009

THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 511–520 Date of Publication: 31 Aug.2009 © National University of Singapore

CHAETODONTOPLUS POLIOURUS, A NEW ANGELFISH (PERCIFORMES: POMACANTHIDAE) FROM THE TROPICAL WESTERN PACIFIC

John E. Randall Bishop Museum, 1525 Bernice St., Honolulu, HI 96817-2704, USA Email: [email protected]

Luiz A. Rocha University of Texas at Austin, Marine Science Institute, 750 Channel View Dr., Port Aransas, TX 78373, USA Email: [email protected]

ABSTRACT. – Chaetodontoplus poliourus is described as a new species of pomacanthid fi sh from 30 specimens collected in New Britain (type locality), other localities in Papua New Guinea, Solomon Islands, Palau, and islands of Indonesia. It was previously regarded as a colour variant of C. mesoleucus (Bloch) by having a grey caudal fi n with a narrow yellow margin instead of a yellow fi n, yellow instead of white pelvic fi ns, and more pale yellow anteriorly on the dorsal fi n. The two species coexist at several islands of Indonesia, but only C. mesoleucus ranges northwest to the coast of southeast Asia, the Philippines and the Ryukyu Islands, and only C. poliourus is found east of the Indonesian province of West Papua. No external morphometric differences could be detected between the two species, but C. poliourus was found to have two supraneural bones, compared to one for C. mesoleucus, modally one fewer pectoral-fi n rays, and a higher average number of anal-fi n rays. Mitochondrial and nuclear DNA analyses revealed signifi cant differences between the species (6.07% sequence divergence on mtDNA and a 25 base pair indel on nDNA), reinforcing their distinct taxonomic status.

KEY WORDS. – Taxonomy, angelfi shes, Chaetodontoplus, new species, western Pacific.

INTRODUCTION Bleeker (1877: 56, pl. 379, fi g. 5) provided a detailed species account of Chaetodontoplus mesoleucus and illustrated it in Bloch (1787: 117, pl. 216, fig. 2) described the first colour. His localities included Singapore, and the Indonesian species of Chaetodontoplus as Chaetodon mesoleucus localities Batu, Java, Sulawesi, Ceram, Halmahera, and (not to be confused with Chaetodon mesoleucos Forsskål, Batjan. an endemic Red Sea butterfl yfi sh). Of all the angelfi shes, Chaetodontoplus mesoleucus most resembles a species of In a review of Philippine butterfl yfi shes and their allies, Chaetodon in body shape and in having a broad black bar Herre & Montalban (1927: 101, pl. 7, fi g. 1) reported 12 through the eye. Bloch gave the type locality as Japan, but specimens as Holacanthus mesoleucus, ranging from 81 to this is questionable because the species is not known from 125 mm in length, from Mindoro, Panay, Masbate, Mindanao, the main islands of Japan. Leyte, Tawitawi, and Jolo. Their detailed colour description mentioned the paired and caudal fi ns as clear lemon yellow Lacepède (1802: 528, 537), Cuvier in Cuvier & Valenciennes and the fi rst one or two dorsal spines as yellow. Their (1831: 170), and Günther (1860: 54) classifi ed Bloch’s species smallest specimen was a female ready to spawn. in the genus Holacanthus. Günther included Chaetodon atratus Gronow in Gray (1854) in his synonymy. He gave Fowler & Bean (1929: 191) listed numerous specimens of the locality for H. mesoleucus as the East Indian Archipelago, Holacanthus mesoleucus ranging in length from 34–150 listing specimens from Macassar and the Molucca Islands. mm from 50 collections made by the steamer Albatross throughout the Philippines from the Sulu Archipelago to Bleeker (1876: 307) described the new angelfish genus Luzon. No life colour notes were given. However, the fi rst Chaetodontoplus, designating Holacanthus septentrionalis author found an unpublished colour painting of a specimen as the type species. In volume 9 of his Atlas Ichthyologique, (linen tag no. 492) in the National Museum of Natural

511 Randall & Rocha: A new species of angelfi sh from the Western Pacifi c

History that was collected during the Albatross cruise at at the northeast end. Chaetodontoplus mesoleucus was not Romblon Island, Sibuyan Sea, central Philippines on 26 seen, but the grey-tailed species was common (Figs. 4 and Mar.1908. It is reproduced here as Fig. 1. The probable artist 5). Specimens were collected and photographed (Fig. 6), was Kumataro Ito (Lisa Palmer, pers. comm.). In addition, and tissue samples were taken. Jeffrey T. Williams provided his colour photograph of a specimen of the yellow-tailed C. mesoleucus from Busuanga In 2006, the second author, Brian W. Bowen, and Matthew (between Mindoro and Palawan) that was collected for the T. Craig determined that only the grey-tailed species of Field Museum of Natural History, Chicago. Chaetodontoplus is found in Palau; six specimens were collected, tissue was removed, and underwater photos taken Borodin (1930: 56) described Holacanthus bicolor var. (Fig. 7). Seven Philippine specimens of the yellow-tailed oahuensis as a new colour variety, supposedly collected C. mesoleucos were obtained from the aquarium trade. An at Oahu, Hawaiian Islands. Fraser-Brunner (1933: 550) analysis of the DNA of the two angelfi shes has confi rmed reviewed the pomacanthid fi shes, then still regarded as a species-level separation. subfamily of the Chaetodontidae. He treated Borodin’s variety as a synonym of Chaetodontoplus mesoleucus and Some problems still remain in the classification of gave the distribution as East Indies, listing specimens from Chaetodontoplus. Fraser-Brunner (1933) recognized seven Singapore, Macassar, Manado, Jolo, and New Britain. species in the genus. He regarded C. dimidiatus (Bleeker) as a synonym of C. melanosoma Bleeker, and he included C. Munro (1967: 373, pl. 51, fi g. 702) included Chaetodontoplus chrysocephalus Bleeker, but considered it “very probably” a mesoleucus in his book, The Fishes of New Guinea. However, variety of C. septentrionalis (Temminck & Schlegel). Whitley he listed no specimens or localities within New Guinea and (1959) described C. ballinae from Ball’s Pyramid, Lord used Herre & Montalban’s illustration for his fi gure of the Howe Island, since reported from New South Wales. Chan species. (1969) described C. niger from a juvenile from the South China Sea, now known to range to southern Japan. Shen In 1968 the fi rst author collected three specimens of an & Lim (1975) named C. cephalareticulatus from northeast angelfish from Palau (Fig. 2), which he provisionally coast of Taiwan, and Yasuda & Tominaga (1976) added identified as Chaetodontoplus mesoleucus, because the C. caeruleopunctatus from the Philippines. Kuiter (1990) caudal fi n was grey with only a narrow yellow posterior described C. meredithi from the eastern coast of Australia. border, instead of yellow with a narrow transparent posterior Pyle & Randall (1994) suggested that C. chrysocephalus is margin, and the pelvic fi ns were yellow instead of white. the hybrid, C. melanosoma x C. septentrionalis. Allen et al. In 1987, while diving with Rudie H. Kuiter at the southern (1998) recognized 11 species of Chaetodontoplus, including Indonesian island of Flores, both the yellow-tailed and grey- C. chrysocephalus, but not C. cephalareticulatus. Gerald R. tailed forms of C. mesoleucus were common on the coral Allen (pers. comm.) now concedes that C. chrysocephalus reefs. The grey-tailed fi sh were generally seen in lesser might be a hybrid. Debelius et al. (2003) accepted C. depths, and when the fi sh were seen in pairs, they were cephalareticulatus and C. chrysocephalus as valid species, the same colour. They concluded that the two colour forms but considered C. caeruleopunctatus a synonym of the latter. were most likely different species. Specimens of both were However, the second author of the book, Hiroyuki Tanaka collected (Fig. 3 is the yellow-tailed C. mesoleucus), and (pers. comm.), did not agree. Allen & Steene (2004) described tissue samples were taken for electrophoresis. The tissue C. vanderloosi as a new species from Papua New Guinea and samples were sent to a colleague, but she failed to complete the electrophoretic study.

Although the difference in the colour of the caudal and pelvic fi ns is lost in preserved specimens of the two presumed species, one useful life colour difference persists in alcohol. The fi rst one or two dorsal spines and membranes of C. mesoleucus are yellow in life, compared to the fi rst three or four of the grey-tailed form.

An early effort was made to fi nd some morphological or meristic difference to separate the two presumed species, but none was detected. Nevertheless, Randall (1998: 233) treated the two as one of 61 Indo-Pacifi c geminate species of fi shes, with an underwater photograph of Chaetodontoplus mesoleucus from Sulawesi as Fig. 41, and Chaetodontoplus sp. from Halmahera as Fig. 42.

In July of 2002, the fi rst author and John L. Earle carried out fi eld research on reef fi shes at Kimbe Bay at the north Fig. 1. Painting of Chaetodontoplus mesoleucus, USNM 182470, Romblon Island, Philippines, Albatross Expedition, 1908 (probable artist, Kumataro shore of New Britain, followed by a dive cruise to Rabaul Ito).

512 THE RAFFLES BULLETIN OF ZOOLOGY 2009 resurrected C. dimidiatus Bleeker from synonymy, noting to the distal tip; caudal-peduncle depth is the least depth, its distribution as the Molucca Islands and the western end and caudal-peduncle length the horizontal distance between of New Guinea. verticals at the rear base of the anal fi n and the caudal-fi n base; lengths of fi n spines and rays are measured from their Tominaga & Yasuda (1975: 82) presented a paper at the extreme base. The scales on the body are small and not in Thirteenth Pacifi c Science Congress at the University of regular rows, so accurate counts cannot be taken. The pored British Columbia in Vancouver, “Revision of the genus lateral-line scales are in two series, the fi rst from the gill Chaetodontoplus (Pomacanthidae) of the world.” They wrote opening to below the posterior base of the dorsal fi n, and in their abstract, “C. mesoleucus and C. niger are different the second mid-laterally on the caudal peduncle. The last in important characteristics from the remaining members of dorsal and anal rays are fully branched to base, but counted Chaetodontoplus and should be excluded from the genus.” as one ray. The rays of the pectoral fi ns were counted on Their revision was never published. In correspondence in both sides. Gill-raker counts were made on the fi rst gill arch 1987 with the fi rst author after the death of Fujio Yasuda, and include rudiments. The raker at the angle is contained Yoshiaki Tominaga wrote, “Both mesoleucus and niger have in the lower-limb count. only one predorsal bone, but I believe these two species are not particularly related.” Pyle (2003: 154, Fig. 2.2) showed In the description of the new species, data in parentheses that C. mesoleucus may have either one or two predorsal refer to paratypes. The data in the table of measurements bones (now termed supraneural bones). His radiographs were of the new species are given as percentages of the standard of specimens of both the yellow and grey-tailed forms. On length. Proportional measurements in the text of the diagnosis checking the x-rays, we fi nd that the grey-tailed specimens and description are rounded to the nearest .05. have one supraneural bone, and the yellow-tailed ones have two. The specimens of C. mesoleucus for the study Genetic Analysis of Tominaga & Yasuda were from Japan where only the yellow-tailed form is found. Nevertheless, C. mesoleucus Total genomic DNA was extracted from tissue samples using and its grey-tailed sister species warrant consideration as the Qiagen DNeasy tissue kit following the manufacturer’s a genus, as does C. niger. A combined morphological and protocol. Segments from the mitochondrial DNA cytochrome genetic study of the classifi cation of the Pomacanthidae is b gene (CytB), and the nuclear encoded S7 intron were planned. amplified for samples from Palau, Papua New Guinea, Philippines and Indonesia. Primers used for amplifi cation and sequencing were 5’ GTG ACT TGA AAA ACC ACC MATERIALS AND METHODS GTT G, 5’ AAT AGG AAG TAT CAT TCG GGT TTG ATG (CytB) and 5’ AAT GGC GAA CCA GAC and 5’ TCA Specimens of the new species of Chaetodontoplus are present TAT TTC TGT TTA CAT CCA ACA A (S7). Polymerase in the collections of the Australian Museum, Sydney (AMS); chain reaction (PCR) and sequencing methods are described Bernice P. Bishop Museum, Honolulu (BPBM); California in detail by Rocha et al. (2008). Academy of Sciences, San Francisco (CAS; SU); Field Museum of Natural History, Chicago (FMNH); Muséum National d’Histoire Naturelle, Paris (MNHN); Museum TAXONOMY Zoologicum Bogoriense, Cibinong, Indonesia (MZB); National Museum of Nature and Science, Tokyo (NSMT); Chaetodontoplus poliourus, new species Royal Ontario Museum, Toronto (ROM); National Museum (Figs. 2, 4–7; Tables 1, 2) of Natural History, Washington, D.C. (USNM); and the Western Australian Museum, Perth (WAM). Chaetodontoplus sp. 1 Kuiter, 1992: 109, Fig. D (Flores). Chaetodontoplus sp. Randall, 1998: 246, Fig. 42 (Halmahera). Lengths of specimens are given as standard length (SL), Chaetodontoplus mesoleucus (non Bloch) Halstead, 2000: 135, measured from the front of the lower jaw to the base of upper Fig. (Papua New Guinea and Solomon Islands). Chaetodontoplus cf mesoleucus Debelius et al., 2003: 132, Figs. the caudal fi n (posterior end of the hypural plate); head A–E (Bali to Flores, Papua New Guinea, Solomon Islands, length (HL) is measured from the same anterior point to Palau). the posterior end of the opercular fl ap; body depth is the greatest depth taken vertically from the internal base of the Material examined. – Holotype: BPBM 39031, male, 81.5 mm spinous portion of the dorsal fi n to the ventral edge of the SL, Papua New Guinea, New Britain, Kimbe Bay, fi rst reef off abdomen; body width is the maximum width just posterior Walindi Plantation, 6–10 m, spear, J. L. Earle, 19 Jul.2002. to the gill opening; snout length is taken from the front of the upper lip to the bony edge or the orbit; orbit diameter Paratypes: USNM 150535, 54.5 mm SL, Solomon Islands, Florida is the greatest bony diameter, and interorbital width the Islands, W. M. Chapman & H. Cheyne, dynamite, 4 May 1944; USNM 169824, 76.0 mm SL, same data as preceding; USNM least bony width; cheek depth is measured from the ventral 169785, 2 ex., 64.0–77.0 mm SL, Solomon Islands, New Georgia, bony edge of the orbit vertically to the ventral margin of the outer reef of Wana-Wana Island and Blacketts Strait, dynamite, W. interopercle; upper-jaw length from the front of the upper M. Chapman & H. Cheyne, 25 Jun.1944; BPBM 6833, 85.0 mm lip to the posterior end of the maxilla; preopercular spine SL, Palau, limestone islet east of Koror, coral reef, 6 m, spear, J. length is the distance from the dorsobasal point of insertion E. Randall, 1 Jun.1968; BPBM 6834, 2 ex., 81.5–92.0 mm SL,

513 Randall & Rocha: A new species of angelfi sh from the Western Pacifi c

Palau, Ngargol Island, west end, coral bottom, 6–12 m, spear, J. E. Randall, 8 Jun.1968; USNM 209956, 81.0 mm SL, Indonesia, Molucca Islands, Saparua, off Kampungmahu, isolated coral patch in 4 m, surrounded by calcareous matrix in 10 m, rotenone, V. G. Springer & M. F. Gomon,18 Jan.1973; AMS I.19881-001, 90 mm SL, Solomon Islands, Sandfl y Passage, Biki Island, coral reef, 20 m, spear, B. Goldman, 24 Jul.1973; USNM 245400, 88.0 mm SL, Indonesia, New Guinea, Papua, Batanta Island, Marchesa Bay, Hawaii Islet, 0°49.8’S 130'56.8"E, 0–6 m, rotenone, RV Alpha Helix, B. B. Collette, 2 Jul.1979; BPBM 32217, 4 ex., 56.0–80.5 mm SL, Indonesia, Flores, off Pertamina oil storage site, Waipare Reef, 8°37'46"S 122°16'35"E, 21 m, rotenone and spear, J. E. Randall, R. H. Kuiter, & L. C. Reynolds, 19 Sep.1987; WAM P.33068- 001, 72.0 mm SL, same data as preceding; BPBM 32239, 2 ex., 60.0–76.0 mm SL, Flores, Wodong Reef, 8°36'10"S 122°25'30"E, 20 m, quinaldine and spear, J. E. Randall, 20 Sep.1987; MZB 17171, 79.5 mm SL, same data as preceding; BPBM 32580, 3 ex.: 76.0–88.0 mm SL, Papua New Guinea, Madang Province, Kranket Fig. 4. Underwater photo of Chaetodontoplus poliourus, Kimbe Bay, New Island, inner lagoon, live coral bottom, 3–4 m, spear, J. E. Randall, Britain (J. E. Randall). 12 Nov.1987; BPBM 32427, 2 ex., 42.0–71.0 mm SL, Madang, off Christiansen Research Institute, spear, P. L. Colin, late 1987; ROM 77374, 75.0 mm SL, Palau, Koror, SSE of Tlutkaraguis Island, off W coast of Ngerubktabel Island, reef between small and

Fig. 5. Head-on underwater photo of Chaetodontoplus poliourus, Kimbe Fig. 2. Chaetodontoplus poliourus, paratype, BPBM 32239, 76.0 mm SL, Bay, New Britain (J. E. Randall). Palau (J. E. Randall).

Fig. 3. Chaetodontoplus mesoleucus, BPBM 32218, 94.0 mm SL, Flores, Fig. 6. Holotype of Chaetodontoplus poliourus, BPBM 39031, 81.5 mm Indonesia (J. E. Randall). SL, Kimbe Bay, New Britain (J. E. Randall).

514 THE RAFFLES BULLETIN OF ZOOLOGY 2009 larger island, 7°17'11.7"N 134°25'34.3"E, 6.1–14.3 m, rotenone, R. Description. – Dorsal rays XII,17 (one of 23 paratypes Winterbottom, W. Holleman, B. Hubley, D. Winterbottom & A. with 16, and one with 18); anal rays III,17 (16 or 17); all Bauman, 26 May 2004; ROM 84401, 77.5 mm SL, same data as dorsal and anal rays branched, the last to base; pectoral holotype; BPBM 40963, 2 ex., 57.0–107.0 mm SL, Palau, Koror, rays 16 (15–17, usually 16), the upper two and lowermost inland channel, 8 m, spear, L. A. Rocha, B. W. Bowen, & M. T. unbranched; pelvic rays I,5; principal caudal rays 17, the Craig, 23 Oct.2006; CAS 227415, 109 mm, MNHN 2009-002, 97.5 mm, NSMT-P 92943, 96.0 mm SL, same data as BPBM 40963; upper and lower unbranched; upper procurrent caudal rays 4, USNM 394206, 89.5 mm SL, Southwest Islands of Palau, Helen the most posterior segmented; lower procurrent caudal rays 3, Reef, east side of lagoon opposite entry channel, just inside of the most posterior segmented; longitudinal scale series about wreck on reef top, 02°51'48"N 131°48'06"E, hard corals, lettuce 80; pored lateral-line scales 32 + 7 (29–35 + 7–9); gill rakers corals, algae on rubble, and sand, 7–23 m, spear, M. W. Westneat 4 + 12; pseudobranchial fi laments 21 (14–23); branchiostegal & J. T. Williams, 16 Sep.2008; FMNH 118117, 89.4 mm SL, same rays 6; vertebrae 10 + 14; supraneural bones 2. data as preceding. Body deep, the depth 1.7 (1.7–1.85) in SL, and compressed, Diagnosis. – Dorsal rays XII,17 (rarely 16 or 18); anal rays the width 3.4 (3.05–3.4) in depth; head length 3.25 (3.15–3.3) III,16 or 17; pectoral rays 15–17 (usually 16); scales small, in SL; dorsal profi le of head forming an angle of about 60°, about 80 in longitudinal series; dorsal series of pored lateral- with a slight concavity above eye and a slight convexity line scales 29–35; gill rakers 4 + 12; supraneural bones 2; before dorsal fi n; snout short, the length 3.0 (2.75–3.1) in body depth 1.70–1.85 in SL; head length 3.15–3.3 in SL; HL; orbit diameter 3.55 (3.1–3.95) in HL; interorbital width fourth to sixth dorsal spines longest,1.1–1.3 in HL; colour in 3.6 (3.35–4.0) in HL; caudal-peduncle depth 2.55 (2.5–2.95) alcohol: head and anterior body pale yellowish grey to an in HL; caudal-peduncle length 6.05 (4.7–6.1) in HL. approximate oblique demarcation connecting base of second to third dorsal spine to anus, gradually changing posteriorly Mouth small, the maxilla reaching to below anterior nostril, in an intermediate zone containing pectoral fi n to one of and strongly oblique when fully closed, forming an angle irregular longitudinal lines on dark brown; a dark brown bar from nape, broadening as it passes through eye, then curving and narrowing as it ends shortly before origin of pelvic fi ns; front of lips brown; dorsal and anal fi ns coloured as adjacent body; caudal fi n abruptly pale grey; paired fi ns pale yellowish; colour in life: dark brown posteriorly with white dots, which merge anteriorly to form narrow irregular white lines; dark brown of body progressively lighter anteriorly, becoming pale grey at demarcation, then gradually changing to pale yellow on head; ocular bar black, narrowly edged in bluish white; snout and chest yellow, the front of lips blue, this colour sometimes continuing as a narrow triangle medially on front of snout; fi rst three to four dorsal spines and membranes yellow, the rest of fi n dark brown with rows of white dots paralleling rays on about basal three-fourths of fi n; a narrow white or blue margin on soft portion of fi n; anal fi n similar, but not yellow anteriorly; caudal fi n grey with a narrow yellow posterior border; pectoral fi ns pale Fig. 8. Underwater photo of Chaetodontoplus mesoleucus, northern Sulawesi grey; pelvic fi ns bright yellow. (J. E. Randall).

Fig. 7. Underwater photo of Chaetodontoplus poliourus, Palau (L. A. Fig. 9. Underwater photograph of Chaetodontoplus mesoleucus, Kerama Rocha). Islands, Okinawa (J. E. Randall).

515 Randall & Rocha: A new species of angelfi sh from the Western Pacifi c of about 60° to horizontal axis of head and body; lower of fi n); caudal fi n densely covered with very small scales; jaw strongly projecting; jaws very protrusible, the angle rays of pectoral fi ns with a row of close-set, quadrangular of mouth reduced to about 20° when jaws fully extended; scales, only those basally on rays with a few cteni; pelvic lips broad, the median depth of upper lip about one-half fi ns with small ctenoid scales on rays. orbit diameter; teeth in jaws in four rows, the inner rows progressively shorter; teeth close-set, long and slender, about Origin of dorsal fi n above fi rst lateral-line scale, the predorsal twice as wide as thick, the tips slightly incurved, expanded length 2.8 (2.7–2.9) in SL; fi rst dorsal spine 2.5 (2.35–3.0) and tricuspid; central cusp of teeth much the largest and in HL; fourth to sixth dorsal spine longest, 1.2 (1.15–1.3) strongly pointed; upper jaw of holotype with 38 teeth in in HL; fi rst dorsal soft ray longest, 1.35 (1.2–1.45) in HL; outer row, and lower jaw with 40 (largest paratype with 34 origin of anal fi n below base of eleventh dorsal spine, the upper teeth and 40 lower teeth); no teeth on palate; tongue preanal length 1.55 in SL; fi rst anal spine 2.0 (1.85–2.4) short and rounded, set far back in mouth; gill membranes in HL; third anal spine longest, 1.35 (1.2–1.45) in HL; narrowly attached to isthmus; gill rakers short, about one- fi rst anal soft ray longest, 1.3 (1.2–1.45) in HL; third to sixth length of gill fi laments. fi fth pectoral rays longest, 1.4 (1.3–1.55) in HL; origin of pelvic fi ns below midbase of pectoral fi ns, the prepelvic Anterior nostril a short fl eshy tubule with small opening a length 2.75 (2.65–2.75); pelvic spine 1.35 (1.3–1.5) in HL; pupil diameter before centre of eye; posterior nostril a narrow fi rst pelvic soft ray longest, reaching posterior to anus, 1.2 elliptical aperture directly dorsoposterior to anterior nostril; (1.05–1.25) in HL. no fl eshy papillae midventrally on head. Colour of holotype in alcohol: head and anterior body A strong spine at corner of preopercle, its length 3.0 (2.6– pale yellowish grey to an approximate oblique demarcation 5.05) in HL; posterior margin of preopercle with 22 (20-38), connecting base of second to third dorsal spines to anus, small, unevenly spaced serrae, some as tiny nodules; lower then gradually changing posteriorly in an intermediate zone margin of preopercle with 10 small serrae on one side of containing pectoral fi n to a pattern of irregular longitudinal holotype and 14 on other (3–15 in paratypes); margin of pale lines on dark brown; a dark brown bar from nape, subopercle with 1 (0–12) small serrae; preorbital with 1 broadening as it passes through eye, then curving and (0–5) small serrae. narrowing as it ends shortly before origin of pelvic fi ns; front of lips dark brown, the dark pigment continuing medially Dorsal part of lateral line strongly arched to middle of body, on front of snout, forming a narrow triangle when viewed then curving downward to end near rear base of dorsal fi n; from the front, the apex above nostrils; dorsal and anal fi ns separate midlateral part of lateral line on caudal peduncle, dark brown as adjacent body except pale yellowish anterior extending about a peduncle length anteriorly; scales on body part of dorsal fi n before an oblique demarcation from base not in regular rows, coarsely ctenoid, with up to 23 cteni, of third dorsal spine to tip of fi fth dorsal spine; caudal fi n continuing as ridges across exposed part of scales; many abruptly pale yellowish grey; paired fi ns pale yellowish, the scales on body with auxiliary scales (also ctenoid); scales membranes translucent. smaller on head, progressively smaller anteriorly; scales extending out on dorsal and anal fi ns as rows of narrow Colour of holotype when fresh as in Figure 6. Figures 4 and oblique ridges, the scales progressively smaller distally; no 5 are underwater photographs of other individuals from the scales on fi rst two dorsal spines and membranes and about type locality of Kimbe Bay, New Britain. Figure 5 shows outer half of next two spines and membranes (naked part of the blue pattern of the lips and snout, as well as the variant fi n not pigmented, in contrast to very dark remaining part with a bright blue margin on the soft portion of the dorsal and anal fi ns (bluish white on holotype).

Etymology. – We have selected the species name poliourus from the Greek meaning grey tail for its most distinguishing colour feature, the predominantly grey caudal fi n.

Genetics. – As mentioned, our earlier efforts to distinguish this species morphologically from the yellow-tailed Chaetodontoplus mesoleucus were not successful, so we decided to check if a molecular difference could be determined. Tissue samples of the new species were obtained from type specimens from New Britain, Indonesia (Raja Ampat) and Palau, and from C. mesoleucus also from Indonesia (collected at the same date and locality as C. poliourus) and from the Philippines (imported for the aquarium fi sh trade).

The genetic analysis revealed a very large difference between Fig. 10. Distribution map of Chaetodontoplus mesoleucus (yellow spots) and C. poliourus (red spots). the species in both mitochondrial (mt) and nuclear DNA

516 THE RAFFLES BULLETIN OF ZOOLOGY 2009 Chaetodontoplus poliourus as percentages of the standard length. n length 21.8 22.4 n 22.9 22.2 24.6 22.8 20.5 21.5 21.4 21.2 20.2 20.6 n length 19.7 20.1 20.1 20.6 19.7 19.5 damaged 19.7 20.9 21.4 21.1 22.4 n n length 27.2 25.1 25.8 25.7 26.7 28.0 26.0 25.7 28.8 28.3 29.7 27.3 n Table 1. Proportional measurements of type specimens Holotype Paratypes Holotype depth width Standard length (mm) 58.2 53.5 56.4 56.6 57.9 57.7 56.0 58.2 58.8 length Body 59.0 58.0 57.9 length Body diameter Head 81.5 17.2 17.2 width 18.5 17.3 16.9 16.8 18.3 18.7 Snout 17.9 BPBM BPBM BPBM BPBM 30.7 ROM BPBM BPBM BPBM 19.0 31.2 BPBM 18.3 18.7 31.6 spine 30.8 31.7 30.8 31.6 30.8 Orbit 10.4 10.0 8.6 32217 9.7 6834 11.4 10.6 30.4 30.4 84401 9.9 9.7 9.1 8.9 8.8 11.6 32580 11.4 10.7 30.8 39031 32217 32427 8.6 8.7 10.5 40963 32239 56 32580 10.0 9.0 8.9 10.8 11.3 10.4 7.5 40963 depth 6834 10.4 8.8 10.5 8.7 12.5 12.4 8.5 7.9 11.7 9.2 8.0 7.9 8.9 Interorbital 11.2 10.2 6.2 12.1 7.8 12.7 10.4 10.2 7.5 12.2 11.6 11.0 8.9 5.5 5.7 12.1 12.6 13.0 10.8 5.7 10.8 11.2 5.2 length 5.6 8.7 6.1 5.1 9.1 5.1 6.5 5.4 8.2 5.5 6.6 Preopercular length Caudal-peduncle 57 spine length Caudal-peduncle spine length Predorsal 35.5 37.3 36.6 36.3 35.6 37.3 37.0 37.2 spine 12.3 dorsal 36.8 12.9 Preanal 60 18.9 13.5 36.4 19.7 34.5 11.7 12.9 12.7 11.5 34.4 20.8 12.3 19.5 64.1 18.6 18.8 18.1 18.4 ray 64.2 12.7 dorsal 18.6 10.8 25.4 Prepelvic 64.8 10.3 27.5 63.7 19.1 36.3 65.5 63.9 64.1 64.2 16.4 27.8 36.7 17.5 64.0 27.5 26.7 26.0 24.8 24.5 37.8 36.7 65.5 24.7 36.9 37.7 36.4 spine 65.0 dorsal 64.6 36.8 25.4 First 23.5 24.8 36.7 36.8 36.7 22.7 23.7 71 spine 26.1 dorsal 24.8 Second 24.2 23.5 21.8 21.9 21.8 22.7 20.8 22.1 spine anal Longest 15.4 15.6 19.5 17.0 22.6 ray 15.2 14.1 13.2 13.7 15.6 anal 24.7 Longest 77.5 13.0 20.9 21.3 20.7 18.7 14.7 18.8 12.8 14.3 19.0 18.0 19.9 anal First 23.0 25.8 25.9 22.9 24.1 24.2 23.4 23.8 21.3 anal 23.4 Second 20.8 26.0 80.5 22.4 22.5 26.8 22.8 24.0 24.4 23.3 22.4 21.5 Third 22.8 23.2 Longest 81.5 length Caudal-fi Pectoral-fi 22.9 22.8 86 23.6 23.3 Pelvic-spine 24.2 22.2 21.0 22.3 22.6 20.7 21.1 Pelvic fi 88 92 107

517 Randall & Rocha: A new species of angelfi sh from the Western Pacifi c

Table 2. Counts of soft rays of fi ns of two species of Chaetodontoplus from the Bishop Museum fi sh collection

Dorsal rays Anal rays Pectoral rays 16 17 18 16 17 18 15 16 17 C. mesoleucus 3 9 1 11 1 1 4 22 C. poliourus 1 22 1 12 12 4 39 5

(nDNA). For the mtDNA, a 757 base pair fragment of the colouration in Japan may be seen in Okamura & Amaoka cytochrome b gene was obtained. There were 46 diagnostic (1997: 404, middle right fi g.). mutations, corresponding to a 6.07% uncorrected sequence divergence between species. This divergence is equal to Allen et al. (1998: 67) reported that Chaetodotoplus or greater than that observed between pairs of closely mesoleucus (they illustrated both mesoleucus and poliourus related sister species of angelfi shes (Bellwood et al., 2004), as yellow-tailed and grey-tailed forms, respectively) feeds wrasses (Rocha, 2004), butterfl yfi shes (Fessler & Westneat, on sponges, tunicates, and algae. 2007), and grunts (Rocha et al, 2008). The nDNA analysis resulted in a 532 base pair segment of the S7 intron in C. Taxonomic notes. – We were concerned that Chaetodon mesoleucus and a 507 base pair segment of the same region atratus Gronow in Gray (1854), with a locality of India, might in C. poliourus. The 25 base pair gap corresponds to an be an earlier name for Chaetodontoplus poliourus. Fraser- insertion or deletion (indel) between positions 220 and 245. Brunner (1933: 550) corrected the locality to Singapore, but This consistent difference in nDNA indicates that there is without explanation. We obtained a photograph of the dried no ongoing hybridization between the two species. skin of the holotype from James Maclaine of the Natural History Museum in London. Only the fi rst dorsal spine and Remarks. – While taking meristic data on additional part of the second is pale, so we confi dently identify this specimens of the two species of Chaetodontoplus, we found taxon as C. mesoleucus. that C. poliourus has modally 16 pectoral-fi n rays, compared to 17 for C. mesoleucus, and a lower average number of There was also a possibility that Holacanthus bicolor var. anal-fi n rays (Table 2). oahuensis Borodin, 1930, placed in the synonymy of C. mesoleucus by Fraser-Brunner, might predate C. poliourus. The distribution of the two species of Chaetodontoplus (Fig. Borodin’s record of this species from Oah’u is obviously a 10) was determined mainly from specimens examined by the locality error, as are three other of his records of fi shes for authors, specimens in the California Academy of Sciences the Hawaiian Islands (Mundy, 2005: 406). His holotype, examined for the authors by David Catania and Richard L. formerly in the Vanderbilt Marine Museum and now in the American Museum of Natural History, was examined Pyle, underwater photographs taken by the fi rst author (Figs. by Richard L. Pyle (pers. comm.), who identifi ed it as C. 8, 9), and the following localities for C. poliourus provided by mesoleucus. Gerald R. Allen from his fi eld work in Indonesia and Papua New Guinea: Cenderwasihi Bay, Milne Bay, D’Entrecasteaux Material of Chaetodontoplus mesoleucus examined. Islands, Woodlark Island, Louisade Archipelago, Manus – INDONESIA: New Guinea, Papua Barat Province, Island, and the northern tip of New Ireland. He added the Waigeo, SU 26739, 81.0 mm SL; Sulawesi, off Kendari, following localities for the Solomon Islands: Choiseul, BPBM 26755, 94.0 mm SL; Flores, Maumere Bay, BPBM Shortland Islands, Russell Islands, and Guadalcanal. He 32218, 94.0 mm SL, BPBM 32240, 2 ex, 107.0–123.0 mm found both species at the islands of Misool and Kofi au off SL; Komodo, BPBM 32371, 2 ex., 85.0–97.0 mm SL; Java, mesoleucus the western end of New Guinea where C. was by Karimundjawa Islands, USNM 280046, 5 ex., 35.0–94.0 far the most common. Conversely, C. poliourus was relatively mm SL, USNM 280048, 6 ex., 32.0–95.0 mm SL; Seribu common along the west side of Halmahera, but only one Islands, USNM 280045, 3 ex., 68.0–92.0 mm SL, USNM individual of C. mesoleucus was observed (at Widi Islands, 280047, 2 ex., 74.0–76.0 mm SL. SINGAPORE, CAS 88113, 0°33.4'S, 128°20.6'E). Other Allen records for C. mesoleucus 2 ex., 65.0–94.0 mm SL. VIETNAM, Nha Trang Bay, CAS include Banggai Island off eastern Sulawesi and the Kimberly 88117, 59.0 mm SL. MALAYSIA, Sabah, Darvel Bay, coast of Western Australia at Cape Bougainville. John L. USNM 345093, 3 ex., 87.0–92.0 mm SL. PHILIPPINES Earle (pers. comm.) observed both species at Raja Ampat (from the aquarium fi sh trade), BPBM 10571, 94.0 mm and at Komodo. He wrote, “They are often observed on SL; BPBM 10922, 4 ex., 42.0–85.0 mm SL; BPBM 40968, the same dive, however not in the same micro-habitat, and 2 ex., 68.0–84.0 mm SL; Sulu Archipelago, Tawi-Tawi, never as mixed species pairs”. SU 25833, 140.0 mm SL; Siluag, CAS 4954l, 107.0 mm SL; Jolo, SU 25832, 2 ex., 110.0–120.0 mm SL; Palawan, Masuda & Kobayashi (1994: 206, Fig. 4) illustrated a juvenile Puerto Princessa Bay, USNM 260909, 74.0 mm SL; Cebu, of C. mesoleucus, 25 mm total length, from a photo taken SU 28531, 125.0 mm SL; Negros, CAS 52746, 107.0 mm at the Yaeyama Islands, Japan. The northernmost record for SL; East of Bais, USNM 280050, 104.0 mm SL; Busuanga, C. mesoleucus is that of Masuda et al. (1975: 314, pl. 12a) FMNH uncat., 90.0 mm SL; Mindoro, SU 29627, 2 ex., from the Amami-Ô-Shima Islands. Another example of live 107.0 mm SL.

518 THE RAFFLES BULLETIN OF ZOOLOGY 2009

ACKNOWLEDGEMENTS Fessler, J. L., & M. W. Westneat, 2007. Molecular phylogenetics of the butterflyfishes (Chaetodontidae): Taxonomy and We thank foremost Gerald R. Allen for providing many biogeography of a global coral reef fi sh family. Molecular Phylogenetics and Evolution 45 records of both Chaetodontoplus mesoleucus and C. poliourus , : 50–68. for this study. He has long suspected they were species, Fowler, H. W. & B. A., Bean, 1929. The fishes of the series not colour morphs. Special thanks are also due Jeffrey T. Capriformes, Ephippiformes, and Squamipennes, collected by the United States Bureau of Fisheries Steamer “Albatross,” Williams, Lisa Palmer and Erika Wilbur of the National chiefl y in Philippine seas and adjacent waters. Bulletin of the Museum of Natural History for providing photographs and United States National Museum, 100, vol. 8: xi + 352 pp. information on specimens, and John L Earle for collecting Fraser-Brunner, A., 1933. A revision of the chaetodont fi shes of the holotype of C. poliourus at New Britain, taking tissue the subfamily Pomacanthinae. Proceedings of the Zoological samples of both species at Raja Ampat, and sharing his Society of London, 103 (3): 36–599. observations. We are also grateful to James Maclaine of Gray, J. E., 1854. Catalogue of fi sh collected and described by the Natural History Museum in London, David Catania and Laurence Theodore Gronow, now in the British Museum. British Mysi Hoang of the California Academy of Sciences, Mary Museum, London. vii + 196 pp. Anne Rogers and Mark W. Westneat of the Field Museum Günther, A., 1860. Catalogue of the Acanthopterygian Fishes in the of Natural History, Amanda Hay of the Australian Museum, Collection of the British Museum. British Museum, London. and Richard L. Pyle, Loreen R. O’Hara, and Arnold Y. xxi + 548 pp. Suzumoto for information on specimens in their care. We Halstead, B., 2000. Coral Sea Reef Guide. Sea Challengers, acknowledge as well the valuable gifts of C. mesoleucus Danville, California. 321 pp. from Coral Fish Hawaii and Modern Pet Center, Honolulu. The manuscript was reviewed by John L. Earle and Helen A. Herre, A. W. & H. R. Montalban, 1927. The Philippine butterfl yfi shes and their allies. The Philippine Journal of Science, 34 (1): Randall. The genetic analysis and fi eld trips by the second 1–113, pls. 1–24. author were fi nancially supported by the HIMB-NWHI Coral Reef Research Partnership (NMSP MOA 2005-008/66882 Kuiter, R. H., 1990. A new species of angelfi sh (Pomacanthidae), Chaetodontoplus meredithi from eastern Australia. Revue to Brian W. Bowen), and the National Science Foundation française d’Aquariologie Herpetologie, 16(4)[1989]: 113– (grant OCE-0453167 to Brian W. Bowen). 116. Kuiter, R. H., 1992. Tropical Reef-Fishes of the Western Pacifi c Indonesia and Adjacent Waters. Penerbit Pt Gramedia Pustaka LITERATURE CITED Utama, Jakarta. xiii + 314 pp.

