/\ccords o(tlic Wcstcrn AlIs/m/wlI MlIs1'l1l1l24: 421428 (2008),

A new species of the freshwater tanaidacean genus Pseudohalmyrapseudes (Crustacea: : Parapseudidae) from Sulawesi

Roger N. Bamber The Natural History Museum, Cromwell Road, London SW? 5BI), United Kingdom, E-mail: [email protected]

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Abstract -A new species of the freshwater apseudomorph tanaidacean genus Psclldohll/lIlympsclldcs is described from Dadeleang Cave in Sulawesi: Psclldolill/lIlyrapsclldcs 1i1l1l1lCi, The range of morphological differences between the three known species of the genus is tabulated, Allopatric speciation between taxa inevitably isolated owing to their freshwater habitat is discussed, as are the links with the closely-related genus HII/Ili1jmpsclldcs,

INTRODUCTION Dadeleang Cave (referred to as Gua Deddelean 1 Freshwater tanaidaceans are rare (see Larsen - SLl in the report by Brouquisse 2002) comprises and Hansknecht 2004, for a brief review of the a main gallery about 50 m in length, with a mud relevant literature), The most widely recorded floor, down the centre of which runs a small is the pantropical-subtropical tanaid Sinelobus stream, one of the sources of the Sungai Salenrang stanfordi (Richardson 1901), a euryokous species on the western border of the Maros massif. There recorded from estuaries, from reduced salinities is a shallow pool outside the cave entrance held in mangrove systems, and in fully freshwater back by a small concrete dam, The gallery extends habitats, including at an altitude of 823 m [sic] until a siphon is reached and within the gallery on St Helena (Monod 1977; see also Stephensen the stream widens into larger pools at intervals, 1936; Gardiner 1975), A further freshwater There is a narrow, flooded gallery parallel to the tanaidomorph, recorded only once, is the main gallery, The tanaidaceans were collected in nototanaid Androtanais beebei (Van Name 1925), this parallel gallery, The new species is described found in a catfish stomach in British Guiana below, (Van Name 1925), Some other estuarine species may extend into freshwater temporarily, most MATERIAL AND METHODS notably the leptocheIiid Heterotanais oerstedi Specimens were collected from the cave by (Kroyer 1842), which has been recorded from sites Damia Jaume (IMEDEA, Mallorca, Spain) using ~ where salinities drop as low as O'X,o at Iow tide or fine-mesh hand net and by capturing individuals seasonally. from the surface water film on the mud using a Apseudomorph tanaidaceans from reduced paint brush, Material was examined using a Wild salinity waters are also rare, The genus M3Z Kombistereo microscope and a Reichert Halmyrapseudes Bacescu and Gutu 1974 is Zetoplan compound microscope; drawings were known from seven species, all from brackish made using a camera lucida, Measurements are waters (as Iow as 10'X,o where salinity was axial, measured in dorsal aspect for the body, in recorded: see Bamber et al. 2002), Th~ only lateral aspect for the appendages, Morphological genus of apseudomorph tanaidacean recorde~1 terminology is as in Bamber and Sheader (2005), from freshwater habitats is the closelv-related including the use of the term "segments" for Pseudohalmljrapseudes, erected by' Larsen serially repetitive body parts, notably those of the and HanskI~echt (2004) for their ne'w species antennular and antennal flagella and uropod rami P. aquadulcis from a freshwater spring in Northern which are without independent musculature, The Territory, Australia (near Darwin), and to which type material has been lodged at the Museum they moved Apseudes mussallensis Shiino 1965; P. Zoologicum Bogoriense (MZB) and the Natural mussaucnsis was recorded from a "brackish" lake History Museum, London (NHM), on Mussau Island, Bismarck Archipelago (Shiino 1965), SYSTEMATICS In 2007, during sampling of Gua Dadeleang, a Suborder Apseudomorpha Sieg 1980 very muddy cave in Sulawesi, Indonesia, 8.7 km from the coast, nine specimens of a distinct, third Superfamily Apseudoidea Leach 1814 species of Pselldohalmyrapsclldes were collected, Family Parapseudidae Gutu 1981 422 R.N. Bamber

