From Singapore, with a Description of a New Cladiella Species

Home , Aglaia spectabilis, Asemonea, Chelipoda, Cladiella, Cladiella australis, Cosmophasis

THE RAFFLES BULLETIN OF ZOOLOGY 2010

THE RAFFLES BULLETIN OF ZOOLOGY 2010 58(1): 1–13 Date of Publication: 28 Feb.2010 © National University of Singapore

ON SOME OCTOCORALLIA (CNIDARIA: ANTHOZOA: ALCYONACEA) FROM SINGAPORE, WITH A DESCRIPTION OF A NEW CLADIELLA SPECIES

Y. Benayahu Department of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Ramat Aviv, Tel Aviv 69978, Israel Email: [email protected] (Corresponding author)

L. M. Chou Department of Biological Sciences, Faculty of Science, National University of Singapore, 14 Science Drive 4, Singapore 117543 Email: [email protected]

ABSTRACT. – Octocorallia (Cnidaria: Anthozoa) from Singapore were collected and identifi ed in a survey conducted in 1999. Colonies collected previously, between 1993 and 1997, were also studied. The entire collection of ~170 specimens yielded 25 species of the families Helioporidae, Alcyoniidae, Paraclcyoniidae, Xeniidae and Briareidae. Their distribution is limited to six m depth, due to high sediment levels and limited light penetration. The collection also yielded Cladiella hartogi, a new species (family Alcyonacea), which is described. All the other species are new zoogeographical records for Singapore. A comparison of species composition of octocorals collected in Singapore between 1993 and 1977 and those collected in 1999 revealed that out of the total number of species, 12 were found in both periods, whereas seven species, which had been collected during the earlier years, were no longer recorded in 1999. Notably, however, six species that are rare on Singapore reefs were recorded only in the 1999 survey and not in the earlier ones. It is not yet clear whether these differences in species composition indeed imply changes over time in the octocoral fauna, or may refl ect a sampling bias. The inclusion of octocorals in Singapore reef-monitoring programs will undoubtedly shed light on possible temporal changes in their species composition. The fi ndings do indicate, however, that the fl eshy octocoral fauna of Singapore is rather impoverished compared to other reefs in the region.

KEY WORDS. – Cnidaria, Octocorallia, Alcyonacea, new species, Cladiella, new records, coral reefs, Singapore.

INTRODUCTION Taxonomic studies of the Singapore Octocorallia are relatively limited in number and deal mainly with gorgonians Singapore consists of a main island and over 60 small (sea fans and sea whips: see Fabricius & Alderslade, 2001). offshore islands with fringing and patch-reefs. The marine These studies were initiated by Verrill (1864) and Studer environment is an important resource that supports one of (1880), who recorded Mopsella elongata and Juncella the world’s busiest ports and one of the largest oil refi neries gemmacea, respectively. Shann (1912) listed for Singapore 11 (Chou, 2006). Close to 60% of the total coral reef areas of species, among which four were new ones, of the following Singapore has been lost through foreshore land reclamation, families: Alcyoniidae (one species), Telestidae (one species), while the remaining reefs are exposed to stress from the high Nephthyidae (four species), Siphonogorgiidae (one species), sediment load (Chou, 1996; Dikou & van Woesik, 2006) Sclerogorgiidae (one species) and Melitodidae (three species). and concerns have been raised regarding the conservation To date, Shann’s study is the only taxonomic account to of these reefs (Todd & Chou, 2005; Chou & Tun, 2007). A have dealt with the fl eshy octocorals (families Alcyoniidae mass bleaching event occurred in 1998 on a scale previously and Nephtheidae) from Singapore. Following a gap of 82 unknown (http://coralreef.nus.edu.sg/; Tun et al., 2004) years, a preliminary survey of the gorgonian octocoral fauna affecting 50% to 90% of reef organisms, including Sinularia of Singapore was published by Goh & Chou (1994), which octocorals (family Alcyoniidae), which suffered particularly revealed six families, comprising at least 11 genera and 21 high mortality rates. species. That study concluded that the gorgonian taxonomy for the region is in a poor state and therefore species identifi cation is uncertain. Based on these fi ndings and also combined with

1 Benayahu and Chou: Octocorallia (Alcyonacea) from Singapore newly collected material, Goh & Chou (1996) published an The present study deals with octocorals from Singapore of the annotated checklist of the gorgonians of Singapore, totaling families Helioporidae, Alyconiidae, Paralcyoniidae, Xeniidae 31 species of 12 genera and six families (Anthothelidae: and Briareidae. It provides for the fi rst time a systematic list Solenocaulon; Subergorgiidae: Subergorgia; Melithaeidae: of octocorals of these families for the area and describes Melithaea, Mopsella and Acabaria; Acanthogorgiidae: Cladiella hartogi, new species. It also compares the fl eshy Acanthogorgia; Plexauridae: Echinomuricea, Astrogorgia, octocoral fauna recorded in the current survey (1999) to the Echinogorgia and Euplexaura; and Ellisellidae: Junceella previous ones (1993–1997). and Ctenocella. Notably, that study identifi ed to species level only part of the specimens. Later, Ofwegen et al., (2000) dealt with species of the family Melithaeidae in Singapore MATERIALS AND METHODS and identifi ed four species of the genera Melithaea, Mopsella and Acabaria, also with reference to Shann (1912). Several During Jul.1999 collections were conducted by us from studies have dealt with other aspects of Singapore gorgonians the following sites: Pulau [=Island] Hantu; Pulau Satumu, other than their taxonomy, such as distribution (Goh & Chou, Raffles Lighthouse; Terumbu Pempang Laut; Raffles 1994), annual growth rate (Goh & Chou, 1995), zonation Marina; Terumbu Pempang Tengah (artifi cial reef site); and (Goh et al., 1997), associated fauna (e.g., Goh et al., 1999) The Sisters (Fig. 1). These sites were reached by boat. An and bioactivity (e.g., Koh et al., 2000, 2002). Recently, examination of a variety of niches was carried out by scuba Goh et al. (2009) identifi ed the following octocoral genera diving, and samples were obtained at a maximal depth of 4–6 from Singapore: Carijoa, Cladiella, Sinularia, Lobophytum, m. At the artifi cial reef site at Terumbu Pempang Tengah, Sarcophyton, Stereonephthya and Nephthea, and indicated the survey included concrete modules and tyre structures the high abundance of the family Alcyoniidae and the lack of and samples were obtained down to its maximal depth knowledge on the species diversity of the fl eshy octocorals. of 14 m. During the nine day-long survey, 14 dives were Furthermore, that study demonstrated high levels of toxicity conducted, each lasted 60–80 minutes and approximately in extracts of Sarcophyton spp. and Cladiella spp. collected 90 samples were collected of the octocoral taxa found at the in Singapore reefs. various sites. Prior to collection some of the colonies were

Fig. 1. Map of Singapore showing location of the study sites.

2 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. List of species of Octocorallia of the orders Helioporacea Bock, 1938, and Alcyonacea (Lamouroux, 1816) from Singapore with indication of inventory numbers of Rafﬂ es Museum of Biodiversity Research (ZRC) and of Zoological Museum Tel Aviv University (ZMTAU Co), collection sites and date of collection. Previous ZRC numbers of material deposited at Tel Aviv University are given in square brackets.

Classiﬁ cation

Helioporidae Blainville, 1830

Genus Heliopora Moseley, 1786

Heliopora coerulea (Pallas, 1766) 6 colonies (ZRC 1999.2280), Pulau Satumu (Rafﬂ es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999; 1 colony (ZMTAU Co 34544) [ZRC 1999.2282], Sisters, coll. Y. Benayahu, 19 Jul. 1999; 3 colonies (ZRC 1999.2282), Sisters, coll. Y. Benayahu, 19 Jul. 1999.

Alcyoniidae Lamouroux, 1912

Genus Cladiella Gray, 1869

Cladiella hartogi, new species Holotype (ZRC 1999.2256), Terumbu Pempang Tengah, 2–4 m, coll. Y. Benayahu, 14 Jul.1999. Paratypes: 1 colony (ZRC 1999.1065), Pulau Hantu (north side of island), reef fl at, coll. S. L. M. Teo & C. S. C. Lee, 30 May 1994; 1 colony (ZMTAU Co 34539) [ZRC 1999.2207], Pulau Hantu, 1 m, coll.Y. Benayahu, 6 Jul. 1999;1 colony and 2 fragments (ZRC1999.2207), Pulau Hantu, 1 m, coll. Y. Benayahu, 6 Jul.1999; 1 colony (ZMTAU Co 34540) [ZRC 1999.2221], Pulau Hantu, 1–4 m, coll. Y. Benayahu, 9 Jul.1999; 1 colony (ZRC 1999.2221), Pulau Hantu, 1–4 m, coll. Y. Benayahu, 9 Jul.1999; 1 colony (ZMTAU Co 34537) [ZRC 1999.2223], Pulau Hantu, 1–4 m, coll. Y. Benayahu, 9 Jul.1999; 2 colonies (ZRC 1999.2223), Pulau Hantu, 1–4 m, coll. Y. Benayahu, 9 Jul.1999; 1 colony (ZMTAU Co 34541) [ZRC 1999.2231], Pulau Hantu, 1–2 m, coll. Y. Benayahu, 9 Jul.1999; 2 colonies (ZRC1999.2231), Pulau Hantu, 1–2 m, coll. Y. Benayahu, 9 Jul.1999; 1 colony (ZMTAU Co 34536) [ZRC 1999.2232], Terumbu Pempang Laut, (patch reef), 2–6 m, coll. Y. Benayahu, 12 Jul.1999; 2 colonies (ZRC 1999.2232), Terumbu Pempang Laut, (patch reef), 2–6 m, coll. Y. Benayahu, 12 Jul.1999; 1 colony (ZRC 1999.2255), Terumbu Pempang Tengah, 2–6 m, coll. Y. Benayahu, 14 Jul.1999; 1 colony (ZMTAU Co 34535) [ZRC 1999.2262], Pulau Satumu (Raffl es Lighthouse), 3-6 m, coll. Y. Benayahu, 15 Jul.1999; 1 colony (ZRC 1999.2262), Pulau Satumu (Raffl es Lighthouse), 3-6 m, coll. Y. Benayahu, 15 Jul.1999; 1 colony (ZRC 1999.2266), Pulau Satumu (Raffl es Lighthouse), 3-6 m, coll. Y. Benayahu, 15 Jul.1999; 1 colony (ZMTAU Co 34538) [ZRC 1999.2281], Sisters Reef, 2-3 m, coll. Y. Benayahu, 19 Jul., 1999; 2 colonies (ZRC 1999.2281), Sisters Reef, 2-3 m, coll. Y. Benayahu, 19 Jul., 1999.

Cladiella pachyclados (Klunzinger, 1887) 1 colony (ZRC 1999.1042), Pulau Semakau, coll. S.L.M. Teo & H. C. Tay, 7 Jun. 1995; 1 colony (ZRC 1999.1090), Pulau Semakau, west side of Is., coll. S.L.M. Teo, 20 Apr. 1995; 3 colonies (ZRC 1999.2259), Pulau Satumu (Raffl es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999; 1 colony (ZRC 1999.2267), Pulau Satumu (Raffl es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999; 3 colonies (ZRC 1999.2271), Pulau Satumu (Raffl es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999; 1 colony (ZRC 1999.2278), Pulau Satumu (Raffl es Lighthouse), 15 Jul. 1999; 1 colony (ZMTAU Co 34542) [ZRC 1999.2279], Pulau Satumu (Raffl es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999.

Genus Lobophytum von Marenzeller, 1886

Lobophytum crassum von Marenzeller, 1886 1 colony (ZRC 1996.480), Pulau Semakau, coll H. C. Tay & S.L.M. Teo, 19 Jun. 1995; 1 colony (ZRC 1996.481), Pulau Semakau, coll. 19 Jun. 1995; 1 colony (ZRC 1996.482), Pulau Semakau, coll. H. C. Tay & S.L.M. Teo, 19 Jun. 1995; 1 colony (ZRC 1999.1044(, Pulau Semakau, coll. S.L.M. Teo & H. C. Tay, 13 Jun. 1995; 1 colony (ZRC 1999.1062), Pulau Hantu, north-west side of Is., coll. S.L.M. Teo & C.S.C. Lee, 23 Jun. 1993; 1 colony (ZRC 1999.1067), Pulau Hantu, north side of Is., coll. S.L.M. Teo & C.S.C. Lee, 30 May 1994; 1 colony (ZRC 1999.1076), Pulau Hantu, north side of Is., coll. S.L.M. Teo & C.S.C. Lee, 6 Oct. 1994; 2 colonies (ZRC 1999.1077), Pulau Hantu, south east side of Is., coll. S.L.M. Teo, 5 Nov.1994; 3 colonies (ZRC 1999.1086), Pulau Semakau, west side of Is., coll. S.L.M. Teo & C.S.C. Lee, 8 Feb. 1993; 2 colonies (ZRC 1999.2233), Terumbu Pempang Laut, coll. Y. Benayahu, 12 Jul. 1999; 1 colony (ZRC 1999.2244), Terumbu Pempang Tengah, coll. S.L.M. Teo & H. C. Tay, 14 Jul. 1999; 2 colonies (ZRC 1999.2245), Terumbu Pempang Tengah, coll. Y. Benayahu, 14 July 1999; 2 colonies (ZMTAU Co 34545) [ZRC 1999.2246], Terumbu Pempang Tengah, coll. Y. Benayahu, 14 Jul. 1999.

Lobophytum paucifl orum (Ehrenberg, 1834) 1 colony (ZRC 1996.484), Pulau Hantu, coll. Juliana Chee. & S. K. Goh, 26 Sep. 1995; 1 colony (ZRC 1999.1053), Pulau Hantu, north west side of Is. coll. S.L.M. Teo & C.S.C. Lee, 9 Jan. 1993; 1 colony (ZRC 1999.1057), Pulau Hantu, south east side of Is., coll. S.L.M. Teo & C.S.C. Lee, 9 Jun. 1993; 2 colonies (ZMTA Co 34546) [ZRC 1999.1079], Pulau Hantu, south east side of Is., coll. S.L.M. Teo,16 Feb. 1995; 5 colonies (ZRC 1999.1079), Pulau Hantu, south east side of Is., coll. S.L.M. Teo,16 Feb. 1995; 1 colony (ZRC 1999.1091), Pulau Satumu (Raffl es Lighthouse), coll. S.L.M. Teo, 18 May 1995; 3 colonies (ZRC 1999.1092), Pulau Satumu (Raffl es Lighthouse), coll. S.L.M. Teo, 18 May 1995; 1 colony (ZRC 1999.1103), St. John’s Is., south east side of Is., coll. C.S.C. Lee, 7 Oct. 1994; 2 colonies (ZRC 1999.2222), Pulau Hantu, coll. Y. Benayahu, 9 Jul. 1999; 3 colonies (ZRC 1999.2238), Terumbu Pempang Laut, coll. Y. Benayahu, 12 Jul. 1999; 1 colony (ZRC 1999.2263), Pulau Satumu (Raffl es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999; 1 colony (ZRC 1999.2269), Pulau Satumu (Raffl es Lighthouse), coll. Y. Benayahu, 15 Jul.1999.

3 Benayahu and Chou: Octocorallia (Alcyonacea) from Singapore

Table 1. Cont'd.

Classiﬁ cation

Lobophytum sarcophytoides Moser, 1919 2 colonies (ZRC 1999.1069), Pulau Hantu, north side of Is., coll. S.L.M. Teo & C.S.C. Lee, 30 May 1994; 4 colonies (ZRC 1999.1096), St.John’s Is., north side of Is., S.L.M. Teo, 13 Jun. 1994; 1 colony (ZRC 1999.1097), St. John’s Is., north side of Is., S.L.M. Teo, 13 Jun. 1994; 1 colony (ZMTAU Co 34547) [ZRC1999.2243], Terumbu, Pempang Tengah, coll. Y. Benayahu, 14 Jul. 1999.

Genus Sarcophyton Lesson, 1834

Sarcophyton crassocaule Moser, 1919 1 colony (ZRC 1996.496), Pulau Hantu, coll. Juliana Chee. & S. K. Goh, 22 Oct. 1995; 2 colonies (ZRC 1999.1075), Pulau Hantu, north side of Is., coll. S.L.M. Teo & C.S.C. Lee, 6 Oct. 1994; 3 colonies (ZRC 1999.1098), St. John’s Is. north side of Is., coll. S.L.M. Teo, 13 Jun. 1994; 1 colony (ZRC 1999.2219), Pulau Hantu, coll. Y. Benayahu, 9 Jul. 1999; 1 colony, (ZRC 1999.2220), Pulau Hantu, coll. Y. Benayahu, 9 Jul., 1999; 1 colony (ZRC 1999.2234), Terumbu Pempang Laut, coll. Y. Benayahu, 12 Jul. 1999; 1 colony ZMTAU Co 34549 [ZRC 1999.2272], Pulau Satumu (Rafﬂ es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999.

Sarcophyton ehrenbergi von Marenzeller, 1886 1 colony (ZRC 1999.1061), Pulau Hantu, north west side of Is., coll. S.L.M. Teo & C.S.C. Lee, 23 Jun. 1993; 1 colony (ZRC 1999.1064), Pulau Hantu, north side of Is., coll. S.L.M. Teo, & C.S.C. Lee, 30 May 1994; 4 colonies (ZRC 1999.1094), St. John’s Is., south east side of Is., coll. S.L.M. Teo, 23 Jun. 1993; 2 colonies (ZMTAU Co 34550) [ZRC 1999.2205], Pulau Hantu, coll. Y. Benayahu, 6 Jul.1999; 3 colonies (ZRC 1999.2218), Pulau Hantu, coll. Y. Benayahu, 9 Jul. 1999; 2 colonies (ZRC 1999.2239), Terumbu Pempang Laut, coll. Y. Benayahu, 12 Jul. 1999; 2 colonies (ZRC 1999.2253), Terumbu Pempang Tengah, coll. Y. Benayahu, 14 Jul. 1999; 3 colonies (ZRC 1999.2260), Pulau Satumu (Raffl es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999; 1 colony (ZRC 1999.2261), Pulau Satumu (Raffl es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999; 3 colonies (ZRC 1999.2275), Pulau Satumu (Raffl es Lighthouse), coll. Y. Benayahu, 15 Jul.1999; 2 colonies (ZRC 1999.2277), Pulau Satumu (Raffl es Lighthouse), 15 Jul. 1999.

Sarcophyton glaucum (Quoy & Gaimard, 1833) 1 colony (ZMTAU Co 34551) [ZRC 1999.1102], St. John’s Is., south east side of Is., Coll. C.S.C. Lee, 7 Oct. 1994; 1 colony (ZRC 1999.1102), St. John’s Is., south east side of Is., Coll. C.S.C. Lee, 7 Oct. 1994; 2 colonies (ZRC 1999.2270), Pulau Satumu (Rafﬂ es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999.

Sarcophyton tenuispiculatum Thomson & Dean, 1931 1 colony (ZRC 1996.490) Pulau Hantu, coll. S.L.M. Teo, 26 Oct. 1995; 1 colony (ZMTAU Co 34553) [ZRC 1999.1078], Pulau Hantu, south east side of Is. coll. S.L.M. Teo, 5 Nov. 1994.

Sarcophyton trocheliophorum von Marenzeller, 1886 1 colony (ZRC 1999.1056), Pulau Hantu, south east side of Is., coll. S.L.M. Teo & C.S.C. Lee, 8 Mar.1993; 1 colony (ZRC 1999.2260), Pulau Satumu (Rafﬂ es Lighthouse), coll. Y. Benayahu,15 Jul. 1999; 4 colonies (ZRC 1999.2227), Pulau Hantu, coll. Y. Benayahu, 9 Jul. 1999; 1 colony (ZRC 1999.2228), Pulau Hantu, coll. Y. Benayahu, 9 Jul. 1999; 1 colony (ZRC 1999.2235), Terumbu Pempang Laut, coll. Y. Benayahu, 12 Jul. 1999; 1 colony (ZMTAU Co 34552) [ZRC 1999.2283], Sisters, coll. Y. Benayahu, 19 July 1999; 1 colony (ZRC 1999.22830, Sisters, coll. Y. Benayahu, 19 July 1999.

Genus Sinularia May, 1898

Sinularia abrupta Tixier Durivault, 1970 1 colony (ZMTAU Co 34554) [ZRC 1999.2274], Pulau Satumu (Rafﬂ es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999; 1 colony (ZRC 1999.2274), Pulau Satumu (Rafﬂ es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999.

Sinularia brassica May, 1898 1 colony, (ZRC 1996.478), Pulau Semakau, coll. H. C. Tay & S.L.M. Teo, 13 Jun. 1995; 2 colonies (ZRC 1999.1095), St. John’s Is., south east side of Is., coll. L.J. Harrison, 23 Jul. 1993; 1 colony (1999.1099), St. John’s Is., north side of Is., coll. S.L.M. Teo, 13 Jun. 1994; 1 colony (ZMTAU Co 34555) [ZRC 1999.2240], Terumbu Penpang Laut, coll. Y. Benayahu, 12 Jul. 1999; 2 colonies (ZRC 1999.2240), Terumbu Penpang Laut, coll. Y. Benayahu, 12 Jul. 1999.

Sinularia capillosa Tixier Durivault, 1970 1 colony (ZMTAU Co 34556) [ZRC 1996.483], Pulau Semakau, coll. H. C. Tay & S.L.M. Teo, 19 Jun. 1995; 1 colony (ZRC 1996.495), St. John’s Is., coll. H. C. Tay & S.L.M. Teo, 28 Sept. 1995; 1 colony (ZRC 1999.1060), Pulau Hantu, south east side of Is., coll. S.L.M. Teo & C.S.C. Lee, 9 June 1993; 3 colonies (ZRC 1999.1068), Pulau Hantu, north side of Is., coll. S.L.M. Teo & C.S.C. Lee, 30 May 1994; 1 colony (ZRC 1999.1074), Pulau Hantu, north side of Is., coll. S.L.M. Teo & C.S.C. Lee, 6 Oct. 1994; 1 colony (ZRC 1999.1081), Pulau Hantu, south east side of Is., coll. S.L.M. Teo, 16 Feb. 1995; 1 colony (ZRC 1999.1089), Pulau Semakau, west side of Is., coll. S.L.M. Teo, 14 Jun. 1994; 1 colony (ZRC 1999.1100), St. John’s Is., south east side of Is., coll. C.S.C. Lee, 7 Oct. 1994.

Sinularia compressa Tixier Durivault, 1945 1 colony (ZMTAU Co 34557) [ZRC 1999.2248], Terumbu Pempang Tengah, coll. Y. Benayahu, 14 Jul. 1999; 1 colony (ZRC 1999.2248), Terumbu Pempang Tengah, coll. Y. Benayahu, 14 Jul. 1999.

Sinularia depressa Tixier Durivault, 1970 1 colony (ZRC 1999.1071), Pulau Hantu, north side of Is., coll. S.L.M. Teo & C.S.C. Lee, 6 Oct. 1994; 1 colony (ZRC 1999.1073), Pulau Hantu, north side of Is., coll. S.L.M. Teo & C.S.C. Lee, 6 Oct. 1994; 1 colony (ZMTAU Co 34558) [ZRC 1999.1082], Pulau Hantu, south east side of Is., 16 Feb. 1995.

4 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. Cont'd.

Classiﬁ cation

Sinularia erecta Tixier Durivault, 1945 1 colony (ZMTAU Co 34559) [ZRC 1999.2257], Terumbu Pempang Tengah, coll. Y. Benayahu, 14 Jul. 1999; 1 colony (ZRC 1999.2257), Terumbu Pempang Tengah, coll. Y. Benayahu, 14 Jul. 1999.

Sinularia exilis Tixier Durivault, 1970 1 colony, ZMTAU Co 34560 [ZRC 1999.2276], Pulau Satumu (Rafﬂ es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999; 1 colony (ZRC 1999.2276), Pulau Satumu (Rafﬂ es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999.

Sinularia gibberosa Tixier Durivault, 1970 1 colony (ZRC 1999.1047), Pulau Hantu, north west end of Is., coll. S.L.M. Teo, K. Low, H. C. Tay, 12 Nov. 1996; 2 colonies (ZRC 1999.1059), Pulau Hantu, south east side of Is., coll. S.L.M. Teo & C.S.C. Lee, 9 Jun. 1993; 1 colony (ZRC 1999.1072), Pulau Hantu, north side of Is., coll. S.L.M. Teo & C.S.C. Lee, 6 Oct. 1994; 1 colony, (ZMTAU Co 34561) [ZRC 1999.1083], Pulau Hantu, south east side of Is., coll. S.L.M. Teo, 16 Feb. 1995; 1 colony (ZRC 1999.1083), Pulau Hantu, south east side of Is., coll. S.L.M. Teo, 16 Feb. 1995; 2 colonies (ZRC 1999.1084), Pulau Hantu, south east side of Is., coll. S.L.M. Teo, 16 Feb., 1995; 1 colony (ZRC 1999.1101), St. John’s Is., south east side of Is. , coll. C.S.C. Lee, 7 Oct. 1994.

Sinularia hirta (Pratt, 1903) 1 colony (ZMTAU Co 34562) [ZRC 1999.1087], Pulau Semakau, west side of Is., coll. S.L.M. Teo & C.S.C. Lee, 10 Apr. 1993; 1 colony (ZRC 1999.1087), Pulau Semakau, west side of Is., coll. S.L.M. Teo & C.S.C. Lee, 10 Apr. 1993; 1 colony (ZRC 1999.2225), Pulau Hantu, coll. Y. Benayahu, 9 Jul. 1999.

Sinularia lochmodes Kolonko, 1926 1 colony (ZRC 1999.1058), Pulau Hantu, south east side of Is., coll. S.L.M. Teo & C.S.C. Lee, 9 May 1993; 3 colonies (ZRC 1999.1085), Pulau Semakau, west side of Is., coll. S.L.M. Teo & C.S.C. Lee, 8 Feb. 1993; 1 colony (ZRC 1999.2202), Raffl es Marina, coll. Y. Benayahu, 6 Jun. 1999; 1 colony (ZMTAU Co 34563) [ZRC 1999.2206], Pulau Hantu, coll. Y. Benayahu, 6 Jul. 1999; 4 colony, (ZRC 1999.2242), Terumbu Pempang Laut, coll. Y. Benayahu, 12 Jul. 1999; 2 colonies (ZRC 1999.2250), Terumbu Pempang Tengah, coll. Y. Benayahu, 14 Jul. 1999; 1 colony (ZRC 1999.2251), Terumbu Pempang Tengah, coll. Y. Benayahu, 14 Jul. 1999; 1 colony (ZRC 1999.2254), Terumbu Pempang Tengah, coll. Y. Benayahu, 14 Jul. 1999; 2 colony (ZRC 1999.2265), Pulau Satumu (Raffl es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999; 3 colonies (ZRC 1999.2273), Pulau Satumu (Raffl es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999.

Sinularia microclavata Tixier Durivault, 1970 1 colony (ZMTAU Co 34564) [ZRC 1999.1088], Pulau Semakau, west side of Is., coll. Y. Benayahu, 14 Jun. 1994; 1 colony (ZRC 1999.1088), Pulau Semakau, west side of Is., coll. Y. Benayahu, 14 Jun. 1994.

Sinularia triangula Tixier Durivault, 1970 1 colony (ZMTAU Co 34565) [ZRC 1999.2237], Terumbu Pempang Laut, coll. Y. Benayahu, 12 Jul. 1999; 1 colony (ZRC 1999.2237), Terumbu Pempang Laut, coll. Y. Benayahu, 12 Jul. 1999.

Paralcyoniidae Gray, 1869

Genus Studeriotes Thomson & Simpson, 1909

Studeriotes spinosa Thomson & Dean, 1931 1 colony (ZMTAU Co 34566) [ZRC 1999.1048], Terumbu Pempang Tengah, coll. S.L.M. Teo & H.C. Tay, 17 Jun. 1996; 1 colony (ZRC 1999.1048), Terumbu Pempang Tengah, coll. S.L.H. Teo & H. C. Tay, 17 Jun. 1996.

Xeniidae Ehrenberg, 1828

Genus Sansibia Alderslade, 2000

Sansibia ﬂ ava (May, 1898) 2 colonies (ZRC 1999.1050), Lazarus Is., coll. S.L.M. Teo, Juliana Chee. & S. K. Goh,5 Jul. 1996; 1 colony (ZRC 1999.1051), Pulau Seringat Kechil, coll. S.L.M. Teo, 25 May 1997; 1 colony (ZMTAU Co 34548) [ZRC 1999.1052], Pulau Seringat Kechil, coll. S.L.M. Teo, 23 Jul. 1997; 1 colony (ZRC 1999.1052), Pulau Seringat Kechil, coll. S.L.M. Teo, 23 Jul. 1997.

Briareidae Blainville, 1830

Genus Briareum Blainville, 1830

Briareum excavatum (Natting, 1911) 3 colonies (ZRC 1999.1045), St. John’s Is., coll. S.L.M. Teo & H. C. Tay, 7 Feb. 1996; 1 colony (ZMTAU Co 34532) [ZRC 1999.2258], Pulau Satumu (Rafﬂ es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999; 2 colonies (ZRC 1999.2258), Pulau Satumu (Rafﬂ es Lighthouse), coll. Y. Benayahu, 15 Jul. 1999.

5 Benayahu and Chou: Octocorallia (Alcyonacea) from Singapore photographed in situ. Samples were fi xed in 4% formalin in sclerite preparations of type material kept at the Zoological seawater overnight, then rinsed in freshwater and transferred Museum, Department of Zoology, Tel Aviv University, to 70% alcohol. An additional ~90 octocoral colonies were Israel (ZMTAU). The specimens are deposited in the ZRC obtained from the Zoological Reference Collection (ZRC) and duplicate material in ZMTAU. Some Sinularia colonies, of the Raffl es Museum of Biodiversity Research (RMBR), mostly of the leptoclados group (see Verseveldt, 1980), and National University of Singapore, and were included in the members of the family Nephtheidae are still being examined current study. These colonies had been collected between (Ofwegen & Benyahau, in prep.). 1993–1997, from some of the above-mentioned sites, and additionally from Pulau Ubin, St. John’s Island, Changi Sailing Club (jetty), Pulau Semakau, Pulau Seringat Kechil TAXONOMY and Lazarus Island (Fig. 1). These ZRC-RMBR samples lack data on collection depth. Duplicate material of the collection The examined material yielded 25 species of the fi ve families was deposited at the Zoological Museum, Tel Aviv University Helioporidae, Alyconiidae, Paralcyoniidae, Xeniidae and (ZMTAU) as indicated below followed by the original ZRC Briareidae (Table 1), and Cladiella hartogi, new species. collection numbers of these colonies given in brackets.

Sclerites were obtained by dissolving the tissues in 10% Cladiella hartogi, new species sodium hypochlorite, and prepared for scanning electron (Figs. 2–5) microscopy as follows: the sclerites were carefully rinsed with double-distilled water, dried at room temperature, Material examined. – Holotype and four microscope slides coated with gold, and then examined with a Jeol 840A (ZRC1999.2256), Terumbu Pempang Tengah, 2–4 m, coll. Y. electron microscope operated at 25 kV. Identiﬁ cation of Benayahu, 14 Jul. 1999. Paratypes: 1 colony (ZRC1999.1065), species was in part facilitated by comparisons with permanent Pulau Hantu (north side of island), reef ﬂ at, coll. S. L. M. Teo & C. S. C. Lee, 30 May 1994; 1 colony (ZMTAU Co 34539) [ZRC

Fig. 2. Cladiella hartogi new species; holotype (ZRC 1999.2256): a, view of colony from above; b, side view of colony; c, paratype (ZRC 1999.2255). Scale bar 10 mm.

6 THE RAFFLES BULLETIN OF ZOOLOGY 2010

1999.2207], Pulau Hantu, 1 m, coll. Y. Benayahu, 6 Jul. 1999; 1 retracted and only occasionally indicated by the tiny pits on colony and 2 fragments (ZRC 1999.2207), Pulau Hantu, 1 m, coll. the surface of the lobes and lobules. Y. Benayahu, 6 Jul.1999; 1 colony (ZMTAU Co 34540) [ZRC 1999.2221], Pulau Hantu, 1–4 m, coll. Y. Benayahu, 9 Jul. 1999; 1 The polyp sclerites vary in size (0.020–0.062 mm) and shape colony (ZRC 1999.2221), Pulau Hantu, 1–4 m, coll. Y. Benayahu, (Fig. 3a). The small ones are fl at with irregular tubercles 9 Jul. 1999; 1 colony (ZMTAU Co 34537) [ZRC 1999.2223], Pulau Hantu, 1–4 m, coll. Y. Benayahu, 9 Jul. 1999; 2 colonies (ZRC along their margins, while in the larger ones the tubercles 1999.2223), Pulau Hantu, 1–4 m, coll. Y. Benayahu, 9 Jul. 1999; are arranged at either end, separated by a bare waist and 1 colony (ZMTAU Co 34541) [ZRC 1999.2231], Pulau Hantu, 1–2 resembling dumb-bells. The lobe surface also features similar m, coll. Y. Benayahu, 9 Jul. 1999; 2 colonies (ZRC 1999.2231), dumb-bells, 0.060–0.095 mm long. Some possess a coarse Pulau Hantu, 1–2 m, coll. Y. Benayahu, 9 Jul. 1999; 1 colony surface and tubercles, mostly conical with blunt tips (Fig. (ZMTAU Co 34536) [ZRC 1999.2232], Terumbu Pempang Laut, 3b). Other dumb-bells have pronounced, relatively high and (patch reef), 2–6 m, coll. Y. Benayahu, 12 Jul. 1999; 2 colonies warty tubercles (Fig. 3c), similar to those revealed in the (ZRC 1999.2232), Terumbu Pempang Laut, (patch reef), 2–6 m, coll. lobe interior. Y. Benayahu, 12 Jul. 1999; 1 colony (ZRC 1999.2255), Terumbu Pempang Tengah, 2–6 m, coll. Y. Benayahu, 14 Jul. 1999; 1 colony (ZMTAU Co 34535) [ZRC 1999.2262], Pulau Satumu (Raffl es The surface of the base (Fig. 4a) and its interior (Fig. 4b) Lighthouse), 3–6 m, coll. Y. Benayahu, 15 Jul.1999; 1 colony (ZRC contain dumb-bells 0.050–0.090 mm long, with distinct waist 1999.2262), Pulau Satumu (Raffl es Lighthouse), 3–6 m, coll. Y. and remarkably wide, tuberculate heads with high warts, up Benayahu, 15 Jul.1999; 1 colony (ZRC 1999.2266), Pulau Satumu to 0.07 mm in diameter. (Raffl es Lighthouse), 3–6 m, coll. Y. Benayahu, 15 Jul.1999; 1 colony (ZMTAU Co 34538) [ZRC 1999.2281], Sisters Reef, 2–3 Colour. – The preserved colony is beige. Numerous m, coll. Y. Benayahu, 19 Jul., 1999; 2 colonies (ZRC 1999.2281), zooxanthellae are found in the tissue. Sisters Reef, 2–3 m, coll. Y. Benayahu, 19 Jul. 1999. Living features. – The expanded polyps are brown (Fig. 5a) Diagnosis. – The holotype is an encrusting colony with a and the colony surface is light gray (Fig. 5b). The colonies maximum cross-section of 120 X 80 mm and a low base were occasionally found growing in patches. of four to eight mm (Fig. 2a, b). The colony has elongated lobes which split at their end or sides into lobules. The Variation. – The 22 paratypes (see list above) differ only in lobes and lobules are mostly arranged in groups, somewhat size (i.e., ZRC 1999.2255: Fig. 2c), the smallest being with fi rm, partially bent and have a tapering tip. All polyps are

Fig. 3. Cladiella hartogi new species; holotype (ZRC 1999.2256): a, polyp sclerites; b, dumb-bells with course surface and tubercles from surface of lobes; c, dumb-bells with warty tubercles from surface and interior of lobes. Scale bar 0.020 mm.

7 Benayahu and Chou: Octocorallia (Alcyonacea) from Singapore a cross-section of 20 × 25 mm and all possess the same Africa: Tanzania (Ofwegen & Benayahu, 1992); South sclerites as the holotype. Africa (Benayahu, 1993); Mozambique (e.g., Benayahu et al., 2003); Indian Ocean: Madagascar (Tixier-Durivault, Etymology. – The species is named after the late Drs. 1966; Verseveldt, 1971); Seychelles (Verseveldt, 1976); Jacobus Cornelis (Koos) den Hartog, former curator of the Laccadives (Vennam & Ofwegen, 1996); Paciﬁ c Ocean: Coelenterata et al., National Museum of Natural History, New Caledonia (Tixier-Durivault, 1970a; Verseveldt, 1974); Leiden, Netherlands, who passed away in October 2000. Gambier (Verseveldt, 1977); Guam (Verseveldt, 1978; Koos greatly assisted Y. Benayahu during the latter’s frequent Benayahu, 1997); Ambon (Ofwegen & Vennam 1994); visits to the octocoral collection in Leiden. Bismark Sea (Ofwegen, 1996); East China Sea: Vietnam (Tixier-Durivault, 1970b); Ryukyu Archipelago (Benayahu, Remarks. – The genus Cladiella is moderately common 2002 and references therein); Taiwan (Benayahu et al., 2004 in shallow Indo-Paciﬁ c coral reef habitats (Fabricius & and references therein). The only revision on octocorals of the Alderslade, 2001). Species of this genus have been collected genus Cladiella is by Tixier-Durivault (1948), who presented in various regions, including the Red Sea (e.g., Verseveldt, 44 nominal species. Since then, an additional 14 new species 1965; Verseveldt & Benayahu, 1978; 1983); east coast have been described: C. aspera Tixier-Durivault, 1970; C.

Fig. 4. Cladiella hartogi new species; holotype (ZRC 1999.2256): a, dumb-bells of surface of the base; b, dumb-bells of interior of base. Scale bar 0.020 mm.

8 THE RAFFLES BULLETIN OF ZOOLOGY 2010 densa Tixier-Durivault, 1970; C. hirsuta Tixier-Durivault, The length of the dumb-bells of the following fi ve Cladiella 1970; C. multilobata Tixier-Durivault, 1970; C. ramosa species falls within the size range of C. hartogi new species; Tixier-Durivault, 1970; C. rotundata Tixier-Durivault, however their head-diameter and tubercles differ. C. laciniosa 1970; C. scabra Tixier-Durivault, 1970; C. subtilis Tixier- (Tixier-Durivault, 1944) has dumb-bells up to 0.09 mm long, Durivault, 1970; C. humesi Verseveldt, 1974 (all from New with head-diameter up to 0.05 mm, and covered by simple Caledonia); C. devaneyi Verseveldt, 1977 (Rurutu Is., south conical tubercles. C. letourneuxi (Tixier-Durivault, 1944) of Tahiti); C. arbusculoides Verseveldt & Benayahu, 1978 has dumb-bells up to 0.08 mm long, mostly with a narrow (northern Red Sea); C. steineri Verseveldt, 1982 (Koh Si- waist, which is often a mere line, their head-diameter up chang, Thailand); C. daphnae; Ofwegen & Benyahau, 1992 to 0.055 mm, and possessing conical tubercles. Cladiella (Tanzania) and C. kashmani Benayahu & Schleyer, 1996 (Tixier Durivault, 1944) has dumb-bells, up to 0.08 mm (Sodwana Bay, South Africa). These fi ndings indicate the long, head-diameter up to 0.05 mm, and covered by conical diversity of the genus Cladiella throughout the entire Indo- or pointed tubercles. C. pulchra (Tixier Durivault, 1944) Pacifi c reef systems, bringing its total number of nominal has non-retracted polyps, and thus differs from C. hartogi species to 58. Undoubtedly, there is need for a thorough new species (see Fig. 2); its dumb-bells are up to 0.09 mm taxonomic revision of Cladiella species. In the absence of long, head-diameter up to 0.04 mm, and it possesses densely such a revision, the description of C. hartogi sp. nov. was placed low-rounded tubercles. C. suezensis (Tixier Durivault, facilitated by the examination of relevant type material of all 1944) has dumb-bells up to 0.10 mm long, head-diameter species designated by Tixier-Durivault (1948, 1970a) and in up to 0.08 mm, and is mostly covered with elongate-pointed the subsequent publications (Verseveldt, 1974, 1977, 1982; tubercles. Verseveldt & Benayahu 1978; Ofwegen & Benayahu, 1992; Benayahu & Schleyer, 1996). The colony shape of the following fi ve Cladiella species resemble that of C. hartogi new species, but their sclerites The elongated and divided lobes (Figs. 2, 5) of C. hartogi differ. C. hirsuta Tixier-Durivault, 1970 has dumb-bells, up new species and the shape and dimensions of its warty to 0.12 mm long, and head-diameter up to 0.08 mm. Unlike tuberculate dumb-bells (Figs. 3, 4) are considered by us as C. hartogi new species, the polyp sclerites of C. hirsuta the diagnostic features of the species. The colony shape of are platelets, often with two transparent centers, pit-like, several Cladiella species resembles, to a certain extent C. and resemble digit 8. C. ramose Tixier-Durivault, 1970 has hartogi new species, but their sclerites differ from those of dumb-bells up to 0.11 long, head-diameter up to 0.07 mm, the newly-described species. and polyp sclerites with both platelets as above and rod-like ones. C. humesi (Verseveldt, 1974) has dumb-bells, up to 0.13 mm long, with waist occasionally reduced to a mere line, head-diameter up to 0.095 mm and possessing tubercles with spiny processes. C. arbusculoides Verseveldt & Benayahu, 1978 has dumb-bells up to 0.12 mm, with hemispherical heads featuring low undulating processes.

Based on the above comparisons, it is evident that C. hartogi new species has a unique suite of characters, both in terms of colony morphology and sclerites, and that it differs from all previously described congenerics.

DISCUSSION

The present study examined the octocoral fauna of Singapore and is the fi rst one, since Shann (1912) to deal with the fl eshy species. It should be noted that the recent study of Goh et al. (2009) provided only genera names, with no reference to any species. All of the species obtained in our study (Table 1) are either new (i.e. C. hartogi, new species) or new zoogeographical records for Singapore. The survey yielded 25 species distributed among seven genera and fi ve families (Table 1). Sinularia was found to be the most specious genus on the studied reefs, with 12 species followed by Sarcophyton (fi ve species), Lobophytum (two), Cladiella (two) and Heliopora, Studeriotes, Sansibia and Briareum (one each). Similar to many other Indo-Pacifi c reefs (Ofwegen, 2002), Sinularia species are prevalent on Singapore’s reefs, Fig. 5. Underwater photographs of colonies of Cladiella hartogi but their diversity is lower compared, for example, to the new species: a, with expanded polyps; b, with retracted polyps in reefs of South China Sea (32) and Indonesia (28) (Ofwegen their natural habitat.

9 Benayahu and Chou: Octocorallia (Alcyonacea) from Singapore

Fig. 6. Underwater photographs of Singapore octocorals a, Lobophytum crassum von Marenzeller, 1886; b, L. pauciﬂ orum (Ehrenberg, 1834); c, Sarcophyton crassocaule Moser, 1919; d, S. ehrenbergi von Marenzeller, 1886; e, Sarcophyton glaucum (Quoy & Gaimard, 1833); f, Sinularia erecta Tixier Durivault, 1945; g, S. lochmodes (Kolonko, 1926) and h, Carijoa sp.

10 THE RAFFLES BULLETIN OF ZOOLOGY 2010

2002), but higher compared to Hong Kong (two) (Benayahu microclavata Tixier Durivault, 1970 and Sansibia flava & Fabricius, 2010) and the Philippines (seven) (Ofwegen, (May, 1898) were collected in the previous years from Pulau 2002). Shann (1912) described Sclerophytum (= Sinularia) Seringat and Pulau Semakau, sites that were not surveyed pinnulatum from Singapore, which was later synonymized in 1999. Six species were recorded only after the bleaching by Verseveldt (1980) with Sinularia capitalis (Pratt, 1903). (1999 survey), including Heliopora coerulea (Pallas, 1766); The examined material in this study did not contain this Sinularia abrupta Tixier Durivault, 1970; S. compressa Tixier species. The nature of the Singapore Alcyoniidae fauna is also Durivault, 1945; S. erecta, Tixier Durivault, 1970; S. exilis demonstrated by the relatively low number of species found Tixier Durivault, 1945 and S. triangula Tixier Durivault, in the genera Cladiella, Lobophytum and Sarcophyton (Table 1970 (Table 1). These latter species were somewhat scarce 1), which in Indo-Pacifi c reefs typically contribute a much on the reefs and, based on their relatively large colony size higher number of species (e.g., Ofwegen and Vennam, 1994; at the time of collection, we assume that they had probably Benayahu, 1997, 2002; Benayahu et al., 2004). Notably, in survived the bleaching event but for some reason were not Singapore, Sansibia fl ava (May, 1898) was the only species recorded in the past collections. The lack of quantitative of the family Xeniidae (Table 1), although this family plays monitoring data on octocorals does not allow interpretation a much more signifi cant role in both the East and South of the above fi ndings as a result of the catastrophic 1998 China Sea reef systems (e.g., Roxas, 1933; Benayahu et al., bleaching event (Tun et al., 2004; Goh et al., 2009). 2004; Benayahu, unpublished data). Thus, we suggest that the environmental conditions prevailing in Singapore have Because the octocorals of Singapore have experienced led to the paucity of Xeniidae, which require high-clarity degradation and loss due to both natural and anthropogenic water (Fabricius and McCorry, 2006). Notably, the collection pressures (Chou, 1996; Dikou & van Woesik, 2006; Goh et data for the zooxanthellate octocorals found in the current al., 2009), it is imperative to include them in a long-term study indicated that none of them were collected below 4- monitoring programme in the region, and to expand such a 6 m, probably similarly due to the water turbidity and the programme to nearby sites. Undoubtedly, octocoral diversity heavy sedimentation load in Singapore (Chou, 1996; Dikou is indicative of the state of the reef and changes in their & van Woesik, 2006; Goh et al., 2009). Hence, it is also not species composition may illuminate the changing state of surprising that most of the species recorded in the current the health of the reef. survey are typical shallow reef dwellers (i.e. Benayahu, 2002; pers. obser.), whose distribution in Singapore reefs to a deeper depth is hampered by the prevailing water quality. ACKNOWLEDGEMENTS These species include, for example, Lobophytum crassum von Marenzeller, 1886 (Fig. 6a); L. paucifl orum (Ehrenberg, We wish to thank L. P. van Ofwegen for comments on the 1834) (Fig. 6b); Sarcophyton crassocaule Moser, 1919 manuscript. We are particularly grateful to the members of (Fig. 6c); S. ehrenbergi von Marenzeller, 1886 (Fig. 6d); S. the Reef Ecology Study Team, Department of Biological glaucum (Quoy & Gaimard, 1833) (Fig. 6e); Sinularia erecta Sciences, National University of Singapore: Lim Liang Jim, Tixier Durivault, 1945 (Fig. 6f) and S. lochmodes (Kolonko, Uma Sachidhanandam, Angela Dikou, James Guest, Sukee 1926) (Fig. 6g). The azooxanthellate octocoral, genus Carijoa Hajisamae, Sasi Nayar, Koh Li Ling and Adelene Tay Hwee (Fig. 6h) was collected from Pulau Hantu, Changi Sailing Boon for help during the fi eld work. We wish to thank Y. Club and Terembu Pempang Tengah (artifi cial reef) down to Delaria for valuable assistance with the scanning electron 14 m, similarly to other regions (Benayahu, pers. obser.). microscopy, V. Wexler for digital editing, M. Alexandroni for photography, A. Shlagman for the professional curatorial The current study examined octocorals collected between skills and N. Paz for skillful editorial assistance. The fi rst 1993-1997, prior to the 1998 bleaching event (http://coralreef. author was supported by a “Raffles Museum Research nus.edu.sg/; Tun et al., 2004), and also following it, in Fellowship” from the Raffles Museum of Biodiversity 1999 (Table 1). These collections were qualitative and in Research to carry out the fi eld surveys in Singapore. part were conducted at the same reef sites (Table 1: e.g., Pulau Hantu; Pulau Satumu, Raffl es Lighthouse). The 1999 survey was comprehensive and aimed at collecting as many LITERATURE CITED taxa as possible. Out of the 25 species, 12 were obtained at the two time points (Table 1). Seven species that were Benayahu, Y., 1993. Corals of the South-West Indian Ocean I. collected prior to the bleaching were no longer recorded in Alcyonacea from Sodwana Bay, South Africa. Oceanographic 1999 [i.e., Sarcophyton tenuiospiculatum Thomson & Dean, Research Institute Investigational Report, 67: 1–15. 1931; Sinularia capillosa Tixier Durivault, 1970; S. depressa Benayahu, Y., 1997. A review of three alcyonacean families Tixier Durivault, 1970; S. gibberosa Tixier Durivault, (Octocorallia) from Guam. Micronesica, 30: 207–244. 1970; S. microclavata Tixier Durivault, 1970; Studeriotes Benayahu, Y., 2002. Soft corals (Octocorallia: Alcyonacea) of spinosa Thomson & Dean, 1931 and Sansibia fl ava (May, the southern Ryukyu Archipelago: The families Tubiporidae, 1898)]. It is interesting to note the absence of S. capillosa Clavulariidae, Alcyoniidae and Briareidae. Galaxea JSRS, 4: 1–21. and S. gibberosa in the 1999 collection, which based on the large number of samples at the ZRC collected prior to Benayahu, Y. & M. H. Schleyer, 1996. Corals of the South-West the event, had in the past been highly abundant. Sinularia Indian Ocean III. Alcyonacea (Octocorallia) of Bazaruto Island, Mozambique: a redescription of Cladiella australis

11 Benayahu and Chou: Octocorallia (Alcyonacea) from Singapore

(Macfadyen, 1936) and description of Cladiella kashmani Alcyonacea). Journal of Experimental Marine Biology and spec. nov. Oceanographic Research Institute Investigational Ecology, 251: 103–115. Report, 69: 1–22. Koh, L. L., T. K. Tan, L. M. Chou, N. K. C. Goh, 2002. Antifungal Benayahu, Y., A. Shlagman & M. H. Schleyer, 2003. Corals of properties of Singapore gorgonians: a preliminary study. Journal the South-west Indian Ocean VI. Alcyonacea (Octocorallia) of Experimental Marine Biology and Ecology, 273: 121–130. of Mozambique with a discussion on soft corals latitudinal Ofwegen, L. P. van, 1996. Octocorallia from the Bismarck Sea (part distribution along south equatorial East African reefs. II). Zoologische Mededelingen Leiden,70: 207–215. Zoologische Verhandelingen Leiden, 344: 49–57. Benayahu, Y., M. -S. Jeng, S. Perkol-Finkel & C. -F. Dai, 2004. Ofwegen, L. P. van, 2002. 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Soft corals (Coelenterata: shallow water gorgonian-associated fauna on coral reefs in Octocorallia: Alcyonacea) from the Laccadives (SW India), with Singapore. Bulletin of Marine Science, 65: 259–282. a re-examination of Sinularia gravis Tixier-Durivault, 1970. Zoologische Mededelingen Leiden, 70: 437–452. Goh, B. P. L., G. L. Tan & L. T. Tan. 2009. Diversity, distribution and biological activity of soft corals (Octocorallia, Alcyonacea) Verrill, A. E., 1864. List of the polyps and corals sent by the Museum in Singapore. Journal of Coastal Development, 12: 90–99. of Comparative Zoology to other institutions in exchange, with annotations. Bulletin of the Museum Comparative Zoology, at Koh, L. L., N. K. C. Goh, L. M. Chou & Y. M. Tan, 2000. Chemical Harvard, 1: 29–60. and physical defenses of Singapore gorgonians (Octocorallia:

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Verseveldt, J., 1965. Reports on the Octocorallia (Stolonifera and Verseveldt, J., 1980. A revision of the genus Sinularia May Alyonacea) of the South Red Sea expedition 1962, with notes (Octocorallia, Alcyonacea). Zoologische Verhandelingen Leiden, on other collections from the Red Sea. Sea Fisheries Research 179: 1–128. Station, Haifa, Bulletin 40, Israel South Red Sea expedition, Verseveldt, J., 1982. New specirs of Alcyonacea (Octocorallia) 1962, Report no. 14: 28–48. from the Great Barrier Reef, South-east Asia, and the Red Sea. Verseveldt, J., 1971. Octocorallia from North-Western Madagascar Zoologische Mededelingen Leiden, 56: 143–151. (Part II). Zoologische Verhandelingen Leiden, 117: 1–73. Verseveldt, J. & Y. Benayahu. 1978. Description of one old and ﬁ ve Verseveldt, J., 1974. Octocorallia from New Caledonia. Zoologische new species of Alcyonacea (Coelenterata: Octocorallia) from the Mededelingen Leiden, 48: 95–122. Red Sea. Zoologische Mededelingen Leiden, 53: 57–74. Verseveldt. J., 1976. Alcyonacea from the Seychelles (Coelenterata Verseveldt, J. & Y. Benayahu, 1983. On two old and fourteen new Octocorallia). Revue Zoologique Africaine, Bruxelles, 90: species of Alcyonacea (Coelenterata, Octocorallia) from the Red 497–513. Sea. Zoologische Verhandelingen Leiden, 208: 1–33. Verseveldt, J., 1977. Octocorallia from various localities in the Web reference: http://coralreef.nus.edu.sg/ Pacific Ocean. Zoologische Verhandelingen Leiden, 150: 1–42. Verseveldt, J., 1978. Alcyonaceans (Coelenerata: Octocorallia) from some Micronesian Islands. Zoologische Mededelingen Leiden, 53: 49–55

THE RAFFLES BULLETIN OF ZOOLOGY 2010

THE RAFFLES BULLETIN OF ZOOLOGY 2010 58(1): 15 –25 Date of Publication: 28 Feb.2010 © National University of Singapore

ANACLASTOCTEDON (DIPTERA: EMPIDIDAE: HEMERODROMIINAE), A NEW GENUS FROM ASIA AND AUSTRALIA

Adrian R. Plant Department of Biodiversity & Systematic Biology, National Museum of Wales, Cathays Park, Cardiff, CF10 3NP, UK Email: [email protected]

ABSTRACT. – Anaclastoctedon new genus (Diptera: Empididae: Hemerodromiinae) is described from Asia and Australia. Five species are described: A. lek new species, and A. antarai new species from Thailand; A. sano new species from Nepal; A. ancistrodes new species and A. prionton new species from Australia. Three further species from Thailand, Vietnam and Australia were characterized but not described as only females are known. The new genus is placed in the tribe Chelipodini and is characterised by: (a) wing with

long veins R2+3, R4+5, M and CuA1 unbranched; (b) antenna with apical stylus lacking basal articles; (c) epandrium separated from hypandrium; (d) male cercus bilobed with upper lobe greatly enlarged and apically broadened. Habitat, biogeography and relationships with other Chelipodini are brieﬂ y discussed.

KEY WORDS. – Diptera, Empididae, Hemerodromiinae, Anaclastoctedon, new genus.

INTRODUCTION The present work describes a new genus of Chelipodini which is considered to be closely related to Chelipoda The Empididae subfamily Hemerodromiinae contains and Achelipoda but distinguished from them primarily by 15 described genera of small predatory fl ies traditionally characters of the antenna, wing and male genitalia. It has classified into two tribal lineages, Hemerodromiini and been found Nepal, Thailand, Vietnam and Australia. Chelipodini (Sinclair & Cumming, 2006; Plant, 2007). Immature stages of Chelipodini are probably terrestrial in moist soils in damp shaded biotopes including temperate and MATERIALS AND METHODS tropical forests, waterfall splash zones and in the Southern Hemisphere also in wet tussock habitats, whereas immature Southeast Asian material used in this study was collected stages of Hemerodromiini are adapted to living in lotic and during 2006 and 2007 as part of a three year project (TIGER– lentic freshwater biotopes. Two genera of Chelipodini are Thailand Insect Group for Entomological Research) sampling found in eastern Asia, Achelipoda Yang, Zhang & Zhang, terrestrial invertebrates in national parks of Thailand. 2007 which has an exclusively east Asian distribution (Plant, Sampling effort was concentrated in the following mostly 2009b) and Chelipoda Macquart, 1823 which is speciose in northern parks: – Doi Inthanon, Nam Nao, Thung Salaeng the region (Yang & Yang, 2004; Plant, 2009c) but with an Luang, Phu Kradueng, Phu Ruea, Pa Nin Ngam, Phu Phan, almost world-wide distribution excepting the Afrotropical Tat Tone, Pha Taem and Khao Yai. A single specimen was Realm, although the phylogeographic relationships of also found in samples of Hemerodromiinae from Vietnam. lineages within the genus are imperfectly understood (Plant, Specimens from Nepal and Australia were sourced from 2007, 2009a, 2009b, 2009c). A third chelipodine genus CNC, Canada. Phyllodromia Zetterstedt, 1837 also occurs in Asia but the single character distinguishing it from Chelipoda (loss of Repository institutions for material were: – CNC, Canadian crossvein dm-cu) has been interpreted as homoplastic and National Collection of Insects, Ottawa, Canada; IRSNB, which has also occurred in other lineages of Chelipoda sens. Royal Belgian Institute of Natural Sciences, Brussels, lat. and is of doubtful generic signifi cance. (MacDonald, Belgium; NMWC, National Museum of Wales, Cardiff, 1993; Plant, 2005, 2007). The Chelipodini of Australia have UK; MNHN, Muséum national d’Histoire naturelle, Paris, been little studied although Chelipoda and the closely related France; QSBG, Queen Sirikit Botanical Garden, Chiang and possibly congeneric Ptilophyllodromia Bezzi, 1904 are Mai, Thailand; ZRC, Zoological Reference Collection of the present (Hardy, 1930; Plant, 2007). Raffl es Museum of Biodiversity Research at the National University of Singapore. Morphological terms of McAlpine (1981) and Stuckenberg (1999) were employed while

15 Plant: Ananclastoctedon, new genus from Asia and Australia interpretation of genitalic homology follows Cumming et TAXONOMY al. (1995) and Sinclair (2000). Colour descriptions refer to ground colour (i.e. not colour due to pruinosity) unless stated Anaclastoctedon new genus otherwise. Orientation is denoted by – av, anteroventral; pd, Type species, Anaclastoctedon lek, new species posterodorsal; pv, posteroventral. C1, C2 and C3 refer to the (Figs. 1–12) front, mid and hind coxae respectively; F1–F3 and T1–T3 to the corresponding femora and tibiae. To facilitate observations, Diagnosis. – A characteristic genus of the Empididae male terminalia were macerated in hot 85% lactic acid and subfamily Hemerodromiinae with raptorial forelegs widely examined in glycerol. During the process of identiﬁ cation, separated from the mid legs and fore femur bearing Hemerodromiinae were given an alphabetic code and these distinct regular rows of setae ventrally. Anaclastoctedon codes are retained for the three unnamed species (species T X is distinguished from other Hemerodromiinae by the

& Y) which are mentioned at the end of the species accounts combination of (1) all long veins (R2+3, R4+5, M & CuA1) but not formally described as only females were available. linear, unbranched; (2) cell br longer than bm; (3) male In addition to full locality / date / collector data, labels for genitalia strongly reﬂ exed anteriorly over abdomen; (4) material collected by the TIGER Project has a unique data epandrium separate from hypandrium; (5) male cercus free, code (preﬁ xed ‘T’) which is quoted on the label and used greatly enlarged, anteriorly or vertically projected, spade-like administratively within the TIGER Project. apically, usually with smaller pointed internal process basally; (6) postpedicel of antenna short, almost globular with apical stylus at least 4× as long and lacking basal article.