Allen, G. R., R. Steene & M. Allen, 1998. A Guide to Angelfi shes Lacepède, B. G. E., 1802. Histoire Naturelle des Poissons, vol. 4: & Butterfl yfi shes. Odyssey Publishing, Australia. 250 pp. xliv + 728 pp, Chez Plassan, Paris. Allen, G. R. & R. Steene, 2004. Chaetodontoplus vanderloosi, a Masuda, H., Araga, C. & Yoshino, T., 1975. Coastal Fishes of new species of angelfi sh (Pomacanthidae) from Papua New Japan. Tokai University Press, Tokyo. 381 pp. + 142 pls. Guinea. aqua, Journal of Ichthyology and Aquatic Biology, Masuda, H. & Kobayashi, Y., 1994. Grand Atlas of Life Fish Modes. 8 (1): 23–30. Tokai University Press, Tokyo. 465 pp. In Japanese. Bellwood, D. R., L. van Herwerden, & N. Konow, 2004. Mundy, B. C., 2005. Checklist of the fishes of the Hawaiian Evolution and biogeography of marine angelfi shes (Pisces: Archipelago. Bishop Museum Bulletin in Zoology, 6: 704 pp. Pomacanthidae). Molecular Phylogenetics and Evolution, 33: 140–155. Munro, I. S. R., 1967. The Fishes of New Guinea. Department of Agriculture, Stock and Fisheries, Port Moresby. xxxvii + Bleeker, P., 1876. Systema Percarum revisum. Pars II. Archives 651 pp., 78 pls. Neerlandais de Sciences Naturelles, Haarlem, 11: 289–340. Okamura, O. & K. Amaoka, 1997. Fishes of Japan. Yama-Kei Bleeker, P., 1877–1878. Atlas Ichthyologique des Indes Orientalis Publishers, Co., Tokyo. 783 pp. In Japanese. Néêrlandaises. Vol. 9. Fréderic Muller et C°, Amsterdam. 80 pp., pls. 355–420. Pyle, R. L., 2003. A Systematic Treatment of the Reef-Fish Family Pomacanthidae (Pisces: Perciformes). PhD thesis, University Bloch, M. E., 1787. Naturgeschichte der ausländischen Fische, vol. of Hawaii, Honolulu. xvi + 419 pp. 3. J. Morino & Comp., Berlin. x + 146 pp., 15 pls. Pyle, R. L. & Randall, J. E., 1994. A review of hybridization in Borodin, N. A., 1930. Scientific results of the yacht “Ara” marine angelfi shes (Perciformes: Pomacantidae). Environmental Expedition during the years 1926 to 1930, while in command Biology of Fishes, 41: 127–145. of William K. Vanderbilt. Fishes. Bulletin of the Vanderbilt Marine Museum, 1 (2): 39–64. Randall, J. E., 1998. Zoogeography of shore fi shes of the Indo-Pacifi c Chan, W. L., 1969. Two new pomacanthid angelfi shes from the region. Zoological Studies, 37 (4): 227–269, 21 pls. Macclesfi eld Bank, South China Sea. Annals and Magazine of Rocha, L. A., 2004. Mitochondrial DNA and color pattern variation Natural History, ser. 13, 8: 325–334. in three western Atlantic Halichoeres (Labridae), with the Cuvier, G. & Valenciennes, A., 1831. Histoire Naturelle des revalidation of two species. Copeia, 2004 (4)s: 770–782. Poissons, vol. 7. F. G. Levrault, Strasbourg. xxix + 531 pp., Rocha, L. A., K. C. Lindeman, C. R. Rocha & H. A. Lessios, 2008. 38 pls. Historical biogeography and speciation in the reef fi sh genus Debelius, H., H. Tanaka & R. H. Kuiter, 2003. Angelfi shes. A Haemulon (Teleostei: Haemulidae). Molecular Phylogenetics Comprehensive Guide to Pomacanthidae. TMC Publishing, and Evolution, 48: 918–928. Chorleywood, UK. 208 pp. Shen, S.-C. & P.-C. Lim,1975. An additional study on chaetodont fi shes (Chaetodontidae) with description of two new species.

519 Randall & Rocha: A new species of angelfi sh from the Western Pacifi c

Bulletin of the Institute of Zoology Academia Sinica (Taipei), Whitley, G. P., 1959. More ichthyological snippets. Proceedings 14 (2): 79–105. of the Royal Zoological Society of New South Wales, 1957- Tominaga, Y. & F. Yasuda, 1975. Revision of the genus 58: 11–26. Chaetodontoplus (Pomacanthidae) of the world. Records of Yasuda, F. & Y. Tominaga, 1976. A new pomacanthid fish, the Proceedings of the Thirteenth Pacifi c Science Congress, Chaetodontoplus caeruleopunctatus, from the Philippines. Vancouver, vol. 1: 82–83 (abstract). Japanese Journal of Ichthyology 23 (3): 130–132.

520 THE RAFFLES BULLETIN OF ZOOLOGY 2009

THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 521–525 Date of Publication: 31 Aug.2009 © National University of Singapore

A NEW BANDFISH, OWSTONIA SARMIENTO (PISCES: PERCIFORMES: CEPOLIDAE: OWSTONIINAE), FROM THE PHILIPPINES WITH A KEY TO SPECIES OF THE GENUS

Yun-Chih Liao Biodiversity Research Center, Academia Sinica, Nankang, 115 Taipei, Taiwan, Republic of China Email: fi [email protected]

Rodolfo B. Reyes Jr. The WorldFish Center, Khush Hall, International Rice Research Institute, Los Baños, Laguna, Philippines Email: [email protected]

Kwang-Tsao Shao Biodiversity Research Center, Academia Sinica, Nankang, 115 Taipei, Taiwan, Republic of China Email: [email protected] (Corresponding Author)

ABSTRACT. – A new bandfi sh, Owstonia sarmiento, is described from specimens collected off East Luzon, Philippines at about 200–300 m depth during the AURORA 2007 Expedition. It differs from other known congeneric species in having more dorsal fi n rays, two anal spines, more vertebral counts, and the least lateral row scale counts. The species is described (colour photo and radiograph included) and a diagnostic key to species of the genus is provided.

KEY WORDS. – Owstonia sarmiento, Owstonia, Cepolidae, new species, Philippines, deep-sea fi sh.

INTRODUCTION form a loop. Currently, there are fi ve species in this genus viz. Owstonia dorypterus (Fowler, 1934a), O. maccullochi Species of the genus Owstonia and its allied species (e.g., Whitley, 1934, O. microlepis Fowler, 1934b, O. totomiensis Sphenanthias) belong in the family Cepolidae (Smith-Vaniz, Tanaka, 1908, and O. weberi (Gilchrist, 1922). However, 1986, 2001; Nakabo, 2002). There are about 12 nominal formally nominal species including O. grammodon (Fowler, Owstonia species recorded in the family (Froese & Pauly, 1934b), O. macrophthalmus (Fourmanoir, 1985), O. 2008). Owstonia has been proposed as a monophyletic nigromarginatus (Fourmanoir, 1985), O. pectinifer (Myers, group, the family Owstoniidae (Smith, 1968; Mok, 1988), 1939), O. simoterus (Smith, 1968), O. tosaensis Kamohara, but currently is treated as the subfamily Owstoniinae 1934, and O. whiteheadi Talwar, 1973, were proposed in the family Cepolidae (Smith-Vaniz, 2001). Five belonging to the genus Sphenanthias with typological genera were placed in this group viz. Owstonia (Tanaka, species S. sibogae Weber, 1913 (Smith, 1968; Smith-Vaniz, 1908), Sphenanthias (Weber, 1913), Parasphenanthias 2001). (Gilchrist, 1922) Loxopseudochromis (Fowler, 1934a) and Opsipseudochromis (Fowler, 1934a) (Smith, 1968; Smith-Vaniz, 2001). Among them, Loxopseudochromis, MATERIALS AND METHODS Sphenanthias, and Parasphenanthias were considered as synonyms of Owstonia (Smith, 1968; Smith-Vaniz, 1986), Specimens were collected during the AURORA 2007 and Opsipseudochromis was a synonym of Sphenanthias, Expedition, one of the series of deep-sea expeditions tentatively considered as a valid genus (Smith, 1968). around the Philippines of the Census of Philippines Deep- We follow the classifi cation by Smith-Vaniz (2001) and Sea Biodiversity. This was part of the Census of Margins recognize two genera, Owstonia and Sphenanthias, in the (CoMarge) theme of the Census of Marine Life. The trawls Owstoniinae. The most important difference between these were conducted and operated by the Research Vessel MV two genera is that in Owstonia the lateral lines of the sides DA-BFAR belonging to the Bureau of Fisheries and Aquatic of the body join as a loop in front of the dorsal fi n, while Resources, Department of Agriculture (Philippines). The in Sphenanthias, the lateral lines are separate and do not research institutions participating in this project included

521 Liao et al.: A new species of Owstonia from the Philippines the National Museum of the Philippines, the Muséum 1922), O. dorypterus (Fowler, 1934a), O. microlepis national d’Histoire naturelle, Paris, France, the National (Fowler, 1934b), and O. maccullochi Whitley, 1934. Among Museum of Natural History (NMNH), Washington, D.C., them, O. microlepis was synonymized with O. weberi, and USA, the Institute of Marine Biology, National Taiwan O. maccullochi was synonymized with O. totomiensis, Ocean University, and Department of Biology, National respectively (Smith, 1968, Smith-Vaniz, 1986; 2001). University of Singapore. Staff members and students of However, they were included in this genus and in the the Biodiversity Research Center, Academia Sinica, were key to species with parentheses for reference (see below). invited to join in and take charge of the study of the fi shes Furthermore, as mentioned above (Smith-Vaniz, 2001), obtained during the expedition. other species, (i.e., O. grammodon (Fowler, 1934b), O. macrophthalmus (Fourmanoir, 1985), O. nigromarginatus Two types of trawls were used in the survey, the 4.2 meter- (Fourmanoir, 1985), O. pectinifer (Myers, 1939), O. wide French-type beam trawl and the otter trawl (head line simoterus (Smith, 1968), O. tosaensis Kamohara, 1934, of 12.40 m). The survey was conducted using the Research and O. whiteheadi Talwar, 1973), formerly belonged Vessel MV DA-BFAR of the Bureau of Fisheries and to the genus Owstonia should be referred to the genus Aquatic Resources, Department of Agriculture (Philippines). Sphenanthias. Photos of freshly dead specimens were taken before tissue samples were collected. Tissue samples were collected and fi xed in absolute ethanol. Voucher specimens were fi xed Key to species of Owstonia sensu Smith (1968) in 10% formalin and then transferred to 70% ethanol for long-term preservation. Type specimens were deposited 1 Lateral series of scales from gill opening to caudal base less in the National Museum of the Philippines (PNMI) and than or equal to 44 ...... 2 the Biodiversity Research Museum, Biodiversity Research – Lateral series of scales from gill opening to caudal base more Center, Academia Sinica, Taiwan (ASIZP, the formerly than 45, about 55–60 ...... O. totomiensis (O. maccullochi) 2 Pelvic fi n long, attending to anal fi n base; anal fi n with one Institute of Zoology, Academia Sinica). Measurement spine ...... 3 follows Nakabo (2002). Abbreviations used in this paper are – Pelvic fi n short, not extending to anal fi n base; anal fi n with as follows: SL, standard length; AMS, Australian Museum, two spines ...... Owstonia sarmiento, new species Sydney; ANSP. Academy of Natural Sciences, Philadelphia; 3 Gill raker upper 9 and lower 15 ...... O. dorypterus FMNH, Field Museum of Natural History, Chicago; – Gill raker upper 14–17 and lower 28–30 ...... SAIAB, South African Institute of Aquatic Biodiversity ...... O. weberi (O. microlepis) (also RUSI, J. L. B. Smith Institute of Ichthyology, South Africa), Grahamstown; NMNH, National Museum of Natural History (also USNM), Washington, D.C. Owstonia sarmiento, new species (Table 1, Figs. 1 A & 1B)

TAXONOMY Material examination. – Holotype, PNMI 17006 (ASIZP0067939), 61 mm SL, 21 May 2007, CP2667-003, Aurora, East Luzon, Owstonia Tanaka, 1908 Philippines, 15.93°N 121.78°E, 307–292 m, French-type beam trawl, coll. MV DA-BFAR. Owstonia Tanaka, 1908: 46 (type species Owstonia totomiensis) Paratypes. – ASIZP0068216, 64 mm SL, 2 Jun.2007, CC2743- Loxopseudochromis Fowler, 1934a: 354 (type species 020, Aurora, East Luzon, Philippines, 16.02°N 121.85°E, 302–309 Loxopseudochromis dorypterus). m, otter trawl, coll. MV DA-BFAR; – ASIZP0067820, 63 mm Parasphenanthias Gilchrist, 1922: 69 (type species SL, 20 May 2007, CP2656-004, Aurora, East Luzon, Philippines, Parasphenanthias weberi). 16.03°N 121.88°E, 262–278 m, French-type beam trawl, coll. MV Sphenanthias Weber, 1913: 210 (type species Sphenanthias DA-BFAR; – ASIZP0068380, 63 mm SL, 20 May 2007, CP2656- sibogae). 004, Aurora, East Luzon, Philippines, 16.03°N 121.88°E, 262–278 m, French-type beam trawl, coll. MV DA-BFAR. Remarks. – Genus Owstonia is characterized by large head, compressed body tapering posteriorly; cycloid Diagnosis. – Dorsal-fi n rays III 23, Anal-fi n rays II 14, scales; large and oblique mouth; maxillary exposed, no Pectoral-fi n rays 19, Pelvic-fi n rays I 5, caudal rays 17–19, supplemental bone; teeth curved, uniserial in jaws with vertebrate counts 29. Branchiostegal rays 6; gill rakers cluster at lower symphysis, palatine and vomer teeth absent; 13–14 (upper) +1(middle) +26–28 (lower). Scales: cheek six branchiostegals, gill opening wide, gill rakers long and with 2–3 rows of 8–10 scales, lateral rows of scale from numerous; anal and dorsal fi ns long, spines slender, caudal gill opening to caudal 27–30 and 3 more scales on caudal fin long with middle rays elongated, pectoral fin short; fi n, lateral line scales 23–29 connected in front of dorsal sensory canals of head prominent; lateral line runs close fi n, other 4 lateral scales downward to gill opening, pre- to dorsal base and ends before caudal peduncle (Smith, dorsal scales 2. Pelvic fin short, not extending to anal 1968). fi n base. Reddish in color, outer margin of fi ns whitish, black pigmentation between membrane of maxilla and There are about fi ve species included in this genus, viz. premaxilla. Owstonia totomiensis Tanaka, 1908, O. weberi (Gilchrist,

522 THE RAFFLES BULLETIN OF ZOOLOGY 2009 9 19 I + 5 29 + 3 29 + 4 19 2 + I + 5 Liao et al., 2009 19 10 I + 5 28 + 4 23 + 4 19 I + 5 21 I + 5 maccullochi 19 I + 5 45 + 6 60 + 4 24 + 4 microlepis 28 I + 5 I + 14 I + 14 I + 14 II + 14 II + 14 II + 14 II + 14 Owstonia (after Fowler, 1934a). 38 + 4 39 + 4 51 + 5 29–30 + 3 27-28 + 3 27 + 3 1 + 18 dorypterus 20 I + 5 I + 14 40 + 4 weberi (29–30) 11072-3 21 N/A (14–15) + 1 9 + 25 16 + 1 31 17 + 1 30 13 + 1 27 14 + 1 26 13 + 1 26 14 + 1 28 I + 5 I + 14 III + 21 III + 21 III + 21 III + 21 III + 22 III + 23 III + 23 III + 23 III + 23 Owstonia Owstonia Owstonia Owstonia Owstonia Owstonia samiento , new species Tanaka, 1908 Gilchrist, 1922 (Fowler, 1934) (Fowler, 1934) Whitley, 1934 FMNH 55424 SAIAB(RUSI) USNM 93166 ANSP 54940 AMS IA5815 ASIZP0067939 ASIZP0068216 ASIZP0067820 ASIZP0068380 c Name S 2 2 8 6 6 9 P2 Caudal 19 18 19 17 15 17 Vert 29 N/A 29 17 28 14 28 N/A Br 27-28 28 GR 6 6 6 6 6 6 Cheek scales absent (lost) 3–4 rows 6 rows 3 rows = 18 5 rows = 40 8 P1 Author Type(s) D A

Table 1. Comparision of the characters species genus Scientifi Pred Lateral row scales 55 + 5 Lateral line scales 52 + 4 37 + (7) totomiensis

523 Liao et al.: A new species of Owstonia from the Philippines

Description. – Body compressed and elongated, tapering dorsal fi n rays and vertebral counts; lower lateral row scale posteriorly. Head large, 26–28% in SL; body depth 24–25% counts than for other species of the genus; pelvic fi n short, in SL. Eye large, 44–50% in HL, inter-orbital distance not extending to anal fi n base. Even though it is similar to O. 32–35% in HL. Mouth large, posterior maxilla not extended dorypterus and O. weberi in having fewer lateral row scale to posterior margin of eye. Fin rays and spines counts: dorsal counts, O. sarmiento differs from O. dorypterus in having fi n III 23, anal fi n II 14, pectoral fi n 19 rays, pelvic fi n I fewer cheek scales (2–3 rows vs. 6 rows in O. dorypterus); 5, caudal fi n 17–19 rays and a few accompanying short more gill rakers; and fewer lateral row scales and lateral rays on the upper and lower margin. Vertebral counts 29. line scales (Table 1). Owstonia sarmiento differs from O. Branchiostegal 6, gill rakers upper 13–14, middle 1, and weberi in having more caudal rays; fewer cheek rows and lower 26–28. Scales: cheek 2–3 rows, 8–10 scales; lateral scales, and fewer lateral row scales. row scales start from gill opening to caudal fi n with 27–30 scales and 3 more scales covered on caudal fi n base; dorsal According to the defi nition of the genus by Smith (1968) lateral line scale 23–29 along dorsal fi n base and connected and Smith-Vaniz (2001), fi ve species were included, viz. in front of dorsal fin, another 4 tube-like lateral scales Owstonia totomiensis Tanaka, 1908, O. weberi (Gilchrist, extended downwards to upper margin of gill opening; pre- 1922), O. dorypterus (Fowler, 1934a), O. microlepis (Fowler, dorsal scales 2. Scales cycloid with 7–10 radii. Pelvic fi n 1934b), and O. maccullochi Whitley, 1934. However, O. short, not extending to anal fi n base. microlepis and O. maccullochi were synonymized with O. weberi and O. totomiensis, respectively (Smith, 1968; Colouration. – Body reddish when fresh, eyes orange, Smith-Vaniz, 1986, 2001). After examination of the type operculum and maxilla reddish to whitish, membrane specimens, we concur with the synonymy. Including O. between maxilla and pre-maxilla entirely pigmented, sarmiento described here, there are now four species in membrane between maxilla and posterior lower jaw Owstonia. pigmented, pectoral fi ns reddish, pelvic fi ns whitish; dorsal, anal, and caudal fi ns reddish with white outer margin and Comparative material. – Owstonia totomiensis, FMNH one red band along the basal of white margin; belly whitish. 55424 (Holotype), 315 mm, 10 Feb.1906, Totomi, Honda, Colour in alcohol nearly uniformly whitish. Japan; NTUM 6857, 373 mm, 9 Jun.1987, NE Taiwan; – Owstonia weberi, SAIAB(RUSI) 11072–3 (Syntype), Distribution. – Currently known only from the type locality 106–175 mm, Durban, South Africa, 2 Jul.1920; – Owstonia in the Philippines. microlepis, ANSP 54940 (Holotype), 265 mm, Durban, Natal, South Africa, 1932; – Owstonia maccullochi, AMS Etymology. – This new species is named after the director of IA5815 (Holotype), 162 mm, NSW, Sydney, Australia, 238 the Bureau of Fisheries and Aquatic Resources (Philippines), m depth. Malcolm Sarmiento, for his support in making this exploration of deep-sea fauna in the Philippines possible. The species name is used as a noun in apposition. ACKNOWLEDGEMENTS

We would like to thank the Bureau of Fisheries and Aquatic DISCUSSION Resources (BFAR), of the Department of Agriculture, Philippines, for their blessing and permission for the Owstonia sarmiento is unique in having the following expedition. Thanks to the offi cers and crew of the Research characters: anal fi n with two spines rather than one; more Vessel MV DA-BFAR for their hard work during the expedition. Special thanks to the leader of the expedition, P. Bouchet (Museum Nationale d’Histoire Naturelle, Paris, France) and Marivenne Manuel-Santos (National Museum of the Philippines, Manila) for their great efforts. In addition, we would also like to thank Betrand Richer de Forges, New Caledonia and Jean-François Barazer, IRD, Nouméa, New Caledonia; Noel Saguil, and R. Ramiscal (Philippines), for their help. M.-Y. Lee (Academia Sinica, Taiwan) assisted with radiography. The following kindly assisted with specimen examinations: M. A. Rogers and W. L. Smith and M. Westneat, FMNH; R. Bills and O. Gon, SAIAB; K. Lundberg, M. S. Pérez and R Meyer, ANSP; K. Matsuura and T. Kawai, National Museum of Nature and Science, Tokyo. Travel support to Y.-C. Liao was provided by the Biodiversity Research Museum, Academia Sinica, Taiwan. This expedition was supported by the Lounsbery Foundation, USA.

Fig 1. Owstonia sarmiento, new species, holotype, PNMI 17006 (ASIZP0067939), 61 mm SL: A, colour photograph; B, radiograph.

524 THE RAFFLES BULLETIN OF ZOOLOGY 2009

LITERATURE CITED Nakabo, T., 2002. Cepolidae. In: Nakabo, T. (ed.), Fishes of Japan with pictorial keys to the species (English edition). Tokai Fowler, H. W., 1934a. Descriptions of new fishes obtained University. v. 2: Pp. i–vii + 867–1749. 1907 to 1910, chiefl y in the Philippine Islands and adjacent Smith-Vaniz, W. F., 1986. Cepolidae. In: Smith, M. M., & P. seas. Proceedings of the Academy of Natural Sciences of C. Heemstra (eds.), Smiths’ Sea Fishes. Smith Institute of Philadelphia, 85: 233–367. Ichthyology, Grahamstown. Pp. 727–728. Fowler, H. W., 1934b. Fishes obtained by Mr. H. W. Bell-Marley Smith-Vaniz, W. F., 2001. Cepolidae. In: Carpenter, K. E., & chiefl y in Natal and Zululand in 1929 to 1932. Proceedings V.H. Niem (ed.), FAO species identifi cation guide for fi shery of the Academy of Natural Sciences of Philadelphia, 86: purposes. The living marine resources of the Western Central 405–514. Pacifi c. FAO, Rome. Pp. 3331–3332. Froese, R. & D. Pauly, 2008. FishBase. World Wide Web Smith, J. L. B., 1968. New and interesting fi shes from deepish water electronic publication. www.fi shbase.org, version (04/2008). off Durban, Natal and southern Mozambique. Investigational Gilchrist, J. D. F., 1922. Deep-sea fi shes procured by the S.S. Report No. 19. Oceanographic Research Institute, Durban. "Pickle" (Part I). Report Fisheries and Marine Biological Pp. 1–30. Survey, Union of South Africa Rep., 2 (part 3): 41–79, Pls. Tanaka, S., 1908. Notes on some Japanese fi shes, with descriptions 7–12. of fourteen new species. Journal of the College of Science, Mok, H. K., 1988. Osteological evidence for the monophyly of Imperial University of Tokyo, 23 (part 7): 1–54. Cepolidae and Owstoniidae. Japanese Journal of Ichthyology, Weber, M., 1913. Die Fische der Siboga-Expedition. E. J. Brill, 34(4): 507–508. Leiden. Fische Siboga Expedition. Pp. i-xii + 1–710, Pls. Myers, G. S., 1939. A new Owstoniid fi sh from deep water off 1–12. the Philippines. Proceedings of the Biological Society of Washington, 52: 19–20.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 527–535 Date of Publication: 31 Aug.2009 © National University of Singapore

NEW SPECIES AND NEW RECORDS OF BORNEAN FROGS (AMPHIBIA: ANURA)

Robert F. Inger & Robert B. Stuebing The Field Museum, 1400 South Lake Shore Drive, Chicago 60605, USA

ABSTRACT. – One hundred fi fty four species of frogs have been recorded from Borneo and the number continues to grow. In this paper we describe two new species, Ansonia echinata and Pelophryne saravacensis (Bufonidae), and a new form of bufonid tadpole. In addition we report on a signifi cant range extension for Meristogenys whiteheadi (Ranidae) and ecological differentiation of two species of the Rana chalconota complex (Ranidae).

KEY WORDS. – Borneo, frogs, new species, geographic & ecological distribution.

INTRODUCTION in 95% ethanol before specimens were placed in formalin. Adults were transferred to 70% ethanol after three to Despite more than fi fty years of rather intensive surveys of fi ve months. Tadpoles remain in formalin. The following the anuran fauna of Borneo, it is clear that much remains measurements of adults were made with a Mitutoyo calipers to be learned both of the number of species that constitute graduated to 0.01 mm: snout-vent length (SVL), tibia length the fauna and of the distributions of those species. One (T) made with the leg fl exed, head width (HW) made at hundred fi fty four species of anurans are currently known the rear of the head. Four measurements on adults were from the island and the number continues to grow. Here made with an ocular micrometer at 12X magnification: we describe two new species of the family Bufonidae and eye diameter, tympanum diameter (TYM), snout length a new form of tadpole of the same family. In addition we from the anterior border of the eye to the tip of the snout, report on a signifi cant range extension of one of the known width of the disc of the third fi nger (dF3). Measurements species (Meristogenys whiteheadi, Family Ranidae)and on on tadpoles were also made using the ocular micrometer ecological distributions of a pair of recently differentiated at 12X magnifi cation: head-body length, head-body width, species (Rana chalconota group, Family Ranidae). total length. Tadpoles were staged using the system of Gosner (1960). We use FMNH as the acronym for The This new information results from our effort to characterize Field Museum. the anuran fauna of a newly developing plantation area of Acacia mangium in west-central Sarawak. Sixty fi ve days Total genomic DNA was extracted from tissues to verify spread over four years were devoted to fi eld work in this association of certain tadpoles with species of adults. area of exotic and natural vegetation, resulting in the fi nding PureGene Animal Tissue DNA Isolation Protocol (Gentra of 45 species of anurans. These frogs were encountered in Systems, Inc.) was used for the extraction. For two larvae plots of Acacia or in the original secondary forests that are of Meristogenys species (FMNH 272643, 272658) and three intercalated between Acacia plots. We also spent 27 days adults of Meristogenys whiteheadi (FMNH 272624, 272628 total in two forested sites peripheral to the plantation area, from Bukit Kana and FMNH 238286 from Purulon, Tenom where 42 species were discovered, including 17 not found District, Sabah) a 442–443 bp fragment of mitochondrial within the plantation area. DNA that encodes part of the 12S rRNA gene was amplifi ed by the polymerase chain reaction (PCR) following Shimada et al., (2007). For three tadpoles of the Rana chalconota MATERIAL AND METHODS species group (FMNH 272647, 272678, 272682), two adult Rana megalonesa (FMNH 272605, 272867), and three Specimens were caught by hand or, in the case of larvae, adult Rana raniceps (FMNH 272602-04) a 572-576 bp by use of electro-fi shing in strong currents and dip nets in fragment of mitochondrial DNA that encodes part of the standing water. Specimens were preserved in 10% formalin. 16S rRNA gene was amplifi ed by PCR using the primers Liver tissue (adults) or tail clips (tadpoles) were preserved L-16SRana (5’-CCTACCGAGCTTAGAGATAGC-3’)

527 Inger & Stuebing: New species and new records of Bornean frogs and H-16SRanaIII (Stuart et al., 2006). PCR products RESULTS were electrophoresed in a 1% low melt agarose TALE gel stained with ethidium bromide and visualized under Ansonia echinata, new species (Bufonidae) ultraviolet light. The bands containing DNA were excised (Figs. 1, 2) and agarose was digested from bands using GELase (Epicentre Technologies). PCR products were sequenced Holotype. – FMNH 272784, collected at Bukit Kana, Bintulu in both directions by direct double strand cycle using Big Division, Sarawak (2°39.363'N 112°54.219'E), on 28 Mar.2007, Dye version 3 chemistry (Perkin Elmer). Cycle sequencing by Leong Tzi Ming, Freddy Julus, Patrick Francis, and Jacinta products were precipitated with ethanol, 3 M sodium Richard. This specimen was collected at night perched on dead leaves at the edge of a small stream (3 m wide) in primary rain acetate, and 1225 mM EDTA, and sequenced with a 3730 forest. DNA Analyzer (ABI). Sequences were edited and aligned using Sequencher v. 4.1 (Genecodes). Sequences were Paratypes. – All collected at the same locality and along the same deposited in GenBank under accession numbers (Field stream as the holotype. FMNH 272785 a male collected on the Museum numbers and fi eld tags in parentheses): same night as the holotype but perched on the leaf of a shrub 1.0 m above ground; FMNH 272787 a male collected 3 Apr.2007, GQ161200 (FMNH 272682 = RFI 52425) perched less than 1.0 m above ground on the leaf of a small herb GQ161201 (FMNH 272699 = RFI 52906) 2.5 m from the water’s edge; FMNH 272788 a male collected on 4 Apr.2007, perched on the leaf of a small herb 3.5 m from the GQ161202 (FMNH 272670 = RFI 52909) water’s edge. GQ161203 (FMNH 272647 = RFI 53249) GQ161204 (FMNH 272602 = RFI53366) Diagnosis. – A small species of Ansonia, adult males 20.0– GQ161205 (FMNH 272605 = RFI 53367) 21.3 mm; males with black spines under mandible; fi rst GQ161206 (FMNH 272603 = RFI 53385) fi nger much shorter than second, tips of outer fi ngers not GQ161207 (FMNH 272604 = RFI 53387) expanded; toes three and fi ve with at least one phalange free of webbing; back with small and large rounded tubercles, GQ161208 (FMNH 272867 = RFI 53389) those in dorsolateral region tipped with small black spines; chest and abdomen with rounded tubercles, ventrolateral Sarawak localities mentioned in text: ones larger and tipped with small black spines, tubercles Bukit Kana 2°39.363'N 112°54.219'E on top of snout set with black spines. Bukit Sarang 2°39'N 113°03'N Matang 1°36'N 110°20'E Etymology. – Specific name from echinatus, Latin for Nanga Tekalit 1°37'N 113°35'E thorny, referring to the spinose tubercles on top of the snout Samarakan 2°56'N 113°07'E and on the sides. Sungai Mina camp 2°47'N 113°10'N Sungai Penyilam camp 2°54'N 113°23'E Description. – Habitus moderately stocky; body wider than Sungai Pesu 3°07'N 113°48'E head in males; snout truncate in dorsal view, oblique in side view, projecting well beyond tip of mandible, snout longer Sungai Segaham 2°44'N 113°55'E than eye diameter; nostril lateral, near tip of snout; canthus TamaAbu mts 3°40'N 115°20'E sharply angular, constricted behind level of nostrils; lores vertical, not concave; eye diameter greater than eye-nostril

Fig. 1. Ansonia echinata new species. Dorsal view of holotype. Scale Fig. 2. Ansonia echinata new species. Ventral view of holotype. Scale in mm. in mm.

528 THE RAFFLES BULLETIN OF ZOOLOGY 2009 distance; interorbital wider than upper eyelid; tympanum from A. echinata in lacking enlarged, spinose tubercles superfi cial, diameter slightly greater than half eye diameter; ventrolaterally, spinose tubercles on top of the snout, and no crests on head. mandibular spines under the jaw. The light streak from below the eye that characterizes A. albomaculata (Inger, Tips of all fi ngers rounded, not expanded; fi rst fi nger much 1960) is absent in A. echinata. shorter than second, not reaching rounded tip of second; subarticular tubercles obscure; palm with low, rounded The relatively short fi rst fi nger and small size distinguish tubercles. Tips of all toes rounded; fi fth toe projecting Ansonia echinata from A. leptopus, A. longidigita, and farther than third; first two toes fully webbed to tips A. spinulifer, all of which have males larger than 30 mm laterally; third toe with 1–1 1/2 phalanges free of web and the fi rst fi nger reaching the swollen tip of the second laterally; fi fth toe with two phalanges free of web medially; (Inger, 1960). Ansonia latidisca, A. guibei, A. fuliginea, fourth toe with three phalanges free; subarticular tubercles and A. torrentis are larger (males >30 mm) than the new obscure; sole of foot with small, low, rounded tubercles; species and none has spinose tubercles dorsolaterally or on two metatarsal tubercles, both oval and slightly raised; no top of the snout (Dring, 1983; Inger, 1966). In contrast to tarsal fold. A. echinata, A. latidisca has the tips of the outer fi ngers expanded while A. guibei males have the web reaching the Dorsal surfaces covered with small and large rounded swollen tips of the third and fi fth toes. The nuptial pad of tubercles, tubercles not arranged in distinct rows, those A. fuliginea consists of a cluster of 15–25 large black spines down center of back and along dorsolateral regions largest; (Inger, 1966), very different from the cluster of very fi ne tubercles along dorsolateral regions tipped with one or spinules in A. echinata. two small black spines; top of head with smaller rounded spinose tubercles, spines of these tubercles larger than As to the continental species, A. ornate Günther, A. those on back; eyelid with similar though smaller tubercles; siamensis (Kiew, 1984), and A. latiffi (Wood et al., 2008) sides and abdomen covered with low rounded tubercles, are signifi cantly larger (males >25 mm snout-vent) than those in ventrolateral region larger (some ca. half diameter A. echinata and differ further in lacking spines on top of of tympanum) and tipped with small black spines; entire the snout. Males of A. malayana, A. ornata, A. rubigina surfaces of limbs covered with spinose tubercles. (Pillai & Pattabiraman, 1981), A. inthanon (Matsui et al., 1998), and A. kraensis (Matsui et al., 2005) differ from A. Colour in preservative dark brown above, raised tubercles echinata in having the third and fi fth toes webbed to the yellowish brown; ventrally light yellowish brown without swollen tips. Ansonia penangensis differs from A. echinata pattern; limbs with dark crossbars; no light streak below in having a longer fi rst fi nger, which reaches the swollen and behind eye. tip of the second (Inger, 1960). None of these continental species has elevated, melanic spines on top of the snout. The Males have subgular vocal sacs with one large slit-like recently described A. jeetsukumarani (Wood et al., 2008) opening on either the right or left side in the fl oor of the is approximately the same size as A. echinata but lacks mouth. The nuptial pad is a dense cluster of very fi ne dark spinose tubercles on the snout and ventrolaterally, such as spinules on the dorsal surface of the fi rst fi nger. The ventral characterize A. echinata, and has the venter dotted with surface of the mandible has black spines, in two or three light spots. The Sumatran species, A. glandulosa (Iskandar irregular rows beneath the symphysis and in a single row & Mumpuni, 2004), is much larger (male 39.6 mm) than A. below the remainder of the jaw. echinata and has no spines on top of the snout.

Measurements (mm) and body proportions (holotype in At the type locality, Bukit Kana, Sarawak, of Ansonia parentheses). – Snout-vent length 20.0–21.3 (20.0); T/SVL echinata we collected three kinds of Ansonia tadpoles, larval 0.470–0.502 (0.470), HW/SVL 0.309–0.315 (0.315), TYM/ A. longidigita (as defi ned in Inger, 1992) plus two unassigned. SVL 0.054–0.075 (0.054), eye/snout 0.711–0.811 (0.811). Although strikingly different from one another, the last two are recognizably larval Ansonia—oral disc expanded and A juvenile (FMNH 272786), SVL 13.5 mm, has the spinose ventral, labial tooth rows 2/3, marginal papillae continuous tubercles characteristic of this species. It was captured in across lower lip, upper beak divided into two separate water of a small stream (width 3 m) at the type locality. pieces, muscular tail with relatively low fi ns. They differ in colouration, in size, in the degree of separation of the halves Comparisons. – Eleven species of Ansonia are known of the upper beak, in relative lengths of the upper and lower currently from Borneo. Only four of these—albomaculata, rows of labial teeth, in papillae of the lower lip, and in hanitschi, minuta, and platysoma—have adult males <25 pattern of the coiling of the gut. One of the unnamed forms mm SVL (Inger, 1960). However, the last three of these four is identical to the Ansonia ‘cruciform’ tadpole described differ from A. echinata (males <22 mm) in having widened, previously (Inger, 1992). Absence of tissues from Ansonia spatulate tips to the outer fi ngers and in lacking enlarged, echinata prevented associating either of these two larval spinose tubercles ventrolaterally and spinose tubercles forms to that species by means of DNA sequencing. on top of the snout. Ansonia albomaculata also differs

529 Inger & Stuebing: New species and new records of Bornean frogs

Tadpole Ansonia sp. “cruciform” (Family Bufonidae) through posterior band and covering caudal muscle except (Figs. 3, 4) for a narrow strip along dorsal margin and a wider light strip along ventral margin; fi ns without pigment except for Material examined. – FMNH 272748-57. narrow dark marginal strip on the dorsal fi n; ventral surface of body immaculate cream-colored. Description. – Headbody ovoid, widest slightly behind eyes, very slightly tapered; snout broadly rounded; nares closer Head-body lengths (HBL) are given in Table 1. Total to eyes than to tip of snout, eye-naris equal to diameter of lengths varied from 13.5 mm (stage 36) to 16.5 mm (stage eye and one-third naris-snout; eyes dorsolateral; internarial 37). HBL/total 0.38–0.43 (n = 6). subequal to interorbital. Oral disc ventral, subequal to width of body; marginal papillae confi ned to lateral quarters These tadpoles were collected at Bukit Kana (250 m ASL) of upper lip, continuous across margin of lower lip; no in large (13–15 m wide), rocky, clear streams, in riffl es, inframarginal papillae on lower lip; distance from lower torrents, and, in the case of one tadpole, in an open pool. beak to P3 subequal to distance from P3 to margin of lip; labial tooth rows 2/3, upper rows of labial teeth longer This larval form is identical to that labelled “Ansonia than lower rows but not curved around ends of lower ones; cruciform” in Inger (1992). The tadpoles studied for beaks slender, smooth; upper beak in separated halves; that publication came from northern Sarawak (Long half of upper beak 0.40–0.90 (median 0.58, n = 11) of gap Seniai 3°27'/114°57'E) and western Sabah (Mendolong between halves. 4°54'N/115°42'E; Poring Station 6°03'N/116°42'E; 6 km E of Tuaran 6°11'N/116°14'E). Spiracle opening midway between eye and end of body, tube fused to body wall. Tadpole Ansonia sp. cruciform2 (Bufonidae) Gut in transverse coils. (Figs. 5, 6)

Tail tapered slightly in distal fourth to rounded tip; caudal FMNH 272705-47. muscle deeper than fi ns except in distal third. Headbody teardrop-shaped, widest at plane through nares, distinctly tapered; snout very broadly rounded; nares much Colouration (in preservative) black and white (cream) at closer to eyes than to tip of snout, eye-naris distance less all stages 27–42; a transverse orbital dark band ca. as wide than eye diameter and one-third naris-snout; internarial as eye diameter, beginning at ventrolateral margin and distance slightly narrower than interorbital. Oral disc extending across body; a pair of wide dark longitudinal ventral, slightly narrower than maximum body width; bands from rostrum through nostrils and narrowly separated marginal papillae of upper lip confi ned to lateral quarters; from dark orbital band; a wide dark transverse band near end marginal papillae continuous across lower lip; inframarginal of body; mid-dorsal dark band from orbital band extending papillae present in lateral thirds of lower lip; distance from lower beak to P3 greater than distance from P3 to margin of lip; labial tooth rows 2/3, upper rows longer, but not curling around ends of lower rows; beaks slender, upper smooth, lower feebly serrate; upper beak in separated

Fig. 3. Ansonia sp cruciform. Dorsal view of larva. Scale in mm.

Fig. 5. Ansonia sp. cruciform2. Dorsal view of larva. Scale in mm.

Fig. 4. Ansonia sp cruciform. Ventral view of larva. Scale in mm. Fig. 6. Ansonia sp. cruciform2. Ventral view of larva. Scale in mm.

530 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Comparison of head-body lengths (mm) of two forms a riffl e. No larval A. longidigita were found in the small of Ansonia tadpoles from Borneo. (width 3 m) streams.