Genus Pseudo1lalmyrapseudes Larsen and article 0.4 times as long as first, some distal outer Hansknecht 2004 setae longer than article; third article half as long as second, with shorter inner and longer Type species outer distal setae; fourth article 0.4 times as long Pselldohalmyrapselldes aqlladlllcis Larsen and as third, naked. Main tlagellum of nine poorly Hansknecht 2004, by original designation. distinguished segments, accessory tlagellum of five segments. Pseudo1lalmyrapseudes linnaei sp. novo Antenna (Figure 1C) proximal peduncle article Figures 1-3 bearing rounded inner apophysis almost reaching distal margin of second article, with five outer Material examined setae; second article just shorter than first, Holotype bearing slender squama with three distal setae, Indonesia: Sulawesi: 2 with oostegites, Gua smaller inner distal seta and longer seta at base Oadeleang, Kab. Pangkajene: co-ordinates of cave of squama; third peduncle article one-third as entrance: 4°55'33"S, 119°36'36"E, 6 September 2007, long as second, with long inner distal seta; fourth O. Jaume (MZB.Cru 1686). and fifth articles as long as second, almost fused. Flagellum of four segments. Paratypes Labrum rounded, sparsely setose. Left mandible Indonesia: Sulawesi: 1 subadult 0 (MZB.Cru (Figure lE) with four cusps on pars incisiva, 1687), 3 2 (MZB.Cru 1688), 3 2 (NHM.2007.964­ four cusps on narrow lacinia mobilis, setiferous 966), 1 2 with oostegites, dissected, same sample lobe with six compound setae, pars molaris as holotype. round, blunt, with marginal setules; palp of three articles, proximal article with three long Description inner setae, second article longest, half as long as whole palp, with ten inner setae largely in Female two rows; third article with six progressively Body (Figure lA) elongate, poorly calcified, longer setae in distal half, distal setae longer than transparent in preserved material; holotype article. Right mandible as left but without lacinia 5.8 mm long (tip of rostrum to posterior mobilis, proximal palp article with four setae. of pleotelson), nine times as long as wide. Labium (Figure 10) angular, outer marginal finely Cephalothorax slightly narrower anteriorly, as denticulate, inner margin setose, palp marginally long as wide, with smoothly rounded rostrum; setose and with single distal spine. Maxillule single lateral seta behind each ocular lobe, longer (Figure IF) inner endite with four setose distal simple lateral seta anterior to each branchial setae and outer apophysis, outer endite with 11 chamber. Eyelobes present, rounded, eyes present distal spines and setose margins; palp of two as group of brown-pigmented ocelli. Epistome articles, distally with five simple setae. Maxilla absent. Six free pereonites; pereonite 1 half as damaged in preparation, with rostral row of 3 long as cephalon, pereonite 2 just shorter than simple setae, fixed endite with trifurcate, simple pereonite 1, both with convex lateral margins; and bifurcate setal groups. Maxilliped (Figure pereonites 3 to 5 subequal, 1.4 times as long as 11) basis with three inner distal setae reaching pereonite 1, with midlateral indentation giving a. distal margin of second palp article, outer distal bilobed outline; pereonite 6 as long as pereonite corner finely denticulate; proximal palp article 1, with bilobed outline (all pereonites respectively with simple outer strong seta, inner margin with 1.9, 1.6, 1.15, 1.15, 1.0 and 1.4 times as wide as single distal seta reaching distal margin of second long). All pereonites with sparse anterolateral palp article; second article with one strong distal and posterolateral simple setae. Pleon one third seta on outer margin, inner margin with two length of body, with five free subequal pleonites rows of ten curved shorter setae, ventral row of bearing pleopods; each pleonite about half as long four longer simple setae; third article with one as pereonite 6 and three times as wide as long, distal and eight inner marginal simple setae; laterally extended into pointed epimera bearing 5 distal article with five simple inner-marginal to 8 plumose setae, dorsally with sparse plumose and distal setae; endite (Figure 1H) with simple, setae. Pleotelson subrectangular, 0.7 times as long slender caudo-distal seta, simple distal spines, as all five pleonites together, 1.7 times as long as three coupling-hooks. Epignath (Figure 1G) large, wide, with plumose lateral and dorsal setae. rounded, setose inner lobe conspicuous, distal Antennule (Figure 18) proximal peduncle article spine setose. 3.5 times as long as wide, with simple setae on Cheliped (Figure 2A) with compact basis inner and outer margins and penicillate setae in twice as long as wide, with long midventral seta proximal half of outer margin; second peduncle exceeding distal tip of basis, five ventrodistal New freshwater tanaidacean from Sulawesi 423