Figs. 1–4. Anaclastoctedon new genus: 1. A. antarai new species, male terminalia. 2–4: A. lek new species. 2. apex of male cercus, internal face; 3. postpedicel and stylus of male; 4. male terminalia. Abbreviations: cer, major lobe of cercus; cip, internal process of cercus; epan, epandrium; hypan, hypandrium; ph, phallus and parameral sheath; sur, surstylus.

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Description. – Head subspherical (Figs. 7, 8), somewhat Thorax. Moderately arched ventrally in profi le (Figs. 7, 8). dorsoventrally fl attened with eyes widely separated on frons; Postpronotum strongly developed, protuberant. Scutum with narrowly separated on face in both sexes, widening towards prescutellar depression broad; supraalar area sometimes mouth; anterior ommatidia slightly enlarged in both sexes. outwardly produced with outer margin rather triangular in A pair of ocellar setae (usually with a few smaller setulae dorsal view. Usually two pairs of dorsocentral setae strongly around ocellar protuberance) and pair of much smaller but developed, anterior pair in line with postpronota, other distinct frontal setae mid way between prominent ocellar slightly anterior of position of notopleurals; often one or protuberance and base of antennae. One pair of distinct two pairs of minute dorsocentrals posteriorly. Supraalar very vertical setae situated close to eye margin. Postocular setae strong, postpronotal and upper notopleural present and usually stout and erect, uniserial, situated some distance behind eye strong. Lower notopleural weak or absent and usually one or margin; uppermost postocular seta sometimes placed on slight more small setae between notopleural and postpronotal areas lateral prominence of vertex between and at same level of weaker still. A pair of scutellar setae present. Laterotergite verticals; series usually becoming weaker and sometimes bearing several setae. 2–3 serial ventrally where sometimes merging into patch of fi ner setae on lower occiput and behind mouth. Legs with front coxa almost as long as thorax (Fig. 7); linear series of setae anteriorly, weak, becoming longer distally and Mouthparts small; proboscis slightly anteriorly directed, no with a few distinct setae at tip. Mid and hind coxae much longer than head is deep, apically pointed. Labellum broadly shorter bearing a few setae laterally and apically in front. ovate bearing fi ne setulae posteriorly. Palpus very small, Front femur as long as front coxa, strongly infl ated, much longer than wide with fi ne but long setulae apically. stouter than other femora, widest at middle; ventrally with double row of strong setae on distal 0.7 between which is Antenna with basal segments as long as wide; scape with double row of short peg-like denticles; dorsal and posterior distinct dorsal seta; pedicel with circlet of setae apically. faces with fi ne setae, anterior face almost bare. Front tibia Postpedicel at most 1.5× long as wide (Fig. 3), almost globular slightly curved, geniculate at extreme base; ventrally with but pointed apically, sometimes appearing rather narrower in single row of minute adpressed denticles which articulate lateral view. Stylus much longer than postpedicel (usually at against corresponding double row of denticles on front least 4× as long), not obviously swollen basally and rather femur when limb is refl exed; an apicoventral ‘fan’ of minute thread-like, almost bare apart from sparse microscopic pile; setulae; otherwise with only short fi ne setulae and scattered basal articles apparently absent. perpendicular cilia (minute erect specialised setae of probable

Figs. 5–8. Anaclastoctedon new genus: 5. A. lek, new species, wing of male; 6. A. antarai new species, wing of female; 7. A. lek, new species, male habitus; 8. A. antarai female habitus. Abbreviation: M2, apical section of vein M2.

17 Plant: Ananclastoctedon, new genus from Asia and Australia sensory function). Mid and hind femora and tibiae rather Cerci free, greatly enlarged, anteriorly or vertically projected, short bearing mostly short setae, longest dorsoapically on spade-like apically (Figs. 1, 2, 4, 9–11); usually with smaller posterior femur and tibia and on mid tibia. Tarsomeres bearing pointed internal process basally (much reduced in A. sano short setulae; longest and strongest anteroventrally on distal new species). Phallus slender, strongly anteriorly directed; segments of mid and hind legs but sometimes longish on front parameral sheath rather broad, often with complex hooked metatarsus. Front tarsomere 1 hardly longer than tarsomere 2, structures apically (Figs. 4, 9–12). the segments becoming progressively and gradually shorter distally with tarsomere 5 slightly fl attened and enlarged; mid Female abdomen with setae sparser and weaker. Cerci and hind tarsal segments similar but tarsomere 1 longer than moderately long, dorsoventrally fl attened (Fig. 8), appearing tarsomeres 1 and 2 combined. narrower in lateral view; bearing some short setae and some longer ones apically. Spermatheca spherical. Male abdomen with tergites 2–6 broad, tergites 7 and 8 reduced. All segments with scattered fi ne setae and longer Wing (Figs. 5, 6) narrow basally with axillary angle hardly setae on tergite 5. Genitalia (Figs 1, 2, 4, 9–12) strongly developed. Vein C circumambient but weak beyond tip of refl exed forward (Fig. 7). Hypandrium greatly enlarged, R4+5. Vein Sc fading apically; R1 rather short, joining C just broader than preceding segments of abdomen, with keel-like beyond end of basal cells. Radio-cubital praefurca short, posterior margin, hypandrial lamellae partially separated linear, not fading basally at junction with R1. Cell br longer posteriorly by narrow micropilose membrane; epandrium than cell bm; cell bm quadrate apically with crossvein bm- smaller, lamellae not fused posteriorly or with hypandrium. cu usually perpendicular (rarely somewhat acute); cell cup

Figs. 9–12. Anaclastoctedon new genus: 9. A. ancistrodes new species, male terminalia; 10. A. sano new species, male terminalia; 11–12. A. prionton new species; 11. male terminalia; 12. apex of parameral sheath, dorsal aspect.

18 THE RAFFLES BULLETIN OF ZOOLOGY 2010

quadrate apically, slightly shorter than bm. Vein A1+CuA2 5. Cell dm open (crossvein dm-cu absent) ...... short, continuing beyond posteroapical margin of cell cup ...... Phyllodromia Zetterstedt but terminating well before wing margin. Crossvein dm-cu – Cell dm closed (crossvein dm-cu present) ...... Chelipoda Macquart absent (cell dm absent). Long veins (R2+3, R4+5 & CuA1) linear, reaching wing margin; vein M usually linear, but occasionally vestige of M2 present at wing margin but completely absent basally (Fig. 6). Marginal cilia short along costa, longer on Key to species of Anaclastoctedon new genus posterior margin. Stigma absent. Basal costal seta present. 1. Very small blackish species (≤1.9 mm); head distinctly dosoventrally fl attened, with dense pile on lower occiput behind Etymology. – The name derives from anaclastos (Greek) mouth [Thailand] ...... A. lek new species meaning reflexed and ctedon (Greek) meaning comb; – Larger blackish or yellowish species (≥ 2.0 mm); head slightly ‘refl exed comb’ in reference to the form of the front leg. dorsoventrally fl attened, with at most only scattered setulae on lower occiput behind mouth ...... 2

Key to genera of Hemerodromiinae from Eastern Asia 2. Ground colour of thorax blackish, (never appearing yellowish

from any viewpoint); T2 with distinct apicoventral seta, clearly The following key should enable recognition of east Asian genera stronger than surrounding setulae; parameral sheath with strong of Hemerodromiinae. The Australian genera are unstudied and recurved dorsal processes ...... 3 poorly understood and are excluded from the key. – Ground colour of thorax yellowish (sometimes appearing blackish from certain viewpoints); T2 without distinct 1. Thorax distinctly elongate; mesonotum usually with only weak apicoventral seta; parameral sheath lacking strong recurved setae dorsally. Laterotergite without setae. Stylus seldom longer dorsal processes ...... 4 than postpedicel. Male terminalia not reﬂ exed anteriorly over abdomen [Hemerodromiini] ...... 2 3. Legs dark yellow; lower postocular setae blackish, weak; wing – Thorax rather quadrate; mesonotum usually with strong setae, membrane and veins brownish; parameral sheath with two at least anteriorly. Laterotergite with setae. Stylus always recurved sharply pointed apical processes [Australia] ...... longer than postpedicel. Male terminalia reﬂ exed anteriorly ...... A. ancistrodes, new species over abdomen [Chelipodini] ...... 3 – Legs pale yellow; lower postocular setae yellowish, strong; wing membrane and veins yellowish; parameral sheath with 2. Cell dm present ...... Chelifera Macquart one sharply pointed apical process [Australia] ...... – Cell dm absent ...... Hemerodromia Meigen ...... A. prionton, new species 4. Scutum clear yellow, with sublateral brown stripes posteriorly 3. Vein M linear. Antenna with stylus lacking basal article. Male [Thailand] ...... A. antarai, new species cercus greatly enlarged ...... – Scutum dirty yellowish, sometimes appearing variably blackish ...... Anaclastoctedon, new genus in certain lights, without darker sublateral stripes [Nepal] ..... – Vein M forked. Antenna with basal article to stylus. Male cercus ...... A sano new species not greatly enlarged ...... 4 Note. – Three species designated T, X and Y are known only from females and although brief descriptions of these are provided to 4. Anal vein absent; CuA2 reaching (or almost reaching) margin; cells br and bm more or less equal in length, quadrate apically facilitate future recognition, they are excluded from the key. with crossveins r-m and bm-cu in line or nearly so ...... Achelipoda Yang, Zhang & Zhang – Anal vein present (if sometimes weak); CuA2 not reaching Anaclastoctedon lek, new species margin; cell br distinctly longer than bm, crossveins closing (Figs. 2–5, 7) them not in line and bm produced posteroapically ...... 5 Material examined. – Holotype. Male, THAILAND: Chiang Mai, Doi Inthanon National Park, Kew Maepan Trail, 18°33.162'N, 98°28.810'E, 2,200 m, Malaise trap, 9–16 Feb.2007, coll. Y. Areeluck (T1795, QSBG).

Paratypes. – Same data as holotype, 8 males, 20 females (QSBG, NMWC); 1 male, 22–29 Dec.2006 (QSBG, T1888); 1 female, 5–12 Jan.2007 (QSBG, T1928); 6 males, 12–19 Jan.2007 (QSBG, T1931); 2 males, 4 females, 23 Feb. –2 Mar.2007 (NMWC, T1771); 4 males, 5 females, 2–9 Mar.2007 (NMWC, T1777); 11 males, 10 females, 16–23 Mar.2007 (NMWC, IRSNB, MNHN, ZRC, T1929); 1 male, 2 females, 16–23 Mar.2007 (NMWC, T1813); 1 male, 2 females, 23 Mar. – 1 Apr.2007 (QSBG, T1819); 2 females, 1–8 May.2007 (QSBG, T1824): Checkpoint 2, 18°31.554'N, 98°29.940'E, 1,700m, 1 male, 22–29 Dec.2006 (QSBG, T1891); 1 male, 29 Dec.2006–5 Jan.2007 (QSBG, T1897); 2 females, 5–12 Jan.2007 (QSBG, T1913); 1 male, 7 females, 2–9 Feb.2007 (QSBG, T1793); 2 females, 16–23 Feb.2007 (QSBG, T1805); 1 female, 23 Feb. –2 Mar.2007 Fig. 13. Known distribution of species of Anaclastoctedon new (QSBG, T1775). Loei, Phu Kradueng National Park, 16°53.092'N, genus.

19 Plant: Ananclastoctedon, new genus from Asia and Australia

101°47.413'E, savannah in pine forest, 1,257 m, coll. T. Srisa-ad, 16 cover of the capture sites probably ensures moist rather cool females, 9–16 Jan.2007 (NMWC, IRSNB, MNHN, ZRC, T1226); 14 conditions throughout the year. An apical remnant of vein females, 16–23 Jan.2007 (QSBG, T1229); savannah near waterfall, M2 is sometimes present at the wing margin, especially in 16°53.443'N, 101°46.946'E, 1,247 m, coll. S. Gongla-sae, 1 male, examples from Loei. The cercus of the single male from 4 females, 28 Dec.2006–3 Jan.2007 (NMWC, T1221). Loei is of slightly different colour and shape to specimens from Chiang Mai but the differences are considered too Diagnosis. – A small species with thorax entirely black. The small to warrant specifi c separation of the Chiang Mai and head is distinctly dorsoventrally fl attened with dense pale Loei populations. pile ventrally. The antenna almost entirely yellow in male but postpedicel black in female. Anaclastoctedon ancistrodes, new species Description. – Male. Length 1.6–1.9 mm. Head distinctly (Fig. 9) dorsoventrally compressed (Fig. 7); black, face paler, all setae whitish yellow; pile behind mouth and on lower occiput long Material examined. – Holotype. Male, AUSTRALIA: NSW, and dense. Mouthparts small, pale; proboscis much shorter Blue Mountains N.P., Blackheath, Govetts Leap [approx. 33°37'S than head is deep, apically darkened. Antenna yellow with 150°17'E], ex. dry scler. / creek, 4 Apr.1994, coll. B. J. Sinclair only apical 0.3 of stylus darkened. Stylus 4× as long as (CNC). postpedicel (Fig. 3). Paratypes. – Same data as holotype: 8 males, 2 females (CNC). Thorax blackish brown, setae yellow; postpronotal setae almost as long as anterior dorsocentral, posterior dorsocentral Diagnosis. – Black species, larger than A. lek new species smaller; upper notopleural and supraalar very large. and with head only moderately dorsoventrally fl attened; distinguished from A. prionton new species primarily by Legs yellow with apical tarsomeres blackish. All setae having wings distinctly brownish, a dark halter and distinctive yellow excepting double row of black denticles ventrally male genitalia. on F1 and single row of black denticles beneath T1. F1 with 4–5 av and 5–6 pv setae, all stout, basal seta of av series Description. – Male. Length 2.5mm. Head moderately sometimes slightly displaced ventrally towards median line dorsoventrally compressed, black, face dusted paler. All and positioned immediately basal of double row of 11–14 setae black, lower postocular setae strong with weaker row in av and 9–11 pv denticles. front close to eye margin, only minute setulae behind mouth. Proboscis blackish, palpus yellow with black seta apically. Abdomen blackish brown; all setae yellowish, longest Basal antennal segments yellow; postpedicel blackish, dorsally on pregenital tergites. Genitalia (Fig. 4) blackish yellowish below; stylus 4–5× long as postpedicel. with phallus and parameral sheath yellow. Major lobe of cercus (Figs. 2, 4) petiolate basally, much broader apically, Thorax black, dusted bluish grey; all setae black, dorsocentrals, with stout spine-like setae and fi ner bristles apically; smaller postpronotal, upper notopleural and supraalar similarly basal lobe apically narrow with small apical spine. Phallus strong. strongly curved apically. Legs brownish yellow, setae black; coxae, F1 dorsally and Wing (Fig. 5) membrane clear, veins yellowish. tibiae obscurely darker; distal tarsomeres brown. F1 very stout, about 5 av and 4–5 pv strong black setae between Female. – Length 1.8–2.3 mm. Similar to male but which are rows of about 17 av and 20 pv denticles; dorsal postpedicel and stylus entirely blackish. F1 with 4–5 av and fringe of setae distinct, longest near base. T2 with strong 5–6 pv setae between which are 11–17 av and 10–12 pv apicoventral seta. denticles. Abdomen blackish brown, becoming rather paler and with longer setae apically. Abdomen brown, rather paler below; sparsely setate, tergite 5 with fan of strong dark setae. Epandrium and hypandrium Etymology. – The specifi c epithet lek (Thai) means small (Fig. 9) dark brown, bearing distinct short setae. Epandrium and refers to the small size of this species. almost circular with short ad lobe bearing regular series of small setulae dorsally. Cercus with major lobe elongate, Remarks. – Known only from northern Thailand on the slightly broader apically, stout spines and strong setae distally; upper slopes of Doi Inthanon, Chiang Mai Province above basal lobe smaller, broadened subapically. Parameral sheath 1,700 m and from about 1,200 m on the mesa sandstone broad with two recurved pointed processes subapically and mountain Phu Kradueng in Loei Province. The Doi Inthanon inverted U-shaped apical process. Phallus dark basally, sites were hill evergreen and moist hill evergreen forests abruptly yellowish distally. while at Phu Kradueng, the habitat was ‘thung’ (savannah grassland) mixed with Pinus. Capture dates range from late Wing membrane vaguely brownish, veins brown; vein M2 December to early May with peak adult activity in February completely absent. Halter greyish-brown. and March coincident with cool dry becoming hot dry general climatic conditions although the high elevation and forest

20 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Female. – Length 2.6–2.8mm. Similar to male but postpedicel especially ventrally. Mid tarsomere 1 with line of minute uniformly dark and tergite 5 without fan of strong setae. erect setulae ventrally. Cercus brownish. Abdomen brownish yellow, paler ventrally, sparsely covered Etymology. – The speciﬁ c epithet ancistrodes (Greek) means with yellow hairs; tergite 5 with stronger yellow setae. Male barbed and refers to the recurved pointed processes on the genitalia (Fig. 1) yellow, hypandrium posteriorly and cercus parameral sheath. apically black. Epandrium and hypandrium bearing longish hairs. Major lobe of cercus petiolate basally, much broadened Remarks – This species is described from the Blue Mountains apically, with ﬁ ne yellow hairs and stout incurved spine-like National Park, New South Wales in eastern Australia during setae apically; smaller basal lobe apically narrow with strong April. The habitat at the type locality is predominantly dry black apical spine. Phallus with short loop apically. sclerophyll forest at about 1,000 m with localised seepages and moisture associated vegetation. Wing (Fig. 6) membrane clear, veins yellow (one wing of

the holotype has short isolated section of vein M2 present at margin but absent in other wing). Halter greyish yellow. Anaclastoctedon antarai, new species (Figs. 1, 6, 8) Female. Similar to male but lacking two narrow stripes on scutum anteriorly and with dark markings on pleura fainter. Material examined. – Holotype. Male, THAILAND: Chiang Abdomen short pubescent, yellow; tergites 2–5 brown. Mai, Doi Inthanon National Park, Checkpoint 2, 18°31.559'N Cercus contrastingly dark brown. Mid tarsomere 1 with short 98°29.941'E, 1,700 m, Malaise trap, coll. Y. Areeluck, 2–10 decumbent setulae ventrally. F3 with a few stronger setae Nov.2006 (QSBG, T389). dorsally near base. Wing with short isolated section of vein M present at margin. Halter whitish. Paratypes. – Same data as holotype, 18°31.554'N, 98°29.940'E, 1 2 female, 24 Nov. –1 Dec.2006 (NMWC, T1870); pan trap, 1 female, 16–17 Nov.2006 (QSBG, T1907). Etymology. – The specific epithet antarai (Thai) means dangerous, in reference to the ﬁ erce raptorial appearance Diagnosis. – A larger species with thorax yellow bearing of the front legs. dark sublateral stripes posteriorly. The head is only slightly dorsoventrally ﬂ attened with only a few setae ventrally. Remarks. –Known only from northern Thailand at 1,700 m on Antenna with basal segments yellow and postpedicel blackish the upper slopes of Doi Inthanon, Chiang Mai Province. in both sexes.

Description. – Length 2.3–2.4 mm. Male. Head moderately Anaclastoctedon prionton, new species dorsoventrally compressed (Fig. 8). Black, somewhat (Figs. 11, 12) shining; face dusted paler. All setae whitish yellow, only a few setae behind mouth and on lower occiput. Mouthparts Material examined. – Holotype. Male, AUSTRALIA: ACT, yellowish, proboscis as long as head is deep. Antenna with Canberra, Black Mountain, CSIRO, 35° 16'S, 149° 06'E, 20 Nov.–6 Dec.1998, coll. G. Gibson YPT (CNC). basal segments yellow, postpedicel blackish, stylus 4–5× as long as postpedicel. Paratypes. – Same data as holotype: 1 male; 1 male, 22–29 Nov. –1998, coll. G. Gibson MT; 1 female 2–8 Nov.1998 (all Thorax clear yellow with scutellum and mediotergite in CNC). brownish. Scutum posteriorly with two sublateral brown stripes commencing dorsal to notopleural area, continuing Diagnosis. – Black species, similar to A. ancistrodes new to posterior margin; anteriorly with two narrower brownish species, distinguished primarily by having wings yellowish, stripes inside line of dorsocentrals, very narrowly separated halter pale and distinctive male genitalia. by median yellow area. Anepisternum posteriorly and katepisternum obscurely brownish. All setae yellow, 2 pairs of Description. – Male. Length 2.5mm. Head moderately dorsocentrals, a postpronotal, upper notopleural and supraalar dorsoventrally compressed, black, dusted greyish; face all strong; irregular line of ﬁ ne setulae between notopleural yellowish. Ocellar, vertical and upper postocular setae black, and postpronotal areas. strong; Lower postocular setae yellowish, strong (particularly below), with weaker row in front close to eye margin. Legs yellow; T1 distally and tarsomeres 1–5 brownish; mid Proboscis yellowish brown, palpus pale with black seta and posterior tarsomeres 5 darkened. All setae yellow except apically. Antenna with scape black, pedicel yellowish brown double row of denticles beneath F1 and single row of denticles or black, postpedicel black; stylus 5× long as postpedicel. beneath T1. F1 dorsally with linear series of rather erect ﬁ ne setae; 4–5 av and 4 pv setae, all stout, basal seta of av series Thorax black, dusted greyish, setae blackish. slightly displaced ventrally towards median line; a double row of 19–21 av and 14 pv denticles positioned between Legs rather pale yellow, distal tarsomeres darker, all setae the large av and pv setae. T2 anteroapically with a few long black. F1 very stout; about 3–5 av and 5–6 pv strong black hairs. Front tarsomeres 1–2 with a few short straggling hairs, setae between which are rows of about 14–15 av and 10–12

21 Plant: Ananclastoctedon, new genus from Asia and Australia

pv denticles. F1 and F3 with distinct dorsal fringe of setae. Thorax ground colour rather variable, usually dirty yellowish,

T2 with strong apicoventral seta. paler on pleura, heavily dusted greyish, appearing almost black in certain light. Setae yellowish black; dorsocentrals, Abdomen brownish yellow, sternites 4–6 sometimes darker. postpronotal, upper notopleural, supraalar and scutellars Tergite 5 with fan of strong dark setae. Epandrium and strong; lower notopleural developed, 0.3× long as upper. hypandrium rather paler than rest of abdomen, bearing distinct setae; parameral sheath darker, black apically; cercus Legs rather pale yellow, apical tarsomeres hardly darker. F1 yellow. Epandrium subcircular, smaller than hypandrium stout, about 5 av and 5 pv strong yellow setae between which (Fig. 11). Cercus with major lobe gradually broadened are rows of about 13–15 av and 11–12 pv black denticles; distally, 6–7 stout black spines apically; basal lobe smaller, dorsal fringe of setae distinct. narrow. Parameral sheath (Figs. 11, 12) long, conspicuously free for most of its length, subapically with curving fl attened Abdomen yellowish brown, tergite 5 with fan of fi ne longish plate-like lateral process from which projects dorsal recurved setae. Genitalia (Fig. 10) brown; epandrium smaller than sharply pointed process; apical process almost detached from hypandrium, subquadrate with long setae posteriorly. Cercus basal part, minutely serrate dorsally about base, broadening with major lobe petiolate basally, broad and bifed distally with at tip. stout spines posteroapically and fi ne setulae anteroapically; basal lobe greatly reduced, inconspicuous. Parameral sheath Wing membrane faintly yellowish, veins brownish-yellow; broadly pointed apically. vein M2 completely absent. Halter yellowish white. Wing membrane distinctly yellowish, veins yellow, basal Female. Similar to male but abdomen darker brown, coastal seta strong. Halter pale yellowish white. postpedicel darker and apicoventral seta on T2 shorter. F1 with denticles rather more numerous, about 15 in pv row. Female. Similar to male but abdomen paler yellowish.

Etymology. – The speciﬁ c epithet prionton (Greek) means Etymology. – The speciﬁ c epithet sano (Nepalese) means serrate and refers to serrate apical process of the parameral small and refers to the small size of this species. sheath. Remarks – This species is known only from a single locality Remarks – This species is known only from Black Mountain in the Nepalese Himalaya at 3,200-3,300 m during April. in Australian Capital Territory in Eastern Australia during The habitat at the type locality is apparently conifer forest November and December. The habitat at the type locality is merging into alpine scrub (I. Juettner, pers. com.). apparently dry sclerophyll forest (G. Gibson via B. Sinclair, pers. com.). Species T

Anaclastoctedon sano, new species Material examined. – THAILAND: Chiang Mai, Doi Inthanon (Fig. 10) National Park, Checkpoint 2, 18°31.554'N 98°29.940'E, 1,700 m, Malaise trap, coll. Y. Areeluck, 1 female 23 Feb.–3 Mar.2007 Material examined. – Holotype. Male, NEPAL: between Ghopte (NMWC, T1775): Phu Kradueng National Park, Loei, Malaise and Thari Pati [Thare Pati], [approx. 28°01'N 85°29'E], 3,200 m, trap, coll. T. Srisa-ad, savannah near waterfall, 16°53.443'N 26 Apr.1985, coll. A. Smetana (CNC). 101°46.946'E, 1,247 m, 1 female, 3–9 Jan.2007 (NMWC, T1224); 2 females, 16–23 Jan.2007 (NMWC, T1230): hill evergreen forest Paratypes. – Four males, 1 female, same data as holotype; 1 at Wang Gwang forest unit, 16°53.362'N 101°47.286'E, 1,262 m, 2 male Nuwakot Dis., betw. Ghopte and Thare Pati 3,200 m, 23–26 females, 3–9 Jan.2007 (NMWC, T1222); 4 females, 16–23 Jan.2007 Apr.[19]85, coll, A. Smetana; 1 male, Bagmati bel. Thare Pati, 3,300 (NMWC, T1228). m, 13 Apr.[19]81, coll. Löbl & Smetana (all in CNC). Diagnosis and Description. – This species resembles A. Diagnosis. – Species with dirty yellowish thorax, appearing antaral new species from which it differs primarily by darker in some lights but lacking obvious dark stripes on the having scutum mostly blackish with black setae. It is only scutum and with distinctive male genitalia. known from females and only a brief description is provided here to facilitate recognition. Length approximately 2 mm. Description. – Male. Length 2.0mm. Head moderately Head black with basal segments of antenna and mouthparts dorsoventrally compressed, black, dusted yellowish grey, yellow; vertical, ocellar and upper postocular setae black; face whitish grey. Setae black with yellowish refl ections; lower occiput with 2–4 strong erect yellow setae behind ocellars conspicuously long, fi ne; lower postoculars 3–4 much weaker lower postoculars. Thoracic dorsum black with serial, fi ne. Proboscis brownish yellow, palpus yellow with notopleuron and lateral margins of scutum yellow. Pleura darker apical seta. Antenna yellow with dark stylus 3× as yellow, katepisternum obscurely darker. All setae black. long as postpedicel which is obscurely darkened, sometimes appearing blackish. Legs yellow with tarsomeres 4–5 darker; dorsal ciliation prominent on F1 and on F3 basally. F1 with approximately 4 av and 5 pv strong setae between which is a double row

22 THE RAFFLES BULLETIN OF ZOOLOGY 2010 of 22 av and 11 pv denticles. Setae and denticles black brown, cerci darker. Wing membrane faintly tinged brown, except basal pv seta which is yellowish. Abdomen brown veins brown. Halter yellowish. dorsally, paler ventrally, with sparse short setae; cercus brown, moderately long. Wing with pale membrane and Remarks – Known only from a coastal sand dune location in brownish veins; short section of vein M2 present at margin New South Wales on the eastern seaboard of Australia. but otherwise completely absent.

Remarks. – Known from 10 females taken at Phu Kradueng DISCUSSION (Loei) and Doi Inthanon (Chiang Mai) in northern Thailand in January and March. The systematic position of Anaclastoctedon new genus in the tribe Chelipodini is demonstrated by a relatively short and distinctly arched thorax with strong setae on the Species X scutum, presence of setae on the laterotergite and male terminalia reﬂ exed anteriorly over the abdomen. The antennal Material examined. – VIETNAM: Lam Dong Province, Bidoup morphology is rather aberrant in Anaclastoctedon in that the – Nui Ba National Park, Hòn Giao Station, near primary rain forest, postpedicel is extremely short and the stylus apparently lacks 12°11'11.3"N 108°42'53.6"E, 1,626 m, light trap, coll. C. Daugeron, a basal article usually present in Chelipodini but probably 1 female, 12 Jun.2008, (MNHN, locality code 2008VIE019). absent in most Hemerodromiini. However as emphasised by Ulrich (1991) and Sinclair & Cumming (2006) the presence Diagnosis and Description – This species is very similar to A. and number of basal articles is subject to homoplasy within antarai new species, from which it differs mainly in thoracic Empidoidea but its absence in Anaclastoctedon is a unique colour and chaetotaxy. Its true identity awaits the discovery apomorphy in Chelipodini. of associated males and only a brief description is provided here to facilitate recognition. Length approximately 2 mm. Anaclastoctedon has similar wing venation to females of Head black, all setae black, only sparse short pile behind the sexually dimorphic genus Monodromia Collin, 1928 mouth. Mouthparts yellow, proboscis much shorter than head from New Zealand which also has all veins unforked and is deep. Basal antennal segments whitish yellow. Thorax no discal cell. However, in Monodromia cells bm and cup entirely clear yellow, setae black; anterior dorsocentral strong, are posteroapically pointed rather than apically quadrate as posterior dorsocentral (in line with notopleuron) very small. in Anaclastoctedon and there are abundant characters of Legs yellow, front tarsomeres 1–5, mid and hind tarsomeres the head, thorax and male genitalia which may be used to 4–5 dark. F1 with double row of black denticles between separate the two genera (Plant, 1993). double row of 4–5 strong yellow setae.

An isolated apical remnant of vein M2 is sometimes present Wing membrane tinged yellowish, veins yellow; cell bm in Anaclastoctedon although it never extends more than with outer angle rather acute. a short distance basally from the wing margin and M is never actually forked (as is the case in Achelipoda which Abdomen brownish-yellow, paler ventrally; cercus yellow, also has otherwise linear long veins and no discal cell but moderately long. has differently proportioned basal cells). Wing venation is notoriously plastic in some Hemerdromiinae (Plant, 2007) and Remarks. – Known from a single female captured in the the intermittent and sometimes even asymmetrical presence of mountains of southern Vietnam in June. a marginal remnant of M2 may indicate that Anactastoctedon is actively in process of losing the fork in M.

Species Y The enlarged keel-like structure of the hypandrium is very similar to the condition found in the Indo Malayan genus Material examined. – AUSTRALIA: NSW, Moonee Beach, 12 km Achelipoda and northern hemisphere forms of Chelipoda N. Coffs Harbour [approx. 30°18'S 153°08'E] ex dune vegetation, 1 Apr.1995, coll. B. J. Sinclair (CNC). (MacDonald, 1993; Plant, 2007; 2009c) suggesting a close relationship between them and Anaclastoctedon. However in Diagnosis and Description – This species is known only both Achelipoda (Plant, 2009b) and most northern hemisphere from a single female and a brief description is provided to species currently attributed to Chelipoda the hypandrium is facilitate future recognition. Length approximately 2.2mm. closely fused with the epandrium whereas in Anaclastoctedon Head black with basal segments of antenna yellow and the plesiomorphic condition in which the two are clearly mouthparts brownish yellow; all setae black, lower postocular separate is present [exceptions being two Nearctic species of setae weakly developed. Thorax brownish yellow dusted Chelipoda where separation of epandrium and hypandrium greyish, somewhat paler on pleura, more clearly yellowish is probably a reversal of the fused condition and in some on postpronotal lobe and propleuron; scutum with narrow southern hemisphere lineages of uncertain relationship with darker median stripe; two dorsocentrals, postpronotal, upper Chelipoda sensu stricto (Plant, 2007; 2009a)]. notopleural supraalar and scutellar setae strong, black. Legs Although bilobed male cerci are present in a few species of yellowish with distal tarsomeres darker; F1 strongly inﬂ ated, ventral spines and denticles black. Abdomen yellowish Chelipodini, for example in Chelipoda ﬂ avida Brunetti and

23 Plant: Ananclastoctedon, new genus from Asia and Australia

C. laisoma Plant, a bilobed cercus in which the upper lobe LITERATURE CITED is greatly enlarged and spade-like apically appears to be a unique apomorphy of Anaclastoctedon. The lower cercal lobe Bezzi, M., 1904. Empididi Indo-Australiani raccolti dal Signor L. is usually long and apically pointed although in A. sano it is Biró. Annales Historico-Naturelles Musei Nationalis Hungarici, greatly reduced and hardly discernable. 2: 320–361. Collin, J. E., 1928. New Zealand Empididae. British Museum Two species groups are tentatively recognized in (Natural History), London, 110 pp. Anaclastoctedon: (1) an Asian group comprising A. antarai, Cumming, J. M., Sinclair, B. J. & Wood, D. M., 1995. Homology A. lek and A. sano in which the upper lobe of the male and phylogenetic implications of male genitalia in Diptera cercus is petiolate basally, the parameral sheath lacks dorsal – Eremoneura. Entomologica scandinavica 26: 121–151. recurved, pointed processes and the mid tibia lacks an Hardy, G. H., 1930. Australian Empididae. Australian Zoologist, apicoventral seta, and (2) an Australian group comprising A. 6: 237–251. ancistrodes and A. prionton in which the upper cercal lobe Heatwole, H. 1987. 5. Major Components and Distributions of the is elongate and not basally petiolate, the parameral sheath Terrestrial Fauna. In: Dyne, G. R. (ed.), Fauna of Australia, has conspicuous recurved pointed processes dorsally and the Volume 1A, General Articles. Bureau of Flora and Fauna, mid tibia has a strong apicoventral seta, clearly distinguished Australian Government Publishing Service, Canberra. Pp from surrounding apical setulae. 101–135. MacDonald, J. F., 1993. Review of the genus Chelipoda Asian Anaclastoctedon species are known from montane Macquart of America north of Mexico (Diptera: Empididae; locations between 1,200 m and 3,300 m in moist forest Hemerodromiinae). Proceedings of the Entomological Society biotopes in Nepal, Thailand and Vietnam (Fig. 13) with of Washington, 95(2): 327–350. a preponderance of records during the dry season. The Macquart, J., 1823. Monographie des insects diptères de la Australian species have a Bassian southeastern temperate famille des empides, observes dans le nord-ouest de la France. distribution with A. ancistrodes and A. prionton present in Recueil des Travaux de la Société d’Amateurs des Sciences, de dry sclerophyll forest on mountains and Species Y on coastal l’Agriculture et des Arts à Lille, 1822,137–165. dune vegetation. Possibly the Australian species are an Old McAlpine, J. F., 1981. Morphology and terminology – Adults Northern Element (Heatwole, 1987) which immigrated from Chapter 2. In: McAlpine, J. F., Peterson, B. V., Shewell, G. Asia as the Australian continent drifted northwards during E., Teskey, H. J., Vockeroth, J. R. & Wood, D.M. (Coords.), the Tertiary. Such elements characteristically have penetrated Manual of Nearctic Diptera, 1. Agriculture Canada Monograph, 27: 9–63. southwards along the eastern Australian ranges (Yeates, et al., 2009) and have typically become isolated in montane Plant, A. R., 2005. The Hemerodromiinae (Diptera, Empididae) of forest refugia, perhaps becoming adapted to increasingly arid New Zealand I. Phyllodromia Zetterstedt. Studia dipterologica 12: 119–138. conditions during the post-Miocene drying. Alternatively, the plesiomorphic separation of the epandrium and hypandrium Plant, A. R., 2007. The Hemerodromiinae (Diptera: Empididae) of is a condition associated with most southern hemisphere New Zealand II. Chelipoda Macquart. Zootaxa, 1537: 1–88. Chelipodini and only rarely found in northern hemisphere taxa Plant, A. R., 2009a. The genus Chelipoda Macquart, 1823 suggesting a southern temperate origin of Anaclastoctedon (Diptera, Empididae, Hemerodromiinae) in Chile. Deutsche with later extension northwards into Asia. Entomologische Zeitschrift, 56(1): 57–71. Plant, A. R., 2009b. Revision of the east Asian genus Achelipoda Yang, Zhang & Zhang, 2007 (Diptera: Empididae: ACKNOWLEDGEMENTS Hemerodromiinae) including designation of a neotype for Achelipoda pictipennis (Bezzi, 1912) and descriptions of six new species. Zootaxa, 2020: 37–50. I thank Bradley Sinclair, Christophe Daugeron and Patrick Grootaert for comments, advice and loan of specimens. For Plant, A. R., 2009c. Diversity of Chelipoda Macquart, 1823 access to TIGER Project material and local expertise in (Diptera: Empididae: Hemerodromiinae) in northern Thailand Thailand I am grateful to Michael Sharkey, Brian Brown, with discussion of a biodiversity ‘hot spot’ at Doi Inthanon. Raffl es Bulletin of Zoology, 57(2): 255–277. Chaweewan Hutacharern and Ratana Lukanawarakul. I gratefully acknowledge the collecting and sorting efforts Sinclair, B. J., 2000. 1.2. Morphology and terminology of Diptera of many staff in Thailand’s national parks and QSBG and male terminalia. In: Papp, L. & Darvas, B. (Eds.), Contributions to a Manual of Palaearctic Diptera 1. General and Applied of Wendy Porras at Instituto Nacional de Biodiversidad, Dipterology. Science Herald, Budapest, pp. 54–74. Costa Rica. Ingrid Juettner’s help with Nepalese geography and language is much appreciated. The TIGER Project is Sinclair, B. J. & Cumming, J. M., 2006. The morphology, higher- level phylogeny and classifi cation of the Empidoidea (Diptera). supported by the USA NSF (grant no. DEB-0542846). Zootaxa, 1180: 1–172. 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.

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Ulrich, H., 1991. Two new genera of parathalassine-like ﬂ ies Yang, D., Zhang, K., Yao, G. & Zhang, J., 2007. World Catalog from South Africa (Diptera, Empidoidea). Bonner Zoologische of Empididae (Insecta: Diptera. China Agricultural University Beiträge, 42: 187–216. Press, Beijing, 599 pp. Yang, D. & Yang, C., 2004. Diptera, Empididae, Hemerodromiinae, Yeates, D. K., Bickel, D., McAlpine, D. K. & Colless, D. H., Hybotinae. In: Fauna Sinica, Insecta 34. Science Press, Beijing, 2009. Diversity, Relationships and Biogeography of Australian 335 pp. Flies. In: Pape, T., Bickel, D. and Meier, R. (eds.), Diptera Diversity: Status, Challenges and Tools. Brill, Leiden, Boston. Pp 227–256.

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THE RAFFLES BULLETIN OF ZOOLOGY 2010 58(1): 27Ð30 Date of Publication: 28 Feb.2010 © National University of Singapore

A SECOND FINDING OF VERCOIA INTERRUPTA KIM & FUJITA, 2004 (CRUSTACEA, DECAPODA, CRANGONIDAE), A REMARKABLE SHRIMP IMITATING DEAD SNAIL SHELLS

Arthur Anker Dickinson Hall, Florida Museum of Natural History, University of Florida, Gainesville, FL, 32611-7800, USA. Email: aanker@ﬂ mnh.uﬂ .edu

ABSTRACT. – Vercoia interrupta Kim & Fujita, 2004, a crangonid shrimp from coral rubble habitats, is reported from Balicasag (Bohol) and Ponson (Cebu), in the central Philippines. This is the ﬁ rst ﬁ nding of this rare species since its discovery in Okinawa and represents a considerable extension of its distribution range southwards. This shrimp also appears to be a remarkable imitator of dead cerithiid shells.

KEY WORDS. – Caridea, Crangonidae, Vercoia, shrimp, shell imitation, Philippines.

INTRODUCTION Aethridae (Aethra), Parthenopidae (e.g. Parthenope, Daldorfia, Heterocrypta), Leucosiidae (e.g., Uhlias, Camoufl age in the form of imitation of shape and colour of Oreotlos, Lithadia), Xanthidae (Glyptoxanthus, Hepatoporus, the surrounding environment has evolved in many families Hypocolpus), Grapsidae (Pseudograpsus, Cyclograpsus), of the large crustacean order Decapoda (Noël, 1999; Ocypodidae (Ocypode) and several other families. The same Debelius, 2001). For instance, many symbiotic decapods camoufl age tactic is used by some dendrobranchiates (e.g., very convincingly imitate the shape and/or the external Sicyonia) and a number of caridean shrimps, mostly from the texture as well as the colour pattern of their living hosts. families Crangonidae (Crangon, Philocheras, Pontophilus, The best-known examples are caridean shrimps, especially Vercoia) and Hippolytidae (Spirontocaris, Trachycaris). in the families Palaemonidae (e.g. Laomenes, Periclimenes, Many crangonid shrimps have very cryptic, sand-imitating Pontonides, Dasycaris, Izucaris), Gnathophyllidae (Levicaris, colour patterns, as well as a dorsoventrally fl attened body Gnathophylloides), Pandalidae (Miropandalus), Hippolytidae and a semi-burrowing life style (Jensen, 1995; Bauer, 2004). (Hippolyte, Tozeuma, Gelastocaris), and Alpheidae (Arete) An alerted crangonid shrimp would quickly submerge most (Debelius, 2001; Minemizu et al., 2001; Bauer, 2004). Many of its body in the sand or mud, except for the frontal region shrimps associated with sea grasses and algae, especially with eyes and the most dorsal portion of the carapace and numerous Hippolytidae (Hippolyte, Latreutes, Heptacarpus, abdomen. Most crangonids are either cold-water or deep- Tozeuma) and some Palaemonidae (Leander), blend in almost water shrimps, with only a few genera, such as Vercoia perfectly with the background when resting on leaves, stems Baker, 1904, found in shallow tropical waters. or algal thalli (Noël, 1999; Debelius, 2001; Bauer, 2004). Host imitation is also not uncommon among brachyuran and Vercoia presently includes four species in the Indo-West anomuran crabs, e.g. in symbiotic species of the families Pacifi c: V. gibbosa Baker, 1904, from southern and eastern Majidae (Hoplophrys), Epialtidae (Xenocarcinus), Portunidae Australia and Marshall Islands; V. socotrana Duris, 1992, (Lissocarcinus, Caphyra), Eumedonidae (Zebrida, Harrovia), from Socotra Island and the Gulf of Aden, Yemen; V. japonica and Porcellanidae (Lissoporcellana, Aliaporcellana) (e.g. Komai, 1995, from Izu Islands, Japan; and V. interrupta Kim Debelius, 2001; Minemizu et al., 2001; Kuiter & Debelius, & Fujita, 2004, from Okinawa, Ryukyu Islands, southern 2009), while some algae-associated Epialtidae (e.g., Mocosoa, Japan (Baker, 1904; Balss, 1921; Devaney & Bruce, 1987; Huenia, Pugettia) are remarkable imitators of Halimeda, Duris, 1992; Komai, 1995; Kim & Fujita, 2004; Duris, 2007). kelp, coralline algae, or other seaweeds (e.g. Jensen, 1995; Despite the wide distribution range of Vercoia, all species Debelius, 2001). of this genus are known from a handful of specimens, in some cases only from the holotype. Imitation of non-living environment, such as sand, rocks or rubble, is also common and widespread among the Decapoda, In 2008 and 2009, two shrimps from the genus Vercoia especially in crabs, including the Calappidae (Calappa), were photographed in situ by Dr. Guido Poppe at two

27 Anker Ð New record of Vercoia interrupta from the Philippines different locations in the central Philippines: the fi rst off Fujita, 2004). Thus, the Balicasag specimen of V. interrupta, Ponson Island, Pilar, Cebu, and the second off Balicasag deposited in the collections of the Oxford University Museum Island near Panglao, Bohol. Only the latter specimen, an of Natural History, Oxford, United Kingdom (OUMNH), is ovigerous female, was collected, preserved in 75% ethanol, the second known specimen of this species, and represents and sent to the author for identifi cation. This specimen was the fi rst record of a species of Vercoia for the Philippines. identifi ed as Vercoia interrupta, a species previously known The carapace length (CL, in mm) was measured along the only from a single holotype, an ovigerous female collected mid-dorsal line from the tip of the rostrum to the posterior at Cape Maeda in Okinawa, at a depth of 8.5 m (Kim & margin of the carapace.

Fig. 1. Vercoia interrupta Kim & Fujita, 2004: AÐD, ovigerous female from Balicasag Island, Panglao, Bohol, Philippines; EÐG, ovigerous female from Ponson Island, Pilar, Cebu, Philippines. A, recently preserved specimen, lateral view; B, same, dorsal view; C, living shrimp in situ, showing microhabitat; D, same, close-up; E, living shrimp (different individual) in situ, lateral view; F, same, dorsolateral view; G, same, anterodorsal view. (CÐG, photographs by Guido Poppe).

28 THE RAFFLES BULLETIN OF ZOOLOGY 2010

TAXONOMY Remarks. – Behavioural observations and photographs of Vercoia spp. are extremely rare. To the author’s best Crangonidae Haworth, 1825 knowledge, the only other published photograph of Vercoia is that of V. gibbosa (Gowlett-Holmes, 2008), which also Vercoia Baker, 2004 seem to mimic shell fragments. All species of Vercoia may be imitators of dead shells or at least shell fragments, based Vercoia interrupta Kim & Fujita, 2004 on their morphological similarity with V. interrupta, although (Fig. 1) the latter species seems to do so most convincingly.

Material examined. – 1 ovigerous female (CL 6.5 mm), OUMNH 2009-18-0046, The Philippines, Bohol, Balicasag Island near ACKNOWLEDGMENTS Panglao, 9¡31'05.07"N 123¡40'52.25"E, early night dive, depth 3Ð5 m, coll. G. Poppe, 26 Jan.2009 [photographed]. The author thanks Dr. Guido Poppe (Conchology Inc., Basak, Lapu-Lapu City, Cebu, the Philippines, and scientiﬁ c Additional specimen observed in situ, not collected. Ð 1 ovigerous female, The Philippines, Cebu, Ponson Island off Pilar, associate of the Royal Belgian Institute of Natural Sciences, 10¡43'54.75"N 124¡31'00.43'E, night dive, rubble, depth 20 m, 12 Brussels, Belgium), who kindly sent him this very interesting Oct. 2008 [photographed]. specimen together with the associated metadata and superb colour photographs, as well as Tomoyuki Komai (Natural Description. – Kim & Fujita (2004) provided an excellent History Museum and Institute Chiba, Japan) for reviewing description of V. interrupta, with numerous illustrations of the manuscript. the adult morphology, as well as the ﬁ rst to fourth zoea.

Colour pattern. – Carapace and abdomen mostly opaque LITERATURE CITED whitish with some greyish areas; walking legs dark purple; antennular fl agella with blackish spot proximally, pale yellow Baker, W. H., 1904. Notes on South Australian decapod Crustacea. distally (Fig. 1). Part I. Transactions and Proceedings and Reports of the Royal Society of South Australia, 28: 146Ð161. Distribution. – Presently known only from the type locality in Balss, H., 1921. Stomatopoda, Macrura, Paguridea and Okinawa, Ryukyu Islands (Kim & Fujita 2004) and Balicasag Galatheidea. Results of Dr. E. Mjöberg’s Swedish Scientifi c (Bohol) and Ponson (Cebu) in the central Philippines Expeditions to Australia, 1910-13. XXXIX. Kungl. Svenska Vetenskapsakademiensis Handlingar, 61: 1Ð24. (present study). The present record of V. interrupta from the Philippines extends its distribution range southwards Bauer, R. T., 2004. Remarkable Shrimps - Adaptations and Natural by around 1,800 km. History of the Carideans. University of Oklahoma Press. Oklahoma City, Oklahoma. 316 pp. Habitat. – Coral rubble with encrusting algae and sponges Debelius, H., 2001. Crustacea Guide of the World. IKAN, Frankfurt. (Fig. 1C), at depths of 3Ð8.5 m, possibly down to 20 m 321 pp. (Kim & Fujita 2004; present study). Devaney, D. M. & A. J. Bruce, 1987. Crustacea Decapoda (Penaeidea, Stenopodidea, Caridea and Palinura) of Enewetak Biology. – Vercoia interrupta uses a rather remarkable Atoll. In: Devaney, D. M., E. S. Reese, B. L. Burch & P. camoufl age strategy. As in other species of Vercoia and Helfrich (eds.), The Natural History of Enewetak Atoll, 2, US Department of Energy, Offi ce of Scientifi c and Technical some other Crangonidae, the body of V. interrupta is lnformation. Oak Ridge, Tennessee. Pp. 221Ð233. compact and heavily sculptured (“bumpy”), being covered with numerous tubercles and several ridges (Fig. 1A, B; see Duris, Z., 1992. Revision of Vercoia Baker (Crustacea: Decapoda: Crangonidae). Invertebrate Taxonomy, 6: 1437Ð1457. also Kim & Fujita 2004), and has a uniform “dirty whitish” colour, the dark purple walking legs being mostly invisible Duris, Z., 2007. New occurrence of Vercoia socotrana Duris, 1992 in dorsal view (Fig. 1B, G). Kim & Fujita (2004) noted that (Crustacea, Decapoda, Crangonidae) in the Gulf of Aden, V. interrupta resembles a “small piece of rubble”, which western Indian Ocean. Senckenbergiana maritima, 37: 1Ð4. would make it cryptic on a rubble bottom. However, by Gowlett-Holmes, K., 2008. A Field Guide to the Marine stretching the abdomen completely, with its tail fan almost Invertebrates of South Australia. Notomares, Sandy Bay, pointing posteriorly (Fig. 1DÐG), the shrimp also remarkably Tasmania. 354 pp. resembles a dead and encrusted cerithiid snail shell, more Jensen, G., 1995. Pacifi c Coast Crabs and Shrimps. Sea Challengers, specifi cally that of Cerithium rostratum G. B. Sowerby II, Monterey, California. 96 pp. 1855, which is common in the area (G. Poppe, pers. comm.). Kim, J. N. & Y. Fujita, 2004. A new species of the genus Vercoia Even when moving V. interrupta resembles a cerithiid shell from Okinawa Island, Japan (Crustacea, Decapoda, Caridea, occupied by a hermit crab more than a shrimp, and would Crangonidae), with descriptions of its zoeal stages. Journal of probably be ignored by most visually hunting predators. Natural History, 38: 2013Ð2031. Night activity (all individuals of V. interrupta were found Komai, T., 1995. Vercoia japonica, a new species of crangonid at night) may further increase the survival chances of this shrimp (Crustacea: Decapoda: Caridea). Natural History peculiar shrimp. Research, 3: 123Ð132.

29 Anker Ð New record of Vercoia interrupta from the Philippines

Kuiter, R. & H. Debelius, 2009. World Atlas of Marine Fauna. Noël, P. Y., 1999. Mimétismes et camouﬂ ages chez les crustacés. IKAN, Frankfurt. 720 pp. Bulletin trimestriel de la Société géologique de Normandie et Minemizu, R., T. Kawamoto & J. Okuno, 2000. Marine Decapod des amis du Muséum du Havre, 86: 15Ð26. and Stomatopod Crustaceans Mainly from Japan. Bun’ichi Sogo, Shuppan, Tokyo. 344 pp.

30 THE RAFFLES BULLETIN OF ZOOLOGY 2010

THE RAFFLES BULLETIN OF ZOOLOGY 2010 58(1): 31–49 Date of Publication: 28 Feb.2010 © National University of Singapore

A REVIEW OF THE SENTINEL AND ALLIED CRABS (CRUSTACEA: BRACHYURA: MACROPHTHALMIDAE), WITH PARTICULAR REFERENCE TO THE GENUS MACROPHTHALMUS

R. S. K. Barnes Department of Zoology, University of Cambridge, Cambridge CB2 1RL, U.K. Email: [email protected]

ABSTRACT. – The systematic position and nature of the erstwhile ocypodid subfamily Macrophthalminae is reviewed; annotated keys to the macrophthalmid subfamilies and genera and to the extant species of the type genus Macrophthalmus are provided; and the subgenera and species groups of Macrophthalmus are described and discussed.

KEY WORDS. – Ocypodoidea, Grapsoidea, Macrophthalminae, key, phylogeny.