Stage Cruciform2 Cruciform Altogether 46 samples of larval Ansonia were collected 5 5.9 at Bukit Kana. Five samples included tadpoles of A. 26 5.4 longidigita and A. cruciform, one sample included larval 27 8.2 3.8 A. cruciform and A. cruciform2, and two samples included all three larval forms. 28 7.4 29 7.9 30 7.5 Pelophryne Barbour (Bufonidae) 31 7.6 32 8.1 5.1 Remarks. – There are two general morphotypes among 33 7.8 5.5 the Bornean species of this genus—one with the tips of 35 8.4 5.9 the fi ngers expanded into truncate discs and one with the 36 8.6 5.8 tips of the fi ngers rounded and not expanded. The latter group includes only three species—P. misera (Mocquard) 37 6.7 known from high elevations on Mt. Kinabalu, P. api Dring 40 6.3 from a wide altitudinal range in northern Sarawak, and the 41 9.4 6.4 recently described P. linanitensis Das—which are easily 42 9.4 6.9 distinguished from one another. n 28 15 Both the recognition of species within the group having expanded finger tips and the association of specimens halves, half of upper beak 0.26–0.39 (median 0.31, n = 19) with named taxa have posed problems. There are six of gap between halves. similar, nominal Bornean taxa in this group: guentheri (Boulenger), macrotis (Boulenger), signata (Boulenger), Spiracle opening low on side, midway between eye and end exigua (Boettger), rhopophilius Inger & Stuebing, and of body, tube fused to body wall. murudensis Das. In the past very small samples and lack Gut in circular coils. of multi-species samples from single localities have made it diffi cult to decide if differences among the morphotypes Tail tapered slightly in distal fi fth to a point; caudal muscle represent intraspecific or interspecific variation. Roux deeper than fi ns except in distal fourth. (1906), for example, placed exigua in the synonymy of guentheri, stating that the type of exigua was merely a Coloration (in preservative) dark brown or black dorsally juvenile guentheri; however, the type of exigua, which and laterally, immaculate white (cream in life?) ventrally; we have examined, is an adult male having vocal sac slightly lighter anterior to eyes; a transverse light band, openings and mandibular spinules. Inger (1966) placed half diameter of eye, across body behind eyes, interrupted both exigua and signata in the synonymy of brevipes mid-dorsally; a light streak beginning ventrolaterally above (Peters), a Philippine species; examination of new material corner of oral disc and extending back to postorbital light calls that decision into doubt (Inger & Tan, 1996). The band; light ventral area curling up behind end of body; recently described species, P. rhopophilius, was the fi rst caudal muscle dark brown except for light ventral margin; species based on a type series of more than two specimens. fi ns whitish with black margins The seven frogs constituting this type series show little variation in size, secondary sex characters, coloration, and Head-body lengths are given in Table 1. Total lengths 22.6 body proportions (Inger & Stuebing, 1996). Das (2008) has (stage 35) to 26.8 (stage 41). recently described P. murudensis, based on a sample of four specimens that also exhibit little intraspecifi c variation. These larvae were collected at Bukit Kana (250 m ASL) in large (width 13–15 m), clear, rocky streams. Fifteen We now have fi ve samples from Sarawak, each consisting samples (79%) were found in torrents, three (16%) in riffl es, of at least fi ve individuals; three of these samples consist and one in an open pool. Of the 70 stations searched on of two morphotypes. One of these morphotypes is small: these streams, 36 (51%) were torrents, 29 (41%) were riffl es, males having vocal sacs, yellowish mandibular spines, and and 5 were open pools or side pools. Search for tadpoles a nuptial pad of fi ne, light spinules measure 13.5–15.9 mm was carried out in smaller (width 3 m) streams, but no larvae snout to vent (n = 9) and adult females 15.3–17.6 mm (n of this species were found. Of the 29 stations on these = 9). They have two consistent elements of coloration: (1) small streams,16 (55%) were riffl es, seven (24%) were open The venter is cream or yellow with small, isolated black pools, three were leaf drifts, and three were side pools. spots; the dark pigment occupies less than one-third of the ventral surface, and the light coloration extends half-way Larval Ansonia longidigita were collected from the same up the side. (2) The side of the head is dark with a wide two large streams, 24 samples from torrents and one from cream or yellow streak running from below the eye under

531 Inger & Stuebing: New species and new records of Bornean frogs the tympanum and over the axilla where it is continuous The type series of P. murudensis Das from northern Sarawak with the light colour of the side. In coloration, size, and consists of males measuring 21.9–25.6 mm (Das, 2008). secondary sex characters, this morphotype agrees with the These differ from the species described below in several types of P. signata (Boulenger) (BM 1947.2.19.25–26), respects (see below). and P. exigua (Boettger) (SMF 3737); we have examined types of both nominal species. We assign this small form to Pelophryne signata (Boulenger) and place Nectophryne Pelophryne saravacensis, new species exigua Boettger in its synonymy. Pelophryne signata, (Figs. 7, 8) as here defi ned, is about the same size as the Philippine species P. brevipes (Peters): males 16.0–17.8 (n = 5), Holotype. – FMNH 223014, adult male collected at Sungai Segaham, females 16.6–17.4 (n = 3), but P. brevipes has brown or Belaga District, Kapit Division, Sarawak (2°44'N/113°55'E), on 6 black pigment covering most of the belly and underside of Jun.1984, by Robert F. Inger and Paul Walker. the hind limb and lacks the uninterrupted light lateral streak Paratypes (all from Sarawak). – FMNH 223012, 223015– present in signata. 17, 223019, 223021–23 from the type locality; FMNH 128131 from Tama Abu Mts., Baram District, Miri Division The second morphotype in each of these multi-species (3°40'N/115°20'E); FMNH 138111 from Nanga Tekalit, Kapit samples is larger: adult males with nuptial pads and vocal Division (1°37'N/113°35"E); FMNH 157119 from Sungai Pesu, sacs measure 17.0–24.6 mm and adult females 19.1–24.3 Bintulu Division (3°07’N/113°48'E). mm. Males do not have conical or spinose tubercles under the mandible. All have the dorsal surface set with small Diagnosis. – Tips of fi ngers expanded into truncate discs, spinose tubercles and scattered larger tubercles that do not tip of third finger equal to or wider than tympanum; form a pattern. Dorsally all are brown (in preservative) with webbing leaving one to 1 ½ phalanges of outer fingers small, irregular darker markings. The side of the head is free; heels meet when legs folded at right angle to body lighter with dark spots. These frogs fall into two groups. axis; no continuous ventrolateral light band; abdomen dark In one (P. rhopophilius), snout-vent length of adult males with small, distinct white spots; males without mandibular (with nuptial pads) ranges from 21.6 to 24.6 mm (mean ± spines; adult males 17–20 mm, adult female 22 mm. SE = 22.70 ± 0.26; n = 11); the single adult female measures 24.3 mm. The abdomen in this group is mottled black and Description. – Habitus slender; head as wide as trunk. white (in preservative), with the light areas elongate and Snout truncate with median projection, vertical in profi le or irregular in shape. The second group is slightly smaller weakly projecting; nostril near tip of snout; canthi rounded, with adult males 17.2–20.0 mm (mean ± SE = 18.98 ± constricted; lores vertical; diameter of eye equal to length 0.65; n = 4) and two adult females 19.1 and 21.6, the last of snout; interorbital about 1.5 times width of eyelid; having enlarged, non-pigmented ova. The abdomen is dark tympanum superfi cial, oval, rim usually visible, about 1/3 with many discreet, small, round, white spots. We treat this to 2/5 diameter of eye. second group as a distinct species that we describe below as Pelophryne saravacensis. Tips of fi ngers expanded, truncate; disc of third fi nger equal to or wider than tympanum; fi ngers with fl eshy web, less The other large form of Pelophryne from Borneo, P. than one phalanx of fi rst fi nger projecting, other fi ngers guentheri (Boulenger), is larger with females 28.3–31.1 mm webbed at bases only; subarticular tubercles obscure. Tips (n = 4) and a mature male 29.9 mm, the last having a row of of toes truncate or rounded, not expanded, smaller than tips mandibular spines. We consider P. macrotis (Boulenger), its of fi ngers; fi fth toe longer than third; webbing fl eshy; only type examined by us, to be conspecifi c with P. guentheri. tips of fi rst three toes projecting from web, fi fth toe webbed to distal subarticular tubercle; fourth toe webbed to middle

Fig. 7. Pelophryne saravacensis, new species. Dorsal view of holotype. Fig. 8. Pelophryne saravacensis, new species. Ventral view of holotype. Scale in cm. Scale in cm.

532 THE RAFFLES BULLETIN OF ZOOLOGY 2009 tubercle; subarticular and metatarsal tubercles indistinct, but Meristogenys whiteheadi (Boulenger) (Ranidae) present; no tarsal ridge; when legs folded at right angles to body axis, heels meet or overlap slightly. Remarks. – Large samples of Meristogenys frogs and tadpoles were collected at Bukit Kana, Bintulu Division, Back and sides with large, round tubercles, most less Sarawak. These frogs are relatively large for species of than half diameter of tympanum; numerous fi ne, colorless Meristogenys. Males measure 48.8–57.4 mm SVL (mean spinules between tubercles of back; dorsal surfaces of limbs ± SE = 54.07 ± 0.39, n = 32); females measure 77.2–79.7 densely covered with conical tubercles; belly coarsely mm (n = 3) (FMNH 272607–41). The rear of the thigh in granular. these frogs is brown with large, irregular areas of lighter color (yellow in life?). The ventral surface of the calf is Color in preservative sandy brown to pale tan dorsally; a dusted with scattered melanophores. All but two have dark interorbital triangle, apex to rear, with thin anterior round black spots on the back, usually covering most of projection; some individuals with a faint dark triangle or the surface. The sides of the body are much lighter than the elongated trapezoid in lumbar region; side of head dark back and are heavily spotted in most individuals. The throat brown with irregular creamy areas, but no continuous light is densely dusted. Only one type of Meristogenys tadpole band from below eye to axilla; side of trunk brown with was collected at Bukit Kana (FMNH 272642–78, Gosner small, irregular light and dark spots; ventrally dark brown stages 25–40). The labial tooth formula of the upper lip is with small, discrete, white spots, dark pigment occupying 7(4-7) (n = 22), that of the lower lip 6(1) (n = 2), 7(1) (n = more than half of surface. In life, several individuals with 15), or 8(1) (n = 4). The upper jaw sheath is divided with small red spots on larger dorsal tubercles. 8–16 ribs in each half. The lower jaw sheath is single with 14–23 ribs. There are 0–5 glands in the ventral fi n (median Adult males 17.2–20.0 mm (n = 4); yellowish nuptial pad = 2). Two tadpoles of this sample differ from three adults on mediodorsal surface of fi rst fi nger; vocal sac openings in only three sites of a 442 bp fragment of 12S, verifying slit-like; no mandibular spines. Only one adult female, 21.6 association of these larvae with the adult species. mm. Body proportions (adults only): T/SVL 0.48–0.53, HW/SVL 0.30–0.34, TYM/SVL 0.049–0.069, dF3/SVL Four species of Meristogenys have been described from 0.053–0.62. Sarawak, one from the southwestern corner of the state and three from central Sarawak. Meristogenys jerboa (Günther, Comparisons. – This species is similar to P. guentheri, P. 1872) from southwestern Sarawak (type locality Matang signata, P. rhopophilius, and P. murudensis in the expanded, 1°36'N 110°20'E, Kuching Division) is relatively small. truncate fi nger discs. However, it is distinctly smaller than Males are 32–41 mm SVL (mean 35.50 ± 0.25, n = 48), and P. guentheri (both sexes > 28 mm SVL), P. rhopophilius females 61–68 mm (mean 63.66 ± 0.77, n = 9). The rear (males 21.6–24.6 mm), and P. murudensis (males 21.9–25.6 of the thigh is brown with irregular large and small light mm; Das, 2008). Pelophryne saravacensis has a longer leg spots. The sides are darker brown than the back. The light than P. guentheri and P. murudensis (T/SVL of P. guentheri median strip of the ventral surface of the calf is immaculate 0.39–0.40, n = 4; of P. murudensis 0.38–0.44, n = 4). Das white or, less often, with a few scattered melanophores. The (2008) noted that the heels of P. murudensis did not meet tympanum of the male is distinctly enlarged compared to when the legs were fl exed at right angles to the body axis; in that of the female. The tadpoles of this species have both P. saravacensis the heels meet or overlap in that position. jaw sheaths divided, three divided rows of labial teeth on the upper lip and six (rarely fi ve) undivided rows of labial Pelophryne saravacensis differs from P. rhopophilius in not teeth on the lower lip (Inger, unpublished data). having a strongly projecting snout and from the latter and P. murudensis in coloration. In P. rhopophilius the abdomen Meristogenys macrophthalmus (Matsui, 1986) (type locality is light with anastamosing, dark lines; less than half of the Sg Pesu, 3°07'N 113°48'E) from the Bintulu Division is area is covered with dark pigment. In P. saravacensis, the small, the unique holotype male measures 36.7 mm. It lacks abdomen is dark with small light spots and much more dark spots on the back. The tympanum is enlarged, TYM/ than 50% of the area is dark. In P. murudensis the lower SVL = 0.114. Larvae have not been assigned to this species, side has a continuous broad band of light (buff) coloration, but three were collected at the type locality. These are small whereas in P. saravacensis that area is brown with small (HBL 5.2–6.7 mm) stage 25 tadpoles having the lower jaw light and dark spots. sheath divided, each half with 6 ribs, and denticular formula 6(4–6)/5(1) (Inger, unpublished data). Pelophryne saravacensis is larger than P. signata; adult males of the latter measure 13.9–15.9 (n = 9) and adult Meristogenys poecilus and M. phaeomerus (Inger & Gritis, females 15.3–17.6 (n = 9). In addition males of the smaller 1983) were described from the Kapit District (Nanga P. signata have mandibular spines, which are lacking in P. Tekalit, 1°37'N 113°35'E). Males of M. poecilus, the larger saravacensis. The abdomen of P. signata is yellow with of these two species, measure 34.5–51.0 (mean 44.08), and small, scattered black spots and the sides of the head and thus are signifi cantly smaller than the Bukit Kana males (see trunk have a continuous light streak, contrasting with the above). The rear of the thigh in M. poecilus has large light coloration of P. saravacensis (see above). areas on a dark brown background. The area behind the tympanum and above the axilla is dark brown. About 10%

533 Inger & Stuebing: New species and new records of Bornean frogs of the paratypes have dark spots dorsally. Tadpoles of M. slowly fl owing streams. We collected both species at two poecilus have both jaw sheaths divided and have only three localities, Sungai Mina and Samarakan that have both fl at divided rows of labial teeth on the upper lip and only 4–5 and hilly terrain. At Samarakan we found R. raniceps in undivided rows on the lower lip (Inger & Gritis, 1983). swamps and along streams, but R. megalonesa only along streams. At Samarakan both were found in a single night Males of M. phaeomerus measure 33.0–43.0 mm (mean along a small stream (width 2 m) fl owing through secondary 38.25) and have the rear of the thigh brown dusted with forest. The lower reaches of that stream passed through a fi ne light spots. The side from behind the tympanum and sedge marsh where the bottom was deep mud. Upstream extending almost to the groin is dark brown. The back is from that segment, the stream fl owed over a rocky bed with marked with small dark spots. Tadpoles of this species have moderate gradient. On that night 15 R. raniceps (FMNH both jaw sheaths divided and only three undivided rows of 272602–4, 272797–810) were caught in the marshy portion labial teeth on the upper lip and fi ve undivided rows on the of the stream, but none in the rocky portion, whereas two lower lip (Inger & Gritis, 1983). R. megalonesa (FMNH 272604, 272867) were found in the rocky area and one in the marshy segment (FMNH 272605). The Bukit Kana species differs from all four of the Sarawak At the Sungai Mina site, both species were found along species—M. jerboa, macrophthalmus, phaeomerus, and stream banks, but only one (of four) R. megalonesa was poecilus––in several ways. Adults are larger than all four found along a small stream (width 2 m) with four (of seven) of those. The relative size of the tympanum in males of the raniceps. At Bukit Kana, an area of steep topography lying Bukit Kana form (median 0.079) is smaller than in males of at 200–300 m ASL in the Bintulu Division, we found only the four Sarawak species (median TYM/SVL 0.096, 0.114, R. megalonesa, all on the banks of streams 3–15 m wide. 0.100, 0.099, respectively Larvae of the Bukit Kana species differ from larvae of jerboa, phaeomerus, and poecilus and These observations indicate that, in the region where the from the larvae found at the type locality of macrophthalmus two species occur, Rana megalonesa has a wider ecological in the denticular formula and in the lack of division of the distribution than R. raniceps, which seems to be restricted lower jaw sheath. to fl at, even swampy, habitats.

The Bukit Kana species is most similar in size of adults and Tadpoles belonging to the Rana chalconota group were larval characters to M. whiteheadi, which is known so far collected at Bukit Kana and at Samarakan. The 16S gene only from Sabah at elevations between 200 and 990 m ASL of three tadpoles, two from Bukit Kana and one from (unpublished data). Males of M. whiteheadi from Sabah Samarakan, differs by 0–9 of 572 bp from two adults of measure 48.7–62.4 mm (mean 53.90, n = 72) and females Rana megalonesa but by 60–64 bp plus six single bp gaps 77.9–86.5 mm (n = 3). Larvae of M. whiteheadi have the out of 576 bp of three adults of Rana raniceps. All fi ve lower jaw sheath single and have four divided rows of labial adults were from Samarakan. We assign the tadpoles to teeth in the upper lip. Thus in both size of adults and these R. megalonesa. These tadpoles agree with the description larval characters there is agreement between the Bukit Kana of larval R. chalconota (Inger, 1985) which, given the species and M. whiteheadi. There are several differences, however. Larvae of M. whiteheadi from Sabah usually have fi ve undivided rows of labial teeth in the lower lip, in contrast to six in the Bukit Kana species. Adults of M. whiteheadi in our Sabah samples lack black spots dorsally, though some individuals have an obscure dark mottling.

Rana chalconota group (Family Ranidae)

Remarks. – It has recently been determined that there are two species of this group in Borneo, Rana raniceps (Peters) and Rana megalonesa Inger, Stuart & Iskandar (2009). The former species has been found so far only in swampy and low-lying coastal areas of Sarawak whereas R. megalonesa has been collected over a wide area of western and northern Borneo (Sarawak and Sabah) (Inger et al., 2009). Both species have been collected at four localities in the Bintulu Division of Sarawak. Two of those localities, Bukit Sarang and Sungai Penyilam, are swamp forests. At Bukit Sarang we found both species along the same slowly fl owing streams, but R. raniceps more often along non-riparian trails: raniceps 6 non-riparian of 8 total; megalonesa 2 non-riparian of 11 total. At Sungai Fig. 9. Ventral view of larval Rana megalonesa showing post-oral patches Penyilam both species were found along the banks of of glands.

534 THE RAFFLES BULLETIN OF ZOOLOGY 2009 localities of the latter, were probably R. megalonesa. The Inger, R. F. & P. A. Gritis, 1983. Variation in Bornean frogs of single difference from those earlier described tadpoles is the Amolops jerboa species group, with description of two new that in the present ones the ventral post-oral glandular patch species. Fieldiana: Zoology (n.s.) No. 19: 1–13 is divided into two separate round groups (Fig. 9). Inger, R. F., B. L. Stuart & D. T. Iskandar, 2009. Systematics of a widespread south-east Asian frog, Rana chalconota (Amphibia: Anura: Ranidae). Zoological Journal of the ACKNOWLEDGEMENTS Linnean Society, 155: 1230–147. Inger, R. F. & R. B. Stuebing, 1996. Two new species of frogs We are indebted to Freddy Julus, Patrick Francis, Leong from southeastern Sarawak. Raffles Bulletin Zoology, 44: Tzi Ming, and Jacinta Richard for valuable assistance in 543–549. the field. We are also grateful to Alan Resetar for the Inger, R. F. & Tan F.-L., 1996. Checklist of the frogs of Borneo. photographs of specimens and much help in the laboratory, Raffl es Bulletin Zoology, 44: 551–574. to Bryan L. Stuart for advice on molecular genetics, and to Iskandar, D. T. & Mumpuni, 2004. A new toad of the genus Abigail Wolfe for preparation of DNA sequences and much Ansonia (Amphibia, Anura, Bufonidae) from Sumatra, other aid in the lab. Financial support for fi eld work came Indonesia. Hamadryad, 28: 59–65. from the Marshall Field III Fund of The Field Museum. We Kiew B.-H., 1984. A new species of toad, Ansonia siamensis express our sincere thanks for the logistical support in the (Bufonidae), from the Isthmus of Kra, Thailand. Natural fi eld supplied by the staff of the Conservation Department, History Bulletin Siam Society, 32: 111–115. Grand Perfect Sdn. Bhd., Bintulu, Sarawak. Matsui, M., 1986. Three new species of Amolops from Borneo (Amphibia, Anura, Ranidae). Copeia, 1986:623–630. Matsui, M., J. Nabhitabhata & S. Panha, 1998. A new Ansonia LITERATURE CITED from northern Thailand (Anura: Bufonidae). Herpetologica, 54:448–454. Das, I., 2008. Two new species of Pelophryne (Anura: Bufonidae) Matsui, M., W. Khonsue, & J. Nabhitabhata, 2005. A new from Gunung Murud, Sarawak (Northwestern Borneo). Raffl es Ansonia from the Isthmus of Kra, Thailand (Amphibia, Anura, Bulletin of Zoology, 56(2):435–443. Bufonidae). Zoological Science, 22: 809–814. Dring, J., 1983. Some new frogs from Sarawak. Amphibia-Reptilia, Pillai, R. S. & R. Pattabiraman, 1981. A new species of torrent toad 4:103–115. (Genus: Ansonia) from Silent Valley, S. India. Proceedings Gosner, K. L., 1960. A simplifi ed table for staging anuran embryos Indian Academy Sciences (Animal Series), 90: 203–208. and larvae with notes on identification. Herpetologica, Roux, J., 1906. Synopsis of the toads of the genus Nectophryne 16:183–190. B. & P., with special remarks on some known species and Günther, A., 1872. On the reptiles and amphibians of Borneo. description of a new species from German East Africa. Proceeding of the Zoological Society of London, 1872: Proceedings Zoological Society London, 1906: 58–65. 586–600. Stuart, B. L., R. F. Inger & H. K. Voris, 2006. High level of cryptic Inger, R. F., 1960. A review of the Oriental toads of the genus species diversity revealed by sympatric lineages of Southeast Ansonia Stoliczka. Fieldiana: Zoology, 39:473–503. Asian forest frogs. Biology Letters, 2: 470–474. Inger, R. F., 1966. The systematics and zoogeography of the Wood, P. L. Jr., L. L. Grismer, N. Ahmad & J. Senawi, 2008. Two Amphibia of Borneo. Fieldiana: Zoology, 52:1–402. new species of torrent-dwelling toads Ansonia Stoliczka, 1870 Inger, R. F., 1985. Tadpoles of the forested regions of Borneo. (Anura: Bufonidae) from Peninsular Malaysia. Herpetologica, Fieldiana:Zoology (n.s.) no. 26, 89 pp. 64: 321–340. Inger, R. F. 1992. Variation of apomorpic characters in stream- dwelling tadpoles of the bufonid genus Ansonia (Amphibia: Anura). Zoological Journal of the Linnean Society, 105: 225–237.

535 THE RAFFLES BULLETIN OF ZOOLOGY 2009

THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 537–542 Date of Publication: 31 Aug.2009 © National University of Singapore

POSSIBLE EXTINCTIONS OF DUNG BEETLES (COLEOPTERA: SCARABAEIDAE) IN BUKIT TIMAH NATURE RESERVE, SINGAPORE

Janice S. H. Lee, Yat Ka Cheung and Lan Qie Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Republic of Singapore Email: [email protected] (Corresponding author); [email protected] (LQ)

Johannes Huijbregts National Museum of Natural History Naturalis, Postbus 9517, 2300 RA Leiden, the Netherlands Email: [email protected] (JH)

ABSTRACT. – Bukit Timah Nature Reserve (BTNR) contains the largest patch (71 ha) of primary rainforest left in Singapore after approximately 95% deforestation by humans over the last century. Floral and faunal diversity have been monitored by the colonial British natural historians and local nature enthusiasts. This information can be used to determine biotic turnover due to deforestation as there is little information available on this subject. We examined dung beetle species collected in the Bukit Timah Nature Reserve from the 1960s to 1970s and compared them with species collected from the same forest patch today. We employed two trapping methods – baited pitfall traps and fl ight interception traps for our survey. Out of the nine species collected from the past, three species – Cartharsius molossus, Onthophagus deliensis and Ont. cf mentaveiensis may be extinct. One of these species, Cartharsius molossus, a large-bodied dung beetle, plays an important role in nutrient recycling in the forest ecosystem. The possible extinctions of dung beetles within a span of 30 years in BTNR highlights the recurring events of species loss in Southeast Asian forests today and the need to preserve whatever remaining refuges of biodiversity.

KEY WORDS. – Tropical forest, insect, Southeast Asia, species survival, dung.

INTRODUCTION is the fauna of Singapore, which has been well studied since 1819 by British natural historians. In Brook et al. Tropical forest loss and degradation by human activities (2003), insects such as butterfl ies have a similar extinction continue to threaten earth’s biodiversity (Brooks et al., rate of 38% as compared to commonly studied taxa such as 2002; Brook et al., 2003; Sodhi et al., 2007). This loss mammals (43%), birds (34%) and vascular plants (26%). of forest habitats may lead to an unprecedented level of species extinctions as forest loss continues to accelerate in Here, we aim to determine the possible extinctions of dung the most biodiverse regions (Myers et al., 2000; Pimm & beetles (Coleoptera: Scarabaeinae) from a small isolated Raven, 2000). The extinction of forest dwelling fauna has forest fragment, Bukit Timah Nature Reserve (hereafter been better studied for more charismatic and larger mammal BTNR), Singapore, by comparing historical documentation and bird species compared to insects (Dunn, 2005) despite of dung beetles from the 1960s to 1970s with an intensive the fact that more than 57% of described living species are collection carried out in present day. The reduction of forest insects (Stork, 1997; IUCN, 2008) and that insects perform size and its isolation from a larger tract of forest can result critical roles in the ecosystem (Didham et al., 1996). The in the decrease in middle to large sized mammal populations lack of assessment of insect survivability has led to broad (Corlett, 1992; Laidlaw, 2000). This decline in mammalian estimations of the percentages of threatened insects between populations may have cascading effects on animals such 0.07% and 50% (IUCN, 2008). Hence the lack of insect as dung beetles, which are generally reliant on mammalian knowledge especially in highly threatened tropical forests dung for nutrition and nesting (Cambefort & Hanski, 1991). may contribute to misleading levels of insect extinctions Hence, dung beetle species richness and abundance can be occurring (McKinney, 1993). Previous assessments of used as a possible indicator of mammal populations in a insect extinctions were often carried out at a local scale, in forest habitat (Andresen & Laurance, 2007; Nichols et al., island systems or isolated forest reserves with a history of 2009). A review by Nichols et al. (2008) also show that biodiversity inventories (Brook et al., 2003; Thomas et al., dung beetles perform a myriad of ecological processes such 2004; Hanski et al., 2007; Sodhi et al., 2009). An example as nutrient recycling (Yokoyama et al., 1991), controlling

537 Possible dung beetles extinction in Singapore pest populations (Bornemissza, 1970) and secondary BTNR. Dennis H. Murphy, a retired NUS entomology seed dispersal (Andresen & Feer, 2005), emphasizing the professor, made most of the dung beetle collection during usefulness and importance of dung beetles in ecosystems. the period of 1960s to 1970s. We interviewed D. H. Murphy Based on the list of beetles from the 1960s to 1970s, we regarding the methods used for collection of the dung beetles aim to determine the absence or presence of each individual and the exact locations where he made his collections. The species and fi nd out if there has been any apparent extinction beetles were collected with a variety of techniques, such of dung beetles in BTNR over the last 40 years. as glycol pitfall traps, light traps and malaise traps. All the beetles were collected opportunistically and there was no systematic sampling design, which could be replicated. MATERIALS AND METHODS Dung beetle survey. – Since past collections of dung Study site. – The Republic of Singapore is a highly urbanized beetles were carried out opportunistically using a variety city-state at the southern tip of the Malay Peninsula (1°14'N of methods, we decided to carry out an intensive dung 103°55'E). Rapid deforestation in Singapore occurred in beetle survey using well-used sampling techniques for two phases, firstly the cultivation of cash crops which dung beetles such as dung baited pitfall traps and fl ight was completed by the end of the nineteenth century and interception traps (Davis et al., 2001). We identifi ed the fi ve secondly, urbanization which led to rapid development and valleys of BTNR (Lasia Valley, Taban Valley, Jungle Fall economic success to the country (Corlett, 1992). Much of Valley, Fern Valley and Seraya Valley) as forest interiors of Singapore’s original vegetation has been cleared and the BTNR and placed our traps in all these valleys. This study largest remnant of primary hill dipterocarp rainforest lies was conducted between January 2008 and March 2008. in the Bukit Timah Nature Reserve (Corlett, 1992). The total size of BTNR is 163 ha, of which approximately Our baited pitfall trap consist of a 500 ml plastic cup 71 ha consists of primary forests disturbed to varying (diameter = 8.5 cm and height = 12 cm) buried fl ushed extents. Records of isolation of the forest on Bukit Timah with the ground. A 15 cm by 15 cm corrugated plastic stretch back to 1843, with accounts of gambier and pepper board served as a rain cover and was supported 10 cm plantations separating Bukit Timah from other forests (for above the surface of the cup by iron wires. We used cow more details, see Corlett, 1988). Legal protection was more dung collected from the Singapore Zoological Gardens as strictly enforced in 1939 where Bukit Timah was gazetted to bait for our traps. The cow dung was kept in an airtight be a nature reserve under the British colonial law (Corlett, container for at least 4 days at room temperature so as to 1988). Several legislations were passed to protect both fl ora obtain a more pungent smell of the decomposing dung. We and fauna in the early 20th century, though these were not used approximately 100 g of cow dung and wrapped it in suffi cient to prevent illegal hunting and logging (Corlett, a 2 mm by 2 mm green mesh, secured with rubber bands 1988). At present, BTNR is surrounded by a matrix of urban and suspended from the surface of the trap by 5 cm with housing and a major expressway, which separates BTNR cotton twine. Each pitfall trap contained formalin, fi lled to from a larger forest fragment (ca. 3,043 ha), the Central a depth of 3 cm, to kill and preserve trapped dung beetles. Catchment Nature Reserve (Fig. 1). A total of 843 forest Traps were organized in quadrants where one trap was 10 m angiosperm species have been recorded in BTNR, with the away from the other and the distance between each quadrant most species coming from the following plant families: was 50 m. The number of quadrants in each valley differed Euphorbiaceae, Orchidaceae, Rubiaceae and Moraceae according to the size of the valley (Table 1). Traps were set (Corlett, 1990). up during the morning and left in the fi eld for two nights before collection. Beetles were collected and stored in 100 The fauna history of BTNR has also been recorded albeit % ethanol and brought back to the laboratory for species not as well studied than the fl ora. The primary forests in identifi cation. BTNR are different from the rest of Southeast Asia namely because all its large mammals, e.g. the Tiger (Panthera Flight interception traps collect dung beetles based on tigris corbetti), Leopard (Panthera pardus), Sambar (Rusa their fl ight activity and is therefore a more unbiased way unicolor), have gone extinct between 1930 and 1940s of catching dung beetles, especially beetles which may (Yang et al. 1990; Tan et al., 2007). Mammals that are specialize on rotting fruits or other types of dung (Davis, extant in BTNR include small to medium sized mammals 2000). Our fl ight interception traps were constructed using such as the Long-tailed Macaques (Macaca fasicularis), a black fabric 2 m wide by 1.3 m long and suspended Common Treeshrews (Tupaia glis), and Slender Squirrels tautly across a forest trail using raffi a strings. The black (Sundasciurus tenuis). The last published survey of fabric intercepts beetles flying along forest trails and mammals found in BTNR was conducted from 1993 to 1997 these beetles fall into collecting trays half-filled with a as part of a larger survey of fauna diversity in the nature saturated salt solution with a small amount of detergent. A reserves of Singapore (Teo & Rajathurai, 1997). large ground sheet secured with raffi a strings above each fl ight interception trap acted as a rain cover and prevented Historical collection of dung beetles. – We searched the the collecting containers from being fl ooded. One fl ight Raffles Museum of Biodiversity Research (RMBR) in interception trap was set up in each valley, except for the National University of Singapore (NUS) for any past Fern Valley, which had two such traps set up (Table 1). collections of dung beetles made in the forest interior of All traps were visited every 7 days and left in the forest

538 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Number of quadrants and fl ight interception traps in each extinct species requires that species should not have been valley of Bukit Timah Nature Reserve. reported or seen in the last 50 years (IUCN, 2008). Hence, we shall classify dung beetles, which were not found in our Site Number of Number of Flight 2008 survey as “possibly extinct”. Based on the historical Quadrants Interception Traps collection in RMBR, we collated a list of nine dung beetle Seraya Valley 2 1 species and 30 individuals collected from the forest interior Jungle Fall Valley 2 1 of BTNR between 1960s and 1970s. We checked for the Fern Valley 6 2 presence of any of these species in our pitfall and fl ight Lasia Valley 3 1 interception traps conducted in February and March 2008. Out of the nine species from the historical records, three Taban Valley 4 1 (33%) were absent and possibly extinct in BTNR (Table 2). Species not caught in our traps and possibly extinct include Cartharsius molossus, Onthophagus deliensis and for a period of 21 days. Captured dung beetle individuals Onthophagus cf. mentaveiensis (Table 2). were preserved in 100% ethanol, and were processed and identifi ed in the laboratory. Where individuals could not be Using both baited pitfall traps and fl ight interception traps, identifi ed, a series of morphospecies numbers were assigned we collected a total of 17 species and 867 individuals (Table to the genus. The dung beetle specimens collected from 3). We recorded 11 species of dung beetles not collected the intensive survey are held in the Raffl es Museum of by D. H. Murphy from BTNR in 2008 viz. Ochicanthon Biodiversity Research, National University of Singapore. peninsularis, Onthophagus angustatus, Ont. defl exicollis, Ont. pedator, Ont. rutilans, Ont. sp. 4, Ont. sp. 5, Ont. sp. 6, Ont. sp. 7, Ont. sp. 8, and Ont. sp. 9. The number of RESULTS species sampled using fl ight interception traps was higher, 16 species compared to 7 species which were found in Dung beetles that were not found in our survey could not our baited pitfall traps (Table 3). Similarly, the number be labeled as “extinct” since our study was conducted of individuals from flight interception traps exceeded approximately 30 years later. Conventional defi nition of the number of individuals from baited pitfall traps, 764 beetles compared to 103 beetles. The majority of dung beetle individuals consisted these three dung beetle species Onthophagus sp. 1, Ont. sp. 2 and Ont. sp. 3, which made up 68% of the total number of individuals caught in fl ight interception traps. There was also a great disparity in the catch of dung beetle species Onthophagus sp. 1 and Ont. sp. 2, where more than a hundred beetles were caught in fl ight intercept traps and only one or no beetles caught using baited pitfall traps (Table 3).

DISCUSSION

Deforestation and alteration of natural habitats have been shown to cause insect population decline and extinction in studies from tropical (e.g. Brook et al., 2003; Hanski et al., 2007; Sodhi et al., 2008) as well as temperate regions (Lobo, 2000; Brandmayr et al., 2008). The loss of forests can lead to a deterioration of habitat conditions (e.g. greater predation risks and microhabitat changes), which are less conducive for certain insect species (Sodhi et al., 2007).

In the case for dung beetles, larger bodied beetles may be more prone to microclimatic changes as they dissipate heat slower (Bartholomew & Heinrich, 1978) and may fi nd themselves vulnerable to over-heating or desiccation in a hotter and drier forest habitat (Chown, 2001). The drier forest can also lead to lower soil humidity that correlates with increased desiccation of large dung beetle larvae in the soil (Anduaga, 2004). Effects of deforestation are also associated with a decline in middle and large mammals, important dung producers in the tropical forests (Laidlaw, Fig. 1. Map showing geographical location of Bukit Timah Nature Reserve in Singapore and location of traps used in the 2008 dung beetle survey. 2000) and this has ramifications on the availability of

539 Possible dung beetles extinction in Singapore

Table 2. List of nine dung beetles which were collected between 1965 and 1976 and their presence or absence in the pitfall traps (PFT) or fl ight intereption traps (FIT) set up between January and March 2008. Functional guild refers to the size and mode of dung removal based on Cambefort (1991). Biomass data was obtained from a separate study conducted by Lee et al. (in preparation).

Species Functional Guild* Biomass (g) PFT FIT Present/Absent (+/-) Catharsius molossus LT 0.5719 ± 0.0670 0 0 - Onthophagus deliensis ST 0.003 0 0 - Onthophagus sp. 1 ST 0.0037 ± 0.0019 1 1 + Onthophagus sp. 2 ST 0.0027 ± 0.0002 0 1 + Onthophagus sp. 3 ST 0.0110 ± 0.0010 1 1 + Onthophagus mentaweiensis ST 0.0040 ± 0.0020 0 0 - Onthophagus semicupreus ST 0.005 1 1 + Onthophagus semifex ST 0.0393 ± 0.0040 1 1 + Paragymnopleurus maurus LR 0.0840 ± 0.0241 1 1 +

* Functional guild of dung beetles include size (L = large, S = small) and mode of dung removal (T = tunneller, R = roller).

Table 3. List of dung beetle species found in pitfall traps (PFT) the presence of large, nocturnal tunnellers account for and fl ight interception traps (FIT). approximately 75% of dung removal and the loss of these beetles may have serious consequences on nutrient recycling Species PFT FIT and secondary seed dispersal processes in BTNR and forests Ochicanthon peninsularis 0 4 of Singapore. Other dung beetle species that were absent Onthophagus angustatus 0 11 from our 2008 survey included Onthophagus deliensis and Onthophagus defl exicollis 0 16 Ont. cf mentaweiensis. Both are small tunnellers (ca. 4–6 mm in length) and have very low biomass. Ont. deliensis Onthophagus pedator 0 30 is a specialist canopy dung beetle with adaptations such as Onthophagus rutilans 3 0 curved and elongated hind metatarsus which is used to carry Onthophagus semicupreus 7 6 dung from the canopy, such as monkey dung, to the forest Onthophagus semifex 41 86 fl oor (Davis et al., 1997). Onthophagus sp. 1 1 198 Onthophagus sp. 2 0 140 Dung beetle species richness in BTNR is much lower in Onthophagus sp. 3 40 186 comparison to a similar study by Davis (2000) in Ulu Onthophagus sp. 4 7 25 Segama Reserve, Sabah, Malaysia. Flight interception traps set up over 7 days in reduced impact logging and Onthophagus sp. 5 0 1 conventionally logged lowland dipterocarp forests collected Onthophagus sp. 6 0 6 57 species and 48 species respectively. In contrast, only Onthophagus sp. 7 0 2 18 species of dung beetles were collected using the same Onthophagus sp. 8 0 24 methods but three times the trapping period in BTNR. The Onthophagus sp. 9 0 27 eleven new species recorded from our 2008 survey together Paragymnopleurus maurus 4 2 with the six previously recorded species from BTNR brings the total number of dung beetle species in BTNR to 17 Total species 7 16 species. Newly recorded species were most likely missed Total individuals 103 764 out due to the opportunistic nature of sampling between 1960s and 1970s. It is unclear if their presence may be due to colonization of the forest fragment after 1970s. Out of suffi cient dung resources for beetles with higher biomass the collected 17 species, only one species was not found in (Larsen et al., 2005). The study by Hanski et al. (2007) on fl ight interception traps and the other 16 species found in dung beetle extinctions in Madagascar cited the reduction either fl ight intercept traps exclusively or in both trap types. in the population of lemurs as a possible reason for the Since fl ight interception traps are passive in nature and dramatic decline of Helictopleurus undatus, a relatively collect dung beetles that have a more diversifi ed diet, they large dung beetle that was common in the past. In our serve as an important complementary trap type to survey study, we identifi ed a single large dung beetle Cartharsius dung beetle species diversity in a locality. Some dung beetle molossus (ca. 0.572 g in dry mass), a nocturnal tunneller species such as Onthophagus sp. 1, Ont. sp. 2 and Ont. sp. to be possibly extinct in BTNR. Cartharsius molossus is 3 are found in much higher abundance in fl ight intercept a widespread species in Southeast Asia and is commonly traps than in baited pitfall traps (Table 3). Considering that found in the interior of primary lowland forests in Johor fl ight intercept traps are left in the fi eld for three consecutive but not present in the forest fragments of Singapore (Lee weeks and baited pitfall traps are set out only three days for et al., in preparation). According to Slade et al. (2007), each sampling period, this disparity in abundance may be

540 THE RAFFLES BULLETIN OF ZOOLOGY 2009 a result of the difference in effective trapping period rather Seedling Establishment. CABI International, Wallingford, than the effi ciency or appropriateness of the trap itself. The Oxfordshire, UK. Pp. 331–349. use of cattle dung instead of human dung as bait for our Andresen, E. & S.G.W. Laurance, 2007. Possible indirect effects pitfall traps might also be another reason for the disparity of mammal hunting on dung beetle assemblages in Panama. in species and number of individuals between the two trap Biotropica, 39: 141–146. types. Since human dung is representative of an omnivorous Anduaga, S., 2004. Impact of the activity of dung beetles diet, using human dung as bait may have been able to attract (Coleoptera: Scarabaeidae: Scarabaeinae) inhabiting pasture a wider range of dung beetle species and a larger number land in Durango, Mexico. Environmental Entomology, 33: of individuals. 1306–1312. Bartholomew, G. A. & B. Heinrich, 1978. Endothermy in African Since the early 19th century, the forest of BTNR has dung beetles during fl ight, ball making and ball rolling. Journal undergone several anthropogenic disturbances ranging of Experimental Biology, 73: 65–83. from the clearance of land for agriculture and plantation Bornemissza, G. F., 1970. Insectary studies on the control of to the modern day infl uences of human developments for the dung breeding fl ies by the activity of the dung beetle, recreation, housing and transport (Corlett, 1988). Between Onthophagus gazella F. (Coleoptera, Scarabaeidae). Journal the time of our sampling and the time of collection of of the Australian Entomological Society, 9: 31–41. dung beetles from the museum, one major disturbance to Brandmayr, P., R. Pizzolotto, G. Colombetta & T. Zetto, 2008. In BTNR was the construction of the six-lane Bukit Timah situ extinction of carabid beetles and community changes n a Expressway (1983 to 1986) that provides an effective protected suburban forest during the past century: the “Bosco barrier between BTNR and the Central Catchment Nature Farneto” near Trieste (Italy). Journal of Insect Conservation, Reserve, restricting the movement of most terrestrial 13: 231–243. animals especially mammals between the two forests. Brook, B. W., N. S. Sodhi, P. K. L. Ng, 2003. Catastrophic Furthermore, walking trails that allow access to all parts of extinctions follow deforestation in Singapore. Nature, 424: BTNR subdivide the forests into smaller areas and expose 420–426. the forests to increased drying effects from the external Brooks, T. M., R. A. Mittermeier, C. G. Mittermeier, G. A. B. da environment (Corlett, 1988). All these human disturbances Fonseca, A. B. Rylands, W. R. Konstant, P. Flick, J. Pilgrim, could have resulted in possible extinctions of the three dung S. Oldfi eld, G. Magin & C. Hilton-Taylor, 2002. Habitat loss and extinctions in the hotspots of biodiversity. Conservation beetles species from BTNR since the 1970s. However, we Biology, 16: 909–923. are cautious not to rule out any possible extinction from faunal relaxation due to earlier disturbance events in the Chown, S. L., 2001. Physiological variation in insects: hierarchical early 19th century. levels and implications. Journal of Insect Physiology, 47: 649–660. Our study focuses on BTNR, a small, isolated forest Corlett, R. T., 1988. Bukit Timah: the history and signifi cance fragment in Singapore and hence, its results may not be of a small rain-forest reserve. Environmental Conservation, 15: 37–44. widely applicable. However, this localized example can still serve as an illustration of the ongoing effects of human Corlett, R. T., 1990. Flora and reproductive phenology of the disturbance on Southeast Asian forest species (Sodhi et al., rain forest at Bukit Timah, Singapore. Journal of Tropical Ecology, 6: 55–63. 2004) and especially less well-documented insect groups. The preservation of forests in BTNR and conservation Corlett, R. T., 1992. The ecological transformation of Singapore, of mammals therein has important consequences for the 1819-1990. Journal of Biogeography, 19: 411–420. continued survival of dung beetles in the forests. Davis, A. J., J. Huijbregts, A. H. Kirk-Spriggs, J. Krikken & S. L. Sutton, 1997. The ecology and behaviour of arboreal dung beetles in Borneo. In: Stork, N. E., J. Adis & R. K. Didham ACKNOWLEGDMENTS (eds.), Canopy . Chapman & Hall, London, UK. Pp. 415–430. We thank the National Parks Board for providing the Davis, A. J., 2000. Does reduced-impact logging help preserve research permits to the Bukit Timah Nature Reserve. We biodiversity in tropical rainforests? A case study from Borneo using dung beetles (Coleoptera: Scarabaeoidea) as indicators. also thank Dr. D. H. Murphy for his time and explanations Environmental Entolmology, 29: 467–475. as well as the Raffl es Museum of Biodiversity Research for materials and equipment provided. This study was Davis, A. J., J. D. Holloway, H. Huijbregts, J. Krikken, A. Kirk- supported by the National University of Singapore (Grant Spriggs & S. L. Sutton, 2001. Dung beetles as indicators of change in the forests of northern Borneo. The Journal of no. R-154-000-331-112). Applied Ecology, 38: 593–616. Didham, R., J. Ghazoul, N. E. Stork & A. J. Davis, 1996. Insects in fragmented forests: A functional approach. Trends in Ecology LITERATURE CITED and Evolution, 11(6): 255–260.