Figure 1 lillllilCl sp. nov., A, holotype, dorsal; B, antennule; C antenna; D, labium; E, left mandible; F maxillule; C, epignath; H, maxilliped endite; I, maxilliped. Scale line = 1.5 mm for A, 0.4 mm for Band C, 0.2 mm for D to I. setae; exopod ite of three articles, d ista I article of small, marginally spinulose teeth on cutting with four plumose setae. Merus subrectangular, edge; moveable finger (dactylus), curved; unguis vent rally with groups of three proximal and exceeding distal spine of fixed finger. three distal setae, dorsally with single simple Pereopod 1 (Figure 2B) with stout basis 2.5 times seta. Carpus elongate, 2.9 times as long as wide, as long as wide, dorsal margin bearing two small with seven ventral marginal setae, outer mesial setae, ventral margin with three simple setae, row of 14 simple setae, inner mesial row of eight ventrod ista1 tu ft of five si mple setae; exopod ite of simple setae. Propodus compact, setose as figured, three articles, distal article with six plumose setae. fixed finger with four ventral setae, saw-like row Ischium short, with two ventrodistal setae. Merus 424 R.N. Bamber

Figure 2 Pseudohalmyrapseudes linnaei sp. nov., A, cheliped; B, pereopod 1, C, pereopod 2; 0, pleopod. Scale line = 0.3 mm.

0.4 times as long as basis, dorsally with subdistal times as long as propodus, with fine ventral pair of longer, distally-tapering setae, distal tuft denticulations and ventrodistal seta, unguis short, of three setae; ventral margin with numerous half as long as dactylus. All marginal spines with distally-tapering setae and ventrodistal spine. finely setulose tips. Carpus subequal in length to merus, numerous Pereopod 2 (Figure 2C) basis compact, 2.6 times distally-tapering marginal spines dorsally and as long as wide, with five dorsal and three ventral ventrally, one dorsodistal spine and two ventral marginal setae, and four simple ventrodistal setae; spines. Propodus shorter than carpus, with three ischium with three ventrodistal setae. Merus, ventral and two dorsal spines, interspersed by carpus and propodus bearing distally-tapering distally-tapering setae. Dactylus curved, 0.3 New freshwater tanaidacean from Sulawesi 425

Figure 3 PsclIdo!lilllllyrapsclIdcs lillllilCi sp. nov., A, pereopod Cl; 13, pereopod 4; C, pereopod5, D; pereopod 6; E, uropod, Scale line 03 mm,

setae, Merus 0.7 times as long as carpus, with l'ereopod 4 (Figure 3B) basis with single slender ventrodistal spine; carpus with midventral dorsal marginal seta, midventral penicillate and ventrodistal slender spines; propodus seta; carpus twice as long as merus, with distal 1,2 times as long as carpus, with dorsod istal, crown of numerous tapering setae and slender midventral and ventrodistal slender spines; spines; propodus with five denticulate distal dactylus and unguis slender, together 0,8 times as spines; dactylus plus unguis 0.4 times as long as long as propodus, dactylus with fine ventrodistal propodus, 0.4 times as long as dactylus plus claw seta. Pereopod 3 (Figure 3A) similar to pereopod of pereopods 3 or 5. 2, but with fewer setae on basis, merus 0,6 times l'ereopod 5 (Figure 3C) similar to pereopod 3, as long as ca rpus, 426 R.N. Bamber

I· Etymology II~ 5'. 0, • . This species is named in honour of Carolus o I Linn~au~, in commemoration of the tercentenary of hIS blfth and the 250th anniversary of the publication of the 10th edition of Systema Naturae.