INTRODUCTION THE FAMILY MACROPHTHALMIDAE

Much has happened with respect to the systematics of For many years, the genus Macrophthalmus and others Macrophthalmus Desmarest, 1823, in the 30+ years since the believed at the time to be related to it were unquestionably author completed his revision of the genus and produced a regarded as representing a component subfamily of the key to its then-known species (Barnes, 1977). Several new Ocypodidae Rafi nesque, 1815, and were thus thought to species have been described and more is now known about the be relatively far removed systematically from members of distribution, morphology, ecology and behaviour of others; the various genera then considered to form the Grapsidae several name changes have been made; and allozyme and MacLeay, 1838. Indeed, these two families were placed molecular sequence data have challenged our understanding in different superfamilies (Ocypodoidea and Grapsoidea). of relationships both within Macrophthalmus and within This, for example, is the system adopted in the recent the larger group to which the sentinel crabs belong (data classifications of Martin & Davis (2001) and Sakai in Serène, 1977; Lewinsohn, 1977; Manning & Holthuis, (2004). Molecular sequence data produced and analysed 1981; Vannini & Valmori, 1981; Serène, 1981; Henmi, by Kitaura, Wada & Nishida (2002), however, strongly 1984; Tirmizi & Ghani, 1988; Zucker, 1988; Wada & Sakai, suggested that Macrophthalmus is more closely related to 1989; Kosuge, 1991; Takeda & Komai, 1991; Huang, Yu & grapsids of the subfamily Varuninae H. Milne Edwards, Takeda, 1992; Karasawa & Matsuoka, 1992; Fransen, 1998; 1853, and to some genera traditionally regarded as being Apel & Türkay, 1999; Kitaura & Wada, 1999; Jennings, members of the grapsid subfamily Sesarminae Dana, 1851 McLay & Brockenhoff, 2000; Henmi, 2000; Ng, Wang, Ho (i.e. Metaplax H. Milne Edwards, 1852, Cyclograpsus H. & Shih, 2001; Kobayashi & Kato, 2003; Kitaura, Nishida Milne Edwards, 1837, and Helice de Haan, 1833) than it & Wada, 2002; Litulo, 2005; Litulo, Macia & Mantelatto, is to any other crab within the Ocypodidae. This includes 2005; Nagai, Watanabe & Naruse, 2006; Schuwerack, Barnes, to the camptandriids that historically (following Tesch, Underwood & Jones, 2006; Barnes & Davie, 2008; Naruse 1918) had also been included within the Macrophthalminae & Kosuge, 2008; etc., and references cited below). Two Dana, 1851, until they were removed to form a separate new allied genera have also been described (Davie, 1993, subfamily within the Ocypodidae by Serène (1974) and later 2009) and other genera have been transferred into and out in several classifi cations (following Ng, 1988) to comprise of close relationship with Macrophthalmus (see Ng, Guinot a separate family within the Ocypodoidea. Kitaura et al.’s & Davie, 2008 and below). This paper seeks to provide a (2002) conclusions were confi rmed by the sequence data of review of the current systematics of the group in the light of Schubart, Cannicci, Vannini & Fratini (2006) that indicated these developments, and to provide new keys to its genera that Macrophthalmus is indeed more closely related to all and species. grapsids, mictyrids and gecarcinids than it is to the typical ocypodid genera Uca Leach, 1814, and Ocypode Weber, 1795, or to Heloecius Dana, 1851. These sequence data

31 Barnes: Review of the brachyuran genus Macrophthalmus also showed that the erstwhile other ocypodid subfamilies species originally described in Ilyograpsus, are even closer to Camptandriinae Stimpson, 1858, and Dotillinae Stimpson, the Macrophthalminae than proposed by Ng et al. (2008) and 1858 (= Scopimerinae Alcock, 1900) also nestled within a do not warrant separation from them in a distinct subfamily. group of grapsid and gecarcinid lines within the traditional Interestingly in the light of the suggested affi nity between Grapsoidea. Macrophthalmus and the varunids on molecular grounds, the DNA sequence data of Cuesta, Schubart & Felder (2005) also The families Ocypodidae and Grapsidae, let alone the suggest close relationships between some asthenognathines superfamilies Ocypodoidea and Grapsoidea, may therefore and the Varunidae; and Ng et al. (2008) transferred the genus have little real systematic or phylogenetic validity as currently Asthenognathus Stimpson, 1858 to that family. Further, constituted (see also Brösing, Richter & Scholtz, 2007). It must Ng et al. (2008) considered that although seven species of be said, however, that although these analyses of sequence Tritodynamia showed affi nity with the Macrophthalmidae, data may seem completely to overthrow the systematic and two other species currently included in the genus are more phylogenetic status quo, those systematists actually concerned likely to be related to the Varunidae. with the day-to-day business of macrophthalmine, varunine and sesarmine species had long realised how diffi cult it was The Macrophthalmidae is today restricted to the Indo-West in fact to decide wherein some of these species should be Pacifi c, although fossil material of Macrophthalmus is known placed because of the considerable ‘overlap in the familial from former brackish-water deposits in Europe (Provence, defi nitions’ (see, e.g., Davie, 1993). France, and the Austrian Vienna Basin). Remy (1952) thought that Macrophthalmus originated in what is now Nevertheless, Ng et al. (2008) have recently strongly defended the Mediterranean, although apart from a recent Lessepsian the traditional morphological basis of the higher systematic migrant into the eastern part of that sea, the family appears to units within the thoracotrematan Brachyura and they defi antly have become extinct in the region of the Mediterranean basins retained the superfamilies Ocypodoidea and Grapsoidea, in the late Miocene or early Pliocene. An Eocene-Oligocene and included Macrophthalmus as a component genus of the origin considerably further east in the former Tethys Sea Ocypodoidea whilst maintaining within the Grapsoidea the was argued by Barnes (1968). Nevertheless, it is curious grapsid genera associated with Macrophthalmus by Kitaura that within the main subfamily, the Macrophthalminae, three et al. (2002) and Schubart et al. (2006). Their view that a of the four component genera are restricted to Australia, concensus of both molecular and morphological approaches to and so is one of the subgenera of Macrophthalmus whilst the question is both possible and will ultimately emerge (Ng another is known only from New Zealand. Perhaps, as Davie et al., 2008: 214), however, is perhaps over-optimistic in the (2009) suggests, the broad-fronted members of the subfamily light of controversies that have run for more than 10 years comprise a separate lineage, that might then have evolved over the relationships on molecular versus morphological around Australia (although note below that the molecular grounds of some arthropod groups (see, e.g., Giribet & sequence analysis of Kitaura, Nishida & Wada (2006) Ribera, 2000; Cook, Yue & Akam, 2005). Pending further places the broad-fronted subgenus Chaenostoma as a highly phylogenetic analysis of the entire ‘Ocypodoidea’ and derived form descended from narrow-fronted ancestors within ‘Grapsoidea’, the Macrophthalmidae seems best regarded Macrophthalmus). as a separate family within the ocypodoid+grapsoid complex of the Thoracotremata Guinot, 1977 or within the Grapsoidea sensu Rathbun (1918) (see Kitaura et al., 2002), ANNOTATED KEY TO MACROPHTHALMID and likewise the Varunidae (see Schubart, Cuesta & Diesel, SUBFAMILIES AND GENERA 2000; Schubart, Neigel & Felder, 2000; Schubart, Cuesta & Felder, 2002). 1. Carapace without anterolateral teeth, transversely oval or hexagonal with its greatest breadth (which is some twice its On this basis, the Macrophthalmidae comprises the four length) near posterior carapace margin, and with lateral margins genera Macrophthalmus, Australoplax Barnes, 1966, markedly converging anteriorly so that distance between external orbital angles < 60% of greatest carapace breadth; dactyl of Enigmaplax Davie, 1993, and Lutogemma Davie, 2009, external (third) maxilliped large, fl attened, articulating at the together it has been argued (see Ng et al., 2008 for details) base of the propodus, so that palp appears biramous ...... with two other genera that have long been regarded as ...... Tritodynamia (Tritodynamiinae) belonging to other taxa entirely: Ilyograpsus Barnard, 1955 [A group of smallish (< 20 mm carapace breadth) crabs restricted (hitherto usually placed in the Grapsidae: Grapsinae) and to East Asian waters from the South China Sea to the Sea of Tritodynamia Ortmann, 1894 (of the pinnotherid subfamily Japan that typically occur in mud fl ats as commensals in the Asthenognathinae Stimpson, 1858). In the scheme put burrows of sedentary polychaetes, enteropneusts, etc. Naruse & forward by Ng et al. (2008), each of the two latter genera is Ng (2009) are describing a new species of Tritodynamia from placed in its own subfamily within the Macrophthalmidae, Singapore. Yang & Tang (2005) give a key to all the species traditionally included and the group is currently being revised the Ilyograpsinae Stevcic, 2005, and Tritodynamiinae Stevcic, by P. J. F. Davie and N. K. Ng.] 2005, respectively, whilst the more traditionally recognised – Carapace with anterolateral teeth, rectangular, with its greatest macrophthalmid genera then constitute the Macrophthalminae breadth located anteriorly to posterior carapace margin, and Dana, 1851. Komai & Wada (2008), however, have recently with its lateral margins not markedly converging anteriorly, if argued strongly that Ilyograpsus, together with a related new at all, so that distance between external orbital angles > 70% of genus, Apograpsus Komai & Wada, 2008, that they erect for a greatest carapace breadth; dactyl of external maxilliped small,

32 THE RAFFLES BULLETIN OF ZOOLOGY 2010

cylindrical, articulating with distal tip of propodus, so that palp and/or detrital organics, although some scrape algae from hard is uniramous ...... 2 (Macrophthalminae) substrata (Wada & Wowor, 1989; Kosuge & Davie, 2001) or browse macrophytes (Woods & Schiel, 1997); the consumption 2. Carapace longer than broad ...... Apograpsus of living or dead animal material has also been recorded [Monotypic for A. paantu (Naruse & Kishino, 2006), a minute (Kitaura & Wada, 2005). Species of Macrophthalmus most species of brackish-water crab (< 7 mm in largest carapace characteristically dominate sheltered, fi nely particulate, marine, dimension) currently known only from the Ryukyu Islands.] lagoonal and estuarine sediments, both coralline and clastic. – Carapace broader than long ...... 3 Many subtidal species probably await discovery. A key to the males of all living species and subspecies is given below; several 3. Carapace with 4 anterolateral teeth, the fi rst 3 large with external others are known only from fossil material, dating back at least orbital angle and 3rd lateral tooth larger and/or more pointed than to the Miocene. Komai, Goshima & Murai (1995) provide a key 2nd lateral; lateral angle of lower orbital border with S-shaped to the females of the 17 species that occur on the Andaman Sea corner; male cheliped small and with chelae not swollen relative coast of Thailand, although not all Macrophthalmus females to the pereiopods, with tips of fi ngers spooned ... Ilyograpsus can easily be identifi ed to species.] [A group of very small (< 12 mm carapace breadth) crabs that occur intertidally in marine or more usually estuarine conditions, 6. Front broad, its breadth between bases of ocular peduncles > often in association with mangroves, on mud, under stones or 40% distance between tips of external orbital angles; palp of amongst leaf litter in pools, from Mozambique, around the external maxilliped without very long setae on inner margins northern shores of the Indian Ocean and the western shores of the reaching to sternum; legs laterally fl attened ...... Enigmaplax Pacifi c to Japan, to New Caledonia and to Queensland, Australia. [A monotypic genus restricted to the east coast of Australia; E. The genus, currently containing fi ve species viz. I. paludicola littoralis Davie, 1993, being a very small (carapace breadth < (Rathbun, 1909), I. rhizophorae Barnard, 1955, I. nodulosus 10 mm) inhabitant of intertidal and shallow subtidal seagrass Sakai, 1983, I. vannini Sawada, Hosogi & Sakai, 2005, and I. meadows, algal mats and benthic rocks.] daviei Komai & Wada, 2008, is treated in detail by Sawada, – Front narrow, its breadth between bases of ocular peduncles < Hosogi & Sakai (2005) and Komai & Wada (2008).] 30% distance between tips of external orbital angles; palp of – Carapace usually with no more than 3 anterolateral teeth of external maxilliped with very long setae reaching to sternum; which only one or both of fi rst 2 large, the 3rd never larger than legs sub-cylindrical ...... Lutogemma 2nd, if four (or more) teeth present then male chelipeds large [A monotypic genus restricted to the north coast of Australia; L. and longer than pereiopods; lateral angle of lower orbital border sandybrucei Davie, 2009, being a very small (carapace breadth without S-shaped corner; male cheliped usually large and with < 10 mm) inhabitant of shallow subtidal seagrass meadows and greatly developed chelae, but if chelipeds small and chelae not soft sediments in estuaries and the sheltered coastal sea, where enlarged then carapace without 4 anterolateral teeth ...... 4 it presumably suspension feeds using its peculiar elongate maxillipedal setae.] 4. Cutting margins of the fi ngers of the male chelae completely obscured in external view by mat of hair; ischium of external maxilliped with line of hairs running transversely across surface ANNOTATED KEY TO LIVING in proximal half ...... Australoplax MACROPHTHALMUS SPECIES (MALES) [A monotypic genus restricted to the east coast of Australia; A. tridentata (A. Milne Edwards, 1873) being a small (carapace breadth up to 15 mm) inhabitant of intertidal muds, especially 1. With stridulatory apparatus; i.e. with short horny ridge on inner those associated with mangroves.] margin, or on inner surface near inner margin, of cheliped merus, – Cutting margins of fi ngers of chelae visible in external view, & lower orbital border with small number of large triangular without obscuring mat of hair; ischium of external maxilliped protuberances along its outer section occupying at least one without transverse line of hairs across surface ...... 5 fi fth of that margin ...... 2 – Without such stridulatory apparatus, although lower orbital 5. Tips of fi ngers of chelae not spooned, either pointed or fl attened; border may be regularly serrated by granules ...... 7 front either broad (breadth between bases of ocular peduncles > 40% distance between tips of external orbital angles) or, if 2. Carapace and propodus of fourth pereiopod with large spines narrower, then palp of external maxilliped bearing elongate or spiniform tubercles ...... M. dentipes setae extending to sternum ...... 6 [Very large (up to 80+ mm carapace breadth) inhabitant of soft – Tips of fi ngers of chelae spooned; front narrow, its breadth mudfl ats around the Arabian Gulf and Arabian Sea. This species between bases of ocular peduncles < 40% distance between tips was previously widely known under the name M. pectinipes of external orbital angles; palp of external maxilliped without Guérin, 1839 (Holthuis 1995).] elongate setae ...... Macrophthalmus – Carapace and propodus of penultimate pereiopod without large [A widespread and abundant genus occurring throughout the spines or spiniform tubercles ...... 3 Indian and west and central Pacifi c Oceans, from South Africa, Red Sea and Arabian Gulf in the west to Sea of Japan in the 3. Inner surface of palm of chela with large spine near articulation north, to Hawaii and Tuamotu Archipelago in the east, and with carpus ...... M. erato to Tasmania and New Zealand in the south, with one species [Small (< 15 mm carapace breadth) inhabitant of stony mudfl ats now extending into the eastern Mediterranean as a Lessepsian or those with mangrove pneumatophores along the northern migrant (Ksiunin & Galil, 2003; Ates, Katagan & Kocatas, shores of the eastern Indian Ocean, eastern Malesia and the 2006). Several subgenera and some 46 species are currently South China Sea.] recognized, ranging in size from < 10 to > 80 mm carapace – Inner surface of palm of chela without spines ...... 4 breadth, and in habitat from high in the intertidal zone to >80 m depth in the subtidal, and from rocky shores to very soft 4. Anterolateral teeth of carapace narrowly separated from each muds. There the majority deposit feed on microphytobenthos other, their external margins forming a smooth curve ...... M. tomentosus

33 Barnes: Review of the brachyuran genus Macrophthalmus

[Large (up to 35+ mm carapace breadth) Malesian mudfl at 11. Ocular peduncle projecting beyond lateral carapace margin species occurring from Andaman Sea and Taiwan, through the for less than 25% of its length, so that cornea located beyond Philippines to New Caledonia.] lateral carapace margin for no more than its total length ...... – Anterolateral teeth, or at least external orbital angles and second ...... M. ryukyuanus lateral teeth, separated from each other by wide V- or U-shaped [A very small species (up to 10mm carapace breadth) known gap, so anterolateral carapace margins appearing jaggedly only from two specimens dredged from a depth of some 20 m toothed ...... 5 off one of the Ryukyu Islands, Japan.] – Ocular peduncle projecting beyond lateral carapace margin for 5. Inner surface of palm of chela with mat of hair; outer surface at least 25% of its length, so that cornea located beyond lateral of palm and index with row of granules near to and subparallel carapace margin for more than its own length ...... 12 with lower margin ...... M. quadratus [Small (< 12 mm carapace breadth) inhabitant of burrows 12. Terminal segments of last pereiopod fl attened and paddle- or crevices beneath driftwood, stones or around mangrove shaped; with furrow demarcating the front from remaining pneumatophores in scattered localities from Thailand to carapace ...... M. latipes Ryukyu Islands, and through Malaysia and Indonesia to New [Known only from sublittoral material from Seychelles and Caledonia.] Maldives; insofar as is known, very small (< 10 mm carapace – Inner surface of palm of chela without mat of hair; outer breadth).] surface of palm and index without row of granules near lower – Terminal segments of last pereiopod not especially fl attened nor margin ...... 6 paddle shaped; no furrow separating the front from remaining carapace ...... 13 6. Greatest carapace breadth across external orbital angles and/or second lateral teeth; index of chela not defl exed ...... 13. With 4 distinct anterolateral carapace teeth; length of cheliped ...... M. boteltobagoe merus > carapace length ...... M. philippinensis [Very small (< 10 mm carapace breadth) inhabitant of holes [Small (< 12 mm carapace breadth) inhabitant of sublittoral excavated by e.g. sipunculans in limestone rocks and on gravelly sediments; known only from limited material from the mudfl ats from Taiwan and the Ryukyu Islands, Hong Kong to Philippines, Vietnam and Taiwan.] New Guinea.] – With no more than 3 anterolateral carapace teeth; length of – Greatest carapace breadth across third lateral teeth; index of cheliped merus < carapace length ...... 14 chela noticeably defl exed ...... M. holthuisi [Very small (< 10 mm carapace breadth) inhabitant of mud-fi lled 14. Ocular peduncles extend beyond tip of external orbital angle depressions in or around mangrove habitats from the Ryukyu for < 36% of their length and for less than a distance equal to Islands, through Indonesia, to New Guinea.] twice length of cornea ...... M. milloti [Medium-sized (up to 20+ mm carapace breadth) inhabitant of 7. Ocular peduncles with a thin terminal fi lament (style) projecting intertidal soft sediments from east Africa to Hawaii and northern distally beyond the cornea ...... 8 Australia.] – Ocular peduncles without a style ...... 9 – Ocular peduncles extend beyond tip of external orbital angle for > 38% of their length and for more than a distance equal 8. Cornea projecting beyond tip of external orbital angles for only to twice the length of the cornea ...... 15 half its length at most; style short ...... M. graeffei [Medium-sized (up to ca. 25 mm carapace breadth) species 15. With poorly differentiated teeth on cutting margins of chelae; known mainly from scattered sublittoral localities from Samoa, lower margin of index concave; may attain a carapace breadth New Caledonia and New Guinea to the Red Sea and Arabian of >35mm ...... M. telescopicus Gulf, and now also established in the eastern Mediterranean [Large inhabitant of mostly subtidal soft sediments from from Israel to the Aegean Sea.] scattered localities throughout the western and central Pacifi c – Ocular peduncles extremely elongate so that whole cornea Ocean.] located well beyond carapace lateral margins; style long – With distinct teeth on cutting edges of chelae; lower margin of (subequal to rest of peduncle in length) and segmented ...... index straight or convex; carapace breadth < 25 mm ...... 16 ...... M. ceratophorus [Large (up to 45+ mm carapace breadth) species known only 16. Lower margin of index of chela straight; second and third from limited sublittoral material from southern Japan to Taiwan anterolateral teeth of carapace spiniform and sharp; branchial and in Seychelles.] regions with soft pubescence ...... M. serenei [Medium-sized (up to some 25 mm carapace breadth) inhabitant 9. Ocular peduncles extremely elongate, at least half of length of of mostly intertidal soft sediments from scattered localities from cornea located beyond lateral carapace margins ...... 10 the Red Sea and East Africa to southern Japan, the Tuamotus – Cornea not extending beyond lateral margin of carapace for and Lord Howe Island.] half length of cornea, if at all ...... 17 – Lower margin of index of chela with distinct convexity; second and third anterolateral teeth of carapace indistinct and lamellar; 10. Carapace at least twice as broad as long; cheliped merus with branchial regions naked (sublittoral) ...... M. microfylacas long spines on all its margins ...... M. transversus [Small (< 15mm carapace breadth) inhabitant of coralline [Medium-sized (carapace breadth up to ca. 25 mm) species sediments from shallow sublittoral localities in Japan.] known from soft intertidal sediments around the Bay of Bengal, Andaman Sea and Strait of Malacca.] 17. Carapace with 4 or 5 anterolateral teeth, external orbital angle – Carapace less than twice as broad as long; cheliped merus with largest and marking position of greatest carapace breadth; or without granules or tubercles but never with long spines .. carapace smooth and shiny ...... M. dentatus ...... 11 [Small (< 15 mm carapace breadth) inhabitant of sublittoral sites scattered through the South China Sea from Hainan Island to Timor.]

34 THE RAFFLES BULLETIN OF ZOOLOGY 2010

– Carapace with 2–4 anterolateral teeth, if 4 present then carapace 26. Outer surface of palm of chela with large hemispherical tubercles surface heavily granular and external orbital angles not marking over upper half ...... M. abbreviatus position of greatest carapace breadth ...... 18 [Large (up to 35+ mm carapace breadth) inhabitant of muddy sandfl ats from South China Sea to southern coasts of Korea and 18. Central region of epistome with a protuberance ...... 19 Japan. Before 1981, M. abbreviatus was widely known under – Central region of epistome straight or with a concavity .... 31 the name M. dilatatus (de Haan, 1835).] – Outer surface of palm of chela finely granular, without 19. Inner surface of palm of chelae with at least 1 spine near hemispherical tubercles over upper half ...... M. crassipes articulation with carpus ...... 20 [Large (carapace breadth >35 mm) inhabitant of muddy sandfl ats – Inner surface of palm of chelae without spines ...... 27 from northern and eastern Australia to the Carolines and Hainan Island.] 20. Merus of cheliped with granules or tubercles on its margins, but without spines except, in some, around distal angle of inner 27. External orbital angle larger than and projecting beyond second margin ...... 21 anterolateral tooth; carapace breadth twice carapace length; – Merus of cheliped with spines on some or all of its margins, branchial regions with clumps of granules ...... 28 not counting any around distal angle of inner margin ...... 22 – External orbital angle smaller than and not projecting as far as second anterolateral tooth; carapace breadth 1.5 × carapace 21. External orbital angle very small and projecting less than second length; branchial regions without clumps of granules (although anterolateral tooth ...... M. grandidieri rows of granules may be present) ...... 30 [Large (up to 35 mm carapace breadth) inhabitant of muddy sandfl ats and seagrasses along eastern coast of Africa from 28. Chelae large & elongate (equivalent to those of other species) South Africa to Gulf of Oman.] with clearly differentiated teeth on cutting margins of fi ngers – External orbital angle elongate and more or less projecting ...... M. convexus equally with second anterolateral tooth ...... M. brevis [Large (carapace breadth up to 35 mm) inhabitant of high-level [Medium-sized (up to 30 mm carapace breadth) inhabitant of sand- or mudfl ats from the Andaman Sea and Ryukyu Islands, fi rm muddy sandfl ats from Bay of Bengal to Ryukyu Islands through Malesia to Hawaii, the Tuamotu Archipelago and and Malesia.] Queensland.] – Chelae small and feeble (as in female Macrophthalmus) with 22. Cutting margin of index of chelae with 2 teeth, one near tip; poorly differentiated or no teeth ...... 29 external orbital angle and second anterolateral tooth separated by wide incision ...... 23 29. Index of male chela with poorly differentiated, long low tooth – Index of chelae with 1 tooth on its cutting margin, without one along proximal half of cutting margin; tip of male fi rst pleopod near tip; external orbital angle and second anterolateral tooth prolonged ...... M. parvimanus separated by a narrow incision ...... 24 [Medium-sized (carapace breadth up to 30 mm) inhabitant of mudfl ats at scattered localities from East Africa through 23. Lines of tubercular granules on branchial regions hook-shaped; the Indian Ocean and Malesia as far east as the Solomon dactylus of chelae with mat of hair over whole or almost whole Islands.] of inner surface ...... M. laevimanus – Index of male chela with small, quadrangular tooth in centre [Medium-sized (carapace breadth > 25 mm) inhabitant of muddy of cutting margin; tip of male fi rst pleopod truncated ...... sandfl ats around the Bay of Bengal and Strait of Malacca.] ...... M. consobrinus – Granules on branchial regions in clumps or lines but not in [Medium-sized (carapace breadth up to 30 mm) inhabitant of hook-shaped rows; inner surface of dactylus of chelae without river-mouth mudfl ats in the Gambier Islands in the Central mat of hair ...... M. laevis Pacifi c Ocean.] [Large (carapace breadth >30 mm) inhabitant of muddy sandfl ats in the Arabian Gulf and Arabian Sea.] 30. Index of chela without a tooth on cutting margin; outer surface of palm and index of chela with longitudinal ridge near to and 24. Second anterolateral tooth projecting markedly beyond external subparallel with lower margin ...... M. latifrons orbital angle ...... 25 [Medium to large (up to 30+ mm carapace breadth) mudfl at – External orbital angle projecting as far as second anterolateral species restricted to south-eastern Australia.] tooth ...... 26 – Index of chela with a large, wedge-shaped tooth on cutting margin; outer surface of chela without longitudinal ridge near 25. External orbital angle projecting < half as far as second lower margin ...... M. teschi anterolateral tooth; tip of cornea projecting distinctly beyond [Medium-sized (up to 25 mm carapace breadth) inhabitant of tip of second anterolateral tooth; index of chela with distinct mudfl ats through western Malesia.] quadrangular tooth on cutting margin ... M. sulcatus sulcatus [Medium-sized (up to 30mm carapace breadth) inhabitant of 31. Merus and ischium of external maxilliped subequal (length of muddy sandfl ats in Arabian Gulf and Arabian Sea.] ischium < 1.4×length of merus); front broad (its breadth across – External orbital angle projecting > half as far as second base of ocular peduncles > 20% of distance between tips of anterolateral tooth; tip of cornea not projecting beyond tip of external orbital angles) ...... 32 second anterolateral tooth; index of chela with indistinct, very – Merus of external maxilliped distinctly smaller than ischium low to slightly dome-shaped tooth on cutting margin ...... (length of ischium > 1.5 × length of merus); front narrow (its ...... M. sulcatus malaccensis breadth across bases of ocular peduncles < 18% of distance [Medium-sized (up to 30 mm carapace breadth) inhabitant of between tips of external orbital angles) ...... 34 muddy sandfl ats in the Bay of Bengal and western Malesia, where it replaces M. sulcatus sulcatus.] 32. Cheliped carpus with large pointed protuberance on upper margin; medium to large-sized (up to 30+ mm carapace breadth); restricted to New Zealand ...... M. hirtipes

35 Barnes: Review of the brachyuran genus Macrophthalmus

[Associated with low-tidal level sandy mudfl ats and with the 39. Greatest carapace breadth across external orbital angles, where seagrass Zostera sp. in estuaries and lagoons; often relatively breadth > 1.7 times carapace length; outer surface of palm and nomadic and not occupying permanent burrows.] index of chela with longitudinal ridge near lower margins; index – Cheliped carpus without protuberance on upper margin; small defl exed ...... M. setosus (< 15 mm carapace breadth); not occurring in New Zealand . [Large (up to 40mm carapace breadth) mud-burrowing species ...... 33 restricted to east coast of Australia.] – Carapace broadest posterior to external orbital angles, where 33. Carapace surface granular ...... M. boscii breadth < 1.7 times carapace length; if longitudinal ridge present [Widespread species usually occurring under stones, in rock on outer surface of palm and index of chela then index not crevices or in sandy tide-pools at high tidal levels in rocky areas defl exed ...... 40 from eastern shores of Africa to Japan, Australia and Fiji.] – Carapace surface without granules ...... M. punctulatus 40. Whole inner surface of palm of chela obscured by mat of [Inhabitant of high-shore mud and stony areas, restricted to hair ...... 41 south-western and eastern Australia.] – At least part of inner surface of palm of chela free from thick hair ...... 42 34. Inner surface of palm of chelae without mat of hair ...... 35 – Inner surface of palm of chelae with mat of hair concealing at 41. Central region of epistome straight; index with large wedge- least part of surface ...... 38 shaped tooth on its cutting margin ...... M. teschi [Medium-sized (up to 25 mm carapace breadth) inhabitant of 35. Dactylus of chela with very large tooth near centre of cutting mudfl ats through the Bay of Bengal and western Malesia.] margin; inner surface of palm of chelae with longitudinal row – Central region of epistome with distinct concavity; index with of hairs near to and subparallel with upper margin ...... low poorly-differentiated tooth on cutting margin ...... M. barnesi ...... M. depressus [Known only from limited material from depths of 10+ m from [Large (up to 35+ mm carapace breadth) inhabitant of mudfl ats Taiwan, Philippines, New Guinea and Seychelles; existing through the western Indian Ocean.] material probably of no more than young adults, < 25 mm carapace breadth.] 42. Inner surface of palm of chela with longitudinal band of hair – Dactylus of chela with tooth near base of cutting margin; inner along upper half; index of chela defl exed ...... M. pistrosinus surface of palm of chelae without row of hairs as above .. 36 [Medium to large-sized (carapace breadth >30+ mm) inhabitant of sandy mudfl ats in Shark Bay, Western Australia.] 36. Branchial regions of carapace without distinct longitudinal – Hair on inner surface of palm of chela not as above; index of rows of granules; carapace margins smoothly converging chela scarcely or not at all defl exed ...... 43 anteriorly ...... M. abercrombiei [Only fi ve specimens of this species currently known, from the 43. Outer surface of index of chela with longitudinal granule-capped shores of the Torres Strait and Gulf of Carpentaria; existing ridge running along centre, subparallel with lower margin .... material obtained from the shallow sublittoral and (though adult) ...... M. crinitus is < 20 mm carapace breadth.] [Medium-sized (up to 25 mm carapace breadth) inhabitant of – Branchial regions of carapace with distinct longitudinal mudfl ats scattered from the Gulf of Aden, through Malesia to rows of granules; carapace margins not smoothly converging southern Japan.] anteriorly ...... 37 – Outer surface of index of chela without longitudinal ridge ...... 44 37. External orbital angle rectangular, not projecting as far as second lateral tooth and not directed anteriorly ...... M. japonicus 44. Cutting margin of index of chela with a differentiated tooth; [Large (up to 40 mm carapace breadth) inhabitant of mudfl ats carapace breadth < 40 mm ...... 45 from Japan and Korea to Singapore. Tai & Song (1984) divided – Cutting margin of index of chela without a differentiated tooth, this species into two subspecies but stated that ‘In many areas, except in individuals of > 45 mm carapace breadth ...... 47 there are intermediate forms. Absolute separation of these forms is often impossible.’: for these reasons, this proposed subdivision 45. Carapace with thick hair laterally and longitudinal rows of hairs is not followed here.] on branchial regions ...... M. darwinensis – External orbital angle pointed, directed partly anteriorly [Little-known inhabitant of mangrove-associated mudfl ats in and projecting as far as second lateral tooth (sibling species northern Australia and New Caledonia, all existing material of the above, differentiated more behaviourally than < 15 mm carapace breadth.] morphologically) ...... M. banzai – Carapace without thick lateral hair and without longitudinal [Medium-sized (up to 30 mm carapace breadth) inhabitant of rows of hairs branchially ...... 46 mudfl ats from Japan and Korea to Taiwan and south coast of China.] 46. Cutting margin of index of chela with distinct, tall, prominent tooth ...... M. leptophthalmus 38. Carapace with concave granular row on each protogastric [Known for certain only from northern shores of the Bay region ...... M. defi nitus of Bengal; limited existing material all < 25mm carapace [Large (exceeding 30 mm carapace breadth) inhabitant of breadth.] mudfl ats from the Andaman Sea and around the western rim – Cutting margin of index of chela with indistinct, long, low, of the Pacifi c Ocean from the Ryukyu Islands to the Solomon crenulated tooth ...... M. dagohoyi Isles and Queensland.] [Small (< 20 mm carapace breadth) inhabitant of shallow subtidal – Carapace without concave granular rows on protogastric organic muds in Bohol, Philippines.] regions ...... 39

36 THE RAFFLES BULLETIN OF ZOOLOGY 2010

47. Carapace smooth to naked eye; inner surface of dactylus of external orbital angles; ischium of external maxilliped > 1.7 chela without mat of hair ...... M. pacifi cus times length of merus; carapace with breadth ca. 1.3 times [Medium-sized (up to 25 mm carapace breadth) inhabitant of length, with lateral margins converging anteriorly, so that (often mangrove-associated) mudfl ats around the western Pacifi c greatest carapace breadth occurs posterior to anterolateral rim from Korea to northern Australia and Samoa, and on both teeth, with small, blunt anterolateral teeth, without specifi c sides of the Malay-Thai peninsula (and possibly India).] – Carapace surface heavily granular; inner surface of dactylus of system of rows or clumps of granules or hairs on branchial chela heavily haired ...... M. latreillei regions; central region of posterior border of epistome [Very large (up to 60+ mm carapace breadth) inhabitant of concave; fi ngers of male cheliped short with index straight low shore and subtidal muds from Mozambique to Japan and or slightly upcurved and with differentiated teeth on both Australasia.] dactylus and index. Shallow subtidal.

Euplax contains two species: M. leptophthalmus (H. Milne SUBGROUPS WITHIN THE GENUS Edwards, 1852) (type species) and M. dagohoyi Mendoza MACROPHTHALMUS & Ng, 2007. The name M. gastrodes Kemp, 1915, was considered by Barnes (1977) to be a synonym of M. It is evident that morphologically the species keyed out leptophthalmus, a view shared by Mendoza & Ng (2007), above fall into a number of distinct clusters or subgroups but Ng et al. (2008) list it, presumably erroneously, as a valid spanning a wide range in body form, several of which have species within the subgenus Venitus (below). The separation been given subgeneric rank; indeed intrageneric diversity of this subgenus from Venitus is discussed by Mendoza & within Macrophthalmus must be one of the greatest in the Ng (2007). Brachyura.

Macrophthalmus (Hemiplax) Heller, 1865 Macrophthalmus (Chaenostoma) Stimpson, 1858 (Fig. 1C) (Fig. 1A) Medium-sized, up to 30+ mm carapace breadth; ocular Small, carapace breadth < 15 mm; ocular peduncles short peduncles short and stout, not projecting beyond lateral and stout, not projecting beyond lateral carapace margins, carapace margins, subequal in length to breadth of front subequal in length to breadth of front or shorter; front or shorter; front very broad, not constricted between bases broad, not constricted between bases of ocular peduncles, of ocular peduncles, where its breadth is ca. 35% the where its breadth is 20–30% the distance between external distance between external orbital angles; ischium of external orbital angles; ischium of external maxilliped some 1.25 maxilliped some 1.3 times length of merus; carapace with times length of merus; carapace with breadth < 1.3 times breadth ca. 1.5 times length, with lateral margins diverging length, with lateral margins parallel, with broad-based anteriorly, with large, broad-based, pointed anterolateral teeth, subrectangular anterolateral teeth, without conspicuous branchial regions with rows of granules including oblique aggregations of granules into rows or clumps on branchial row extending from 3rd anterolateral tooth to position above regions; central region of posterior border of epistome insertion of 4th pereiopod and transverse row extending from straight; males without stridulatory apparatus; fi ngers of tip of 3rd anterolateral tooth; central region of posterior border male chela short with index straight or slightly downfl exed, of epistome straight; males without stridulatory apparatus; and with a differentiated tooth only on dactylus. Intertidal, fi ngers of male chela elongate with index downfl exed and a but unusually for Macrophthalmus, mainly associated with differentiated tooth only on dactylus; breadth of base of male rocky or stony habitats. telson < breadth of 6th abdominal segment. Intertidal.

Two species are included in Chaenostoma (= Mopsocarcinus Hemiplax is a monotypic subgenus for M. hirtipes (Jacquinot, Barnes, 1967): M. boscii Audouin, 1825 (type species) and in Hombron & Jacquinot, 1846), restricted to New Zealand, M. punctulatus Miers, 1884. This subgenus was suggested the only macrophthalmid in that region. Its zoeal larval stage by Barnes (1967) to approximate the form of the ancestral is similar to that of Heloecius cordiformis (H. Milne Edwards, Macrophthalmus, but the molecular sequence analysis 1837) (currently in the monotypic family Heloeciidae) but of Kitaura, Nishida & Wada (2006) places it as a highly is unlike those of the other Macrophthalmus species so far derived form. investigated (Wear, 1968; Fielder & Greenwood, 1985), albeit that the larval stages of relatively few species are known.

Macrophthalmus (Euplax) H. Milne Edwards, 1852 (Fig. 1B) Macrophthalmus (Macrophthalmus) Desmarest, 1823 (Figs. 2A, 2B, 2C; 3A, 3B) Small to medium-sized (< 25 mm carapace breadth); corneas reduced, ocular peduncles elongate but not projecting beyond Large, up to 40 mm carapace breadth; ocular peduncles lateral carapace margins, much longer than breadth of front; elongate to extremely elongate, projecting or not projecting front narrow but not constricted between bases of ocular beyond lateral carapace margins, much longer than breadth peduncles, where its breadth is ca. 15% the distance between of front; front narrow, constricted between bases of ocular

37 Barnes: Review of the brachyuran genus Macrophthalmus peduncles, where its breadth is 7–17% the distance between clumps of granules longitudinally aligned; central region of external orbital angles; ischium of external maxilliped > 1.7 posterior border of epistome with a central protuberance; times length of merus; carapace with breadth > 1.5 and usually fi ngers of male chelae short to elongate with index straight or > 2 times length, with large, well-developed, outwardly downfl exed, differentiated teeth on both dactylus and index, directed, pointed anterolateral teeth of which external inner surface of palm often with large spine near joint with orbital angle often narrowly-based, with lateral margins carpus. Intertidal to subtidal, the intertidal species usually in diverging anteriorly, branchial regions without longitudinal fi rmer, sandier substrata than those inhabited by Mareotis. or transverse granular rows of granules but with three distinct

Fig. 1. Form of the carapace and adult male chela of subgroups of the genus Macrophthalmus I: (a) subgenus Chaenostoma, (b) subgenus Euplax and (c) subgenus Hemiplax. Scale bars = 5mm.

38 THE RAFFLES BULLETIN OF ZOOLOGY 2010

The type subgenus contains 21 species, divisible into Crosnier, 1965, M. philippinensis Serène, 1971, M. ryukyuanus two speciose groups and three small ones, two of them Naruse & Kosuge, 2008, M. serenei Takeda & Komai, 1991 monotypic: (‘M verreauxi H. Milne Edwards, 1848’ in Barnes, 1976; 1977) and M. telescopicus (Owen, 1839). In these species (Fig. 2A), the ocular peduncles are extremely elongate so The Macrophthalmus telescopicus group that part of, and usually all, the cornea is positioned beyond the lateral carapace margins and in several of the species This comprises: M. ceratophorus Sakai, 1969, M. graeffei the peduncle projects beyond the carapace for half its total A. Milne Edwards, 1873, M. latipes Borradaile, 1903, M. length; the tip of peduncle also sometimes bears a terminal microfylacus Nagai, Watanabe & Naruse, 2006, M. milloti style projecting beyond the cornea. Other distinguishing

Fig. 2. Form of the carapace and adult male chela of subgroups of the genus Macrophthalmus II, the subgenus Macrophthalmus part 1: (a) M. telescopicus group, (b) M. brevis group, and (c) M. convexus group. Scale bars = 5mm.

39 Barnes: Review of the brachyuran genus Macrophthalmus features include: front relatively broad (breadth 13-17% that Macrophthalmus transversus of carapace); carapace moderately broad (breadth = 1.5–1.7 × length), with three variably-developed but usually spiniform The intertidal type species of the genus, M. transversus anterolateral teeth; male chela without spine near carpal joint, (Latreille, 1817) (Fig. 3A), does not fi t easily into any of with short fi ngers and undefl exed index. A mainly sublittoral the three subgroups above, although it does possess the group (in depths of up to 80m), though M. milloti and M. typical broad carapace (breadth > 2 × length) and narrow serenei are common intertidally. front (breadth ca. 12% that of carapace) of the subgenus. It has extremely long ocular peduncles with projecting corneas like the M. telescopicus group and anterolateral teeth The Macrophthalmus brevis group equivalent to those of the M. brevis group, but is singular in its elongate, defl exed and highly laterally fl attened, blade-like This comprises: M. abbreviatus Manning & Holthuis, 1981, chelae which bear spiniform teeth on their cutting margins; M. brevis (Herbst, 1804), M. crassipes H. Milne Edwards, the chelae, however, do bear the typical spine of the M. 1852, M. grandidieri A. Milne Edwards, 1867, M. laevimanus brevis group on the palm near the carpal joint. The carapace, H. Milne Edwards, 1852, M. laevis A. Milne Edwards, 1867 chelipeds and pereiopods also bear tubercles and spines to a and M. sulcatus H. Milne Edwards, 1852 which is divisible degree greater than any other species in the genus except the into a western M. sulcatus sulcatus and an eastern M. sulcatus very large M. (Venitus) dentipes (Barnes, 1970). malaccensis Tweedie, 1937 (see Barnes 1970 for details under the name M. dilatatus sulcatus). In this group (Fig. 2B), the corneas are not positioned beyond lateral carapace margins Macrophthalmus dentatus and no style is present; carapace very broad (breadth > 2 × length), with a small pointed external orbital angle and larger, The equally singular M. dentatus Stimpson, 1858 (Fig. 3B), broad-based, fl at, second lateral tooth; front narrow (breadth only known from sublittoral material, similarly possesses < 14% that of carapace); male chela with spine/s near carpal the characteristic broad carapace (greatest breadth 2 × joint, with elongate and usually downfl exed fi ngers. Intertidal length), narrow front (breadth 10% that of carapace) and in muddy sandfl ats. The names M. gallardoi Serène, 1971, elongate but not projecting ocular peduncles of the subgenus M. hilgendorfi Tesch, 1915 and M. sandakani Rathbun, 1914 Macrophthalmus, but although it otherwise shares some listed by Ng et al. (2008) as extant species are still, as earlier features with the M. telescopicus group (extremely elongate (Barnes, 1977), regarded by this author as being synonyms cheliped meri, short undefl exed fi ngers on the chelae) it is of species within this group. aberrant within the genus in possessing 4-5 anterolateral teeth occupying most of the lateral carapace margins, of which the external orbital angle is very large and fl aring forwards The Macrophthalmus convexus group and outwards, and in details of its carapace granulation, external maxilliped structure, and some other features (see This intertidal group comprises only M. consobrinus Nobili, Barnes, 1971). 1906, M. convexus Stimpson, 1858 and M. parvimanus Guérin, 1834 (Fig. 2C). Although broadly similar to the M. brevis group above, it was shown to be separate by allozyme Macrophthalmus (Mareotis) Barnes, 1967 and molecular sequence data (Horii, Kitaura, Wada & (Figs. 3C, 4A) Nishida, 2001; Kitaura et al., 2006), and morphologically it differs from them in possessing a large, fl at, forwardly curved Large, up to 40 mm carapace breadth; ocular peduncles external orbital angle and in lacking the spine on the palm of elongate but not projecting beyond lateral carapace margins, the male chela. Like the M. brevis group, however, the corneas much longer than breadth of front; front narrow, usually do not project, the carapace is broad (breadth > 2 × length) constricted between bases of ocular peduncles, where its and the front narrow (breadth < 10% that of carapace). The breadth is 8–15% distance between external orbital angles; status of the various isolated geographical populations of M. ischium of external maxilliped > 1.5 times length of merus parvimanus is currently somewhat uncertain. It is possible (usually 1.7–2.5 times); carapace with breadth 1.3–1.7 times that several populations of M. convexus have given rise to M. length (and in one species > 1.8 times length), with large, parvimanus-like forms in different areas. Poupin (e.g. 1997) broad-based, subrectangular anterolateral teeth, with lateral has been followed here and the Gambier Islands form, M. margins subparallel or arched (so that greatest carapace consobrinus, included as a distinct species, pending revision breadth not across external orbital angles or even second of the group. The M. convexus group is closely allied with anterolateral teeth), with longitudinal and/or transverse rows the M. telescopicus group on both allozyme and molecular of granules and/or hairs on branchial regions but without sequence data, and the two appear only distantly related to the clumps of granules; central region of posterior border M. brevis group (Horii et al., 2001; Kitaura et al., 2006). of epistome straight, with marked concavity or (in some populations of one species) with a central protuberance; males of one species with stridulatory apparatus as described below in Paramareotis; fi ngers of male chelae usually elongate with index downfl exed and with differentiated teeth on both

40 THE RAFFLES BULLETIN OF ZOOLOGY 2010 index and dactylus or on dactylus only. Intertidal, usually in The M. crinitus group relatively soft muds. In M. crinitus Rathbun, 1913, M. darwinensis Barnes, 1971, Twelve species are included which have been divided between and M. paciﬁ cus Dana, 1851 (Fig. 3C) the front is relatively two subgroups on morphological grounds (the groups A and broad and unconstricted, the central region of epistome is B of Komai et al., 1995): straight, the characteristic longitudinal ridges of the branchial

Fig. 3. Form of the carapace and adult male chela of subgroups of the genus Macrophthalmus III: (a, b) the subgenus Macrophthalmus part 2, M. transversus (a) and Macrophthalmus dentatus (b); (c) the M. crinitus group of the subgenus Mareotis. Scale bars = 5mm.

41 Barnes: Review of the brachyuran genus Macrophthalmus regions are poorly marked, and the fi ngers of the male chela pointed anterolateral teeth, without conspicuous aggregations are short, with an undefl exed index. The specimen described of granules into rows or clumps on branchial regions by Pretzmann (1974) as M. pacifi cus tjiljapensis in fact (indistinct rows present in some); central region of posterior belongs to M. defi nitus in the other subgroup of Mareotis. border of epistome usually straight (with convexity in one species); males with stridulatory apparatus in all species (i.e. with short horny ridge on ventorofl exor margin, or on inner The M. japonicus group surface near ventorofl exor margin, of cheliped merus, and lower orbital border with 1–2 large triangular protuberances The M. japonicus group comprises M. abercrombiei Barnes, occupying at least one fi fth of that margin); fi ngers of male 1966, M. banzai Wada & Sakai, 1989, M. defi nitus Adams chela short with index straight or slightly downfl exed and & White, 1848, M. depressus Rüppell, 1830, M. japonicus with differentiated teeth on both fi ngers. Intertidal, with one (de Haan, 1838) (the type species of Mareotis), M. setosus species often occurring in holes in limestone rocks and the H. Milne Edwards, 1852, M. pistrosinus Barnes & Davie, others often associated with mangrove pneumatophores. 2008, M. teschi Kemp, 1919, and M. tomentosus Souleyet, 1841 (which possesses the stridulatory apparatus) (Fig. Four species are included: M. boteltobagoe (Sakai, 1969), 4A). In these, the front is narrow and markedly constricted, M. erato de Man, 1888, M. holthuisi Serène, 1973, and M. the central region of epistome bears a concavity (except in quadratus A. Milne Edwards, 1873 (the type), Kosuge & M. teschi – see below), the characteristic transverse and Davie (2001) having demonstrated that M. boteltobagoe and longitudinal branchial ridges of Mareotis are usually well- M. holthuisi are distinct species contra the opinion of Barnes marked, and the fi ngers of the male chela are elongate with (1976). Molecular sequence data (Kitaura et al., 2006) suggest the index being strongly downfl exed especially in large that M. erato + M. quadratus are only distantly related to M. individuals. The morphology of M. teschi appears somewhat holthuisi + M. boteltobagoe, but instead are related to the M. less straightforward than seemed earlier (Barnes, 1971) in that brevis group of the subgenus Macrophthalmus. a north-south cline is now evident: Thai populations (Komai et al., 1995) display a relatively parallel-sided carapace and straight central region of the epistome; in Indonesia Macrophthalmus (Tasmanoplax) Barnes, 1967 (Barnes, 1971) the second lateral tooth projects beyond the (Fig. 5A) external orbital angle and the central region of the epistome is protuberant; whereas material examiner by the author from Medium-sized, up to 30+ mm carapace breadth; ocular Selangor in peninsular Malaysia is equivalent to that from peduncles elongate but not projecting beyond lateral carapace Thailand in its epistome but to that from Indonesia in the margins, longer than breadth of front; front moderately form of its anterolateral carapace teeth. narrow, not constricted between bases of ocular peduncles, where its breadth is ca. 20% distance between external Molecular sequence data (Kitaura et al., 2006) confi rm the orbital angles; ischium of external maxilliped ca.1.2 times existence of two groupings within Mareotis but not the two length of merus; carapace with breadth 1.5–1.6 times length, identifi ed on morphological grounds by Komai et al. (1995). with lateral margins subparallel, with large, broad-based, Sequence analysis groups M. darwinensis and M. defi nitus subrectangular anterolateral teeth, branchial regions with on the one hand, but, on the other, groups M. banzai, M. transverse and longitudinal rows of granules; central region japonicus, M. tomentosus, M. pacifi cus and M. pistrosinus, of posterior border of epistome with large convexity; males and allies them with the subgenus Venitus and the M. convexus without stridulatory apparatus; fi ngers of male chelae elongate and M. telescopicus groups of Macrophthalmus sensu stricto with index downfl exed and with clearly differentiated tooth instead (see Fig. 6). The allozyme data of Horii et al. (2001), on dactylus only. Intertidal in soft sediments. however, which did not include M. darwinensis, grouped M. defi nitus with M. japonicus and M. banzai in a Mareotis This is a monotypic subgenus for M. latifrons Haswell, 1882, cluster distinct from although allied to M. convexus and the restricted to south-eastern Australia, the only macrophthalmid M. telescopicus group. in that region. It appears to differ behaviourly from other Macrophthalmus in that allocleaning (foraging on the carapace or walking legs of other conspecifi c individuals) Macrophthalmus (Paramareotis) is not displayed (Kitaura & Wada, 2004). Komai, Goshima & Murai, 1995 (Fig. 4B) Macrophthalmus (Venitus) Barnes, 1967 Small, carapace breadth < 15 mm; ocular peduncles short (Fig. 5B) and stout, not projecting beyond lateral carapace margins, subequal in length to breadth of front or shorter; front broad, Often very large (up to 80+ mm carapace breadth, and leg not constricted between bases of ocular peduncles, where its span of up to 30 cm); ocular peduncles elongate but not breadth is 20–30% distance between external orbital angles; projecting beyond lateral carapace margins, much longer ischium of external maxilliped ca. 1.25 times length of merus; than breadth of front; front narrow, constricted between carapace with breadth 1.3–1.6 times length, with lateral bases of ocular peduncles, where its breadth is 5–15% the margins subparallel, with broad-based subrectangular or distance between external orbital angles; ischium of external

42 THE RAFFLES BULLETIN OF ZOOLOGY 2010 maxilliped > 1.7 times length of merus; carapace with described above in Paramareotis; fi ngers of male chelae breadth from, in small species/individuals, 1.3 to, in large usually moderately elongate with index straight and with a species/individuals, 1.7 times length, with lateral margins differentiated tooth only on dactylus; pereipods often with subparallel or diverging posteriorly, with large and often large tubercles or spines. Low intertidal and subtidal, in very projecting, broad-based, subtriangular, pointed anterolateral soft muds; intertidally, the mouth of the burrow is often teeth (especially in large adults), heavily granular surface located in a large, water-fi lled, saucer-shaped depression. but without specifi c system of rows or clumps of granules; central region of posterior border of epistome straight; males Venitus contains three species: M. barnesi Serène, 1971, M. of one species (M. dentipes) with stridulatory apparatus as dentipes Lucas, 1836, and M. latreillei (Desmarest, 1817)

Fig. 4. Form of the carapace and adult male chela of subgroups of the genus Macrophthalmus IV: (a) the M. japonicus group of the subgenus Mareotis (both the relatively parallel-sided and relatively rounded carapace types), and (b) subgenus Paramareotis. Scale bars = 5mm.

43 Barnes: Review of the brachyuran genus Macrophthalmus

(type species). The names M. serratus Adams & White, therefore, a case could clearly be made for elevating some 1849 and M. vietnamensis Serène, 1971 listed by Ng et al. or all of the subgroups within Macrophthalmus to generic (2008) as extant species are still, as earlier (Barnes, 1977), level, it might be wise to await a complete set of molecular regarded by this author as being synonyms of species within data and more information derived therefrom and from further this group. morphological analyses on the monophyly or otherwise of putative genera and on potential phyletic relationships between them before so doing. Equivalent molecular sequence Relationships between the subgroups data on the relationships between Macrophthalmus and the other genera in the family would also be valuable. Clearly there is considerable lack of agreement between clades identified by analyses of allozyme data and of nucleotide sequences from mitochondrial 16S rRNA (Horii ACKNOWLEDGEMENTS et al., 2001; Kitaura et al., 2006) (Fig. 6) and those based on morphological similarity/difference, and Kitaura et al. I am most grateful to Peter Dworschak of the Naturhistorisches (2006) identify a correlation between type of sediment Museum, Vienna, Austria, for sending me information on the inhabited and morphology indicating that considerable Macrophthalmus paciﬁ cus tjiljapensis material in his care; functional convergence in body form may have occurred and, for their invaluable comments and advice, to Peter between members of different clades. To date, however, Davie of the Queensland Museum, Australia, Peter Ng of considerably less than half the Macrophthalmus species, and the National University of Singapore and Keiji Wada of the no representatives at all from four of the subgroups identiﬁ ed Nara Women’s University, Japan. above, have been subject to molecular analysis. Although,

Fig. 5. Form of the carapace and adult male chela of subgroups of the genus Macrophthalmus V: (a) subgenus Tasmanoplax and (b) subgenus Venitus. Scale bars = 5mm.

44 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Fig. 6. The relationships between and within some subgroups of Macrophthalmus suggested by the nucleotide sequence analyses of Kitaura et al. (2006).

45 Barnes: Review of the brachyuran genus Macrophthalmus

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Serène, R., 1977. Crustacés Hippidés ets Brachyoures des iles Tweedie, M.W.F., 1937. On the crabs of the family Ocypodidae in Séchelles (2me partie). Revue de Zoologie Africaine, 91: the collections of the Rafﬂ es Museum. Bulletin of the Rafﬂ es 748–765. Museum, 13: 140–170. Serène, R., 1981. Macrophthalmus (Macrophthalmus) kempi sp. nov. Vannini, M. & P. Valmori, 1981. Researches on the coast of (Crustacea, Decapoda, Brachyura). Bulletin du Muséum national Somalia. The shore and the dune of Sar Uanle. 31. Ocypodidae d’Histoire naturelle (Paris), Série 4, A3(4): 1139–1142. and Gecarcinidae (Decapoda Brachyura). Monitore Zoologico Souleyet, L.F.A., 1841. Crustacés. In: Eydoux, F. & L.F.A. Souleyet, Italiano, Supplement 14: 199–226. Voyage autour du monde execute pendant les années 1836 et Wada, K. & K. Sakai, 1989. A new species of Macrophthalmus 1837 sur la corvette ‘La Bonite’, commandée par M. Vaillant, closely related to M. japonicus (de Haan) (Crustacea: Decapoda: 1, 219–244. Paris. Ocypodidae). Senckenbergiana Maritima, 20: 131–146. Stevcic, Z., 2005. The reclassification of Brachyuran crabs Wada, K. & D. Wowor, 1989. Foraging on mangrove pneumatophores (Crustacea: Decapoda: Brachyura). Fauna Croatica, 14(1): by ocypodid crabs. Journal of Experimental Marine Biology & 1–159. Ecology, 134: 89–100. Stimpson, W., 1858. Prodromus descriptionis animalium Wear, R.G., 1968. Life-history studies on New Zealand Brachyura invertebratorum, quae Expeditio ad Oceanum Pacificum 3. Family Ocypodidae. First stage zoea larva of Hemiplax Septentrionalem a Republica Federata missa, Cadwaladano hirtipes (Jacquinot, 1853). New Zealand Journal of Marine Ring-gold et Johanne Rogers ducibus, observavit et descripsit. and Freshwater Research, 2: 698–707. Pars V. Crustacea Ocypodidae. Proceedings of the Academy of Weber, F., 1795. Nomenclator entomologicus secundum Natural Sciences of Philadelphia, 10: 31–40 & 93–110. Entomologiam systematicam ill. Fabricii adjectis speciebus Tai, A-Y & Y-Z. Song, 1984. Macrophthalmus (Decapoda, recens detectis et varietatibus. 171pp. Chilonii & Hamburgi. Brachyura) of the seas of China. Crustaceana, 46: 76–86. Woods, C. M. C. & D. R. Schiel, 1997. Use of seagrass Zostera Takeda, M. & T. Komai, 1991. Japanese species of the novazelandica (Setchell, 1933) as habitat and food by the Macrophthalmus telescopicus complex (Crustacea: Decapoda: crab Macrophthalmus hirtipes (Heller, 1862) (Brachyura: Brachyura: Ocypodidae). Bulletin of the National Science Ocypodidae) on rocky intertidal platforms in southern New Museum, Tokyo, Series A, 17: 165–171. Zealand. Journal of Experimental Marine Biology & Ecology, Tesch, J.J., 1915. The catometopous genus Macrophthalmus 214: 49–65. as represented in the collections of the Leiden Museum. Yang, S.L. & B.P. Tang, 2005. A new species of Tritodynamia Zoölogische Mededelingen, Leiden, 1(3–4): 149–204. (Decapoda, Brachyura, Pinnotheridae) from the Bohai Sea, Tesch, J.J. (1918) The Decapoda Brachyura of the Siboga China, with a key to the genus Tritodynamia Ortmann, 1894. Expedition. Hymenosomidae, Retroplumidae, Ocypodidae, Crustaceana, 78: 781–786. Grapsidae and Gecarcinidae. Siboga Expeditie Monographie, Zucker, N., 1988. Preliminary observations of cheliped use during 39C: 1–148. social activities in sentinel crabs (Brachyura, family Ocypodidae, Tirmizi, N.M. & N. Ghani, 1988. The rediscovery of Macrophthalmus genus Macrophthalmus) from northern Queensland, Australia. (Macrophthalmus) laevis A. Milne Edwards, 1867, in the Arabian Bulletin of Marine Science, 43: 98–102. Sea (Decapoda Brachyura). Crustaceana, 55: 253–256.

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THE RAFFLES BULLETIN OF ZOOLOGY 2010 58(1): 51–55 Date of Publication: 28 Feb.2010 © National University of Singapore

A NEW SPECIES OF THE GENUS KARSTARMA (CRUSTACEA: DECAPODA: BRACHYURA: SESARMIDAE) FROM ANCHIALINE CAVES IN THE PHILIPPINES

Daniel Edison M. Husana Department of Natural Environmental Studies, Graduate School of Frontier Science, the University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8561, Japan E-mail: [email protected]

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

Tomoki Kase Department of Geology and Paleontology, National Museum of Nature and Science, 3-23-1 Hyakunincho, Shinjuku-ku, Tokyo, 169-0073 Japan E-mail: [email protected]

ABSTRACT. – A new cavernicolous crab of the genus Karstarma is described from anchialine caves in Samal and Boracay islands, Philippines. The new species, K. philippinarum, is morphologically most similar to K. ultrapes (Ng, Guinot & Illife, 1994) from the Solomon Islands, but differs in having shorter ambulatory legs and an obtuse external orbital angle. A supraorbital convexity tends to be slightly larger in the new species. This paper increases the number of the species of the genus Karstarma to 15 and records the third species of the genus from the Philippines.

KEY WORDS. – Anchialine cave, Karstarma philippinarum, new species, Philippines, Brachyura, taxonomy.

INTRODUCTION one in Boracay Island, central Philippines and the other in Samal Island, southern Philippines. Although K. boholano The sesarmid crab genus Karstarma Davie & Ng, 2007, is (Ng, 2002) and K. sulu (Ng, 2002) have been recorded from currently represented by 14 species from Indo-West Pacifi c Palawan and Bohol respectively, the species from Boracay (Ng et al., 2008; Wowor & Ng, 2009). Although Karstarma and Samal resembles K. ultrapes (Ng, Guinot & Iliffe, 1994) is morphologically similar to Sesarmoides Serène & Soh, whick is only known only from the Solomon Islands. Our 1970, especially in the markedly long ambulatory legs, Davie detailed comparison with the type specimens of K. ultrapes & Ng (2007) distinguished Karstarma from Sesarmoides has revealed that the species from Boracay and Samal is new primarily by the absences of a milled suborbital ridge of to science. We here described this new species and briefl y documented the habitats. the carapace and a stridulatory crest on the merus of the cheliped. Ng (2002) and Davie & Ng (2007) also noted an Measurements provided are the carapace length (CL) by the interesting correlation between the stridulatory mechanism carapace width in mm. The terminology follows that of and habitat preferences. Sesarmoides with stridulatory Davie & Ng (2007). Specimens examined are deposited in mechanism inhabits tidal mangrove, estuarine and coastal the Muséum national d’Histoire naturelle, Paris (MNHN); the caves, whereas this mechanism is absent in Karstarma and National Museum of the Philippines, Manila (NMCR); the the species of the genus have exclusively been found in National Museum of Nature and Science (formerly National karst areas. Science Museum), Tokyo (NSMT); and the Zoological Reference Collection, Raffles Museum of Biodiversity During stygofaunal surveys conducted in various caves in Research, National University of Singapore (ZRC). The the Philippines, the fi rst and third authors obtained several abbreviations G1 and G2 are used for male fi rst and second specimens assigned to Karstarma from two anchialine caves, gonopods, respectively.

51 Husana et al.: New Karstarma from Philippines

TAXONOMY furrow present along median epi- and protogastric regions, diverging on meso- and metagastric regions and surrounding Sesarmidae Dana, 1851 gastro-cardiac groove, with inward-curving setae along epi- and protogastric furrow, tips of setae partly interlocked Karstarma Davie & Ng, 2007 especially in dorsal part; cervical furrow distinct but shallow on anterior part whereas indistinct on posterior part; gastro- Karstarma philippinarum, new species cardiac and cardio-intestinal furrows shallow; postorbital (Figs. 1–3) and epigastric protuberances slightly rugose. Frontal region gently granulose. Frontal margin defl exed, bilobed, medially Material examined. – Holotype: male (23.8 × 30.2 mm, NMCR separated by U-shaped concavity in dorsal view; downwardly 27063), Bat Cave, Boracay Island, 11°59.954'N 121°55.442'E, coll. inclined towards antennular septum in anterior view (Fig. E. Husana, 5 Dec.2004. 3c), ventral extensions of front embracing median tip of proepistome; supraorbital margin cristate, compressed W- Paratypes: 1 male (22.1 × 27.7 mm, NSMT-Cr2007.0105), 1 shaped, submedian part gently produced; external orbital female (25.2 × 31.1 mm, NMCR 27064), 1 female (18.9 × 24.0 mm, NSMT-Cr2007.0107), 1 male (19.8 × 24.6 mm, NSMT- angle relatively produced, inner margin straight, base Cr2007.0108), 1 male (20.6 × 26.0 mm, NSMT-Cr2007.0109), 1 of inner margin concave; infraorbital margin medially juvenile male (13.0 × 17.0 mm, NSMT-Cr2007.0110), 1 juvenile broader, laterally reaching as far as below external orbital male (11.4 × 14.4 mm), 1 male (19.2 × 24.0 mm), 1 female (20.7 angle; suborbital crista present, lateral three-fi fths thinly × 25.7 mm) (NSMT-Cr2007.0111), Tagbaobo Cave, Samal Island, raised, forming keel, edge of keel lined with microscopical 7°00.730'N 125°46.810'E, coll. E. Husana, T. Kase & S. Kinjo, 28 granules. Anterolateral and anterior half of posterolateral & 29 Jan.2004; 1 female (22.6 × 29. 2 mm, NSMT-Cr2007.0096), margin continuous, no clear demarcation, strongly diverging 1 male (28.3 × 36.1 mm, NSMT-Cr2007.0097), 1 female (29.3 × posteriorly, cristate, with 3 distinct teeth including external 36.8 mm, NSMT-Cr2007.0098), 1 female (24.1 × 30.6 mm, NSMT- orbital angle, fi rst and second teeth separated by deep, narrow Cr2007.0099), 1 male (25.7 × 31.8 mm, NSMT-Cr2007.0100), 1 male (25.0 × 31.2 mm, NSMT-Cr2007.0101), 1 female (30.8 × fi ssure, third tooth separated from second tooth by shallow 37.5 mm, NSMT-Cr2007.0102), 1 female (28.2 × 34.7 mm, NSMT- V-shaped notch, tip of second tooth slightly closer to that of Cr2007.0103), 1 female (29.4 × 36.9 mm, NSMT-Cr2007.0104), fi rst tooth than to third tooth, third tooth followed posteriorly Bat Cave, Boracay Island, 11°59.954'N 121°55.442'E, coll. E. by few small notches. Posterior half of posterolateral margin Husana, 5 Dec.2004. subcristate, converging abruptly towards gently sinuous posterior carapace margin. Epistome with posterior margin Comparative material. – Karstarma ultrapes (Ng, Guinot & Iliffe, 1994). Holotype: male (22.9 × 28.9 mm, MNHN-B24796), Mbetibula Cave (station 88-083), Florida Islands, Nggela Pile Island, Solomon Islands, coll. T. M. Iliffe & S. Sarbu, 15 Aug.1988; Paratype: 1 female (32.5 × 39.4 mm, MNHN- B24797), data same as holotype.