Andresen, E. & F. Feer, 2005. The role of dung beetles as Dunn, R. R., 2005. Modern insect extinctions, the neglected secondary seed dispersers and their effect on plant regeneration majority. Conservation Biology, 19: 1030–1036. in tropical rainforests. In: Forget, P. M., J. E. Hulme, P. E. Cambefort, Y. & I. Hanski, 1991. Dung Beetle Population Biology. Vander Wall (eds.), Seed Fate: Predation, Dispersal and In: Hanski, I. & Y. Cambefort (eds.), Dung Beetle Ecology. Princeton University Press, New Jersey, US. Pp. 36–50.

541 Possible dung beetles extinction in Singapore

Cambefort, Y., 1991. Biogeography and Evolution. In: Hanski, Stork, N. E., 1997. Measuring global biodiversity and its decline. I. & Y. Cambefort (eds.), Dung Beetle Ecology. Princeton In: Reaka-Kudla, M. L., D. E. Wilson & E. O. Wilson (eds.), University Press, New Jersey, US. Pp. 51–67. Biodiversity II. Joseph Henry Press, Washington DC. Pp. Hanski, I., H. Koivulehto, A. Cameron & P. Raghagalala, 2007. 41–68. Deforestation and apparent extinctions of endemic forest Sodhi, N. S., L. P. Koh, B. W. Brook & P. K. L. Ng, 2004. beetles in Madagascar. Biology Letters, 3: 344–347. Southeast Asian biodiversity: An impending disaster. Trends IUCN (World Conservation Union), 2008. Red list of threatened in Ecology and Evolution, 19: 654–660. species. IUCN, Gland, Switzerland. Available from http:// Sodhi, N.S., B.W. Brook & C. J. A. Bradshaw, 2007. Tropical www.iucnredlist.org/ (accessed November 2008). Conservation Biology. Blackwell Publishers Limited, Oxford, Laidlaw, K. R., 2000. Effects of habitat disturbance and protected UK. areas on mammals of peninsular Malaysia. Conservation Sodhi, N. S., D. S. Wilcove, R. Subaraj, D. L. Yong, T. M. Lee, Biology, 14: 1639–1648. H. Bernard & S. L. H. Lim, 2009. Insect extinctions on a Larsen, T. H., N. M. Williams & C. Kremen, 2005. Extinction small denuded Bornean island. Biodiversity and Conservation order and altered community structure rapidly disrupt (accepted). ecosystem functioning. Ecology Letters, 8: 538–547. Tan, H. T. W., L. M. Chou, D. C. J. Yeo & P. K. L. Ng. 2007. Lobo, J. M., 2001. Decline of roller dung beetle (Scarabaeinae) The Natural Heritage of Singapore. Prentice Hall, Pearson, populations in the Iberian peninsula during the 20th century. Singapore. vii + 271 pp. Biological Conservation, 97: 43–50. Teo, R. C. H. & S. Rajathurai, 1997. Mammals, reptiles and McKinney, M. L., 1999. High rates of extinction and threat in amphibians in the nature reserves of Singapore – Diversity, poorly studied taxa. Conservation biology, 13: 1273–1281. abundance and distribution. Gardens’ Bulletin Singapore, 49: 353–425. Myers, N., R. A. Mittermeier, C. G. Mittermeier, G. A. B. da Fonseca & J. Kent, 2000. Biodiversity hotspots for Thomas, J. A., M. G. Telfer, D. B. Roy, C. D. Preston, J. J. D. conservation priorities. Nature, 403: 853–858. Greeenwood, J. Asher, R. Fox, R. T. Clarke & J. H. Lawton, 2004. Comparative losses of British butterfl ies, birds, and Nichols, E., S. Spector, J. Louzada, T. Larsen, S. Amezquita, plants and the global extinction crisis. Science, 303: 1879– M. E. Favila & The Scarabaeinae Research Network, 2008. 1881. Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biological Conservation, 141: Yang, C. M., K. Yong, K. K. P. Lim. 1990. Wild mammals of 1461–1474. Singapore. In: Chou, L. M. & P. K. L. Ng (eds.), Essays in Zoology. Department of Zoology. National University of Nichols, E., T. A. Gardner, C. A. Peres & S. Spector, 2009. Co- Singapore. Pp. 1–23. declines in large mammals and dung beetles: an impending ecological cascade. Oikos, 118: 481–487. Yokoyama, K., H. Kai, T. Koga & T. Aibe. 1991. Nitrogen mineralization and microbial populations in cow dung, dung Pimm, S. L. & P. Raven, 2000. Biodiversity: Extinction by balls and underlying soil affected by paracoprid dung beetles. numbers. Nature, 403: 843–845. Soil Biology and Biochemistry, 23: 649–653. Slade, E. M., D. J. Mann, J. F. Villanueva & O. T. Lewis, 2007. Experimental evidence for the effects of dung beetle functional group richness and composition on ecosystem function in a tropical forest. Journal of Animal Ecology, 76: 1094–1104.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 543–550 Date of Publication: 31 Aug.2009 © National University of Singapore

ONTOGENETIC SHIFTS IN CARAPACE PATTERNING AND/OR COLOURATION IN INTERTIDAL AND SUBTIDAL BRACHYURAN CRABS

Peter A. Todd*, Wenjie Qiu and Kwek Yan Chong Marine Biology Laboratory, Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Blk S1 #02-05, Singapore 117543 *Email: [email protected]

ABSTRACT. – Some juvenile intertidal and subtidal crabs are known to exhibit carapace polymorphism, crypsis, or disruptive colours which are lost as the crabs mature, i.e. they undergo ontogenetic shifts in patterning and/or colouration. These patterns and colours are thought to protect young crabs from visual predators. The transformation is often dramatic and most likely refl ects a critical life-stage that is possibly unique to marine arthropods. Two main hypotheses have been proposed to explain changes in colouration as crabs grow: they no longer need such a defense as they become bigger and stronger or, they migrate from nursery habitats to areas where such patterns and colours do not confer protection. To identify the extent of ontogenetic shifts in intertidal and subtidal crab patterning and/or colouration, a database was assembled from the literature (primary and grey); from expert scientifi c opinions (via personal interviews and email correspondence); and website-derived observations from non-professionals worldwide.

KEY WORDS. – Camoufl age, crypsis, disruptive colouration, polymorphism, visual predator.

INTRODUCTION hypotheses have been proposed to explain ontogenetic shifts in colouration as C. maenas grow: that they no longer need Camoufl age is a predator evasion strategy employed by many defensive camoufl age as they become bigger and stronger; animals (Endler, 1978, 1984; Ruxton et al., 2004). Several or they migrate from nursery habitats to areas where forms have been described, including crypsis (background carapace patterns no longer confer protection (Hogarth, matching) where an organism possesses colouration or 1978; Palma et al., 2003; Todd et al., 2006). markings that are similar to the substrates they are found on (Endler, 1978, 1984), and disruptive colouration, where Carapace polymorphism can also protect juvenile crabs from the outline of the body is broken up, making it diffi cult for predation, although it has been studied less in the Brachyura a visual predator to detect its true form (Cott, 1940; Cuthill compared to other marine invertebrates (Palma et al., 2003). et al., 2005). Disruptive colouration has been observed in an A population exhibiting a variety of morphs makes it more array of organisms ranging from molluscs, crustaceans and diffi cult for a visual predator to create a search image (e.g. insects to snakes, birds and mammals (Ruxton et al., 2004) Pietrewicz & Kamil 1979). For example, the bivalve Donax and has been shown experimentally to successfully reduce faba is relatively conspicuous on its usual sandy habitat, predation (Cuthill et al., 2005, 2006; Stevens et al., 2006). but its polymorphism appears to protect it from predation (Smith, 1975). The protective effect of polymorphism has It has been well-documented that juvenile shore crabs, also been proposed to explain the range of colour and Carcinus maenas (Linnaeus, 1758), possess carapace pattern morphs found in Littorina saxatilis (Ekendahl & patterns that are lost as they mature (Crothers, 1968; Johannesson, 1997), Donacilla cornea (Whiteley et al., Hogarth, 1975, 1978; Bedini, 2002; Palma et al., 2003; Todd 1997) and Cepea sp. (Jones et al., 1977; Goodhart, 1987). et al., 2005, 2006). Todd et al. (2005) noted that age-specifi c The morphs in polymorphic populations are often also habitat shifts could be an underlying cause for this change cryptic, especially on polychromatic backgrounds (Jones in carapace patterning. The larvae of shore crabs settle on et al., 1977; Goodhart, 1987; Palma & Steneck, 2001; nursery grounds such as seagrass (Hovel & Lipcius, 2002) Parsonage & Hughes, 2002; Wente & Phillips, 2003). and mussel beds (Thiel & Dernedde, 1994). These habitats Using predator exclusion experiments, Palma & Steneck tend to be polychromatic and complex compared to the more (2001) found that polymorphic rock crabs (Cancer irroratus homogeneous background of sand, macroalgae and rock that Say, 1817) were harder to fi nd against a background of the adults generally inhabit. Two, non-mutually exclusive, cobblestones and sand than one made of grey plastic. Thus,

543 Todd et al: Ontogenetic shifts in crab colouration. polymorphism in juvenile crabs may also be associated adult patterning and/or colouration, all species in the fi nal with living among the complex substrates that are often database were mapped onto a taxonomic tree based on characteristic of their nursery grounds. the nomenclature and systematics described in Ng et al. (2008). The hypothesis that patterned adult C. maenas are rare because they are preferentially preyed upon when young was dismissed by Hogarth (1978) based on the fact that, RESULTS if the absence of patterned adults was due to predation pressure on juveniles, then the genes for patterning would A total of 21 species that undergo ontogenetic shifts in be removed from the population over time and therefore no patterning and/or colouration were described in published such crabs would exist at any life stage. But the inverse is literature. Sixteen species are polymorphic and/or patterned true, with a high number of juvenile patterned shore crabs as juveniles and become monochromatic or much plainer identifi ed by Hogarth (1975) and, 30 years later, by Todd as they mature (Table 1). Two species, Atergatis fl oridus et al. (2005, 2006). The same argument can be used for (Linnaeus, 1767) and A. integerrimus (Lamark, 1818) are age-dependent changes from polymorphic to monomorphic patterned as both juveniles and adults, but the patterns change. populations and, throughout this paper, we assume that One species, Pugettia producta (Randall, 1840), changes the species listed in Table 1 undergo ontogenetic shifts as from one monomorphic colour (red) to another (amber). opposed to juveniles being preferentially preyed upon. The remaining two species, Chiromantes haematocheir (De Haan, 1833) and (male) Portunus pelagicus (Linnaeus, In the species that are known to change from patterned 1758) have more complex colour patterns as adults than as and/or polymorphic to monochromatic with maturity; the juveniles. transformation is dramatic and most likely refl ects a critical life-stage that is possibly unique to marine arthropods The 29 species, including the eight described by Palma et (Palma & Steneck, 2001). Palma et al. (2003) identifi ed al. (2003), span nine Eubrachyura superfamilies (Fig. 1) and eight species of near-shore brachyuran crabs in central represent a worldwide distribution (Table 1). The Xanthinae Chile that are polymorphic, and often cryptically coloured, contain six species of crabs that undergo ontogenetic as juveniles but not as adults. In this study, we build on shifts in patterning and/or colouration. Cancridae contains Palma et al.’s (2003) work by determining the prevalence fi ve species, Portunidae contains four species, Epialtidae of these ontogenetic shifts in intertidal and subtidal crabs three, Menippidae and Hymenosomatidae two each, and worldwide. Data were gathered from primary and grey the families Platyxanthidae, Pilumnidae, Pilumnoididae, literature (including website searches) and via direct Pseudoziidae, Sesarmidae, Varunidae and Ocypodidae all correspondence with crustacean biologists around the globe. contain one species that change colour with age. We aim to establish whether the juvenile-to-adult change in carapace patterning observed in C. maenas is representative Numerous other species were proposed by scientists of a wider predator-avoidance strategy among crab species contacted by email as undergoing shifts in patterns and/ that live in intertidal and subtidal habitats. or colours that could not be confi rmed in the literature, including: Glebocarcinus amphioetus (Rathbun, 1898), Chasmagnathus convexus (De Haan, 1835), Eriphia MATERIALS AND METHODS sebana (Shaw & Nodder, 1803), Eriphia smithii (Shaw & Nodder, 1803), Gaetice depressus (De Haan, 1835), The database of subtidal and intertidal crabs that are Leucosia anatum (Herbst, 1783), Leptodius exaratus (H. known to shift from patterned to unpatterned and/or from Milne Edwards, 1834), Ocypode stimpsoni Ortmann, 1897, polymorphic to monomorphic populations was assembled Pseudozius caystrus (Adams & White, 1849), Uca crassipes from a variety of sources: 1) primary literature via the (White, 1847), and Uca tetragonon (Herbst, 1790). online resources Web of Science and JSTOR using combinations of approximately 20 key words; 2) primary We have not included the eight species listed by Palma et al. and grey literature via electronic and manual searches of (2003) in Table 1 as there is too little information regarding the National University of Singapore library, the Raffl es their preferred habitats; however, they have been mapped Museum of Biodiversity library and Prof. Peter Ng’s onto the taxonomic tree in Fig. 1. personal collections; 3) primary literature, grey literature, and website searches via Google and Google Scholar using combinations of approximately 20 key words; 4) via expert DISCUSSION scientific opinions, through personal interviews, email correspondence and a general query posted on CRUST- Through a combination of literature searches and anecdotal L (a mailing list for crustacean biologists). Whenever observations we have established that at least 21 species of possible, differences in juvenile and adult habitats, and their subtidal and intertidal crabs undergo ontogenetic shifts in geographical distribution, were noted. carapace patterning and/or colouration. Together with the eight identifi ed by Palma et al. (2003), the list now totals To examine the spread among superfamilies, familes and 29 species. This number is likely to be an underestimate sub-families for taxa that display different juvenile and as, for many species, information on juvenile carapace

544 THE RAFFLES BULLETIN OF ZOOLOGY 2009

) Palma et al. (1998); Castro (Pers. comm.) Palma & Steneck (2001) c McLay (1988) c Wicksten (2008) c Meinkoth (1981) c Jensen (1995)

Atlantic Todd et al. (2005; 2006) Southeast Asia South China Sea to Mediterranean Muiño et al. (1999) Japan to Hong Kong Ades et al. (2006) Queensland, Australia

Red with patterns aged as

carapace Dull grey white spots are common white patches white red, markings red, and occasionally and orange and white white band across their white band and sand or shell hash anterior portion of become dull maroon often dull with white, Geographical distributions from the Integrated Taxonomic Information System (2008). .

ne muddy Polymorphic with Pale reddish-brown Northeast Atlantic Ng (1998); fi subtidal or in crevices around carapace sand or gravel patterned comprising seasonal marshes, rocky outcrops and white, orange, brown. brick red intertidal to shallow dark, yellow streams, river banks Intertidal to subtidal Purple with Greenish blue/ brown c, Western Pacifi Ng & Davie (2007) muddy or shell bottoms colour; camoufl Coral reefs, under rocks Red with white margin Red with white spots c, Southwest Pacifi Tan & Ng (1988) sandy or gravel bottoms Can also be patterned. Bays and estuaries; sandy, More variable in Olive grey-green Northeast Pacifi

– – – beds Musselbeds, Rocky shore and Juveniles are Generally a dull East and Indo-west Crothers (1968); intertidal zone shallow subtidal when available seaweed beds. polymorphic and green/grey/brown c, east and west Pacifi Hogarth (1975; 1978) Pebble beaches Rocky and cobble shores Some dark patches No patches Red Sea to Japan and Simoes et al. (2001) lower intertidal) lower intertidal) ecked with black, fl black tints. or muddy ground; or muddy ground; with white patches mid to low intertidal cobble; mid and low e.g. white, brown, tan, remainder dark Randall, Cancer productus Kelp and eelgrass maenas Carcinus Sheltered areas with Polymorphic, e.g. red, Homogeneously dull Callinectes arcuatus Northeast Pacifi Cancer pagurus Linnaeus, Under boulders, coarse Under boulders, coarse White or purple-brown Reddish-brown Northeast Atlantic Bennett (1995 Hemigrapsus oregonensis Intertidal (under rocks) Intertidal (under rocks) White or mottled patterns Dark or grey-green Northeast Pacifi Chiromantes haematocheir Chiromantes Coastal Bays Back mangroves innominatus Halicarcinus Intertidal (especially Intertidal (especially Pale yellow carapace Brown with green or Southwest Pacifi Echinoecus pentagonus Shallow-subtidal Shallow-subtidal Dark red-brown with a Females tend to lose Hawaii to Australia Chia et al. (1999) Leptodius exaratus Say, Cancer irroratus Either sand or cobble; Highest survival on Colour polymorphism, Mostly brown, the Northwest Atlantic Haefner (1976); – Subtidal; depurator – Liocarcinus Species name oridus fl Atergatis integerrimus Atergatis Juvenile habitat Adult habitat Juvenile carapace Adult carapace Distribution References Ordway, 1863 (De Haan, 1833)

1758 5 1840 6 Linnaeus, 1758) 7

4 Richardson, 1949 11 (Dana, 1851) 8 10 9 (A. Milne Edwards, 1879)

12 (H. Milne Edwards, 1834) 1817 (Lamarck, 1818) 3 (Linnaeus, 1758) 13 (Linnaeus, 1767) 1 2 Table 1. Species that exhibit ontogenetic shifts in carapace patterning and /or colouration

545 Todd et al: Ontogenetic shifts in crab colouration. 6)

Stachowicz (2008) c c Crane (1975) c Wicksten (2008)

Red Sea to Simoes et al. (2001) Alaska to Mexico Hultgren &

Amber females dull females greenish-brown

Red patterned occasionally patterned Southwest Pacifi pinkish hue with white spots; c to Eastern Pacifi Svane & Hooper (2004) transverse stripes Pale-coloured with Males bright blue Western Indian Ocean Jensen (1995); brown or tan markings

habitats subtidal Cobble beaches Polymorphic, often Polymorphic, in bays and estuaries carapace with white, yellowish-orange Intertidal; among rocks May have mottled Brownish-red to Northeast Pacifi

colours

– – subtidal Crevices among Burrows and crevices Wide variety of colours Brownish red with Western North Atlantic Geiger & Bert (2006) (brackish water) (brackish water) bright and striking in colour than juveniles red algae habitats creeks and mudfl ats) creeks and mudfl intertidal and shallow intertidal and shallow polymorphic; white polymorphic Northeast Atlantic Schubart (2007) Intertidal and subtidal Subtidal giant kelp (Olivi, Xantho poressa Colourful pebbles; Rocky substrate; Higher proportion Lower proportion Mediterranean and Reuschel & Menippe mercenaria Menippe mercenaria anthonyi Metacarcinus Portunus pelagicus Intertidal (mangrove , Pugettia producta Subtidal Species name Menippe adina Williams Interstices of oyster Mixed hard and muddy Wide variety of colours Juvenile habitat Uniformly dark, Adult habitat Western North Juvenile carapace Geiger & Bert (200 Adult carapace Distribution References Pseudozius caystrus Uca capricornis Crane, River/stream mouths River/stream mouths Often patterned with Darker and duller Southwest Pacifi (Randall, 1840) 21 1792) (Linnaeus, 1758) & Felder, 1986 15 (Say, 1818) 16 (Rathbun, 1897) shells 17 barnacles, sponges, among rocks in seagrass bottoms, mud borrows, and markings and markings 19 (Adams and White, 1849) tunicates, calcareous algae and bryozoans and sand/shell hash blue/black spots habitats oyster reefs. from North Carolina Atlantic, North to Belize Carolina to Belize Table 1. (Continued). 14

18 20 1975

546 THE RAFFLES BULLETIN OF ZOOLOGY 2009 patterns and colours (and habitat preference) is absent. & Steneck, 2001). Alternatively, the information regarding Changes in patterning and/or colouration are not restricted their habitats might be incomplete. We found that the most to any particular taxon of crabs, suggesting that they could critical information, i.e. the microhabitat where the juvenile have arisen independently in many families—perhaps as spends the majority of its time and is thus most potentially a response to local environmental conditions where such at risk (Endler, 1978), was frequently missing, making it shifts could confer a selective advantage. diffi cult to decipher what reported changes in patterning/ colouration mean. Of the 16 species listed in Table 1 that are polymorphic and/or patterned as juveniles and monochromatic as The rationalisations above do not elucidate why Atergatis adults, the juvenile habitat is only known for ten. Six of floridus, A. integerrimus and Pugettia producta are these species move from one environment to another as patterned or coloured (albeit differently) as both juveniles they mature and it is possible the accompanying shift in and adults or why Chiromantes haematocheir and (male) patterning and/or colouration is adaptive, i.e. there exists Portunus pelagicus have more brightly coloured adults phenotype-environment matching that reduces predation than juveniles. There are various reasons that may explain risk (Todd et al., 2006). The remaining four species, Cancer these incongruous fi ndings; the most likely is that adults pagurus Linnaeus, 1758, Echinoecus pentagonus (A. Milne- move to another type of habitat where camoufl age might Edwards, 1879), Halicarcinus innominatus Richardson, be better provided by different patterns or colours. For 1949 and Hemigrapsus oregonesis (Dana, 1851) undergo example, Pugettia producta changes from red to amber changes from colourful juvenile morphs to duller adults, with age (a result of sequestration of pigments from the but do they not appear to migrate between environments algae it inhabits and eats) and yet maintains an excellent with age. This non-migration was also inferred for the eight phenotype-environment match (Hultgren & Stachowicz, species in Palma et al. (2003), as the authors did not record 2008). Alternatively, it is possible that ontogenetic shifts in separate habitats for juveniles and adults. If the juvenile colouration are not predation-related, but instead associated colours are camoufl aging, they could be lost at maturity with intraspecifi c, or intrageneric, communication, e.g. for simply because adults are less vulnerable and thus do not crabs to signal their social status or breeding condition. need this kind of protection from visual predators (Palma Finally, bright adult colouration could be aposematic; but

Fig. 1. Taxonomic tree showing spread among superfamilies, families and sub-families among the species found to exhibit different carapace patterns between adults and juveniles. Species from Palma et al. (2003) are marked with an asterisk (*). Taxonomy and nomenclature follows Ng et al. (2008).

547 Todd et al: Ontogenetic shifts in crab colouration. aposematism is associated with distastefulness (Ruxton et to his personal library. Peter Hogarth fi rst suggested this al., 2004) which most crabs are not (although they might study and various members of the 2008 Marine Biology be mimicking a distasteful organism). class, NUS, provided input. This project was supported by Singapore’s Ministry of Education grant number R-154- Berke & Woodin (2008) list ontogentic shifts in setal 000-414-133. morphology and decorating behaviour in many species of decorator crab. Decoration is an effective camoufl age (Hultgren & Stachowicz, 2008) and its loss with age is LITERATURE CITED analogous to the ontogentic loss of carapace patterns and colours discussed in this paper. Berke & Woodin (2008) Adams, A. & A. White, 1849. Crustacea. Part 2. In: A. demonstrate an energetic cost to decorating, arguing that Adams (ed.), The zoology of the voyage of H.M.S. that this, combined with the size-refuge achieved by adults, Samarang under the command of Captain Sir Edward Belcher, would lead to a shift away from decorating. A similar during the years 1843–1846. Benham & Reeve, London. i–viii, mechanism may be involved in the ontogentic shifts in 33–67, pls. 7–13. carapace patterns and colouration discussed in this paper. Ades, G. W. J., R. O. Baretto, M. Kilburn, R. W. Lewthwaite, K. Todd et al. (2006) noted that the process of losing markings A. Baretto, R. C. Kendrick, M. W. N Lau & S. C. Ng, 2006. Tai in C. maenas could be accentuated if the pigments involved Po Kau Headland – Conservation Study and S.S.S.I. Proposal. require an energetic cost to maintain. This potential cost has not yet been quantifi ed, but it is unlikely to be as great as Bedini, R., 2002. Color change and mimicry from juvenile to adult: it is for decorator crabs. Xantho poressa (Olivi, 1792) (Brachyura, Xanthidae) and Carcinus maenas (Linnaeus, 1758) (Brachyura, Portunidae). Crustaceana 75 Some crabs, such as Uca capricornis (Crane, 1975), can , : 703–710. undergo rapid changes in colouration (Detto et al. 2008), but Bennett, D. B., 1995. Factors in the life history of the edible crab it is probable that the shifts discussed here occur between (Cancer pagurus L.) that infl uence modelling and management. moults. More work is required on the species listed in ICES Marine Science Symposia, 199: 89–98. Table 1 to confi rm this. Crothers (1968) kept a single C. Berke, S. K. & S. A. Woodin, 2008. Energetic costs, ontogenetic maenas through three moults and noted that it fi rst gained shifts and sexual dimorphism in majoid decoration. Functional some white pigment before losing it again. Hogarth (1983) Ecology, 22: 1125–1133. found that approximately 30% of young C. maenas changed Chia, D. G. B., P. Castro, & P. K. L. Ng, 1999. A revision of patterns between moults, but only a third of these did so the genus Echinoecus Rathbun, 1894 (Crustacea: Decapoda: dramatically. The precise timing of ontogenetic shifts in Brachyura: Eumedonidae). Journal of Crustacean Biology, 19: 809–824. colours and patterns is also poorly known, as is the potential for multiple changes over time. Cott, H. B., 1940. Adaptive colouration in animals. New York: Oxford University Press. The results presented in Table 1 represent a wide range Crane, J., 1975. Fiddler crabs of the world: Ocypodidae: Genus of searches and sources, but they are not exhaustive. For Uca. Princeton University Press, Princeton, New Jersey. example, it was not feasible to search foreign language Crothers, J. H., 1968. The biology of the shore crab Carcinus papers for mention of ontogenetic shifts in the same manner maenas (L.) 1. The background—anatomy, growth and life that we searched English language articles. Geographic history. Field Studies, 2: 407–434. biases in where reports originate are evident, for instance, Cuthill, I. C., M. Stevens, J. Sheppard, T. Maddocks, C. A. by searching specifi cally for polymorphic and/or patterned Párraga & T. S. Troscianko, 2005. Disruptive coloration and juvenile crabs Palma et al. (2003) found eight species in background pattern matching. Nature, 434: 72–74. central Chile alone. Very few papers describe both juvenile Cuthill, I. C., M. Stevens, A. M. M. Windsor & H. J. Walker, 2006. and adult patterns and colours in subtidal and intertidal The effects of pattern symmetry on detection of disruptive species and we predict that more directed studies would and background-matching coloration. Behavioral Ecology, uncover similar trends to Palma et al. (2003). Generally, 17: 828–832. a better understanding of microhabitat use, as well as Dana, J. D., 1851. Conspectus crustaceorum quae in orbis behaviour and ecology in relation to defence, would help terrarum circumnavigatione, Carol Wilkes e classe republicae elucidate the function of ontogenetic shifts in carapace foederatae duce, lexit e descripsit. Proceedings of the Academy patterning and/or colouration in intertidal and subtidal of Natural Sciences of Philadelphia, 5: 267–272. brachyuran crabs. Detto T., J. M. Hemmi & P. R. Y. Backwell, 2008. Colouration and colour changes of the fi ddler crab, Uca capricornis: A descriptive study. PLoS ONE 3: e1629. ACKNOWLEDGEMENTS Ekendahl, A. & K. Johannesson, 1997. Shell colour variation in Littorina saxatilis Olivi ( Prosobranchia: Littorinidae): We would like to thank all the scientists who so generously a multifactor approach. Biological Journal of the Linnaean shared their observations and data with us. We are also Society, 62: 401–419. extremely grateful to the Raffl es Museum of Biodiversity Endler, J. A., 1978. A predator’s view of animal color patterns. and its Director, Prof. Peter Ng, who kindly offered access Evolutioary Biology, 11: 319–364.

548 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Endler, J. A., 1984. Progressive background matching in , McLay, C. L., 1988. Crabs of New Zealand. University of and a quantitative measure of crypsis. Biological Journal of Auckland, Leigh Marine Laboratory, Christchurch, New the Linnaean Society, 22: 187–231. Zealand. Geiger, S. P, & T. M. Bert, 2006. Coloration characterization of Meinkoth, N. A., 1981. National Audubon Society fi eld guide to postsettlement juvenile stone crabs (genus Menippe De Haan, North American seashore creatures. Alfred A. Knopf Inc., 1833) in the Gulf of Mexico. Crustaceana, 79: 1369–1391. New York. 813 pp. Goodhart, C. B., 1987. Why are some snails visibly polymorphic, Milne-Edwards, A., 1879. Description de quelques Crustacés and others not? Biological Journal of the Linnaean Society, nouveaux. Bulletin de la Société philomatique, Paris 7(3): 31: 35–58. 103–110, pls. 1–2. Haan, W. de, 1833. Crustacea. In: von Siebold P. F. Fauna (ed.) Milne Edwards, H., 1834. Histoire naturelle des Crustacés, Japonica, sive Descriptio animalium, quae in itinere per comprenant l’anatomie, la physiologie et la classifi cation de Japoniam, jussu et auspiciis superiorum, qui summum in India ces animaux. Librairie Encyclopédique de Roret. Vol. 1. Paris: Batava imperium tenent, suscepto, annis 1823–1830 collegit, Roret. 468 pp. notis, observationibus et adumbrationibus illustravit P.F. de Muiño, R., L. Fernández, E. González-Gurriarán, J. Freire & Siebold. Conjunctis studiis C.J. Temminck et H. Schlegel pro J. A.Vilar, 1999. Size at maturity of Liocarcinus depurator Vertebratis atque W. de Haan pro Invertebratis elaborata Regis (Brachyura: Portunidae): a reproductive and morphometric aupicus edita. Leiden, Lugundi-Batavorum. Decas II, 25–64, study. Journal of the Marine Biological Association of the pls. 9–15, 17, C, D. United Kingdom, 79: 295–303. Haefner, P. A., 1976. Distribution, reproduction and moulting of Ng, P. K. L., 1998. Crabs. In: Carpenter, K.E. & Niem, V.H. (eds.), the rock crab, Cancer irroratus Say, 1817, in the mid-Atlantic The Living Marine Resources of the Western Central Pacifi c. Bight. Journal of Natural History, 10: 377–397. Vol. 2. Cephalopods, crustaceans, holothurians and sharks. Herbst, J. F. W., 1783. Versuch einer Naturgeschichte der Krabben Food and Agriculture Organisation of the United Nations und Krebse nebst einer systematischen Beschreibung ihrer (Rome). Pp. 1045–1156. verschiedenen Arten, 1(2–5): 87–182, pls. 2–9. Ng, P. K. L. & P. J. F. Davie, 2007. On the identity of Atergatis Herbst, J. F. W., 1790. Versuch einer Naturgeschichte der Krabben fl oridus (Linnaeus, 1767) and Atergatis ocyre (Herbst, 1901) as und Krebse, nebst einer systematischen Beschreibung ihrer a valid species from the Indian Ocean (Crustacea: Brachyura: verschiedenen Arten, 1(8): 239–274, pls. 18–21. Xanthidae). Raffles Bulletin of Zoology Supplement, 16: Hogarth, P. J., 1975. Pattern polymorphism in the shore crab 169–175. Carcinus maenas (L.). Crustaceana, 28: 316–319. Ng, P. K. L., D. Guinot & P. J. F. Davie, 2008. Systema Hogarth, P. J., 1978. Variation in carapace pattern of juvenile Brachyurorum: Part I, An annotated checklist of the extant Carcinus maenas. Marine Biology 44: 337–343. Brachyuran crabs of the world. Raffl es Bulletin of Zoology, 17: 1–286. Hogarth, P. J., 1983. Crabs in labs: the shore crab (Carcinus maenas) as teaching material. Journal of Biological Education, Olivi, G., 1792. Zoologia Adriatica ossia Catalogo ragionato degli 17: 105–111. Animali del Golfo e delle Lagune di Venezia; preceduto da una Dissertazione sulla Storia fi sica e naturale del Golfo; e Hovel, K. A. & R. N. Lipcius, 2002. Effects of seagrass habitat accompagnato da Memorie, ed Osservazioni di Fisica Storia fragmentation on juvenile blue crab survival and abundance. naturale ed Economia. 334 pp. Journal of Experimental Marine Biology and Ecology, 271: 75–98. Ordway, A., 1863. Monograph of the genus Callinectes. Journal of the Boston Society of Natural History 7: 567–583. Hultgren, K. & J. J. Stachowicz, 2008. Alternative camoufl age strategies mediate predation risk among closely related co- Ortmann, A. E., 1897. Carcinologische Studien. Zoologischer occurring kelp crabs. Oecologia, 155: 519–528. Jahresbericht, Abteilung für Systematik, Geographie und Biologie der Thiere, 10: 258–372, pl. 17. Integrated Taxonomic Information System, 2008. Integrated Taxonomic Information System online database. early post-settlement strategies between American lobsters Homarus americanus and rock crab Cancer irroratus in Jensen, G. C., 1995. Pacific coast crabs and shrimps. Sea the Gulf of Maine. Marine Ecology Progress Series, 162: Challengers, Monterey (California). 215–225. Jones J. S., B. H. Leith & P. Rawlings, 1977. Polymorphism in Palma, A. T. & R. S. Steneck, 2001. Does variable coloration in Cepaea: A problem with too many solutions? Annual Review juvenile marine crabs reduce the risk of predation? Ecology, Ecology and Systemetics, 8: 109–143. 82: 2961–2967. Lamarck, J. B. P. A. de, 1818. Histoire naturelle des animaux sans Palma, A., C. Orrego & M. Arriagada, 2003. Crypsis in early vertèbres. Vol. 5. Paris. 612 pp. benthic phases of Brachyura decapod crustaceans in central Linnaeus, C., 1758. Systema Naturae per Regna Tria Naturae, Chile. Revista Chilena de Historia Natural, 76: 149–156. Secundum Classes, Ordines, Genera, Species, cum Pietrewicz, A. & Kamil A. C., 1979. Search image formation in the Characteribus, Differentiis, Synonymis, Locis. Edition 10. Vol. blue jay (Cyanocitta critata). Science, 204: 1332–1333. 1. Holmiae [Stockholm]: Laurentii Salvii. 823 pp. Parsonage, S. & J. Hughes, 2002. Natural selection and the Linnaeus, C., 1767. Systema Naturae per Regna Tria Naturae, distribution of shell colour morphs in three species of Littoraria Secundum Classes, Ordines, Genera, Species, cum (Gastropoda: Littorinidae) in Moreton Bay, Queensland. Characteribus, Differentiis, Synonymis, Locis. Edition 12. Biological Journal of the Linnaean Society, 75: 219–232. Vol. 1. Vindoboniae. Pp. 533–1327.