Remarks ..,.... The three species of Pseudolzalmyrapseudes are very similar to each other. Larsen and Hansknecht (2004) listed a number of differences between P. mussauensis and P. i aquadulcis, which are expanded upon herein, although distinctions of the male are not feasible for the present species as the male of P. limzaei was not mature. The ~onspicuous difference between the three species IS the shape of the inner apophysis of the proximal antennal peduncle article, that of P. mussauensis being triangular, exceeding the distal margin of the second peduncle article, and with outer and distal marginal setae; the apophysis of P. aquadulcis is rectangular, not quite reaching the distal margin of the second peduncle article, with distal setae on the straight apex; the apophysis of P. linnaei is rounded, again not quite reaching the distal margin o~ the second peduncle article, with setae evenly dIspersed around the outer margin. The third antennal article is much shorter proportionately in P. linnaei, although it may have been present but Figure 4 D is t rib uti 0 n 0 f k now n s p e c ie s 0 f Pseudohalmyrapseudes: 1 P. mussauensis; 2 ­ unobserved in P. aquadulcis, otherwise it is difficult P. aquadulcis; 3 - P. linnaei. to interpret the inevitable five peduncle articles. The poor articulation between articles 4 and 5 of but basis sparsely setose. Pereopod 6 (Figure 3D) the antenna in P. linnaei, in contrast with the clear basis with six plumose dorsal setae, eight ventral articulation in the other species, was present in all marginal setae each plumose over its proximal specimens (as was also the case for the antennule half, and four distally-tapering ventrodistal setae; main flagellum and uropod endopod). The ischium dorsally naked; merus with six dorsal conformation of the epignath appears to be quite plumose setae, six ventral distally-tapering setae; distinct between the three species, that of P. linnaei carpus with eight dorsal plumose setae, small being almost circular, that of P. mussauensis being ventrodistal spine; propodus with proximal oval, while that of P. aquadulcis is unusually ventral slender spine, marginal row of 22 elongate, and without setae on either the inner lobe compound leaf-like spines, dactylus and unguis or the distal spine. Finally, P. linnaei has plumose as pereopod 3. pleonite setae restricted to the lateral epimera, while there are almost none on the dorsal surface Pleopod (Figure 20) biramous, basis with three of the pleotelson, while in both of the other species dorsal plumose setae, ventral margin naked; these setae extend onto the dorsal surfaces of the exopod longer than endopod, outer proximal seta pleonites and are numerous on the dorsal surface with trifurcate tip; endopod with single proximal of the pleotelson. outer seta; all setae plumose. A range of other differences between the Uropod (Figure 3E) biramous, basis with three species is shown in Table 1. Pseudolzalmyr­ two outer and one long inner distal plumose apseudes aquadulcis is distinct from the other hvo setae; endopod longer than basis, of one short species in having 4 segments in the antennule and three longer segments; exopod showing accessory flagellum (5 in the other two), only two poor segmentation, of perhaps nine or ten setae on the proximal article of the mandibular segments, longer than pleotelson and pleonite five palp (3 or 4 in the oth"er two), apparently no combined. distal spine on the labial palp (1 in P. linnaei, 2 in Subadult male 2.8 mm long, similar to female, P. mussauensis), only 4 plumose setae on the exopod with penial tubercle ventrally on pereonite 6. of pereopod 1 (6 in the other two), a plumose seta Paratype females 5.7 (female with oostegites), 4.8, on the ischium of pereopod 6 (none in the other 4.7, 4.3, 4.0, 4.0 and 3.9 mm long. New freshwater tanaidacean from Sulawesi 427