Description. – Carapace (Figs. 2a, b, 3a) approximately trapezoidal, widest between bases of second and third ambulatory legs; dorsal surface distinctly rugose, especially on branchial regions, with scattered minute setae and short stiff black setae on entire surface. Deep longitudinal

Fig. 1. Live coloration of Karstarma philippinarum, new species, Fig. 2. Karstarma philippinarum, new species. Holotype male (23.8 in its natural habitat, Bat Cave, Boracay Island, Philippines. × 30.2 mm, NMCR 27063). a, habitus; b, carapace, dorsal view.

52 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Fig. 3. Karstarma philippinarum, new species. Paratype male NSMT-Cr2007.0105. a, carapace; b, abdomen and telson; c, cephalothorax, frontal view; d, left cheliped, dorsal view; e, left fourth ambulatory leg, dorsal view; f, left cheliped, carpus; g, left chela, outer view; h, left antenna, ventral view; i, G1, ventral and dorsal views; j, left third maxilliped, ventral view. Scale bars: a–e, g = 5.0 mm; f = 2.0 mm; h–j = 1.0 mm.

53 Husana et al.: New Karstarma from Philippines cristate, bent anteriorly, trilobed, median projection longest, Remarks. – Karstarma philippinarum, new species, closely triangular. resembles K. ultrapes. They could easily be misidentifi ed as the same species because of their similar body pigmentations Eyes (Fig. 3a, c) well developed, well pigmented, cornea and appearances. But obvious distinction between the two wider than peduncle in dorsal view. Third maxilliped (Fig. species could easily be noticed if they are compared side by 3j) elongated; ischium as long as merus, with oblique median side. The clear difference between them is the proportions of groove; merus with crest adjacent to inner margin, lined with the ambulatory legs; K. philippinarum has shorter ambulatory setae; exopod slender, with long fl agellum. legs than those of K. ultrapes. For example, the merus of the third ambulatory leg of K. philippinarum is 3.83–5.12 Thoracic sternites 2 and 3 fused, lateral margin strongly times width (mean = 4.39, n = 14) and 1.08–1.60 times CL convex outwards, suture indistinct; suture between 3 and 4 (mean = 1.37, n = 14), while that of K. ultrapes is 5.45 visible, concave towards the anterior part. and 5.47 times width (mean = 5.46, n = 2) and 1.40 and 1.66 times CL (mean = 1.53, n = 2) (also see Figs. 2a, 4a; Chelipeds (Fig. 2a) equal, more robust in males than females, Ng et al., 1994: fi g. 5). In addition, K. philippinarum has merus (Fig. 3d) triangular in cross-section, all margins blunter external orbital angle and larger projection on the granulated, inner surface with two longitudinal rows of supraorbital margin. In K. philippinarum, the inner margin black fi ne setae, subdistal part of ventral inner margin with of the external orbital angle is convex and the submedian short, longitudinal non-corneous raise; carpus (Fig. 3f) with convexity of the supraorbital margin is more produced, inner angle slightly foliaceous, fringed with small teeth, forming a rounded concavity between them. While in K. outer margin with several low teeth; chela (Fig. 3d, g) with ultrapes, the inner margin of the angle is gradually confl uent slightly infl ated palm, palm sparsely granulated on lower half; with the supraorbital margin, the submedian convexity of movable fi nger slightly shorter than palm, immovable fi nger the supraorbital margin is lower (Figs. 2b, 3a, 4b; Ng et al., with 2 median longitudinal ridges along outer edge, cutting 1994, fi gs. 5–7a). edges lined with numerous triangular teeth. Ambulatory legs (Figs. 1, 2a, 3e) very long, third pair longest, fourth When Davie & Ng (2007) established Karstarma, they used pair shortest. Meri rugose on dorsal surfaces, merus of third two spellings, “Karstarma” and “Karstama”, for the genus ambulatory leg 3.83–5.12 times width (mean = 4.39, n = name. Although Davie & Ng (2007: 229) clearly stated that 14), 1.08–1.60 times CL (mean = 1.37, n = 14). Margins of the genus name is derived from an arbitrary combination propodi and dactyli lined with stiff and long black setae, inner and outer margins of dactyli of fi rst and second ambulatory legs with mat of dense short black setae.

Abdominal somites segments, all freely segmented. Male abdomen (Fig. 3b) triangular, wide; somites 1 and 2 short; lateral margins of somites 3 strongly convex; somites 4 and 5 trapezoidal in shape, lateral margins straight or gently sinuous; lateral margins of somites 6 convex; telson rounded on distal margin. Female abdomen rounded, very wide, somites 3 trapezoidal in shape; somites 4 to 5 with convex lateral margins, almost reaching proximal half of coxa; lateral margin of somites 6 convex; telson distinctly sunken into distal margin of somites 6. G1 (Fig. 3i) very stout, almost straight, outer margin and subdistal area covered with dense long setae, covering pectinated distal part; distal part spade-like.

Colouration. – Karstarma philippinarum, new species, has a semi-circular bright orange pattern on the anterior half of the dorsal surface of the carapace (Fig. 1). The posterior part of the dorsal surfaces of the carapace, including the intestinal region, is brownish in male live specimen. Females, on the other hand, have whitish intestinal region. The meri and carpi of the ambulatory legs are orange, and the propodi and dactyli are white. The chelipeds are orangish, except for whitish distal ends of the ﬁ ngers in males and whitish palm and ﬁ ngers in females.

Etymology. – The species name, philippinarum, was derived Fig. 4. Karstarma ultrapes (Ng, Guinot & Iliffe, 1994). Holotype from the Philippines, where the present new species was male (22.9 × 28.9 mm, MNHN-B24796). a, habitus; b, carapace, collected. dorsal view.

54 THE RAFFLES BULLETIN OF ZOOLOGY 2010 of “karst” and “Sesarma”, Ng, Guinot & Davie (2008) their constructive comments and suggestions. This research consistently spelled the genus as “Karstama” without any was permitted by Department of Environment and Natural comment. Indeed, the authors have not been aware of the Resources-Protected Area and Wild Life Bureau, Philippines, presence of the second spelling (P. J. F. Davie & P. K. L. and funded by NUS (grant no. R-154-000-334-112) to Ng, pers. comm.). According to the ICZN Article 24.2.3, DEMH, the Sasakawa Scientifi c Research Grant from Japan we select the spelling “Karstarma” as a correct original Science Society (no. 18-805M) to DEMH, the Japanese spelling (see also Wowor & Ng, 2009). Government (Monbukagakusho) Scholarship program to DEMH, the Merlion France-Singapore project RV10.01.06 to Notes on habitat. – Karstarma philippinarum, new species, TN, and by grants from the Japan Society for the Promotion was found in two anchialine caves that are fi lled with normal of Science (no. 18253007) and National Museum of Nature high saline seawater. Tagbaobo Cave is located in a remote and Science, Tokyo to TK. area on the eastern side of Samal Island just south of Davao City in Mindanao. The entrance of this cave is located on a limestone sea cliff about four meters above the high tide line LITERATURE CITED and inside is gloomy, with a direct underground and below sea-level connection to the sea. The animals co-occurred Clark, J., 1989. Koror mysticius, new genus, new species (Decapoda: with K. philippinarum in this cave are the hyppolitid shrimp Hippolytidae), a cave shrimp from Palau. Journal of Crustacean Parhippolyte misticia (Clark, 1989), undetermined ostracods Biology, 9: 445–452. and mysids. Bat Cave is in a limestone body and its entrance Dana, J. D., 1851. Conspectus crustaceorum quae in Orbis Terrarum is about 100 m away from the sea. The cave extends seaward circumnavigatione, Carolo Wilkes e Classe Reipublicae and appears to connect to the sea because dim light is visible Faederatae Duce, Lexit et descripsit J. D. Dana. Pars VIII. from the water at the innermost part of the cave. Other Proceedings of the Academy of Natural Sciences of Philadelphia, 5: 247–254. crustaceans collected inside this cave are the gecarcinid crabs Discoplax gracilipes Ng, 2002 and Gecarcoidea lalandii Davie, P. J. F. & P. K. L. Ng, 2007. A new genus for cave-dwelling H. Milne Edwards, 1837. Many bats inhabit both caves. crabs previously assigned to Sesarmoides (Crustacea: Dcapoda: Raffl es Bulletin of Zoology Karstarma philippinarum was observed in water and dry Brachyura: Sesarmidae). , Supplement No. 16: 227–231. parts of the cave fl oors and walls, seemingly feeding on bat feces and other organic materials in both caves. Milne Edwards, H. 1837. Histoire naturelle des Crustaces, comprenant l’anatpmie, la physiologie et la classifi cation de ces animaux, 2: 1–531, atlas 1–32, pls. 1–42. Distribution. – Karstarma philippinarum, new species, is currently known only from Boracay Island and Samal Ng, P. K. L., 2002. New species of cavernicolous crabs of the Island, Philippines. genus Sesarmoides from the western Pacifi c, with a key to the genus (Crustacea: Decapoda: Brchyura: Sesarmidae). Raffl es Bulltein of Zoology, 50(2): 419–435. ACKNOWLEDGEMENTS Ng, P. K. L., D. Guinot & T. M. Iliffe, 1994. Sesarmoides ultrapes new species, a remarkable sesarmine crab from caves in the Solomon Islands (Decapoda: Brachyura: Grapsidae). Crustacean The fi rst author thanks S. Kojima (Ocean Research Institute, Research, 23: 12–22. the University of Tokyo) for his supervision in the graduate research, P. K. L. Ng (Department of Biological Sciences, Ng, P. K. L., D. Guinot & P. J. F. Davie, 2008. Systema Brachyurorum: Part I. An annotated checklist of extant National University of Singapore) for his supervision on brachyuran crabs of the world. Raffl es Bulletin of Zoology, crab taxonomy and short-term invitation to NUS, and Supplement No. 17: 1–286. Régis Cleva (MNHN) for providing some photographs of Seréne, R. & C. L. Soh, 1970. New Indo-Pacifi c genera allied to the specimen to the fi rst author. Danièle Guinot and Régis Sesarma Say, 1877 (Brachyura, Decapoda, Crustacea). Treubia, Cleva (MNHN) kindly allowed the second author (TN) 27(4): 387–416. access to the material under their care and. We also thank Wowor, D. & P. K. L. Ng, 2009. Two new species of sesarmid crabs S. H. Tan (Department of Biological Sciences, National (Crustacea: Decapoda: Brachyura) associated with limestone University of Singapore) and two anonymous reviewers for formations in West Papua, Indonesia. Zootaxa, 2025: 21–31.

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THE RAFFLES BULLETIN OF ZOOLOGY 2010 58(1): 57–74 Date of Publication: 28 Feb.2010 © National University of Singapore

THE EUXANTHINE CRABS (CRUSTACEA: BRACHYURA: XANTHIDAE) OF 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]

Peter K. L. Ng Tropical Marine Science Institute, National University of Singapore, 14 Kent Ridge Road, Singapore 119223; Department of Biological Sciences, Faculty of Science, National University of Singapore, 14 Science Drive 4, Singapore 117543 Email: [email protected]

ABSTRACT. – Several marine expeditions have been conducted in the Philippine Archipelago since the early part of the 19th century, and have documented the rich diversity of crustaceans collected from these islands. In addition, the recently concluded PANGLAO 2004 and 2005 expeditions to the central Philippines, and the AURORA 2007 expedition to the northeastern Philippines have yielded a diverse array of shallow and deep-water marine animals, particularly brachyuran crustaceans. The family Xanthidae is among the best represented of these brachyurans. As part of a continuing effort to fully document the Brachyura of the Philippines, we report here the occurrence of 25 species belonging to the subfamily Euxanthinae (Brachyura: Xanthidae), with two recently described new genera, ﬁ ve recently described new species and six new country records.

KEY WORDS. – Philippines, Brachyura, Xanthidae, Euxanthinae, Bohol, Panglao, Balicasag.

INTRODUCTION of Science are no longer in existence the collector’s numbers are retained in the revised list for purposes of record with The Brachyura of the Philippines is still not well known. reference to geographical distribution and for materials that Estampador (1937) provided a checklist of the decapod were given as exchange with foreign workers. Dr. Cowles, crustaceans from the Philippines based on collections of the former head of the Department of Zoology, had made such University of the Philippines and the then Bureau of Science, negotiation.” If any of Estampador’s xanthoid specimens and also on the reports resulting from surveys such as the U.S. appearing in the list survived, none have been found as yet, Exploring Expedition (1838-1842), the Samarang expedition despite repeated efforts by the authors and others. (1843–1846), the Challenger expedition (1873–1876) and the Siboga expedition (1899-1900). There were 55 families, Other workers have composed similar lists based on 195 genera and 507 species included in this checklist. This collections made by private collectors (Ward, 1941), the was followed by an updated and more comprehensive listing Albatross expedition (Griffi n, 1976; Garth & Kim, 1983; Tan, after the Second World War (Estampador, 1959). About 1996), the MUSORSTOM expeditions (Serène & Vadon, 58 families, 207 genera and 522 species were listed in 1981; Moosa, 1981; Goeke, 1985) and the Pele Sulu Sea this revised checklist. Of these, there were 307 brachyuran expedition (Serène & Umali, 1972). Ward (1941) reported on species, with 45 species in the Xanthidae sensu lato. Due the Brachyura collected in 1936 and 1937 from and around to the major changes in brachyuran systematics since these the Davao Gulf, southern Philippines. He listed 148 species, checklists were published, there is a need to re-examine the with 1 new genus, 15 new species and 2 new subspecies species listed therein. Unfortunately, many of the specimens described. Griffi n (1976) listed 63 species of spider crabs referred to in these two checklists were lost, as Estampador from the Philippines, 53 of which were collected by the US (1959: 1, 3) states, “The collections of both the University steamer Albatross from 1908 to 1910. Garth & Kim (1983) of the Philippines and the then Bureau of Science were listed a total of 60 species of the Xanthidae sensu lato and completely destroyed during World War II, along with the described three new genera, 13 new species and one new scientifi c libraries in these two institutions.”, and furthermore, subspecies. Tan (1996) reported on the leucosiid crabs from “Though the specimens of the University and the then Bureau the same expedition, recording 36 species in 17 genera and

57 Mendoza & Ng: Euxanthine crabs of the Philippines describing one new species. Serène & Umali (1972) recorded M = intertidal hand-picking, P = tangle nets, R = hand- 22 species (four new) from the Philippines, collected mostly collecting by SCUBA diver, and T = trawling (see description by the Pele Sulu Sea expedition in 1964, among which there of methods in Bouchet et al., 2009). For PANGLAO 2005 were fi ve xanthid species, mostly Euxanthinae. Serène & and AURORA 2007 stations, CP = beam trawl and DW = Vadon (1981) provided a tentative list of the Brachyura Warén dredge (see description of methods in Richer de Forges collected by the MUSORSTOM I expedition to the waters et al., 2009). All measurements of the material examined around southern and southwestern Luzon. They reported 155 are expressed as carapace width by carapace length, in species, excluding Portunidae, many of which were only the millimeters. The following contractions are used: coll. = second known records for the species or new records for collected by; purch. = purchased by; Stn. = station; and Is. the Philippines. They also described one new genus, two = Island. The synonymies listed herein are only the names new species and one new subspecies, all within Xanthidae. used for species collected from the Philippines as they were Subsequent workers on this considerable collection dealt written in the original reports or publications. The specimens with specifi c families such as the Portunidae (Moosa, 1981), in this report are deposited in the following museums: the Dorippidae (Chen, 1985), Majidae (Guinot & Richer de Crustacean Reference Collection of National Museum of the Forges, 1985), Raninidae (Goeke, 1985), and Dromiidae Philippines, Manila (NMCR), Muséum national d’Histoire (McLay, 1993), adding more species. naturelle, Paris (MNHN), Kanagawa Prefectural Museum of Natural History, Odawara (KPMNH), National Science Recently, research on the decapod crustaceans in the Museum, Tokyo (NSMT), and the Zoological Reference Philippines experienced a resurgence after several discoveries Collection of the Raffl es Museum of Biodiversity Research, were made in the island of Balicasag, in the Bohol Sea. Singapore (ZRC). A list of the euxanthine crabs found in the Rare and interesting species (e.g. Takeda & Manuel, 2000; Philippines, with geographic references and historical records Komatsu et al., 2005; Takeda & Manuel-Santos, 2007) and is provided in Table 1. The system of classifi cation follows many new genera and species (e.g. Ng & Liao, 2002; Ng, that of Ng et al. (2008). 2003; Ng & Ho, 2003; Ng & McLay, 2005; McLay & Ng, 2005; Castro, 2007; Manuel-Santos & Ng, 2007; Ng & Manuel-Santos, 2007; Richer de Forges & Ng, 2007a, b, c) TAXONOMY were being collected by local fi shermen using tangle nets, along with the targeted mollusc species for the shell trade. Xanthidae MacLeay, 1838 Material from Balicasag has contributed considerably to the elucidation of the taxonomy of various brachyuran groups Euxanthinae Alcock, 1898 (see Crosnier, 2002; McLay & Ng, 2004; Castro, 2007; Ng & Manuel-Santos, 2007). For an account of the crustacean Alainodaeus Davie, 1993 collections from Balicasag Island, see Ng et al. (2009). Alainodaeus fi lipinus Mendoza & Ng, 2008 In recent years, the collections of the two PANGLAO expeditions conducted in 2004 and 2005 in the central Alainodaeus fi lipinus Mendoza & Ng, 2008a: 55, Figs. 1–4. Philippines (see Bouchet et al., 2009; Richer de Forges et al., 2009) have yielded many new taxa, some with wide- Material examined. – Holotype male, 16.5 × 12.0 mm (NMCR- ranging implications on the taxonomy of their affi liated 27161), Balicasag Is., 100–500 m, from fi shermen with tangle nets, coll. P. K. L. Ng, 2 Mar.2004; paratypes: 1 male, 8.8 × 6.4 mm groups. For the Xanthidae in these collections, relatively (ZRC 2008.0895), from fi shermen with tangle nets, 100–500 m, more work has been done on the Euxanthinae and this has Balicasag Is., coll. P. K. L. Ng, Dec.2000; 1 male, with bopyrid resulted in the description of two new genera and fi ve new isopod in branchial chamber, 21.8 × 15.0 mm (ZRC 2008.0896), species (Mendoza & Ng, 2008a, b). The AURORA 2007 tangle net, 100–300 m, Maribohoc Bay, Bohol, coll. J. Arbasto, expedition, which was conducted along the eastern coast of between Nov.2003 to Apr.2004; 1 female, 11.2 × 8.2 mm (ZRC Luzon, particularly the provinces of Aurora and Quezon, 2008.0897), from fi shermen with tangle nets, 100–500 m, Balicasag also yielded an interesting array of marine benthic fauna, and Is., coll. P. K. L. Ng, Mar.2004; 1 female, 11.1 × 8.0 mm (ZRC work has barely just begun on this collection. The primary 2008.0898), from fi shermen with tangle nets, 50–500 m, Balicasag aim of this paper is to record all the euxanthine crabs that Is., coll. PANGLAO 2004 Marine Biodiversity Project, 14 Jun.2004; 1 male, 15.5 × 10.8 mm, 1 female, 13.0 × 8.9 mm (ZRC 2008.0899), have been described and/or recorded from the Philippines Stn. DW2402, off Balicasag Is., 101–118 m, 9°30.8'N 123°41.5'E, to date. This paper is intended to eventually contribute to coll. MV DA-BFAR, PANGLAO 2005 Cruise, 31 May 2005. a complete checklist of the brachyuran crustaceans of the Philippines in the near future. Remarks. – This species was recently described from Balicasag Island (Mendoza & Ng, 2008a). It represents a remarkable range expansion for Alainodaeus, being found in MATERIALS & METHODS the northernmost and westernmost extent of the known range of this genus. It is known only from the central Philippines In the most recent expeditions to the Philippines, each thus far. sampling station has an alphanumeric code, wherein the letter prefi x denotes the sampling method utilized. For PANGLAO 2004 stations, B = coral brushing, L = “lumun-lumun” nets,

58 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. List of euxanthine crabs from the Philippines, with geographic references and historical records. Species names preceded by an asterisk (*) are new country records.

Species Record from Philippines Alainodaeus fi lipinus Mendoza & Ng, 2008 Balicasag Is., Bohol Sea (Mendoza & Ng, 2008a) Cranaothus deforgesi Ng, 1993 Maluso Bay, Basilan Is., Sulu Sea (Serène & Umali, 1972); Panglao & Balicasag Is., Bohol Sea (this paper) Crosnierius carinatus Serène & Vadon, 1981 off Lubang Is., South China Sea (Serène & Vadon, 1981); Bohol Sea & eastern coast of Luzon, Philippine Sea, off Batangas coast, South China Sea (this paper) *Epistocavea mururoa Davie, 1993 Panglao & Balicasag Is., Bohol Sea (this paper) Euxanthus exsculptus (Herbst, 1790) Philippines (no specifi c locality) (White, 1847); Davao Gulf (Ward, 1941); Catanduanes Is., Philippine Sea (Guinot-Dumortier, 1960); Luzon Is. (Batangas, Cagayan & Sorsogon), Lubang Is., Mindoro Is., Panay Is., Samar Is., Sibuyan Is. (this paper) Euxanthus herdmani Laurie, 1906 Camiguin Is., Bohol Sea (Garth & Kim, 1983); Puerto Galera, Mindoro Is., South China Sea (Serène, 1984); Panglao Is., Bohol Sea (this paper) Euxanthus huonii (Hombron & Jacquinot, 1846) Philippines (no specifi c locality) (Miers, 1884); Panglao Is., Bohol Sea (this paper) Guinotellus melvillensis Serène, 1971 Cape Melville, Balabac Is., Sulu Sea (Serène, 1971; Serène & Umali, 1972); Balabac Is., Cuyo, Is., Sibutu Is., Sulu Sea & Batangas, South China Sea (Mendoza et al., 2009) *Hepatoporus orientalis (Sakai, 1935) Off Batangas coast, South China Sea (this paper) Hepatoporus pumex Mendoza & Ng, 2008 Panglao Is., Bohol Sea (Mendoza & Ng, 2008b) *Hypocolpus abbotti (Rathbun, 1894) Panglao & Balicasag Is., Bohol Sea (this paper) Hypocolpus haanii Rathbun, 1909 Jolo Is., Sulu Sea (Buitendijk, 1960); Panglao & Balicasag Is., Bohol Sea (this paper) Hypocolpus kurodai Takeda, 1980 Marinduque Is., Sibuyan Sea (Takeda & Manuel, 2000) Ladomedaeus fungillus Manuel-Santos & Ng, 2007 Panglao & Balicasag Is., Bohol Sea (Manuel-Santos & Ng, 2007); Bohol Sea & eastern coast of Luzon, Philippine Sea (this paper) Medaeops granulosus (Haswell, 1882) Quezon, Palawan Is., South China Sea (Serène & Umali, 1972); off Lubang Is., South China Sea (Serène & Vadon, 1981); Manigo-nigo Is., Iloilo, Visayan Sea (this paper) Medaeus elegans A. Milne-Edwards, 1867 Pearl Bank, Sulu Archipelago (Serène & Umali, 1972) Miersiella cavifrons Takeda, 1989 off Lubang Is., South China Sea (Serène & Vadon, 1981); Bohol Sea, (this paper) *Miersiella haswelli (Miers, 1886) Balicasag Is., Bohol Sea (this paper) Paramedaeus globosus Serène & Vadon, 1981 off Lubang Is., South China Sea (Serène & Vadon, 1981); Bohol Sea (this paper) Paramedaeus simplex (A. Milne Edwards, 1873) Batangas, South China Sea (Serène & Umali, 1972); Panglao Is., Bohol Sea (this paper) *Paraxanthodes cumatodes (MacGilchrist, 1905) Panglao Is., Bohol Sea (this paper) *Paraxanthodes obtusidens (Sakai, 1965) Balicasag Is., Bohol Sea & eastern coast of Luzon, Philippine Sea (this paper) Rizalthus anconis Mendoza & Ng, 2008 Panglao Is., Bohol Sea (Mendoza & Ng, 2008b) Visayax estampadori Mendoza & Ng, 2008 Panglao Is., Bohol Sea (Mendoza & Ng, 2008b) Visayax osteodictyon Mendoza & Ng, 2008 Panglao Is., Bohol Sea (Mendoza & Ng, 2008b)

59 Mendoza & Ng: Euxanthine crabs of the Philippines

Cranaothus Ng, 1993 9°33.5'N 123°48.6'E, Arco Point, Panglao Is., coll. PANGLAO 2004 Marine Biodiversity Project, 31 May 2004; 2 males, 4.7 × Cranaothus deforgesi Ng, 1993 3.6 mm to 4.9 × 3.7 mm (ZRC 2008.1364), 1 male, 5.9 × 4.3 mm (Fig. 1A) (MNHN-B30703), Stn. B9, caves in reef wall, 8–10 m, 9°33.1'N 123°44.0'E, Napaling, Panglao Is., coll. PANGLAO 2004 Marine Biodiversity Project, 08 Jun.2004; 1 male, 8.0 × 5.5 mm (ZRC Paramedaeus noelensis – Serène & Umali, 1972: 68, Pl. 7 Figs. 2008.1365), Stn. R59, coral patches and platform with thin layer 7–9, not Medaeus noelensis Ward, 1934. of sand, 2–20 m, 9°36.1'N 123°44.9'E, Momo Beach, Panglao Is., coll. PANGLAO 2004 Marine Biodiversity Project, 22 Jun.2004; Material examined. – 1 male, 7.5 × 5.3 mm (NMCR-1521), Stn. 1 male, 5.4 × 3.8 mm, 1 female, 6.0 × 4.3 mm (ZRC 2008.1366), D1, 25 fathoms (46 m), Maluso Bay, Basilan Is., coll. Pele-Sulu 1 male, 5.7 × 4.0 mm (MNHN-B30702), Stn. S5, rock and coral Sea Expedition, 15 Feb.1964; 1 male, 5.2 × 3.8 mm, 1 female, patches with brown algae, 2–4 m, 9°37.1'N 123°46.1'E, Napaling, 4.4 × 3.2 mm (ZRC 2008.1363), Stn. B3, base of reef slope, 8 m,

Fig. 1. Live colouration of euxanthine crabs from the Philippines: A, Cranaothus deforgesi Ng, 1993, male (8.0 × 5.9 mm) (R59, Panglao Is., ZRC 2008.1365); B, Crosnierius carinatus Serène & Vadon, 1981, female (15.6 × 11.8 mm) (CP2737, eastern coast of Luzon, ZRC 2008.1370); C, Epistocavea mururoa Davie, 1993, male (33.2 × 23.5 mm) (L36, Panglao Is., ZRC 2008.1371); D, Euxanthus herdmani Laurie, 1906, male (10.0 by 7.6 mm) (S32, Panglao Is., NMCR-27334); E) Euxanthus huonii (Hombron & Jacquinot, 1846), male (31.9 × 21.9 mm) (M17, Panglao Is., ZRC 2008.1376); F, Hepatoporus orientalis (Sakai, 1935) male (8.1 × 6.0 mm) (CP2862, off Batangas coast, ZRC 2008.1379).

60 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Panglao Is., coll. PANGLAO 2004 Marine Biodiversity Project, 8 Comparative material. – Crosnierius gracilipes Ng & Chen, 2005: Jun.2004; 2 females, 4.7 × 4.3 mm to 6.5 × 4.7 mm (NMCR-27331), Holotype male, 9.1 × 7.0 mm (ZRC 2005.0015), Stn. 6080, South Stn. S10, coral plateau with fi ne sand covering rocks, 6–14 m, China Sea, near Hong Kong, coll. 2 Apr.1959. 9°29.4'N 123°56.0'E, Pamilacan Is., coll. PANGLAO 2004 Marine Biodiversity Project, 11 Jun.2004; 2 males, 5.0 × 3.5 mm to 7.1 × Remarks. – The genus Crosnierius contains two species, C. 5.0 mm (NMCR-27330), Stn. S22, hard bottom covered with sand, carinatus, the type species, and C. gracilipes Ng & Chen, 15–20 m, 9°29.4'N 123°56.0'E, Pamilacan Is., coll. PANGLAO 2004 2005, which is known only by the male holotype, collected Marine Biodiversity Project, 21 Jun.2004; 1 male, 5.8 × 4.2 mm near Hong Kong in the South China Sea. Crosnierius (ZRC 2008.1367), Stn. S32, hard plateau with sand covering rocks, 2–3 m, 9°35.8'N 123°44.6'E, Looc, Panglao Is., coll. PANGLAO carinatus is thus far known only from the Philippines, with 2004 Marine Biodiversity Project, 28 Jun.2004. this report being only the second record for this species since it was fi rst described. The recently collected Philippine Remarks. – This species was erroneously reported from specimens agree well with the description and fi gures of the Philippines by Serène & Umali (1972) as Paramedaeus Serène & Vadon (1981). The largest male in this series (19.5 noelensis (Ward, 1934). Remarking on the illustrations they × 15.0 mm) is considerably larger than the male holotype provided, Ng (1993) stated that their specimen was not (13.0 × 9.0 mm). In life, the carapace and pereopods are a conspecifi c with Paramedaeus. noelensis, but was actually uniform reddish-orange, sometimes with whitish mottling Cranaothus deforgesi, a new genus and new species he was on the central portions of the carapace and on the meri of describing from Chesterfi eld Island in the Coral Sea. This was the ambulatory legs, especially in female specimens. Ng & confi rmed by Mendoza & Ng (2008b) when they examined Chen (2005) commented that they could not locate the type the specimen in question in the NMCR. specimens in the MNHN. A fresh search by the authors as well as the collections manager was also unsuccessful (R. The present specimens have a few minor differences with the Cleva, pers. comm.). holotype as fi gured in Ng (1993). The front of the holotype is more produced beyond the orbits, and its lobes are more In their comparison of Crosnierius gracilipes with illustrations divergent, resulting in a deeper, V-shaped, medial incision; of the holotype of C. carinatus, Ng & Chen (2005) noted the and the vermicular ridges are also more pronounced. Attempts following differences: 1) the ambulatory legs (last ambulatory were made to locate the holotype deposited and catalogued leg, P5) are longer and more slender in C. gracilipes than in the MNHN but these were not successful and it could not in C. carinatus, particularly with regard to the merus and be located (R. Cleva, pers. comm.). The Philippine specimen propodus; 2) the spines on the anterior margin of the merus reported from Basilan Island by Serène & Umali (1972) is of P5 are more widely spaced apart in C. gracilipes; 3) the more similar to the holotype, particularly in the condition anterolateral teeth are lower in C. gracilipes; and 4) the of the frontal lobes which are also more produced and dilated median part of the G1 is subequal in length to the divergent. However, the condition of the G1 of the different spinulated distal one-third in C. gracilipes (vs. distinctly male specimens examined did not differ signifi cantly and the shorter in C. carinatus). We compared the holotype of C. observed differences are regarded as intra-specifi c. gracilipes with similarly sized C. carinatus specimens at hand and made the following observations. The ambulatory legs of C. gracilipes are slightly longer and more slender than Crosnierius Serène & Vadon, 1981 those of C. carinatus, with the merus of P5 extending past the tip of the last anterolateral tooth when the leg is folded Crosnierius carinatus Serène & Vadon, 1981 against the posterolateral carapace margin. In C. carinatus (Fig. 1B) the distal tip of the merus just touches the tip of the last anterolateral tooth, in smaller specimens, or does not reach Crosnierius carinatus Serène & Vadon, 1981: 131, Figs. 1, 2c, d, the tip, in the case of larger specimens. The teeth on the Pl. 3 Fig. C. anterior edge of P5 are indeed spaced more widely apart in C. gracilipes due to their smaller size. In C. carinatus, these Material examined. – 1 male, 19.5 × 15.0 mm (NMCR-27332), are larger and longer. Also, the spinulose terminal portion of Stn. CP2349, off Pamilacan Is., 219–240 m, 9°31.6'N 123°55.7'E, the G1 is also relatively shorter in C. gracilipes. However, Bohol Sea, coll. MV DA-BFAR, PANGLAO 2005 Deep-Sea Cruise, we do not agree with Ng & Chen’s (2005) assessment that 24 May 2005; 1 female, 12.1 × 9.2 mm (ZRC 2008.1368), Stn. the anterolateral teeth are lower and that the propodus of P5 CP2348, off Pamilacan Is., 196–216 m, 9°29.6'N 123°52.5'E, Bohol Sea, coll. MV DA-BFAR, PANGLAO 2005 Deep-Sea Cruise, 24 is longer in C. gracilipes, these resulting from the manner May 2005; 1 female, 12.3 × 9.4 mm (ZRC 2008.1369), 1 male, in which the holotype of C. carinatus was photographed, 12.7 × 9.8 mm, 1 female, 10.9 × 8.6 mm (MNHN-B30701), Stn. making the structures appear different. Aside from the CP2407, Maribojoc Bay, 256–258 m, 9°41.3'N 123°48.5'E, Bohol differences between C. gracilipes and C carinatus mentioned Sea, coll. MV DA-BFAR, PANGLAO 2005 Deep-Sea Cruise, 01 by Ng & Chen (2005), the following were also noted: 1) the Jun.2005; 1 female, 15.6 × 11.8 mm (ZRC 2008.1370), Stn. CP dorso-external surface of the cheliped carpus is smooth and 2737, 269–272 m, 16°01.91'N 121°59.23'E, off the eastern coast infl ated in C. gracilipes (vs. eroded in C. carinatus); 2) the of Luzon, coll. MV DA-BFAR, AURORA 2007 Deep-Sea Cruise, external surface of the palm in both chelipeds is smooth in 01 Jun.2007. C. gracilipes (vs. external surface with an additional, weak, irregular keel near the upper margin in C. carinatus; and 3) there is no distinct keel on the dorsal surface of the carpus

61 Mendoza & Ng: Euxanthine crabs of the Philippines of the ambulatory legs in C. gracilipes (vs. present in C. (NMCR-453), Calatagan, Batangas, coll. G. Alcasid & G. Edaño, carinatus). As such, we continue to recognize C. gracilipes 17-20 Nov.1958; 5 males, 39.5 × 25.4 mm to 54.3 × 34.2 mm, 3 as distinct from C. carinatus. females, 37.6 × 24.2 mm to 40.7 × 26.4 mm (NMCR-568), Barrio Rizal, Gubat, Sorsogon, coll. B. Reyes, 4 May 1959; 1 female, 39.8 × 26.0 mm (NMCR-963), Lubang Is., coll. E.A. Engao, 13-17 May 1961; 1 male, 44.4 × 28.7 mm (ZRC 1970.1.7.9), Puerto Galera, Epistocavea Davie, 1993 Mindoro, coll. R. Serène, 15 Feb.1966; 1 female, 51.4 × 34.2 mm (ZRC 1973.10.30.37), Puerto Galera, Mindoro, Philippines, coll. V. Epistocavea mururoa Davie, 1993 P. Marula, 22 Jun.1971; 3 males, 37.5 × 24.2 mm to 55.4 × 35.7 (Figs. 1C, 4A, B) mm, 1 ovig. female, 50.5 × 32.5 mm (NMCR-1714), littoral zone at low tide, under rocks, corals & near sargasum, Palo Bandera, Material examined. – 1 male, 21.5 × 15.5 mm (ZRC 2001.0657), Calatagan, Batangas, coll. P.C. Gonzales et al., 16 Dec.1971; 3 Balicasag Is., 50–500 m, coll. local fi shermen with tangle nets, 28 males, 45.6 × 29.5 mm to 58.6 × 37.0 mm, 1 female, 54.3 × 35.2 Nov.2001; 5 males, 21.4 × 17.4 mm to 31.1 × 22.1 mm, 3 females, mm (NMCR-4642), Casing, Silom, Magdiwang, Sibuyan Is., coll. 21.3 × 16.4 mm to 26.3 by 18.4 mm (NMCR-27333), Balicasag P.C. Gonzales et al, Mar.1972; 1 juv. male, 12.5 × 8.5 mm (NMCR- Is., 50–500 m, coll. local fi shermen with tangle nets, Mar.2004; 8910), dead coral, 4 m, Bugtung Bato, Ibajay, Aklan, coll. M.R. 1 male, 33.2 × 23.5 mm (ZRC 2008.1371), Stn. L36, 9°36.7'N Manuel, Aug.1986; 1 male, 27.0 × 17.1 mm (ZRC 2008.1375), 123°45.8'E, Looc, Panglao Is., 85–90 m, coll. PANGLAO 2004 rocky/sandy intertidal, with coral rubble and patches of seagrass, Expedition, 21 Jun.2004; 1 male, 30.2 × 21.4 mm (MNHN-B31886), near lighthouse, 18°24.029'N 122°07.580'E, Barangay Racat, Santa Stn. L40, 9°37.3'N 123°46.5'E, Tangnan, Panglao Is., 100–120 m, Ana, Cagayan, coll. J. C. E. Mendoza & T. Naruse, 22 Apr.2007. coll. PANGLAO 2004 Expedition, 24 Jun.2004; 1 male, 15.2 × 11.6 mm, 1 female, 17.1 × 12.9 mm (ZRC 2008.1372), Stn. L44, Remarks. – This species is common in rocky intertidal areas, 9°30.8'N 123°41.0'E, Balicasag Is., 85–100 m, coll. PANGLAO and is easily one of the most commonly encountered species 2004 Expedition, 03 Jul.2004; 1 female, 23.0 × 16.3 mm (MNHN- in the Philippines. Euxanthus exsculptus is known to occur B31887), 1 female, 26.1 × 18.9 mm (ZRC 2008.1373), Stn. L45, 9°36.6'N 123°45.4'E, Bingag, Panglao Is., 80–90 m, coll. throughout most of the Indo-West Pacifi c, from the Bay of PANGLAO 2004 Expedition, 03 Jul.2004; 1 female, 25.1 × 17.8 Bengal, Indian Ocean to the Tuamotu Archipelago in the mm (ZRC 2008.1374), Stn. P2, 9°36.6'N 123°45.4'E, Maribohoc southwestern Pacifi c (Guinot-Dumortier, 1960). Bay, Bohol Is., 400 m, coll. PANGLAO 2004 Expedition, 30 May 2004. Euxanthus herdmani Laurie, 1906 Remarks. – The monotypic genus Epistocavea was (Fig. 1D) established for a unique crab, several of which were collected by traps set in deep water (100–240 m) in French Polynesia. Euxanthus herdmani – Garth & Kim, 1983: 669; Serène, 1984: The present Philippine specimens agree well with Davie’s 85, Pl. 11 Fig. D. (1993) excellent description and illustrations of E. mururoa, and there is no doubt that they are conspecifi c. It is interesting Material examined. – 1 male, 10.0 × 7.6 mm (NMCR-27334), Stn. S32, 9°35.8'N 123°44.6'E, Looc, Panglao Is., 2–3 m, coll. to note that all the Philippine specimens were collected either PANGLAO 2004 Expedition, 28 Jun.2004. by tangle net or by “lumun-lumun” (see Bouchet et al., 2009; Ng et al., 2009, for a description of these methods) and Remarks. – This is a rarely reported species and the single not by any other method employed during the PANGLAO male specimen agrees well with the original description expeditions. This is only the second time that E. mururoa has and fi gure as well as those in Serène (1984). The carapace been reported since it was described. Moreover, the record is orange, with blotches of dark brown on the supraorbital from the Philippines represents a remarkable range extension region and portions of the fi rst and second anterolateral teeth. by over 9,600 km to the west. The live colouration of adults The cardiac and medial intestinal regions are brownish- and juveniles is uniformly dull reddish-orange on the carapace orange. The posterolateral concavity for the coadaptation and pereopods, with very small patches of yellow or white of ambulatory legs is white. The meri of the chelipeds and especially on the ambulatory legs. Some paler orange forms P2–P4 are generally white, the carpi, propodi, and dactyli have been observed as well. The fi ngers of the chela in both are pinkish-purple. In P5, only the proximal portions of the male and female crabs are coloured dark brown throughout merus and dactylus are pinkish-purple, with the rest being their length. white. Euxanthus herdmani has previously been recorded from Camiguin Island, in the Philippines (Garth & Kim, 1983), as well as Sri Lanka and Seychelles, in the western Euxanthus Dana, 1851 Indian Ocean (Guinot-Dumortier, 1960; Serène, 1984). Euxanthus exsculptus (Herbst, 1790) Euxanthus huonii (Hombron & Jacquinot, 1846) Atergatis melissa – White, 1847: 14. Euxanthus punctatus – Ward, 1941: 2. (Fig. 1E) Euxanthus exsculptus – Guinot-Dumortier, 1960: 170. Euxanthus sculptilis – Miers, 1884: 204. Material examined. – 3 males, 60.2 × 37.6 mm to 62.1 × 38.9 mm, 4 females, 40.7 × 25.9 mm to 70.2 × 44.9 mm (NMCR-452), San Material examined. – 1 male, 31.9 × 21.9 mm (ZRC 2008.1376), Julian, Samar, coll. J. Hang, Nov.1958; 1 female, 50.0 × 32.3 mm Stn. M17, 9°33.4'N 123°43.0'E, Pontod Islet, Panglao Is., 0–1 m,

62 THE RAFFLES BULLETIN OF ZOOLOGY 2010 coll. PANGLAO 2004 Expedition, 09 Jun.2004; 1 female, 19.0 × from Amakusa and the East China Sea (Sakai, 1935, 1976). 13.2 mm (ZRC 2008.1377), Stn. S7, 9°38.5'N 123°49.2'E, Sungcolan This is the first time this species is recorded from the Bay, Panglao Is., 1–4 m, coll. PANGLAO 2004 Expedition, 09 Philippines. Jun.2004; 1 female, 23.6 × 16.3 mm (ZRC 2008.1378), Stn. S18, 9°35.7'N 123°44.4'E, Looc, Panglao Is., 0–2 m, coll. PANGLAO 2004 Expedition, 18 Jun.2004. Hepatoporus pumex Mendoza & Ng, 2008 Remarks. – This is a common species throughout the Indo- Hepatoporus pumex Mendoza & Ng, 2008b: 398, Figs. 7, 8, 9D. West Pacifi c region, from the Red Sea and the Persian Gulf to Tahiti, though it has not been recorded from Japan or the Material examined. – Male holotype, 8.0 × 5.7 mm (NMCR-27510), southwest Indian Ocean (Guinot-Dumortier, 1960). The live Stn. B11, coral rubble, 2–4 m, 9°29.4'N 123°56.0'E, Pamilacan Is., specimens are drab in colour, with a splotchy mix of light coll. PANGLAO 2004 Marine Biodiversity Project, 11 Jun.2004. and dark browns as well as gray in some specimens, which Paratypes: 1 male, 4.0 × 3.0 mm (ZRC 2008.0221), Stn. S28, reef probably help the crab camoufl age itself in the intertidal and wall with small caves, 28–32 m, 9°37.2'N 123°46.4'E, Napaling, shallow subtidal areas where it lives. Panglao Is., coll. PANGLAO 2004 Marine Biodiversity Project, 24 Jun.2004; 1 male, 3.8 × 2.7 mm (ZRC 2008.0222), Stn. S10, coral plateau with fi ne sand covering rocks, 6–14 m, 9°29.4'N 123°56.0'E, Pamilacan Is., coll. PANGLAO 2004 Marine Biodiversity Project, Guinotellus Serène, 1971 11 Jun.2004.

Guinotellus melvillensis Serène, 1971 Remarks. – This species was recently described by Mendoza & Ng (2008b), and is known only from the central Guinotellus melvillensis Serène, 1971: 905, Pl. 2 Fig. A; Serène Philippines. & Umali, 1972: 60, Pl. 6 Figs. 1–6; Mendoza et al., 2009: 43, Figs. 1-5.

Material examined. – Male holotype, 14.0 × 12.0 mm (MNHN- Hypocolpus Rathbun, 1897 B8363), 13–42 fathoms (24–77 m), off Cape Melville, Balabac Strait, coll. A. F. Umali, Pele Expedition, Sulu Sea, 9 Mar.1964; 2 Hypocolpus abbotti (Rathbun, 1894) males, 46.2 × 37.7 mm, 35.3 × 29.6 mm, 1 female, 43.4 × 36.4 mm (Fig. 3A, B) (MNHN-B8356), 1 male, 39.1 × 32.7 mm, 1 female, 38.1 × 33.4 mm (MNHN-B20292), 4°31'N 119°22'E, Sibutu Is., Sulu Archipelago, Material examined. – 2 males, 46.3 × 32.5 mm, 51.1 × 36.0 mm, coll. B. R. Wilson, Pele Expedition, Sulu Sea, 25 Feb.1964; 1 1 female, 45.0 × 30.8 mm (ZRC 2001.0469), Balicasag Is., 50–200 male, 51.0 × 41.2 mm, 1 female, 44.0 × 39.2 mm (NMCR-5427), m, coll. local fi shermen with tangle nets, Dec.2000; 1 male, 42.4 1 male, 42.0 × 35.0 mm, 1 female, 37.0 × 33.0 mm (NMCR-8867), × 29.1 mm (ZRC 2001.0673), Balicasag Is., 50–500 m, coll. local 3 males, 37.0 × 32.0 mm to 41.0 × 35.0 mm (NMCR-5435), Putic fi shermen with tangle nets, 28 Nov.2001; 1 male, 48.7 × 34.4 mm Is., Cuyo Is. Group, coll. P. C. Gonzales, V. Palpal-latoc, R. Rivera, (NMCR-27335), Balicasag Is., 50–200 m, coll. local fi shermen with P. Castaneda & J. Tahil, 6 Jul.–17 Aug.1975; 1 male, 36.0 × 32.0 tangle nets, 02 Mar.2004; 1 male, 41.6 × 28.7 mm (MNHN-B31888), mm (NMCR-5423), Calubcub II, San Juan, Batangas Province, Balicasag Is., 50–200 m, coll. local fi shermen with tangle nets, 29 Philippines, coll. R. Garcia & R. Rivera, March 1976. May 2004; 1 male, 39.1 × 27.1 mm (NMCR-27336), Balicasag Is., 50–200 m, coll. local fi shermen with tangle nets, May 2004; 1 Remarks. – This rare and unusual species has been recorded female, 7.9 × 5.8 mm (NMCR-27337), Stn. B19, reef slope with only from the Philippines thus far. Mendoza et al. (2009) cave, 17 m, 9°29.4'N 123°56.0'E, Pamilacan Is., coll. PANGLAO provide a redescription of this species, based on adult 2004 Marine Biodiversity Project, 21 Jun.2004. characters, as the holotype (cf. Serène, 1971; Serène & Umali, 1972) is a juvenile male. Remarks. – This species is easily differentiated from other species of Hypocolpus by its densely setose carapace and the morphology of the subhepatic cavity, which is divided Hepatoporus Serène, 1984 by two subparallel crests. All the adult specimens were collected in tangle nets. This species was fi rst described Hepatoporus orientalis (Sakai, 1935) from Aldabra Island in the Indian Ocean (Rathbun, 1894), (Fig. 1F) and has also been reported from nearby Madagascar (Guinot- Dumortier, 1960; Serène, 1984). In the western Pacifi c, it has Material examined. – 1 male, 8.1 × 6.0 mm (ZRC 2008.1379), Stn. been found in Amami-Oshima in southern Japan (Takeda, CP2862, 124–101 m, off western coast of Batangas, South China 1972) and Taiwan (Ho et al., 2000). This is the fi rst record Sea, coll. MV DA-BFAR, 23 Mar.2008. of Hypocolpus abbotti in the Philippines.

Comparative material. – Holotype male, 8.6 × 6.5 mm (KPM- NH0107080), between Ito City and Hatsushima Islet, Sagami Bay, Japan, coll. T. Sakai, 1932.

Remarks. – This species was originally described from Sagami Bay in Japan, and has subsequently been reported

63 Mendoza & Ng: Euxanthine crabs of the Philippines

Hypocolpus haanii Rathbun, 1909 4.0 × 2.9 mm (ZRC 2008.1381), Stn. B6, coral patches, 12–14 m, (Figs. 2A, 3C, D) 9°31.1'N 123°41.3'E, Black Forest, Balicasag Is., coll. PANGLAO 2004 Marine Biodiversity Project, 04 Jun.2004; 1 male, 4.1 × 3.1 Hypocolpus granulatus – Buitendijk, 1960: 308. mm, 2 females, 11.5 × 7.9 mm to 11.8 × 8.0 mm (ZRC 2008.1382), Stn. B8, subtidal reef platform, 3 m, 9°37.1'N 123°46.1'E, Napaling, Material examined. – 1 male, 25.1 × 17.7 mm (NMCR-27338), Panglao Is., coll. PANGLAO 2004 Marine Biodiversity Project, Balicasag Is., 50–200 m, coll. local ﬁ shermen with tangle nets, 02 07 Jun.2004; 1 male, 11.5 × 8.0 mm (ZRC 2008.1383), Stn. B11, Mar.2004; 1 male, 49.5 × 34.5 mm (NMCR-27339), Balicasag Is., coral rubble, 2–4 m, 9°29.4'N 123°56.0'E, Pamilacan Is., coll. 50–200 m, coll. local ﬁ shermen with tangle nets, 29 May 2004; PANGLAO 2004 Marine Biodiversity Project, 11 Jun.2004; 1 male, 1 male, 6.2 × 4.2 mm (ZRC 2008.1380), Stn. B5, reef slope with 7.6 × 5.4 mm, 1 female, 7.1 × 4.9 mm (ZRC 2008.1384), Stn. B19, overhangs, 4 m, 9°35.2'N 123°50.4'E, Biking, Panglao Is., coll. reef slope with cave, 17 m, 9°29.4'N 123°56.0'E, Pamilacan Is., PANGLAO 2004 Marine Biodiversity Project, 02 Jun.2004; 1 male, coll. PANGLAO 2004 Marine Biodiversity Project, 21 Jun.2004;

Fig. 2. Live colouration of euxanthine crabs from the Philippines: A, Hypocolpus haanii Rathbun, 1909, male juv., (11.5 × 8.0 mm) (B11, Pamilacan Is., ZRC 2008.1383); B, Ladomedaeus fungillus Manuel-Santos & Ng, 2007, male juv. (9.7 × 7.0 mm) (CP2708, ZRC 2008.1389); C, Miersiella cavifrons Takeda, 1989, male (9.8 × 6.6 mm) (L36, Panglao Is., ZRC 2008.1391); D, Paramedaeus globosus Serène & Vadon, 1981, male (6.0 × 4.6 mm) (T36, Cervera Shoal, MNHN-B31891); E, Paramedaeus simplex (A. Milne-Edwards, 1873), female (9.7 × 6.8 mm) (S7, Panglao Is., NMCR-27356); F, Paraxanthodes obtusidens (Sakai, 1965), male (18.6 × 13.0 mm) (CP2747, ZRC 2008.1410).

64 THE RAFFLES BULLETIN OF ZOOLOGY 2010

1 male, 5.2 × 3.7 mm (ZRC 2008.1385), Stn. B22, rubble on Cruise, 28 May 2005; 1 male, 9.7 × 7.0 mm (ZRC 2008.1390), Stn. mixed bottom, 15–20 m, 9°29.4'N 123°56.0'E, Pamilacan Is., CP2708, 309 m, 15°07.61'N 121°36.95'E, off the eastern coast of coll. PANGLAO 2004 Marine Biodiversity Project, 24 Jun.2004; Luzon, coll. MV DA-BFAR, AURORA 2007 Deep-Sea Cruise, 1 male, 8.2 × 5.8 mm (ZRC 2008.1386), Stn. B24, fl oor of cave, 28 May 2007. 38 m, 9°29.4'N123°56.0'E, Pamilacan Is., coll. PANGLAO 2004 Marine Biodiversity Project, 25 Jun.2004; 1 female, 17.6 × 11.6 mm Remarks. – Ladomedaeus Štev i , 2005, was established for (ZRC 2008.1387), Stn. B37, fl oor of cave, with corals and sponges, an unusual species of Medaeus, M. serratus Sakai, 1965, from 19–20 m, 9°30.9'N 123°40.8'E, Balicasag Is., coll. PANGLAO 2004 Japan. A second species, L. fungillus from the Philippines, Marine Biodiversity Project, 02 Jul.2004; 1 male, 6.1 × 4.1 mm was described by Manuel-Santos & Ng (2007) based on (ZRC 2008.1388), Stn. S10, coral plateau with fi ne sand covering rocks, 6–14 m, 9°29.4'N 123°56.0'E, Pamilacan Is., coll. PANGLAO material collected from the islands of Balicasag and Panglao. 2004 Marine Biodiversity Project, 11 Jun.2004. Material reported here are those that have not been listed by Manuel-Santos & Ng (2007). Live specimens are basically Remarks. – This is one of the most common euxanthine reddish-orange, with juveniles having a mottling of white species to be collected from the Bohol Sea. The live on the carapace and chelipeds, and a more-or-less regular colouration of the juvenile form is noted here: the carapace banded pattern of white and orange on the ambulatory legs. is basically rosy pink, with splotches of red or purple; the The fi ngers of the chela are brown to black throughout their chelipeds are similarly hued but lighter and more mottled, entire length, but not extending into the palm. This species the inner surface of the palm and carpus is white, and the is known only from the Philippines. fi ngers are a light brown, becoming even lighter at the tips; the ambulatory legs are a mottled brown and white. Many of the specimens collected are juveniles, and these were Medaeops Guinot, 1967 collected by coral brushing or vacuum suctioning. All of the adults were collected by tangle net. Hypocolpus haanii has Medaeops granulosus (Haswell, 1882) been reported previously from Japan and Thailand (Guinot- (Fig. 4G) Dumortier, 1960). Medaeops granulosus – Serène & Umali, 1972: 65, Pl. 7: Figs. 1, 2; Serène & Vadon, 1981: 122. Hypocolpus kurodai Takeda, 1980 Material examined. – 1 male, 12.0 × 8.5 mm, 2 females, 12.5 × (Fig. 3E, F) 9.0 mm, 13.0 × 9.5 mm (NMCR-9705), among dead coral, 2 m, Manigo-nigo Is., Carles, Iloilo, coll. V. G. Bautista, May 1989. Hypocolpus kurodai – Takeda & Manuel, 2000: 153, Fig. 3D, E. Remarks. – This species is apparently restricted to the Material examined. – 1 male, 21.0 × 13.5 mm (NMCR-6609), western Pacific and eastern Indian oceans, particularly Kasili, Santa Cruz, Marinduque, coll. J. Cabrera, R. Garcia & R. Velarde, 21 Aug.1979. Australia (type locality), the eastern coast of China, and Japan (Guinot,1967a). It has also been recorded from Remarks. – This little-known species has only been recorded Korea, Singapore and Taiwan, (Buitendijk, 1950; Kim & from Japan (type locality) and the Philippines. The specimen Kim, 1982; Ng et al., 2001). In the Philippines, it has been reported here is the same one recorded by Takeda & Manuel previously recorded from Quezon, Palawan Island (Serène & (2000) in their report on some rare Philippine crabs. Umali, 1972) and Lubang Island, off the southwestern coast of Luzon (Serène & Vadon, 1981). Records of Medaeops granulosus elsewhere, e.g. the Persian Gulf, the Red Sea, Ladomedaeus Štev i , 2005 Mauritius, India and South Africa (cf. Stephensen, 1945; Barnard, 1950; Michel, 1964) should be considered as those Ladomedaeus fungillus Manuel-Santos & Ng, 2007 for a similar species, Medaeops neglectus (Balss, 1922) (see (Fig. 2B) Guinot, 1967a; Serène, 1984).

Ladomedaeus fungillus Manuel-Santos & Ng, 2007: 181, Figs. 3–5. Medaeus Dana, 1851

Material examined. – 2 males, 17.1 × 11.8 mm to 17.8 × 12.5 Medaeus elegans A. Milne-Edwards, 1867 mm (NMCR-27341), Stn. P4, local ﬁ shermen with tangle nets, ca. 100 m, 9°31.1'N 123°41.5'E, Balicasag Is., coll. PANGLAO 2004 Medaeus elegans – Serène & Umali, 1972: 63, Pl. 6 Figs. 7–10. Marine Biodiversity Project, 31 May 2004; 1 female, 8.6 × 6.1 mm (NMCR-27342), Balicasag Is., 50–200 m, coll. local ﬁ shermen with Material examined. – 1 male, 13.9 × 11.0 mm, 1 ovig. female, tangle nets, Feb.2004; 2 males, 11.0 × 8.2 mm to 11.1 × 7.9 mm, 13.9 by 10.0 mm (ZRC 1973.10.31.102–103), Stn. D7, 10 fathoms 2 females, 10.2 × 7.0 mm to 11.7 × 8.2 mm (NMCR-27343), Stn. (18 m), Pearl Bank, Sulu Sea, coll. A. F. Umali, Pele-Sulu Sea CP2380, Dipolog Bay, 150–163 m, 8°41.3'N 123°17.8'E, Bohol/ Expedition, 15 Feb.1964. Sulu seas sill, coll. MV DA-BFAR, PANGLAO 2005 Deep-Sea Cruise, 28 May 2005; 1 male, 12.7 × 9.1 mm (NMCR-27344), Stn. Remarks. – This species was described from New Caledonia CP2381, Dipolog Bay, 259–280 m, 8°43.3'N 123°19.0'E, Bohol/ (A. Milne-Edwards, 1867) and has been reported from Hawaii Sulu seas sill, coll. by MV DA-BFAR, PANGLAO 2005 Deep-Sea (Edmondson, 1925, 1962; Guinot, 1967a). Serène & Umali,

65 Mendoza & Ng: Euxanthine crabs of the Philippines

(1972) reported one male and one ovigerous female from Philippine material as “Medaeus elegans” is provisionally Pearl Bank in the Sulu archipelago, collected during the followed pending further revisions. Pele Sulu Sea Expedition. There have been no other reports of this species from the Philippines since. The taxonomy of this species will pose problems. The authors have noted key Miersiella Guinot, 1967 differences between the New Caledonian (type), Hawaiian and Philippine specimens (unpublished data), and it is likely Miersiella cavifrons Takeda, 1989 that Medaeus elegans, as presently known, is actually a (Fig. 2C) species complex. Although Serène & Umali (1972) make detailed comparisons between their Philippine material and Miersiella haswelli – Serène & Vadon, 1981: 134, Pl. 3 Fig. B, not other specimens recorded elsewhere, including the type, they Medaeus haswelli Miers, 1886. were based on published text and fi gures and not on the actual specimens themselves. In any case, their identifi cation of the Material examined. – 1 male, 8.5 × 6.0 mm (NMCR-27345), Balicasag Island, 50–200 m, coll. local fi shermen with tangle nets,

Fig. 3. Hypocolpus abbotti (Rathbun, 1894), male, (41.6 by 28.7 mm) (Balicasag Is., MNHN-B31888): A, dorsal view; B, fronto-lateral view of subhepatic cavity; Hypocolpus haanii Rathbun, 1909, male (49.5 × 34.5 mm) (Balicasag Is., NMCR-27339); C, dorsal view; D, fronto-lateral view of subhepatic cavity; Hypocolpus kurodai Takeda, 1980, male (21.0 × 13.5 mm) (Marinduque, NMCR-6609); E, dorsal view; F, fronto-lateral view of subhepatic cavity.