549 Todd et al: Ontogenetic shifts in crab colouration.

Randall, J. W., 1840. Catalogue of the Crustacea brought by Stevens, M., I. C. Cuthill, A. M. M. Windsor, & H. J. Walker, Thomas Nuttall and J. K. Townsend, from the west coast of 2006. Disruptive contrast in animal camoufl age. Proceedings North America and the Sandwich Islands, with descriptions of of the Royal Society B, 273: 2433–2438. such species as are apparently new, among which are included Svane I. & G. Hooper, 2004. Blue Swimmer Crab (Portunus several species of different localities, previously existing in the pelagicus) Fishery. Fishery Assessment Report to PIRSA collection of the Academy. Journal of the Academy of Natural for the Blue Crab Fishery Management Committtee. South Sciences of Philadelphia, 8(1): 106–147. Australian Research and Development Institute (Aquatic Rathbun, M. J. 1897. Description of a new species of Cancer from Sciences), Adelaide. Lower California, and additional note on Sesarma. Proceedings Tan, L. W. H. & P. K. L. Ng, 1988. A guide to seashore life. The of the Biological Society of Washington, 11: 111–112. Singapore Science Centre. Rathbun, M. J., 1898. The Brachyura collected by the U.S. Fish Thiel, M. & T. Dernedde, 1994. Recruitment of shore crabs Commission Steamer Albatross on the voyage from Norfolk, Carcinus maenas on tidal fl ats: mussel clumps as an important Virginia to San Francisco, California, 1887-1888. Proceedings refuge for juveniles. Helgolander Meeresun. 48: 321–332. of the United States National Museum, 21: 567–616. Todd, P. A., R. J. Ladle, R. Briers & A. Brunton, 2005. Quantifying Reuschel, S. & C. D. Schubart, 2007. Contrasting genetic diversity two-dimensional dichromatic patterns using a photographic with phenotypic diversity in coloration and size in Xantho technique: case study on the shore crab (Carcinus maenas, poressa (Brachyuran:Xanthidae) with new results on its L.). Ecological Research, 20: 497–502. ecology. Marine Biology, 28: 1–10. Todd, P. A., R.A. Briers, R. J. Ladle & F. Middleton, 2006. Richardson, L. R., 1949. A guide to the Oxyrhyncha, Oxystomata Phenotype-environment matching in the shore crab (Carcinus and lesser crabs. Tuatara: Journal of the Bioloigcal Society of maenas). Marine Biology, 148: 1357–1367. New Zealand, 2(2): 58–69. Wente, W. H. & J. B. Phillips, 2003. Fixed green and brown color Ruxton, G. D., T. N. Sherratt & M. P. Speed, 2004. Avoiding morphs and a novel color-changing morph of the Pacifi c tree attack - The evolutionary ecology of crypsis, warning signals frog Hyla regilla. American Naturalist, 162: 461–473. and mimicry. Oxford University Press, New York. White, A., 1847. List of the specimens of Decapoda Crustacea Say, T., 1817. An account of the Crustacea of the United States. in the collection of the British Museum. London. Trustees of Journal of the Academy of Natural Science of Philadelphia, British Museum, i–viii, 1–143. 1(1-2): 57–63, 65–80, 97–101, 155–160, 161–169, pl. 4. Wicksten, M. K., 2008. Decapod Crustacea of the Californian Say, T., 1818. An account of the Crustacea of the United States. and Oregonian zoogeographic provinces. Scripps Institution Journal of the Academy of Natural Sciences of Philadelphia, of Oceanography Library. Paper 26. Shaw, G. & F. P. Nodder, 1803. Naturalist’s Miscellany, 15: Pls. Williams, A. B. & D. L. Felder, 1986. Analysis of stone crabs: 589–612. Menippe mercenaria (Say), restricted, and a previously Simoes, N., M. Apel & D. A. Jones, 2001. Intertidal habitats and unrecognized species described (Decapoda: Xanthidae). decapod faunal assemblages (Crustacea: Decapoda) of Socotra Proceedings of the Biological Society of Washington 99: Island, Republic of Yemen. Hydrobiologia, 449: 81–97. 517–543. Smith, D. A. S., 1975. Polymorphism and selective predation Whiteley, D. A. A., D. F. Owen & D. A. S. Smith, 1997. Massive in Donax faba Gmelin (Bivalvia: Tellinacea). Journal of polymorphism and natural selection in Donacilla cornea (Poli, Experimental Marine Biology and Ecology, 17: 205–219. 1791) (Bilvalvia: Mesodesmatidae). Biological Journal of the Linnaean Society, 62: 475–494.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 551–560 Date of Publication: 31 Aug.2009 © National University of Singapore

VERTICAL ZONATION AND HEAT TOLERANCE OF THREE LITTORINID GASTROPODS ON A ROCKY SHORE AT TANJUNG CHEK JAWA, SINGAPORE

Su-Li Lee Anglo-Chinese Junior College, 25 Dover Close East, Singapore 139745, Republic of Singapore

Shirley S. L. Lim Ecology Laboratory, Natural Sciences & Science Education, National Institute of Education, Nanyang Technological University, 1 Nanyang Walk, Singapore 637616, Republic of Singapore Email: [email protected] (Corresponding author)

ABSTRACT. – Three common rocky shore littorinid taxa, i.e., Littoraria spp. (a collective term for L. strigata and L. articulata), Echinolittorina malaccana and E. vidua occupied different tidal heights based on fi eld observations carried out at Tanjung [=Cape] Chek Jawa, Pulau [=Island] Ubin, Singapore in 2002. Littoraria spp. were consistently observed at a lower level on the shore than E. malaccana and E. vidua. Manually translocated littorinids returned to their preferred zones in the fi eld, i.e., E. malaccana returned to the region above the MHWS level of 2.7 m while Littoraria spp. remained below the region occupied by E. malaccana. Further, E. malaccana individuals with their shell nodules removed by fi ling did not occupy a lower zone than intact conspecifi cs in the fi eld. Although signifi cant temperature differences (TD)

were observed between rock and shell surfaces in the laboratory (TDLittoraria ≈ TDfi led E. malaccana < TDE. malaccana), preference for a particular height on the shore is probably governed more by physiological factors (e.g., heat tolerance) than by morphological adaptation (e.g., shell morphology). As the upper shore is exposed to the sun for longer periods of time, it is expected that the heat tolerance of inhabitants of the higher shore would be greater than those occupying the lower regions. Results of a 1-hour lethal temperature experiment

support this hypothesis: the temperature at which 50% mortality (1h LT50) was observed was highest for E. malaccana (50.4°C) compared to E. vidua, (48.1 °C) and Littoraria spp. (47.5°C), possibly refl ecting their relative tidal positions on the shore. Enzyme stability may also account for high heat tolerance of E. malaccana. Incubation of the enzyme, glutamate oxaloacetate transaminase (GOT) at 55°C showed that E. malaccana sustained high GOT activity compared to those of Littoraria spp. and E. vidua which decreased sharply at the same temperature, again suggesting inherent physiological adaptation in E. malaccana.

KEY WORDS. – Zonation; heat tolerance; enzyme stability; Littoraria sp.; Echinolittorina malaccana; Echinolittorina vidua.

INTRODUCTION spanning many days (McMahon, 1990). Desiccation may be overcome by behavioural adaptations such as the The intertidal rocky shore is universally divided into withdrawal of the foot and closure of the shell opening zones according to characteristic intertidal fl ora and fauna with an operculum to reduce evaporation. Attachment to (Raffaelli & Hawkins, 1996): the supralittoral, midlittoral the substratum using a mucous sheet – the mucous holdfast and sublittoral zones. Such zonation is due to the stresses of (Bingham, 1972; Lim, 2008), further ensures that they will varying intensities along the height of the shore. Higher levels not be dislodged easily or maintain minimal contact with the of the shore (e.g., supralittoral zone) are exposed to the air and heated substratum when out of water. Survival in prolonged sun for a longer period of time when compared with lower aerial exposure also depends on physiological adaptations shore levels (Newell, 1979; Cleland & McMahon, 1989). such as the reduction of metabolic rates, e.g., in Littorina Despite the extreme physical conditions in the supralittoral saxatilis (see McMahon & Russell-Hunter, 1977) and zone, many gastropod species have adapted successfully to elevated thermal tolerance, e.g., in Nodilittorina pyramidalis, life in this harsh zone. Gastropods living above the high tide N. granularis and Littorina brevicula (see Fraenkel, 1966) mark are especially vulnerable to desiccation and thermal as well as Austrolittorina unifasciata (= N. unifasciata; see stress, as they typically experience prolonged aerial exposure Reid, 2007) (see McMahon, 1990).

551 Lee & Lim: Vertical zonation and heat tolerance of Singapore littorinids

Common littorinids found on the rocky shores of Singapore in the cell (Cooper & Meister, 1985). The metabolic include Littoraria articulata (Philippi, 1846), L. strigata importance of GOT is that it brings about a free exchange (Philippi, 1846) (often as Littorina undulata in previous of amino groups between glutamate and aspartate; both of literature) and Echinolittorina malaccana (Philippi, 1847) which are required for separate but essential steps in the (also referred to in the literature variously as Nodilittorina urea cycle for ammonia detoxication and nitrogen excretion. pyramidalis or N. trochoides; see Reid, 2007). A less The free movement of nitrogen between the glutamate and common rough periwinkle, Echinolittorina vidua (Gould, aspartate pools is an important balancing process that is vital 1859) (previously Nodilittorina vidua; see Reid, 2007) is for normal cell metabolism (Cooper & Meister, 1985). also found in certain rocky areas in Singapore.

Two previous littorinid distribution studies have been MATERIAL AND METHODS conducted in Singapore on the south-eastern coast of Singapore; one at a man-made breakwater (see Lam, 1980) Distribution studies and the other at a monsoon drain (see Tan, 1988). To date, there is no published literature with quantitative data on Two distribution studies were carried out at the rocky the vertical distribution of Littoraria spp., Echinolittorina shore of Tanjung Chek Jawa on Pulau Ubin (approx. 1° malaccana and E. vidua at natural rocky shores in Singapore. 24’N, 103° 59’E), an island off the north-eastern coast of The purpose of the fi rst part of this study was to determine Singapore. The mean high water spring tide level (MHWS) the zonation pattern of these littorinids at the rocky shores at the study site is 2.7 m (Hydrographic Department, 2001). of Tanjung [=Cape] Chek Jawa, Pulau [=Island] Ubin, These studies were made at (i) a vertical rock and (ii) a Singapore, through a distribution survey. sloping rock (angle of inclination ≈ 35.6°). The vertical rock is located further inland (i.e., more up-shore in a little A translocation experiment involving Littoraria spp. and ‘cove-like’ recess) as compared to the sloping rock located E. malaccana was also carried out to verify the zonation at a small spit jutting out seawards. Hence, the vertical rock pattern observed. Dislodged littorinids are able to crawl surface studied is exposed earlier by the receding tide and upwards to their original zone, e.g., N. exigua (see Ohgaki, inundated later by the incoming tide when compared to the 1988a), Littorina littorea (see Petraitis, 1982) and Littorina sloping rock. Both rocks have sparse algal cover and a fair unifasciata (see Chapman, 1999). It is hypothesized that number of crevices. displaced Littoraria spp. and E. malaccana individuals in this study would return to their preferred zones. Reid (1986) reported that the two closely related species Littoraria articulata and L. strigata possess shells with Shell sculpturing was reported by Vermeij (1973) to reduce similar shape, colour and banding pattern, and without the relative effective areas for absorption, i.e., area in a plane examination of internal anatomical features, it was diffi cult that is perpendicular to incident sun’s rays. This implies that to ascertain their identities in the fi eld. Thus, these two there is greater heat loss by refl ection of solar radiation by littorinid species are collectively referred to as Littoraria an uneven surface, thereby reducing heat absorption. The spp. in this study as dissection of every individual shell of E. malaccana is nodulated while that of Littoraria encountered was neither feasible nor possible. Data from the spp. individuals is smooth. Since E. malaccana occupies vertical rock were collected during three sampling sessions: a higher region of the shore, the nodulation may be an June/July, September and December 2002, with a total advantage for survival under prolonged aerial exposure. of 10 transect belts laid at each session. The distribution The increased surface area of the shell due to the presence surveys were all carried out during three to fi ve days of of nodules could facilitate convection and heat loss from consecutive spring tides. Accessibility to the study site the shell. To test this hypothesis, the nodulated shells of was only possible when the tides were suitably low. Each E. malaccana individuals were fi led down and included belt transect consisted of a transparent 10 cm-wide plastic in the translocation study to elucidate the possible role of strip with a measuring tape attached. The position of each nodulation in zonation. The effect of nodulation on heat Littoraria spp. (collectively Littoraria) and Echinolittorina refl ection was tested both in the fi eld (for E. malaccana and malaccana (E. malaccana) individual encountered beneath Littoraria spp.) and in the laboratory (for E. malaccana, the strip was recorded to the nearest 0.5 cm. Distribution both intact and fi led, and Littoraria spp.). The temperature of Littoraria, E. malaccana and E. vidua was similarly difference between rock and shell surfaces was used as the determined at the sloping rock on 28 and 29 August 2002. response variable. A region covered by a total of 18 belt transects, each 15 cm in width, was surveyed. The tide level (TL) at the top Two laboratory experiments were conducted to establish of the vertical rock is 0.1 m above MHWS. possible physiology-related reasons for the zonation pattern: (1) a heat tolerance test, represented by 1 hour lethal temperatures (1h LT50), of the littorinids, and (2) a Translocation experiment heat stability test of the enzyme, glutamate oxaloacetate transaminase (GOT), extracted from these littorinids. The A translocation experiment was conducted in December enzyme GOT, also known as aspartate aminotransferase, 2002. Thirty individuals of Littoraria and 60 E. malaccana was chosen because it is one of the most active enzymes individuals were collected and transported to the laboratory

552 THE RAFFLES BULLETIN OF ZOOLOGY 2009 in a container (with seawater from the study site) for colour- would not be confounded by other factors, e.g., shade or coding with nail polish. The nodules of 30 E. malaccana refl ection of heat from adjacent surfaces. adult individuals were fi led off (henceforth termed “fi led E. malaccana”) using an ordinary machinist’s file. All The temperature difference (TD) between rock surface and experimental snails were returned to the study site within that of the shell surface (i.e., TD = Trock surface – Tshell surface) two days to minimize stress and ensure their survival during for E. malaccana and Littoraria were tested separately for the translocation experiment. Based on the distribution signifi cance using t-tests. TDLittoraria and TDE. malaccana were patterns observed from previous sampling periods, the then compared using the Mann-Whitney test statistic, as MHWS level (2.7 m) was found to approximately separate there was non-normality in the data set. In the laboratory, the regions occupied by Littoraria and E. malaccana. 25 E. malaccana, 25 fi led E. malaccana and 25 Littoraria Thus, the marked littorinids were returned to the 2.7 m were used in an experiment involving heat treatment. Five TL with the MHWS level clearly marked at the study E. malaccana, fi ve fi led E. malaccana and fi ve Littoraria site. Crowe & Underwood (1999) suggested that a snail’s were placed on a piece of relatively smooth rock that behaviour changed by merely dislodging it from its original most resembled that at the fi eld site. The rock was then position. This may affect the results of the translocation placed approximately 20 cm beneath a lamp and left to study. However, Chapman (1999) found that although warm up for 5 minutes. Pairs of temperature readings translocation affected the distance moved by the snails, it were then measured: the temperature of the shell surface did not result in any change in the direction at which the and the average temperature of the substrate surface at the snails dispersed. perimeter of the snail. The procedure was repeated until all 75 animals were used. A one-way ANOVA was used to test

During the next four consecutive days (16 to 20 December for signifi cant differences among TDLittoraria, TDE. malaccana and

2002), the distance between the locations of every marked TDfi led E. malaccana. In order to maintain approximately equal individual from the MHWS level was measured to the variances, two obvious outliers were removed prior to nearest 0.1 cm. The mean tidal level occupied by each ANOVA analyses. The distance of the infrared thermometer species on each of the four days was calculated. Crowe & from the surface was kept as constant as possible by Underwood (1999) cited that upon disturbance, littorinids maintaining the laser spot at approximately the same size are likely to require two days before resuming their natural during each measurement. ways. Thus, four days would be suffi cient for the duration of the translocation study. Data collected were analysed with one-way Analysis of Variance (ANOVA) tests to ascertain Lethal temperatures study whether the preferred zones occupied by the two species differed signifi cantly. The Tukey’s multiple comparison test Littoraria, E. malaccana and E. vidua individuals with shell was applied when ANOVA results were signifi cant. lengths between 7–11 mm were collected from the sloping rock at Tanjung Chek Jawa in November 2002. Snails were used within 24 hours of collection. The experiment Effect of shell nodulation of E. malaccana involved 12 temperature treatments between 44 and 52°C on heat refl ection (see below). For each temperature treatment, 30 littorinid individuals (i.e., 10 Littoraria, 10 E. malaccana and 10 E. Collection of data was carried out on two occasions: at vidua) were placed in an aluminium can containing 100ml Tanjung Chek Jawa and in the laboratory. Temperature of artifi cial seawater. Heat treatment of the snails submerged measured by a Raynger® ST™ infrared thermometer in seawater served to eliminate the effect of desiccation (see (Raytek®) was taken as an indication of the amount of Evans, 1948). A plastic cover was placed over the can to heat energy given off by the littorinid. The thermometer prevent water loss due to evaporation during heating. The detects emitted energy (e.g., radiated heat energy from seawater was brought to the required temperature in a water within the snail/gastropod) and refl ected heat energy (from bath from room temperature (22–23°C). The temperature an external source e.g., the sun). At Tanjung Chek Jawa, the of the seawater was measured with “K” type thermocouple average temperature of the shell of the rough periwinkle, probe connected to an AI 104 humidity temperature meter E. malaccana, was measured using the average-function of (Azex Instruments (S) Pte. Ltd.). The probe was inserted the infrared thermometer. The average temperature of the through a hole in the plastic cover. Once the required rock surface, i.e., at the perimeter of the animal, was then temperature was attained, the time was noted and the measured. Likewise, the temperatures of the shell surface seawater was maintained at a relatively constant temperature of the smooth periwinkle, Littoraria, and the surrounding for an hour (the temperature was monitored and recorded surface were measured under direct sunlight. A total of 55 at 15 minute intervals). This length of time was used by pairs of temperature readings were recorded for individuals Fraenkel (1966) in a heat stress experiment conducted of various sizes in each species. All individuals, whose shell on 12 species of intertidal prosobranchs in south-western temperatures were measured, were selected such that they Japan. The time taken for the seawater to reach the required were found on relatively smooth surfaces and not in any temperature ranged between 20 and 30 minutes. Monitoring sort of pit or crevice. This was to ensure that measurements of seawater temperatures indicated that the seawater could

553 Lee & Lim: Vertical zonation and heat tolerance of Singapore littorinids not be assumed to be at the temperature shown by the water calculated. Glutamate oxaloacetate transaminase (GOT) bath as the temperature probe that was inserted into the activity (µmol NADH/min/g wet weight) was calculated experimental container registered some fl uctuations. Hence, according to the following formula: the temperature of each heat treatment was taken to be the average temperature of the temperatures recorded during the (ΔA/min) (total volume) (volume of buffer hour. The resultant 12 temperature treatments were 44.1°C, + wet weight of tissue) × 50 44.7°C, 45.6°C, 47.0°C, 47.4°C, 48.0°C, 48.4°C, 48.7°C, GOT = 49.5°C, 50.3°C, 50.8°C and 51.8°C. The temperature range 6.22 × sample volume × wet weight of tissue selected was based on temperatures observed in the fi eld. There were six replicates for each of the four temperature After heat treatment, the littorinids were then transferred to treatments for all three littorinid taxa. GOT activity was the centre of a holding tank containing artifi cial seawater converted to a percentage value based on the results and an algae-covered rock. The tank was left in a normal of previous temperatures, as an indication of change in external environment (i.e., out of the air-conditioned activity due to increase in temperature. Data were arcsine- laboratory). At the end of 24 hours in the holding tank, transformed and analysed with one-way ANOVA. This the number of live individuals was recorded. An individual was performed only on data for 50°C and 55°C, as most was considered to be alive if it displayed foot attachment, of the data for 25°C and 45°C were greater than 100% and had scaled up the sides of the tank, moved onto the rock or could not be arcsine-transformed. All statistical analyses responded to gentle prodding of the foot. The percentage in this study were carried out using MINITAB (Release mortalities obtained were converted into probit values and 12.21, 1998). graphed against temperature. The 1-hour lethal temperature

(1h LT50) of each group was taken to be the temperature at which there was 50% mortality. As it was not feasible to RESULTS have a large sample size, statistical analyses of the 1h LT50s was not carried out. Distribution studies

At the vertical rock study site, Littoraria and E. malaccana Heat stability of GOT were found in two distinct regions of the high intertidal zone in June/July (Fig. 1a): Littoraria occupied the lower region Six samples of tissues (each consisting approximately 0.5 g and E. malaccana, the higher region. The boundary between fresh weight of pooled fl esh from a few individuals) of each the two regions was located approximately at 2.6 m (0.1 m of the three littorinid taxa were frozen using liquid nitrogen below MHWS). The mean tide level (mean TL) occupied and stored at -80°C. The frozen samples were pounded to by E. malaccana was 2.8 ± 0.2 m (range = 2.4 m to 3.6 m) powder in liquid nitrogen, reweighed and homogenised while that of Littoraria was 2.0 ± 0.2 m (range = 1.8 m to with thrice their weight of cold 0.05M Tris-HCl buffer 3.1 m) (Fig. 1a). In September 2002, the mean TL occupied (from Sigma), pH 7.0. Homogenisation was done using a by E. malaccana increased to 3.0 m ± 0.3 m (range = 2.1 Polytron PT1300D homogeniser for a duration of 3 × 20 s m to 3.5 m), while that of Littoraria also increased to 2.3 with 20 s intervals. The homogenates were sonicated with ± 0.2 m (range = 1.9 m to 3.2 m) (Fig. 1b). The band of E. a Heat Systems sonicator at 40% output power for one malaccana had a 0.6 m overlap with of the Littoraria band. minute. The mixtures were centrifuged at 9000 rpm, 4 °C In December 2002, the overlapping region decreased to 0.3 for 10 min in a Beckman J2-MC refrigerated centrifuge. The m in width (Fig. 1c). E. malaccana was found between TL supernatants were pipetted into clean test tubes, which were of 2.5 m to 3.6 m (mean TL = 3.2 ± 0.3 m) and Littoraria kept in ice. Enzyme analyses were conducted within a few was found between TL of 2.0 m to 3.5 m (mean TL = 2.4 of hours of sample preparation using the GOT optimized ± 0.2 m) (Fig. 1c). At the sloping rock, E. malaccana also aspartate-aminotransferase EC 2.6.1.1 UV-test kit (Sigma). occupied the highest region of the rock (range = 2.6m to The sample used for enzyme analyses was a 50× dilution 2.8 m) while E. vidua individuals occupied a region that of the extract (0.03 ml of the supernatant mixed with 1.47 overlapped with that of Littoraria (Fig. 2). The distribution ml of Tris-HCl buffer, pH 7.0). Prior to enzyme analyses, of E. vidua extended slightly higher than the Littoraria zone Reagent A (260 mmol/L aspartate, 104 mmol/L phosphate but was distinctly below that of E. malaccana. buffer pH 7.4, 0.234 mmol/L NADH, 780 U/L MDH and 1560 U/L LDH) and the samples were incubated separately at 25°C, 45°C, 50°C and 55°C for 30 minutes. After the Translocation experiment 30 min incubation, 0.1 ml of sample was added to 1.3 ml of Reagent A and mixed by inversion. After a minute of The mean TL occupied by Littoraria on the four consecutive incubation in a temperature controlled cuvette compartment days was slightly lower than the MHWS level of 2.7 m while of a UV-1601 spectrophotometer with a CPS temperature E. malaccana and fi led E. malaccana were found at least controller (Shimadzu), 0.125 ml of Reagent B (156 mmol/L 0.3 m above the MHWS level (Table 1). One-way ANOVA 2-oxoglutarate) was added and mixed. The absorbance of results showed that on all four days there was a signifi cant the mixture was recorded eight times at 25 s intervals and difference (P < 0.05) among the mean TLs occupied by the mean absorbance change per minute (ΔA/min) was the three species of littorinids (Table 2). Tukey’s multiple

554 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Fig. 1. Kite diagrams showing the distributions of Littoraria spp. (LL) and Echinolittorina malaccana (EM) on a vertical rock at Tanjung Chek Jawa in (a) June/July, (b) September, and (c) December 2002. (MHWS is represented by dashed line).

Fig. 2. Kite diagrams showing the distributions of Littoraria spp. (LL), Echinolittorina malaccana (EM) and E. vidua (EV) on a sloping rock (angle of elevation of approximately 35.6°) at Tanjung Chek Jawa. (MHWS is represented by dashed line).

555 Lee & Lim: Vertical zonation and heat tolerance of Singapore littorinids

Table 1. Mean tide levels occupied by marked Littoraria spp. (Littoraria), Echinolittorina malaccana (E. malaccana) and fi led E. malaccana (fi led E. malaccana) on four consecutive days (16 – 20 Dec.2002) at Tanjung Chek Jawa, Singapore.

Mean tide level ± S.D. (m) Littoraria E. malaccana Filed E. malaccana Day 1 2.69 ± 0.20 3.11 ± 0.23 3.03 ± 0.23 Day 2 2.54 ± 0.24 3.11 ± 0.20 3.04 ± 0.23 Day 3 2.59 ± 0.25 3.14 ± 0.19 3.11 ± 0.26 Day 4 2.67 ± 0.21 3.16 ± 0.21 3.09 ± 0.21

Table 2. Results of one way ANOVA and Tukey’s multiple comparison for tide levels that were occupied by marked Littoraria spp. (Littoraria), Echinolittorina malaccana (E. malaccana) and fi led E. malaccana (fi led E. malaccana) on four consecutive days (16 – 20 December 2002) at Tanjung Chek Jawa, Singapore. (*: signifi cant).

ANOVA Tukey’s test

F df1, df2 P

Day 1 29.99 2, 87 0.00 * Littoraria < fi led E. malaccana ≈ E. malaccana Day 2 54.23 2, 87 0.00 * Littoraria < fi led E. malaccana ≈ E. malaccana Day 3 52.41 2, 87 0.00 * Littoraria < fi led E. malaccana ≈ E. malaccana Day 4 33.84 2, 87 0.00 * Littoraria < fi led E. malaccana ≈ E. malaccana comparison tests showed that there was no significant 50.4°C (Fig. 3). Echinolittorina vidua had an intermediate difference between the TLs occupied by fi led E. malaccana 1 h LT50 of approximately 48.1°C (Fig. 3). and E. malaccana on the four days (P > 0.05) (Table 2). Both E. malaccana and fi led E. malaccana were found at a signifi cantly higher TL (P < 0.05) than Littoraria (i.e., Heat stability of GOT Littoraria < fi led E. malaccana ≈ E. malaccana) (Table 2). Incubation of GOT at 45°C resulted in increased GOT activity for all three species of littorinids with greatest increase in GOT activity seen in E. malaccana (236.48 ± Effect of shell nodulation of EM on heat refl ection 6.11%, Table 4). The maximum GOT activity for E. vidua occurred after incubation at 50°C while those of Littoraria

Results from t-tests showed that TDLittoraria and TDE. malaccana and E. malaccana were at 55°C (Fig. 4). ANOVA results recorded at Tanjung Chek Jawa were both signifi cantly showed that after incubation at 50°C, the mean percentage greater than 0°C (t = 3.36 and t = 7.61 respectively, P < GOT activity remaining for E. malaccana was signifi cantly 0.05 for both). The mean TD between rock surface and shell greater than that of E. vidua but not signifi cantly different surface for E. malaccana and Littoraria were 0.55 ± 0.54°C from that of Littoraria (P < 0.05, E. vidua < Littoraria < and 0.15 ± 0.34°C respectively. TDE. malaccana was signifi cantly E. malaccana). After incubation at 55°C, mean percentage greater than TDLittoraria (W = 3942.5, P < 0.05). GOT activity remaining for E. malaccana was signifi cantly greater than those from E. vidua and Littoraria, and that of The ANOVA results of the laboratory heat experiment Littoraria signifi cantly greater than that of E. vidua (P < showed that mean TD varied significantly with the 0.05, E. vidua < Littoraria < E. malaccana). treatment group of littorinids in question (Table 3, P < 0.05). Tukey’s multiple comparison test showed that there was no signifi cant difference between TDLittoraria and TDfi led DISCUSSION

E. malaccana but TDE. malaccana was signifi cantly greater than both

TDLittoraria and TDfi led E. malaccana (TDLittoraria ≈ TDfi led E. malaccana < During all three sampling periods, Littoraria (i.e., L.

TDE. malaccana) (Table 3). articulata and L. strigata) was generally found below the MHWS level of 2.7 m. In consultation with the Singapore Tide Tables and Port Information (Hydrographic Lethal temperature study Department, 2001), it was estimated that the MHWS level could be left dry for at least eight days during a two-week

Littoraria recorded the lowest 1h LT50 of approximately tidal cycle before the next high tide wetted the region. 47.5°C, and E. malaccana, the highest, at approximately Littoraria individuals may not be able to cope with the physical stresses beyond the MHWS level during the

556 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 3. Results of one-way ANOVA and Tukey’s multiple comparison of the variable, temperature difference (TD) between rock surface and shell surface of Littoraria spp. (Littoraria), Echinolittorina malaccana (E. malaccana) and fi led E. malaccana in the laboratory. (*: signifi cant).

ANOVA Variable Mean ± S.D. (°C) Tukey’s test F df1, df2 P

TDLittoraria 0.128 ± 0.177

TDE. malaccana 0.300 ± 0.204 5.85 2, 72 0.004 * TDLittoraria≈ TDfi led E. malaccana < TDE. malaccana

TDfi led E. malaccana 0.163 ± 0.174 aerial exposure. At the sloping rock, E. vidua was found Littorina granularis) and Littoraria (as L. undulata), Lam to occupy a region distinctly below that of E. malaccana (1980) found that E. malaccana was most tolerant to and it overlapped with the upper region in which Littoraria desiccation at 38 ± 1ºC, a trait that partly accounts for its were found. successful survival above the MHWS level.

Echinolittorina malaccana was generally found above The distributions of Littoraria and E. malaccana were and at the MHWS level. Lam (1980) also reported that E. generally distinct from each other, with the former found malaccana (as Tectarius malaccensis) inhabited the splash at a lower level than the latter. This zonation observed zone above MHWS on a man-made breakwater. A similar at Tanjung Chek Jawa was verifi ed by the translocation distribution pattern was observed by Ohgaki (1988b) study, whereby displaced individuals of Littoraria and E. for another rough periwinkle, Nodilittorina exigua, in malaccana returned to their preferred regions on the shore. Shirahama, Japan. Ohgaki (1988b) suggested that N. exigua Such movements were also observed in Austrolittorina remained above and around the MHWS level to escape unifasciata (as L. unifasciata) and Nodilittorina pyramidalis harsh conditions (e.g., strong wave action) that exist lower in New South Wales, Australia by Chapman (1999). In down the shore. In addition, these nodulated littorinids addition, physical removal of shell nodules in E. malaccana are adapted for survival under prolonged aerial exposure. did not result in a change of preference for a tide level, i.e., Among E. malaccana (as T. malaccensis), E. vidua (as the fi led E. malaccana did not move to a level signifi cantly lower or higher than that of their unfiled counterparts. However, results from the laboratory experiment showed that fi led Echinolittorina shells and smooth Littoraria shells were both warmer than nodulated shells, as evidenced by

the mean TDE. malaccana being signifi cantly greater than both

TDfi led E. malaccana and TDLittoraria. This suggests that although shell ornamentation helps to reduce shell temperature, it is probably not a major factor in determining the choice of tidal level at which the species remained.

Rough, nodulated shells reflect more heat energy (Nybakken, 2001). The higher TD of the rough periwinkle, E. malaccana, observed in this study may be due to this reason, as the infrared thermometer senses refl ected heat energy (refer to Raynger® STTM manual). The signifi cant

difference between TDLittoraria and TDE. malaccana at Tanjung Chek Jawa suggested that the nodulation on E. malaccana helped in reducing the amount of heat transmitted into the body of the littorinid. This is because the more heat energy is refl ected, less is absorbed and transmitted (Jones, 2000). Another factor that may account for the difference in TDs is colour, which affects absorption and refl ection of heat. According to Vermeij (1973), a light-coloured surface absorbs less radiation from visible light. Many high shore gastropods (e.g., Nerita peleronta, Tectarius muricatus and Littorina unifasciata antipodium) are light coloured while gastropods at lower shores have darker shells (Nyabakken, 2001; Vermeij, 1973). The nodules on E. malaccana are of a much lighter colour (pale yellow) than the rest of the Fig. 3. Probit response curves of Littoraria sp. (●), Echinolittorina vidua shell (dark brown). This colouration may further enhance

(●) and E. malaccana (■), from which the 1h LT50 values are obtained.

557 Lee & Lim: Vertical zonation and heat tolerance of Singapore littorinids

Table 4. Mean percentage glutamate oxaloacetate transaminase (GOT) activity remaining for Littoraria sp. (Littoraria), Echinolittorina vidua and E. malaccana after incubation at 45°C, 50°C and 55°C.

Mean percentage GOT activity ± S.D. (%) Species 25°C 45°C 50°C 55°C Littoraria 100.00 ± 0.00 176.32 ± 69.78 112.27 ± 56.57 67.87 ± 7.95 E. vidua 100.00 ± 0.00 191.99 ± 10.39 98.41 ± 9.39 47.27 ± 8.73 E. malaccana 100.00 ± 0.00 236.48 ± 6.11 101.94 ± 22.97 97.59 ± 33.69 heat refl ection by the nodules. Filed shells were much darker an almost terrestrial life above and about MHWS such that in colour than intact conspecifi cs. McQuaid and Schermann it is unable to cope with prolonged immersion. Interspecifi c (1988) reported that the pale-shelled L. a. africana had competition between Littoraria and E. malaccana could a lower body temperature than the dark brown morph L. also infl uence the zonation pattern. However, more studies a. knysnaensis. They also found that there was a higher would have to be conducted to elucidate the interaction mortality rate among individuals of the two sub-species that between the two genera at the study site. were painted black.

The 1h LT50s of the three taxa of littorinids in this study The preference for a higher or lower shore level may increased with their relative position on the shore. Littoraria likely be due to physiological adaptations. McMahon found lowest on the shore had the lowest 1h LT50 of (2001) hypothesized that mid-shore gastropods had 47.5°C while the inhabitant of the highest level on the modified respiratory systems for aerial and aquatic gas shore, E. malaccana, had the highest 1h LT50 of 50.4°C. exchange, which disabled them from surviving in aquatic The 1h LT50 of E. vidua (48.1°C) reflected its position environments. Likewise, E. malaccana may have adapted to on the shore relative to E. malaccana and Littoraria, i.e., between the two genera. The increase in thermal tolerance with increase in position on the shore is consistent with fi ndings of other researchers. Southward (1958) found that the high-shore top-shells Monodonta lineata and Gibbula umbilicalis tolerated higher temperatures that G. cineraria and Callipstoma zizyphinum, which inhabited low water. Fraenkel (1966) observed that N. pyramidalis at the upper part of the intertidal zone was most heat resistant, while Chlorostoma argyrostoma lischkei collected from the water’s edge was least resistant. In addition, Wolcott (1973) reported that two littoral fringe limpets (Acmaea digitalis and A. scabra) maintained higher tissue temperatures that two other species (A. pelta and A. testudinalis scutum) present in the eulittoral zone.

The 1h LT50 value for N. pyramidalis in Japan was determined by Fraenkel (1966) to be 48.5°C, which was

lower than the 1h LT50 of 50.4°C obtained in this study. His samples were heated in air instead of seawater, which may have resulted in some degree of desiccation (see Evans, 1948) thus affecting the thermal tolerance of the littorinid. Wolcott (1973) reported that removal of body water by desiccation reduced the thermal tolerance of the limpet A. digitalis by about 3°C.

In addition, the different 1h LT50 may be due to the geographical location in which the species inhabits. Thermal tolerance is reportedly negatively correlated to latitude (Fraenkel, 1968; McMahon, 2001). This may be a result of the higher level of solar radiation all year round in the tropics when compared with that of temperate areas Fig. 4. Mean glutamate oxaloacetate transaminase (GOT) activities (µmol (Moore, 1972). Southward (1958) reported that Littorina NADH/min/g wet weight) of Littoraria sp., Echinolittorina malaccana and neritoides found in North Africa was more heat tolerant than E. vidua from Tanjung Chek Jawa at four temperatures: 25 °C, 45 °C, L. saxatilis found all around Britain. Of the 60 gastropods 50 °C and 55 °C. (Vertical bars represent standard errors). Littoraria sp. collected from various localities (e.g., Australia, England, ●––––●; Echinolittorina malaccana, ●...... ●; E. vidua ■------■.

558 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Hong Kong, Jamaica, Texas), McMahon (2001) found that Chapman, M. G., 1999. Assessment of variability in responses Nodilittorina ziczac from Jamaica (18°N) had the highest of intertidal periwinkles to experimental transplantations. mean heat coma temperature (HCT) of 46.9°C. Littorina Journal of Experimental Marine Biology and Ecology, 236: mariae found in Robin Hoods Bay, England (54°N) had 171–190. the lowest mean HCT of 26.4°C. Similarly, N. pyramidalis Cleland, J. D. & R. F. McMahon, 1989. Upper thermal limit of nine at Wakayama, Japan (34°N) had a slightly lower thermal intertidal gastropod species from a Hong Kong rocky shore in tolerance than E. malaccana found Tanjung Chek Jawa, relation to vertical distribution and desiccation associated with Proceedings of the Second International Singapore (approx. 1°N). Tropical E. malaccana possibly evaporative cooling. Marine Biological Workshop: The Marine Flora and Fauna adapted to higher temperatures near the equator. This of Hong Kong and Southern China, Hong Kong. Hong Kong species is found on rocks that may be heated to temperatures University Press, Hong Kong, pp. 1141–1152. of 45°C to 50°C (Lim & Fahmy, 2008). McMahon (2001) Cooper, A. J. L. & A. Meister, 1985. Metabolic significance reported a HCT of 46.3°C for E. malaccana in Hong Kong of transamination. In: Christen, P. & D. E. Metzler (eds.), (22°N) (c.f. 1h LT50 50.4°C recorded in this study). This Transaminases. Wiley, New York. Pp. 533–563. is further evidence for the resilience of this species under Crowe, T. P. & A. J. Underwood, 1999. Differences in dispersal high temperatures. of an intertidal gastropod in two habitats: the need for and design of repeated experimental transplantation. Journal of Enzyme stability, such as that observed for GOT in E. Experimental Marine Biology and Ecology, 237: 31–60. malaccana, may account for the relatively high heat Evans, R. G., 1948. The lethal temperatures of some common tolerance of this littorinid in the current study. Glutamate British littoral molluscs. Journal of Animal Ecology, 17: oxaloacetate transaminase is required for the regulation of 165–173. carbon and nitrogen fl ow in various biochemical pathways Fraenkel, G., 1966. The heat resistance of intertidal snails at (Cooper & Meister, 1985). An enzyme’s function is highly Shirahama, Wakayama-ken, Japan. Publications of the Seto dependent on its structure. The stability of this structure is Marine Biological Laboratory, 14: 185–195. temperature-sensitive (Somero, 1978), denaturing at high Fraenkel, G., 1968. The heat resistance of intertidal snails at temperatures. Among Littoraria sp., E. malaccana and Bimini, Bahamas; Ocean Springs, Mississipi; and Woods E. vidua, the percentage of GOT activity remaining after Hole, Massachusetts. Physiological Zoology, 41: 1–13. incubation at 55 °C was highest for E. malaccana. This Gould, A. A., 1859. Descriptions of new species of shells brought indicated that GOT from E. malaccana was most stable, home by the North Pacifi c Exploring Expedition. Proceedings even at a temperature above its 1h LT50 (50.4°C). Somero of the Boston Society of Natural History, 7: 138–142. (1978) reported that enzymes denature at temperatures that Hydrographic Department, 2001. Singapore Tide Tables and Port are usually higher than the upper lethal temperature of the Information. 2002. Hydrographic Department, Maritime and species. After incubation at this temperature, the activity Port Authority of Singapore. 239 pp. of GOT from Littoraria and E. vidua fell sharply, a likely Hull, S. L., J. Grahame & P. J. Mill, 1999. Heat stability result of denaturation of the enzymes. Hull et al. (1999) and activity levels of aspartate aminotransferase and also found that enzymes of high shore animals (e.g., high alanine aminotransferase in British Littorinidae. Journal of shore L. saxatilis and L. arcana) were more stable, i.e., had Experimental Marine Biology and Ecology, 237: 255–270. higher activity rates at 56°C, than those of low shore groups Jones, H.R.N. 2000. Radiation heat transfer. Oxford University (e.g., L. obtusata, L. neglecta and L. littorea). This trend of Press, New York. 83 pp. increased stability with increased height on the shore was Lam, Y. K., 1980. Some studies on the East Coast breakwater also evident within a single species, L. saxatilis, found at fauna, with particular reference to the vertical distribution high and mid-shore levels. of the periwinkles (Littorinidae) and their tolerances to oil pollution. Unpublished Honours thesis, University of Singapore, Singapore. Pp 97 + 9 appendices. ACKNOWLEDGEMENTS Lim, S. S. L., 2008. Body posturing in Nodilittorina pyramidalis and Austrolittorina unifasciata (Mollusca: Gastropoda: The authors thank the Nature Conservation Branch Littorinidae): a behavioural response to reduce heat stress. (National Parks Board) for the permit to conduct research In: Davie, P. J. F. & J. A. Phillips (eds.), Proceedings of and to collect specimens at Pulau Ubin Nature Park. The the Thirteenth International Marine Biological Workshop, staff of the National Parks Board Offi ce at Pulau Ubin is The Marine Fauna and Flora of Moreton Bay, Queensland. acknowledged for their assistance in fi eld logistics. Financial Memoirs of the Queensland Museum – Nature, 54: 339–347. support for this study was provided by a grant (RP 19/97 Lim, S. S. L. & M. Fahmy, 2008. Is ‘standing’ posture an effective LSL) from the National Institute of Education, Nanyang behavioural adaptation to reduce heat stress in Echinolittorina Technological University to the second author (SSLL). malaccana? Abstracts of the IX International Symposium on Littorinid Biology and Evolution, University of Vigo, Spain, p. 17. LITERATURE CITED McMahon, R. F., 1990. Thermal tolerance, evaporative water loss, air-water oxygen consumption and zonation of intertidal prosobranchs: a new synthesis. Hydrobiologia, 193: 241– Bingham, F. O., 1972. The mucus holdfast of Littorina irrorata 260. and its relationship to relative humidity and salinity. The Veliger, 15: 48–50.