Table 1 Distinctions between the three described species of I':;C11 dol III I1ll1/rav,;clIdc.'; , E lillllaei p, aqlladlllcis E mllssallcllsis Pleotelson length v pleonites 1~5 length 0] x >0]5 <0,6 Antennule accessory flagellum, female 5 segments 4 segments 5 segments Antenna apophysis on proximal article Round, setae Rectangular, setae Triangular. setae evenly marginal distal on straight apex evenly marginal Maxilliped basis outer-distal corner DentiCLllate Denticulate Smooth Maxilliped basis distal setae 3 3 2 Dactylus + unguis pereopod 4 0,4 x length of those 0,4 x length of those > 05 length of those of P3 and 1'5 of 1'3 and 1'5 of 1'3 and 1'5 Cephalothorax length: width 1.0 1.1 1.2 Mandible palp, setae on proximal article 3 or 4 2 3 Labial palp distal spines o 2 Epignath Round; s('lose Elongate; naked Oval; setose Pereopod 1, distal exopod article setae 6 4 6 Pereopod 1 dactylus Denticulate Not denticulate Denticulate Pereopod 6, ischium plumose setae o o Pleopod endopod outer margin 1 proximal seta Naked Naked Uropod basis plumose setae 3 5

two), no denticulation on the dactylus of pereopod southwestern Sulawesi, off the FICHes Sea, 1 (denticulate in the other two) and only one P. aquadulcis further south from near Darwin, plumose distal seta on the uropod basis (3 or more Australia, off the Timor Sea, and P. mussauCllsis in the other two species), Larsen and Hansknecht further east from Mussau Island in the northern (2004) describe only nine distal spines on the outer Melanesian waters of the Bismarck Archipelago. endite of the maxillule, but this is likely to be a It is to be expected that further species may be miscount, both of the other species having 11. present isolated on other islands of this region. As well as the dorsal pleon setation, and The closely-related genus Halmympseudes shows antennule and epignath features, P. lillllaei differs a different zoogeography (Bamber et al. 2(02), from P. lI1ussauellsis in having a denticulate three of the known species being found in the outer-distal corner to the maxilliped basis Caribbean and Gulf of Mexico, the other four (smooth in P. lI1ussauellsis), three distal setae on occurring around the Indian Ocean. Soemodinoto the maxilliped basis (2), one distal spine on the et al. (1995) recorded large numbers of a species labial palp (2), and a proximal seta on the pleopod attributed to H. killaiyellsis Balasubrahmanyan endopod outer margin (naked in both of the other 1959 from an estuary in Java, although that species). P. lI1ussauellsis has a proportionately material has been lost (A. Soemodinoto, pers. shorter pleotelson, and a proportionately longer comm.): rediscovery of this taxon would be cephalothorax. I believe that the short proximal valuable as a putative link between these two segment of the uropod exopod of P. lI1ussauellsis genera. The tanaidacean fauna of the Indonesian was missed by Shiino (1965), and thus it too was region is conspicuously understudied. of four segments, as in the other two species. ACKNOWLEDGEMENTS DISCUSSION Thanks are due to Damia Jaume (IMEDEA) for 'rhis group of closely-related species shows collecting the materiaL Sampling in Sulawesi was inevitable reproductive isolation, owing to conducted during an international expedition, its restriction to sites of freshwater habitat Zoological /1lZ'esligatiolls ill tile Karsts 50uth separated by extensive areas of fully-marine alld 50utheast 5ulawesi, organized by Or Louis sea-water, which would be expected to lead to Deharveng of the Museum national d'Histoire genetic drift and allopatric speciation. A range naturelle, Paris in collaboration with Or Yayuk of subtle if consistent distinctions in a generally Suhardjono and Cahyo Rahmadi of the Lembaga conservative morphology is thus not surprising as Ilmu Pengethuan Indonesia (LIPI ~ the Indonesian an expression of this evolution. Institute of Sciences). The expedition operated The genus remains distributed around the under research permits granted by LIP!. The Australasian region (Figure 4), P. lillllilei from specimens were gathered during fieldwork carried out by the aquatic team of Damia Jaume, Ceoff 428 R.N. Bamber