66 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Fig. 4. Epistocavea mururoa Davie, 1993, male (33.2 × 23.5 mm) (L36, ZRC 2008.1371): A, dorsal view; B, frontal view; Miersiella haswelli (Miers, 1886), male (7.4 × 5.5 mm) (CP2343, Pamilacan Is., ZRC 2008.1400); C, dorsal view; D, ventral view; Paraxanthodes obtusidens (Sakai, 1965), female (30.1 × 20.3 mm) (Balicasag Is., NMCR-27357); E, dorsal view; F, frontal view; G, Medaeops granulosus (Haswell, 1882), female (12.5 × 9.0 mm) (Iloilo, NMCR-9705); H, Paraxanthodes cumatodes (MacGilchrist, 1905), male (5.7 × 4.1 mm) (T1, Panglao Is., ZRC 2008.1409).

67 Mendoza & Ng: Euxanthine crabs of the Philippines

Apri.2004; 1 male, 6.9 × 4.7 mm (NMCR-27346), Stn. B12, reef Figs. 17–20; Serène & Vadon, 1981: 134, Figs. 2g–i, 3, slope, 24–27 m, 9°35.6'N 123°43.2'E, Doljo Point, Panglao Is., Pl. 3). Takeda (1989: 162, Figs. 12–13) described a new coll. PANGLAO 2004 Marine Biodiversity Project, 14 Jun.2004; species, Miersiella cavifrons, from one male and one female 1 male, 4.0 × 2.7 mm (NMCR-27347), Stn. B16, coral rubble on specimen collected in the Ryukyu Islands and Kii Peninsula sand and gravel, 20 m, 9°37.6'N 123°47.3'E, Bingag, Panglao Is., in Japan. He, however, made no mention of the report of coll. PANGLAO 2004 Marine Biodiversity Project, 17 Jun.2004; 1 male, 9.8 × 6.6 mm (ZRC 2008.1391), Stn. L36, 85–90 m, 9°36.7'N Serène & Vadon (1981). The present collection agrees well 123°45.8'E, Looc, Panglao Is., coll. PANGLAO 2004 Marine with the illustrations provided by Takeda (1989) and Serène Biodiversity Project, 21 Jun.2004; 3 females, 5.8 × 4.0 mm to 6.4 × & Vadon (1981). In the current series of specimens, the G1 4.4 mm (NMCR-27348), Stn. L40, 100–120 m, 9°37.3'N 123°46.5'E, of the adult males resembles that seen in Serène & Vadon Tangnan, Panglao Is., coll. PANGLAO 2004 Marine Biodiversity (1981), more than in Takeda (1989), but this can be attributed Project, 24 Jun.2004; 3 females, 4.7 × 3.3 mm to 6.6 × 4.6 mm to the fact that Takeda’s male paratype is still immature (ZRC 2008.1392), Stn L41, 90–100 m, 9°31.3'N 123°41.2'E, in and the G1 has not yet developed fully. Comparison of the front of PTA compound, Panglao Is., coll. PANGLAO 2004 Marine Philippine specimens with the male paratype and female Biodiversity Project, 1 Jul.2004; 4 males, 3.6 × 2.4 mm to 9.3 × 6.5 holotype from Japan confi rms this. As such, M. cavifrons mm, 7 females, 3.4 × 2.6 mm to 7.1 × 4.6 mm (MNHN-B30704), Stn. L42, 80–90 m, 9°31.2'N 123°40.7'E, Balicasag Is., coll. PANGLAO is now known from southwestern Japan (Ryukyu Islands) 2004 Marine Biodiversity Project, 02 Jul.2004; 1 female, 5.4 × 3.8 and the Philippines (South China Sea and Bohol Sea). This mm (ZRC 2008.1393), Stn. L44, 85–100 m, 9°30.8'N 123°41.0'E, species is one of the most abundant euxanthine crabs to be Balicasag Is., coll. PANGLAO 2004 Marine Biodiversity Project, 3 collected from the Bohol Sea. Jul.2004; 1 male, 8.0 × 5.6 mm (NMCR-27349), Stn. L46, 90–110 m, 9°30.9'N 123°41.2'E, Balicasag Is., coll. PANGLAO 2004 Marine Biodiversity Project, 4 Jul.2004; 1 male, 4.1 × 3.0 mm, 4 Miersiella haswelli (Miers, 1886) females, 3.4 × 2.5 mm to 6.1 × 4.2 mm (NMCR-27350), Stn. P1, (Fig. 4C, D) 90–200 m, 9°36.1'N 123°45.0'E, Maribohoc Bay, Bohol Is., coll. PANGLAO 2004 Marine Biodiversity Project, 30 May 2004; 1 Material Examined. – 1 male, 7.4 × 5.5 mm, 2 females, 5.6 × 4.1 male, 4.2 × 3.0 mm, 1 female, 3.5 × 2.7 mm (ZRC 2008.1394), mm to 6.4 × 4.6 mm (ZRC 2008.1400), Stn. CP2343, off Pamilacan Stn. P2, 400 m, 9°39.0’N 123°43.8’E, Maribohoc Bay, Bohol Is., Is., 273–356 m, 9°27.4'N 123°49.4'E, Bohol Sea, coll. MV DA- coll. PANGLAO 2004 Marine Biodiversity Project, 30 May 2004; BFAR, PANGLAO 2005 Deep-Sea Cruise, 23 May 2005; 1 male 1 male, 6.7 × 4.8 mm (ZRC 2008.1395), Stn. T1, mud and many (damaged), 5.0 × 3.7 mm (ZRC 2008.1401), Stn. DW2376, off sponges, 83–102 m, 9°32.4'N 123°47.3'E, Bolod, Panglao Is., coll. Aligbay Is., 189–219 m, 8°40.7'N 123°16.1'E, Bohol/Sulu seas PANGLAO 2004 Marine Biodiversity Project, 30 May 2004; 2 sill, coll. MV DA-BFAR, PANGLAO 2005 Deep-Sea Cruise, 28 males, 6.9 × 4.7 mm, 7.0 × 4.9 mm, 2 females, 5.5 × 3.8 mm, 5.7 May 2005. × 3.9 mm (ZRC 2008.1396), Stn. T11, sponges and muddy sand, 78–95 m, 9°40.9'N 123°50.0'E, Maribohoc Bay, Bohol Is., coll. PANGLAO 2004 Marine Biodiversity Project, 16 Jun.2004; 2 males, Remarks. – This species was described from New South 6.6 × 4.6 mm, 7.8 × 5.5 mm, 1 female, 5.1 × 3.5 mm, 1 juv., 2.6 Wales, eastern Australia as Medaeus haswelli Miers, 1886. × 2.0 mm (ZRC 2008.1397), Stn. T13, with sponges, 90–100 m, Guinot (1967a) established a new genus, Miersiella, and 9°40.5'N 123°49.5'E, Maribohoc Bay, Bohol Is., coll. PANGLAO designated it as the type species. The present specimens agree 2004 Marine Biodiversity Project, 17 Jun.2004; 2 males, 6.1 × 4.3 well with the illustrations provided by Miers (1886: 117, mm, 7.5 × 5.3 mm, 2 females, 4.7 × 3.4 mm, 5.1 × 3.5 mm, 1 juv., Pl. XI, Fig. 2) and Guinot (1967a: 359–362, Figs. 17–20). 3.2 × 2.1 mm (ZRC 2008.1398), Stn. T38, sponge bed, 80–140 m, Miersiella haswelli has been erroneously reported from the 9°32.3'N 123°42.3'E, Balicasag Is., coll. PANGLAO 2004 Marine Philippines by Serène & Vadon (1981), but their specimens Biodiversity Project, 4 Jul.2004; 2 males, 8.0 × 5.4 mm, 8.2 × 5.6 mm, 1 juv., 2.3 × 1.9 mm (ZRC 2008.1399), Stn. T41, 110–112 m, are actually Miersiella cavifrons (see earlier Remarks). 9°29.7'N 123°50.2'E, Cervera Shoal, west of Pamilacan Is., coll. Therefore, this report is in fact the fi rst record of Miersiella PANGLAO 2004 Marine Biodiversity Project, 6 Jul.2004. haswelli from the Philippines. The species has previously been recorded from Christmas Island in the Indian Ocean, and Comparative material. – Holotype female, 8.7 × 5.7 mm (NSMT-Cr Japan, New Caledonia, the Loyalty Islands, Norfolk Ridge, 9723), Stn. 20, coarse sand & shell, 45 m, west side of Nominoura, Wallis Island, Waterwitch Bank and Kermadec Island, in Oshima Passage, Amami-Oshima, southwestern Japan coll. M the Western Pacifi c (Davie, 1997; Takeda & Weber, 2006; Takeda, 6 Aug.1988; paratype male, 5.4 × 3.8 mm (NSMT-Cr Ahyong, 2008). 9724), 40–70 m, off Kushimoto, Kii Peninsula, central Japan, coll. S. Nagai, 5 Sep.1979.

Paramedaeus Guinot, 1967 Remarks. – This species was first reported from the Philippines by Serène & Vadon (1981) as Miersiella haswelli Paramedaeus globosus Serène & Vadon, 1981 (Miers, 1886). However, the ﬁ gures they provided did not (Fig. 2D) agree with the known description of Miersiella haswelli, particularly in the form of the ﬁ rst two anterolateral teeth Paramedaeus planifrons globosus Serène & Vadon, 1981: 130, (larger, distally spiniform and curved anteriorly vs. smaller, Pl. 3 Fig. A. broadly triangular in Miersiella haswelli), the ambulatory legs (longer and more slender vs. shorter and stouter in Miersiella Material examined. – 1 male, 3.2 × 2.6 mm (ZRC 2008.1402), haswelli), and the G1 (longer and more slender, and with a Stn. P2, local fishermen with tangle nets, 400 m, 9°39.0'N different terminal conformation) (cf. Guinot, 1967a: 359–362, 123°43.8'E, Maribojoc Bay, Bohol Is., coll. PANGLAO 2004

68 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Marine Biodiversity Project, 30 May 2004; 1 male, 8.9 × 6.6 mm Paramedaeus simplex (A. Milne-Edwards, 1873) (NMCR-27351), 5 males, 3.1 × 2.5 mm to 5.6 × 4.3 mm, 7 females, (Fig. 2E) 3.3 × 2.6 mm to 7.2 × 5.4 mm, 4 juv., 2.4 × 2.1 mm to 3.2 × 2.5 mm (ZRC 2008.1403), Stn. T1, mud and many sponges, 83–102 Paramedaeus simplex – Serène & Umali, 1972: 67, Pl. 7 Figs. m, 9°32.4'N 123°47.3'E, Bolod, Panglao Is., coll. PANGLAO 2004 3–4. Marine Biodiversity Project, 30 May 2004; 1 male, 9.2 × 6.8 mm (MNHN-B30705), 2 males, 5.5 × 4.3 mm to 7.7 × 5.9 mm, 3 females, Material examined. – 1 male, 14 × 9.0 mm (ZRC 1965.8.4.1), 4.7 × 3.6 to 7.4 × 5.6 mm (ZRC 2008.1404), Stn. T2, coarse sand, Batangas, coll. P. Palarca, 25 Apr.1963; 2 juv., 3.9 × 3.0 to 4.1 152 m, 9°32.4'N 123°47.8'E, Bolod, Panglao Is., coll. PANGLAO × 3.0 (NMCR-27355), Stn. B14, coral rubble, 2–4 m, 9°38.5'N 2004 Marine Biodiversity Project, 31 May 2004; 7 males, 4.1 × 3.1 123°49.2'E, Sungcolan Bay, Panglao Is., coll by Panglao Marine mm to 5.8 × 4.6 mm, 5 females, 3.9 × 3.0 mm to 5.4 × 4.2 mm, 1 Biodiversity Project, 16 Jun.2004; 1 male, 9.0 × 6.2 mm, 1 ovig. juv., 2.5 × 2.1 mm (NMCR-27352), Stn. T4, many large sponges, female, 11.1 × 7.8 mm, 1 juv., 4.7 × 3.4 mm (ZRC 2008.1408), 82 m, 9°33.0'N 123°48.5'E, Bolod, Panglao Is., coll. PANGLAO Stn. B18, blocks dispersed among seagrass, 3–5 m, 9°38.5'N 2004 Marine Biodiversity Project, 01 Jun.2004; 1 male, 4.4 × 3.4 123°49.7'E, Sungcolan Bay, Panglao Is., coll. PANGLAO 2004 mm, 2 females, 5.7 × 4.3 mm to 8.1 × 6.1 mm (ZRC 2008.1405), Marine Biodiversity Project, 20 Jun.2004; 1 female, 9.7 × 6.8 mm Stn. T5, coarse muddy sand, 84–87 m, 9°35.3'N 123°52.2'E, west (NMCR-27356), Stn. S7, sand with seagrass, 1–4 m, 9°38.5'N of Baclayon, Bohol Is., coll. PANGLAO 2004 Marine Biodiversity 123°49.2'E, Sungcolan Bay, Panglao Is., coll. PANGLAO 2004 Project, 02 Jul.2004; 12 males, 4.3 × 3.3 mm to 6.2 × 4.9 mm, 4 Marine Biodiversity Project, 09 Jun.2004. females, 4.5 × 3.4 mm to 5.5 × 4.2 mm, 1 ovig. female, 4.6 × 3.5 mm (ZRC 2008.1406), Stn. T9, fi ne sand with seagrass, 97–120 m, Remarks. – This species was described from Madagascar (A. 9°33.5’/9°33.9'N 123°49.5'/123°50.5'E, off San Isidro, Panglao Is., coll. PANGLAO 2004 Marine Biodiversity Project, 14 Jun.2004; Milne-Edwards, 1873) and has been reported from various 1 female, 5.9 × 4.5 mm (NMCR-27353), Stn. T10, mud and fi ne localities in the Indian Ocean (Ward, 1942; Guinot, 1967a; sand, 117–124 m, 9°33.4'/9°33.8'N 123°49.6'/123°51.5'E, off San Serène, 1984) and in the Pacifi c Ocean (De Man, 1902; Isidro, Panglao Is., coll. PANGLAO 2004 Marine Biodiversity Rathbun, 1906; Edmonson, 1925; Takeda, 1972, 1976; Ng Project, 15 Jun.2004; 1 male, 6.1 × 4.7 mm (ZRC 2008.1407), Stn. & Clark, 2002). This species has been previously reported T19, mud, 10–26 m, 9°42.2'N 123°50.8'E, Cortes, Bohol Is., coll. from the Philippines by Serène & Umali (1972), based on PANGLAO 2004 Biodiversity Project, 20 Jun.2004; 1 male, 5.9 × a single male collected from Batangas. It is interesting to 4.6 mm (NMCR-27354), Stn. T28, muddy sand, 80 m, 9°35.0'N note that all of the specimens reported in this paper, one of 123°51.4'E, Biking-Catarman, Panglao Is., coll. PANGLAO 2004 them ovigerous, are much smaller than this male specimen Biodiversity Project, 01 Jul.2004; 1 male, 7.4 × 5.2 mm, 1 female, 4.7 × 3.4 mm (MNHN-B30706), Stn. T29, mud, 77–84 m, 9°34.5'N (carapace, 14.0 × 9.0 mm). Ng & Clark (2002) remarked on 123°50.6'E, Biking, Panglao Is., coll. PANGLAO 2004 Marine the differences in size at maturity of the specimens found Biodiversity Project, 01 Jul.2004; 2 males, 4.2 × 3.2 mm to 6.0 × in Hawaii, Guam, New Caledonia and the Philippines and 4.6 mm (MNHN-B31891), Stn. T36, sand bed with echinoderms, suggested that Paramedaeus simplex may be a species 95–128 m, 9°29.3'N 123°51.5'E, Cervera Shoal, west of Pamilacan complex. The present material also indicates that a revision Is., coll. PANGLAO 2004 Biodiversity Project, 04 July 2004; 2 of this species is clearly necessary. females, 3.3 × 2.6 mm to 5.8 × 4.6 mm (MNHN-B31892), Stn. T41, 110–112 m, 9°29.7'N 123°50.2'E, Cervera Shoal, west of Pamilacan Is., coll. PANGLAO 2004 Marine Biodiversity Project, Paraxanthodes Guinot, 1967 06 July 2004. Paraxanthodes cumatodes (MacGilchrist, 1905) Remarks. – This species was fi rst collected in the Philippines (Fig. 4H) by the MUSORSTOM I expedition and described as a new subspecies of Paramedaeus planifrons Sakai, 1965, by Serène Material examined. – 1 male, 5.7 × 4.1 mm (ZRC 2008.1409), & Vadon (1981) and then subsequently elevated to full species Stn. T1, mud and many sponges, 83–102 m, 9°32.4'N 123°47.3'E, rank by Davie (1997). The holotype in MNHN cannot be Bolod, Panglao Is., coll. PANGLAO 2004 Marine Biodiversity located (R. Cleva, pers. comm.) and there are no paratypes. Project, 30 May 2004. This species is one of the most abundant euxanthines collected from the Bohol Sea. It is found in a variety of habitats, but Remarks. – This species was fi rst placed in Xanthodes Dana, more commonly in muddy to sandy substrate, and often 1852, by MacGilchrist (1905), but was later transferred to found where there are sponges and echinoderms. Individuals a new genus, Paraxanthodes, by Guinot (1967b) together are quite variable in their live colour patterns, though the with Paraxanthodes obtusidens (Sakai, 1965). It has been carapace and pereopods are basically white, with patches reported from the Red Sea and the Persian Gulf (Guinot, of light or dark brown, yellow- or reddish-orange. The 1976b), and also from New Caledonia in the Pacifi c (Davie, fi ngers of the chelae are dark brown throughout their length, 1997). The present specimen agrees with the illustrations though not extending into the palm. Outside the Philippines, provided by MacGilchrist (1905) and Guinot (1967b). This Paramedaeus globosus has also been collected from New is the fi rst record of this species in the Philippines. Davie Caledonia and the Loyalty Islands (Davie, 1997). (1997) argued that Paraxanthodes is closely allied to the genera Alainodaeus, Medaeus, Medaeops, Paramedaeus and Monodaeus and forms a monophyletic grouping with these based on the condition of the carapace, sternum, male abdomen and the anterior portion of the carapace anterolateral margin. For this reason, he included Paraxanthodes in the

69 Mendoza & Ng: Euxanthine crabs of the Philippines

Euxanthinae. Ng et al. (2008) also noted that like other Visayax Mendoza & Ng, 2008 euxanthine genera, Paraxanthodes possesses a strongly differentiated basal tooth on the dactylus of the major chela. Visayax estampadori Mendoza & Ng, 2008 Consequently, Paraxanthodes is provisionally placed in Euxanthinae. Visayax estampadori Mendoza & Ng, 2008b: 395, Figs. 5, 6, 9C.

Material examined. – Holotype male, 6.7 × 4.6 mm (NMCR- Paraxanthodes obtusidens (Sakai, 1965) 27509), Stn. B17, reef wall with small caves, 3–21 m, 9°37.5'N 123°46.9'E, Bingag, Panglao Is., coll. PANGLAO 2004 Marine (Figs. 2F, 4E, F) Biodiversity Project, 19 Jun.2004; paratype male, 4.5 × 3.3 mm (ZRC 2008.0220), Stn. B21, reef wall with small caves, 20–21 m, Material examined. – 1 male, 31.5 × 22.2 mm, 1 female, 30.1 × 20.3 9°37.2'N 123°46.4'E, Napaling, Panglao Is., coll. PANGLAO 2004 mm (NMCR-27357), Balicasag Is., 50–200 m, coll. local fi shermen Marine Biodiversity Project, 24 Jun.2004. with tangle nets, purch. P. K. L. Ng, 25 Oct.2003; 1 male, 18.6 × 13.0 mm (ZRC 2008.1410), Stn. CP2747, 118–124 m, 15°55.53'N Remarks. – This species was recently described by 121°42.12'E, off the eastern coast of Luzon, coll. MV DA-BFAR, AURORA 2007 Deep-Sea Cruise, 2 Jun.2007. Mendoza & Ng (2008b), and is known only from the central Philippines. Remarks. – This species was fi rst assigned to Micropanope by Sakai (1965), but was later transferred to a new genus, Paraxanthodes, by Guinot (1967b), wherein she designated Visayax osteodictyon Mendoza & Ng, 2008 it as the type species. The Philippine material agrees well with the illustrations provided by Sakai (1965a: 103, Figs. Visayax osteodictyon Mendoza & Ng, 2008b: 392, Figs. 3, 4, 9B. 2c, 3e, f) and Guinot (1967b: 723–726, Figs. 51a, b, 59). The Material examined. – Holotype male, 6.3 × 4.3 mm (NMCR- live colouration is as follows; the carapace and chelipeds and 27508), Stn. S22, hard ground covered with sand, 15–22 m, ambulatory legs are deep reddish-orange, with lighter areas 9°29.4'N 123°56.0'E, Pamilacan Is., coll. PANGLAO 2004 Marine of yellowish-white immediately surrounding the third and Biodiversity Project, 21 Jun.2004; paratypes – 1 male, 2.3 × 1.7 fourth anterolateral teeth. There are small patches of white mm (ZRC 2008.0218), Stn. B17, reef wall with small caves, 3–21 particularly in the cardiac region and in the grooves between m, 9°37.5'N 123°46.9'E Bingag, Panglao Is., coll. PANGLAO 2004 the bases of 2M and 3M. The fi ngers of the chela are dark Marine Biodiversity Project, 19 Jun.2004; 1 male, 3.3 × 2.2 mm, brown all throughout their length, but not extending to the 1 female, 3.4 by 2.3 mm (ZRC 2008.0219), Stn. B39, reef wall palm. Other than the type locality (Sagami Bay, Japan), it with small caves, 17–25 m, 9°32.8'N 123°42.1'E, Pontod Lagoon 1, Panglao Is., coll. PANGLAO 2004 Marine Biodiversity Project, has also been recorded from Muroto-zaki, Kii Nagashima, 2 Jul.2004. Kii Minabe, and Tosa Bay, all in Japan (Yokoya, 1933; Sakai, 1965b, 1976), and also from the South China Sea Remarks. – This is the type species of Visayax, recently (Guinot, 1967b). This is the fi rst record of this species in described by Mendoza & Ng (2008b). It is known only from the Philippines. the central Philippines.

Rizalthus Mendoza & Ng, 2008 GENERAL DISCUSSION

Rizalthus anconis Mendoza & Ng, 2008 As a result of the present review, there are now 25 species of Euxanthinae, distributed among 16 genera, known from Rizalthus anconis Mendoza & Ng, 2008b: 387, Figs. 1, 2, 9A. the Philippines (Table 1). Six of these, Epistocavea mururoa, Material examined. – Holotype male, 12.5 × 7.9 mm (NMCR- Hepatoporus orientalis, Hypocolpus abbotti, Miersiella 27507), Stn. R30, reef slope with black coral, 15–37 m, 9°37.1'N haswelli, Paraxanthodes cumatodes and Paraxanthodes 123°46.1'E, Napaling, Panglao Is., coll. PANGLAO 2004 Marine obtusidens, are new records for the country. While most Biodiversity Project, 8 Jun.2004; paratypes – 2 females, 7.8 × 4.5 of these have been recorded from the Western Paciﬁ c or mm to 11.2 × 7.3 mm (MNHN-B30700), 1 ovigerous female, 12.7 Southeast Asia, there are some that represent a remarkable × 8.1 mm (ZRC 2008.0215), Stn. B39, reef wall with small caves, range extension (i.e. Alainodaeus and Epistocavea mururoa). 17–25 m, 9°32.8'N 123°42.1'E, Pontod Lagoon 1, Panglao Is., coll. One species, Crosnierius carinatus, is here reported only for PANGLAO 2004 Marine Biodiversity Project, 2 Jul.2004; 1 male, the second time from the Philippines and has not been found 4.2 × 2.7 mm (ZRC 2008.0216), Stn. B10, reef wall with small elsewhere. Many of the species listed here were collected from caves, 3–14 m, 9°36.5'N 123°45.6'E, Momo Beach, Panglao Is., coll. PANGLAO 2004 Marine Biodiversity Project, 10 Jun.2004; the Panglao-Balicasag area, in the Bohol Sea, which, together 1 female, 7.0 × 4.3 mm (ZRC 2008.0217), Stn. B17, reef wall with with recent studies on other crab groups – Dromiidae and small caves, 3–21 m, 9°37.5'N 123°46.9'E Bingag, Panglao Is., coll. Dynomenidae (McLay & Ng, 2004, 2005); Homolodromiidae PANGLAO 2004 Marine Biodiversity Project, 19 Jun.2004. (Ng & McLay, 2005); Homolidae (Takeda & Manuel-Santos, 2007; Richer de Forges & Ng, 2007b); Calappidae (Ng, Remarks. – This is the type species of the monotypic genus 2002); Leucosiidae (Komatsu et al., 2005; Galil & Ng, 2007); Rizalthus, recently described by Mendoza & Ng (2008b), Hymenosomatidae (Naruse et al., 2008) – gives credence and known only from the central Philippines.

70 THE RAFFLES BULLETIN OF ZOOLOGY 2010 to the claim that this area is species-rich for marine fauna, Chen, H. L., 1985. Decapod Crustacea: Dorippidae. Resultats des particularly (but not limited to) brachyurans. campagnes MUSORSTOM. I et II – Philippines (1976, 1980). Tome 2. Mémoires du Muséum national d’Histoire naturelle, Sér. A, Zoologie, 133: 179–204. ACKNOWLEDGEMENTS Castro, P., 2007. A reappraisal of the family Goneplacidae Macleay, 1838 (Crustacea, Decapoda, Brachyura) and revision of the We thank the organizers and participants of the PANGLAO subfamily Goneplacinae, with the description of ten new genera, Zoosystema 29 2004 and 2005 and the AURORA 2007 expeditions: and eighteen new species. , (4): 609–774. particularly the principal investigators, Philippe Bouchet Crosnier, A., 1997. Hypocolpus pararugosus, espèce nouvelle (MNHN) and Danilo Largo (USC), for PANGLAO 2004, de l’Indo-Ouest Pacifi que (Crustacea, Decapoda, Brachyura, and Philippe Bouchet and Ludivina Labe (NFRDI), for Xanthidae). Bulletin du Muséum national d’Histoire naturelle, 18 (3–4): 557–564. PANGLAO 2005, and Philippe Bouchet and Marivene Manuel-Santos (NMP) for AURORA 2007, as well as the Crosnier, A., 2002. Révision du genre Parathranites Miers, main logistician, Noel Saguil (USC). We are grateful for the 1886 (Crustacea, Brachyura, Portunidae). Zoosystema, 24(4): 799–825. positive reception of these expeditions from Senator Ernesto Angara and the local governments of Bohol and Aurora. Davie, P. J. F., 1993. Deepwater xanthid crabs from French The TOTAL Foundation, the Museum national d’Histoire Polynesia (Crustacea, Decapoda, Xanthoidea). Bulletin du Muséum national d’Histoire naturelle, 4e sér., 14A(2): 501–561. naturelle (MNHN) in Paris, the University of San Carlos Pls. 1–13. (USC) in Cebu, the Philippine Department of Agriculture’s Bureau of Fisheries and Aquatic Resources (BFAR), the Davie, P. J. F., 1997. Crustacea Decapoda: deep water Xanthoidea National Fisheries Research and Development Institute from the south-western Pacifi c and the western Indian Ocean. In : A. Crosnier (ed.) Resultats des campagnes MUSORSTOM, (NFRDI), the National Museum of the Philippines (NMP), Volume 18. Memoires du Muséum national d’Histoire naturelle, and the National University of Singapore (NUS) all provided 176: 337–387. valuable logistical support. We are grateful for the help of Dana, J. D., 1851. On the classifi cation of the Cancroidea. American our colleagues, Daniéle Guinot, Régis Cleva, Tan Swee Journal of Science and Arts, 12(34): 121–131. Hee, Chan Tin Yam, Marivene R. Manuel-Santos, Joelle Lai, Lin Chia Wei and Lawrence Liao during our museum Dana, J. D., 1852. Conspectus Crustaceorum quae in Orbis Terrarum circumnavigatione lexit et descripsit. Conspectus of visits and fi eldwork. Hiroshi Namikawa & Hironori Komatsu the Crustacea of the Exploring Expedition under Capt. Wilkes (NSMT) and Takehiro Sato (KPMNH) kindly provided us U.S.N. Proceedings of the Academy of Natural Sciences of with the Japanese type specimens used in this paper. Thanks Philadelphia, 6: 73–86. are also due to Paul Clark and an anonymous reviewer for Edmondson, C. H., 1925. Crustacea. In: Marine Biology of Tropical their helpful comments and suggestions for the improvement Central Pacifi c. (Tanager Expedition Publ. 1). Bulletin of the of this paper. This study was supported by ARF Grant No. Bernice P. Bishop Museum, Honolulu, 27: 1–62, Pls. 1–4. R-154-000-334-112. Edmondson, C. H., 1962. Xanthidae of Hawaii. Occasional Papers of Bernice P. Bishop Museum, Honolulu, Hawaii, 22(13): 215–309. LITERATURE CITED Estampador, E., 1937. A check list of Philippine crustacean decapods. Philippine Journal of Science, 62: 465–559. Ahyong, S. T., 2008. 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Wyville Thomson, Knt., F.R.S. & Regis Professor of MacGilchrist, A. C., 1905. Natural history notes from the R.I.M.S.S. Natural History in the University of Edinburgh of the civilian Investigator. Ser. III, No. 6. An account of the new and some scientifi c staff on board and now of John Murray one of the of the rarer decapod Crustacea obtained during the surveying naturalists of the expedition. Zoology, Published by Order of seasons 1901–1904. Annals and Magazine of Natural History, Her Majesty’s Government. London, Edinburgh and Dublin, 7, 15: 233–268. HMSO. 17: i–l+1–362, Pls. 1–29. MacLeay, W. S., 1838. Illustrations of the Annulosa of South Africa; Milne-Edwards, A., 1867. Descriptions de quelques espèces being a portion of the objects of natural history chiefl y collected nouvelles de Crustacés Brachyures. Annales de la Societé during an expedition into the interior of South Africa, under Entomologique de France, 4e série 7: 263–288. the direction of Dr. Andrew Smith, in the years 1834, 1835, and 1836; fi tted out by the “Cape of Good Hope Association Milne-Edwards, A., 1873. Recherches sur la faune carcinologique de for Exploring Central Africa.” In: Smith, A. (ed.), Illustrations la Nouvelle-Calédonie, Deuxième Partie. Nouvelles Archives du of the zoology of South Africa investigations. London: Smith, Muséum d’Histoire naturelle, Paris, 9: 155–332, Pls. 4–18. Elder and Co., pp. 1–75, Pls. 1–4. Moosa, K., 1981. Crustacés Décapodes: Portunidae. Résultats des Man, J. G. de, 1902. Die von Herrn Professor Kükenthal im indischen Campagnes MUSORSTOM, I – Philippines (18–28 mars 1976), Archipel gesammelten Dekapoden und Stomatopoden. In: W. Tome 1. Collection Mémoires ORSTOM, 91: 141–150. Kükenthal (ed.) Ergebnisse einer zoologischen Forschungsreise

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New or rare species of Brachyura, collected by the simplex (A. Milne-Edwards, 1873) and Metaxanthops acutus Misago during the zoological survey around the Izu Peninsula. Serène, 1984 (Decapoda, Brachyura, Xanthoidea, Xanthidae). Science Reports of the Tokyo Bunrika Daigaku 2(32): 63–88, Crustaceana, 75(3–4): 527–538. Pls. 6–8. Ng, P. K. L., D. Guinot & P. J. F. Davie, 2008. Systema Sakai, T., 1939. Studies on the crabs of Japan. IV. Brachygnatha, Brachyurorum: Part I. An annotated checklist of extant Brachyrhyncha. Yokendo Co., Tokyo. Pp. 365–741, Pls. brachyuran crabs of the world. Raffl es Bulletin of Zoology, 42–111. Supplement No. 17: 1–286. Sakai, T., 1965a. On two new genera and fi ve new species of Ng, P. K. L. & P. H. Ho, 2003. Mathildella rubra, a new species xanthoid crabs from the collection of His Majesty the Emperor of deep-water carcinoplacine crab (Decapoda, Brachyura) from of Japan made in Sagami Bay. Crustaceana, 8(1): 97–106. the Philippines. Crustaceana, 76(3): 333–342. Sakai, T., 1965b. The Crabs of Sagami Bay, collected by His Ng, P. K. L. & L. Liao, 2002. On a new species of Euryozius Majesty the Emperor of Japan. Maruzen Co., Tokyo. i–xvi, Miers, 1886 (Crustacea: Decapoda: Brachyura: Pseudoziidae) 1–206, (English text), Figs. 1–27, Pls. 1–100: 1–92 [Japanese from the Philippines, with notes on the taxonomy of the genus. text]: 1–26 [references and index in English]: 27–32 [index in Proceedings of the Biological Society of Washington, 115(3): Japanese], 1 map. 585–593. Sakai, T., 1976a. Crabs of Japan and the Adjacent Seas. Kodansha Ng, P. K. L. & M. R. Manuel-Santos, 2007. Establishment of the Ltd, Tokyo. [In 3 volumes]: (1) English text: i–xxix, 1–773, Vultocinidae, a new family for an unusual new genus and Figs 1–379, (2) Plates volume: 1–16, Pls 1–251, (3) Japanese new species of Indo-West Pacifi c crab (Crustacea: Decapoda: text: 1–461, Figs 1–2, 3 maps.) Brachyura: Goneplacoidea), with comments on the taxonomy of the Goneplacidae. Zootaxa, 1558: 39–68. Serène, R., 1971. Observations préliminaires sur des brachyoures nouveaux ou mal connus du sud-est Asiatique (Crustacea Ng, P. K. L. & C. L. McLay, 2005. Dicranodromia danielae, a new Decapoda). Bulletin du Muséum national d’Histoire naturelle, species of homolodromiid crab from the Philippines (Crustacea: Paris, 42(5): 903–918, Pls. 1–6. Decapoda: Brachyura). Zootaxa, 1029: 39–46. Serène, R., 1984. Crustacés Décapodes Brachyoures de l’océan Ng, P. K. L., J. C. E. Mendoza & M. R. Manuel-Santos, 2009. Indien occidental et de la mer Rouge. Xanthoidea: Xanthidae Tangle net fi shing, an indigenous method used in Balicasag et Trapeziidae. Avec un addendum par A. Crosnier: Carpilidae Island, central Philippines. Raffl es Bulletin of Zoology, Suppl. et Menippidae. Faune tropicale, 24: 1–400, Pls. 1–48. No. 20: 39–46. Serène, R. & A. F. Umali, 1972. The family Raninidae and other new Ng, P. K. L., C. H. Wang, P. H. Ho & H. T. Shih, 2001. An and rare species of brachyuran decapods from the Philippines annotated checlist of brachyuran crabs from Taiwan (Crustacea: and adjacent regions. Philippine Journal of Science, 99(1–2): Decapoda). National Taiwan Museum Special Publication 21–105, Pls. 1–9. Series, No. 11, 86 p. Serène, R. & C. Vadon, 1981. Crustacés Décapodes: Brachyoures. Rathbun, M. J., 1894. Descriptions of two new species of crabs from Liste préliminaire, description de formes nouvelles et remarques the Western Indian Ocean, presented to the National Museum taxonomiques. Résultats des Campagnes MUSORSTOM, I by Dr. W. L. Abbott. Proceedings of the United States National – Philippines (18–28 mars 1976), Tome 1. Collection Mémoires Museum, 17(979): 21–24. ORSTOM, 91: 117–140, Pls. 1–4. Rathbun, M. J., 1897. A revision of the nomenclature of the Stephensen, K., 1945. The Brachyura of the Iranian Gulf with an Brachyura. Proceedings of the Biological Society of Washington, appendix: the male pleopod of the Brachyura. Danish Scientifi c 11: 153–167. Investigations in Iran, 4: 57–237, Figs. 1–60. Rathbun, M. J., 1906. The Brachyura and Macrura of the Hawaiian Štev i , Z., 2005. The reclassification of brachyuran crabs Islands. Bulletin of the United States Fish Commission, 23(3): (Crustacea: Decapoda: Brachyura). Fauna Croatica, 14(Suppl. 827–930, Pls. 1–24. 1): 1–159.

73 Mendoza & Ng: Euxanthine crabs of the Philippines

Takeda, M., 1972. Further notes on the unrecorded xanthid crabs Tan, C. G. S., 1996. Leucosiidae of the Albatross expedition to from the Ryukyu Islands. Biological Magazine, Okinawa, 9: the Philippines, 1907–1910 (Crustacea: Brachyura: Decapoda). 15–24, Pl. 1. Journal of Natural History, 30(7): 1021–1058. Takeda, M., 1976. Studies on the Crustacea Brachyura of the Palau Ward, M., 1934. Notes on a collection of crabs from Christmas Islands, III. Xanthidae. Researches on Crustacea, Tokyo, 7: Island, Indian Ocean. Bulletin of the Raffl es Museum, Singapore, 69–99. 9: 5–27, Pls. I–III. Takeda, M., 1980. A new xanthid crab from the Ryukyu Islands. Ward, M., 1941. New Brachyura from the Gulf of Davao, Mindanao, Bulletin of the Biogeographical Society of Japan, 35(3): Philippine Islands. American Museum Novitates, 1104: 1–15. 39–44. Ward, M., 1942. Notes on the Crustacea of the Desjardins Museum, Takeda, M., 1989. Shallow-water crabs from the Oshima Passage Mauritius Institute, with descriptions of new genera and species. between Amami-Oshima and Kakeroma-jima Islands, the Bulletin of the Mauritius Institute, Port Louis, 2(2): 49–113, Northern Ryukyu Islands. Memoirs of the National Science Pls. 5–6. Museum, (22): 135–184, Pl. 4. White, A., 1847. List of the specimens of Crustacea in the collection Takeda, M. and M. R. Manuel, 2000. Taxonomic accounts of some of the British Museum. London, i–viii + 1–143 pp. rare crabs new to the Philippines. National Science Museum Yokoya, Y., 1933. On the distribution of decapod crustaceans Monographs, 18: 149–162. inhabiting the continental shelf around Japan, chiefl y based Takeda, M. & M. R. Manuel-Santos, 2007. Crabs from Balicasag upon the materials collected by S.S. Sôyô-Maru, during the Island, Bohol, the Philippines: Dromiidae, Dynomenidae, years 1923–1930. Journal of the College of Agriculture, Tokyo Homolidae, Raninidae, Dorrippidae and Calappidae. Memoirs Imperial University, 12(1): 1–226. of the National Science Museum, Tokyo, 44: 83–104 (published 2007). Takeda, M. & R. Weber, 2006. Crabs from the Kermadec Islands in the South Pacifi c. In: Y. Tomida (ed.), Proceedings of the 7th and 8th Symposia on Collection Building and Natural History Studies in Asia and the Pacifi c Rim. National Science Museum Monographs, 34: 191–237.

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THE RAFFLES BULLETIN OF ZOOLOGY 2010 58(1): 75–78 Date of Publication: 28 Feb.2010 © National University of Singapore

ON THE MALE OF APHANODACTYLUS LOIMIAE KONISHI & NODA, 1999 (CRUSTACEA: BRACHYURA: PINNOTHEROIDEA: APHANODACTYLIDAE)

Peter K. L. Ng Department of Biological Sciences, National University of Singapore, Kent Ridge, Singapore 119260, Republic of Singapore Email: [email protected]

Shane T. Ahyong Marine Biodiversity and Biosecurity, National Institute of Water and Atmospheric Research, Private Bag 14901, Kilbirnie, Wellington, New Zealand Email: [email protected]

Tomoyuki Komai Natural History Museum and Institute, Chiba 955-2 Aoba-cho, Chuo-ku, Chiba 260-8682, Japan. Email: [email protected]

ABSTRACT. – The pinnotheroid genus Aphanodactylus currently includes four species, of which A. loimiae Konishi & Noda, 1999, was described from Kuroshima Island, Yaeyama Islands, Japan, based on a single ovigerous female. Here, we report the ﬁ rst known male specimen of A. loimiae. Characters used by Konishi & Noda (1999) to distinguish species of Aphanodactylus are reevaluated and additional distinguishing features are recognized.

KEY WORDS. – Brachyura, Pinnotheridae, Aphanodactylus loimiae, sexual dimorphism, Japan.

INTRODUCTION Collection (ZRC) of the Raffl es Museum of Biodiversity Research, National University of Singapore. Carapace Four species of the pinnotheroid crab genus, Aphanodactylus width and length are abbreviated as cw and cl, respectively. Tesch, 1918, are currently known (see Ng et al., 2008): A. Morphological terminology follows Ahyong & Ng (2007, sibogae Tesch, 1918 (type species; type locality: Indonesia), 2009). The walking legs, i.e., pereopods 2–5, respectively, A. brevipes (A. Milne-Edwards, 1853) (type locality: are abbreviated as P2–5. Mayotte), A. edmondsoni Rathbun, 1932 (type locality: Hawaii), and A. loimiae Konishi & Noda, 1999 (type locality: Japan). Ahyong & Ng (2009) recently referred them to a new TAXONOMY family, Aphanodactylidae. All species are from the Indo- Pacifi c and, where known, are commensal with polychaete Pinnotheridae De Haan, 1833 worms of the genus Loimia (Terebellidae). Only one species is known from Japan, Aphanodactylus loimiae Konishi & Aphanodactylus loimiae Konishi & Noda, 1999 Noda, 1999, described from an ovigerous female collected from Yaeyama Islands, Ryukyu Islands. Aphanodactylus loimiae Konishi & Noda, 1999: 223–227, Figs. 1, 2 [type locality: Kuroshima Island, Yaeyama Islands, Japan, in tube of Loimia ingens Grube, 1878 (Polychaeta)]; Ng et In 1995 and 1999, the third author obtained additional al., 2008: 247 (list); Ng & Naruse, 2009: 284; Ahyong & Ng, specimens of A. loimiae from the Ryukyu Islands, including 2009: 36, Figs. 1, 2. the fi rst known male, collected by his colleague K. Nomura of the Kushimoto Marine Park, Japan. All three specimens Material examined. – 1 male (10.3 × 7.4 mm), 1 ovigerous female are clearly referable to A. loimiae. The male of the species (13.9 × 8.6 mm) (CBM 5341), Kyan, Kuroshima Island, Yaeyama is reported for the fi rst time and aspects of its taxonomy are Islands, Ryukyus, Japan, 10 m deep, coral reef, in tube of Loimia ingens discussed. Specimens are deposited in the Natural History , 10 Oct. 1999, coll. K. Nomura on SCUBA; 1 ovigerous female (15.3 × 9.1 mm) (CBM 5443), Ahra Beach, Kume-jima Museum, Chiba (CBM), Japan; The Naturalis, Nationaal Island, Okinawa Islands, Ryukyus, Japan, 10 m deep, coral reef, Natuurhistorisch Museum (ex Rijksmuseum van Natuurlijke inhabited in tube of Loimia ingens, 15 Jun. 1995, coll. K. Nomura Historie, RMNH), Leiden; and Zoological Reference on SCUBA.

75 Ng et al.: A record of male Aphanodactylus loimiae

Comparative specimens of Aphanodactylus edmondsoni. – 1 male also in A. sibogae, based on Tesch’s (1918) lack of comment (11.5 × 8.2 mm), 1 female (16.9 × 10.2 mm) (ZRC 2000.0542), on sternal differences. Thus, the unusual corneal shape and Oahu, Hawaii, coll. C. H. Edmondson. deep sternal grooves will immediately distinguish A. loimiae from A. edmondsoni and A. sibogae. Remarks. – Discovery of a male specimen of Aphanodactylus loimiae permits documentation of sexual dimorphism in this Availability of additional females of A. loimiae also permits species. As in other species of Aphanodactylus, the carapace documentation of intraspecific variation. The carapace of A. loimiae is proportionally narrower in the male than width to length ratio of the present females is 1.62–1.68, females (width: length ratio 1.39 versus 1.62–1.76); the which is slightly lower than that recorded for the holotype front is more distinctly concave medially; the male chelipeds (1.76), and the frontal margin is slightly sinuous rather than are more robust than in females; and the male abdomen is straight as recorded by Konishi & Noda (1999). All three narrowly triangular and tapering to a rounded apex. Perhaps specimens examined in this study also differ from the type the most signiﬁ cant differences between male and female description of A. loimiae in the ventral armature of the meri A. loimiae, however, are in the shape of the cornea and of the walking legs. Konishi & Noda (1999) recorded 4–6 thoracic sternal structures. The cornea of female A. loimiae ventral teeth on the posterior margins of the meri of P2–4 is a simple oval shape in anterior view, but in males, the and one prominent tooth and two vestigial ventral teeth cornea is strongly constricted medially, forming a distal bulb. on the posterior margins of the merus of P5. The present As far as is known for Aphanodactylus species, this corneal specimens bear 3–5 ventral teeth on the posterior margins of dimorphism is unique to A. loimiae, being neither present in A. the meri of P2–4, none of which are prominently enlarged, edmondsoni nor A. sibogae (based on Tesch [1918]). Thoracic and no ventral teeth on the merus of P5. These variations sternites 5–7 of male A. loimiae are separated by deep, wide in the ambulatory meral armature are presently interpreted grooves, whereas in females, the sternites are demarcated by as intraspeciﬁ c variation. narrow, shallow grooves. As with the corneal dimorphism, the sternal dimorphism in A. loimiae is apparently unique Features used by Konishi & Noda (1999) to distinguish in the genus. This sternal differentiation is similar in both species of Aphanodactylus were the width to length ratio sexes in A. edmondsoni (present observation), and presumably of the carapace, dorsal punctuation of the carapace, shape

Fig. 1. Aphanodactylus loimiae Konishi & Noda, 1999 (CBM 5341). A, C, dorsal views. B, D, ventral views. A, B, male (10.3 × 7.4 mm); C, D, female (13.9 × 8.6 mm).

76 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. Comparison of selected morphological features of both sexes of A. loimiae, A. edmondsoni and A. sibogae. Based on Tesch (1918) Edmondson (1946, 1962), Konishi & Noda (1999) and specimens examined herein.

Male A. loimiae A. edmondsoni A. sibogae cw:cl 1.39 1.40 1.47 Merus P2–4 ventral teeth 4–6 1–3 4 Merus P5 ventral teeth 0 1 0 Sternal grooves wide, deep shallow, narrow shallow, narrow

Female A. loimiae A. edmondsoni A. sibogae cw:cl 1.62–1.76 1.65–1.69 1.62–1.88 Merus P2–4 ventral teeth 4–6 1–3 ? Merus P5 ventral teeth 0–1 + 2 small vestigial 2 1 Sternal grooves shallow, narrow shallow, narrow shallow, narrow

of the frontal margin (straight or concave), the number of males, and overlap in females (Table 1). The shape of the antennular segments, and the ventral armature of the meri carapace front, presence or absence of dorsal pits on the of P2–5. Most of the characters used by Konishi & Noda carapace, and antennular segmentation appear to be similar (1999) to distinguish species of Aphanodactylus are invalid, in A. loimiae, A. edmondsoni and A. sibogae. The front is though other features are available for species identiﬁ cation. slightly sinuous in females and distinctly sinuous in males The width to length ratios of the carapace of A. loimiae, of all three species. Similarly, the presence of dorsal pits on A. edmondsoni and A. sibogae are similar to each other in the carapace, cited as diagnostic of A. sibogae by Konishi

Fig. 2. Aphanodactylus loimiae Konishi & Noda, 1999, male (10.3 × 7.4 mm) (CBM 5341). A, left anterior of carapace; B, right P5; C, abdomen; D, E, left G1, abdominal and sternal view, respectively. Scales: A–B = 1.5 mm, C = 3.0 mm, D–E = 1.0 mm.

77 Ng et al.: A record of male Aphanodactylus loimiae

& Noda (1999) appears to be unreliable — both A. loimiae REFERENCES and A. edmondsoni have similar, pits, but were probably overlooked in the original accounts because the pits are Ahyong, S. T., & P. K. L. Ng. 2007. The pinnotherid type material not very deep and can be diffi cult to observe unless the of Semper (1880), Nauck (1880) and Bürger (1895) (Crustacea: carapace surface is dried. The carapace pits of A. sibogae, Decapoda: Brachyura). Raffl es Bulletin of Zoology, Supplement as depicted by Tesch (1918), are deeper and more prominent No. 16: 191 -226. than they actually are. A female syntype of A. sibogae Ahyong, S. T. & P. K. L. Ng, 2009. Aphanodactylidae, a new (RMNH D2162, cw. 8.8 mm, cl. 5.4 mm) in the Nationaal family of thoracotreme crabs (Crustacea: Brachyura) symbiotic Natuurhistorisch Museum, Leiden, examined by T. Naruse with polychaete worms. Zootaxa, 2289: 33 -47. (National University of Singapore) at our request has very Cases, E. & V. Storch, 1981. Decapods associated with invertebrates shallow carapace pits, as presently observed in A. loimiae from Cebu. Philippine Scientist, 18: 15 -26. and A. edmondsoni. The antennular fl agellum in all three Edmondson, C. H., 1946. Reef and shore fauna of Hawaii. species appears to number about seven segments. Tesch Occasional Papers of Bernice P. Bishop Museum, Special (1918) cited three segments for female and seven for male Publication 22: 1–381. A. sibogae, but, the low female number is likely to be the Edmondson, C. H., 1962. Hawaiian Crustacea: Goneplacidae, result of damage. The differences in meral armature of P2–4 Pinnotheridae, Cymopolidae, Ocypodidae, and Gecarcinidae. appears to be a useful distinguishing feature, at least for A. Occasional Papers of Bernice P. Bishop Museum, 23(1): edmondsoni (1–3 teeth) and A. loimiae (4–6 teeth). 1–27. Haan, H. M. De, 1833–1849. Crustacea. In: P. F. von Siebold, Cases & Storch (1981) reported A. sibogae from Poro, Fauna Japonica, sive Descriptio animalium, quae in itinere Camotes Islands, Cebu, Philippines. Although the size and per Japoniam, jussu et auspiciis superiorum, qui summum in sex of the Cebu specimen was not specifi cally stated, it India Batavia imperium tenent, suscepto, annis 1823–1830 collegit, notis, observationibus a adumbrationibus illustravit. appears to be a male with carapace proportions (width: length Lugduni Batavorum, fasc. 1–8: I–xxi+vii–xvii+ix–xvi+1–243, ratio 1.45) similar to that of male A. sibogae reported by Pls. 1–55, A–Q, Circ., Pl. 2. Tesch (1918). Notably, Cases & Storch (1918: Fig. 9) did not show dorsal carapace pits, suggesting that if present, the Konishi, K. & H. Noda, 1999. A new species of commensal crab genus Aphanodactylus (Crustacea: Brachyura: Pinnotheridae) dorsal pits were probably shallow and therefore overlooked. from the Yaeyama Islands, southern Japan. Publications of the The identity of the Philippines specimen will need to be Seto Marine Biological Laboratory, 38(5/6): 223–229. checked to see if they are really A. sibogae or perhaps even Milne Edwards, H., 1853. Mémoire sur la famille des Ocypodiens. A. loimiae. Attempts to locate the specimen(s), supposedly Suite, Annales des Sciences Naturelles, Zoologie et Biologie in the zoological museum of the University of San Carlos, Animale, 20(3): 163–228, Pls. 6–11. Cebu City, Philippines, were unsuccessful. The material Ng, P. K. L., D. Guinot & P. J. F. Davie, 2008. Systema appears to be lost. Brachyurorum: Part I. An annotated checklist of extant brachyuran crabs of the world. Raffl es Bulletin of Zoology, The present specimens of A. loimiae were all found to inhabit Supplement No. 17: 1 -286. the tubes of a large polychaete, Loimia ingens, as with the Ng, P. K. L. & T. Naruse, 2009. On the identity of Pinnixa brevipes holotype (see Konishi & Noda, 1999). The heterosexual H. Milne Edwards, 1853, and a new species of Aphanodactylus pair (CBM-ZC 5341) was collected from the same tube (K. Tesch, 1918 (Crustacea: Decapoda: Brachyura: Pinnotheroidea) Nomura, pers. comm.). It is still unclear if Aphanodactylus from the Philippines. Raffl es Bulletin of Zoology, Supplement loimiae is only found with Loimia ingens. 20: 283 -290. Rathbun, M. J., 1932. A new pinnotherid crab from the Hawaiian Islands. Journal of the Washington Academy of Sciences, 22: ACKNOWLEDGEMENTS 181 -182. Tesch, J. J., 1918. Decapoda Brachyura II. Goneplacidae and Special thanks are extended to Keiichi Nomura, the collector Pinnotheridae. Siboga Expeditie Monographie, 39c1: 149–295, of the specimens of A. loimiae studied here. Tohru Naruse Pls. 7–18. is gratefully acknowledged for checking the syntype of Aphanodactylus sibogae in RMNH. Support to the first author from Research Fellowships from the Raffl es Museum Note added in proof: This paper was supposed to have been of Biodiversity Research, National University of Singapore, published in a supplementary volume of the Raffl es Bulletin in Biosecurity New Zealand (contract ZBS 200524) and the 2008. As this supplement was badly delayed for a variety of Foundation for Research, Science and Technology (BBBI063) reasons, this paper is published only now; and as such, some is gratefully acknowledged. of the ideas contained here have since been supplemented by Ng & Naruse (2009) and Ahyong & Ng (2009).

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THE RAFFLES BULLETIN OF ZOOLOGY 2010 58(1): 79–85 Date of Publication: 28 Feb.2010 © National University of Singapore

A NEW SPECIES OF CHAERILUS SIMON, 1877 (SCORPIONES, CHAERILIDAE) FROM THAILAND

Wilson R. Lourenço Muséum national d’Histoire naturelle, Département de Systématique et Evolution, Section Arthropodes (Arachnologie), CP 053, 57 rue Cuvier 75005 Paris, France E-mail: [email protected]

Dong Sun College of Life Science, Hebei University, Baoding, Hebei Province, 071002, P. R. China E-mail: [email protected]

Mingsheng Zhu College of Life Science, Hebei University, Baoding, Hebei Province, 071002, P. R. China E-mail: [email protected]

ABSTRACT. – A new species belonging to the genus Chaerilus Simon, 1877, Chaerilus thai, new species, is described from an evergreen rain forest in Bala-Hala Wildlife Sanctuary in the South of Thailand. For comparative purposes a precise diagnosis is again proposed for Chaerilus celebensis Pocock, 1894, originally described from Luwu Celebes Islands (Sulawesi). This species was recently redescribed by Lourenço & Ythier (2008) and proved to be the subject of subsequent misidentiﬁ cations.

KEY WORDS. – Scorpion, Chaerilidae, Chaerilus, new species, Thailand.

INTRODUCTION MATERIALS AND METHODS

In recent publications several historical aspects, but also other Specimens were examined and measured under a Wild M5 insights concerning the taxonomy of the genus Chaerilus stereomicroscope with an ocular micrometer. Illustrations Simon, 1877 were the subject of discussion (Qi et al., 2005; were produced using a Leica M165c stereomicroscope with Lourenço, 2008; Lourenço & Ythier, 2008; Lourenço & Zhu, a drawing tube. All measurements follow Stahnke (1970) 2008; Zhu et al., 2008). These studies clearly suggest that and are given in millimetres (mm). Trichobothrial notations publications done in absence of the necessary background, follow Vachon (1974) and morphological terminology mostly such as the revision by Kova ík (2000), remain unsatisfactory. follows Hjelle (1990). Specimens used in this taxonomic Presently, other studies concerning obscure or poorly work come from the Muséum national d’Histoire naturelle, Paris (MNHN), Natural History Museum, London (BMNH), characterized species of this genus are in preparation by Zoologisches Museum, Hamburg (ZMUH) and Museum of the senior author. One good example, already discussed by Hebei University, Baoding (MHBU). Lourenço & Ythier (2008) and Lourenço & Zhu (2008), is the one represented by Chaerilus celebensis Pocock, 1894. This species, originally described from Luwu, Celebes (Sulawesi) TAXONOMY Island, was the subject of several misidentiﬁ cations; see for example the description of Chaerilus petrzelkai Kova ík, Chaerilidae Pocock, 1893 2000 from the South of Vietnam (Kova ík, 2000, Lourenço & Zhu, 2008). For this reason, Lourenço & Ythier (2008) Chaerilus Simon, 1877 recently proposed a redescription of this species, based on freshly collected material in Luwu, Celebes (Sulawesi) Island. Chaerilus celebensis Pocock, 1894 In this contribution we propose again a precise diagnosis (Figs. 1, 2, 5B,D; Table 1) for C. celebensis, followed by some previously unpublished illustrations of this species. Moreover, one new species is Chaerilus celebensis Pocock, 1894: 93; Kraepelin, 1899: 158; described from an evergreen rain forest in Bala-Hala Wildlife Kraepelin, 1913: 145; Fage, 1946: 72 (misidentiﬁ cation); Takashima, Sanctuary in the South of Thailand. 1945: 99; Kova ík, 2000: 43; Lourenço & Ythier, 2008: 27.

79 Lourenço et al.: a new species of Chaerilus from Thailand

Table 1. Morphometric values (in mm) of Chaerilus celebensis, female from Malino, Luwu, Celebes (MNHN) and Chaerilus thai, new species, female holotype (MHBU).

Morphometric Parameters Chaerilus celebensis (Female) Chaerilus thai (Female)

Total length 25.8 15.8 Carapace: – length 4.2 2.8 – anterior width 2.3 1.6 – posterior width 4.3 2.9 Metasomal segment I: – length 1.5 0.9 – width 2.2 1.3 Metasomal segment II: – length 1.8 1.0 – width 1.8 1.2 Metasomal segment III: – length 1.9 1.1 – width 1.7 1.1 Metasomal segment IV: – length 2.0 1.3 – width 1.5 1.1 Metasomal segment V: – length 3.4 2.1 – width 1.5 1.0 – depth 1.3 0.9 Vesicle: – width 1.6 1.3 – depth 1.4 1.1 Pedipalp: – Femur length 3.8 2.1 – Femur width 1.6 1.0 – Patella length 4.1 2.4 – Patella width 1.9 1.1 – Chela length 7.8 4.5 – Chela width 2.6 1.5 – Chela depth 2.4 1.6 Movable ﬁ nger: – length 3.8 2.2

Material examined. – 1 female-juvenile holotype (BMNH- Coloration. – Basically reddish-yellow to yellowish-brown. 1896.10.6.5.), Indonesia, Luwu, Celebes (Sulawesi) Island, coll. M. Carapace reddish to reddish-brown, with two posterior spots Weber, 6 Jun.1896; 1 female (ZMUH), Indonesia, Luwu, Celebes on posterior edge; tergites yellowish, intensely marked with (Sulawesi) Island, Sadara-Spitze, coll. Sarasin, 4 Mar.1897; 1 brownish confl uent spots. Metasoma: All segments yellowish female (MNHN), Indonesia, Luwu, Celebes (Sulawesi) Island, with variegated brownish spots; dorsal surface of segments Malino, slopes of the Lompobatang, 1500 m alt., coll. P. Leclerc, 6 Jul.1986; 1 male-juvenile (MHNH), Indonesia, Luwu, Celebes not spotted; carinae dark reddish-brown. Telson yellowish (Sulawesi) Island, Tacipi-Lampo, Bone, coll. P. Leclerc, 17 Jul.1986; with diffused brownish spots; aculeus reddish. Chelicerae 1 female-juvenile (MHBU), Indonesia, Luwu, Celebes (Sulawesi) yellowish with rather diffused variegated spots; fi ngers with Island, Tacipi-Lampo, Bone, coll. P. Leclerc, 15 Jul.1986. reddish teeth. Pedipalps: reddish to reddish-brown with some diffused brownish spots; carinae blackish-brown; chela Diagnosis. – Species with small to moderate size in relation fi ngers very dark. Legs yellowish with diffused brownish to the other species of the genus with 22 to 26 mm in total variegated spots. Venter and sternites yellowish; with the length. exception of the pectines, all other structures are marked with rather diffused brownish spots (note: coloration is extensively

80 THE RAFFLES BULLETIN OF ZOOLOGY 2010 described because of the diagnostic importance of this Distribution. – C. celebensis has been cited from different character in relation to closely related species).Morphology: locations, including some outside Indonesia. These Carapace with the anterior margin weakly concave; carinae correspond, however, to misidentifi cations, and this species weakly marked; moderately granular in males, more densely can only be confi rmed up to know from Celebes (Sulawesi) granular in females; furrows moderately to weakly deep. Island. Metasomal carinae moderately to strongly granular; ventral carinae absent from segment I. Dentate margins of fi xed and movable fi ngers of pedipalp chela with 6-7 rows of granules, Chaerilus thai, new species not well delimited. Pectinal tooth count 3-4 in males, 3 in (Figs. 3, 4, 5A, C, E; Table 1) females. Genital operculum plates have a sub-oval shape. Trichobothriotaxy of type B, orthobothriotaxic. Material examined. – Holotype: female (MHBU), Thailand, Narathiwat Province, Waeng District, Bala-Hala Wildlife Sanctuary (250 m alt., evergreen rain forest), coll. D. Huber, 8 Jun.1998.