559 Lee & Lim: Vertical zonation and heat tolerance of Singapore littorinids

McMahon, R. F., 2001. Acute thermal tolerance in intertidal Philippi, R. A., 1847. Abbildungen und Beschreibungen neuer gastropods relative to latitude, superfamily, zonation and oder wenig gekannter Conchylien. Vols 2, 3. Theodor Fischel, habitat with special emphasis on the Littorinoidea. Journal of Cassel; Vol. 3: 1–50. Shellfi sh Research, 20: 459–467. Raffaelli, D. & S. Hawkins, 1996. Intertidal Ecology. Chapman & McMahon, R. F. & W. D. Russell-Hunter, 1977. Temperature Hall, New York. 356 pp. relations of aerial and aquatic respiration in six littoral snails Reid, D. G., 1986. The littorinid molluscs of mangrove forests in in relation to their vertical zonation. Biological Bulletin, 152: the Indo-Pacifi c region: the genus Littoraria. British Museum 182–198. (National History), London. Pp. 227 + xv. McQuaid, C. D., & P.A. Schermann, 1988. Thermal stress in a high Reid, D. G., 2007. The genus Echinolittorina Habe, 1956 shore intertidal environment: morphological and behavioural (Gastropoda: Littorinidae) in the Indo-West Pacifi c Ocean. adaptations of the gastropod Littorina africana. In: Chelazzi, Zootaxa, 1420: 1–161. G. & M. Vannini (eds.), Behavioural Adaptation to Intertidal Life. Plenum Press, New York. Pp. 213–224. Somero, G. N., 1978. Temperature adaptation of enzymes: biological optimization through structure-function compromises. Annual MINITAB, INC., 1998. MINITAB User’s Guide 2: Data analysis Review of Ecology and Systematics, 9: 1–29. and quality tools. Release 12 for Windows. State College, PA, USA. 22 Chapters [paginated by chapters]. Southward, A. J., 1958. Note on the temperature tolerances on some intertidal animals in relation to environmental Moore, H. B., 1972. Aspects of stress in the tropical marine temperatures and geographical distribution. Journal of the environment. Advances in Marine Biology, 10: 217–269. Marine Biological Association of the United Kingdom, 37: Newell, R. C., 1979. Biology of intertidal animals. Marine 49–66. Ecological Surveys Ltd., U.K. Pp. 781 + ix. Tan, K. S., 1988. The distribution of littorinids and movement Nybakken, J.W., 2001. Marine biology: an ecological approach. tracking of Nerita lineata in an intertidal drain. Unpublished Benjamin Cummings, San Francisco. 516 pp. Honours thesis, National University of Singapore, Singapore. Ohgaki, S., 1988a. Rain and the distribution of Nodilittorina exigua Pp 68 + iii. (Dunker) (Gastropoda: Littorinidae). Journal of Experimental Vermeij, G. J., 1973. Morphological patterns in high-intertidal Marine Biology and Ecology, 122: 213–223. gastropods: adaptive strategies and their limitations. Marine Ohgaki, S., 1988b. Vertical migration and spawning in Nodilittorina Biology, 20: 319–346. exigua (Gastropoda: Littorinidae). Journal of Ethology, 6: Wolcott, T. G., 1973. Physiological ecology and intertidal zonation 33–38. in limpets (Acmaea): a critical look at “limiting factors”. Petraitis, P. S., 1982. Occurrence of random and directional Biological Bulletin, 145: 389–422. movements in the periwinkle, Littorina littorea (L.). Journal of Experimental Marine Biology and Ecology, 59: 207–217. Philippi, R. A., 1846. Descriptions of a new species of Trochus, and of eighteen new species of Littorina, in the collection of H. Cuming, Esq. Proceedings of the Zoological Society of London, 1845: 138–143.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 561–568 Date of Publication: 31 Aug.2009 © National University of Singapore

SPACE USE AND HABITAT SELECTION OF HOUSE CROWS IN A TROPICAL URBAN ENVIRONMENT: A RADIO-TRACKING STUDY

Haw Chuan Lim Department of Biological Sciences, National University of Singapore, 14, Science Dr. 4, Republic of Singapore 117543 Current address: Department of Biological Sciences and Museum of Natural Science, Louisiana State University, Baton Rouge, 70803, USA. Email: [email protected] (Corresponding author)

Navjot S. Sodhi Department of Biological Sciences, National University of Singapore, 14, Science Dr. 4, Republic of Singapore 117543 Email: [email protected]

ABSTRACT. – The house crow (Corvus splendens) is an invasive bird in many parts of Asia. A radio- tracking study was conducted on 13 randomly selected birds caught throughout the port city of Singapore. We found that house crows returned faithfully to specifi c daytime areas and roost sites. Home range (95% fi xed kernel utilization distribution [UD]) size ranged from 1.3 to 158.1 ha while core area (50% UD) size ranged from 0.2 to 22.3 ha. Crows that have formed pair bonds remained in their core areas for longer each day, and possessed smaller home ranges and core areas compared to other birds. In the middle part of the day, house crows remained in their core areas where the bulk of feeding occurred. In addition, they used supplementary feeding sites, which coincided with afternoon gathering points. House crows in Singapore travelled only short distances (maximum = 3.5 km) to their roost sites, unlike house crows studied elsewhere. Habitat selection analyses carried out at two spatial scales showed that house crows preferred commercial and public housing land uses, corroborating results from a count-based study. This was probably due to the higher amount of anthropogenic food found in these places. By understanding the crows’ movement patterns and habitat preferences, management practices can be more focused and successful.

KEY WORDS. – Anthropogenic food, invasive species, wildlife management, radio-telemetry, urban ecology.

INTRODUCTION birds/ha (Lim et al., 2003). This high density, combined with its raucous nature and a tendency to form large, noisy The house crow (Corvus splendens), though originally and polluting colonial roosts near residential areas, led to from a geographic region stretching from southern Iran to the desire to control the population in Singapore (Hails, Thailand, has successfully spread to many towns and cities 1985). To develop effective management strategies for the surrounding the Indian Ocean (Meininger et al., 1980; Long, species, several studies have been carried out in Singapore 1981). It is a highly gregarious species that has survived to shed light on the following aspects of their ecology: alongside humans by scavenging and generally relying on roosting behavior and roost site selection (Peh, 2002; Peh a versatile diet (Madge & Burn, 1994). Its invasions have & Sodhi, 2002), nest site selection (Soh et al., 2002), and attracted attention of wildlife managers because of the their habitat-abundance relationship (Lim et al., 2003). bird’s well documented negative impact on native wildlife, Knowledge gleaned from these studies formed the basis of agricultural crops, and—by harboring of pathogens that an eradication program that aimed to cut crow population cause enteric disorders—even human health (Jennings, in Singapore by about 90% (Brook et al., 2003). 1992; Ryall, 1992; Archer, 2001). The purpose of this paper is to report on a further study of House crows probably invaded Singapore during the house crows in Singapore, specifi cally their use of space 1940s as stowaways on ships (Gibson-Hill, 1952). Having and habitats. Whether the crows are faithful to particular established a population of 200–400 in a port area by daytime areas and nocturnal roost sites is unknown, as 1968 (Ward, 1968), they experienced explosive growth is whether the crows use one area during the course of a in 1980s and 1990s, with population size reaching about day, or are there multiple sites of concentrated activity. 132,000 in 2000 and local densities as high as about 9 In particular, the aims of this study are to: (1) document

561 Radio-tracking study of house crows home range and diurnal movement patterns; (2) study food congregated in communal roosts. Up to three crows were selection, and evaluate if use of sites coincide with feeding tracked simultaneously. activities; and (3) test if the use of habitat types occurs in proportion to availability. Finally, we recommended We located birds on foot using a receiver (LA12-Q, AVM management strategies for effective and effi cient control of Instruments, Colfax, California) with a hand-held four- house crows based on our fi ndings. element Yagi antenna. When a signal could not be detected, we attempted to fi nd the bird by driving in a vehicle with a roof-mounted omni-directional antenna. Three levels of MATERIAL AND METHODS accuracy could be ascribed to the radio-locations obtained with the Yagi antenna: direct sighting and identifi cation of Study Area. – Singapore (1o20'N 103o50'E), is a densely bird (type I, most accurate); triangulation within a short populated tropical island-state with more than four million (approximately ≤ 30 m) distance (type II, sometimes a people in an area of about 700 km2 (Singapore Department group of crows was sighted but the radio-tracked bird was of Statistics, 2007). Most of the original vegetation (mainly not identifi ed); triangulation from more than 30 m away lowland tropical rainforest) has been lost to development, (type III). For triangulation from more than 30 m, two and only about 1,700 ha remains (Corlett, 1992). Farmland bearings were taken no more than 10 min apart to minimize covers a small proportion of the total land area (746 ha; the chance of bird movement. Because the antenna was Agri-Food and Veterinary Authority of Singapore 2007). As field tested before actual tracking, error polygon sizes much as 50% of the land is considered built-up, but is often could be calculated. The error polygon size of type II interspersed with an assortment of managed green spaces, radio-locations are not given because they are generally urban parks and wayside vegetation (Corlett, 1992). very small. We retained most type III locations because it is more problematic to introduce systematic errors by Trapping and radio-tracking. – To capture house crows, we routinely censoring some locations (e.g. those from the more divided the main island of Singapore into 2 km2 grid cells inaccessible parts of the home ranges) than to introduce and visited them at random. At each site, we attempted to imprecision by including radio-locations with larger error capture crows for up to four days. We caught most crows polygons (Nams, 1989). We plotted all radio-locations and by sedation with buttered bread cubes (1 cm3) laced with bearing locations on 1:7500 maps before transferring them 0.02g of 10% alpha-chloralose (Stouffer & Caccamise, to the computer. 1991a). Each crow was held in captivity overnight and then fi tted with a 4.9g radio-transmitter (Advanced Telemetry When the behavior of a radio-tracked crow could be Systems, Isanti, Minnesota) the next day. The transmitter observed (type I locations) or inferred (type II locations), we was attached to one of the two central rectrices with its noted whether the bird was foraging (consuming, handling, antenna extending beyond the feather. The weight of a or acquiring food), and the type of food being consumed. transmitter was less than 2% of the average mass (± SE) of Other activities of the crows were not recorded because the the crows trapped (251.5 ± 6.4g). Each radio-tracked crow resources involved might not have been limiting (e.g. perch was also fi tted with colored plastic leg bands. We assigned sites) or were tied to certain habitat types. crows to the following age categories based on the methods of Davison (1979): juvenile (< 6 months), immature (6–18 Home range, habitat selection and foraging. – We months) and adult (> 18 months). Sexing of birds was not used the fixed kernel method to estimate home ranges carried out because sexes were not distinguishable based (Worton, 1989). Calculations were carried out using on plumage. Animal Movement (Hooge & Eichenlaub, 2000), a program extension of ArcView software (ESRI, Redlands, Each crow was radio-tracked for 4–5 days per week until the California). The least-square cross validation method was transmitter failed or when home range size did not increase used to fi nd the optimal smoothing parameter (Silverman, substantially with increasing number of radio-locations. 1986). Home range and core area of a bird were defi ned We attempted to obtain three radio-locations separated by as the 95% and 50% utilization distributions (UDs), at least 30 min each day a bird was followed. The radio- respectively. Error polygons were plotted in the GIS locations of a crow collected within the same day were environment using the program LOAS (Ecological Software autocorrelated (Swihart & Slade, 1985). However, we felt Solutions, Sacromento, California). that this was not important because in the subsequent habitat selection analyses, we used the animals’ home ranges and For analysis of habitat selection, we compared available and not individual radio-locations as the sampling units (Otis & used habitats at two spatial scales: study area (i.e. Singapore White, 1999). Further, use of completely independent radio- main island) versus home range (landscape level), and home locations is also not necessary when estimating home ranges range versus core area (home range level). These levels of using the kernel method adopted here (Swihart & Slade, selection corresponded to Johnson’s (1980) second-order 1997). To ensure unbiased sampling of the daylight period selection (i.e. of home ranges) and third-order selection (of (approximately 06:30–19:30 hr, inclusive of twilight), habitat components within home ranges), respectively. At we separated time into one-hour blocks and attempted to the landscape level, availability of habitats was estimated obtain similar number of radio-locations within each time by placing 30 randomly-placed circular plots in Singapore block. House crows were not active in the evening as they (radius = 250 m, see Lim et al., 2003 for more details).

562 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 1. Description of land use categories. Each type includes land uses that are auxiliary to the main use (e.g. parking lots as part of PUBLIC).

Land use type Code Descriptions Public housing PUBLIC Public high-rise apartments, includes apartments with commercial outlets on ground fl oor; high-rise dormitories Private apartment PRIV Private high-rise apartments; condominiums House HOUSE Low-rise (< 3 surface storey) residential buildings Commercial COM Buildings used for commercial purposes; retail centers; shopping areas Industrial INDUS Light, general or heavy industries; warehouses; ports Urban green UGREEN Managed green open spaces (treed or turfed); urban parks; wayside vegetation Institution, INSTIT Schools; built-up sports facilities; civic and community buildings; army camps; offi ce community facility buildings and offi ce Natural/semi-natural NAT Unmanaged vegetation; nature parks; unused ground left to regenerate environment Agricultural AGRI Vegetable and animal farms

Used habitats were those found within the home ranges RESULTS (area bounded by 95% UDs). At the home range level of selection, used habitats were those within the core areas Home range, movements and food selection. – We tracked (50% UDs), whereas available habitats were those within 13 crows (N = 8 adults, 3 immatures, and 2 juveniles) for the home ranges. We studied habitat selection using UDs an average of 21.2 ± 0.9 days, and obtained an average of because this approach treated individual animals as the 35.6 ± 3.0 radio-locations per bird (Table 2). The proportion sampling units and defi ned use probabilistically based on of radio-locations per bird derived through direct sightings overall movement patterns (Millspaugh et al., 2006). (type I radio-locations) ranged from 19.2–75.0% (mean = 45.2 ± 5.2%). The average size of 95% error polygons from Nine habitat types were defi ned based on anthropogenic land uses (Table 1). Other defi nitions of habitat types (e.g. natural habitats based on vegetation type) were not employed because house crows in Singapore occur mainly in areas infl uenced heavily by humans. At the landscape level, we compared the proportion of land use types in the circular plots and home ranges using Mann-Whitney U-tests, one category at a time, to determine if house crows preferred certain land use types when it comes to selecting their home ranges. Compositional analysis (Aebischer et al., 1993) was used to analyze habitat selection at the home range level because it overcomes the problem of non-independence of habitat proportions via log-ratio transformation (Aitchison, 1986). We calculated all possible pairwise differences in log-ratios between used and available habitats (i.e. ln[xui/xai]

- ln [xuj/xaj], where xu is an individual’s proportional habitat use, xa is an individual’s proportional habitat availability, i = 1, 2…, p and i ≠ j given p habitat types; Aebischer et al., 1993), and then averaged the matrices across all individuals. Signifi cant departure of means from zero were tested using t-tests (mean/standard error), and a positive value signifi ed that row land use type was preferred over the corresponding column land use type (see Results). To rank habitat types in order of preference, the number of positive values across a row was summed. Habitat types with more positive values were more preferred. All following values are presented as mean ± SE.

Fig. 1. Average number of radio-locations per bird (a) outside or (b) inside core areas within each 2-hr time block. Number of House Crows = 13. Labels on x-axis indicate midpoint of each time block. Error bars denote standard errors.

563 Radio-tracking study of house crows

Table 2. Size of home ranges and core areas (defi ned by the fi xed kernel method) and other information on 13 House Crows radio-tracked between 13 May 2000 and 8 Feb.2002.

Approx. distance from 2 Bird Age1 No. of No. of Home range Core area MCP (ha) roost(s) to core area(s) days tracked radio-locations (ha) (ha) (ha) (km) 51 I 17 21 82.3 15.7 37.9 0.90 62 A (P) 16 23 1.3 0.2 1.2 1.67 130 A 24 46 44.6 9.0 92.5 1.78 157 A 44 60 19.4 2.3 34.3 3.50 166 I 18 20 32.3 3.6 28.7 1.53 182 A (P) 23 33 9.4 3.1 15.0 1.17 183 A (P) 23 43 2.4 0.5 14.7 0.87 271 J 23 40 9.8 2.0 6.4 2.32 293 A 26 37 62.2 7.8 175.3 2.86 389 A 22 34 130.5 22.3 425.4 3.42 424 I 25 35 84.8 11.8 178.6 1.01 565 A 25 36 158.1 14.5 212.4 1.27 630 J 18 35 9.5 0.9 8.9 0.51

1 A = adult, I = immature, J = juvenile and P = pair-bonded 2 MCP = minimum convex polygon type III radio-locations was 5.0 ± 1.2 ha (N = 40). Three occurred in the core areas, with another peak during late adults formed pair bonds (displayed affi liative behavior; afternoons (Fig. 2). Although 73% of feeding occurred Brown & Veltman, 1987), but did not nest (lay eggs, within core areas, χ2 tests indicated that this proportion was incubate or brood). not signifi cant (P = 0.36, d.f. = 1) because more type I and II locations also fell in core areas (67%). However, we felt Home range sizes ranged from 1.3 ha to 158.1 ha. Paired that this lack of statistical signifi cance was an artifact of adults had smaller home ranges (mean = 4.4 ± 2.5 ha) how the crows were radio-tracked. They generally moved and core areas (mean = 1.3 ± 0.9 ha) than the other crows faster during the early morning and late afternoon (moving (mean home range size = 63.4 ± 14.6 ha; mean core area away or towards their roosts), and were consequently harder size = 9.0 ± 2.0 ha). Between paired adults and other crows, to sight. Therefore, even if the crows did not forage often differences in size of core areas and home ranges were both outside of their core areas, observations relating to this were statistically signifi cant (Mann-Whitney U-test, core area: diffi cult to collect. P = 0.049, home range: P = 0.007). The mean distance between approximate centers of core areas and roost sites Food of ‘natural’ origin (not directly derived from humans) was 1.8 ± 0.3 km (N = 13). Crows tended to remain in their accounted for 20.5% of the total observed. These food items respective core areas in the middle part of the day, but were included beach and canal bank debris, insects, and fruits on found outside the core areas during early morning and late trees. The crows used a variety of feeding techniques such afternoon (Fig. 1). Daily afternoon departures from core as gleaning off beaches, ground or other substrates, probing areas to roost sites occurred later for paired crows than for tree bark, and fl ycatching. The largest proportion of food unpaired crows. The latest a paired crow was detected at was litter or food offered deliberately to crows or other the core area was, on average, 18:36 hr (range: 18:10–19:02 hr, N = 3), whereas the latest time for unpaired birds was 16:30 hr (range: 14:04–18:45 hr, N = 10). Six of 13 crows had at least one substantially-utilized home range portion (≥ 8% of the bird’s total number of radio-locations) that was discontinuous from the core area (based on fi xed kernel defi nition of home range confi guration). Throughout our study, only two birds switched roost. One bird moved to an existing roost 1.25 km away because its original roost was subjected to shooting. Another bird switched to an alternative roost 400 m away even though the fi rst was not subjected to any apparent disturbance. Fig. 2. Average number of radio-locations per bird associated with feeding Overall, 44 radio-locations (10.4% of type I and II radio- within each 2-hr time block. Number of House Crows = 13. Labels on locations) were associated with foraging. Most feeding x-axis indicate mid point of each time block. Error bars denote standard errors.

564 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Table 3. Comparison of the proportion of land use types in 30 PUBLIC was the largest component (41.2–97.4%) in the random plots located in Singapore and those within home ranges core areas for six of the crows. Three other crows had (95% fi xed kernel utilization distribution) of 13 crows. AGRI UGREEN as the major component (53.0–90.4%). The (agricultural land uses) was excluded from the analysis because largest core area components of the other four crows were none of the home ranges contained this land use type. INDUS (95.3%), INSTIT (63.8%) and HOUSE (81.8% and Land use Random plots (%) Home ranges (%) 100.0%). For two land use types, COM and PUBLIC, use by type Mean (SE) Mean (SE) house crows increased linearly with availability at the home range level (Fig. 3). Although there are positively signifi cant PUBLIC 10.1 (3.7) 27.8 (6.9)** relationships between use and availability for some of the PRIV 4.5 (2.2) 1.3 (0.7) other land use types, those regressions were affected by high HOUSE 7.3 (2.2) 16.9 (7.3) leverage values (i.e. one or a few points having unduly large COM 1.0 (0.3) 2.8 (1.0)* infl uence on the regression; Montgomery, 1997). INDUS 8.7 (4.0) 14.2 (5.7) UGREEN 16.6 (2.9) 19.6 (5.3) DISCUSSION INSTIT 5.5 (2.0) 11.6 (3.3)** NAT 21.2 (5.2) 6.0 (2.3) Home ranges and movements. – House crows are a AGRI 6.6 (3.9) – community-territorial species, which form loose nesting colonies and benefi t from close association with each other ** Mann-Whitney U test, signifi cantly different at P = 0.05; * through the collective defence of nests and mobbing of signifi cantly different at P = 0.10 predators (Lamba, 1963; Rowley, 1973; Soh et al., 2002). Despite the difference in social organization, home range animals (e.g. Rock Pigeons Columbus livia) (55.0%). Due sizes of house crows in Singapore are comparable to those to good municipal practices, a relatively small proportion of similarly-sized Corvus species that defend territories. (8.5%) came directly from waste disposal sites or spillage. The remaining food items were of uncertain origin. The small number of feeding observations precluded detailed analyses on individual birds (e.g. relative proportions of each type of food) but the data and locations of core areas suggested that individual birds vary in their reliance on natural food.

Habitat selection. – Proportions of the two land use types differed signifi cantly within the study area and the home ranges (Mann-Whitney U-test, P = 0.05) (Table 3). Home ranges contained a signifi cantly greater proportion of PUBLIC and INSTIT. Home ranges also had larger proportions of COM compared to the study area, but this was signifi cant only at P = 0.10. Crows appeared to avoid areas with natural vegetation and private apartments, although the relationships were not statistically signifi cant (Table 3). AGRI was excluded from the analysis because none of the home ranges contained this land use type.

Multivariate analysis showed overall departure from random use when land use compositions of core areas and home ranges were compared (Wilks’ Λ = 0.3, P < 0.05 when 2 compared to χ 7). The ranking of preference (descending order) based on the number of positive mean log-ratio differences in each row is: PUBLIC > COM > INDUS > PRIVATE > UGREEN > NAT > INSTIT > HOUSE (Table 4). Some lack of congruence within this dataset was noticeable. For instance, although COM was signifi cantly preferred over INDUS (P = 0.04), the t-test did not show that PUBLIC was signifi cantly preferred to INDUS, even though PUBLIC was ranked higher than COM. Therefore, the fi nal ranking of habitat preference should be viewed as a general ranking that shows the average preference of a sample of crows. Fig. 3. The proportions of (a) commercial and (b) public housing land uses in core areas (y-axis) against proportions in home ranges (x-axis) for 13 House Crows.

565 Radio-tracking study of house crows

Table 4. Matrix of means and standard errors of differences in log-ratios calculated from use/availability (core area/home range) data of 13 House crows. A positive matrix element signifi es that the row land use type is preferred over the column land use type. Means are tested for signifi cant differences from zero using t-test (in bold, signifi cant at P = 0.05). The rank on the right is the sum of the number of positive values in the row.

PUBLIC PRIV HOUSE COM INDUS UGREEN INSTIT NAT Rank PUBLIC 2.09 ± 1.15 3.46 ± 1.39 0.97 ± 1.31 1.97 ± 1.57 2.62 ± 1.27 3.03 ± 1.08 2.78 ± 1.13 7 PRIV -2.09 ± 1.15 1.37 ± 1.12 -1.99 ± 1.47 -0.12 ± 1.76 0.69 ± 1.38 0.95 ± 1.22 0.69 ± 1.38 4 HOUSE -3.46 ± 1.39 -1.37 ± 1.12 -3.37 ± 1.61 -1.49 ± 1.81 -0.84 ± 1.32 -0.43 ± 1.48 -0.68 ± 1.00 0 COM -0.97 ± 1.31 1.99 ± 1.47 3.37 ± 1.61 1.87 ± 0.79 2.53 ± 1.80 2.94 ± 1.43 2.68 ± 1.48 6 INDUS -1.97 ± 1.57 0.12 ± 1.76 1.49 ± 1.81 -1.87 ± 0.79 0.65 ± 2.03 1.06 ± 1.79 0.81 ± 1.67 5 UGREEN -2.62 ± 1.27 -0.69 ± 1.38 0.84 ± 1.32 -2.53 ± 1.80 -0.65 ± 2.03 0.41 ± 1.49 0.16 ± 0.95 3 INSTIT -3.03 ± 1.08 -0.95 ± 1.22 0.43 ± 1.48 -2.94 ± 1.43 -1.06 ± 1.79 -0.41 ± 1.49 0.25 ± 1.57 1 NAT -2.78 ± 1.13 -0.69 ± 1.38 0.68 ± 1.00 -2.68 ± 1.48 -0.81 ± 1.67 -0.16 ± 0.95 0.25 ± 1.57 2

Minimum convex polygon home range sizes of some peak in feeding, at a time when crows have moved out of of the other Corvus species that have been studied are: their core areas. We found that such supplementary feeding American crow, with a 26–49 ha group territory (Stouffer often occurred at convergence sites which the crows visited and Caccamise 1991b); carrion crow (C. corone), 22–29 before proceeding to the vicinity of roosts for pre-roosting. ha (Nakamura 1998); Torresian crow (C. orru), 131 ha Chia (1976) also documented the presence of such late (average), and Australian Raven (C. coronoides), 109 afternoon convergence sites (termed post-feeding assembly ha (average) (Rowley, 1973). However, because house points), but he did not explicitly determine if supplementary crows only defend nests or nest trees, and not territories, feeding was carried out. The use of supplementary feeding they can achieve much higher local densities if suffi cient sites at varying distances from territories by American crows resources are available. Crowding of high quality sites has has also been documented (Stouffer & Caccamise, 1991b; also been observed in American crows, albeit to a lesser Caccamise et al., 1997). Because of the lack of seasonality in extent, where their territories of overlap in food-rich areas food abundance in Singapore, such supplementary feeding (Marzluff & Neatherlin, 2006). Paired adult house crows sites may be less important to house crows than they would possessed signifi cantly smaller activity areas in contrast to be for temperate corvid species. birds that did not form pair bonds. This suggests that they either established themselves in higher quality sites, or that We found that the birds in Singapore returned to their core they were more dominant when competing for temporarily areas faithfully, even though they roost communally. This abundant food within their home ranges. behavior has been reported for other communally roosting species as well, e.g. common grackle (Quiscalus quiscula) The crows we radio-tracked travelled short distances to roost (Caccamise et al., 1983); European starling (Sturnus (maximum = 3.5 km). Other studies on house crows reported vulgaris) (Morrison & Caccamise, 1985); common myna distances of 8.5 km in Kuala Lumpur, Malaysia (Chia, (Acridotheres tristis) and Javan myna (A. javanicus) (Kang, 1976) and 25 km in Mauritius (Feare & Mungroo, 1990). 1989). Tangentially, we note that our fi ndings of fi delity to Difference in study design may partially account for these such daytime centers, and the observation that the majority travel differences. These earlier studies had only a single roost of feeding was carried out within core areas, are inconsistent in their study areas, allowing the detection of maximum travel with the information center hypothesis of communal distances. However, we believe two other factors may also roosting behavior (Ward & Zahavi, 1973), which generally contribute to the shorter distances travelled by house crows in predicts a roost-centered distribution of foraging sites. This Singapore. First, the high density of crows in Singapore (Lim et pattern is expected because the hypothesis posits that birds al., 2003) permits a relatively small area to provide an adequate exchange information at their roost sites, resulting in naïve number of birds for communal roost formation. The smallest birds following knowledgeable roost-mates to profi table roost in Singapore detected by Peh (2002) contained about 50 feeding sites. Despite this apparent lack of support for the birds. Second, there is no shortage of suitable roost trees in hypothesis, we acknowledge that house crows in Singapore Singapore because of an intensive urban greening program (> may not represent a strong case against the information 1 million trees planted in parks and roadsides; Anonymous, center hypothesis. This is because food resources in 2003). Thus, if roosts are just passive aggregations of birds Singapore may not be temporally and spatially ephemeral (Caccamise et al., 1997), and suitable roost trees are not enough, such that crows need to follow knowledgeable limiting, we should expect roosts to be located such that they roost-mates in order to feed successfully (Sonerud et al., minimize travelling cost to daytime centers. 2001). Studies in places where food occurrence is more sporadic (e.g. coast) at the day-to-day time scale are needed Although core areas may be responsible for the bulk of to test if house crows indeed use roosts for information the food intake, our study shows an interesting secondary exchange (Tye, 1993).

566 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Habitat selection. – Our radio-tracking study agrees with a ACKNOWLEDGMENTS count-based study (Lim et al., 2003) in indicating that house crows in Singapore prefer public housing and commercial The Agri-food and Veterinary Authority of Singapore areas. Both this and the count-based study show that crows partially funded this study. We thank Simon Lim for were attracted to these land uses because of the high extensive help during field work and Tommy Tan for amount of anthropogenic food. The two studies, however, logistics support. We are grateful to Frederick Sheldon, disagree on house crows’ preference for institutional land Norman Lim and Benjamin Lee for comments on drafts uses (they were found to be negative predictors of crow of this paper. abundance in the count-based study). We believe the cause of the discrepancy lies in how home ranges were derived. Mathematically constructed home ranges, which LITERATURE CITED are partially based on spatial extrapolation from actual radio-locations, may sometimes include less preferred sites Agri-Food and Veterinary Authority of Singapore [online]. 2007. (i.e. institutes) because they intermix with or are embedded Statistics. < http://www.ava.gov.sg/Publications/Statistics/> within more preferred ones (e.g. schools adjacent to public (12 December 2007) housing). However, at the home range level of analysis, Anonymous 2003. National Parks Board Annual Report institutional use sites were strongly avoided, thus showing 2002/2003. National Parks Board, Singapore. that, overall, they are indeed not favored. Aebischer, A. E., P. A. Robertson & R. E. Kenward, 1993. Compositional analysis of habitat use from animal radio- We believe that frequently used habitats are of better quality tracking data. Ecology 74: 1313–1325. by virtue of their more abundant food resources. There is Aitchison, J., 1986. The statistical analysis of compositional data. evidence that the existence of extra food caused increased Chapman and Hall, London. 416 pp. fecundity and survival in other species of crows (Richner, Archer, A. L. 2001. Control of the Indian House Crow Corvus 1992; Marzluff & Neatherlin, 2006). Even if survival or splendens in eastern Africa. Ostrich Supplement, 15: 147– reproductive success of individual crows did not improve 152. because of increased crowdedness in preferred habitats, Brook, B. W., N. S. Sodhi, M. C. K. Soh & H. C. Lim, 2003. density, which is an important indicator of habitat quality Abundance and projected control of invasive house crows in (Van Horne, 1983), was clearly elevated in food-rich habitat Singapore. Journal of Wildlife Management, 67: 808–817. types. Direct evidence for this was found by Lim et al.’s Brown, E. D. & C. J. Veltman, 1987. Ethogram of the Australian (2003) count-based study. Moreover, we provided indirect Magpie (Gymnorhina tibicen) in comparison to other evidence here by showing that use of commercial and public Cracticidae and Corvus species. Ethology, 76: 309–333. housing areas increased linearly with their availability. If Caccamise, D. F., L. A. Lyon & J. Fischl, 1983. Seasonal patterns crows only need to extract a fi xed amount of resources in roosting fl ocks of starlings and Common Grackle. Condor, (i.e. food) from commercial or public housing areas, the 85: 474–481. use of these areas should plateau after the birds’ needs are Caccamise, D. F., L. M. Reed, J. Romanowski & P. C. Stouffer, met (Garshelis, 2000). This will not be the case if more 1997. Roosting behavior and group territoriality in American available habitat also attracts more birds, forcing individuals Crows. Auk, 114: 628–637. to increase use of commercial or public land uses in order Chia, P. K. 1976. Some aspects of the natural history of the House to maintain the same intake level. Crow Corvus splendens Vieillot in Kuala Lumpur. Honours Thesis, University of Malaya, Kuala Lumpur. 27 pp. Management implications. – This study shows that Corlett, R., 1992. The ecological transformation of Singapore management efforts (e.g. shooting, food limitation) are 1819-1990. Journal of Biogeography, 19: 411–420. most profi table when they are carried out in habitats that Davison, G. W. H., 1979. Kuala Lumpur and her crows. Malayan make up the crows’ core areas. Areas occupied by potential Naturalist, Jan 1979: 23–25. breeders or paired crows may be of particularly high quality since these birds can be sustained by rather small habitat Feare, C. J. & Y. Mungroo, 1990. The status and management Corvus splendens area. These sites can usually be identifi ed by presence of of the House Crow (Vieillot) in Mauritius. Biological Conservation, 51: 63–70. active or used nests. By reducing the attractiveness of these habitats through food limitation and access denial (e.g. Garshelis, D. L., 2000. Delusions in habitat evaluation: measuring through frequent shooting, placement of scaring devices), use, selection and importance. In: Boitani, L. & T. K. Fuller (eds.), Research techniques in animal ecology: controversies crows would be forced to use lower-quality or less familiar and consequences. Columbia University Press, New York. habitats. In contrast, management actions that focus on roost Pp. 111–164. sites are less likely to be effective because birds can change Gibson-Hill, C.A., 1952. Notes on the alien birds recorded roosts without much apparent cost; studies from elsewhere from Singapore island. Bulletin of the Raffl es Museum, 24: have shown that crows can cover much longer distances in 240–256. their daily fl ights between roosts and daytime sites. Hails, C.J., 1985. Studies of problem bird species in Singapore: II Corvidae (Crows). Report for the Commissioner for Parks and Recreation. Ministry of National Development, Singapore. 20 pp.

567 Radio-tracking study of house crows

Hooge, N. & B. Eichenlaub, 2000. Animal movement extension to Peh, K.S.-H., 2002. Roosting behaviour of House crow (Corvus ArcView. Ver. 2.0. Alaska Science Center - Biological Science splendens) in relation to environment variables. Raffles Offi ce, U.S. Geological Survey, Anchorage. Bulletin of Zoology, 50: 257–262. Jennings, M. C., 1992. The House Crow Corvus splendens in Peh, K. S.-H. & N. S. Sodhi, 2002. Characteristics of nocturnal Aden (Yemen) and an attempt at its control. Sandgrouse, 14: roosts of House Crows in Singapore. Journal of Wildlife 27–33. Management, 66: 1128–1133. Johnson, D. H., 1980. The comparison of usage and availability Richner, H., 1992. The effect of extra food on fi tness in breeding measurements for evaluating resource preference. Ecology, carrion crows. Ecology, 73: 330–335. 61: 65–71. Rowley, I., 1973. The comparative ecology of Australian corvids. Kang, N., 1989. Comparative behavioural ecology of the Mynas, II. Social organization and behaviour. CSIRO Wildlife Acridotheres tristis (Linnaeus) and A. javanicus (Cabanis), Research, 18: 25–66. in Singapore. Ph.D. dissertation, National University of Ryall, C., 1992. Predation and harassment of native bird species Singapore, Singapore. by the Indian house crow Corvus splendens, in Mombasa, Lamba, B. S., 1963. The nidifi cation of some common Indian Kenya. Scorpus, 16: 1–8. birds - Part 1. Journal of Bombay Natural History Society, Silverman, B. W., 1986. Density estimation for statistics and data 60: 121–133. analysis. Chapman and Hall, London. 175 pp. Lim, H. C., N. S. Sodhi, B. W. Brook & M. C. K. Soh. 2003. Singapore Department of Statistics, 2007. Year book of statistics. Undesirable aliens: factors determining the distribution of Ministry of Trade and Industry, Singapore. 299 pp. three invasive bird species in Singapore. Journal of Tropical Ecology, 19:685–695. Soh, M. C. K., N. S. Sodhi, R. K. H. Seoh & B. W. Brook, 2002. Nest site selection of the House Crow (Corvus splendens), an Long, J. L., 1981. Introduced birds of the world. Universe Books, urban invasive bird species in Singapore and implication for its New York. 528 pp. management. Landscape and Urban Planning, 59: 217–226. Madge, S. & H. Burn, 1994. Crows and jays: a guide to crows, Sonerud, G.A., Smedshaug, C.A. & Brathen, O., 2001 Ignorant jays and magpies of the world. Christopher Helm, London. hooded crows follow knowledgeable roost-mates to food: 191 pp. support for the information centre hypothesis. Proceedings of Marzluff, J. M. & E. Neatherlin, 2006. Corvid response to human the Royal Society of London B., 268: 82–831. settlements and campgrounds: causes, consequences, and Stouffer, P. C. & D. F. Caccamise, 1991a. Capturing American challenges for conservation. Biological Conservation, 130: Crows using alpha-chloralose. Journal of Field Ornithology, 301–314. 62: 450–453. Meininger, P. L., W. C. Mullie & B. Bruun, 1980. The spread of Stouffer, P.C. & D.F. Cacamise, 1991b. Roosting and diurnal the house crow, Corvus splendens, with special reference to movement of radio-tagged American Crows. Wilson Bulletin, the occurrence in Egypt. Le Gerfaut, 70:245–250. 103: 387–400. Millspaugh, J. J., R. M. Nielson, L. McDonald, J. M. Marzluff, Swihart, R. K. & N. A. Slade, 1985. Testing for independence of R. A. Gitzen, C. D. Rittenhouse, M. W. Hubbard & S. L. observation in animal movements. Ecology, 66: 1176–1184. Sheriff, 2006. Analysis of resource selection using utilization distributions. Journal of Wildlife Management, 70: 384–395. Swihart, R. K. & N. A. Slade, 1997. On testing for independence of animal movements. Journal of Agricultural, Biological and Montgomery, D. C., 1997. Design and analysis of experiments, 4th Environmental Statistics, 2: 1–6. edition. John Wiley and Sons, New York. 704 pp. Tye, A., 1993. “Diurnal activity centers” and “information Morrison, D. W. & D. F. Caccamise, 1985. Ephemeral roosts and centers”: a need for more critical study. Wilson Bulletin, 105: stable patches? A radio-telemetry study of communal roosting 368–372. starlings. Auk, 102: 793–804. Van Horne, B., 1983. Density as a misleading indicator of habitat Nakamura, S., 1998. The territorial behaviour of the Carrion quality. Journal of Wildlife Management, 47: 893–901. Crows Corvus corone corone in Japan. Japanese Journal of Ornithology, 46: 213–223. Ward, P., 1968. Origin of the avifauna of urban and suburban Singapore. Ibis, 110:239–255. Nams, V. O., 1989. Effects of sample size and bias when testing for habitat selection. Canadian Journal of Zoology, 67: Ward, P. & A. Zahavi, 1973. The importance of certain 1631–1636. assemblages of birds as “information centres” for food fi nding. Ibis, 115: 517–534. Otis, D. L. & G. C. White, 1999. Autocorrelation of location estimates and the analysis of radiotracking data. Journal of Worton, B. J., 1989. Kernel methods for estimating the utilization Wildlife Management, 63: 1039–1044. distribution in home-range studies. Ecology, 70: 164–168.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 569–575 Date of Publication: 31 Aug.2009 © National University of Singapore

PROJECTED CLIMATE CHANGE EFFECTS ON NUTHATCH DISTRIBUTION AND DIVERSITY ACROSS ASIA

Shaily Menon Department of Biology, Grand Valley State University, Allendale, Michigan 49401 USA. Email: [email protected] (Corresponding author)

M. Zafar-ul Islam Bombay Natural History Society, Mumbai, India. (Current Address: National Wildlife Research Center, Taif, Saudi Arabia) Email: [email protected]

A. Townsend Peterson Natural History Museum and Biodiversity Research Center, The University of Kansas, Lawrence, Kansas 66045, USA. Email: [email protected]

ABSTRACT. – We used ecological niche modeling approaches to explore climate change implications for one family of birds, the Sittidae, in Asia. Quantitative niche models based on present-day distributions for each of 13 species were projected onto future climate change scenarios. Species’ potential distributional areas tended to be predicted to retract along their southern fringes, and at lower elevations along mountain ranges. As observed in other studies, montane systems were relatively more robust to the horizontal effects of climate change on species’ distributions compared to fl atland systems, so range contractions were focused in Southeast Asia and peninsular India.

KEY WORDS. – nuthatch, distribution, diversity, climate change, niche modeling.