Boxshall (NHM) and Daisy Wowor (Museum Larsen, K. and Hansknecht, T. (2004). A new genus and Zoologicum Bogoriense). The support of the species of freshwater tanaidacean, Pseudohalmyra­ fieldwork by the Percy Sladen Memorial Fund pseudes aquadulcls (Apseudomorpha: Parapseudidae), (administered by the Linnean Society of London) from Northern Territory, Australia. Journal of Biology 24: 567-575. . is gratefully acknowledged. Leach, W.E. (1814). Crustaceology. In: Brewster, D., The Edinburgh Encyclopaedia: 383-437. Edinburgh. REFERENCES Monod, T. (1977). La faune terrestre de I'ile de Sainte­ Bacescu, M. and Gutu, M. (1974). Halmyrapseudes Helene. Quatrieme partie. 5. Tanaidacea. Annales du cubanensis n.g.n.sp. and H. bahamensis n.sp., brackish Musee Royal de I'Afrique Cmtrale. Tervuren, Belgiqlle water species of Tanaidacea (Crustacea). Travaux Annales. Serie in 8". Sciences Zoologiques 220: 457-465. du Museum d'Histoire naturelle "Grigore Antipa" 15: Richardson, H. (1901). Papers from the Hopkins Stanford 91-101. Galapagos Expedition, 1898-1899. VI. The isopods. Bamber, R.N., Ariyananda, T. and Silva, E.I.L. (2002). Proceedmgs of the Washington Academy of Sciences 3: The male of Halmyrapseudes srilankaensis (Bacescu, 565-568. 1981) comb. novo and an analysis of the genus Shiino, S. M. (1965). Tanaidacea from the Bismarck Halmyrapseudes Bacescu and Gutu, 1974 (, Archipelago. Videnskabelige Meddeleiser fra Dansk Tanaidacea). Journal ofCrustacean Biology 22: 287-297. Natllrhistorisk Forening i Kjobenhavn 128: 177':"203. Bamber, R. N. and Sheader, M. (2005). Apseudomorph Sieg, (1980). Sind die Dikonophora eine polyphyl­ Tanaidacea (Crustacea: : Peracarida) J. etJsche Gruppe? Zoologischer Anzieger 205: 401-416. from shallow waters off Sabah, Malaysia. Sllstematics and Biodiversity 2: 281-303. . Soemodinoto, A., Oey, B. L. and Ibkar-Kramadibrata, H. (1995). Effect of salinity decline on macrozoobenthos Brouquisse, F. (2002). Expt;dition Maros 99 - Rapport community of Cibeureum river estuary, Java, speIeologique. Association Pyreneenne de Speleologie, Indonesia. Indian Journal ofMarine Sciences 24: 62-67. Toulouse. 39 pp. Stephensen, K. (1936). A tanaid (Tanais stanfordi Gardiner, L. F. (1975). A fresh- and brackish-water Richardson) found in freshwater in the Kurile Islands, tanaidacean, Tanais stanfordi Richardson, 1901, from a with taxonomic remarks on the genus Tanais sensu hypersaline lake in the Galapagos Archipelago, with a lat. (Tanais Audouin et Milne-Edwards 1829, and report on West Indian specimens. Crustaceana 29 (2): Anatanais Nordenstam 1930). Annotationes Zoological' 127-140. Japonenses 15 (3): 361-373. Gutu, M. (1981). A new contribution to the systematics Van Name, W. G. (1925). The isopods of Kartabo Bartica and phylogeny of the suborder Monokonophora District, British Guiana. Zoologica (New York) 6: 461­ (Crustacea, Tanaidacea). TravalL"( du Museum National 503. d' Histoire Naturelle "Grigore Antipa" 23: 81-108. Kroyer, H. (1842). Nye Arter af SI