Paratypes. – No paratypes.

Diagnosis. – New species of small size compared to the other species of the genus, with a total length of 15.8 mm. Carapace with the anterior margin straight, almost acarinate and weakly granulated to smooth; furrows shallow. Metasomal carinae moderately marked; ventral carinae vestigial on segments I and II, weakly marked on segment III. Dentate margins of ﬁ xed and movable ﬁ ngers of pedipalp chela with 6 rows of granules, not well delimited. Pectinal tooth count 4-4 in female. Genital operculum plates have a sub-oval shape. Trichobothriotaxy of Type B, orthobothriotaxic.

Relationships. – By its general morphology and the pattern of pigmentation, Chaerilus thai, new species, can be associated with Chaerilus celebensis Pocock. The new species can, however, be distinguished by the following features: (i) a smaller total size and distinct morphometric values (see Table 1), (ii) a carapace very weakly granulated to smooth, (iii) an overall darker pigmentation than that of C. celebensis; are particularly marked the dorsal surface of metasomal segments I to IV, pedipalps, chelicerae and ventral aspect, including pectines.

Description. – Female (holotype).

Coloration: Basically yellowish, with a dark variegated pigmentation on body and appendages. Carapace yellowish, strongly marked with blackish pigmentation, in particular on the anterior half. Tergites with the same colour and pigmentation of the carapace. Metasoma: All segments yellowish with dark variegated pigmentation; dorsal surface of segments I-IV with dark square-shaped spots; carinae not darker than the tegument. Telson yellowish with diffused brownish spots; aculeus yellowish at the base and reddish at the extremity. Chelicerae yellowish intensely marked with variegated spots; ﬁ ngers with reddish teeth. Pedipalps: yellowish with dark variegated pigmentation; femur and patella with dark brown spots, better marked on femur; chela ﬁ ngers much darker than chela hand. Legs yellowish intensely marked with brownish spots. Venter and sternites brownish-yellow; all the structures are marked with brownish spots, including pectines.

Morphology: Carapace with anterior margin straight, almost Fig. 1. Chaerilus celebensis Pocock, 1894. Female (MHBU). acarinate and very weakly granular to smooth; furrows Habitus. Scale bar = 1.0mm.

81 Lourenço et al.: a new species of Chaerilus from Thailand

Fig. 2. Chaerilus celebensis Pocock, 1894. Female (MHBU). A–C: Chela, dorso-external (A), ventral (B) and internal (C) view; D, E: Chelicera, ventral (D) and dorsal (E) view; F–H: Patella, dorsal (F), ventral (G) and external (H) view; I, J: Femur, dorsal (I) and external (J) view. Scale bars = 1.0mm.

82 THE RAFFLES BULLETIN OF ZOOLOGY 2010 shallow. Two pairs of lateral eyes; median eyes moderate, pedal spurs moderately developed. Tarsi with two rows of about twice the size of lateral eyes; median eyes anterior to thin setae. the centre of the carapace. Tergites with only very minute granulation; carinae obsolete. Sternum pentagonal, longer Etymology. – The specifi c name makes reference to Thailand, than wide; genital operculum plates with a sub-oval shape. the country where the new species was collected. Pectinal tooth count 4-4 in female holotype. Sternites smooth with spiracles small and round; carinae absent from VII. Distribution. – Narathiwat Province, Thailand (present Metasoma: Segments I and II wider than long; III as long as study). Chaerilus thai new species, is the fi rst record properly wide; IV and V longer than wide. All the carinae moderately documented of the presence of this genus in Thailand. granular; ventral carinae vestigial on segments I and II, Kova ík (2000) indicated, as a new record, the presence weakly marked on segment III; segment V with fi ve carinae of Chaerilus cavernicola Pocock from Trang Thailand. and spinoid granules on ventral surface. Vesicle smooth, This species, however, was described from Caves Ngalau with a short aculeus. Pedipalps: Femur with fi ve carinae; near Pajacombo in Sumatra, and its presence in Thailand is dorsal internal and dorsal external moderately granular; doubtful. Moreover, this last species has no possible affi nities ventral internal weakly granular; ventral external vestigial. with the new species. Patella with fi ve to six carinae; dorsal and ventral weakly granular to smooth. Chela with seven to eight carinae, all weakly granular; ventral median carinae weak. Tegument ACKNOWLEDGMENTS with very few granulations almost smooth. Finger almost as long as manus with 6 rows of granules on the dentate We are most grateful to Dr. Janet Beccaloni, Natural History margins, not well delimited. Chelicerae characteristic of Museum, London, for the loan of the type specimen of the family Chaerilidae (Vachon, 1963). Trichobothriotaxy Chaerilus celebensis and to Dr. Hieronymus Dastych, of type B; orthobothriotaxic (Vachon, 1974); femur with 9 Zoologisches Museum, Hamburg, for the loan of specimens trichobothria, patella with 14, and chela with 14. Legs with of Chaerilus celebensis. This work was supported by grants from the National Natural Science Foundation of China (NSFC-30670254) and the Doctor Program Foundation of Chinese Ministry of Education, China (20050075002) to Ming-Sheng Zhu.

LITERATURE CITED

Fage, L. 1946 [1944]. Scorpions et Pédipalpes de l’Indochine française. Annales de la Société entomologique de France, 113: 71–80. Hjelle, J. T. 1990. Anatomy and morphology. In: Polis, G. A. (ed.), The Biology of Scorpions. Stanford Univ. Press, Stanford. Pp. 9–63. Kova ík, F. 2000. Revision of family Chaerilidae (Scorpiones), with description of three new species. Serket, 7 (2): 38–77. Kraepelin, K. 1899. Scorpiones und Pedipalpi. In: F. Dahl (ed.). Das Tierreich. Herausgegeben von der Deutschen zoologischen Gesellschaft. 8(Arachnoidea). Verlag von R. Friedländer und Sohn, Berlin. Pp. 1–265. Kraepelin, K. 1913. Neue Beiträge zur Systematik der Gliederspinnen. III. A. Bemerkungen zur Skorpionenfauna Indiens. B. Die Skorpione, Pedipalpen und Solifugen Deutsch-Ost-Afrikas. Mitteilungen aus dem Naturhistorischen Museum (2. Beiheft zum Jahrbuch der Hamburgischen wissenschaftlichen Anstalten, 1912), 30: 123–196. Lourenço, W. R. 2008. Description du mâle de Chaerilus agilis Pocock, 1899 (Scorpiones, Chaerilidae). Boletin de la Sociedad Entomológica Aragonesa, 42: 139–142. Lourenço, W. R. & E. Ythier 2008. A new species of Chaerilus Simon, 1877 (Scorpiones, Chaerilidae) from the Philippines. Boletin de la Sociedad Entomológica Aragonesa, 42: 27–31. Lourenço, W. R. & M. S. Zhu 2008. Description of two new species of the genus Chaerilus Simon, 1877 (Scorpiones, Chaerilidae) from Laos and Vietnam. Acta Zootaxonomica Sinica, 33(3): Fig. 3. Chaerilus thai, new species. Female holotype (MHBU). 462–474. Habitus. Scale bar = 1.0mm.

83 Lourenço et al.: a new species of Chaerilus from Thailand

Fig. 4. Chaerilus thai, new species. Female holotype (MHBU). A–C: Chela, dorso-external (A), ventral (B) and internal (C) view; D, E: Chelicera, ventral (D) and dorsal (E) view; F–H: Patella, dorsal (F), ventral (G) and external (H) view; I, J: Femur, dorsal (I) and external (J) view. Scale bars = 1.0mm.

84 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Pocock, R. I. 1894. Scorpions from the Malay Archipelago. Vachon, M. 1963. De l’utilité, en systématique, d’une nomenclature In: Weber, M. (ed.). Zoologische Ergebnisse einer Reise in des dents des chélicères chez les Scorpions. Bulletin du Muséum niederländisch Ost-Indien. Verlag von E. J. Brill, Leiden, 3. national d’Histoire naturelle, Paris, (2) 35, 161–166. Pp. 84–99. Vachon, M. 1974. Etude des caractères utilisés pour classer Qi, J. X., M. S. Zhu & W. R. Lourenço 2005. Eight new species les familles et les genres de Scorpions (Arachnides). 1. La of the genera Scorpiops Peters, Euscorpiops Vachon, and trichobothriotaxie en arachnologie. Sigles trichobothriaux et Chaerilus Simon (Scorpiones: Euscorpiidae, Chaerilidae) from types de trichobothriotaxie chez les Scorpions. Bulletin du Tibet and Yunnan, China. Euscorpius, 32: 1–40.Stahnke, H. L. Muséum national d’Histoire naturelle, Paris, 140: 857–958. 1970. Scorpion nomenclature and mensuration. Entomological Zhu, M. S., G. X. Han & W. R. Lourenço. 2008. The Chaerilid News 81: 297-316. scorpions of China (Scorpiones: Chaerilidae). Zootaxa, 1943: Takashima, H. 1945. Scorpions of Eastern Asia. Acta Arachnologica, 37–52. 9(3–4): 68–106.

Fig. 5. A, C, E, Chaerilus thai, new species. Female holotype (MHBU); B, D, Chaerilus celebensis Pocock, 1894. Female (MHBU); A, B, Ventral view showing the pigmentation of coxapophyses, sternum, genital operculum and pectines; C–D, Metasomal segment V and telson, lateral view; E, Metasomal segment I–V and telson, dorsal view. Scale bars = 1.0mm.

THE RAFFLES BULLETIN OF ZOOLOGY 2010

THE RAFFLES BULLETIN OF ZOOLOGY 2010 58(1): 87Ð91 Date of Publication: 28 Feb.2010 © National University of Singapore

PSEUDOMYSTUS FUNEBRIS, A NEW SPECIES OF CATFISH FROM BORNEO (TELEOSTEI: BAGRIDAE)

Heok Hee Ng Rafﬂ es Museum of Biodiversity Research, Department of Biological Sciences, National University of Singapore, 6 Science Drive 2, #03-01, Singapore 117546, Republic of Singapore Email: [email protected]

ABSTRACT. – Pseudomystus funebris, a new species of bagrid catfi sh is described from blackwater habitats in southern Borneo. The new species can be distinguished from congeners except for P. heokhuii by its unique colour pattern of a pale midlateral stripe and pale oblique bands on the sides of the body. It is distinguished from P. heokhuii in having a shorter adipose-fi n base (14.2Ð17.7% SL vs. 18.2Ð22.8), more slender caudal peduncle (7.3Ð8.9% SL vs. 8.8Ð10.5), wider head (24.4Ð26.2% SL vs. 21.7Ð23.8) and larger eye (11.2–14.7% HL vs. 8.5–10.7) and a slightly convex (vs. evenly sloping) predorsal profi le.

KEY WORDS. – Siluriformes, Rungan, Kahayan, peat swamps, Kalimantan Tengah.

INTRODUCTION number of specimens with that particular count. Institutional abbreviations follow Ferraris (2007). Members of the bagrid genus Pseudomystus Jayaram, 1968, are commonly known as bumblebee catfi shes due to a recurring colour pattern of contrasting vertical bars or Pseudomystus funebris new species blotches. There are currently 19 valid species of these small- (Figs. 1, 2a, 4a) to mid-sized freshwater catfi shes endemic to Southeast Asia (Lim & Ng, 2008). Material examined. – Holotype: MZB 17181, 41.8 mm SL, Borneo: Kalimantan Tengah, Rungan River drainage in the vicinity of Recently, I was given the opportunity to examine Tangkiling, 2¡1'S 113¡44'E, coll. P. Yap, 22 Oct. 2007. Pseudomystus from the Rungan River drainage in southern Paratypes: MZB 17182, 11 ex., 30.7Ð37.7 mm SL; UMMZ 248771, Borneo collected for the aquarium trade. These specimens 12 ex., 28.6Ð50.0 mm SL, locality as for holotype, P. Yap, 3 Dec. had been collected from blackwater habitats, and were 2007. ZRC 51845, 13 ex., 30.8Ð40.6 mm SL; data as for holotype; initially identifi ed as P. heokhuii (the only species known ZRC 51846, 4 ex., mm SL; locality as for holotype, coll. P. Yap, from such habitats to date). Closer examination revealed 21 Jan. 2009. enough differences to justify the recognition of the Bornean material as belonging to a distinct, unnamed species. The Diagnosis. – Pseudomystus funebris can be distinguished from description of this material as Pseudomystus funebris new congeners except for P. heokhuii (from Sumatra) in having a species forms the basis of this study. colour pattern consisting of a pale midlateral stripe and two pale oblique bands on the sides of the body. It differs from P. heokhuii in having a shorter adipose-fi n base (14.2Ð17.7% MATERIALS AND METHODS SL vs. 18.2Ð22.8), more slender caudal peduncle (7.3Ð8.9% SL vs. 8.8Ð10.5), wider head (24.4Ð26.2% SL vs. 21.7Ð23.8) Measurements were made point to point with a pair of and larger eye (11.2Ð14.7% HL vs. 8.5Ð10.7) and a slightly dial calipers and data recorded to tenths of a millimeter. convex (vs. evenly sloping or slightly concave) predorsal Counts and measurements were made on the left side of profi le (Fig. 2). Additional characters for distinguishing P. specimens whenever possible. Subunits of the head are funebris from congeners are mentioned in the Discussion. presented as proportions of head length (HL). Head length and measurements of body parts are given as proportions Description. – Biometric data as in Table 1. Head depressed; of standard length (SL). Measurements follow those of Ng dorsal profi le slightly convex and ventral profi le almost & Kottelat (1998). Asterisks after meristic counts indicate straight; snout acutely rounded or truncate when viewed values for holotype and numbers in parentheses indicate the dorsally. Bony elements of dorsal surface of head covered

87 Ng: New Pseudomystus from Borneo

Table 1. Biometric data for Pseudomystus funebris (n=20).

Parameter Holotype Range Mean ± SD %SL Predorsal length 38.8 38.3Ð42.5 39.8 ± 1.25 Preanal length 69.1 64.6Ð70.7 67.6 ± 1.92 Prepelvic length 53.6 52.5Ð54.6 53.3 ± 0.71 Prepectoral length 26.1 23.1Ð26.1 24.7 ± 0.99 Length of dorsal-fi n base 14.8 12.5Ð15.3 13.8 ± 0.86 Dorsal-spine length 18.4 15.7Ð19.8 17.6 ± 1.18 Anal-fi n length 16.0 14.4Ð16.9 15.6 ± 0.82 Pelvic-fi n length 12.9 12.9Ð15.6 14.4 ± 0.89 Pectoral-fi n length 24.2 20.7Ð25.5 23.0 ± 1.31 Pectoral-spine length 21.5 17.6Ð21.7 19.9 ± 1.19 Caudal-fi n length 35.4 33.5Ð44.0 38.3 ± 3.26 Length of adipose-fi n base 17.7 14.2Ð17.7 16.2 ± 1.05 Dorsal to adipose distance 13.2 13.2Ð16.7 15.2 ± 1.19 Post-adipose distance 16.7 16.3Ð20.7 18.2 ± 1.34 Caudal peduncle length 18.4 16.9Ð20.3 18.5 ± 1.07 Caudal peduncle depth 8.1 7.3Ð8.9 8.1 ± 0.54 Body depth at anus 19.1 14.6Ð19.2 17.2 ± 1.43 Head length 29.4 27.6Ð30.4 29.0 ± 0.97 Head width 25.8 24.4Ð26.2 25.3 ± 0.57 Head depth 20.7 18.4Ð20.9 20.0 ± 0.79 %HL Snout length 31.7 30.2Ð34.5 32.4 ± 1.44 Interorbital distance 35.8 32.1Ð36.4 34.2 ± 1.60 Eye diameter 11.4 11.2Ð14.7 13.0 ± 1.35 Nasal barbel length 68.3 56.0Ð79.4 65.0 ± 6.16 Maxillary barbel length 91.1 91.1Ð114.3 99.8 ± 8.39 Inner mandibular barbel length 48.0 32.7Ð57.3 46.4 ± 6.62 Outer mandibular barbel length 60.2 60.2Ð85.5 73.7 ± 6.61

with thin skin; bones visible, especially on posterior half of unpaired, continuous across midline; smoothly arched along neurocranium, and ornamented with numerous ﬁ ne, radial anterior margin, of equal width throughout and wider than grooves. Midline of cranium with fontanelle extending premaxillary band; band narrower than premaxillary band from behind snout to just beyond level of posterior orbital at midline, widening laterally and then tapering to a sharp margin. Supraoccipital process moderately broad, with point posterolaterally. gently converging sides and blunt tip; extending to nuchal plate. Supratemporal with short posterior process, about Barbels in four pairs. Maxillary barbel slender, extending to half as long as postcleithral process. Eye ovoid, horizontal middle of pectoral-ﬁ n base. Nasal barbel slender, extending axis longest, subcutaneous; located entirely in dorsal half of to dorsal insertion of opercle. Inner mandibular-barbel origin head. Gill openings wide, extending from post-temporal to close to midline; barbel thicker and longer than nasal barbel beyond isthmus. Gill membranes free from isthmus, with 8 and extending for two thirds of head length. Outer mandibular (20) branchiostegal rays. First branchial arch with 3+7 (2), barbel originating posterolateral of inner mandibular barbel, 4+6 (1), 3+8 (6) or 4+7* (1) gill rakers. extending to base of pectoral spine.

Mouth subterminal. Oral teeth small and viliform, in Body slightly compressed, becoming more so toward caudal irregular rows on all tooth-bearing surfaces. Premaxillary peduncle. Dorsal profi le rising evenly but not steeply from tip tooth band in a shallow arc, of equal width throughout. of snout to origin of dorsal fi n and sloping gently ventrally Dentary tooth band much narrower than premaxillary tooth from origin of dorsal fi n to end of caudal peduncle. Ventral band at symphysis, tapering laterally. Vomerine tooth band profi le slightly convex to anal-fi n base, then sloping slightly

88 THE RAFFLES BULLETIN OF ZOOLOGY 2010 dorsally to end of caudal peduncle. Skin smooth; lateral line Adipose fin with convex margin for entire length, with complete and midlateral in position. Vertebrae 14+21 (4), deeply-incised posterior portion and origin at or immediately 15+20 (1), 16+19 (1), 14+22 (2), 15+21* (5), 16+20 (3), anterior to vertical through base of fi rst anal-fi n ray; fi n-base 15+22 (3) or 16+21 (1). moderate, spanning about one-third of postdorsal distance. Anal fi n base at or just posterior to vertical through origin Dorsal fi n with spinelet, spine, and 7 (20) rays. Origin of of adipose fi n, with iv,8,i (3); iv,9 (13); v,8* (1) or iv,10 (3) dorsal fi n anterior to mid-body, about two-fi fths of body. rays and curved posterior margin. Dorsal fi n margin convex, usually with anterior branch of fi n rays longer than other branches. Dorsal fi n spine short, Caudal peduncle moderately deep. Caudal fi n deeply forked, straight and slender, posterior edge without serrations. Nuchal with i,7,8,i (20) principal rays; upper and lower lobes slender shield moderately broad, with rounded tip anteriorly. and lanceolate. Procurrent rays extend anterior to fi n base.

Pectoral fi n with stout spine, sharply pointed at tip, and 6,i Colouration. – In 70% ethanol: Body dark brownish-gray (11) or 7* (9) rays. Anterior spine margin smooth; posterior above, dusky below. Sides with pale stripe over the lateral line spine margin with 9Ð15 large serrations along entire length from middle of body below dorsal fi n origin to base of caudal (number of serrations is ontogenetically related; 9 serrations peduncle. Ventral surfaces of head and body dark yellow. in specimens ca. 30 mm SL and 15 serrations in specimens Caudal fi n hyaline with dark brownish gray submarginal ca. 50 mm SL). Pectoral fi n margin straight anteriorly, convex bar on each caudal lobe, and two separate spots in middle posteriorly. Postcleithral process of moderately broad, with of upper and lower caudal lobes; spots faintly coalescent slightly convex dorsal margin and extending for half of to form irregular bar in some individuals. Three irregular pectoral-spine length. yellowish bars: fi rst (indistinct in some individuals) over nape, second from immediately posterior to dorsal fi n base to Pelvic fi n origin posterior to vertical through posterior end immediately posterior to pelvic origin, third on anterior part of dorsal-fi n base, with i,5 (20) rays and slightly convex of caudal peduncle from immediately posterior to adipose margin; tip of adpressed fi n reaching base of second or fi n base to immediately posterior to anal-fi n base. Small third anal-fi n ray. Anus and urogenital openings located at yellowish blotches also present on anterior part of upper and vertical through middle of adpressed pelvic fi n. Males with lower procurrent caudal rays, adipose fi n origin, and along an elongate conical genital papilla reaching to base of fi rst anal fi n base. Dorsal, anal and pelvic fi ns hyaline with dark anal-fi n ray.

Fig. 2. Predorsal proﬁ les of: a, Pseudomystus funebris, ZRC 51845, Fig. 1. Pseudomystus funebris, MZB 17181, holotype, 41.8 mm paratype, 36.3 mm SL; b, P. heokhuii, ZRC 39069, paratype, 42.6 SL; Borneo: Kalimantan Tengah, Rungan River drainage. mm SL. Images not to scale.

89 Ng: New Pseudomystus from Borneo basal and submarginal bars; dark markings nearly absent in In addition to the characters described in the diagnosis, P. anal and pelvic fi ns of some individuals. Posterior edge of funebris further differs from P. breviceps, P. bomboides, P. adipose fi n hyaline. fl avipinnis, P. siamensis, P. sobrinus, P. stenomus and P. vaillantii in having a wider head (24.4Ð26.2 %HL vs. 17.4Ð Live colour similar, with more pronounced yellow 22.2), and from P. carnosus, P. fumosus and P. moeschii in colouration. having the post-temporal with a posterior process that is only two-thirds as long as (vs. as long as) the postcleithral process. Distribution. – Known currently only from the Rungan River Pseudomystus funebris can be further distinguished from P. in southern Borneo (Fig. 3). The Rungan River is part of the inornatus, P. mahakamensis, P. rugosus and P. stenogrammus Kahayan River drainage. in having a deeper caudal peduncle (7.3Ð8.9% SL vs. 5.4Ð7.6) and wider head (24.4Ð26.2% SL vs. 15.1Ð18.4), and from P. Etymology. – The specifi c epithet comes from the Latin myersi in having the posterior end of the adipose fi n not in funebris, meaning “of a funeral”. Being clothed in black is contact (vs. confl uent) with the upper procurrent caudal rays. traditionally associated with funerals, and the name alludes It further differs from P. robustus in having a moderately (vs. to the blackwater habitat of this species. very) broad postcleithral process and the pelvic fi n reaching (vs. not reaching) the anal-fi n base.

DISCUSSION COMPARATIVE MATERIAL Pseudomystus funebris, like the allopatric P. heokhuii, is found in fl oodplain peat swamps, in tannin-stained, very Pseudomystus heokhuii: ZRC 41951, 6 paratypes, 38.0Ð51.6 acidic (pH below 5) water. It superfi cially resembles P. mm SL, Sumatra: Jambi, Batang Hari drainage at Rantau leiacanthus (from Sumatra and the Malay Peninsula), but Panjang; ZRC 39069, 17 paratypes, 31.5Ð46.6 mm SL, can be distinguished from it in having two (vs. one) dark Sumatra: Riau, Indragiri drainage, peat swamp draining narrow irregular bars on the caudal fi n, longer caudal fi n into Sungai Bengkwan, tributary of Indragiri River; ZRC (33.5Ð44.0% SL vs. 25.7Ð31.9) with pointed (vs. rounded) 46151 12 paratypes, 37.4Ð54.0 mm SL, Sumatra: Sumatera lobes, longer nasal and maxillary barbels (56.0Ð79.4% HL vs. Selatan, Layang drainage, Sungai Sentang, 12 km from 31.3Ð51.5 and 91.1Ð114.3% HL vs. 70.9Ð91.3 respectively; Jambi to Bayung Lencir (216 km to Palembang) near Desa nasal barbel reaching to dorsal insertion of opercular fl ap vs. Sukajaya. to just beyond posterior orbital margin and maxillary barbel reaching just beyond base of last pectoral-fi n ray vs. to base See Lim & Ng (2008) for additional list of comparative of pectoral spine), material.

In addition to the difference in size, the shapes of the adipose ﬁ n in P. funebris and P. heokhuii also appear to differ slightly: the dorsal margin of the former species appears more steeply- and evenly-sloping than in the latter species (Fig. 4). However, this difference is slight and is thus not used in the diagnosis to distinguish between the two species.

Fig. 4. Postdorsal views of: a, Pseudomystus funebris, ZRC 51845, paratype, 36.3 mm SL; b, P. heokhuii, ZRC 39069, paratype, 36.1 Fig. 3. Map showing collection localities of blackwater Pseudomystus mm SL, showing differences in shapes of adipose ﬁ n. Images not species (P. funebris and P. heokhuii). to scale.

90 THE RAFFLES BULLETIN OF ZOOLOGY 2010

ACKNOWLEDGMENTS LITERATURE CITED

I thank John Lundberg (ANSP), Mohammad Zakaria-Ismail Ferraris, C. J., 2007. Checklist of catfishes, recent and fossil (BIRCUM), James Maclaine (BMNH), David Catania (CAS), (Osteichthyes, Siluriformes) and catalogue of siluriform primary Maurice Kottelat (CMK), Mary Anne Rogers (FMNH), types. Zootaxa, 1418: 1Ð628. Renny Hadiaty (MZB), Martien van Oijen (RMNH), Douglas Lim, K. K. P. & H. H. Ng, 2008. Pseudomystus heokhuii, a new Nelson (UMMZ), Lynne Parenti (USNM), Klaus Busse species of bagrid catﬁ sh from Sumatra (Teleostei: Bagridae). (ZFMK), Isaäc Isbrücker (ZMA) and Kelvin Lin (ZRC) for Zootaxa, 1686: 37Ð47. permission to examine material under their care. I am also Ng, H. H. & M. Kottelat, 1998. Hyalobagrus, a new genus of grateful to Patrick Yap for making the material available for miniature bagrid catfish from Southeast Asia (Teleostei: study. This work was partially supported by research grant Siluriformes). Ichthyological Exploration of Freshwaters, 9: R-154-000-318-112 of the National University of Singapore 335Ð346. to Heok Hui Tan.

THE RAFFLES BULLETIN OF ZOOLOGY 2010

THE RAFFLES BULLETIN OF ZOOLOGY 2010 58(1): 93Ð102 Date of Publication: 28 Feb.2010 © National University of Singapore

CASTELNAU’S COLLECTION OF SINGAPORE FISHES DESCRIBED BY PIETER BLEEKER

Barry C. Russell Arafura Timor Research Facility, Department of Natural Resources Environment and the Arts, 23 Ellengowan Drive, Brinkin, NT 0810, Australia Email: [email protected] (Corresponding author)

Thomas H. Fraser Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL 34236-1096, USA Email: cardinalﬁ [email protected]

Helen K. Larson Museum and Art Gallery of the Northern Territory, PO Box 4646 Darwin, NT 0801, Australia Email: [email protected]

ABSTRACT. – Recently discovered watercolour paintings of Singapore fi shes by the French naturalist F. L. Castelnau in the Zoological Museum of the University of Liège, Belgium, include illustrations of seven hitherto unrecognized species of apogonid fi shes and a gobiid fi sh that formed the basis of new species descriptions by Pieter Bleeker in 1860. Based on examination of the paintings, we assign Bleeker’s species as follows: Apogonichthys taeniopterus Bleeker, 1860, is a junior synonym of Jaydia truncata (Bleeker, 1854); Cheilodipterus polystigma Bleeker, 1860, is a junior synonym of Pseudamia amblyuroptera Bleeker, 1856; Cheilodipterus singapurensis Bleeker, 1860, is a valid species; Apogonichthys macrophthalmus Bleeker, 1860, is a valid species, but because it has not been used in the literature is unavailable and Apogon compressus Smith & Radcliffe in Radcliff, 1911 (nomen protectum) is retained for this species; and Gobius melanopus Bleeker, 1860, is shown to be the senior synonym of Cryptocentrus leptocephalus Bleeker, 1876. The identities of the remaining species are uncertain: Apogon melanurus Bleeker, 1860, may represent a species of Cheilodipterus, possibly C. macrodon (Lacépède, 1802); Apogon singapurensis Bleeker, 1860 (nomen oblitum) is identifi ed as a synonym of Apogon endekatania Bleeker, 1852, based on dried skins; the painting may represent a member of the Apogon hartzfeldii complex, possibly Apogon cavitensis (Jordan & Seale, 1907) (nomen protectum); and Apogon arenatus Bleeker, 1860, may represent a species of Zoramia, possibly Z. leptacantha (Bleeker, 1856Ð57).

KEY WORDS. – Apogonid ﬁ shes, Cryptocentrus, Singapore, F.L. Castelnau, Pieter Bleeker.

INTRODUCTION François Louis Nompar de Caumont Laporte, comte de Castelnau (henceforth Castelnau; also variously known In one of a series of papers on the fi shes of Singapore, Pieter as Francis de la Porte de Castelnau; Francis de La Porte Bleeker (1860c) described seven new apogonid and one new Castelnau; Francis Louis Laporte; Francis Louis Laporte, gobiid species based on watercolour paintings by the French comte de Castelnau; François Louis Nompar de Caumont de diplomat, explorer and naturalist F. L. Castelnau. Except Laporte; Francis Louis de la Porte, comte de Castelnau), was for one of these species (Cheilodipterus singapurensis) a widely traveled naturalist and diplomat. Born in London type specimens are unknown, and the status of the others on 25 December 1810 (some sources give his year of birth has remained uncertain (Eschmeyer et al., 2009). During a as 1812), he studied natural science in Paris under Baron visit to the Zoological Museum of the University of Liège Cuvier, Geoffroy Saint-Hilaire and other noted zoologists. (ZMUL), Belgium in 2004, the fi rst author became aware of In 1837Ð41 he led an expedition to the United States, the a collection of fi shes made by Castelnau together with fi ve (then) Republic of Texas and Canada, where he studied the annotated sketchbooks. Amongst the many illustrations and fauna and political systems. In 1843Ð47, under the patronage paintings in the sketchbooks, approximately 400 are of fi shes of King Louis-Philippe of France, he led an expedition to from Singapore, including those described by Bleeker. South America, crossing from the Mato Grosso to Peru and returning via the Amazon River (Howgego, 2004; Loneux,

93 Russell et al.: Castelnau’s Singapore ﬁ shes described by Bleeker

2006). After the 1848 French revolution, he took up a sketchbook pages, which Bleeker must have seen at the time. diplomatic career. In the years between 1848 and 1855, he As Bleeker dated most of his publications (date of writing), was the French Consul at Salvador, Bahia, Brazil. In 1855, and using these dates (Table 1), it is possible to deduce that he returned to France and later travelled by steamer to the Castelnau must have made his paintings between 1859 and Cape of Good Hope, where he was French Consul from 1856 1861. A few paintings labeled ‘Singapore’ are dated: June to 1858 (Almanach de Gotha, 1857, 1858). He was posted 1859; 16 October 1860; and 19 June 1861. A letter found as the French Consul to Siam (Thailand) from 1858 to 1862 amongst the sketchbooks at ZMUL dated 12 June 1860 to (Ministère des Affaires étrangères, 1859, 1860, 1861, 1862) Castelnau from John Siellarttieu and Fredrick Keslar for the and during this time, he also visited India, Malacca, Sumatra, payment of insect and bird collections from Malacca also Java, Ceylon (Sri Lanka) and Singapore (Whitley, 1965). In indicates Castelnau was in Singapore then. 1863, Castelnau was appointed Consul-General for France in Melbourne (Birch & Robinson, 1867) where he remained after his retirement in 1877 until his death on 4 February CASTELNAU’S SINGAPORE FISHES 1880 (Whitley, 1965, 1974). DESCRIBED BY BLEEKER

Castelnau was a prolifi c ichthyologist, who described a total Apogonichthys taeniopterus Bleeker, 1860 of 469 new species of fi shes from Brazil and Peru (Castelnau, 1855), South Africa (Castelnau, 1861) and Australia Apogonichthys taeniopterus Bleeker, 1860c, is based on two (Castelnau, 1872, 1873a & b, 1875, 1876, 1878aÐc, 1879 a & coloured paintings by Castelnau, No. 93 (Fig. 1) and No. b). He was also the fi rst European to study the fi shes of Siam 342 (Fig. 2). No specimen has been identifi ed that served as (Smith, 1945). The collections and sketchbooks in the ZMUL the basis for the painting and the name. Bleeker provided a reveal that Castelnau made extensive collections of fi shes brief accurate description in Latin and made no additional from Siam and Singapore, many of which were illustrated comments. In his second description of this species, Bleeker in colour in two of his fi ve sketchbooks. Castelnau’s work (1874) changed two words in an otherwise repeated Latin between 1858Ð1862, during his time in Siam and Singapore, description. These words were “3” for “4” in reference to the remained largely unknown. For over 140 years, Castelnau’s body depth (about 4.3 from the painting) in its length and collections from these two countries and sketchbooks were “vitta” for “fascia”. He provided remarks on characteristics thought to be lost, until recently uncovered by Dr Michelle he could not determine, such as number of fi n elements, Loneux in the ZMUL (Loneux, 2002, 2006). number of scales and an uncertainty of serration on the preopercle. He believed the colour pattern was distinct. In Castelnau’s sketchbooks, together with collections of birds Bleeker’s “Atlas Ichthyologique” (1871–1876: 99) the Latin (697 specimens), fi shes (291 specimens Ð not yet surveyed description reverted to the original description although his for missing or unknown types), mammals (45 specimens) remarks were brief with sentences lifted from his 1874 paper. and a few marine invertebrates, were purchased in 1865 by In the latter two publications Bleeker placed this species just Jean-Theodore Lacordaire, Professor of Natural Sciences at after Apogon truncatus Bleeker, 1854. the University of Leige, to improve the ZMUL collections (Loneux, 2002, 2006). The sketchbooks include landscape Weber & de Beaufort (1929) listed Bleeker’s name as pencil sketches and paintings of fi shes from Bahia’s Bay, a synonym of Apogon ellioti Day, 1875, pre-empted by Brazil; and paintings of fi shes from Île Bourbon (Réunion) Apogon taeniopterus Bennett, 1836. Gon (1996) reviewed and the Cape of Good Hope (in 1856), Algoa Bay (in 1857), the nomenclature of Apogon truncatus in his revision of and various parts of Siam, Bangkok, Saigon (Ho Chi Minh the species group but did not list or comment on Bleeker’s City), Malacca, Palembang, Banka, Batavia (Jakarta) and taeniopterus. Gon’s illustration and Day’s (1875) description Singapore (variously dated between 1859Ð1861). and fi gure of Apogon ellioti agree on most of the diagnostic colour pattern present in Castelnau’s painting. The fi gure Each sketchbook page contains between one to 12 illustrations, of Apogon truncatus in Bleeker’s Atlas (1871–76, Pl. 41) most numbered and named, and some with annotations such shows only the distal dark portion of the fi rst dorsal fi n. No as fi n counts or other characters handwritten in pencil. All other markings were present. of the species discussed below had notes accompanying the illustrations that gave a new name along with authorship We conclude that Apogonichthys taeniopterus is a junior and abbreviations such as ‘nov sp’ indicating Castelnau’s synonym of Apogon truncatus, agreeing with Weber & opinion on the specimen in question. de Beaufort. Gon (1996) treated Apogon truncatus in the subgenus Jaydia, now recognized as a genus, removing the No correspondence between Castelnau and Bleeker were homonym confl ict with Bennett’s description of Apogon found in the collections at the ZMUL, and Castelnau’s taeniopterus in 1836. sketchbooks are mostly undated. However, it is known that Castelnau passed through Batavia en route to Siam in 1858 (Money, 1861: 10) where he undoubtedly met Bleeker. The Cheilodipterus polystigma Bleeker, 1860 two evidently remained in close contact, as Bleeker’s papers on Singapore fi shes published between 1860 and 1861, were Cheilodipterus polystigma Bleeker, 1860c, is based on a based largely on various fi sh paintings found in Castelnau’s coloured painting by Castelnau, No. 137 (Fig. 3). Bleeker

94 THE RAFFLES BULLETIN OF ZOOLOGY 2010 provided a brief description in Dutch based on this painting. In dark vent” (Lachner original notes). Four specimens were his revision of the Apogonidae, Bleeker’s (1874) redescription present when Fraser examined the lot in 1972. The largest in Latin of this species was based on two specimens, one specimen in the lot is about 144 mm TL not 149 mm. Martin from Singapore (collected during a ten day stopover on his Boeseman (in litt.) suggested that Bleeker may have made a return to Europe in 1860) and the other from Ambon (RMNH 5 mm error reading his ruler, the printer misread a 9 for a 3, 5610). Bleeker’s translated remarks (1874) are as follows: or the holotype was in the second lot of the Auction Catalog “Rem. I described this species for the fi rst time in the year and went elsewhere, or is lost. 1859 according to a drawing of Mr. the Count de Castelnau. At the time of my passage to Singapore, in the year 1860, We regard the largest specimen as the probable holotype and I obtained a beautiful specimen, and I also have a smaller one of the two smaller specimens mentioned by Bleeker is a specimen, poorly preserved from Ambon. One easily can paratype. The third specimen has no type status. No Bleeker identify the species by the eye-like black mark offset dorsally specimen has been reported at the British Museum, another on the side of the caudal peduncle”. possible repository for the specimen. The specimen with the dark vent was identifi ed as Cheilodipterus truncatus (139 Randall et al. (1985) mention these specimens in their material mm TL) and removed to RMNH 26674 in 1972. While there list of Pseudamia amblyuroptera (Bleeker, 1856) but did not are two interpretations of the signifi cance of the blackish identify either of them as a possible syntype. Castelnau’s vent (Lachner, 1953; Gon 1993), neither Bleeker’s written painting is the representation of the type specimen, lost or descriptions nor Castelnau’s fi gure provide any evidence possibly yet to be located among the preserved/dried material that they observed this colour pattern. We conclude that at the ZMUL. As both the Singapore specimen and the Ambon Castelnau’s fi gure of an adult was used appropriately by specimen apparently were obtained after Bleeker’s original Bleeker. description of C. polystigma was published, neither can be regarded as types. In their remarks, Randall et al. (1985) discuss their reasons why Pseudamia polystigma should be Apogon melanurus Bleeker, 1860 considered a synonym of P. amblyuroptera as the result of variation associated with size. The painting of Apogon melanurus Bleeker, 1860c, No. 149 (Fig. 5), has the mouth closed so placement in Cheilodipterus The coloured painting can be easily identifi ed with the species is not certain, however, the drawn specimen was slender. treated by Randall et al. (1985) and with Bleeker’s fi gure of Bleeker (1860c) thought this species was similar to Apogon Cheilodipterus polystigma (Bleeker, 1875Ð1876: Pl. 70). The aureus based on the caudal marking, but differed in its body fi gure of Pseudamia amblyuroptera (Bleeker, 1871Ð1876: Pl. shape and the stripe-like spots. No known species of Apogon, 32) appears more diagrammatic. We agree that Pseudamia sensu lato, has this combination of colours on the head, body amblyuroptera is the senior synonym of P. polystigma. or fi ns. Perhaps Apogon taeniopterus Bennett, 1836, could be considered a possible candidate, but it has well-defi ned dark mid-stripes in the second dorsal and anal fi ns, characteristics Cheilodipterus singapurensis Bleeker, 1860 absent from the painting and descriptions. Cheilodipterus macrodon (Lacépède, 1802) as described by Gon (1993) Cheilodipterus singapurensis Bleeker, 1860c, is based on and the photos (Kuiter & Kozawa, 2001) of Cheilodipterus a specimen which was related to a coloured painting by octolineatus appear to be close to Castelnau’s painting. The Castelnau, No. 67 (Fig. 4), with notes “Cheilodipterus painting differs from both of these possibilities by lacking singaporensis Cast. Blk octovittatus Cu ? Val nov. spec.”. The stripes on the head, by having a blackish distal area on the mouth is partly open and shows large teeth. In the original anal fi n and a uniform fi rst dorsal fi n. The blackish portions Latin description, Bleeker (1860c) lists a single specimen of of the caudal peduncle and caudal fi n are consistent with 149 mm total length (TL) and in the Dutch remarks he refers some species of Cheilodipterus. to another specimen of 119 mm TL. By 1874 Bleeker had added three more specimens and modifi ed his description. A Other species of Cheilodipterus drawn by Castelnau are fi gure was provided by Bleeker (1875Ð1876b: Pl. 35) in the similar: C. lineatus, No. 507 (Fig. 6), C. quinquelineatus, Atlas. No changes were made to the description or remarks in No. 574 (Fig. 7) and C. octovittatus, No. 575 (Fig. 8). 1876 from the additions in 1874. The descriptions by Bleeker, All are slender species. We consider this painting to be his fi gure and Castelnau’s painting do not show a black a Cheilodipterus of unknown identity, perhaps a poor mark in the area of the anal and genital openings. Bleeker’s representation of Cheilodipterus macrodon which is known (1875–1876) fi gure was based on the juvenile colour pattern, from Singapore. probably from one of the smaller specimens. Gon (1993) provided the most recent revision of Cheilodipterus and recognized C. singapurensis as a valid species. Apogon singapurensis Bleeker, 1860

Although Gon listed Bleeker’s material, RMNH 5619 with The painting of Apogon singapurensis, No. 208 (Fig. 9), is three specimens, no types are mentioned or discussed. of an Apogon, sensu lato, with at least six fi rst dorsal spines. Ernest A. Lachner examined Bleeker’s material in 1956. He Cardinalfi sh without stripes in the dorsal and anal fi ns, with recorded four specimens present, one with a “conspicuously reddish and golden or yellowish stripes and a medium-sized

95 Russell et al.: Castelnau’s Singapore fi shes described by Bleeker blackish peduncle spot include Apogon cavitensis and Apogon fi ns, II,8 for the anal fi n and 13–14 fi n rays in the pectoral chrysotaenia. None of these species has been well-studied. fi n. The basicaudal spot was round, relatively large and Kuiter & Kozawa (2001) suggest that there are three species blackish, consistent with Apogon endekataenia Bleeker, in this grouping identifi ed as the Apogon hartzfeldii complex. 1852b. The eighth dorsal spine was probably hidden under Bleeker (1876) thought this species had some similarity to the skin in life. No other dark stripes or other darkish marks Apogon wassinki. However, the presence of the blackish were present on these specimens. caudal peduncle spot eliminates any candidate species in the Apogon cyanosoma complex. If either or both dried specimens represent the material that Castelnau used for his painting, then the painting may be Two Castelnau specimens, both dried mounts from Singapore, a poor representation of Apogon endekataenia. The darkish are listed in the Catalogue of the ZMUL as 2378a, 2378b, stripes on these specimens of Apogon endekataenia are not 72Ð75 mm SL or about 90 mm TL (Fig. 10, 11) as Apogon as intensely black as the basicaudal spot in life (see Kuiter singapurensis. These specimens have VIII-I,9 in the dorsal & Kozawa, 2001: 20, Figs. A, B) or in preservation (Fraser,

Figs. 1–9. Castlenau’s paintings numbers 93, 342, 137, 67, 149, 507, 574, 575 and 208, respectively.

96 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. Publication dates and dates of writing of Bleeker’s papers on Singapore ﬁ shes.

Publication date Journal Date of writing Based on Castelnau No species sketches reported Bleeker 1851 Nat. Tijdschr. Ned. Ind., 1: 480Ð481 Undated No 122 Bleeker 1852a Nat. Tijdschr. Ned. Ind., 3: 51Ð86 December 1851 No 73 Bleeker 1858 Nat. Tijdschr. Ned. Ind., 15: 241Ð254 January 1858 No 80 Bleeker 1860a1 Nat. Tijdschr. Ned. Ind., 20: 216Ð217 11 August 18592 Yes 29 Bleeker 1860b1 Nat. Tijdschr. Ned. Ind., 20: 236Ð239 24 August 18592 Yes 88 Bleeker 1860c1 Nat. Tijdschr. Ned. Ind., 20: 446Ð456 October 1859 Yes 123 Bleeker 1860d Nat. Tijdschr. Ned. Ind., 21: 334 9 February 18602 Yes 4 Bleeker 1861a Nat. Tijdschr. Ned. Ind., 22: 101Ð102 10 May 18602 Yes 11 Bleeker 1861b Versl. Akad. Amsterdam, 12: 28Ð63 10 January 1861 Yes 155

Notes: 1 The publication dates of Bleeker (1860a-c) are problematical. These papers appeared in the 1859-1860 volume of “Natuurkundig Tijdschrift voor Nederlandsch Indie” (vol. 20). As Kottelat (2000) has pointed out, the publication pattern of this journal was somewhat irregular, with two or three volumes appearing every year between 1855 and 1860. Volume 17 is dated 1858Ð59, volumes 18 and 19 as 1859, volume 21 as 1860 and volume 22 as 1861 (The decrease in publication rate after 1860 is apparently linked with Bleeker’s departure from Batavia in September 1860) (Kottelat, 2000). Volume 20 was distributed as a single issue and as the last paper was dated December 1859 (date of writing), it seems difﬁ cult (if not impossible) that it could have appeared in 1859 (Kottelat, 2000), and we agree with Kottelat that the actual date of publication was most likely early in 1860. 2 Although Bleeker dated most of his publications (date of writing), a few (Bleeker, 1860a, b, d and e) were not dated. In a footnote, however, Bleeker (1861b: 29) provides the dates for them indicated here, presumably the dates upon which they were completed and submitted for publication.

1974: Fig. 1). The alternating stripes may have changed None of the known cardinalfi sh in Apogonichthys, Foa, colours post-mortem and may have been lost in preservation. Fowleria, Neamia, the Apogon taeniatus complex or the The reddish and yellowish markings in the post-mortem Apogon poecilopterus complex has any stripes. We assume watercolour would certainly be lost in preservation. that the caudal fi n was probably emarginate, not deeply forked. We regard the Apogon hartzfeldii complex as the most likely candidate grouping for the painting. Apogon cavitensis There are several species of striped cardinalfi sh which have Jordan & Seale, 1907, is known from Singapore and the some similarity in stripes to Castelnau’s painting: Apogon painting may represent this species in the absence of compressus, Apogon kalosoma and Apogon brevicaudatus. the actual specimen(s). If so, then Bleeker’s name is not However, none has a good fi t to the painting. Two species, available because singapurensis (nomen oblitum) has not Apogon kalosoma and Apogon brevicaudatus, have convex been consistently used as a valid name since its description second dorsal and anal fi ns. The fi n markings of Apogon and the clear identity of cavitensis (nomen protectum) to brevicaudatus and the restricted distribution of this species the present in literature (see Eschmeyer et al., 2009, for a (Kuiter & Kozawa, 2001) make it an improbable candidate. partial list), books and electronic media. We regard Apogon There are more narrow stripes present on the body of Apogon endekataenia as the most likely name for the dried specimens kalosoma than depicted in the painting, but dark edges on (ZMUL 2378a-b) based on the size of the basicaudal spot. We the caudal fi n shown in the painting may be present on this have no evidence that Castelnau used, if at all, one or both species. The body stripes of Apogon compressus are more specimens as the basis for the painting. The best course of consistent with the painting. This species has six fi rst dorsal action is to treat Apogon singapurensis as a junior synonym spines and nine rays in the anal fi n and a relatively deeper of Apogon endekataenia because of Castelnau’s dried material body. The painting depicts a fi sh with relatively short fi rst from Singapore. dorsal fi n and a relatively large eye, which could be consistent with Apogon compressus. However, Apogon compressus has a slightly concave anal fi n with a longer base, not seen in Apogonichthys macrophthalmus Bleeker, 1860 the painting.

Castelnau’s painting of Apogonichthys macrophthalmus Both Apogon compressus and A. kalosoma have been collected Bleeker, 1860c, No. 163 (Fig. 12) is striking with the large at Singapore. We believe the species that Castelnau drew was eye, reddish stripes and dark edges to the truncated or rounded a specimen of Apogon compressus. Specimens of Apogon caudal fi n. Bleeker did not alter his descriptions signifi cantly compressus has been easily identifi ed by ichthyologists since from the original description (1860c), the revision (1874) or it was described by Smith & Radcliffe in Radcliffe (1911). the “Atlas” (1876). His comments added little information. There have been no subsequent synonyms. It seems unusual

97 Russell et al.: Castelnau’s Singapore ﬁ shes described by Bleeker

Figs. 10–17. Figures 10, 11: dried mounted specimens in the collection of the Zoological Museum of the University of Liège , Beligium (ZMUL), catalogue numbers 2378a and 2378b. Figures 12–17: Castlenau’s paintings, numbers 163, 171, 482, 483, 625 and 193, respectively.

98 THE RAFFLES BULLETIN OF ZOOLOGY 2010 that no one other than Bleeker described this species from Unless another undescribed species of Zoramia is recognized the West Pacifi c prior to 1911. Bleeker’s name should be and corresponds with arenatus, Bleeker’s name should be considered as unavailable because macrophthalmus (nomen treated as a junior synonym of Zoramia leptacantha. oblitum) has never been used as a valid name and the clear identity of compressus (nomen protectum) to the present in literature (see Eschmeyer, et al. 2009 for a partial list), books Gobius melanopus Bleeker, 1860 and electronic media. Castelnau painting No. 193 (Fig. 17) is labeled as “Gobius sp. nov.” and “Gobius melanopus Cast.” Gobius melanopus Apogon arenatus Bleeker, 1860 was described by Bleeker in 1860c, based on Castelnau’s fi gure and the name attributed to Castelnau. No type material Apogon arenatus Bleeker, 1860c, No. 171 (Fig. 13), has is known. The species name has been used as a valid name few markings other than small reddish or pinkish spots and by Larson (in Randall & Lim 2000: 637); where it was cited some yellowish area, on the snout. The angled mouth and as ‘Cryptocentrus’ melanopus, as at that time it was thought body shape suggests a fairly compressed fi sh. A species that the species name may refer to a group of species that from among Zoramia, Archamia, Siphamia, and Apogon include Cryptocentrus russus and C. voigtii Ð species that could be considered based on the absence of any stripes, may belong to a separate genus. bars or dark marks. The notes refer to “Apogon sp nov, macropteroides CV même qui 483, Apogon arenatus The species illustrated by Castelnau agrees with Cryptocentrus Castelnau”. Castelnau drew at least two, perhaps three species leptocephalus Bleeker, 1876, based on a specimen from now in Archamia: Apogon macropteroides, No. 482 (Fig. Singapore (RMNH 4665). Castelnau’s painting clearly shows 14); Apogon macropteroides, No.483 (Fig. 15); and Apogon the large pink spots and short pink streaks on the head, dorsal bleekeri, No. 625 (Fig. 16). These species are painted with fi ns and pectoral fi n base, dark anal fi n, the oblique pinkish long anal fi n bases in contrast to the painting of Apogon brown bars on the body, and the characteristic pinkish red arenatus. Bleeker did not alter the original description in and yellow-striped pelvic fi ns with blackish tips (compare his later publications. Bleeker’s abbreviated comments on with photos in Kuiter & Tonozuka, 2001: 631; Senou et al., this species provide little help in determining the identity of 2004: 316Ð317). Hence, Cryptocentrus melanopus Bleeker, this fi sh. A few species were considered: Apogon gularis, 1860c, is the senior synonym of C. leptocephalus Bleeker, Zoramia leptacantha, Archamia fucata and Siphamia jebbi. 1876. Under the 2000 ICZN Code, precedence must be None of these species have been recorded from Singapore, maintained, as reversal of precedence (Article 23.9) cannot but all have distributions that suggest they are likely to be met since the senior synonym has been used as a valid occur there. Apogon gularis and Siphamia jebbi are found name after 1899 (although the junior synonym has been used in deeper waters, and therefore, less likely to be collected for the species by at least 10 authors). or seen by Bleeker. Siphamia jebbi has a bioluminous organ system located along the side of the abdomen extending on to the peduncle (Allen, 1993). Presumably, this structure DISCUSSION would have been noticed by Castelnau and subsequently included in his painting. Apogon gularis has a dark mark on Apogon melanurus, A. arenatus, A. singapurensis and the snout (Fraser & Lachner, 1984) which is not present in Apogonichthys macrophthalmus, all described in Bleeker the painting. Zoramia leptacantha (Bleeker, 1856Ð57) is the (1860c) are based on coloured paintings by Castelnau. only species of Zoramia without clusters of melanophores No specimens are mentioned in any of his subsequent and/or a dark spot on the caudal peduncle or basicaudal descriptions (Bleeker, 1874, 1876). Weber & de Beaufort region. This species can have a very long filamentous (1929) treated these as doubtful species; their descriptions spinous dorsal spine, and has a few yellowish bars on the are translations from Bleeker’s Latin descriptions. No opercle and adjacent body, a line present along the base of subsequent publications have associated these names with the dorsal fi ns onto the peduncle and a line along the base any recognized species (Eschmeyer et al., 2009). Most of of the anal fi n onto the peduncle (Fraser & Lachner, 1985; the basic characteristics on which Bleeker based his usual Kuiter & Kozawa, 2001). These distinctive characteristics descriptions from specimens were not available to him via are all absent in the painting. Archamia fucata has a very the watercolour paintings or in any subsequent ichthyological long anal fi n, fi nely curved bars on the body and a yellowish literature. snout. Most photographs of Archamia fucata show a darkish basicaudal spot except one photograph of a specimen from Based on examination of the paintings, we assign Bleeker’s Bali with a very faint and diffused caudal marking (Kuiter species as follows: Apogonichthys taeniopterus Bleeker, & Kozawa, 2001). The anal fi n and dorsal fi n base are not 1860c, is a junior synonym of Jaydia truncata (Bleeker, signifi cantly different in their lengths in the painting which 1854); Cheilodipterus polystigma Bleeker, 1860c, is a would eliminate any Archamia, but not Zoramia. junior synonym of Pseudamia amblyuroptera Bleeker, 1856; Cheilodipterus singapurensis Bleeker, 1860c, is a valid We believe that the painting of Apogon arenatus is most species; Apogonichthys macrophthalmus Bleeker, 1860c, is a likely from a specimen of Zoramia, probably Z. leptacantha valid species, but because it has not been used in the literature (Bleeker,1856–57) without the fi lamentous dorsal spine. is unavailable and Apogon compressus Smith & Radcliffe in

99 Russell et al.: Castelnau’s Singapore ﬁ shes described by Bleeker

Radcliff, 1911 (nomen protectum) is retained for this species; Bleeker, P., 1852b. Bijdrage tot de kennis der ichthyologische and Gobius melanopus Bleeker, 1860c, is shown to be the fauna van het Eiland Banka. Natuurkundig Tijdschrift voor senior synonym of Cryptocentrus leptocephalus Bleeker, Nederlandsche-Indië, 3: 443Ð460. 1876. The identities of the remaining species are uncertain: Bleeker, P., 1854. Specierum piscium javanensium novarum Apogon melanurus Bleeker, 1860c, may represent a species vel minus cognitarum diagnoses adumbratae. Natuurkundig of Cheilodipterus, possibly C. macrodon (Lacépède, 1802); Tijdschrift voor Nederlandsche-Indië, 7: 415Ð448. Apogon singapurensis Bleeker, 1860c (nomen oblitum) is Bleeker, P., 1856. Bijdrage tot de kennis der ichthyologische identifi ed as a synonym of Apogon endekataenia Bleeker, fauna van het Eiland Boere. Natuurkundig Tijdschrift voor 1852b, based on dried skins; the painting may represent a Nederlandsche-Indië, 11: 383Ð414. member of the Apogon hartzfeldii complex, possibly Apogon Bleeker, P., 1856-57. Achtste bijdrage tot de kennis der cavitensis (Jordan & Seale, 1907) (nomen protectum); and ichthyologische fauna van Ternate. Natuurkundig Tijdschrift Apogon arenatus Bleeker, 1860c, may represent a species of voor Nederlandsch Indië, 12: 191Ð210. Zoramia, possibly Z. leptacantha (Bleeker, 1856Ð57). Bleeker, P., 1858. Tweede bijdrage tot de kennis der vischfauna van Singapore. Natuurkundig Tijdschrift voor Nederlandsch Now that these paintings have been rediscovered there is more Indië, 15: 241Ð254. clarity for the Bleeker names. The Castelnau watercolour Bleeker, P., 1860a. Vischsoorten van Singapore, verzameld paintings and the dried skins may prove valuable in sorting door Fr. Graaf de Castelnau. Natuurkundig Tijdschrift voor out the identities of other fi shes with limited descriptions. Nederlandsche-Indië, 20: 216Ð217. Bleeker, P., 1860b. Nieuwe vischsoorten van Singapore, verzameld door Fr. Graaf de Castelnau. Natuurkundig Tijdschrift voor ACKNOWLEDGEMENTS Nederlandsche-Indië, 20: 236Ð239. Bleeker, P., 1860c. Derde bijdrage tot de kennis der vischfauna We thank Michelle Loneux for providing information and van Singapoera. Natuurkundig Tijdschrift voor Nederlandsche- Christian Michel for providing access to the Castelnau Indië, 20: 446Ð456. collection and sketchbooks at the Zoological Museum Bleeker, P., 1860d. Zoetwatervisschen van Singapoera, verzameld of the University of Liège, Belgium. K. Van Egmond door F. Graaf de Castelnau. Natuurkundig Tijdschrift voor at the Rijksmuseum van Natuurlijke Histoire (Leiden, Nederlandsch Indië, 21: 334. Netherlands) provided information on Cheilodipterus Bleeker, P., 1861a. Vischsoorten, nieuw voor de kennis der fauna truncatus. Rudie Kuiter and Gerry Allen provided information van Singapoera, verzameld door Fr. Graaf de Castelnau. on the identifi cation of Apogon singapurensis. William N. Natuurkundig Tijdschrift voor Nederlandsch Indië, 22: Eschmeyer provided comments regarding the Zoological 101Ð102. Code and use of old names absent from most of the Bleeker, P., 1861b. Mededeeling omtrent vischsoorten, nieuw voor literature. de kennis der fauna van Singapoera. Verslagen en Mededeelingen der Koninklijke Akademie van Wetenschappen. Afdeling Natuurkunde, 12: 28Ð63. LITERATURE CITED Bleeker, P., 1871Ð76. Atlas ichthyologique des Indes Orientales Néêrlandaises, publié sous les auspices du Gouvernement colonial Allen, G. R., 1993. Cardinalfishes (Apogonidae) of Madang néêrlandais. Percoides I, Priacanthiformes, Serraniformes, Province, Papua New Guinea, with descriptions of three new Grammisteiformes, Percaeformes, Datniaeformes. Atlas species. Revue francaise d’ Aquariologie, 20(1): 9Ð19. ichthyologique des Indes Orientales Néêrlandaises, publié sous Almanach de Gotha, 1857. Annuaire diplomatique et statistique les auspices du Gouvernement colonial néêrlandais. Tome VII: pour l’année 1857. Quatre-vingt-quatorzième année. Justus 1Ð126. Perthes, Gotha. 754 pp. Bleeker, P., 1874. Révision des espèces Indo-Archipélagiques Almanach de Gotha, 1858. Annuaire diplomatique et statistique du groupe des Apogonini. Natuurkundige Verhandelingen pour l’année 1858. Quatre-vingt-quinzième année. Justus der Hollandsche Maatschappij der Wetenschappen, Series 2, Perthes, Gotha. 852 pp. 3(1):1Ð82. Bennett, E. T., 1836 (1835). Characters of several fi shes from Bleeker, P., 1875-76. Atlas ichthyologique des Indes Orientales the Isle de France. Proceedings of the Zoological Society of Néêrlandaises, publié sous les auspices du Gouvernement London, (3): 206Ð208. colonial néêrlandais. Percoides II, (Spariformes), Bogodoides, Cirrhitéoides. Atlas ichthyologique des Indes Orientales Birch, A.N. & W. Robinson, 1867. The Colonial Offi ce List for 1867. Néêrlandaises, publié sous les auspices du Gouvernement Comprising historical and statistical information respecting colonial néêrlandais. Tome VIII: 1–156. the colonial dependencies of Great Britain. Harrison, London. 259 pp. Bleeker, P., 1876. Description de quelques espèces insulindiennes inédites des genres Oxyurichthys, Paroxyurichthys et Bleeker, P., 1851. Visschen van Straat Malakka, Prince of Cryptocentrus. Verslagen en Mededeelingen der Koninklijke Wales Island en Singapore. Natuurkundig Tijdschrift voor Akademie van Wetenschappen. Afdeling Natuurkunde Amsterdam, Nederlandsch Indië, 1: 480Ð481. Series. 2, 9: 138Ð148. Bleeker, P., 1852a. Bijdrage tot de kennis der ichthyologische fauna Castelnau, F. L., 1855. Poissons. In: Animaux nouveaux or rares van Singapore. Natuurkundig Tijdschrift voor Nederlandsch recueillis pendant l’expédition dans les parties centrales de Indië, 3: 51Ð86. l’Amérique du Sud, de Rio de Janeiro à Lima, et de Lima au Para; exécutée par ordre du gouvernement français pendant