INTRODUCTION projections across future climate projections (Bakkenes et al., 2002; Berry et al., 2002; Erasmus et al., 2002; Current rapid changes in global climate reveal a strong Peterson et al., 2002; Pearson & Dawson, 2003; Huntley tendency toward warmer temperatures and greater variability et al., 2004; Peterson et al., 2004; Thuiller et al., 2005a; of climate events (IPCC, 2007). The biological implications Araújo et al., 2006; but see Pearson et al. 2006), but also of these changes, however, remain somewhat obscure: a growing understanding of the sensitivity, assumptions, although numerous recent publications document effects and limitations of the approach (Pearson & Dawson, 2003; already manifested (Visser et al., 1998; Parmesan et al., Hampe, 2004; Araújo et al., 2005b; Peterson et al., 2005). 1999; Parmesan & Yohe, 2003; Lovejoy & Hannah, 2005), anticipating changes already initiated but as yet not Here, we use ENM approaches to explore climate change manifested is a major challenge (Peterson et al., 2005). implications for one family of birds, the Sittidae. This study Several modeling efforts have explored such predictive builds on a previous ecological and geographic analysis challenges (e.g., Thomas et al., 2004), but consensus as (Menon et al. 2008) of the family. Nuthatch species serve to likely effects and their dimensions has not been easy as an interesting group for such studies as their distributions (Pearson & Dawson, 2003; Araújo et al., 2005b; Araújo & range from narrow endemism to broad distributions across Rahbek, 2006). continents. Specifi cally, we focus on members of the family distributed in Asia, the region that holds by far the richest Ecological niche modeling (ENM) provides a predictive nuthatch assemblage (Harrap & Quinn, 1995). We develop framework for anticipating spatial implications of global quantitative ecological niche models based on present-day climate change for biodiversity (Pearson & Dawson, 2003; distributions of each species, and then project those models Soberón & Peterson, 2005). Extensive methodological onto future, changed climates. The result is a picture of testing has produced not just consistent and robust likely spatial (geographic) effects of changing climates on

569 Menon et al.: Climate Change Effects on nuthatches

Table 1. Summary of occurrence data available to us for model development, projected current distributional areas (derived from trimmed raw ENM results), and projected proportional range loss under two scenarios of climate change for each nuthatch species occurring in Asia.

Number of Current area Percent loss Percent loss Species occurrence points (km2) under HA2 under HB2 Sitta cashmirensis 17 510,594 35.2 35.3 Sitta castanea 69 4,204,746 45.2 39.3 Sitta europaea 40 18,018,741 64.8 64.7 Sitta formosa 63 739,304 5.5 5.1 Sitta frontalis 60 3,944,852 47.7 38.9 Sitta himalayensis 27 552,488 22.2 18.1 Sitta leucopsis 23 967,920 11.5 11.7 Sitta magna 45 705,941 24.0 18.0 Sitta nagaensis 27 901,572 17.4 15.9 Sitta tephronota 34 2,822,247 15.1 18.3 Sitta villosa 10 1,116,444 80.4 79.8 Sitta yunnanensis 7 284,822 47.7 43.6 Tichodroma muraria 56 10,846,541 20.0 20.0 each species’ distributional potential. We synthesize these Field Museum of Natural History, University of Kansas results into a picture of regional change in nuthatch species Natural History Museum, and the U.S. National Museum composition and diversity. of Natural History; data were also drawn from databases developed by BirdLife International (Collar et al., 2001). Textual descriptions of occurrence localities were translated METHODS into geographic coordinates in decimal degrees via the GeoNet Names Server (National Geospatial Intelligence Input Occurrence Data. – We included all Eurasian Agency, 2007) and BioGeomancer (Chapman & Wieczorek nuthatches, specifi cally all species in the genera Sitta and eds., 2006). The fi nal dataset consisted of 7-69 occurrences Tichodroma occurring in the region. Occurrence information per species (Table 1, Figure 1; see Menon et al., 2008 for was drawn from natural history museums across North more detail). America, including the Museum of Comparative Zoology,

Fig. 1. Occurrence points for 12 Sitta species and one Tichodroma species used in this study. Sitta solangiae and S. victoriae each had fewer than 5 occurrence points and were excluded from the analysis.

570 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Environmental Data Sets. – Climate data were drawn from testing data). Distributional data are converted to binary a global summary for 1960-1990 at 0.5° resolution (New et raster layers, and by random resampling from training al., 2002). In particular, we used data layers summarizing and intrinsic test data and areas of ‘pseudoabsence’ (areas annual precipitation, mean annual temperature, maximum lacking known presences), two data sets are created, each of annual temperature, minimum annual temperature, diurnal 1250 points; these data sets are used for rule generation and temperature range, and vapor pressure. We supplemented model testing, respectively (Stockwell & Peters, 1999). these data sets with information from the U.S. Geological Survey’s Hydro-1K dataset (http://edc.usgs.gov/products/ Within GARP’s processing, the first rule is created by elevation/gtopo30/hydro/) for topography and landform applying a method chosen randomly from a set of inferential (slope, aspect, compound topographic index). We resampled tools (e.g., logistic regression, bioclimatic rules). The all data sets to 0.1° resolution for analysis to avoid genetic algorithm consists of specially defi ned operators overinterpretation of the precision of the point occurrence (e.g. crossover, mutation) that modify the initial rules, and data. thus the result is models that have “evolved”—after each modifi cation, the quality of the rule is tested (to maximize To represent future climatic conditions, we used output both signifi cance and predictive accuracy) and a size-limited from the HadCM3 general circulation model (GCM). We set of best rules is retained. Because rules are tested based assessed both a conservative (HB2) and a less-conservative on independent data (the intrinsic test data), performance (HA2) view of future atmospheric condition and consequent values refl ect expected performance of rules, an independent climate change. These climate model results are presented verifi cation that gives a more reliable estimate of true rule in terms of a 30-year average around 2055 (2040-2069), performance. so our results do not take into account the potential effects of increased climate variability (e.g., El Niño events) on Following recent best-practices recommendations (Anderson species’ distributions. Because GCM results are provided et al., 2003), for each species, we developed 100 replicate at a spatial resolution of 2.5 x 3.75° grid cells, expected random-walk GARP models, and fi ltered out 90% based changes in temperature and precipitation under each on consideration of error statistics, as follows. The ‘best scenario were extracted from the coarse raw data sets--these subsets’ methodology consists of an initial fi lter removing expected changes were applied to the New et al. (2002) models that omit (omission error = predicting absence at current climate data layers (0.5 x 0.5° grid cells), thus points of known presence) heavily based on the extrinsic achieving a reasonable spatial resolution. testing data, and a second filter based on an index of commission error (= predicting presence in areas of known Ecological Niche Modeling. – Several studies have absence), in which models predicting very large and very compared potential distributional estimates resulting from small areas are removed from consideration. Specifi cally, in different ecological niche modeling approaches, concluding GARP, we retained only the 20% of models that showed that algorithms capable of fi tting complex and non-linear lowest omission errors, and then retained only the central relationships generally provide better predictions than simpler 50% of the frequency distribution of proportional area analogues (Segurado & Araújo, 2004; Elith et al., 2006). In predicted present (an index of commission error); the result these studies, however, measures of model performance did was 10 ‘best subsets’ models (binary raster data layers) not often assess the full predictive challenge, often focusing that were summed to produce a best ensemble estimate of more on challenges of interpolation than on challenges of geographic projection. transferability (Araújo et al., 2005a). As a consequence, and in spite of years of exploration and testing, little Range Loss Scenarios. – Projections of potential guidance can be provided regarding selection of ‘best’ ENM distributional areas for present and future climate scenarios algorithms for applications related to transferability (Lobo were summarized as follows. First, we decided on particular et al., 2007; Peterson et al., 2007). predictive thresholds (= suitability scores) above which model predictions would indicate suitable conditions, and Here, we used the Genetic Algorithm for Rule-Set below which model predictions would indicate unsuitable Projection (GARP; Stockwell & Peters, 1999), a method conditions—we used the lowest training presence threshold that has been used successfully in studies involving (= lowest suitability score assigned to any of the occurrence transferability—training niche models on one landscape for points on which the model was based; Pearson et al., 2007). projection to different landscapes as predictions (Iguchi et Raw ENM results for each species were inspected relative al., 2004, Peterson et al., 2007). GARP is an evolutionary- to known occurrences and relative to published range maps computing method that builds ENMs based on nonrandom (Harrap & Quinn, 1995) and disjunct areas of overprediction associations between known occurrence points for species removed. This step is equivalent to an assumption that the and sets of GIS coverages describing variation in several range is reasonably well sampled at coarse geographic ecological parameters of environments. Occurrence data resolutions, and that disjunct areas represent areas of are used by GARP as follows: 50% of occurrence data overprediction for reasons of limited dispersal across points are set aside for an independent fi ltering to assure geographic barriers (Soberón & Peterson, 2005). We are predictive ability of models (extrinsic testing data), 25% comfortable with the general assumption of negligible are used for developing models (training data), and 25% are dispersal ability because nuthatches are generally associated used for tests of model quality internal to GARP (intrinsic with forest or woodland habitats, and because they show

571 Menon et al.: Climate Change Effects on nuthatches little affi nity to disturbed areas. We assume explicitly that groups with diverse evolutionary histories will make for sampling has been suffi cient to detect and document the more robust conclusions. major features of each species’ range. The ecological niche modeling approach to such forecasting Projections of ENM rule sets onto future climate conditions of climate change implications for biodiversity is itself not require explicit consideration of the dispersal abilities of the without limitations. Most importantly, such forecasts depend species in question (Pearson & Dawson, 2003). In the case rather critically on the assumption that species’ ecological of the nuthatches, we assume negligible dispersal abilities, niches will be conservative in the face of changing given that nuthatches are generally restricted to forest. In conditions (Peterson, 2003a)—this assumption has, addition, the forested habitats themselves are unlikely to nonetheless, now seen considerable support in numerous shift broadly (i.e., on geographic scales) in response to empirical assessments (Peterson et al., 1999; Martínez- rapid climate change over just a few decades. As such, our Meyer et al., 2004; Wiens, 2004; Wiens & Graham, hypothesized future distribution for each species was the 2005; Martínez-Meyer & Peterson, 2006; Kambhampati area determined by the intersection of the present-day and & Peterson, 2007). Beyond this fundamental assumption, future predictions (Peterson et al., 2001). the ecological niche models may or may not be robust and predictive, and many considerations enter into their training, testing, and application, although considerable attention in RESULTS the literature is now clarifying the pitfalls and challenges in the modeling process (Midgley et al., 2003; Thuiller et al., Individual nuthatch species are projected to experience diverse effects from changing climates across Asia. Sitta tephronota and S. frontalis provide good illustrations of general tendencies (Figure 2): their potential distributional areas tend to retract along their southern fringes, and at lower elevations along mountain ranges. Projected climate change effects on species’ potential distributions ranged from 5.1- 79.8% areal loss under the B2 scenario, and 5.5-80.4% under the A2 scenario (Table 1). These tendencies—in general at least—are well known, and have been both predicted in previous climate change forecasting studies (Peterson et al. 2005) and documented in real-world observations of climate change effects on species (Parmesan, 1996; Parmesan et al., 1999; Parmesan & Yohe, 2003).

These general tendencies of range loss, when summed across many species, can be used to produce a picture of expected Fig. 2. Model predictions of species distribution area retained (gray) changes in biodiversity across the continent (Peterson et al., and lost (black) due to climate change for two example species, Sitta 2002), which can be considered in a variety of dimensions. tephronota (white triangles, western area) and S. frontalis (dotted squares, Expected local losses of species (Figure 3, upper left panel) eastern area). are focused in the Himalayan foothills, the fl atlands areas of Southeast Asia, and the Indian Subcontinent; viewing these numbers as percentages of the existing community emphasizes the fl atlands of Southeast Asia and the Indian Subcontinent (Figure 3, upper right panel). Translating these numbers into estimates of current and future species richness (Figure 3, bottom panels), Southeast Asia and much of peninsular India are seen to lose signifi cant portions of their nuthatch faunas, in many cases (e.g., Cambodia) losing nuthatches essentially completely.

DISCUSSION

This study offers a first likely view of biodiversity implications of changing climates across Asia. It is a limited view, however, as it focuses on a single clade of birds that probably is itself constrained as to its ecological potential Fig. 3. Model predictions regarding number and percent of nuthatch species by its evolutionary history—as such, these analyses offer lost due to climate change, along with estimated current and future species only a partial view of what effects climate change will have richness for nuthatches. Shading ramps range from white (minimum) to dark gray (maximum) as follows: number of species lost 0-5, percent of on biodiversity. Broadening this study to consider more species lost 0-100, and current and future species richness 0-9 species.

572 THE RAFFLES BULLETIN OF ZOOLOGY 2009

2004; McNyset, 2005; Soberón & Peterson, 2005; Thuiller LITERATURE CITED et al., 2005b; Peterson & Nakazawa, 2008; Peterson et al., 2008). Anderson, R. P., D. Lew, & A. T. Peterson, 2003. Evaluating predictive models of species’ distributions: Criteria for Given these caveats, the results of this set of analyses selecting optimal models. Ecological Modelling, 162: 211- nonetheless point to some general expectations for 232. biodiversity changes across Asia with changing climates. In Araújo, M. B., R. G. Pearson, W. Thuiller, & M. Erhard, 2005a. particular, in terms of range contraction, the foci of effects Validation of species-climate impact models under climate documented herein were Southeast Asia and peninsular change. Global Change Biology, 11:1504-1513. India, with broad range retractions anticipated across several Araújo, M. B., & C. Rahbek, 2006. How does climate change species. As has been observed in other studies (Peterson, affect biodiversity? Science, 313: 1396-1397. 2003b; Siqueira & Peterson, 2003; Peterson et al., 2004), Araújo, M., W. Thuiller, & R. G. Pearson, 2006. Climate warming montane systems appear to be relatively robust to spatial and the decline of amphibians and reptiles in Europe. Journal (i.e., horizontal) effects of climate change on species; of Biogeography, 33: 1712-1728. fl atlands systems, in contrast, appear considerably more Araújo, M. B., R. J. Whittaker, R. J. Ladle, & M. Erhard, 2005b. vulnerable. That is, range retractions appear to concentrate Reducing uncertainty in projections of extinction risk from in flatlands areas, where relatively small changes in climate change. Global Ecology and Biogeography, 14: 529- conditions can translate into appreciable spatial shifts. Jetz 538. et al. (2007) provided future distributional scenarios for Bakkenes, M., J. R. M. Alkemade, F. Ihle, R. Leemansand, & J. B. many of the same species as are examined herein; however, Latour, 2002. Assessing effects of forecasted climate change their methods (ranges summarized as extent of occurrence on the diversity and distribution of European higher plants for maps, coarse resolution) at best serve to give a general 2050. Global Change Biology, 8: 390-407. picture of overall tendencies, but do not suffi ce as genuine Berry, P. M., T. P. Dawson, P. A. Harrison, & R. G. Pearson, forecasts for individual species. 2002. Modelling potential impacts of climate change on the bioclimatic envelope of species in Britain and Ireland. Global Of the nuthatch species included in this study, four (S. Ecology and Biogeography, 11: 453-462. solangiae, S. yunnanensis, S. formosa, S. magna) have BirdLife International. 2008. The BirdLife checklist of the wide ranges, but are considered threatened by habitat loss birds of the world, with conservation status and taxonomic and degradation; two (S. formosa and S. magna) listed as sources. Version 1. Downloaded from http://www.birdlife.org/ datazone/species/downloads/BirdLife_Checklist_Version_ Vulnerable in the IUCN Red List Category, have small, 1.zip [.xls zipped 1 MB]. declining, and severely fragmented ranges; and two (S. solangiae and S. yunnanensis), listed as Near Threatened Brooks T. M., S. L. Pimm, V. Kapos, and C. Ravilious. 1999. Threat from deforestation to montane and lowland birds in the IUCN Red List Category, are impacted by ongoing and mammals in insular South-east Asia. Journal of Animal habitat loss and degradation (Matthysen, 1998; BirdLife Ecology, 68: 1061-1078. International, 2008). Our results show that climate change effects will exacerbate the effects of habitat loss and Chapman, A.D. and J. Wieczorek (Editors). 2006. Guide to Best Practices for Georeferencing. Copenhagen: Global degradation especially in the fl atlands. However, climate Biodiversity Information Facility. Copenhagen, Denmark. change will have relatively less impact on the montane areas www.gbif.org/prog/digit/data_quality/BioGeomancerGuide. of nuthatch distribution, at least in horizontal dimensions. pdf (accessed 10 August 2007). Collar, N. J., A. V. Andreev, S. Chan, M. J. Crosby, S. Subramanya, Middle elevation forests hold the highest nuthatch species & J. A. Tobias, 2001. Threatened Birds of Asia: The diversity (Menon et al., 2008). Unfortunately, montane areas BirdLife International Red Data Book. BirdLife International, generally, and middle elevation forests especially, are not Cambridge, UK. immune to pressures from deforestation and fragmentation Elith, J., C. H. Graham, R. P. Anderson, M. Dudik, S. Ferrier, leading to habitat loss and isolation of populations, and A. Guisan, R. J. Hijmans, F. Huettman, J. R. Leathwick, A. exacerbating any climate change effects (Brooks et al. 1999, Lehmann, J. Li, L. G. Lohmann, B. A. Loiselle, G. Manion, Pandit et al. 2007). In light of the vulnerability of fl atlands C. Moritz, M. Nakamura, Y. Nakazawa, J. M. Overton, A. T. to climate change effects, our study further emphasizes the Peterson, S. J. Phillips, K. Richardson, R. Scachetti-Pereira, importance of middle elevation habitats in this region for R. E. Schapire, J. Soberón, S. E. Williams, M. S. Wisz, & N. the conservation of this group. E. Zimmerman, 2006. Novel methods improve prediction of species’ distributions from occurrence data. Ecography, 29: 129-151. ACKNOWLEDGMENTS Erasmus, B. F. N., A. S. Van Jaarsveld, S. L. Chown, M. Kshatriya, and K. J. Wessels, 2002. Vulnerability of South African animal taxa to climate change. Global Change Biology, 8: 679-693. We thank colleagues Jorge Soberón and Monica Papes¸ for their always-helpful ideas and assistance. This work was Hampe, A. 2004. Bioclimate envelope models: What they detect developed with support from a National Science Foundation and what they hide. Global Ecology and Biogeography, 13: Research Opportunity Award (DBI-0345448). 469-471. Harrap, S., & D. Quinn, 1995. Chickadees, Tits, Nuthatches & Treecreepers. Princeton University Press, Princeton, N.J.

573 Menon et al.: Climate Change Effects on nuthatches

Huntley, B., R. E. Green, Y. C. Collingham, J. K. Hill, S. G. Parmesan, C., N. Ryrholm, C. Stefanescu, J. K. Hill, C. D. Thomas, Willis, P. J. Bartlein, W. Cramer, W. J. M. Hagemeijer, & C. H. Descimon, B. Huntley, L. Kaila, J. Kullberg, T. Tammaru, J. Thomas, 2004. The performance of models relating species J. Tennent, J. A. Thomas, & M. Warren, 1999. Poleward shift geographical distributions to climate is independent of trophic of butterfl y species’ ranges associated with regional warming. level. Ecology Letters, 7: 417-426. Nature, 399:579-583. Iguchi, K., K. Matsuura, K. McNyset, A. T. Peterson, R. Scachetti- Parmesan, C., & G. Yohe, 2003. A globally coherent fi ngerprint Pereira, K. A. Powers, D. A. Vieglais, E. O. Wiley, & T. Yodo, of climate change impacts across natural systems. Nature, 2004. Predicting invasions of North American basses in Japan 421:37-42. using native range data and a genetic algorithm. Transactions Pearson, R. G., & T. P. Dawson, 2003. Predicting the impacts of of the American Fisheries Society, 133: 845-854. climate change on the distribution of species: Are bioclimate IPCC, 2007. Climate Change 2007: The Physical Science Basis. envelope models useful? Global Ecology and Biogeography, Cambridge University Press, Cambridge. 12: 361-371. Jetz, W., D. S. Wilcove, and A. P. Dobson. 2007. Projected impacts Pearson, R. G., C. Raxworthy, M. Nakamura, & A. T. Peterson, of climate and land-use change on the global diversity of birds. 2007. Predicting species’ distributions from small numbers PLoS Biology 5(6): e157.doi:10.1371/journal.pbio.0050157. of occurrence records: A test case using cryptic geckos in Kambhampati, S., & A. T. Peterson, 2007. Ecological niche Madagascar. Journal of Biogeography, 34: 102-117. conservation and differentiation in the wood-feeding Pearson, R. G., W. Thuiller, M. B. Araújo, E. Martinez-Meyer, L. cockroaches, Cryptocercus, in the United States. Biological Brotons, C. McClean, L. Miles, P. Segurado, T. P. Dawson, Journal of the Linnean Society, 90:457-466. and D. C. Lees. 2006. Model-based uncertainty in species Lobo, J. M., A. Jimenez-Valverde, & R. Real, 2007. AUC: range prediction. Journal of Biogeography 33: 1704-1711. A misleading measure of the performance of predictive Peterson, A. T. 2003a. Predicting the geography of species’ distribution models. Global Ecology and Biogeography, 17: invasions via ecological niche modeling. Quarternary Review 145-151. of Biology, 78: 419-433. Lovejoy, T. E., & L. Hannah, eds., 2005. Climate Change and Peterson, A. T. 2003b. Projected climate change effects on Rocky Biodiversity. Yale University Press, New Haven, Conn. Mountain and Great Plains birds: Generalities of biodiversity Martínez-Meyer, E., & A. T. Peterson, 2006. Conservatism of consequences. Global Change Biology, 9: 647-655. ecological niche characteristics in North American plant Peterson, A. T., E. Martínez-Meyer, C. González-Salazar, & P. species over the Pleistocene-to-Recent transition. Journal of Hall, 2004. Modeled climate change effects on distributions Biogeography, 33: 1779-1789. of Canadian butterfl y species. Canadian Journal of Zoology, Martínez-Meyer, E., A. T. Peterson, & W. W. Hargrove, 2004. 82: 851-858. Ecological niches as stable distributional constraints on Peterson, A. T. & Y. Nakazawa, 2008. Environmental data mammal species, with implications for Pleistocene extinctions sets matter in ecological niche modeling: An example with and climate change projections for biodiversity. Global Solenopsis invicta and Solenopsis richteri. Global Ecology Ecology and Biogeography, 13: 305-314. and Biogeography, 17: 135-144. Matthysen E. 1998. The Nuthatches. T. and A. D. Poyser, Peterson, A. T., M. A. Ortega-Huerta, J. Bartley, V. Sánchez- London. Cordero, J. Soberón, R. H. Buddemeier, & D. R. B. Stockwell, McNyset, K. M. 2005. Use of ecological niche modelling to predict 2002. Future projections for Mexican faunas under global distributions of freshwater fi sh species in Kansas. Ecology of climate change scenarios. Nature, 416: 626-629. Freshwater Fish, 14: 243-255. Peterson, A. T., M. Papes ¸, & M. Eaton, 2007. Transferability and Menon, S., Z. Islam, J. Soberón, & A. T. Peterson, 2008. model evaluation in ecological niche modeling: A comparison Ecological and geographic analysis of the Asian nuthatches of GARP and Maxent. Ecography, 30: 550-560. (Aves: Sittidae). Wilson Journal of Ornithology, 120(4): 692- Peterson, A. T., M. Papes ¸ , & J. Soberón, 2008. Rethinking receiver 699. operating characteristic analysis applications in ecological Midgley, G. F., L. Hannah, D. Millar, W. Thuiller, & A. Booth, niche modelling. Ecological Modelling, 213: 63-72. 2003. Developing regional and species-level assessments of Peterson, A. T., V. Sánchez-Cordero, J. Soberón, J. Bartley, R. climate change impacts on biodiversity in the Cape Floristic H. Buddemeier, & A. G. Navarro-Sigüenza, 2001. Effects of Region. Biological Conservation, 112: 87-97. global climate change on geographic distributions of Mexican National Geospatial-Intelligence Agency. 2007. GEOnet Names Cracidae. Ecological Modelling, 144: 21-30. Server (GNS). http://earth-info.nga.mil/gns/html/index.html Peterson, A. T., J. Soberón, & V. Sánchez-Cordero, 1999. (accessed 10 August 2007). Conservatism of ecological niches in evolutionary time. New, M., D. Lister, M. Hulme, & I. Makin, 2002. A high- Science, 285: 1265-1267. resolution data set of surface climate over global land areas. Peterson, A. T., H. Tian, E. Martínez-Meyer, J. Soberón, V. Climate Research, 21: 1-25. Sánchez-Cordero, & B. Huntley, 2005. Modeling distributional Pandit, M. K., N. S. Sodhi, L. P. Koh, A. Bhaskar, and B. W. shifts of individual species and biomes. Pages 211-228 in T. E. Brook. 2007. Unreported yet massive deforestation driving Lovejoy & Hannah, L. (eds.) Climate Change and Biodiversity. loss of endemic biodiversity in Indian Himalaya. Biodiversity Yale University Press, New Haven, Conn. Conservation, 16: 153-163. Segurado, P., & M. B. Araújo, 2004. An evaluation of methods Parmesan, C. 1996. Climate and species’ range. Nature 382: for modelling species distributions. Journal of Biogeography, 765-766. 31: 1555-1568.

574 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Siqueira, M. F. d. & A. T. Peterson, 2003. Global climate change Thuiller, W., S. Lavorel, M. B. Araújo, M. T. Sykes, & I. C. consequences for cerrado tree species. Biota Neotropica, 3 Prentice, 2005a. Climate change threats to plant diversity in http://www.biotaneotropica.org.br/v3n2/en/abstract?article+B Europe. Proceedings of the Natural Academy of Sciences, USA N00803022003 102: 8245-8250. Soberón, J. & A. T. Peterson, 2005. Interpretation of models Thuiller, W., D. M. Richardson, P. Pysek, G. F. Midgley, G. O. of fundamental ecological niches and species’ distributional Hughes, & M. Rouget, 2005b. Niche-based modelling as a areas. Biodiversity Informatics, 2: 1-10. tool for predicting the risk of alien plant invasions at a global Stockwell, D. R. B. & D. P. Peters, 1999. The GARP modelling scale. Global Change Biology, 11: 2234-2250. system: Problems and solutions to automated spatial prediction. Visser, M. E., A. J. van Noordwijk, J. M. Tinbergen, & C. M. International Journal of Geographic Information Science, 13: Lessells,1998. Warmer springs lead to mistimed reproduction 143-158. in great tits (Parus major). Proceedings of the Royal Society Thomas, C. D., A. Cameron, R. E. Green, M. Bakkenes, L. J. B, 265:1867-1870. Beaumont, Y. C. Collingham, B. F. N. Erasmus, M. Ferreira Wiens, J. J. 2004. Speciation and ecology revisited: Phylogenetic de Siqueira, A. Grainger, L. Hannah, L. Hughes, B. Huntley, niche conservatism and the origin of species. Evolution, 58: A. S. Van Jaarsveld, G. E. Midgely, L. Miles, M. A. Ortega- 193-197. Huerta, A. T. Peterson, O. L. Phillips, & S. E. Williams, 2004. Wiens, J. J., & C. H. Graham. 2005. Niche conservatism: Extinction risk from climate change. Nature, 427: 145-148. Integrating evolution, ecology, and conservation biology. Thuiller, W., L. Brotons., M. Araújo, & S. Lavorel, 2004. Effects Annual Review of Ecology, Evolution and Systematics, 36: of restricting environmental range of data to project current and 519-539. future species distributions. Ecography, 27: 165-172.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 577–586 Date of Publication: 31 Aug.2009 © National University of Singapore

OBSERVATIONS ON THE ECOLOGY, DISTRIBUTION AND BIOGEOGRAPHY OF FOREST BIRDS IN SABAH, MALAYSIA

Frederick H. Sheldon and Haw Chuan Lim Museum of Natural Science and Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70808 USA Email: [email protected] (Corresponding author)

Jamili Nais and Maklarin Lakim Sabah Parks, P.O. Box 10626, 88806 Kota Kinabalu, Sabah, Malaysia

Augustine Tuuga and Peter Malim Sabah Wildlife Department, 1st Floor A Block, Wisma MUIS, 88100 Kota Kinabalu, Sabah, Malaysia

Jaffi t Majuakim and Albert Lo Sabah Museum, Locked Bag No. 2015, 88566 Kota Kinabalu, Sabah, Malaysia

Menno Schilthuizen Universiti Malaysia Sabah, Locked Bag No. 207, 88999 Kota Kinabalu, Sabah Malaysia

Peter A. Hosner and Robert G. Moyle Natural History Museum and Biodiversity Research Center and Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence KS 66045, USA

ABSTRACT. – From January 2004 to July 2008, we surveyed and collected birds at 15 sites in Sabah, Malaysian Borneo. This work was designed to (1) document bird occurrence in areas and habitats that had been poorly surveyed in the past, (2) provide specimens for molecular genetic studies of bird evolution in Borneo, and (3) examine the occurrence of forest birds in agricultural and industrial tree plantations. The research disclosed new elevational, habitat, and breeding records for numerous species. It also provided insight into the biogeography of lowland endemic species in Sabah and montane endemic species in Borneo. The hypotheses formulated from these biogeographic discoveries should serve as useful frameworks for future phylogeographic work on Bornean birds.

KEY WORDS. – Borneo, elevation, endemism, oil palm, peatswamp, Southeast Asian biogeography.

INTRODUCTION same time that the forests of Sabah have been changing, so has interest in the wildlife inhabiting those forests. In the last 30 years, the forests of Southeast Asia have Ecotourism and natural history research have boomed in changed dramatically as a result of logging and development the state in recent years and have produced a mass of new (Curran et al., 2004; Sodhi et al., 2004; Koh & Wilcove, information on wildlife. 2008). Typical of such change are forests in the Malaysian state of Sabah in northernmost Borneo. In 1970, only 16% Much recent information on the birds of Borneo is being of the land area of Sabah had been infl uenced substantially compiled and included in new publications, including an by humans (Thomas et al., 1976; Sheldon et al., 2001), but annotated checklist (Mann, 2008) and planned fi eld guides by the year 2000 more than 80% of the forest had been (S. Myers and Q. Phillipps, pers. comm.). To contribute to markedly disturbed (Marsh & Greer, 1992; McMorrow & the updating process, we report here on recent ornithological Talip, 2001). Today, the only large stands of undisturbed research in Sabah. Starting in January 2004 and ending forest remaining in Sabah are in parks (Kinabalu National in July 2008, we conducted a series of bird surveys and Park and Crocker Range National Park) and special collections in Sabah. The purpose of the work was (1) to preserves (e.g., Danum Valley and Maliau Basin). At the document bird occurrence in areas and habitats that had

577 Sheldon et al.: Observations on Sabah birds been poorly surveyed in the past, (2) to collect specimens Samples from this collection were used by Moyle et al. for studies of bird evolution in Borneo and Southeast Asia, (2008). and (3) to examine the use of agricultural and industrial tree plantations by Borneo’s forest birds. By themselves, the Kinabalu National Park, 24–28 February 2005. – Netted many small facts we have collected during our surveys and at Laban Rata (6o03.52'N 116o33.97'E) and Layang Layang subsequent studies may not appear profound, but together (6o02.75'N 116o33.61'E). Elevation: at Laban Rata 3270 they provide substantial insight into the natural history m, at Layang Layang 2730 m. Habitat: ericaceous forest. of Bornean birds. Of special importance are emerging Publications: Samples from this collection were used by biogeographic patterns that shed light on the evolution of Moyle et al. (2008; 2009). bird diversity in Borneo, particularly in regard to endemicity. Also documented is evidence of recent shifts in bird Kinabalu National Park, 20–25 June 2008. – Netted around distribution in Borneo promoted by the opening of montane park headquarters (6o00'19"N 116o32'36"E). Elevation: forest by logging and plantation development, and perhaps 1500 m. Habitat: primary and secondary montane forest. also promoted by global warming. This new information should be of substantial interest to biogeographers, Klias Forest Reserve, 5–12 February 2004. – Worked in the ornithologists, wildlife managers, birdwatchers, and other northwest corner of Klias FR using the Forestry Department with a stake in Bornean birdlife. rest house as a base, about 8 km southwest of Beaufort (05o10'34"N 115o40'25"E). Elevation: sea level. Habitat: primary and secondary peatswamp forest and scrub. Results MATERIALS AND METHODS of this survey are reported in Sheldon et al. (2009a) and specimens were used in Sheldon et al. (2009b). Remarks: At each site described below (except Sabah Softwoods), This site is of particular interest because it is one of the we captured birds with mistnets and observed them last remaining stands of accessible peatswamp in Sabah informally in the wild. In some cases, we tape-recorded and home to some species that are rare or uncommon in singing birds. These tape-recordings are archived at the Sabah, including Hook-billed Bulbul (Setornis criniger) Macaulay Library at Cornell University and are available and Grey-breasted Babbler (Malacopteron albogulare) online at www.animalbehaviorarchive.org. Specimens (Sheldon, 1987). from the project were divided among several collections, depending on locality. Specimens from parks were split Masikuan, Padas Damit, 3–4 June 2008. – Netted briefl y between the Sabah Park Collection and Louisiana State at his site on Klias Peninsula ca. 25 km west of Beaufort Museum of Natural Science (LSU). Specimens collected (5o19'40"N 115o30'48"E). Elevation: sea level. Habitat: outside of parks were divided between Sabah Museum and heavily disturbed swamp forest, scrub, and plantation. LSU. Some specimens have been loaned permanently by Remarks: This site was a source of coastal and west coast LSU to the American Museum of Natural History and the specimens. University of Kansas Natural History Museum. At Sabah Softwoods, instead of making a collection, we conducted a Mt. Meliau, 22–31 May 2006. – We approached Mt. Meliau formal point-count survey of birds as described by Styring from the east through Pamol and the Meliau oil palm et al. (2007). plantation to make camp on an old logging road on the north side of the Meliau River (05o50'44"N 117o10'57"E). Most of our descriptions of natural history are qualitative, We set nets from the base camp up to a ridge northeast of but we have made some preliminary genetic comparisons Mt. Meliau proper (05o52'08"N 117o09'59"E). Elevation: 75 among taxa. Unless otherwise specifi ed, these are based – 1067 m. Habitat: logged forest on ultrabasic soils to 400 on sequences of mitochondrial nicotinamide adenine m; primary ultrabasic forest at higher elevation. This forest dinucleotide dehydrogenase subunit 2 (ND2) DNA, as consisted mainly of narrow, pole-like trees, interspersed described by Sheldon et al. (2009b). with thickets of climbing bamboo. Remarks: We were interesting in discovering whether montane species inhabit Work Sites the ultrabasic forest at higher elevations.

Inobang, Penampang, 30 May–1 June 2008. – Netted Mendolong and Mt. Lumaku, 15–18 January 2005. – This briefl y at this site, just outside Crocker Range National site included two locations ca. 25 km southeast of Sipitang: Park (5o51'25"N 116o08'00"E). Elevation: 400 m. Habitat: one near the Sabah Forest Industries plantation rest house upland secondary forest. Remarks: This site was of interest (4o54.181'N 115o41.522'E), and the other on the fl anks of as a source of lowland specimens from the west coast for Mt. Lumaku (4o51.027'N 115o41.963'E). Elevation: 550 phylogeographic comparison with specimens from sites east m in the plantation and 1100 m on Mt. Lumaku. Habitat: across the Crocker Range. scrub adjacent to Acacia plantation and, on Lumaku, small stands of primary forest on ridges surrounded by heavily Kinabalu National Park, 8–11 August 2004. – Netted logged slopes. Remarks: This site is important not only swiftlets at the Park headquarters (6o00'19"N 116o32'36"E). for its elevation but also its location in the taxic transition Elevation 1500 m. Habitat: roads and buildings. Publications: zone between Sarawak and Sabah. Publications: Samples

578 THE RAFFLES BULLETIN OF ZOOLOGY 2009 from this collection were use by Haines (2007) and Sheldon of bananas and gingers, Ulu Kimanis headquarters had a et al. (2009b) remarkable number of spiderhunters of various species.