100 THE RAFFLES BULLETIN OF ZOOLOGY 2010

les années 1843 à 1847, sous la direction du comte Francis Gon, O., 1996. Revision of the cardinalfish subgenus Jaydia de Castelnau. Part 7, Zoology. Paris. Vol. 2: iÐxii, 1Ð112, (Perciformes, Apogonidae, Apogon). Transactions of the Royal Pls. 1Ð50. Society of South Africa, 51: 147Ð194. Castelnau, F. L., 1861. Mémoire sur les poissons de l’Afrique Howgego, R.J., 2004. Encyclopedia of Exploration 1800 to 1850. australe. Paris. vii, 78 p. Hordern House, Potts Point, NSW. xi, 690 p. Castelnau, F. L., 1872. Contribution to the ichthyology of Australia. International Commission on Zoological Nomenclature, 2000. Proceedings of the Zoological and Acclimatisation Society of International Code of Zoological Nomenclature. Fourth Edition, Victoria, 1: 29Ð247. http://www.iczn.org/iczn/index.jsp. Castelnau, F. L., 1873a. Contribution to the ichthyology of Australia. Jordan, D. S. & A. Seale, 1907. Fishes of the islands of Luzon and Proceedings of the Zoological and Acclimatisation Society of Panay. Bulletin of the Bureau of Fisheries, 26:1–48, 20 fi gs. Victoria, 2: 37Ð158. Kottelat, M., 2000. The type species of Acheilognathus Bleeker. Castelnau, F. L., 1873b. Notes on the edible fi shes of Victoria. 1860 (Teleostei: Cyprinidae). Ichthyological. Research, 47(12): Intercolonial Exhibition Essays, 1872-3, 5: 1Ð17. 198Ð200. Castelnau, F. L., 1875. Researches on the fi shes of Australia No. Kuiter, R. H. & T. Kozawa, 2001. Apogonidae Pictorial Guide 2. Philadelphia Centennial Expedition of 1876. Intercolonial Fishes of the Indo-West Pacifi c. Zoonetics Edition, Seaford, Exhibition Essays, 1875-6. 52 pp. Australia. Pp. 1–132, 1 fi g., 3 maps, many color plates. Castelnau, F. L., 1876. Mémoire sur les poissons appelés barramundi Kuiter, R.H. & T. Tonozuka, 2001. Pictorial guide to Indonesian par les aborigènes du nord-est de l’Australie. Journal de reef fi shes Part 3 Jawfi shes – sunfi shes. Zoonetics: Melbourne Zoologie, 5: 129Ð136. 302 pp. Castelnau, F. L., 1878a. Australian fi shes. New or little known Lachner, E. A., 1953. Family Apogonidae: cardinal fi shes. In: species. Proceedings of the Linnaean Society of New South Schultz, L.P. & collaborators. Fishes of the Marshall and Wales, 2(3): 225Ð248. Marianas Islands. Bulletin, United States National Museum, Castelnau, F. L., 1878b. Notes on the fi shes of the Norman River. 202(1): 412Ð498. Proceedings of the Linnaean Society of New South Wales, Lacépède, B.G.E., 1802. Histoire Naturelle des poissons. Plassan, 3(1): 41Ð51. Paris. Vol. 4. 728 pp. Castelnau, F. L., 1878c. On several new Australian (chiefl y) fresh- Lacépède, B.G.E., 1802. Histoire Naturelle des poissons..Plasson, water-fi shes. Proceedings of the Linnaean Society of New South Paris. Vol. 7. 428 pp. Wales, 3(2): 140Ð144. Loneux, M., 2002. Trèsors des collections scientifi ques du Musèe de Castelnau, F. L., 1879a. On a new ganoïd fi sh from Queensland. zoologie (ULg) : atouts pour la connaissance de la faune belge. Proceedings of the Linnaean Society of New South Wales, Bulletin de l’Institut Royal des Sciences Naturelles, Biologie, 3(3): 164Ð165. 72-Supplement: 263Ð269. Castelnau, F. L., 1879b. Essay on the ichthyology of Port Jackson. Loneux, M., 2006. The Castelnau’s fi sh collection and watercolour Proceedings of the Linnaean Society of New South Wales, 3(4): notebooks. In: Segers, H., P. Desmet & E. Baus, ‘Tropical 347Ð402. Biodiversity: Science, Data, Conservation’. Proceedings of Day, F., 1875. The Fishes of India; being a natural history of the 3rd GBIF Science Symposium, Brussels, 18-19 April 2005: the fi shes known to inhabit the seas and fresh water of India, 91Ð94. Burma, and Ceylon. London, D. R. Hillman and Sons Ltd., Ministère des Affaires étrangères,1859. Annuaire diplomatique de Part 1: 1Ð168, Pls. 1Ð40. l’Empire français pour l’annee 1859 Deuxième Année. Librairie Eschmeyer, W.N., C.J. Ferraris, Jr., M.D. Hoang & D.L. Long, de Veuve Berger-Levrault et fi ls, Strasbourg. 2009. Part I. In: Catalog of Fishes. California Academy of Ministère des Affaires étrangères,1860. Annuaire diplomatique de Sciences, Available from http://research.calacademy.org/ l’Empire français pour l’annee 1860 Troisième Année. Librairie research/Ichthyology/catalog/fi shcatsearch.html (accessed 9 de Veuve Berger-Levrault et fi ls, Strasbourg. Sep. 2009). Ministère des Affaires étrangères,1861. Annuaire diplomatique de Fraser, T. H., 1974. Redescription of the cardinal fi sh Apogon l’Empire français pour l’annee 1861 Quatrième Année. Librairie endekataenia Bleeker (Apogonidae) with comments on previous de Veuve Berger-Levrault et fi ls, Strasbourg. usage of the name. Proceedings of the Biological Society of Ministère des Affaires étrangères,1862. Annuaire diplomatique Washington, 87(1): 3Ð9, Fig. 1, Tab. 1. de l’Empire français pour l’annee 1862 Cinquième Année. Fraser, T. H. & E. A. Lachner, 1984. An unusual Indo-West Pacifi c Librairie de Veuve Berger-Levrault et fi ls, Strasbourg. cardinalfi sh of the genus Apogon (Teleostei: Apogonidae). Money, J.W.B., 1861. Java; or, how to manage a colony showing a Proceedings of the Biological Society of Washington, 97(3): practical solution of the questions now affecting British India. 632–636, 2 fi gs. Vol I. Hurst and Blackett, London. 331 pp. Fraser, T. H. & E. A. Lachner, 1985. A revision of the cardinalfi sh Radcliffe, L., 1911. Notes on some fi shes of the genus Amia, family subgenera Pristiapogon and Zoramia of the Indo-Pacifi c region of Cheilodipteridae, with descriptions of four new species from (Teleostei: Apogonidae). Smithsonian Contribution to Zoology, the Philippine Islands. Proceedings of the United States National 412: 1–47, 20 fi gs., 4 tabs. Museum, 41(1853): 245Ð261. Gon, O., 1993. Revision of the cardinalfi sh genus Cheilodipterus Randall, J. E., E. A. Lachner, & T. H. Fraser, 1985. A revision of the (Perciformes: Apogonidae) with description of fi ve new species. Indo-Pacifi c apogonid fi sh genus Pseudamia with descriptions Indo-Pacifi c Fishes, 22: 1Ð59. of three new species. Indo-Pacifi c Fishes, 6: 1Ð23.

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Randall, J. E. & K. K. P. Lim, 2000. A checklist of the fi shes of Plesiopidae, Pseudoplesiopidae, Priacanthidae, Centropomidae. the South China Sea. Raffl es Bulletin of Zoology, Supplement E. J. Brill Ltd., Leiden: iÐxiv, 1Ð458. No. 8: 569Ð667. Whitley, G. P., 1965. Francois Laporte, Count Castelnau, Australian Senou, H., T. Suzuki, K. Shibukawa, & K. Yano, 2004. A Zoologist, 13: 93Ð102. photographic guide to the gobioid fi shes of Japan. Heibonsha: Whitley, G. P., 1974. Laporte, François Louis Nompar de Caumont Tokyo. 534 pp. (1810Ð1880). In: Australian Dictionary of Biography. Melbourne Smith, H. M., 1945. The fresh-water fi shes of Siam, or Thailand. University Press. Volume 5: 64Ð65. Bulletin of the United States National Museum, 188: 1Ð633. Weber, M. & L.F. de Beaufort, 1929. The fi shes of the Indo-Australian Archipelago. V. Anacanthini, Allotriognathi, Heterosomata, Berycomorphi, Percomorphi: Families: Kuhliidae, Apogonidae,

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THE RAFFLES BULLETIN OF ZOOLOGY 2010 58(1): 103–111 Date of Publication: 28 Feb.2010 © National University of Singapore

THE DISTRIBUTION AND STATUS OF GIANT CLAMS (FAMILY TRIDACNIDAE) – A SHORT REVIEW

Ahmad Syukri bin Othman Marine Environmental Group, Tropical Marine Science Institute, National University of Singapore, 18 Kent Ridge Road, Singapore 119227, Republic of Singapore

Gideon H. S. Goh and Peter A. Todd Marine Biology Laboratory, Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Blk S1 #02-05, Singapore 117543, Republic of Singapore Email [email protected] (PAT)

ABSTRACT. – In this review on the distribution, density and status of giant clams (family Tridacnidae) we combine reports derived from primary and grey literature with sighting data provided by Reef Check – a non-profi t reef-monitoring organisation. Density records from 15 countries typically range from 10-3 to 10-5 individuals per square meter, however, some populations can achieve numbers in excess of 100 individuals per square meter. Tridacna maxima has the most cosmopolitan distribution; almost encompassing the entire geographical range of all the other giant clams species. In contrast, the more recently discovered T. costata, T. rosewateri, T. teveroa and H. porcellanus have the most restricted geographical ranges. Reef Check data includes records of (unidentifi ed to species-level) giant clams beyond previously defi ned geographical boundaries; extending their known occurrence slightly west to near Cape Agulhas, South Africa. Overfi shing, habitat loss, pollution, and increases in sea surface temperatures all contribute to decreases in giant clam populations. Restocking efforts provide an opportunity to redress this decline but, without enhanced protection and enforcement, these efforts may be unsuccessful.

KEY WORDS. – Giant clams, distribution, abundance, density.

INTRODUCTION Giant clams are considered a valuable fishery in many countries, for instance, their adductor, gonads, muscle and Giant clams, with their large size, characteristic shell structures mantle are used for food, they are popular aquarium animals and colourful mantles, are iconic coral reef invertebrates that (so much so that they were among the top ten of the most play important ecological roles both as a food source and traded ornamental invertebrates worldwide; Wabnitz et al., as a substrate for reef-associated organisms (Alcazar, 1986; 2003) and their shells are used for ornaments, soap dishes, Mingoa-Licuanan & Gomez, 2002). There are ten established salad bowls, and fl oor tiles (Usher, 1984). As is the case members of the giant clam family Tridacnidae: Tridacna for many marine organisms, giant clam numbers have gigas (Linnaeus, 1758), Hippopus hippopus (Linnaeus, been greatly reduced due to overfi shing and loss of habitat 1758), T. maxima (Roding, 1798), T. derasa (Roding, 1798), (CITES, 2004a,b,c,d). Furthermore, they are susceptible T. crocea (Lamarck, 1819), T. squamosa (Lamarck, 1819), to stress-induced bleaching (expulsion of their symbiotic H. porcellanus (Rosewater, 1982), T. teveroa (Lucas, Ledua zooxanthellae) which is often associated with increased & Braley, 1991), T. rosewateri (Sirenko & Scarlato, 1991) sea surface temperatures (Norton et al., 1995; Leggat et al., and T. costata (Richter, Roa-Quiaoit, Jantzen, Al-Zibdah & 2003). According to the 2007 World Conservation Union’s Kochzius, 2008). All species host symbiotic photosynthetic Red List of Threatened Species (http://www.iucnredlist. zooxanthellae algae, Gymnodinium microadriaticum, in their org) eight species of giant clams are listed as either “Lower mantles and they are therefore found in relatively shallow Risk Conservation Dependent” or “Vulnerable”; with only and clear waters, such as those associated with coral reefs T. crocea classifed as ‘Lower Risk Least Concern’ (Wells, (Yonge, 1975; Trench et al., 1981; Sutton & Hoegh-Guldberg, 1996). Tridacna crocea burrows into substrates and is 1990). Past research has shown the range of giant clams to relatively small, making it more diffi cult, and less economical, span from East Africa to the east Pacifi c, and from Japan to to harvest. However, T. crocea has also been overfi shed Australia, but there is presently no review of their current in areas of Fiji, Japan and Vietnam. Giant clams are also distribution and status. deleteriously affected by increases in sedimentation and

103 Othman et al.: Distribution and status of giant clams pollution (Roberts et al., 2002). One species, T. costata, has Reef Check were converted from sexagesimal to decimal only very recently been discovered (Richter et al., 2008) and format and saved as *.dbf (version IV) fi les. The Geographical is therefore not yet listed, but Richter et al. (2008) propose Information System (GIS) freeware DIVA GIS was then “Critically Endangered” as the appropriate category. used to make a point shapefi le with the *.dbf coordinates superimposed on a continent map with Equal-Area Cylindrical Giant clams are under the protection of the Convention on projection centered on longitude150°E. We also extracted International Trade in Endangered Species of Wild Fauna the distribution of giant clams from the works of Rosewater, and Flora (CITES), of which 172 countries worldwide are (1965; 1982); Lucas (1988); Sims & Howard (1988); Zann signatories, but illegal trade and poaching continue to be a & Ayling (1988); Mingoa-Licuanan & Gomez (2002) and major problem (Lucas, 1994). The family Tridacnidae are Richter et al. (2008) to obtain species-specifi c ranges. listed under Appendix II, i.e. “not necessarily threatened with extinction, but in which trade must be controlled in order to avoid utilization incompatible with their survival” RESULTS AND DISCUSSION (CITES, 2008) and international trade may only take place upon granting of a permit. Nevertheless, wide disparities in Giant clams live along shallow shorelines and on reefs yearly giant clam trade fi gures (CITES, 2004a,b,c,d) suggest between 30°E and 120°W (South Africa to beyond French that some countries have failed to exert control on the clam Polynesia) and between 36°N and 30°S (Japan to Australia). trade. Local extinctions of several species of giant clams Distribution is not even, with greater diversity found in the have been reported for sites in the Philippines, Indonesia, central Indo-Pacifi c (Spalding et al., 2007). Where records Micronesia (Lucas, 1994), Malaysia (Tan & Zulfi gar, 2003) exist, densities typically range from 10-3 to 10-5 individuals per and Singapore (Guest et al., 2007), while many other countries square meter. Ashmore, Mermaid and Cartier Reefs, located have only low stocks remaining. within the Great Barrier Reef, host populations in excess of 100 individuals per square meter and Tatakoto, French Since Rosewater’s 1965 seminal review paper, many aspects Polynesia, has a population density of 90.9 individuals per of giant clam biology, from their symbiotic relationship with square meter (Rees et al., 2003, Gilbert et al., 2006). At the Symbiodinium sp. to their physiology and behaviour have other extreme, some sites in the Philippines, Vanuatu, and been examined in detail (e.g. Alcazar et al., 1987; Lucas, the Republic of Kiribati have densities of < 10-6 individuals 1994; Muscatine, 1990; Huang et al., 2007; Han et al., 2008). per square meter (Table 1). Tridacna maxima has the most Yet, even though most giant clam species are considered cosmopolitan distribution; almost encompassing the entire threatened, there has not been a consolidated update of their geographical range of all the other giant clam species (Fig. global distribution in more than four decades. The aim of 1). In contrast, the recently discovered species T. costata, this paper is to draw together data on giant clam presence T. rosewateri, T. teveroa and H. porcellanus have the most and abundance to provide a resource for workers interested restricted geographical ranges. Reef Check data includes in giant clam ecology and conservation. records of (unidentifi ed to species-level) giant clams beyond previously defi ned geographical boundaries; extending their known occurrence to near Cape Agulhas, South Africa. MATERIALS AND METHODS Seven species (T. gigas, T. derasa, T.squamosa, T. crocea, T. To determine the distribution and, when possible, density of maxima, H. hippopus and H. porcellanus) can be found in giant clams primary literature was searched for and retrieved Southeast Asia (Table 1), but many populations are in sharp using the online resources Web of Science, JSTOR, Science decline or, in some cases, functionally extinct. For instance, Direct and Google Scholar. In addition, other papers and six species (T. crocea, T. derasa, T. maxima, T. squamosa, H. grey literature were extracted from the National University hippopus and H. porcellanus) can be found in Malaysia, but of Singapore library as well as the World Wide Web. only T. crocea has a stable population (Tan & Zulfi gar, 2003). Finally, 75 scientists known to work, or have worked, on Tridacna gigas is probably extinct in Peninsular Malaysia giant clams were contacted directly via email. The search while H. porcellanus and T. derasa are restricted to Sabah, was not exhaustive and there exists relatively rare literature, Eastern Malaysia (Tan & Zulfi gar, 2003). In Singapore, H. including market surveys and technical reports (often not in hippopus is locally extinct, T. maxima is functionally extinct English), by organisations such as the Japan International and T. squamosa and T. crocea are present only in very low Cooperation Agency and Overseas Fishery Cooperation numbers (Guest et al., 2007). Of the three species of giant Foundation of Japan. clam found in Thailand, T. squamosa and T. maxima are considered “scarce” (Thamrongnavasawat et al., 2001). Little We also contacted Reef Check (www.reefcheck.org), an is known about giant clam distribution in other Southeast international nongovernmental organisation that surveys Asian countries including Brunei Darussalam, Cambodia, and monitors coral reefs worldwide through a network of Laos, Myanmar and Vietnam, although anecdotal evidence volunteers, and asked them to provide records of giant clam by SCUBA divers indicate their presence. sightings. Reef Check surveys include the presence/absence of giant clams, but they do not collect species-level or To the east and south, giant clams, albeit at lower diversity, abundance/density data; or survey giant clam communities can be found throughout Oceania, i.e. Australasia, Melanasia, found in non-reef areas. Raw coordinate data courtesy of Micronesia and Polynesia (Table 1). Clam diversity decreases

104 THE RAFFLES BULLETIN OF ZOOLOGY 2010 with increasing distance from Australia; from seven species The data presented here indicate that giant clam densities in Near Oceania to only T. maxima at the furthest boundary are low in many countries. This is most likely a result of of giant clam distribution in the east Pacifi c (Fig. 1). Data increased fi shing pressure and habitat destruction. Lucas by Reef Check indicates that there are populations of giant (1994) lists four main reasons for giant clam overfi shing clams beyond the species-specifi c boundaries described by in recent times: increased human population, improved Rosewater, (1965; 1982); Lucas (1988); Sims & Howard technology available to subsistence fi shermen, expanded (1988); Zann & Ayling (1988) and Mingoa-Licuanan & international/inter-island trade and poaching of giant clam Gomez (2002). Wells (1996) noted that T. derasa, T. gigas meat, and expanded international trade in shell specimens and T. squamosa have been introduced during various and artefacts. In 1987, Heslinga & Fitt suggested local mariculture efforts in areas including the US (e.g. Hawaii) communities could use giant clam culture to supplement and the Federated State of Micronesia. The naturally rare T. subsistence fi shing. A number of countries, inluding Tonga, tevoroa is found exclusively in a small locale, mainly on the Palau, Fiji, the Soloman Islands and the Cook Islands, have barrier reefs of Tonga and the Lau islands of Fiji (Klumpp tried to counter the decline of their giant clam populations & Lucas, 1994). While the abundance of giant clams in through local aquaculture and restocking progammes (e.g. Oceania has generally been declining, there are instances of Clarke et al., 2003 where young clams are introduced into unusually high numbers; for example Ashmore, Cartier and ocean nurseries in reserves or other protected areas. Mermaid Reefs, Australia, host densities in excess of 100 giant clams per m2 (Rees et al., 2003). Monitoring efforts are limited and measures to protect reintroduced clams are often poorly enforced. Nevertheless, To the west and north, T. costata, T. maxima, T. rosewateri the Marine Science Institute (MSI) at the University of the and T. squamosa inhabit coastlines of the Indian Ocean Philippines has a long and successful record of rearing, having (Fig. 1). Tridacna maxima and T. squamosa are relatively cultured giant clams to restore depleted supplies for the last cosmopolitan in distribution, whereas T. costata and T. 20 years. Over 40 sites have received cultured clams and rosewateri are geographically restricted to the northern MSI promote giant clam farming as a sustainable livelihood Red Sea and Mauritius, respectively (Richter et al., 2008; with restocking activities occurring in collaboration with CITES, 2008). Tridacna costata is a new discovery; only local groups. Overfi shing of giant clams in Japan led to a being described by Richter et al. in 2008. Japan represents reduction in catch from 578 tonnes in 1975 to just 28 tonnes the northernmost boundary to the distribution of giant clams in 1995 and, as a result, stricter regulations were introduced. (T. crocea, T. maxima, T. squamosa and H. hippopus). In fact, Furthermore, the Okinawa Prefectural Fisheries Experimental the southern islands of Okinawa, especially Ishigaki Island, Station introduced seed production operations (for culture and are the main supplier of giant clams for Japan with T. crocea sea-ranching) to boost giant clam supply (Okada, 1997). making up 90% of total landings (Okada, 1997).

Fig. 1. Distribution of giant clams. Adapted from Rosewater (1965, 1982); Lucas (1988); Howard (1988); Zann & Ayling (1988); Gomez & Mingoa-Licuanan (2002) and Richter et al. (2008). The blue triangles represent Reef Check records and therefore the species are unknown. Abbreviation used for genera: T., Tridacna; H., Hippopus.

105 Othman et al.: Distribution and status of giant clams

Table 1. Summary of giant clam distribution and density data. Abbreviation used for genera: T., Tridacna; H., Hippopus.

Sites surveyed Method of Approx. area Species Population density References survey surveyed (m2) (per m2) (population survey) Australia T. derasa The Great Barrier Reef SCUBA Braley, 1987 diving T. gigas T. derasa 2.90 × 10-4 The Great Barrier Reef SCUBA Braley, 1987 - North diving T. gigas 7.80 × 10-4 T. derasa 5.90 × 10-4 The Great Barrier Reef SCUBA Braley, 1987 - South diving T. gigas 6.00 × 10-4. T. maxima 1.58 × 102 Mermaid Reef T. gigas 5.88 Rees et al., 2003 H. hippopus 4.15 T. maxima 2.18 × 101 Cartier Reef Rees et al., 2003 H. hippopus 1.51 × 102 T. maxima 3.83 × 101 Ashmore Reef T. gigas 6.12 Rees et al., 2003 H. hippopus 1.14 × 102 Caroline Islands T. crocea 1.39 × 10-1 T. derasa 5.45 × 10-3 T. gigas 1.82 × 10-3 Palau 1.10 × 102 Hardy & Hardy, 1969 T. maxima 5.45 × 10-3 T. squamosa 6.36 × 10-3 H. hippopus 3.64 × 10-3 Cook Islands Tongarew Lagoon 6.75 × 104 T. maxima 4.2 × 10-1 Chambers, 2007 Aitutaki Lagoon 8.00 × 101 T. maxima 4.738 Sims & Howard, 1988 Manihiki Lagoon 8.25 × 102 T. maxima 2.87× 10-1 Sims & Howard, 1988 Suwarrow Lagoon 2.24 × 102 T. maxima 8.75× 10-2 Sims & Howard, 1988 Egypt and Jordan T. maxima 4.70 × 10-3 Gulf of Aqaba Roa-Quiaoit, 2005 T. squamosa 3.10 × 10-3 Northern Red Sea and 1.28 1.1× 104 T. costata 9.0 × 10-4 Richter et al. 2008 Gulf of Aqaba Egypt T. maxima Present Zuschin & Piller, 1997 French Polynesia Remote Fangatau Atoll 4.05 × 106 T. maxima 5.84 Andrefouet et al., 2005 Sensing Tatakoto Remote 1.15 × 107 T. maxima 7.71 Gilbert et al., 2006 Sensing Tubuai Remote 1.63 × 107 T. maxima 2.91 Gilbert et al., 2006 Sensing Malaysia T. crocea 9.92 × 10-3 SCUBA Pulau Tioman 2.62 × 103 T. maxima 5.38 × 10-2 Tan et al., 1998 diving T. squamosa 2.52 × 10-2

106 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. Cont'd.

Sites surveyed Method of Approx. area Species Population density References survey surveyed (m2) (per m2) (population survey) New Zealand (Tokelau Islands) T. maxima 1.75 × 10-1 Fakaofo Atoll Braley, 1989 T. squamosa 8.20 × 10-5 T. maxima 6.86 × 10-1 Nukunonu Atoll Braley, 1989 T. squamosa 4.10 × 10-5 Atafu T. maxima 8.41 × 10-2 Braley, 1989 Papua New Guinea T. crocea 1.49 × 10-3 T. derasa 3.40 × 10-5 T. gigas 8.20 × 10-5 Milne Bay Province Kinch, 2002 T. maxima 1.79 × 10-4 T. squamosa 1.37 × 10-4 H. hippopus 4.10 × 10-5 The Phillipines T. crocea 1.63 × 10-4 Snorkelling & Central Visayas SCUBA 5.30 × 105 T. maxima 8.00 × 10-5 Alcala, 1986 diving T. squamosa 6.67 × 10-5 T. crocea 2.29 × 10-4 Snorkelling & Western Visayas SCUBA 7.00 × 104 T. maxima 3.00 × 10-4 Alcala, 1986 diving T. squamosa 1.31 × 10-3 T. crocea 1.81 × 10-3 Snorkelling & Cagayan, Sulu Sea SCUBA 5.65 × 104 T. maxima 2.55 × 10-3 Alcala, 1986 diving T. squamosa 1.24 × 10-4 T. crocea 5.16 × 10-4 T. gigas 1.60 × 10-5 SCUBA Cagayancillo Island 6.50 × 104 T. maxima 2.61 × 10-3 Juinio et al., 1989 diving T. squamosa 4.70 × 10-5 H. hippopus 7.80 × 10-5 T. crocea 3.29 × 10-1 Snorkelling & T. derasa 3.81 × 10-5 Palawan Regions SCUBA 2.10 × 105 T. maxima 2.67 × 10-4 Alcala, 1986 diving T. squamosa 2.71 × 10-4 H. hippopus 1.38 × 10-4 T. crocea 7.40 × 10-5 SCUBA Western Pangasinan 5.30 × 105 T. maxima 1.10 × 10-5 diving Juinio et al., 1989 T. squamosa 3.20 × 10-5 T. crocea 3.40 × 10-2 T. derasa 2.90 × 10-5 T. gigas 1.00 × 10-5 Polillo SCUBA 2.10 × 105 Juinio et al., 1989 diving T. maxima 5.33 × 10-4 T. squamosa 7.00 × 10-4 H. hippopus 2.40 × 10-5 T. crocea 1.83 × 10-4 SCUBA Zambales 1.04 × 105 T. maxima 6.70 × 10-5 Juinio et al., 1989 diving T. squamosa 1.00 × 10-5

107 Othman et al.: Distribution and status of giant clams

Table 1. Cont'd.

Sites surveyed Method of Approx. area Species Population density References survey surveyed (m2) (per m2) (population survey) T. crocea 8.21 × 10-4 SCUBA Albay 1.45 × 105 T. maxima 7.03 × 10-4 Juinio et al., 1989 diving T. squamosa 4.14 × 10-4 T. crocea 3.11 × 10-4 SCUBA Sorsogon 1.48 × 105 T. maxima 8.18 × 10-4 Juinio et al., 1989 diving T. squamosa 2.70 × 10-5 T. crocea 1.26 × 10-4 SCUBA Calatagan 1.11 × 105 T. maxima 1.08 × 10-4 Juinio et al., 1989 diving T. squamosa 2.61 × 10-4 T. crocea 5.64 × 10-4 T. maxima 1.48 × 10-4 Lubang Island SCUBA 1.49 × 105 Juinio et al., 1989 diving T. squamosa 1.34 × 10-4 H. hippopus 7.00 × 10-6 T. crocea 2.68 × 10-4 T. derasa 3.60 × 10-5 SCUBA T. gigas 4.00 × 10-7 Ambil Island 2.50 × 105 Juinio et al., 1989 diving T. maxima 4.48 × 10-4 T. squamosa 3.28 × 10-4 H. hippopus 8.00 × 10-6 T. crocea 5.64 × 10-4 T. maxima 1.48 × 10-4 Lubang Island SCUBA 1.49 × 105 Juinio et al., 1989 diving T. squamosa 1.34 × 10-4 H. hippopus 7.00 × 10-6 T. crocea 2.95 × 10-4 SCUBA T. derasa 1.10 × 10-5 Apo Reef 8.80 × 104 Juinio et al., 1989 diving T. maxima 9.43 × 10-4 T. squamosa 1.10 × 10-5 T. crocea 2.70 × 10-5 SCUBA Puerto Galera 1.46 × 105 T. maxima 9.60 × 10-5 Juinio et al., 1989 diving T. squamosa 9.60 × 10-5 T. crocea 6.90 × 10-5 SCUBA Northeast Negros 2.90 × 104 T. maxima 3.40 × 10-5 Juinio et al., 1989 diving T. squamosa 3.40 × 10-5 T. crocea 1.10 × 10-3 T. maxima 9.00 × 10-5 SCUBA El Nido 2.55 × 105 T. squamosa 4.90 × 10-4 Juinio et al., 1989 diving H. hippopus 4.70 × 10-5 H. porcellanus 4.00 × 10-6 T. derasa 6.90 × 10-5 SCUBA Inagauan-Aborlan 4.50 × 104 T. maxima 2.20 × 10-5 Juinio et al., 1989 diving T. squamosa 2.20 × 10-5 T. crocea 1.13 × 10-4 SCUBA Camiguin 2.13 × 105 T. maxima 3.10 × 10-4 Juinio et al., 1989 diving T. squamosa 1.55 × 10-4 Republic of Kiribati T. gigas 2.30 × 10-4 Abemama Atoll Tow 2.86 × 107 T. squamosa 1.15 × 10-5 Munro, 1988 H. hippopus 3.51 × 10-4

108 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. Cont'd.

Sites surveyed Method of Approx. area Species Population density References survey surveyed (m2) (per m2) (population survey) T. gigas 5.49 × 10-5 Abiang Atoll Tow 8.99 × 107 T. squamosa 5.92 × 10-5 Munro, 1988 H. hippopus 2.21 × 10-4 T. gigas 7.68 × 10-5 Maiana Atoll Tow 2.80 × 107 T. squamosa 9.21 × 10-5 Munro, 1988 H. hippopus 5.71 × 10-5 T. gigas 1.89 × 10-5 Tarawa Atoll Tow 2.96 × 107 T. squamosa 2.64 × 10-5 Munro, 1988 H. hippopus 1.69 × 10-5 Samoan Archipelago Samoan Archipelago 5.05 × 105 T. maxima 5.65 × 10-3 Green & Craig, 1999 Singapore T. crocea 7.24 × 10-4 SCUBA Southern Islands 9.76 × 103 T. maxima 1.02 × 10-4 Guest et al., 2007 diving T. squamosa 1.55 × 10-3 Thailand T. crocea 2.44 × 10-1 Lee-Pae Island Tow 6.40 × 103 T. maxima 6.29 × 10-2 Chantrapornsyl et al., T. crocea abundant Mu Ko Surin 1996 Snorkelling T. squamosa scarce National Park T. maxima scarce Vanuatu Port Anatom Snorkelling T.maxima 1.60 × 10-3 Zann & Ayling, 1988 T.maxima 5.00 × 10-3 Inyeug Island Snorkelling Zann & Ayling, 1988 H. hippopus 1.00 × 10-3 Port Patrick Snorkelling T.maxima 1.60 × 10-3 Zann & Ayling, 1988 Lakariata Snorkelling T.maxima 5.00 × 10-4 Zann & Ayling, 1988 T. maxima 3.00 × 10-4 Lelepa Snorkelling T.crocea 3.00 × 10-4 Zann & Ayling, 1988 H. hippopus 3.00 × 10-4 T. maxima 1.00 × 10-3 Cook’s Reef Snorkelling Zann & Ayling, 1988 H. hippopus 2.50 × 10-3 T.maxima 6.00 × 10-4 Pentecost Snorkelling Zann & Ayling, 1988 H. hippopus 9.00 × 10-4 SCUBA Loltong Bay T.maxima 2.00 × 10-3 Zann & Ayling, 1988 diving T. maxima 9.00 × 10-4 Lesalav Bay SCUBA Zann & Ayling, 1988 diving H. hippopus 1.00 × 10-4 Snorkelling & T. maxima 1.30 × 10-3 Reef Island Zann & Ayling, 1988 SCUBA diving H. hippopus 2.30 × 10-3 Snorkelling & T.maxima 2.00 × 10-4 Hog Bay Zann & Ayling, 1988 SCUBA diving H. hippopus 2.00 × 10-4

109 Othman et al.: Distribution and status of giant clams

The ten species of giant clam identifi ed to date vary greatly Chantrapornsyl, S., K. Kittiwattanawong & K. Adulyanukosol, in their distribution and abundance, but all are threatened 1996. Distribution and abundance of giant clam around Lee-Pae by overexploitation and habitat degradation. Even though Island, the Andaman Sea, Thailand. Phuket Marine Biological they are listed by ICUN and international trade is CITES Center Special Publication, 16: 195–200. regulated, giant clam populations continue to decline. Most Clarke, P. J., T. Komatsu, J. D. Bell, F. Lasi, C. P. Oengpepa & clam fi sheries are relatively small scale and community- J. Leqata, 2003. Combined culture of Trochus niloticus and based marine resource management has been proposed as giant clams (Tridacnidae): benefi ts for restocking and farming. Aquaculture 215 the best solution to tackle overharvesting (e.g. Johannes, , : 123–144. 1998). Giant clams are suitable for aquaculture and this CITES, 2004a. Tridacna crocea. AC22 Doc. 10.2 Annex 8c. URL: offers an opportunity to maintain or increase numbers. http://www.cites.org/eng/com/AC/22/E22-10-2-A8c.pdf. However, as emphasised by Gomez & Mingoa-Licuanan CITES, 2004b. Tridacna derasa. AC22 Doc. 10.2 Annex 8d. URL: (2006), community involvement is again vital if restocked http://www.cites.org/eng/com/ac/22/E22-10-2-A8d.pdf. clams are to be safeguarded. CITES, 2004c. Tridacna gigas. AC22 Doc. 10.2 Annex 8e. URL: http://www.cites.org/eng/com/aC/22/E22-10-2-A8e.pdf. CITES, 2004d. Tridacna squamosa. AC22 Doc. 10.2 Annex 8g. ACKNOWLEDGEMENTS URL: www.cites.org/eng/com/AC/22/E22-10-2-A8g.pdf. CITES, 2008. Convention on International Trade in Endangered We would like to thank all the scientists who so generously Species of Wild Fauna and Flora Appendices I, II and III. Pp. shared their observations and data with us, especially Edgardo 32. URL: www.cites.org/eng/app/E-Jul01.pdf. Gomez and Suzanne Licuanan of the Marine Science Institute, Gilbert, A., G. Remoissenet, L. Yan & S. Andrefout, 2006. The University of the Philippines, Diliman; Rick and Nell Braley giant clam Tridacna maxima communities of three French of the Aquasearch Lab, Australia; William A. Newman, Polynesia islands: comparison of their population sizes and Kongkiat Kittiwattanawong and Kanjana Adulyanukosol of structures at early stages of their exploitation. ICES Journal of the Phuket Marine Biological Center. We also thank Reef Marine Science, 63: 1573–1589. Check (www.ReefCheck.org) for providing data on the Gomez, E. D. & S. S. Mingoa-Licuanan, 2006. Achievements and distribution of giant clams which were used in this paper. lessons learnt in restocking giant clams in the Phillippines. Various members of the 2008 Marine Biology class, NUS, Fisheries Research, 80: 46–52. provided input. This research is supported by Singapore’s Green, A., & P. Craig, 1999. 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THE RAFFLES BULLETIN OF ZOOLOGY 2010

THE RAFFLES BULLETIN OF ZOOLOGY 2010 58(1): 113–124 Date of Publication: 28 Feb.2010 © National University of Singapore

INTRASPECIFIC INTERACTIONS ASEMONEA TENUIPES, A LYSSOMANINE JUMPING SPIDER (ARANEAE: SALTICIDAE) FROM SINGAPORE

Yilin Tay Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Republic of Singapore

Daiqin Li Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543, Republic of Singapore College of Life Sciences, Hubei University, Wuhan 430062, Hubei, P. R. China Email: [email protected] (Corresponding author)

ABSTRACT. – The display and courtship behaviour of a Singapore population of Asemonea tenuipes (O. P. –Cambridge, 1869) was studied. This is an iridescent lyssomanine jumping spider and the present study is the fi rst to be carried out on this species under a full-spectrum light. A previous study was carried out on a population of this same species from Sri Lanka, but under light conditions lacking of UV. Findings from the present and the earlier study are, on the whole similar, but there are also some differences that may represent interpopulation variation or may be a consequence of the different lighting conditions. A. tenuipes is most often found on the underside of leaves in mangroves. Colours are sexually dimorphic. Males have bluish-purple iridescence and orange colour on the dorsal abdomen, while females are generally a pale whitish-green. Twenty-fi ve major displays are described. While the intraspecifi c display repertoire of Singapore A. tenuipes was similar to the Sri Lanka population, the context (male-female, male-male and female-female interactions) in which certain displays were performed differed between the two populations. In addition, although zigzag dancing was not observed in the Sri Lankan population, a variation of this display was observed in the Singapore A. tenuipes. Rotated posturing is an aberrant display, observed in A. tenuipes but not other salticid species. Whether this display might function to advertise honestly male quality is discussed. One of the most interesting fi ndings is that males of the Singapore A. tenuipes males often perform prolonged display posturing even when their anterior-median eyes are not aligned with the female. The anterior-median eyes of salticids are the part of the visual system responsible for seeing detail based on high spatial acuity. That A. tenuipes males display in the absence of detail from these eyes suggests that there is unusually strong reliance on chemical cues by this species during courtship.

KEY WORDS. – Spider, Asemonea tenuipes, courtship, agonistic display, Lyssomaninae.

INTRODUCTION The salticid’s two anterior median (principal) eyes are especially large and they face forward. It is these eyes that Jumping spiders (Araneae, Salticidae) are the most diverse are primarily responsible for seeing spatial detail, giving spider family with approximately 5,237 named species from salticids remarkable ability to discriminate between classes 567 genera (Platnick, 2009). Most salticid species appear to be of objects such as prey, mate, and conspeciﬁ c of same sex cursorial hunters that generally adopt stalk-and-leap predatory (Foster, 1982a; Harland & Jackson, 2000, 2002), and the sequences rather than building webs to ensnare their prey secondary (lateral and posterior) eyes primarily aid detection (Forster, 1982a, b). Salticids have complex eyes and vision of long range movement (Land, 1985). The anterior-median based on high spatial acuity (Land, 1969, 1985; Blest et al. eyes are also responsible for colour vision, with their retinas 1990; Land & Nilsson, 2002) and, owing to their exceptional having, besides photoreceptors maximally sensitive to light in eyesight, salticids have distinctive vision-mediated predatory the range visible to the human eye, photoreceptors maximally routines (Jackson & Pollard, 1996; Li & Jackson, 1996) sensitive to UV (Land, 1969; DeVoe, 1975; Yamashita and elaborate vision-mediated courtship and threat displays & Tateda, 1976; Peaslee & Wilson, 1989; Nakamura & (Peckham & Peckham, 1889, 1890, 1894; Crane, 1949a, b; Yamashita, 2000). Recent experimental evidence has shown Drees, 1952; Forster, 1982a; Jackson, 1982). that many salticids reﬂ ect UV light (Lim & Li, 2006a; Li et al., 2008a), and that UV cues are not only necessary for

113 Tay & Li: Intraspecifi c interactions of Asemonea tenuipes agonistic (Lim & Li, 2006b) and courtship displays (Lim controlled-environment laboratory (80–85% RH; 25 ± 1°C; et al., 2007) but also important in female mate choice (Li light regime 12 hrs:12 hrs, lights switched on at 0800 hrs). et al., 2008b; Lim et al., 2008). Although this implies that Spiders were fed fi ve fruit fl ies (Drosophila melanogaster) the intraspecifi c interactions of salticids should be observed once a week. Testing procedure and terminology were under full-spectrum light, the majority of previous studies similar to those in earlier studies of salticids (Jackson have been performed under light conditions without UV & Hallas, 1986b). These included the convention that wavelength. expressions such as “usually” or “generally,” “sometimes” or “occasionally,” and “infrequently” or “rarely” were used Jackson & Blest (1982) proposed that salticids might have to indicate frequencies of occurrence of >80%, 20–80%, or evolved from web-spinning spiders that had poor eyesight <20%, respectively. Voucher specimens have been deposited and that the unique, high-acuity visual system of salticids in the Raffl es Museum of Biodiversity Research (RMBR), evolved in conjunction with ancestral web-building spiders National University of Singapore. becoming specialized spider-eating predators that used aggressive mimicry in the context of invading the webs of Inter- and intrasexual interactions. – Whenever intraspecifi c a wide range of other spiders with diverse kinds of webs. interactions of A. tenuipes were observed, we used a fresh This hypothesis, which was suggested by an initial study leaf (Simpoh Air, Dillenia suffructicosa; length 24 ± 3 cm; of Portia, a genus from the salticid subfamily Spartaeinae, width 13 ± 3 cm). The leaf was clamped to a stand and held led to studies on other salticids, especially other spartaeine horizontally 25 cm above a table top. Two individuals (a genera (see Su et al., 2007). However, comparative data pair of males, a pair of females or one male and one female) from a wider range of salticids is critically important for were introduced onto the leaf at opposing ends (which spider evaluating this hypothesis. introduced fi rst decided at random. All interactions began on the adaxial surface of the leaf but before interactions began, The Spartaeinae appears to be a basal branch in salticid individuals were fi rst placed on opposite sides of the leaf phylogeny (Su et al., 2007), but there is another basal for acclimatization to the experimental set-up (duration: 3 subfamily (the Lyssomaninae) that has been largely neglected min). Subsequently, the individual on the abaxial surface in the literature. This subfamily includes about 120 species in was coaxed, by gently prodding, to the adaxial surface of seven genera, and they are found in tropical and subtropical the leaf to facilitate the start of interactions. As interactions regions of the New World (Chinoscopus and Lyssomanes) never started until a few minutes after the prodding event, and the Old World genera (Asemonea, Goleba, Macopaeus, we considered the spiders that were originally on the abaxial Onomastus and Pandisus) (Platnick, 2009). Lyssomanine eyes surface to have had suffi cient time to acclimatize to the other have unusual characteristics, consistent with this subfamily side of the leaf. Our procedure allowed us to make detailed having branched off early branching in salticid phylogeny and complete observations of progression from behaviour (Blest, 1983, 1985; Blest & Sigmund, 1984; Su et al., 2007). that occurred at a distance to behaviour that occurred while However, details of lyssomanine behaviour are available for closer and the contact. only 10 species from four genera (Crane, 1949a, b; Jackson & Hallas, 1986; Jackson, 1990; Jackson & Macnab, 1991). The leaf set-up we adopted was similar to that used in the previous study on A. tenuipes from Sri Lanka (Jackson & In this study, we examined the intraspecifi c interactions of Macnab, 1991), but lighting conditions were different. In the Asemonea tenuipes (O. P. – Cambridge, 1869), a lyssomanine earlier study, normal fl orescent lighting was used without UV. species known from tropical Asia (specifi cally Andaman However, we used an arrangement of 10 equi-spaced Voltarc Islands, Burma, India, Sri Lanka, Thailand and Singapore; Ultra Light tubes (110W each) held 130 cm above the table Murphy & Murphy, 2000; Platnick, 2009). This species is of was used to provide full-spectrum illumination (300–700 nm) particular interest because the males have iridescent markings. during observations. The rationale for this was recent research The only previous behavioural study on this species was based (Lim & Li, 2006b) showing that the presence of ultraviolet on a population from Peradeniya in Sri Lanka (Jackson & light (300–400 nm) is important for enabling salticids to use Macnab, 1991). Our study is different because we consider UV signals. A total of 36 males and 50 females were used a different population (Singapore) and also because we for these staged encounters. No male and no female spider consider, for the fi rst time, the intraspecifi c interactions of were used more than twice (fi rstly in an intrasexual encounter a lyssomanine species under a full-spectrum light. and, subsequently, in an intersexual encounter). There was a rest period of at least three days between the two tests using any one spider was allowed before a spider was reused in a METHODS different test. All inter- and intrasexual interactions were video recorded and the video recordings were used for thorough Collection and maintenance of spiders. – Our fi eld site was observation of behavioural elements and determination of mangroves at Lim Chu Kang mangroves in Singapore. Our intraspecifi c interaction duration, copulation duration and laboratory observations were based on 143 individuals of palp insertion duration via video playback. Asemonea tenuipes (62 males and 81 females) collected in the fi eld site (all collecting was in the morning, 0700–1000 hrs). Organization of behaviour. – Behavioural patterns occurring The spiders collected were subsequently kept individually during intrasexual interactions were categorized and then in cylindrical cages (diameter: 4.5 cm; height: 6.0 cm) in a further subdivided into stages. On this basis, increasing

114 THE RAFFLES BULLETIN OF ZOOLOGY 2010 intensity of interactions could be discerned. Watch indicates Females were generally pale yellow in colouration (entire the start of an interaction and the spider remains stationary body), with greenish blue or brown spots on the abdomen when this occurs. Distant displays indicate periods during (Figs. 3, 4). The female had short spinnerets, but the male’s which the spider postures with one or a combination of spinnerets were black and distinctive; the posterior pair being behavioural elements: i.e. a raised body, fl exed/bent abdomen elongate and having curled terminal articles. The male’s (mostly for males) or leg postures (hunched and arched-out) abdomen was slimmer than the female’s, but the legs of both when it is far away (more than 8 cm) from the other spider. sexes were pale-yellow, long and slender. Sub-adult males The spider does not advance while it postures. Approach (i.e. the instar one molt before maturity) resembled adult indicates periods when the spider moves towards the other females and they acquired their striking colouration only spider, with or without concurrent displays. Close proximity after they molted and reached sexual maturity. displays occur only after approach. It is similar to distant displaying but also includes zigzag dancing and propulsive Locomotion. – Like most salticids, A. tenuipes walked displays (long leap, strike) that did not result in contact. in a stop-and-go gait (usually moving 10–40 mm before Contact refers to propulsive displays that resulted in the pausing). In general, our observations of locomotion for the collision of spiders. Stage 1: watch and distant displays; Singapore A. tenuipes resembled earlier observations on the Stage 2: approach; Stage 3: close-proximity displays and Sri Lankan A. tenuipes (Jackson & Macnab, 1991). The Sri Stage 4: contact. We interpret progression from lower to Lankan A. tenuipes males often fl exed their abdomens up higher stages as the spiders expressing successively higher while stepping and during pauses between stepping bouts, levels of aggressiveness. and bobbed their abdomens during, or immediately after, each bout of stepping. For the Singapore A. tenuipes, bobbing of For male-female interactions, these categories are slightly the abdomen was observed in all males but the tendency to modifi ed and there are additional categories. Close proximity bob during or immediately after each bout of stepping was displays in male-female interactions refer to the earlier not very pronounced. Bobbing, when it occurred, had the defined displays performed by males during male-male appearance of slow deliberate fl exing down then up (0.5–1s; interactions and also includes rotated posturing, zigzag dance 10–20°) of the abdomen within the sagittal plane. Bobbing and side switching (alternating between two sides of the leaf). occurred regardless of whether or not the spider’s abdomen Premount tap refers to the male tapping the female with his was fl exed up. legs as he attempts to mount the female. These categories were used to construct fl ow charts for female-female, male- Males and females of the Singapore A. tenuipes behaved male and male-female interactions. differently, with the female’s gait being more rapid stop- and-go and based longer stepping distance up to 90 mm between pauses. Females were not observed to bob their OBSERVATIONS abdomens (i.e. they generally kept their abdomens parallel to the substrate). Habitat. – Asemonea tenuipes was found in peripheral vegetation, especially on the undersides of the leaves of Spiders held their palps in front of the faces, thereby partially two common mangrove trees Brugeria and Avicennia. The (females) or entirely (males) hiding their chelicerae. Palps mangrove environment was characterized by a high canopy were never observed to be fully extended or erected during cover and small gaps in the canopy that allowed patches of normal locomotion. While at rest, palps were usually direct sunlight. positioned in close proximity to each other but not touching the substrate. During normal locomotion, palps were Morphology. – Asemonea tenuipes is a small salticid (body sometimes waved (duration about 1s, moving up and down length: adult male 4–5 mm; adult female ca. 4–6 mm). Sexual in matching phase). colour dimorphism is pronounced. Males were brightly coloured, they had stocky red palps (Figs. 1, 2) and the anterior portions of the male’s abdomen had an iridescent RESULTS dark bluish purple band covered (Fig. 5). This band seemed to be without pigment, colour coming instead from iridescence. Behavioural elements. – Inter- and intrasexual interactions The posterior portion of the male’s abdomen had an orange staged on leaves began when one spider “saw” another spider band (covered by orange and brown pigmented scales) with (defi nition: fi xated the gaze of the anterior median eyes on a black tinged tip (Fig. 6). another spider). Interactions ended when at least one spider decamped (Fig. 7) and the other spider failed to watch and The male had two types of scales, granular and clear. Clear follow. If no interaction took place within 30 min, the test scales were shiny and usually iridescent. The characteristic was terminated and considered void. colour of granular scales came from pigments. The male’s iridescent scales were transparent under light transmission Twenty fi ve major elements of behaviour were observed microscopy and they were highly refl ective under incident (Table 1): (1) arched-forward legs (Fig. 8); (2) arched-out light. legs (Fig. 9); (3) charge; (4) elevated legs; (5) fl exed up, fl exed down, and bent abdomen (Figs. 10–12); (6) hunched legs; (7) jerk; (8) long leap; (9) lunge; (10) mounting; (11)

115 Tay & Li: Intraspeciﬁ c interactions of Asemonea tenuipes postmount tap with legs; (12) posturing; (13) premount tap General trends during intraspeciﬁ c interactions. – Male- with legs; (14) propulsive displays; (15) raised cephalothorax; male and female-female interactions were much shorter (16) raised and lowered body (Figs. 13, 14); (17) rotate than male-female interactions, with male-male agonistic abdomen; (18) rotate cephalothorax; (19) rotated posturing; interactions (18 pairs) lasting up to 4.65 min, female-female (20) scrape with palps; (21) strike; (22) stroke; (23) truncated (25 pairs) lasting up to 5.48 min and male-female (37 pairs) leap; (24) waving of elevated legs; and (25) zigzag dance. lasting up to 21 min (time in copula excluded; Table 3). For the contexts in which displays occurred, see Table 2. Median male-male interaction duration was two times longer

Figs. 1–6. Adult Asemonea tenuipes male and female as well as scales from adult male. Male A. tenuipes (1) (dorsal view) possess a bluish-purple iridescence and orange colour on the dorsal abdomen with the former hue also on the lateral carapace (2) (lateral view) with distinctive reddish-brown enlarged palps. Female A. tenuipes (3) (dorsal view) are generally paler in colouration (whitish-green) and (4) possess a short and plump abdomen in contrast to the slim and elongated abdomen of males. (5) Scales were gently removed from the spider with a sticky tape and placed on a glass slide for viewing under light microscope: 40× magniﬁ cation scales on the bluish-purple region of the male anterior dorsal abdomen. The scales are translucent. (6) Light microscope: 40× magniﬁ cation scales on the orange region of the male posterior dorsal abdomen.

116 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. Elements of behaviour (listed alphabetically) during intraspeciﬁ c interactions of Singapore Asemonea tenuipes (adapted from Jackson & Macnab, 1991).

No. Element Description 1 Raised cephalothorax A raised cephalothorax was held higher than normal above the substrate; the anterior end of cephalothorax was often held higher than the posterior. 2 Flexed up, fl exed down, From the cephalothorax, the abdomen was held down c. 20° (fl exed down, Fig. 10), tilted and bent abdomen up 20–80º (fl exed up, Fig. 11), or 20° to either side (bent, Fig. 12). Often, A bent abdomen was also fl exed down or fl exed up. Bent abdomens usually were also lowered. The cephalothorax was always raised when the abdomen was fl exed down. 3 Raised and lowered body A lowered body was held near or on the substrate (Fig. 13). A raised body was held higher than normal above the substrate, with the anterior cephalothorax was occasionally held higher than the posterior. The abdomen was held about parallel to the substrate (Fig. 14). 4 Elevated legs Erect and semi-erect are referred to jointly as elevated legs. Erect legs appeared stiff since all joints were fully extended than in semi-erect legs. Only legs I alone were held erect. Two modal positions were observed. Position 1. Legs were fully extended forward about parallel to the substrate and to each other. In Position 1, legs were always erect. Position 2. Legs extended 20–45° to the side and 10–45° up. In Position 2, legs were either erect or semi-erect. 5 Waving of elevated legs Elevated legs were waved up and down in matching-phase 20–60° at 1–3/s (femoral movement; no alteration of femur-patella joints). Legs were held in Position 1 or Position 2 while elevated waving. 6 Hunched legs Hunched legs (I, or I & II) were held in a plane perpendicular to the sagittal plane of the body or as much as 45° forward (Fig. 20). They were highly fl exed at the femur-patella joints. Tarsi pointed down and sometimes medially. Tarsi were only slightly off or touching the substrate. The cephalothorax was usually raised, with abdomen fl exed down and bent. 7 Arched-out legs Legs I and II were arched-out. Patella and tibia usually remained nearly parallel to the substrate but may angle downward by as much as 45°. Femora of arched-out legs (Fig. 9) angled up c. 45° and forward by no more than 45°. Metatarsus and tarsus extended sharply downward to the substrate. Tarsi I and II were sometimes held c. 1 mm above the substrate; more often, they remained on the substrate. Arched-out legs I were held out to the side 45–90° with legs II being more or less parallel to legs I whether or not they were also arched out. 8 Arched-forward legs Arched-forward legs were similar to arched-out legs except that arched-forward legs I angled forward more or less parallel to the body’s sagittal plane (Fig. 8). Legs II may also be arched-forward and held about parallel to legs I. A more extreme version of arched- forward posturing with femora more or less perpendicularly up is commonly adopted. 9 Posturing A spider postured by standing or stepping while holding its legs arched-out (arched-out posturing), arched-forward (arched-forward posturing), elevated (elevated posturing), or hunched (hunched posturing). 10 Rotate cephalothorax A spider tilted its cephalothorax over to the left or right so that the sagittal plane of the cephalothorax was c. 45° to the substrate when rotating. The spider held its abdomen normally aligned to the substrate (i.e. cephalothorax’s and abdomen’s sagittal planes were c. 45° to each other). 11 Rotated posturing A spider held its cephalothorax rotated and abdomen raised for the two types of rotated posturing. When arched rotated posturing, legs I (or I & II) on the other side of the cephalothorax were arched-forward. When erect rotated posturing, these legs were erect in Position 1. The other side of the spider’s cephalothorax was on or very near the substrate. Legs I and II on this side extended forward, legs I sometimes being erect but on the substrate. Switching back and forth between arched and erect rotated posturing was very common. 12 Jerk A spider jerked by suddenly and rapidly moving its body up then down 2–3 mm (cycle duration less than 0.1 s). 13 Zigzag dance A spider zigzag danced by stepping sideways and spiralling towards its partner, with legs raised. Stepping was deliberate and smooth. The abdomen was bent away from the side toward which it stepped while dancing. 14 Strike The spider held its legs I elevated just before striking. A strike was executed by very rapidly stepping 20–50 mm toward the other spider, and simultaneously, bringing legs I rapidly and forcefully down and forward onto the substrate or the other spider. 15 Charge In charging, a spider suddenly and rapidly ran 20–40 mm forward, then suddenly stopped 10–20 mm in front of the other spider.

117 Tay & Li: Intraspeciﬁ c interactions of Asemonea tenuipes

Table 1. Cont'd.