Sabah Softwoods, 23 June–12 July 2005. – Sabah Ulu Lauhon, Maligan Range, 5–11 June 2008. – We Softwoods Sdn. Bhd. is an exotic tree plantation in the made a substantial collection at this site ca. 58 km SSE of Tawau District of southeastern Sabah. We surveyed birds Sipitang (4o34'28"N 115o41'45"E). Elevation: 1700 – 1800 near its headquarters at Brumas, ca. 50 km NNW of Tawau m. Habitat: roadside scrub, heavily logged lower montane (4o37'N, 117o44'E). Elevation: 150 – 200 m. Habitat: forest, and some primary forest on ridges. Remarks: This logged forest on steep hills, scrub, Albizia (Paraserienthis) site is important not only for its elevation but also its falcataria, Acacia mangium, and oil palm. Remarks: location in the taxic transition zone between Sarawak and Our survey was a follow-up to previous work at Sabah Sabah. Softwoods (Mitra & Sheldon, 1993). Ulu Rukuruku, 13–19 August 2004. – This site includes a Serinsim Substation, Kinabalu National Park, 17 Class I forest reserve within the Tawai Forest Reserve, ca. 8 January–1 February 2004. – This substation is located km east of Telupid (5o36.940'N, 117o11.660'E). Elevation: in the northeastern corner of Kinabalu Park (6o17'36"N 130 m. Habitat: primary and disturbed kerangas on 116o42'29"), ca. 30 km south of Kota Marudu. Elevation: ultrabasic soils and primary and disturbed forest growing on 200 – 450 m. Habitat: Mainly heavily disturbed scrub and a complex of ultrabasic and limestone soils. Remarks: This forest and lightly logged dipterocarp forest. Remarks: We site was of interest for endemic ultrabasic forest species, were interested in Serinsim because no birds have been such as Grey-breasted Babbler (Malacopteron albogulare) collected on the mainland of northern Sabah since colonial and Scarlet-breasted Flowerpecker (Prionochilus thoracicus) times. Publications: Results of this survey are reported by (Davies & Payne, 1982). Sheldon et al. (2009c) and specimens were used in Sheldon et al. (2009b). RESULTS Tawau Hills Park, 23 January–10 February 2005. – Work was conducted in two areas in the Park: near the headquarters Key Distributional and Taxonomic Observations (4o23.87'N 117o53.28'E) and on Mt. Lucia (4o27.63'N 117o53.34'E). Elevation: 280 m at the headquarters; 900 Bornean Swiftlet (Collocalia dodgei). – Cranbrook et al. – 1150 m on Mt. Lucia. Habitat: near the headquarters, (2005) and Moyle et al. (2008) described the occurrence of secondary forest and oil palm plantation; on Mt. Lucia, this endemic swiftlet at higher elevations on Mt. Kinabalu. primary forest. Remarks: Mt. Lucia is of interest for its Moyle et al. (2008) suggested it might also occur on other isolated montane bird population. Publications: Samples mountains in Borneo, but has not been recognized because from this collection were use by Haines (2007) and Moyle of its similarity to the Glossy Swiftet (C. esculenta), which et al. (2009) is common up to ca. 1600 m. This prediction proved true, as we captured an individual of Bornean Swiftlet at 1800 m on Trus Madi, 21 July–2 August 2005. – This survey was a logging road at Ulu Lauhon in the Maligan Range. It was based at the Forestry Department rest house located at genetically identical to the C. dodgei specimens from Mt. 1450 m on the highest logging road on the north side of Kinabalu (GenBank # FJ798744). Unfortunately, we cannot the mountain (05o35'09"N 116o29'26"E). We also set nets provide useful wing measurements, as the outer primaries and observed birds for brief periods at four other locations: in the specimen are still sheathed. The bird is very small, the helicopter platform at 1629 m (5o34'12"N 116o28'58"E), noticeably smaller in the fi eld than Glossy Swiftlet, with 26-28 July 2005; Taman Bunga at 2350 m (5o33'27"N which it was feeding over a logging road. 116o30'03"E), 29–30 July 2005; the summit at 2600 m (5o33'20"N 116o30'34"E), 29 July 2005; and northeast of the Bornean Barbet (Megalaima eximia). – We captured this rest house at 1600m (05o35'25"N 116o29'38"E), 30 July – 1 species on Trus Madi (1450 m) and Mt. Lucia (900 m), August 2005. Habitats: logged lower montane forest and where it was often heard calling. A specimen from Mt. primary upper montane and ericaceous forest. Publications: Lucia disputes the endemic Mt. Kinabalu subspecies M. Older reports include Sheldon & Francis (1985) and Moyle e. cyanea, which has a blue forehead and throat. The Mt. & Wong (2002). Samples from the 2005 collection were Lucia specimen also had a blue forehead and throat, but was used by Gawin (2006) and Haines (2007). immature. The blue coloring is likely to be a characteristic of young birds. Ulu Kimanis Substation, Crocker Range National Park, 14-18 June 2008. – Netted briefly at this site ca. 53 Bornean Leafbird (Chloropsis kinabaluensis). – Specimens km south of Kota Kinabalu (5o30'17"N 116o00'48"E). from Trus Madi provide additional evidence that the Elevation: 565 m at the substation headquarters. Habitat: montane blue-winged leafbird of Borneo, formerly C. upland primary and secondary forest and gardens. Remarks: cochinchinensis fl avocincta, is a species distinct from the This site was a source of lowland specimens from the west lowland form, C. c. viridinucha, found in Borneo outside coast for phylogeographic comparison with sites east across of Sabah (Wells et al., 2003). Not only does the female the Crocker Range. Because of its extensive plantings C. kinabaluensis have a black throat like the male, which

579 Sheldon et al.: Observations on Sabah birds distinguishes it from C. cochinchinensis (Peters, 1940), but secondary forest on 4 November 1998, and there are early there are additional distinguishing characteristics. Only the records from the Padas River district (Smythies, 1957). male--not the female--has a blue malar stripe (moustache), Conversely, C. stricklandii extends and overlaps with C. and the female has green plumage surrounding the black on malabaricus to the Lawas region of Sarawak (Smythies, the head and throat (as in MacKinnon & Phillipps, 1993), 1957). On the eastern side of Sabah, C. malabaricus has as opposed to yellow in the male. (A juvenile male we been reported to reach Silam near Lahad Datu (Smythies, collected had female plumage.) The parapatric distribution 1957). Apparent introgressed individuals of C. stricklandii of C. kinabaluensis in highland areas and C. cochinchinensis were caught in Danum Valley, inland of Silam, in 1976 in lowland areas of Borneo is strong a priori evidence of (Kiew, 1977). These birds had white crown feathers species distinction (see Discussion). extensively tipped in black. Davison (1999) reviewed the species status of C. malabaricus and C. stricklandii. He Straw-headed Bulbul (Pycnonotus zeylanicus). – This concluded that they hybridize over a wide area (in some species was previously one of the most common birds of cases hundreds of kilometers), and their status as species padi and river edges in Sabah. Now it is rare. For example, depends on the stability of their hybrid zone. Genetically, in surveys at Sabah Softwoods in 1982, Mitra and Sheldon the two taxa are quite distinct between Sabah and Bintulu, (1993) commonly recorded it along rivers in Albizia Sarawak (uncorrected ND2 distance, 2.6% – 3.2%). falcataria groves. However, it was not recorded in surveys Because they are also distinct morphologically, we treat in 2005 at Sabah Softwoods in any habitat. Indeed, the only them as different species (see Discussion). location where we have found it in the last fi ve years is on the Kinabatangan River near Sukau. Others have recorded Bornean Forktail (Enicurus borneensis). – Moyle et it along rivers at Danum Valley (S. Myers pers. comm.). al. (2005) demonstrated that the highland form of E. This species appears to have been extirpated from most of leschenaulti in Borneo (E. l. borneensis) is different its range in Sabah (and other areas in Borneo), presumably phylogenetically and morphologically from the lowland by pet traders (Holmes, 1997). form, E. l. frontalis (see Discussion). As such, the endemic montane form is a different species. We suggest Bornean Oriental Magpie-Robin (Copsychus saularis). – We Forktail as an appropriate name for E. borneensis. collected individuals of this species at Klias FR, Mendolong, Serinsim, and Tawau Hills and examined specimens from Streaky-breasted Spiderhunter (Arachnothera affi nis). other localities in Sabah (Sheldon et al., 2009b). In principle, – Confusion still exists concerning this species and its three subspecies occur in Borneo (Collar, 2005): (1) musicus similar congener, Grey-breasted Spiderhunter, A. modesta in the southwest, with a white belly and black and white (Mann, 2008). Arachnothera modesta is a lowland species tail; (2) adamsi in Sabah, with a dark belly and all black that does not occur in Sabah; only A. affi nis is found in the tail; and (3) pluto in eastern Kalimantan, with a dark belly state (in both the lowlands and mountains; see Discussion). and white in the tail. Our molecular comparisons, however, Comparison of mitochondrial ND2 and ND3 genes between show only two genetic groups: musicus types (with white lowland and montane specimens from Sabah confi rmed they bellies and white in the tail) and adamsi/pluto types (with are all A. affi nis (Haines, 2007). At Ulu Kimanis, we netted black bellies and usually white in the tail). It appears many individuals of this species. Males averaged ca. 27 g, that musicus has invaded Borneo relatively recently from females 20 g. The much larger size of the males may cause the west and is hybridizing extensively with (presumably birdwatchers to think there are two species. native) black-bellied birds (Mees, 1986), resulting in a variety of plumage combinations and possibly swamping Pygmy White-eye (Oculocincta squamifrons). – Netted on the black-bellied form. We found individuals of the two Mt. Lucia at 1000 – 1100 m in primary forest. Previously, genotypes together on Klias Peninsula and at Ulu Kimanis. it was recorded on nearby Mt. Magdalena by the British Those of musicus genotype had typical musicus plumage, Museum expedition of 1956 at ca. 1200 m (Smythies, 1957). but those of adamsi/pluto genotype had either black bellies Genetic comparisons with other white-eyes (Moyle et al., and a little white in the tail or white bellies and substantial 2009) indicate that Oculocincta is a member of a clade with white in the tail. Thus, hybridization of musicus and adamsi Lophozosterops (Wallacean white-eyes) that is embedded appears to be extensive on the western side of Sabah, and among Philippine babblers (Dasycrotapha, Sterrhoptilus, it may be diffi cult nowadays to fi nd individuals with the and Zosterornis previously in Stachyris). This unusual all-black adamsi plumage. (Historically, adamsi occurred group is sister to typical white-eyes (Zosterops). on the coast from Tuaran up to Banggi and Balambangan islands and down through Sandakan to Tawau.) Mountain Black-eye (Chlorocharis emiliae). – Netted at Laban Rata (3270 m) and also on Mt. Trus Madi (at 1600 White-rumped Shama (Copsychus malabaricus). – In and 2600 m). The Trus Madi specimens were used in a general, the White-crowned Shama, C. stricklandii, is genetic comparison of Sabah and Sarawak populations considered the shama of Sabah and C. malabaricus occurs (Gawin, 2006). The Laban Rata specimens were used in a elsewhere in Borneo. However, C. malabaricus enters the phylogenetic study of white-eye relationships (Moyle et al., western side of Sabah. The Sabah Park Collection has a 2009), which found Chlorocharis to be a typical white-eye specimen from Mendolong (#16761), a male collected in embedded within Zosterops.

580 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Other Species Accounts Collared Owlet (Glaucidium brodiei). – Recorded on Mt. Lucia at 950 m. The species records below were included because they supplement substantially the information on distribution Short-tailed Frogmouth (Batrachostomus poliolophus). and breeding in Smythies (1999), Sheldon et al. (2001), – Netted on Mt. Trus Madi in primary forest at 1650 m. Moyle (2003) and Mann (2008). We have not mentioned Its main food was beetles. marginal increases in elevation or breeding records of common species. (These are included in unpublished Sunda Frogmouth (Batrachostomus cornutus). – The reports available from the authors.) We have, however, Sabah Park Collection has two specimens collected on included records of rarer birds, even if the information Balambangan Island on 25 and 27 May 2003. was predictable from earlier knowledge. The quality of the information is indicated by its source, i.e., whether it is Waterfall Swift (Hydrochrous gigas). – The Sabah Park based on mistnetting, observation, or voice (=recorded). Collection has six specimens collected at Batu Kapur on Balambangan Island on 23 May 2003. Oriental Honey-Buzzard (Pernis ptilorhyncus). – Observed in 7 year old Acacia at Sabah Softwoods. Diard’s Trogon (Harpactes diardi). – Netted in secondary peatswamp scrub 0.5 km from substantial forest at Klias Blue-breasted Quail (Coturnix chinensis). – Recorded in FR. oil palm at Sabah Softwoods. Rufous Piculet (Sasia abnormis). – Netted up to 1450 m Scaly-breasted Partridge (Arborophila charltonii). on Trus Madi. – Recorded in 7 year old Acacia at Sabah Softwoods. Rufous Woodpecker (Celeus brachyurus). – Netted in Crested Partridge (Rollulus rouloul). – Numerous primary peatswamp at Klias FR and in ultrabasic forest at individuals were netted commuting to the oil palm Ulu Rukuruku. plantation at Tawau Hills Park headquarters from adjacent forest. This species was also observed in the oil palm at Great Slaty Woodpecker (Mulleripicus pulverulentus). Sabah Softwoods. – Observed excavating a nest hole in a 9 year old Albizia tree at Sabah Softwoods on 11 July 2005. The site was ca. Crested Fireback (Lophura ignita). – Three males were 200 m from logged native forest. displaying to a female in 7 year old Acacia at Sabah Softwoods. Hose’s Broadbill (Calyptomena hosii). – Sabah Museum has a specimen collected on Mt. Lumaku on 20 July 1996 Pink-necked Green Pigeon (Treron vernans). – Birds in in disturbed forest (no elevation). breeding condition were collected at Klias FR on 9 February 2004: testes 14x5 mm, 16x8 mm, yolked egg 15x15 mm. Dusky Broadbill (Corydon sumatranus). – Observed at Sabah Softwoods in 7 year old Acacia. It is also commonly Plaintive Cuckoo (Cacomantis merulinus). – An individual recorded on the edge of the Kinabatangan River at Sukau. with a shelled oviduct egg was collected on 7 February 2004 at Klias FR. Giant Pitta (Pitta caerulea). – Commonly recorded along the Kinabatangan River near Sukau. Little Bronze Cuckoo (Chrysococcyx minutillus). – Recorded in old tall trees at Sabah Softwoods in Eucalyptus, Blue-banded Pitta (Pitta arquata). – Recorded at Sabah Acacia, and Albizia groves. Softwoods in steep, logged forest and at Bumbalai Hill in Tawau Hills Park. The Sabah Park Collection has a Chestnut-winged Cuckoo (Clamator coromandus). – Two specimen from a ridge in Tawau Hills Park. Sabah Museum were netted in thick primary peatswamp forest at Klias FR has a specimen from Tagodon, a submontane site on the in February 2004. These records suggest this scarce migrant western side of the Crocker Range, east of Penampang. This may prefer coastal or peatswamp forest for overwintering. scarce species seems to prefer steep forest sites.

Bornean Ground Cuckoo (Carpococcyx radiatus). Lesser Cuckooshrike (Coracina fi mbriata). – Parent birds – Recorded numerous times in recent years in the riverine were observed feeding a recent fl edgling on 31 May 2006 forest along the Menanggul River, Sukau. A voice recording at Meliau base camp. is stored at Macaulay Library, ML# 129446. Black-and-white Bulbul (Pycnonotus melanoleucos). Rajah Scops Owl (Otus brookii). – The Sabah Park – Netted in primary and secondary ultrabasic forest at Ulu Collection has a mounted male specimen collected at 1650 Rukuruku and Meliau. m on Mt. Kinabalu on 20 August 1998. Grey-bellied Bulbul (Pycnonotus cyaniventris). – Common in ultrabasic roadside scrub at Meliau.

581 Sheldon et al.: Observations on Sabah birds

Flavescent Bulbul (Pycnonotus flavescens). – A few Mountain Wren Babbler (Napothera crassa). – Observed recorded at 1500 m in roadside scrub on Trus Madi; more at the summit of Trus Madi (2600 m) foraging on tree trunks common in the ericaceous forest at the summit (2300 in the ericaceous forest. – 2600 m). Eyebrowed Wren Babbler (Napothera epilepidota). Olive-winged Bulbul (Pycnonotus plumosus). – Netted at – Netted on Mt. Trus Madi at 1450 m in dark woods near 1600 m along a logging road at Ulu Lauhon. streams and observed on Mt. Lucia at 1000 m in a dense tangle on a ridge. Grey-cheeked Bulbul (Alophoixus bres). – Netted in primary ultramafi c forest at Ulu Rukuruku and Meliau. Striped Tit Babbler (Macronous gularis). – Netted at 1600 m at Ulu Lauhon and 1450 m on Mt. Trus Madi, in both Yellow-bellied Bulbul (Alophoixus phaeocephalus). cases in scrub along logging roads. – Netted in primary ultramafi c forest at Ulu Rukuruku. Fluffy-backed Tit Babbler (Macronous ptilosus). – A Hook-billed Bulbul (Setornis criniger). – Netted in specimen in breeding condition was netted at Klias FR: 7 peatswamp at Klias FR. Two specimens were in breeding February 2004, 15 mm oviduct yolk. condition on 8 February 2004 (testes 10x5 mm and 8x8 mm). White-necked Babbler (Stachyris leucotis). – Netted in primary ultrabasic forest at Ulu Rukuruku and observed Streaked Bulbul (Ixos malaccensis). – Common in in primary dipterocarp forest at Mt. Lucia (700 m). This ultramafi c forest at Meliau. scarce species was also captured by Moyle (2003) at the Crocker Range National Park headquarters near Keningau. Buff-vented Bulbul (Iole olivacea). – Common in It appears to prefer steep slopes. ultramafi c roadside scrub at Meliau, and also at other sites in Sabah in edge habitat. Chestnut-rumped Babbler (Stachyris maculata). – Specimens in breeding condition collected at Klias: 7 Chestnut-capped Thrush (Zoothera interpres). – Netted in February 2004, testes 9x5 mm, 9 mm yolk and enlarged both primary and secondary forest along the Serinsim River, oviduct. where an individual in breeding condition was collected on 29 January 2004 (testes 8x4 mm). A. Biun (pers. comm.) White-browed Shrike Babbler (Pteruthius fl aviscapis). reported that several nests were found by Park staff in – Netted at 2340 m on Trus Madi in ericaceous forest. August 1998 along the Serinsim River. The nests were near the ground or up to 3 m high. They were cups built Brown Fulvetta (Alcippe bruneicauda). – Netted at 500 of twigs and placed in saplings. Most nests contained 2 and 1000 m on Mt. Meliau in primary ultrabasic forest. We eggs or 2 chicks. also observed (apparent) family groups collecting nesting material at Ulu Kimanis on 16-17 June 2008. Fruithunter (Chlamydochaera jefferyi). – We observed an adult feeding a recent fl edgling at Kinabalu Park on 12 Chestnut-crested Yuhina (Yuhina everetti). – Netted at April 2002. 1000 m in ultrabasic forest at Meliau.

Temminck’s Babbler (Pellorneum pyrrogenys). – Netted Golden-bellied Gerygone (Gerygone sulphurea). – in ultrabasic forest at 1000 m on Mt. Meliau. Common at 1450 m and recorded up to 1800 m on Trus Madi; also at 1800 m at Ulu Lauhon. A bird was observed Short-tailed Babbler (Malacocincla malaccensis). collecting nesting material in 5 year old Acacia at Sabah – Netted at 1600 m in heavily logged, roadside scrub at Softwoods on 10 July 2005. Ulu Lauhon. Bornean Stubtail (Urosphena whiteheadi). – Netted and Horsfield’s Babbler (Malacocincla sepiarium). – A observed on Trus Madi (1450 – 2200 m) and netted at Ulu specimen in breeding condition was netted in old secondary Lauhon (1700 m). forest at Serinsim: 27 January 2004, testes 8x5 mm. Sunda Bush Warbler (Cettia vulcania). – Two males in Grey-breasted Babbler (Malacopteron albogulare). breeding condition were collected on Trus Madi on 29 July – Netted at Klias FR in peatswamp and at Ulu Rukuruku 2005 (testes 7x5 mm and 5x4 mm) at 1500 m. A young in ultrabasic forest. bird collected at 2350 m had distinctly buffy-yellow, rather than greyish-white, underparts and supercilium. We also Bornean Wren Babbler (Ptilocichla leucogrammica). netted this species at 3270 m on Kinabalu and recorded it – Netted in primary ultrabasic forest at Ulu Rukuruku. at Ulu Lauhon (1700 m).

582 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Mountain Leaf Warber (Phylloscopus trivirgatus). Grey-chested Jungle Flycatcher (Rhinomyias umbratilis). – Recorded from 1450 – 2600 m on Trus Madi. The birds – Common in the peatswamp forest at Klias FR and were the bright yellow form, P. t. sarawacensis. It was also ultrabasic forest at Meliau. netted at Ulu Lauhon (1700 m). Purple-throated Sunbird (Nectarinia sperata). – This Yellow-breasted Warbler (Seicercus montis). – Recorded at species was unusually common in the ultrabasic forest and Mt. Lucia (1050 m) and netted at Ulu Lauhon (1700 m). scrub from 100 - 1000 m on Mt. Meliau.

Yellow-bellied Warbler (Abroscopus superciliaris). Scarlet-breasted Flowerpecker (Prionochilus thoracicus). – Family groups observed and netted at Mt. Meliau (100 – This poor-soil forest specialist was common in the primary – 1000 m) in ultrabasic forest; also observed on Trus Madi and secondary forest at Klias FR, Ulu Rukuruku, and Mt. (1450 m), and Mt. Lucia, and netted on Kinabalu in a Meliau (up to 1000 m). A male with testes 5x4 mm was headquarter’s garden (1600 m). collected at Klias on 8 February 2004.

Rufous-tailed Tailorbird (Orthotomus sericeus). – Netted Plain Sunbird (Anthreptes simplex). – Netted from 100 at Ulu Lauhon (1700m). – 1000 m in ultrabasic forest at Meliau.

Ashy Tailorbird (Orthotomus rufi ceps). – Sympatric with Everett’s White-eye (Zosterops everetti). – Common in O. atrogularis in ultrabasic scrub at Meliau. A bird in large fl ocks at Sabah Softwoods in older groves of Albizia breeding condition was collected at Klias FR on 6 February and Acacia. 2004 (testes 5x3 mm). Bornean Bristlehead (Pityriasis gymnocephala). – Spotted Fantail (Rhipidura perlata). – Netted in ultrabasic Observed in 7 year old Acacia at Sabah Softwoods. It has forest at Ulu Rukuruku and Mt. Meliau. also been seen in Acacia near Sepilok Orangutan Reserve (K. Ickes, pers. comm.). Pied Fantail (Rhipidura javanica). – Recorded in oil palm at Brumas and up to 1100 m on Mt. Lumaku. Tawny-breasted Parrotfi nch (Erythrura hyperythra). – Birds in breeding condition were collected at Klias FR Observed on Trus Madi in primary forest from 1700 – 2350 on 8-9 February 2004 (testes 9x4 mm, yolk 12 mm, m. At 2350 m, a fl ock of ca. 10 individuals was observed respectively). in a coniferous tree. Its call is a high-pitched note with a burry quality and a tremor (very fi nch-like). Compared to Grey-headed Canary Flycatcher (Culicicapa ceylonensis). the illustration in MacKinnon & Phillipps (1993), the birds – Observed on Mt. Lucia, Mt. Lumaku (1100 m), and Ulu had more black on the forehead and only males (or adults) Lauhon (1600 m). had blue on the head. The belly and fl anks were the same green color as the back and wings. The breast was much Verditer Flycatcher (Eumyias thalassina). – Observed at paler than illustrated, much more like the bird depicted in Ulu Kimanis in logged forest (500 m). Robson (2000).

Hill Blue Flycatcher (Cyornis banyumas). – Recent Black Magpie (Platysmurus leucopterus). – Observed in specimen records indicate that this species is fairly common 10 year Albizia at Sabah Softwoods. in submontane forest. LSU has specimens from the Crocker Range National Park headquarters (1000 m) and Mt. Lucia House Crow (Corvus splendens). – Now a common (900 m). The Sabah Museum has specimens from Sayap resident in the Filipino Market in Kota Kinabalu. (1000 m), Ulu Tomani (selectively logged forest southwest of Tenom), Ulu Senagang (near Keningau on the west side of the Crocker Range), and Long Pasia. DISCUSSION

Mugimaki Flycatcher (Ficedula mugimaki). – Netted on Biogeographic patterns. – Recent work in the field Mt. Lumaku (1100 m, 17 January 2005) and Mt. Kinabalu and laboratory has disclosed interesting patterns in the (3270 m, 25 February 2005). An apparent summering male, distribution and biogeography of Bornean birds. The most which was assuming adult plumage, was observed at 2600 important of these patterns relate to the evolution of lowland m on Trus Madi (29 July 2005). endemics in Sabah and montane endemics in Borneo as a whole. Fulvous-chested Jungle-Flycatcher (Rhinomyias olivacea). – Caught at Serinsim and Masikuan. We found In its lowlands, Sabah has endemic bird species that are this species at Serinsim in scrub and old forest, where one complemented by close congeners in other parts of Borneo. would normally expect Grey-chested Jungle Flycatcher (R. An example is the White-fronted Falconet (Microhierax umbratilis). A male at Serinsim was in breeding condition latifrons) in Sabah, which is replaced by the Black-thighed (testes 7x4 mm on 27 January 2004). Falconet (M. fringillarius) elsewhere. Other examples are the Black-and-crimson Pitta (Pitta ussheri) versus Garnet

583 Sheldon et al.: Observations on Sabah birds

Pitta (P. granatina) and the shamas Copsychus stricklandii by paleoclimatic changes (e.g., Bird et al., 2005; Mann, and C. malabaricus. There are also numerous lowland 2008). Perhaps most importantly, there may be genetic subspecies endemic to Sabah, such as Copsychus saularis tension zones that inhibit the eastward diffusion of genes by adamsi discussed above (Mann, 2008:18, provides an reducing the inherent fi tness of hybrids (Barton & Hewitt, extensive list). Molecular comparisons suggest that some 1985). This reduction in gene fl ow would not necessarily of Sabah’s endemic lowland bird populations may represent be related to environmental conditions, nor would it occur remnants of native Bornean taxa that have been replaced on in the same place for all taxa, thus making the zone diffi cult the rest of the island by closely related, relatively recent to fi nd without extensive molecular comparisons. Detailed invaders from the west (Moyle et al., 2005; Sheldon et exploration and examination of the molecular population al., 2009b). These invaders would have colonized Borneo genetic composition of taxa throughout Borneo and from Sumatra, Malaya, or mainland Asia via land bridges surrounding areas will be required to identify all the forces exposed during lowered sea levels in glacial periods of that have created Sabah’s distinct lowland faunas. the mid-Pleistocene (Heaney, 1986; Inger & Voris, 2001). This scenario is suggested not only by the morphological In the mountains of Borneo, a different biogeographic story distinctiveness of Sabah’s populations, but also by a genetic is emerging for birds. At least some montane endemics dichotomy in Borneo; some bird populations from western are more closely related to congeners in Java than to Borneo are closer genetically to populations in Malaya and similar taxa in the lowlands of Borneo. Molecular and Sumatra than to those in Sabah. This is true of several morphological comparisons have shown that the montane taxa, including forktails (Enicurus leschenaulti; Moyle et Bornean Swiftlet, Collocalia dodgei, is more closely related al., 2005), magpie-robins (Copsychus saularis; Sheldon et to C. linchi of Java than to C. esculenta in the lowlands al., 2009b), and shamas (C. malabaricus; Sheldon et al. in of Borneo (Somadikarta, 1986; Moyle et al., 2008). preparation). Previously both taxa were considered parapatric subspecies of C. esculenta. In a similar case, the Bornean Forktail The hypothesis that some of Sabah’s lowland birds are relicts (Enicurus borneensis) appears to be more closely related to of once widely distributed populations, and that western E. leschenaulti leschenaulti of Java than to E. l. frontalis in invaders are moving eastward and may eventually overrun the lowlands of Borneo (Moyle et al., 2005). (Wells, 2007, Sabah, must be tempered by the observation that a variety of mentioned alternative relationships for the two taxa based ecologically disparate organisms—with presumably different on juvenile plumages, but provided no details.) dispersal capabilities—share the taxic discontinuity between Sabah and the rest of Borneo. This is true of birds (e.g., Based on morphological comparisons, Davison (1999) canopy falconets, terrestrial pittas, forest shamas, and open- argued that Borneo’s montane Streaky-breasted Spiderhunter country magpie-robins) and also mammals; for example, (Arachnothera affi nis everetti) is most closely related to the tree-shrews, bats, and various rodents exhibit population, Javan form (A. a. affi nis), whereas its lowland counterpart, subspecies, and species discontinuities between Sabah and A. modesta concolor, is the same subspecies as the form the rest of Borneo (Medway, 1977; Payne et al., 1985; Han, in Sumatra. An interesting twist on this example is that 2000; Gorog et al., 2004; S. Murray, pers. comm., M. T. it supports both the explanation for lowland patterns of Abdullah, pers. comm.). It is unlikely that such distinct endemism in Sabah and the montane pattern of endemism groups would invade from the west at the same time and in Borneo. Arachnothera modesta is a fairly recent invader move across Borneo at the same rate so that all are poised from Sumatra, judging from the similarity of the Sumatran at the same moment on the border of Sabah. Moreover, we and Bornean forms. It occurs in most, but not all, of the have evidence that Copsychus saularis and C. malabaricus lowlands of Borneo. Where A. modesta occurs in lowland invaded Borneo about a million years ago (Sheldon et al., areas, it is replaced in the mountains by A. affi nis. However, 2009b; in preparation), certainly long enough for their genes A. modesta is not found in Sabah. In Sabah, the erstwhile to have diffused throughout the entire island. montane form, A. affinis, occurs in both the mountains and lowlands. Presumably, in the future, if A. modesta A variety of paleontological, ecological, physiographic, invades Sabah, A. affi nis will become restricted to higher and genetic forces probably have played a role in shaping elevations. Sabah’s distinctive lowland bird and mammal faunas. Sabah is a small, almost peninsular, part of Borneo that is The Bornean Leafbird (Chloropsis kinabaluensis) presents adjacent to Palawan and the Sulu Archipelago in the north a case remarkably like the spiderhunter. Previously, it was and bordered by fairly substantial mountains in the west considered to be a parapatric subspecies of the widespread (Maligan and Crocker ranges) and south (Maitland and Witti lowland species, C. cochinchinensis (Smythies, 1999). ranges). Philippine taxa undoubtedly have invaded Sabah Wells et al. (2003) have now separated it as an endemic periodically and may have hybridized with indigenous taxa, Bornean species. We predict that genetic comparisons of adding to their distinctiveness. Lowland populations to these taxa will show that the lowland C. cochinchinensis is the west and south of Sabah probably have been deterred a relatively recent invader from western Sundaland (as it from invading the state by its bordering mountains. does not occur in Sabah) and the montane C. kinabaluensis Potential invaders may also have been influenced by will be most closely related to the Javan taxon, C. altered distributions of forest and other habitats caused cochinchinensis nigricollis.

584 THE RAFFLES BULLETIN OF ZOOLOGY 2009

Other patterns. – Our surveys disclosed some other ACKNOWLEDGEMENTS interesting patterns in Sabah’s birds. A remarkable number of species was breeding at Klias Forest Reserve in early For help, we thank Matius Anghaus, Junaidi Atim, Alim February 2004. Groups in breeding condition included: Biun, Benedict Butit, Robert Chong, Patrick Francis, pigeons (Treron vernans), cuckoos (Cacomantis merulinus), Mansuit Gamalang, Dency Flenny Gawin, Tony Greer, woodpeckers (Sasia abnormis), swallows (Hirundo Cheryl Haines, Safrie Hatimin, Aminah Imat, Freddie tahitica), bulbuls (Pycnonotus goiavier, P. simplex, and Julus, Alison Kabi, Mohd. Hattah Jaafar, Clifford James, Setornis criniger), thrushes (Trichixos pyrrhopygus and George Jonis, S. P. Kenney, Kohming, David Kung, Johnny Copsychus saularis), babblers (Malacopteron albogulare, Lapidin, Ben Marks, Iggy Olim Marsh, Martinah Latim, Macronous ptilosis, Stachyris nigricollis, S. maculata, Julia Raddatz, Nor Salmizar, Rashid Abdul Samad, Suati and S. erythroptera), warblers (Orthotomus ruficeps), Selimon, Majim Silim, David Simpongul, Maureen Tapuong, fl ycatchers (Rhipidura javanica, Rhinomyias umbratilis, and Dominique Tinggoh, Wilfred Torimoh, Gwendolyn Vu, Hypothymis azurea), fl owerpeckers (Prionochilus thoracicus, Paul Yambun and Anna Wong. Geoffrey Davison helped P. xanthopygius, and Dicaeum trigonostigma), sunbirds improve the discussion of the rationale for lowland bird (Anthreptes singalensis, Hypogramma hypogrammicum, endemicity in Sabah. For permission to undertake research and Aethopyga siparaja), and waxbills (Lonchura malacca). in Malaysia, we thank the Prime Minister’s Department and Wells (1976) and Sheldon et al. (2001) previously reported Sabah Chief Minister’s Department. We also thank Sabah congregations of parrots, pigeons, bulbuls, and other Wildlife Department, Sabah Parks, Sabah Museum, and frugivores breeding along Sabah’s southwestern coast in late Sabah Softwoods Sdn. Bhd. for extensive logistic support. winter months, when fruit is plentiful. Numerous species The Macaulay Library at Cornell University loaned were also found breeding at Serinsim in January, as reported recording equipment and archived recordings. Funding by Sheldon et al. (2009c). was supplied by the American Museum of Natural History, Kansas University Museum of Natural History, Louisiana Our survey at Ulu Lauhon in the Meligan Range produced State University Museum of Natural Science, the Coypu several remarkable elevational records. This site, at 1700 Foundation, and the U.S. National Science Foundation – 1800 m, had recently been cleared for the development (DEB-0228688). of Acacia mangium plantation. Thus, an opportunity was created for lowland scrub-dwelling birds to travel high into the mountains and mix with resident montane species. LITERATURE CITED At 1700 m, such lowland species as Pycnonotus goiavier, P. simplex, P. plumosus, Malacocincla malaccense, Barton, N. H. & G. M. Hewitt, 1985. Analysis of hybrid zones. Macronous gularis, and Orthotomus sericeus occurred Annual Review of Ecology and Systematics, 16: 113–148. alongside the montane species expected at this elevation, Bird, M. I., D. Taylor & C. Hunt, 2005. Palaeoenvironments such as Pycnonotus flavescens, Alophoixus ochraceus, of insular Southeast Asia during the last glacial period: a Hemixos fl avala, Stachyris nigriceps, Cettia vulcania, and savanna corridor in Sundaland? Quaternary Science Reviews, Orthotomus cucullatus. Although recent logging seems to 24: 2228–2242. have been the cause of these high elevation records, the Chen, I. C., H. J. Shiu, S. Benedick, J. D. Holloway, V. K. Cheye, possibility that temperature changes from global warming H. S. Barlow, J. K. Hill & C. D. Thomas, 2009. Elevation increases in assemblages over 42 years on a tropical had some influence (Colwell et al., 2008) should be mountain. Proceedings of the National Academy of Sciences considered in light of the recent discovery of elevational of the United States of America, 106: 1479–1483. shifts in moths on Mt. Kinabalu (Chen et al., 2009). Collar, N. J., 2005. Family Turdidae (thrushes). In: del Hoyo, J., A. Elliott & D. Christie (eds.), Handbook of the birds of the Surveys in the ultrabasic forests of eastern Sabah, at Ulu world, Vol. 10. Lynx Edicions, Barcelona. Pp. 514–807. Rukuruku and Mt. Meliau, revealed the expected poor- Colwell, R. K., G. Brehm, C. L. Cardelus, A. C. Gilman & J. soil specialists Malacopteron albogulare and Prionochilus T. Longino, 2008. Global warming, elevational range shifts, thoracicus. We did not encounter Setornis criniger at those and lowland biotic attrition in the wet tropics. Science, 322: sites, however. It appears largely restricted to peatswamp 258–261. in Sabah (Sheldon, 1987). The forest at Ulu Rukuruku also Cranbrook, E., S. Somadikarta, G. W. H. Davison, C. K. Lim & yielded Stachyris leucotis, a scarce species, and the Bornean H. S. Möller, 2005. The Kinabalu Linchi swiftlet, Collocalia endemic Ptilocichla leucogrammica. On Mt. Meliau (1336 linchi dodgei Richmond: an unresolved puzzle. Sabah Society m), we were particularly interested in investigating the Journal, 21: 189–200. occurrence of montane species. The 1956 British Museum Curran, L. M., S. N. Trigg, A. K. McDonald, D. Astiani, Y. expedition failed to fi nd any montane birds there (R. Sims, M. Hardiono, P. Siregar, I. Caniago & E. Kasischke, 2004. unpublished manuscript), but we expected them because of Lowland forest loss in protected areas of Indonesian Borneo. the proximity of Mt. Meliau to the Crocker Range and the Science, 303: 1000–1003. presence of such species on several isolated peaks in Sabah Davies, G. & J. Payne, 1982. A faunal survey of Sabah. IUCN/ (e.g., Mt. Lucia). Although we did not spend much time at WWF Project No. 1692. Kuala Lumpur, World Wildlife Fund high elevation, we confi rmed the presence of at least two (Malaysia). pp. montane species on Meliau, Pellorneum pyrrogenys and Davison, G. W. H., 1999. Notes on the taxonomy of some Bornean Yuhina everetti. Undoubtedly others occur there as well. birds. Sarawak Museum Journal., 54: 289–299.

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Gawin, D. F. A., 2006. Patterns of variation in the mountain forktail Enicurus leschenaulti in Borneo. Journal of Avian blackeye (Chlorocharis emiliae) in selected mountain tops Biology, 36: 96–101. in Sabah and Sarawak, Malaysia. M.S. thesis, Universiti Moyle, R. G. & A. Wong, 2002. The lower montane avifauna of Malaysia Sarawak, Kuching, Sarawak. 164 pp. Mt. Trus Madi. Raffl es Bulletin of Zoology, 50: 199–204. Gorog, A. J., M. H. Sinaga & M. D. Engstrom, 2004. Vicariance Payne, J., C. M. Francis & K. Phillipps, 1985. A fi eld guide to or dispersal? Historical biogeography of three Sunda shelf the mammals of Borneo. Kuala Lumpur, Sabah Society, Kota murine rodents (Maxomys surifer, Leopoldamys sabanus and Kinabalu, Sabah; and World Wildlife Fund Malaysia. Maxomys whiteheadi). Biological Journal of the Linnean Society, 81: 91–109. Peters, J. L., 1940. Birds from Mt. Kina Balu, North Borneo. Bulletin of the Museum of Comparative Zoology., 87: Haines, C. L., 2007. Comparative phylogeography of four montane 195–211. bird species in Sabah, Malaysian Borneo. M.S. thesis, Louisiana State University, Baton Rouge, Louisiana. 51 pp. Robson, C., 2000. A guide to the birds of Southeast Asia. Princeton, New Jersey, Princeton University Press. 504 pp. Han, K. H., 2000. Phylogeny and biogeography of tree shrews (Scandentia: Tupaiidae). Ph.D. dissertation, Louisiana State Sheldon, F. H., 1987. Habitat preferences of the Hook-billed University, Baton Rouge, Louisiana. 88 pp. Bulbul (Setornis criniger) and the White-throated Babbler (Malacopteron albogulare) in Borneo. Forktail, 3: 17–25. Heaney, L. R., 1986. Biogeography of mammals in SE Asia: estimates of rates of colonization, extinction and speciation. Sheldon, F. H., G. Davison, B. D. Marks, A. Wong & R. G. Biological Journal of the Linnean Society, 28: 127–165. Moyle, 2009a. Birds in Peatswamp Forest at Klias Forest Reserve and Environs, Sabah, Malaysia. Sabah Parks Nature Holmes, D. A., 1997. Kalimantan bird report - 2. Kukila, 9: Journal, In press. 141–169. Sheldon, F. H. & C. M. Francis, 1985. The birds and mammals of Inger, R. F. & H. K. Voris, 2001. The biogeographical relations of Mount Trus Madi, Sabah. Sabah Society Journal, 8: 77–88. the frogs and snakes of Sundaland. Journal of Biogeography, 28: 863–891. Sheldon, F. H., D. J. Lohman, H. C. Lim, F. Zou, S. M. Goodman, D. M. Prawiradilaga, K. Winker, T. M. Braile & R. G. Moyle, Kiew, B. H., 1977. A survey of the proposed Sungai Danum 2009b. Phylogeography of the magpie-robin species complex National Park, Sabah. Kuala Lumpur, World Wildlife Fund (Aves: Turdidae: Copsychus) reveals a Philippine species and (Malaysia). 73 pp. novel dispersal patterns in the Indian Ocean and S. E. Asia. Koh, L. P. & D. S. Wilcove, 2008. Is oil palm agriculture really Journal of Biogeography, 36: 1070–1083. destroying tropical biodiversity. Conservation Letters, 1: Sheldon, F. H., R. G. Moyle & J. Kennard, 2001. Ornithology 60–64. of Sabah: history, gazetteer, annotated checklist, and MacKinnon, J. & K. Phillipps, 1993. A fi eld guide to the birds of bibliography. Ornithological Monographs., 52: 1–285. Borneo, Sumatra, Java, and Bali. Oxford, Oxford University Sheldon, F. H., J. Nais, M. Lakim, B. D. Marks & R. G. Moyle, Press. 491 pp. 2009c. A Survey of Birds at Serinsim Substation, Kinabalu Mann, C. F., 2008. The birds of Borneo, an annotated checklist. Park. Sabah Parks Nature Journal, (in press). Peterborough, United Kingdom, British Ornithologists’ Union Smythies, B. E., 1957. An annotated checklist of the birds of and British Ornithologists’ Club. 440 pp. Borneo. Sarawak Museum Journal., 7: 523–818. Marsh, C. & A. G. Greer, 1992. Forest land-use in Sabah, Smythies, B. E., 1999. The birds of Borneo, fourth edition. Kota Malaysia: and introduction to Danum Valley. Philosophical Kinabalu, Malaysia, Natural History Publications. 853 pp. Transactions of the Royal Society B Biological Sciences, 335: 331–339. Sodhi, N. S., L. P. Koh, B. W. Brook & P. K. L. Ng, 2004. Southeast Asian biodiversity: an impending disaster. Trends McMorrow, J. & M. A. Talip, 2001. Decline of forest area in in Ecology and Evolution, 19: 654–660. Sabah, Malaysia: Relationship to state policies, land code and land capability. Global Environmental Change-Human and Somadikarta, S., 1986. Collocalia linchi Horsfi eld & Moore--a Policy Dimensions, 11: 217–230. revision. Bull. Brit. Ornith. Club, 106: 32–40. Medway, L., 1977. Mammals of Borneo. Monogr Malay Br Roy Styring, A. R., F. H. Sheldon, R. Ragai & J. Unggang, 2007. Asiatic Soc, 7: 1–172. Determining the diversity of birds in Bornean tree plantations. In: Stuebing, R., J. Unggang, J. Ferner, J. Ferner, B. Giman Mees, G. F., 1986. A list of the birds recorded from Bangka Island, & K. K. Ping (eds.), Proceedings of the Regional Conference Indonesia. Zoologische Verhandelingen Leiden, 232: 1–176. of Biodiversity Conservation in Tropical Planted Forests in Mitra, S. & F. H. Sheldon, 1993. Use of an exotic tree plantation Southeast Asia, 15-18 January 2007. Forest Department, by Bornean lowland forest birds. Auk, 110: 529–540. Sarawak Forestry Corporation, and Grand Perfect Sdn Bhd, Moyle, R. G., 2003. Bird diversity within Sabah Parks: A survey Kuching, Sarawak, Malaysia. Pp. 138–151. of Mt. Kinabalu, the Crocker Range, and Tawau Hills. Sabah Thomas, P., F. K. C. Lo & A. J. Heburn, 1976. The land capability Parks Nature Journal, 6: 103–116. classifi cation of Sabah. Land Resources Division, Ministry of Moyle, R. G., C. E. Filardi, C. E. Smith & J. M. Diamond, Overseas Development, Surbiton, United Kingdom. 2009. Explosive Pleistocene diversifi cation and hemispheric Wells, D. R., 1976. Some bird communities in western Sabah, expansion of a “great speciator”. Proceedings of the National with distributional records, March 1975. Sarawak Museum Academy of Sciences of the United States of America, 106: Journal., 24: 277–286. 1863–1868. Wells, D. R., 2007. The birds of the Thai-Malay Peninsula, volume Moyle, R. G., P. A. Hosner, J. Nais, M. Lakim & F. H. Sheldon, 2, passerines. London, Christopher Helm. 800 pp. 2008. Taxonomic status of the Kinabalu ‘linchi’ swiftlet. Wells, D. R., E. C. Dickinson & R. W. R. J. Dekker, 2003. Bulletin of the British Ornithologists’ Club, 128: 94–100. Systematic notes on Asian birds. 37. A preliminary review of Moyle, R. G., M. Schilthuizen, M. A. Rahman & F. H. Sheldon, the Chloropseidae and Irenidae. Zoologische Verhandelingen 2005. Molecular phylogenetic analysis of the white-crowned Leiden, 344: 25–42.

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THE RAFFLES BULLETIN OF ZOOLOGY 2009 57(2): 567 Date of Publication: 31 Aug.2009 © National University of Singapore

CORRIGENDUM

Ngoc-Ho, N. & M. de Saint Laurent, 2009. The genus Thalassina Latreille, 1806 (Crustacea: Thalassinidea: Thalassinidae). Raffl es Bulletin of Zoology, Supplement No. 20: 121–158.

An error occured resulting in the captions for Fig. 16B and 16C being inverted.

Figure 16B is Thalassina squamifera De Man, 1915. Figure 16C is Thalassina spinosa, new species.

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