No. Element Description

16 Lunge A spider lunged by suddenly and rapidly moved its body forward 3–4 mm by extending its rear legs. A lunging spider did not leap (i.e. tarsi of rear legs did not leave the substrate) but always moved its body back to its original position immediately after lunging. A spider arched-out or elevated postured while it lunged and may contact the other spider with its legs during the forward motion of the lunge. A spider sometimes charged immediately before it lunged. 17 Truncated leap A truncated leap was made by suddenly leaping 2–5 mm toward the other spider, but making no contact with the other spider. A spider might make as many as fi ve truncated leaps in rapid succession, but despite the number of leaps it made, a truncated leaping spider usually stopped only 2–5 mm away from its rival. 18 Long leap A spider executed long leaps by suddenly propelling itself forward 20–80 mm and either contacting (mostly face-on), or landing within 5 mm of, the other spider. 19 Propulsive displays Striking, charging, lunging, truncated leaps, and long leaps, each of which involved sudden and rapid forward locomotion of the spider, are termed “propulsive displays”. Propulsive displays were performed intermittently and seemingly unpredictably, the spider usually turning and running away immediately afterwards. 20 Premount tap with legs With legs I up and down (ca. 2/s; 1–2 mm; femoral; alternating phase; bout lengths 1–2 s), males premount tapped over a female repeatedly, bringing their tarsi into contact with her carapace or, less often, her legs I, palps, chelicerae, or abdomen. 21 Mounting Males mounted by walking over females, usually premount tapping as they did so and usually with two spiders face-to-face. 22 Postmount tap with legs Males fl exed legs I more and more as they moved over females. When a female faces him, then the male’s femur-patella and tibia-metatarsus joints were fl exed 90–135° by the time his cephalothorax was over her anterior abdomen. Once mounted, a male tapped the female’s abdomen by moving his highly fl exed legs I up and down in the same fashion as during premount tapping, except that phasing was now usually matching. By doing so, the male lifts her abdomen towards him such that her abdomen is now fl exed up 70–80°. 23 Stroke. A male leaned to one side and stroked with the opposite leg I or vice versa; he stroked by moving tarsi of legs repeatedly across the female’s ventral abdomen (1–3 mm; 1–2/s) with tarsi not fl exed up from metatarsi. 24 Rotate abdomen A female’s abdomen rotated to the left or right while a male stroked, so that the ventral surface of her abdomen was brought closer to the male’s stroking leg. 25 Scrape with palps A male moved his palps back and forth across the ventral surface of a female’s rotated abdomen in the vicinity of her epigynum before engaging his palps and starting to copulate. Males often continued to stroke while scraping with palps.

than median female-female interaction. Median male-female male-male individual interactions ending at stage 2. That interaction duration when the female was receptive (i.e. is, a larger proportion of male-male interactions escalated copulation resulted) and when the female was unreceptive to the more intense stages (i.e. stage 3 and 4). Contact was was similar (Table 3). No instances of cannibalism were rare in male-male and in female-female interactions (5.6% observed for any of the interactions. for males and 14% for females).

Intrasexual interactions (Figs. 15 & 16). – In 8% of the Male-male agonistic interactions began when one or both male-male and 12% of the female-female interactions, the spiders started to display (raised bodies, arched-out or spiders apparently ignored each other throughout the test. hunched legs and fl exed-up abdomens, abdomens sometimes During intrasexual interactions, spiders usually postured also bent) at about 10–15 cm away. Both males then slowly while standing or while repeatedly stepping toward then zigzag danced towards each other until they were about 1–3 away from each other. The most common sequence of body lengths apart. Males zigzag danced by adopting an behaviour for females was to watch and display for a few arched-out posture and fl exing-up their abdomen (60–80°) seconds before decamping. For males, however, it was while stepping sideways. Stepping sideways involves a left- to watch and posture, followed by a zigzag dance before right sideways motion in a semi-circle arc that progressively decamping. When a male zigzag dances, he was mirrored by closes the distance from his partner. Abdomens were bent his test partner. About 60% of the observed female-female away from the direction of stepping and the degree of interactions ended at stage 2 compared to about 39% of the abdomen fl exion increased with decreasing distance from the

118 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 2. Types of interactions during which different displays (listed alphabetically) were performed by Singapore Asemonea tenuipes (A). X: did not to occur.

Male-female* Male-female** Male-male Female-female Arched-forward posturing A X A1 X Arched-out posturing A A A A Charge X A X A Elevated posturing A A1 A1 X Position 1 A A1 A1 X Position 2 A A1 A1 X Erect A A1 X X Semi-erect A1 X A1 X Flickering of elevated legs X X X X Flickering of erect palps X X X X Hunched posturing X A A A Jerk A X X X Long Leap X X A A Lunge X A X2 X2 Postmount tap with legs A X X X Premount tap with legs A X X X Rotated posturing A X X X Scrape with legs X X X X Scrape with palps A X X X Strike X A1 A1 A Stroke A X X X Truncated leap X X2 X A Twitch abdomen A A A A Waving of elevated legs A1 A A1 X Zigzag dance A1 X A1 A1

*Displays performed by males during male-female interactions. **Displays performed by females during male-female interactions. 1 Observed in this study but not in the Sri Lankan population (same species) by Jackson & Macnab (1991). 2 Observed by Jackson & Macnab (1991) but not in this study.

Table 3. Durations (sec) of intraspeciﬁ c interactions (see text).

Male-female Male-female Male-male Female-female (female receptive)* (female unreceptive) Median 158 165 62 38 Maximum 1215 1327 279 329 Minimum 21 51 13 5 No. 8 29 18 25

*Interaction duration before copulation. other spider. The interaction usually ended with one male raised body, ﬂ exed-up abdomens, and hunched legs. Females suddenly decamping by running off. There were two instances tended to not ﬂ ex their abdomens as often as males and, of Contact (strike or long leap at the other male). when they did, the abdomen was raised 20–50° (60–80% for males). Instead of zigzag dancing to approach another Although the beginnings of female-female and male- female, females usually stayed still or approached by rapid male agonistic interactions were similar, there were some stepping. Females usually made contact by charging and interesting differences. The distant displays of males were they adopted especially pronounced hunched posture (raised

119 Tay & Li: Intraspeciﬁ c interactions of Asemonea tenuipes

Table 4. Data from copulations (mean ± SE). to the left or right and usually engaged their palps soon after mounting. A male usually backed away when the female’s Asemonea tenuipes abdomen did not rotate. Males sometimes mounted females No. of pairs that copulated 8 without initiating palp engagement and later decamped No. of copulations 18 voluntarily before the female became active.

Copulation duration 2.1 ± 0.26 min Copulation. – There were eight pairs that copulated and Palp engagement duration 1.8 ± 0.23 min copulation always took place on the leaf underside. Data on copulation duration and palp engagement duration are presented in Table 4. While copulating, the female usually body and slightly flexed-up abdomen) before charging. had her abdomen raised 20–45° and rotated 45–90°, with Occasionally, the other spider decamped just before a female her cephalothorax lowered and resting on the substrate. charged. Most intrasexual interactions ended after the fi rst Copulatory posture was similar to that described in the instance of decamping. Sri Lanka population directions [copulatory posture No. 2, (Gerhardt & Kaestner, 1938); male standing over and leaning Intersexual interactions (i.e. male-female interactions) across the female, spiders facing in opposite directions]. (Fig. 17). – The primary behaviour of males was to posture while standing, while stepping nearer or while stepping away Unlike many other species, and unlike the Sri Lanka from a female. Females, on the other hand, usually watched Asemonea tenuipes, copulations did not end when the female displaying males for a few seconds before decamping. Males became active and decamped but, instead, it usually ended were always the fi rst to initiate an interaction (watch, distant because males that decamped fi rst. The males usually quickly displays and approach), after which, 76% proceeded to move away from the female while the female remained still close-proximity displays. Rotated posturing was the most in her characteristic copulatory posture. Eight pairs copulated, common close-proximity display (86%) performed by males with three copulating only once and fi ve copulating two to and it occurred in all interactions that resulted in copulation. four times. In these cases, after the males decamped, they About 30% of the interactions ended after close proximity attempted to court the female again by performing close displays when males decamped. Another 38% proceeded from proximity displays such as rotated posturing before mounting close proximity displays to embrace. The sequence of events her again. In the subsequent copulation for multiple mating, after embrace was varied considerably, with 43% of these copulating males sometimes switched over to a different palp proceeding to mount. Some males then failed to initiate and from the one used previously. only 11% of all interactions resulted in copulation.

Males usually approached and backed away repeatedly from DISCUSSION females that remained more or less stationary, often switching repeatedly from rotated to arched-up posturing. They also Comparison of fi ndings from this study and the earlier zigzag danced (with abdomen fl exed up, stepping sideways study. – On the whole, the size and complexity of the while progressively moving closer to the female). Regardless display repertoire of the Singapore A. tenuipes observed which side of the leaf the female was on (usually underside under full-spectrum light largely resembles that of the Sri of the leaf), males often alternated between two sides of Lanka population observed under light conditions lacking the leaves while courting a female He usually remained of UV light (Jackson & Macnab, 1991). However, there motionless on the side of the leaf without the female but were some differences and we need fi rst to consider whether posture once he returned to the side with the female and, in having adopted somewhat different defi nitions for elements most cases, he started rotated posturing if the female was of behavior might have been important. Zigzag dancing is an watching. Usually, males stopped posturing altogether when example. Jackson & Macnab (1991) used the term ‘zigzag losing sight of females that moved away. dance’ for male courtship behaviour seen for other salticids (Jackson & Pollard, 1997), including other lyssomanine Females always initiated contact in intersexual interactions. species. It referred to specifi cally instances of the male Females usually attacked males by charging or, rarely, stepping sideways and spiraling towards its partner in by striking or lunging during close-proximity displays or conjunction with other courtship display (e.g. erect forelegs). while males tried to embrace them. Although intrasexual For the Singapore population of A. tenuipes, we observed the int±eractions generally ended as soon as one spider decamped, spider perform sideways stepping in same-sex interactions sometimes males followed again immediately after the female while spiraling towards its partner, but without the spider or they themselves decamped, with the male displaying again doing this in conjunction with other display behavior such if the female stopped. However, he soon ceased to follow as erect legs. With defi nitions being somewhat different, if she did not stop. it is not so simple to say the use of zigzag dancing is unique to the Singapore A. tenuipes. However, terminology Mounting and postmount behaviour. – While attempting to notwithstanding, the zigzag approaches reported here for mount females, males switched from an arched rotated posture same-sex interactions were not reported in the study on the Sri to erect rotated posturing (Position 1). The male premount Lanka population, a spiraling stepping pattern in the absence tapped the female as he tried to mount. Males tended to lean of other display behaviour was not reported in the study on

120 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Figs. 7–14. (7) Left: female; Right: male. Male decamped just after performing a close proximity display. (8) Male (facing left) displays with arched-forward legs. (9) Male (facing to right) displays with raised body, arched-out legs and fl exed-up abdomen. (10) Side view of male: displays with fl exed-down abdomen. (11) Female: bent abdomen to her right. (12) Side view of male: displays with highly fl exed-up abdomen and arched-forward legs. 17, 18. Raised and lowered body postures. (13) Female (side view, facing to left) with lowered body and raised cephalothorax. (14) Male (side view, facing to left) with raised body parallel to substrate.

121 Tay & Li: Intraspecifi c interactions of Asemonea tenuipes the Sri Lanka population. Unfortunately, the absence of a report of this behaviour cannot so simply be taken as being evidence that this behaviour did not occur. For example, taking a spiraling path might be less conspicuous than the display-associated zigzag dancing during the courtship rituals of many salticid species and that might have led to it being overlooked. This highlights a diffi culty with basing comparisons on what is and in not reported in the literature. Statements about what was observed and recorded can be made with considerable confi dence, but concluding that something does not occur on the basis of it not having been reported is usually subject to considerably less confi dence. It would be of interest to repeat the study on the Sri Lanka A. tenuipes now that we have the study on the Singapore A. tenuipes to inform us of what to look for.

On the whole, the present study of the Singapore A. tenuipes has revealed new elements of behaviour more often than there having been elements of behaviour recorded for the Sri Lanka A. tenuipes that were not observed for the Singapore A. tenuipes (Table 1). This suggests that full-spectrum light made the spiders inclined to perform behaviour that was not performed when UV was lacking. It is particularly striking that almost all the new elements observed under full-spectrum Fig. 16. Summary of interactions by 36 individuals (18 pairings) light were leg postures while the elements present only in between adult males on leaf. Distant displays predominantly refer to raised body, ﬂ exed/bent abdomen and leg postures (hunched and the absence of UV were propulsive displays (truncated leap arched-out). Approach includes both with and without concurrent and lunge). An intriguing possibility is that, as showed in displays. Close proximity displays for males are similar to above deﬁ ned displays but also include zigzag dance and propulsive displays (long leap, strike) that did not result in contact unlike in Contact.

Fig. 15. Summary of interactions by 50 individuals (25 pairings) between adult females on leaf. Distant displays predominantly refer to raised body and leg postures (hunched and arched-out). Approach includes both with and without concurrent displays. Close proximity Fig. 17. Summary of 37 interactions between adult males and females displays for females are similar to above defi ned displays but also on leaf. WDA is the summation of the Watch, Distant displays include propulsive displays (truncated leap, charge) that did not and Approach categories of the intra-gender specifi c interactions. result in contact unlike in Contact. Unbracketed numbers refers Close proximity displays for males include raised body, fl exed/ to the number of individuals that proceeded to the next category bent abdomen and leg postures (hunched and arched-out), rotated while bracketed numbers refer to the number of interactions that posturing, zigzag dance and side switching. Females predominantly proceeded after the fi rst decamp. attack males by charging or rarely, by striking or lunging.

122 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Cosmophasis (Lim & Li, 2006b; Lim, 2007), the presence LITERATURE CITED or absence of UV light has a strong infl uence on the level of aggressiveness exhibited during interactions. Blest, A. D., 1983. Ultrastructure of secondary retinae of primitive and advance jumping spiders (Araneae: Salticidae). Rotated posturing. – Rotated posturing is of particular Zoomorphology, 102: 125–141. interest because, although the rest of the repertoire of A. Blest, A. D., 1985. The fi ne structure of spider photoreceptors tenuipes consists of behaviour similar to behaviour reported in relation to function. In: Barth, F. G. (ed.), Neurobiology for other salticids, rotated posturing has never been recorded of Arachnids. Springer, Berlin Heidelberg, New York. Pp. for any other salticid species. It was observed for both the 79–102. Singapore and the Sri Lanka A. tenuipes and, observing A. Blest, A. D. & C. Sigmund, 1984. Retinal mosaics of the principal tenuipes males in the rotated posture, it is easy to suggest as eyes of two primitive jumping spiders, Yaginumantis and a hypothesis that males of low quality would have diffi culty Lyssomanes: clues to the evolution of salticid vision. Proceedings of the Royal Society of London B 211 sustaining this posture (Jackson & Macnab, 1991). Testing , : 111–125. this hypothesis, however, will require experiments that have Blest, A. D., D. C. O’Carroll & M. Carter, 1990. Comparative not yet been carried out, and the hypothesis will probably ultrastructure of Layer I receptor mosaics in principal eyes of need refi nement. Perhaps simply the ability to adopt this jumping spiders: the evolution of regular arrays of light guides. Cell and Tissue Research, 262: 445–460. posture is not what is important. After all, this unusual posture preceded all observed copulations. However, for Crane, J., 1949a, Comparative biology of salticid spiders at Rancho the female, what matters might be details concerning how Grande, Venezuela. Part III. Systematics and behavior in representative species. Zoologica, 34: 31–52. the male expresses this display, with these details varying with male quality. Crane, J., 1949b, Comparative biology of salticid spiders at Rancho Grande, Venezuela. Part IV. An analysis of display. Zoologica, 34: 159–214. Displaying by males when no other spider is in view. – The typical pattern in salticids is for males, when they encounter DeVoe, R. D., 1975. Ultraviolet and green receptors in principal females in nests, to adopt displays that do not depend on eyes of jumping spiders. Journal of General Physiology, 66: vision (Jackson & Pollard, 1997). However, when they 193–207. encounter females out in the open, they typically display Drees, O., 1952. Untersuchungen über die angeborenen specifi cally at a female that is in sight (Crane, 1949a; Drees, Verhaltensweisen bei Springspinnen (Salticidae). Zeitschrift 1952). Lyssomanines may be different. In the earlier study für Tierpsychologie, 9: 169–207. (Jackson & Macnab, 1991), the males of three lyssomanine Forster, L. M., 1982a. Visual communication in jumping spiders species, A. tenuipes, Goleba puella and Lyssomanes viridis, (Salticidae). In: Witt, P. N. & J. S. Rovner (eds.), Spider sometimes initiated courtship displaying before they made Communication: Mechanisms and Ecological Signifi cance. Princeton University Press, Princeton, New Jersey. Pp. eye contact with a female, and males readily held display 161–212. postures during the interaction even at times even when a female was not within his line of sight. On the whole, the Forster, L. M., 1982b. Vision and prey-catching strategies in jumping observations in the present study of the Singapore A. tenuipes spiders. American Scientist, 70: 165–175. are consistent. The Singapore A. tenuipes males also held Gerhardt, U. & A. Kaestner, 1938. Araneae. In: Kukenthal, W.G. & their posture for up to a minute even when there was no T. Krumbach (eds.), Handbuch de Zoologie, Vol. 3. De Gruyter, direct eye-contact with females during interactions or after a Berlin. Pp. 394–656. female decamped. A hypothesis currently being investigated Harland, D. P. & R. R. Jackson, 2000. Cues by which Portia is that lyssomanine males rely especially strongly on olfactory fimbriata, an araneophagic jumping spider, distinguishes pheromones from females. jumping-spider prey from other prey. Journal of Experimental Biology, 203: 3485–3494. Harland, D. P. & R. R. Jackson, 2002. Infl uence of cues from ACKNOWLEDGMENTS anterior medial eyes of virtual prey on Portia fi mbriata, an araneophagic jumping spider. Journal of Experimental Biology, 205: 1861–1868. We are grateful to Poh Moi Goh for providing the fruit fl ies. Thanks to Wong Teck Min, Choo Yuan Ting, Eunice J. M. Jackson, R. R., 1982. The behavior of communicating in jumping Tan, Victor Y. S. Lim and Jeremy R. W. Woon for their spiders (Salticidae). In: Witt, P. N. & J.S. Rovner, eds.), Spider Communication: Mechanisms and Ecological Signifi cance. assistance in the collection of A. tenuipes. Comments and Princeton University Press, Princeton, New Jersey. Pp. suggestions from Robert R. Jackson and Matthew L. M. Lim 213–247. greatly improved the manuscript. This work was supported Jackson, R. R., 1990. Comparative study of lyssomanine jumping by grant to D. Li from the Ministry of Education (MOE) spiders (Araneae: Salticidae): silk use and predatory behaviour Academic Research Fund (AcRF: R-154-000-199-112 and of Asemonea, Goleba, Lyssomanes, and Onomastus sp. n. New R-154-000-355-112). Zealand Journal of Zoology, 17: 1–6. Jackson, R. R. & A. D. Blest, 1982. The biology of Portia fi mbriata, a web-building jumping spider (Araneae: Salticidae) from Queensland: utilization of webs and predatory versatility. Journal of Zoology, London, 196: 255–293.

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Jackson, R. R. & S. E. A. Hallas, 1986. A comparative study of Lim, M. L. M. & D. Li, 2006a. Extreme ultraviolet sexual Old and New World Lyssomanines (Araneae, Salticidae): dimorphism in jumping spiders (Araneae: Salticidae). Biological utilization of silk and predatory behavior of Asemonea tenuipes Journal of the Linnean Society, 89: 397–406. and Lyssomanes viridis. New Zealand Journal of Zoology, 13: Lim, M. L. M. & D. Li, 2006b. Behavioral evidence of ultraviolet 543–551. sensitivity in jumping spiders (Araneae: Salticidae). Journal of Jackson, R. R. & A. M. Macnab, 1991. Comparative study of the Comparative Physiology A, 192: 871–878. display and mating behavior of lyssomanine jumping spiders Lim, M. L. M., M. F. Land & D. Li, 2007. Sex-specifi c UV and (Araneae: Salticidae), especially Asemonea tenuipes, Goleba fl uorescence signals in jumping spiders. Science, 315: 481. puella, and Lyssomanes viridis. New Zealand Journal of Zoology, 18: 1–23. Lim, M. L. M., J. J. Li & D. Li, 2008. Effect of UV-refl ecting markings on female mate -choice decisions in Cosmophasis Jackson, R. R. & S. D. Pollard, 1996. Predatory behavior of jumping umbratica, a jumping spider from Singapore. Behavioral spiders. Annual Review of Entomology, 41: 287–308. Ecology, 19: 61–66. Jackson, R. R. & S. D. Pollard, 1997. Jumping spider mating Murphy, F. & J. Murphy, 2000. An Introduction to the Spiders of strategies: sex among cannibals in and out of webs. In Choe, South East Asia. Malaysian Nature Society. United Selangor J. & B. Crespi (eds.), Mating Systems in Insects and Arachnids. Press, Sdn. Bhd. Cambridge University Press, Cambridge. Pp. 340–351. Nakamura, T. & S. Yamashita, 2000. Learning and discrimination Land, M. F., 1969. Structure of the retinae of the principal eyes of of colored papers in jumping spiders (Araneae: Salticidae). jumping spiders (Salticidae: Dendryphantinae) in relation to Journal of Comparative Physiology A, 186: 897–901 visual optics. Journal of Experimental Biology, 51: 443–470. Peaslee, A. G. & G. Wilson, 1989. Spectral sensitivity in jumping Land, M. F., 1985. The morphology and optics of spider eyes. In spiders (Araneae: Salticidae). Journal of Comparative Bath, F.G. (ed.), Neurobiology of Arachnids. Springer, Berlin Physiology A, 164: 359–363. Heidelberg, New York. Pp. 53–78. Peckham, G. W. & E. G. Peckham, 1889. Observations on sexual Land, M. F. & D. E. Nilsson, 2002. Animal Eyes. Oxford University selection in spiders of the family Attidae. Occasional Papers Press, Oxford. of the Wisconsin Natural History Society, 1: 3–60. Li, D. & R. R. Jackson, 1996. Prey preferences of Portia fi mbriata, Peckham, G. W. & E. G. Peckham, 1890. Additional observations an araneophagic, web-building jumping spider (Araneae: in sexual selection in spider of the family Attidae. Occasional Salticidae) from Queensland. Journal of Insect Behavior, 9: Papers of the Wisconsin Natural History Society, 1: 117–151. 613–642. Peckham, G. W. & E. G. Peckham, 1894. The sense of sight in Li, J. J., M. L. M. Lim, Z. T. Zhang, Q. Q. Liu, F. X. Liu, J. Chen spiders with some observations of the color sense. Transactions & D. Li, 2008a. Sexual dichromatism and male colour morph of the Wisconsin Academy of Sciences, Arts and Letters, 10: in ultraviolet-B refl ectance in two populations of the jumping 231–261. spider Phintella vittata (Araneae: Salticidae) from tropic China. Biological Journal of the Linnean Society, 94: 7–20. Platnick, N. I., 2009. The World Spider Catalog, Version 10.0. American Museum of Natural History, online at http://research. Li, J. J., Z.T. Zhang, F. X. Liu, Q. Q. Liu, J. Chen, M. L. M. Lim amnh.org/entomology/spiders/catalog/index.html & D. Li, 2008b. UVB-based mate choice cues used by females of the jumping spider Phintella vittata. Current Biology, 18: Su, K. F. Y., R. Meier, R. R., Jackson, D. P. Harland & D. Li, 699–703. 2007. Convergent evolution of eye ultrastructure and divergent evolution of vision-mediated predatory behaviour in jumping Lim, M. L. M., 2007. UV Vision in Jumping Spiders (Araneae: spiders. Journal of Evolutionary Biology, 20: 1478–1489. Salticidae): Sexual Selection and Foraging Behaviour. PhD thesis, National University of Singapore. 262 pp. Yamashita, S. & H. Tateda, 1976. Spectral sensitivities of jumping spider eyes. Journal of Comparative Physiology A, 105: 29–41.

124 THE RAFFLES BULLETIN OF ZOOLOGY 2010

DIEL VARIATIONS AND DIVERSITY OF FISH COMMUNITIES ALONG THE UNRECLAIMED SHALLOW COASTAL HABITATS OF CHANGI POINT BEACH, SINGAPORE

J. T. B. Kwik, P. Z. Chen & P. K. L. Ng Systematics and Ecology Laboratory, Department of Biological Sciences, 14 Science Drive 4, Singapore 117543, Republic of Singapore Email: [email protected] (JTBK; Corresponding author)

T. M. Sin Tropical Marine Science Institute, National University of Singapore, 14 Kent Ridge Road, Singapore 119223, Republic of Singapore

ABSTRACT. – Shallow coastal habitats function as nursery, feeding and breeding grounds for many marine and estuarine fi shes. Even though fi sh diversity in Southeast Asia is high, there is a paucity of information with regards to the fi sh ecology of shallow coastal habitats in Singapore. To investigate the possible function of Changi Point Beach (an unreclaimed shallow coastal habitat) and the diversity of the fi sh community inhabiting this area, monthly nocturnal and diurnal samplings were performed. Results indicate that, although impacted, Changi Point Beach appears to be a nursery area and supports a large diversity of fi sh species. This includes several species which are economically important as a food resource. Changi beach is also a popular recreational area, which is frequented by the local citizenry as well as tourists. With increasing coastal habitat degradation due to anthropogenic activities, it is important to conserve these habitats for the benefi t of both the immediate fi sh community as well as for maintaining fi sh diversity in Singapore.

KEY WORDS. – Fish community, Changi, subtidal, diversity, conservation.

INTRODUCTION (Robertson & Duke, 1990; Santos & Nash, 1995), 2) between different substratum types (Chong et al., 1990; Jenkins & Worldwide, the icthyofaunal ecology of different shallow Wheatley, 1998; Lugendo et al., 2006) and 3) with different coastal habitats has been relatively well studied. These environmental variables such as diel and tidal rhythms (Jaafar productive habitats are important to numerous coastal fi sh et al., 2004). Given the complex dynamics of different species at various life stages (Rountree & Able, 1997; shallow coastal habitats (Blaber, 1997), an understanding of Jenkins & Wheatley, 1998; Hajisamae & Chou, 2003; fi sh ecology in Singapore is needed before a comprehensive Hajisamae et al., 2003; Jaafar et al., 2004; Unsworth et al.., model of a shallow coastal ecosystem can be developed. 2006; Crona & Rönnbäck, 2007; Kopp et al., 2007). Besides being permanent habitats for certain smaller fi sh species Tropical coastal ecosystems in Southeast Asia are rich in such as Sillago sihama, Ambassis kopsii and Stolephorus aquatic resources (Blaber, 1997; Chou, 1996), but little indicus (Hajisamae & Chou, 2003), these habitats are widely reserach on fi sh ecology (Pinto, 1988; Chong et al., 1990; recognised to function as nursery grounds (Parrish, 1989; Poovachiranon & Satapoomin, 1994; Jaafar et al., 2004) Blaber et al., 1995; Paterson & Whitfi eld, 2000; Hajisamae has been conducted regionally, with Singapore particularly & Chou, 2003; Crona & Rönnbäck, 2007), feeding (Heck poorly studied (Hajisamae et al., 2003; Hajisamae & Chou, & Orth, 1980; Chong et al., 1990) and refuge sites (Jenkins 2003; Jaafar et al., 2004). Due to rapid development, a tenth & Wheatley, 1998; Paterson & Whitfi eld, 2000) for the of Singapore’s 660km2 total lands mass has been reclaimed, larvae and juveniles of many fi sh species (e.g. Sillaginodes mainly to the southern and northeastern coast of the island. punctata and Acanthaluteres spp.). Shallow coastal areas Shallow littoral habitats, which were once a common feature are also hunting grounds for larger piscivorous nocturnal of Singapore coasts, cover only 0.5% (approximately 3.3km2) fi sh species that patrol during high tide searching for prey of the land area (Jaafar et al., 2004). The shallow coastal (Parrish, 1989; Rountree & Able, 1997; Nagelkerken et habitat of Changi Point Beach is presently unaltered by al.., 2000). It is known that fi sh abundance and diversity in reclamation projects (Chou L.M., pers. comm.). To date, shallow coastal habitats can vary 1) spatially and temporally no intensive studies have been conducted on Changi Point

125 Kwik et al.: Changi beach ﬁ sh diel variations and diversity

Beach, with only visual observations made in 1994 (Loo to the laboratory, and preserved in 70% alcohol. et al., 1994) and in 2005 (Goh, 2005). Results from these two researchers indicate a change in coastal vegetative Laboratory analysis. – In the laboratory all fi sh were sorted species over the last few years and suggested that a change and identifi ed. The abundance and standard lengths (SL) for in the fi sh community of Changi Point Beach might have each species was recorded. For more abundant fi sh species, a occurred, as found in the seagrass beds in Australia and the random sub-sample of 20 specimens was measured. Vernier Mediterranean (Young, 1981; Abal et al., 1998; Guidetti & callipers (± 0.01 mm) were used to measure small specimens Bussotti, 2000). under a SL of 150 mm, while a 300 mm ruler (± 0.5 mm) was used for specimens larger than 150 mm. This paper is a preliminary investigation in an attempt to describe (a) species composition, (b) density, (c) diel Data analysis. – All fi sh densities were expressed as relative variations in the icthyofaunal community and (c) the abundances, i.e. as percentages of total fi sh catch. Mean possible function of Changi Point Beach’s shallow coastal richness of species per sampling occasion was calculated habitat for the more common species. In Singapore’s ever as the average of the total number of species found in three changing coastal environment, it is important to provide a replicate catches performed on each sampling occasion. The baseline for the species found in this unreclaimed area for Shannon-Wiener diversity index of was also calculated for future reference. each sampling occasion (Pielou, 1975).

Information of fi sh maturation size for each species was MATERIALS AND METHODS determined (based on literature) and the fi shes were classifi ed into three size groups, i.e. juvenile (a third or less of the Study site. – The shallow coastal habitat of Changi Point maximum length of the species), subadult (more than a third Beach (CPB) is located on the northeastern coast of Singapore to two-thirds of the maximum length of the species) and (1°23'18'N 104°0'50'E) at the entrance of Sungei Changi and adult (more than two-thirds of the maximum length of the exposed to the Straits of Singapore (Fig. 1). CPB is one of species). Classifi cation of size class in this way was tested the few remaining unreclaimed shallow coastal habitats of and confi rmed by Nagelkerken & van der Velde (2004). Singapore and stretches approximately 1,500 m. CPB has a Two-sample t-Tests for independent samples were used to mixed sandy and muddy bottom with a patchy distribution compare fi sh abundance and species diversity between day of Halophila ovalis (Hydrocharitacea) and Ulva lactuca and night (Ulvaceae) at the subtidal zone. During low tide, the gradient at CPB is gentle (approx. 12o) and the beach generally consists of coarse sand at the supra-littoral zone with gradually fi ner RESULTS sand and mud towards the sublittoral zone. Species composition and density. – A total of 4,062 fi sh Fish collection. – During spring tides, beach seines (20 m belonging to 75 fi sh species and 45 families were collected at x 1.7 m x 5 mm mesh and 0.5 m cod end) were performed CPB during the three months. Of the total catch, most were nocturnally and diurnally every four weeks during a three juveniles and adults of small-sized fi sh species. Engraulids month period from October 2006 to Dec.2006. Spring tides were the most abundant family making up 24.86% of the were targeted as it was only possible to seine over the total catch followed by Teraponids (13.61%), Monacanthids seagrass beds during this time when low tides were 0.5 m (11.2%), Syngnathids (11.18%) and Apogonids (7.63%). below standard datum, this approach also avoided any tidal Among the icthyofanual species, Thryssa spp (Engraulididae) bias. During each sampling period, three haphazard 40 m (24.84%), Pelates quadrilineatus (Terapontidae) (12.04%), seine tows were performed, covering 800 m2 per haul. All Monacanthus chinensis (Monacanthidae) (11.1%), fi sh specimens collected were immediately iced, transported Hippichthys cyanospilus (Syngnathidae) (11.05%) and Choerodon oligacanthus (Labridae) (4.73%) were the most widely occurring species (Table 1). The other species made up less than 4% of the total catch, with many species represented by a single individual only. Based on all catches, a Shannon-Weiner’s diversity index, H’, of 2.79 was calculated for CPB.

Comparison of community between day and night. – Even though more fi sh were collected during nocturnal sampling (51.8%) as compared to diurnal sampling (48.2%), an unpaired t-Test (df = 17) indicated that there was no signifi cant difference in fi sh abundances between nocturnal and diurnal communities at CPB. Similarly, there was no signifi cant difference in total species richness between day Fig. 1. Map of study area showing site by name (CPB: Changi and night. During the entire three month period, one third (25 Point Beach) out of 75) of the species were found every month at CPB.

126 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. Relative abundance (%) of ﬁ sh species caught at Changi Beach Point between the months of Oct. and Dec.2006 (species marked with a * and in bold denote the ﬁ ve most abundant species).

Family Species Relative abundance (%) Ambassidae Ambassis kopsii 0.24 Apogonidae Apogon hyalosoma 0.98 Apogon margaritophorus 3.49 Apogon quadrifasciatus 2.90 Cheilodipterus quinquelineatus 0.02 Sphaeramia orbicularis 0.02 Atherinidae Atherinomorus duodecimalis 0.02 Batrachoididae Batrachomeous trispinosus 0.07 Belonidae Strongylura strongylura 0.02 Callionymidae Callionymus schaapi 0.81 Carangidae Alectis indicus 0.02 Gnatahanodon speciosus 0.05 Chaetodontidae Chaetodon octofasciatus 0.02 Chanidae Chanos chanos 0.02 Clupeidae Anodontosoma chacunda 0.14 Escualosa thoracata 2.58 Sardinella albella 0.45 Cynoglossidae Cynoglossus puncticeps 1.32 Dasyatidae Dasyatis kuhlii 0.02 Himantura Walga 0.02 Engraulididae Stolephorus indicus 0.02 Thryssa spp* 24.15 Ephippidae Platax teira 0.02 Haemulidae Diagramma labiosum 0.02 Pomadasys maculatum 0.02 Hemiramphidae Hyporhamphus quoyi 0.02 Hyporhamphus limbatus 0.02 Labridae Choerodon oligacanthus* 4.60 Halichoeres bicolor 0.43 Halichoeres nigrescens 0.05 Latidae Psammoperca waigiensis 1.10 Leiognathidae Gazza minuta 0.07 Gazza oyena 0.12 Leiognathus elongatus 1.34 Leiognathus equulus 0.36 Secutor hanedai 0.91 Lethrinidae Lethrinus lentjan 0.69 Lutjanidae Lutjanus malabaricus 0.02 Lutjanus russelli 0.10 Lutjanus johnii 0.05 Monacanthidae Anacanthus barbatus 0.02 Monacanthus chinensis* 10.79 Paramonacanthus choirocephalus 0.07 Muraenesocidae Muraenesox bagio 0.02

127 Kwik et al.: Changi beach ﬁ sh diel variations and diversity

Table 1. Cont'd.

Family Species Relative abundance (%) Mugilidae Mugilidae spp 1.75 Ellochelon vaigiensis 0.17 Mullidae Upeneus tragula 0.86 Nemipteridae Nemipterus nemurus 0.02 Pentapodus setosus 0.05 Ophichthidae Pisodonophis cancrivorus 0.07 Paralichthyidae Pseudorhombus arsius 0.67 Pegasidae Pegasus volitans 0.12 Platycephalidae Cymbacephalus nematophthalmus 2.06 Plotosidae Plotosus canius 1.70 Plotosus lineatus 0.19 Scatophagidae Scatophagus argus 0.14 Sciaenidae Johnius belangerii 0.02 Scorpaenidae Paracentropogon longispinus 2.03 Trachicephalus uranoscorpus 0.74 Serranidae Centrogenys vaigiensis 0.05 Siganidae Siganus canaliculatus 1.27 Sillaginidae Sillago ciliata 0.50 Sillago sihama 0.96 Soleidae Brachirus orientalis 0.02 Zebrias zebra 0.07 Sphyraenidae Sphyraena jello 0.26 Syngnathidae Hippichthys cyanospilus* 10.75 Hippocampus kuda 0.12 Synodontidae Saurida tumbil 0.02 Terapontidae Pelates quadrilineatus* 11.70 Terapon jarbua 1.46 Terapon theraps 0.07 Tetraodontidae Lagocephalus lunaris 0.02 Triacanthidae Tripodichthys blochii 0.77 Gobiidae Gobiidae 3.04

Of these 25 species, only Sphyraena jello was found during chinensis (Monacanthidae), Hippichthys cyanospilus the day. These 25 common species made up 89% (3,614 (Syngnathidae), Choerodon oligacanthus (Labridae) and individuals) of the total catch during the entire sampling Apogon margaritophorus (Apogonidae) were constructed period (Table 1). to determine how each species might utilize the habitat at CPB. For most species, numbers-per-size-class were normally Size class distribution of five most common species. distributed with the exception of P. quadrilineatus, which – Juveniles of Pelates quadrilineatus (Terapontidae) and showed no clear distribution pattern. Monacanthus chinensis (Monacanthidae) were found in high numbers, while small-sized Hippichthys cyanospilus Pelates quadrilineatus can attain SL of up to 300 mm (Paxton (Syngnathidae) and Apogon margaritophorus (Apogonidae) et al., 1989) but all specimens caught ranged from 10 mm to generally occured in subadult to adult size ranges. Based 89.9 mm, and were thus considered juveniles. The majority on maximum and minimum sizes of individual species, we of specimens were between 20 mm and 79.9 mm. Smaller found that larger juveniles were generally caught during individuals were caught more often in the day, while larger the night while smaller sized adult fish species were individuals were more abundant at night. There was no clear caught more often in the day. The size class distributions size distribution pattern for P. quadrilineatus (Fig. 2). of Pelates quadrilineatus (Terapontidae), Monacanthus

128 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Monacanthus chinensis can reach SL up to 380 mm (Shen, Apogon margaritophorus can reach size of up to 65 mm SL 1993). Size distribution of M. chinensis at CPB was normally (Allen, 1997). The size range of A. margaritophorus was distributed with a mean size class of 50 mm to 59.9 mm normally distributed with a mean size class of 20 mm to 29.9 (Fig. 3). Overall, specimens ranged from <10 mm to 109.9 mm (Fig. 6). Most of the specimens were in the size class mm, and all were classed as juveniles. Smaller individuals range of subadults and adults. As with H. cyanospilus, more were caught more often in the day, while larger individuals individuals were found to occur at night than in the day. were more abundant at night.

The maximum SL of Hippichthys cyanospilus was 160 mm (Dawson, 1985). Size distribution of H. cyanospilus at CPB was slightly skewed to larger sizes (Fig 4), but generally exhibited a normal distribution pattern. Although H. cyanospilus had a mean size class of 80.0 mm to 89.9 mm, the size class mode ranged from 90 mm to 99.9 mm. Most of the specimens were well within the size range of subadults and adults. More individuals of this species were caught in the day than at night.

Choerodon oligacanthus can attain sizes of up to 282 mm SL (De Beaufort, 1940). Size distribution of C. oligacanthus was normal with a mean size class of 50 mm to 59.9 mm. Similar to both P. quadrilineatus and M. chinensis, smaller Fig. 4. Size class distribution of H. cyanospilus captured by day individuals of C. oligacanthus appeared to occur more in and night seines at Changi Point Beach between Oct. to Dec.2006 the day than at night, while larger ones were more prevalent (error bars ± S.E.). at night (Fig. 5).

Fig. 2. Size class distribution of P. quadrilineatus captured by day Fig. 5. Size class distribution of C. oligocanthus captured by day and night seines at Changi Point Beach between Oct. to Dec.2006 and night seines at Changi Point Beach between Oct. to Dec.2006 (error bars ± S.E.). ( error bars ± S.E.).

Fig. 3. Size class distribution of M. chinensis captured by day Fig. 6. Size class distribution of A. margaritophus captured by day and night seines at Changi Point Beach between Oct. to Dec.2006 and night seines at Changi Point Beach between Oct. to Dec.2006 (error bars ± S.E.). (error bars ± S.E.).

129 Kwik et al.: Changi beach ﬁ sh diel variations and diversity denote those that were caught during all three months). bold Night Day Night Day Night Day Night Day Night

0.00 0.00 0.67 0.58 3.00 1.00 0.33 0.58 0.00 0.00 1.00 1.00 2.52 0.00 1.00 1.51 4.67 0.58 0.00 0.00 0.58 3.51 1.00 0.33 0.67 0.00 0.00 0.00 0.00 0.33 0.00 3.67 0.58 3.00 0.00 0.00 0.00 0.00 0.00 0.58 0.00 3.46 0.00 0.00 0.67 0.00 0.00 0.58 0.00 0.58 0.00 0.33 0.00 0.00 4.00 0.00 0.58 0.00 0.58 0.58 0.00 0.58 0.00 0.33 0.33 0.00 0.00 0.00 3.00 0.58 3.00 0.00 1.33 0.00 2.00 0.00 0.33 0.33 0.00 0.00 0.00 0.58 0.33 0.58 0.00 0.00 0.00 0.00 0.33 2.65 0.00 0.00 21.00 0.00 0.00 0.00 0.00 5.29 0.00 16.00 0.00 7.00 0.33 10.00 2.00 0.00 5.33 1.15 2.00 0.00 9.24 0.58 0.00 0.58 0.00 0.00 0.00 0.58 0.00 0.00 7.00 0.00 17.32 8.82 10.00 0.00 5.86 0.67 0.00 9.33 16.17 0.33 0.33 0.00 0.58 0.00 0.00 3.00 0.58 0.00 0.33 5.20 0.00 1.73 3.06 6.33 4.00 0.00 3.46 4.00 0.00 0.00 0.00 0.33 0.00 0.33 0.00 0.00 1.00 1.00 4.67 0.00 0.00 2.00 0.00 0.00 0.00 0.00 0.00 1.15 1.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.67 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.33 0.58 0.58 0.00 0.00 16.44 15.33 0.00 0.67 0.58 0.00 0.33 0.58 0.67 0.58 1.33 0.00 10.58 2.31 8.00 1.15 2.33 0.00 9.85 11.00 4.36 4.00 0.33 10.02 7.67 0.00 0.00 1.53 3.33 sh caught during day and night samples between Oct. Dec.2006 (species marked with a * in Ambassidae Ambassis kopsii* Apogonidae Apogon hyalosoma* Apogon margaritophorus* Apogon quadrifasciatus* Cheilodipterus quiquelineatus Sphaeramia orbicularis Atherinidae Average Atherinomorus duodecimalis Batrachoididae SD(±) Batrachomeous trispinosus Average Belonidae SD (±) strongylura Strongylura Callionymidae Average Callionymus schaapi* SD (±) Carangidae Average Alectis indicus SD (±) Gnathanodon speciosus Chaetodontidae Average Chaetodon octofasciatus SD (±) Chanidae Average Chanos chanos SD (±) Culpeisdae Anodotosoma chacunda Escualosa thoracata* albella Sardinella Cynoglossidae Cynoglossus puncticeps* Dasyatidae Dasyatis kuhlii Himantura Walga October November December November Species October Fish Day Table 2. Average abundance of ﬁ

130 THE RAFFLES BULLETIN OF ZOOLOGY 2010 Night Night Day Night Day Night

0.00 0.00 0.33 0.58 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.58 0.00 0.58 0.00 0.00 0.00 0.00 0.00 0.58 0.00 0.00 0.33 0.00 0.33 0.58 0.00 0.00 0.00 0.00 0.00 0.00 0.33 0.00 0.00 0.00 0.33 0.00 1.16 0.00 0.58 0.00 0.00 0.71 0.00 0.00 5.29 0.00 5.20 4.00 21.55 0.00 118.29 0.00 3.06 0.00 122.32 21.67 3.67 0.00 0.67 225.67 0.33 0.00 81.33 3.50 0.00 0.00 1.15 0.00 8.14 3.00 0.00 0.00 0.00 0.00 0.00 11.53 1.00 0.00 0.00 0.00 0.00 0.00 0.67 2.00 1.15 0.00 5.67 3.79 0.00 0.00 1.00 0.00 1.73 0.00 1.00 11.00 9.45 0.00 0.00 2.00 0.00 0.00 0.67 3.06 2.67 0.00 0.58 1.00 1.53 3.79 1.15 0.00 1.00 0.00 7.33 0.00 0.00 3.00 0.00 0.00 5.69 0.00 4.67 2.67 0.00 0.33 0.00 1.00 2.89 3.67 2.00 0.00 2.67 7.64 0.67 0.00 6.35 0.00 22.33 0.00 1.00 0.00 0.00 11.33 0.00 11.59 16.64 0.58 0.00 8.67 0.00 15.00 0.00 2.31 1.73 0.00 1.67 0.00 0.58 0.58 0.00 0.00 1.00 0.00 0.00 0.58 0.58 0.00 0.33 0.00 1.73 1.33 0.00 5.51 5.00 0.00 0.00 0.58 0.33 0.33 1.00 0.00 0.00 0.00 0.00 0.00 0.33 0.33 0.00 0.00 2.00 0.00 6.67 0.00 1.15 0.33 0.00 1.00 0.00 0.00 0.00 0.00 0.58 0.00 1.73 0.00 0.00 0.00 0.67 0.00 0.00 0.00 0.00 0.00 0.33 1.00 0.00 0.00 0.00 0.58 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.33 0.00 0.00 0.00 0.00 9.67 7.37 0.00 14.00 7.00 13.89 38.00 10.21 46.33 22.14 19.67 15.01 22.67 Engraulididae Stolephorus indicus Thryssa spp* Ephippidae Platax teira Haemulidae Diagramma labiosum Pomadasys maculatum Hemiramphidae Average quoyi Hyporhamphus limbatus Hyporhamphus SD(±) Labridae Average oligacanthus* Choerodon SD (±) bicolor* Halichoeres nigrescens Halichoeres Average Latidae SD (±) vaigiensis* Psammoperca Average Leiognathidae SD (±) Gazza minuta Gazza oyena Average Leiognathus elongatus SD (±) Leiognathus equulus Secutor hanedai* Average Lethrinidae SD (±) Lethrinus lentjan* Lutjanidae Lutjanus malabaricus Lutjanus russelli Lutjanus johnii Monacanthidae Anacanthus barbatus Monacanthus chinensis* Paramonacanthus choirocephalus October November December November Table 2. Cont’d. Species October Fish Day

131 Kwik et al.: Changi beach ﬁ sh diel variations and diversity Night Day Night Day Night Day Night Day Night

0.00 0.00 0.00 0.00 0.33 0.58 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00 1.53 1.15 0.00 0.00 0.00 0.00 2.00 3.33 0.00 0.58 0.00 1.33 0.58 0.00 0.00 1.15 1.73 0.00 3.00 0.00 0.33 0.00 0.33 1.73 0.00 0.00 0.00 0.67 0.58 1.00 0.00 0.00 0.00 0.00 0.00 1.00 0.00 0.58 0.00 0.00 0.00 0.00 0.58 1.33 1.00 0.00 0.00 0.00 0.00 0.00 0.00 1.67 1.15 0.00 0.00 0.58 1.67 1.00 10.50 0.00 0.00 0.00 0.00 0.00 1.15 0.58 0.67 0.00 0.00 0.67 0.00 0.00 0.00 14.67 1.53 0.00 1.00 1.33 0.00 0.00 0.33 0.00 0.00 0.00 0.00 2.89 0.00 1.67 1.16 1.00 0.00 0.00 0.00 1.15 0.00 0.00 2.52 3.33 1.00 0.00 1.15 4.67 0.00 0.00 0.58 0.67 0.00 0.00 9.54 4.04 3.67 0.00 1.00 0.67 0.00 0.00 0.00 0.00 0.33 1.53 1.53 3.67 0.00 12.00 4.62 0.00 1.73 0.00 0.00 2.64 0.00 0.00 0.58 1.67 1.67 3.79 0.00 3.67 0.00 1.00 1.15 2.00 3.79 0.00 0.00 1.00 0.33 1.67 2.08 2.08 2.67 0.58 0.00 0.00 0.00 0.67 4.04 3.67 0.00 0.58 1.00 0.00 0.67 0.58 1.53 5.67 0.00 0.33 0.00 4.51 11.33 1.15 0.00 4.51 2.33 5.13 0.33 5.67 6.35 2.33 0.00 8.96 2.00 9.67 0.00 0.67 1.53 5.33 1.00 1.00 3.67 0.00 2.00 0.00 0.00 1.67 3.33 2.52 0.00 0.00 0.00 0.00 Muraenesocidae Muraenesox bagio Mugilidae Ellochelon vaigiensis Mullidae Upeneus tragula* Upeneus sulphureus Nemipteridae Nemipterus nemurus Average Pentapodus setosus SD(±) Ophichthidae Pisodonophis cancrivorus Average Paralichthyidae SD (±) arsius* Pseudorhombus Average Pegasidae Pegasus volitans SD (±) Platycephalidae Average Cymbacephalus nematophthalamus* SD (±) Plotosidae Plotosus canius* Average Plotosus lineatus SD (±) Scatophagidae Average Scatophagus argus SD (±) Sciaenidae Johnius belangerii Scorpaenidae longispinus* Paracentropogon uranoscorpus* Trachicephalus Serranidae vaigiensis Centrogenys Siganidae Siganus canaliculatus October November December November Table 2. Cont’d. Species October Fish Day

132 THE RAFFLES BULLETIN OF ZOOLOGY 2010 Night Day Night Day Night Day Night Day Night

0.00 0.00 0.00 0.00 0.67 1.15 0.33 0.58 0.00 0.00 6.00 3.61 4.00 0.00 6.00 0.58 0.58 5.00 0.58 0.58 0.00 0.00 0.33 7.02 0.33 0.58 0.00 0.33 1.15 0.33 0.00 0.00 7.33 0.00 1.00 0.33 0.00 0.00 0.00 0.67 0.00 0.00 0.58 0.00 0.00 0.00 2.00 0.00 0.58 0.00 0.00 0.00 0.00 0.00 0.67 0.58 0.00 1.00 0.00 0.00 0.00 0.33 0.00 0.00 0.00 1.73 0.00 0.00 0.00 0.33 0.00 0.00 1.00 0.00 0.00 0.00 0.00 3.46 1.00 1.73 0.00 0.00 0.00 0.00 0.00 0.00 0.58 0.00 6.81 2.00 0.58 1.00 0.58 0.00 0.00 0.00 2.08 0.00 1.00 0.33 1.53 5.33 0.58 0.33 0.00 0.58 0.00 0.33 0.00 0.00 1.00 14.67 0.58 2.52 5.67 1.00 0.00 0.67 0.58 0.33 0.00 6.56 5.67 3.46 3.33 4.04 3.00 0.00 0.58 0.33 4.93 6.00 3.00 1.53 2.33 0.00 0.00 0.33 4.93 9.33 2.89 2.67 0.00 4.04 5.67 1.67 5.67 13.00 7.00 8.00 2.65 18.00 7.81 57.00 21.52 19.67 15.95 34.00 46.86 34.00 15.95 21.52 19.67 7.81 57.00 2.65 18.00 7.00 8.00 13.00 13.00 14.42 9.67 9.61 57.67 27.57 40.00 43.31 11.00 9.85 31.67 28.88

Sillaginidae Sillago ciliate Sillago sihama* Soleidae Brachirus orientalis Zebrias zebra Sphyraenidae Sphyraena jello* Syngnathidae Average Hippichthys cyanospilus* Hippocampus kuda SD(±) Synodontidae Average Saurida tumbil SD (±) Terapontidae Pelates quadrilineatus* Average jarbua* Terapon SD (±) theraps Terapon Average Tetraodontidae SD (±) Lagocephalus lunaris Triacanthidae Average blochii* Tripodichthys SD (±) Gobiidae* Average SD (±) October November December November Table 2. Cont’d. Species October Fish Day

133 Kwik et al.: Changi beach ﬁ sh diel variations and diversity

DISCUSSION the density of transient species during day and night was very low. Nevertheless, more larger-sized juveniles were Although previous surveys around the coastal areas of caught at night than smaller individuals, and more small- Singapore indicate that CPB is likely to be heavily impacted sized adult fi sh species were caught during in the day than at (Chou, 1996), CPB appears to be an important ecosystem, night. The fewer occurrences of smaller individuals at night supporting an abundant and diverse assemblage of juveniles could be due to avoidance of predation by larger reef fi shes of large-sized fi sh species and subadults and adults of small- which are known to migrate to shallow coastal habitats to sized fi sh species. At least 75 fi sh species from 45 families feed nocturnally (Parrish, 1989). were found in CPB and comparisons to other local sites indicate that the species list found at CPB is larger than The function of vegetated coastal habitats as nursery grounds other locations along similar coastal habitats in Singapore for juveniles (Nagelkerken et al., 2000), for feeding (Chong (Hajisamae & Chou, 2003; Jaafar et al., 2004). Previous et al., 1990; Hajisamae & Chou, 2003) and for shelter research by Hajisamae & Chou (2003) reported 43 species (Paterson & Whitfi eld, 2000) for juveniles of large-sized fi sh from Sembawang Site (west of CPB), 61 and 68 species species and subadults to adults of small-sized fi sh species from Pasir Ris (north of CPB) site A and site B respectively have all been well documented. Moreover, Hajisamae & (Site A: a completely reclaimed sandy beach and Site B: a Chou (2003) reported that even impacted coastal habitats replanted mangrove habitat). Jaafar et al. (2004) reported can serve as nursery grounds for fi sh. Size class distribution 71 species from a reforested mangrove habitat at Pasir Ris from our study suggest that CPB possibly functions as a and 67 species from a sandy habitat at Pasir Ris. Signifi cantly nursery for at least two of the fi ve most abundant species, more species were caught in the vegetated habitat of CPB and is a potential feeding ground and refugia for juveniles as compared to less or non-vegetated habitats, such as those of large-sized fi sh species and subadults to adults of small- reported at Sembawang site (Hajisamae & Chou, 2003). sized fi sh species. This is consistent with various studies which note that vegetated coastal habitats support higher number of fi sh In conclusion, CPB supports a highly diverse fi sh community species as compared to less or non-vegetated ones (Jenkins and possibly functions as a nursery. Contrary to other studies, & Wheatley, 1998; Jaafar et al., 2004; Nagelkerken & van fi sh community structure at CPB is not signifi cantly infl uenced der Velde, 2004). by diel variations. This indicates that fi sh communities found in Singapore may exhibit different traits than found in other The diversity (H’) of 2.79 found at CPB can be considered regions and this is worthy of further study. Impacted coastal high when compared to other Singapore coastal habitats habitats such as CPB should be conserved because they such as Sembawang, H’ = 0.95, and Pasir Ris, H’ = 2.38 still perform important ecological functions. Appropriate (Hajisamae & Chou, 2003; Jaafar et al. ., 2004), indicating coastal management to prevent further habitat degradation that the fi sh community of CPB is more diverse and thus less is recommended. likely to be dominated by a single species. At least four fi sh species (Thryssa spp (Engraulididae), Pelates quadrilineatus (Terapontidae), Monacanthus chinensis (Monacanthidae), ACKNOWLEDGEMENTS Hippichthys cyanospilus (Syngnathidae) co-dominated the coastal habitat of CPB. In addition, the fi sh diversity found This research was supported by the Department of Biological at CPB is comparable to that at Saiburi estuary, Gulf of Sciences, National University of Singapore. We would like Thailand with a H’ value of 2.75 (Hajisamae et al.., 1999), to express our gratitude to Zeehan Jaafar, Joelle Lai, Wong and Malaysia mangrove systems and adjacent habitats with Poh Poh and Chou Loke Ming for their assistance with H’ values between 2.59 and 3.24 (Chong et al., 1990) literature research, and Ng Ngan Kee, Jose Christopher E. suggesting that, although heavily impacted, CPB supports Mendoza, Martyn Low and Tohru Naruse for their assistance a regionally-comparable diversity of fi sh species. in the fi eld.

Diel comparisons in species diversity and fi sh abundance indicated that there was no signifi cant difference between LITERATURE CITED day and night. This is consistent with previous research in the vegetated coastal habitats of Australia (Gray et al., 1998) Abal, E. G., Dennison, W. C. & M. H. O’Donohue, 1998. Seagrasses and Portugal (Ribeiro et al., 2006). However, some studies and mangroves in Moreton Bay. In: Tibbetts, R., N. J. Hall & (Rountree & Able, 1993; Guest et al., 2003; Unsworth et al., W. C. Dennison (eds.), Moreton Bay and Catchment. University of Queensland, Brisbane. 269–278 pp. 2006) noted higher number of species and fi sh abundance at night, while Jaafar et al. (2004) reported a greater mean fi sh Allen, G. R., 1997. The marine fi shes of tropical Australia and south-east Asia density during the day. These contrasting reports indicate . Western Australian Museum, Perth, Western Australia, 292 pp. that the dynamics of each fi sh community can differ and coastal habitats should be studied on estuary-by estuary or Blaber, S. J. M., D. T. Brewer & J. P. Salini, 1995. Fish communities and the nursery role of a tropical bay in the bay-by-bay, and species-by species basis (Blaber, 1997). Gulf of Carpentaria, Australia. Estuarine, Coastal and Shelf Signifi cant differences in abundance and diversity of fi sh Science, 40: 177–193. were probably not observed because (a) there was equal Blaber, S. J. M., 1997. Fish and fi sheries of tropical estuaries. exchange of transient species between day and night or (b) Chapman and Hall, London. 367 pp.

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Duke, 1990. Mangrove fi sh communities Heck, K. L. & R. J. Orth, 1980. Structural components of eelgrass in tropical Australia: spatial and temporal patterns in densities, (Zostera marina) meadows in the lower Chesapeak Bay decapod biomass and community structure. Marine Biology, 104: crustaceans. Estuaries, 3: 289–295. 369–379. Jaafar, Z., S. Hajisamae, L. M. Chou & Y. Yatiman, 2004. Rountree, R. A. & K. W. Able, 1997. Nocturnal Fish use of New Community structure of coastal fi shes in relation to heavily Jersey marsh creek and adjacent bay Shoal Habitats. Estuarine, impacted human modified habitats. Hydrobiologia, 511: Coastal and Shelf Science, 44: 703–711. 113–123. Santos, S. R. & R. D. M. Nash, 1995. Seasonal changes in a sandy Jenkins, G. P. & M. J. Wheatley, 1998. The infl uence of habitat beach fi sh assemblage at Porto Pim, Faial, Azores. Estuarine, structure on nearshore fi sh assemblages in a southern Australian Coastal and Shelf Science, 41: 579–591. embayment: Comparison of shallow seagrass, reef-algal and unvegetated sand habitats, with emphasis on their importance Shen, S. C., 1993. Fishes of Taiwan. Department of Zoology, to recruitment. Journal of Experimental Marine Biology and National Taiwan University, Taipei. 960 pp. Ecology, 221: 147–172. Unsworth, R. K. F., E. Wylie, D. J. Smith & J. J. Bell, 2006. Diel Kopp, D., Y. Bouchon-Navaro, M. Louis & C. Bouchon, 2007. trophic structuring of seagrass bed fi sh assemblages in the Diel differences in the seagrass fi sh assemblages of a Caribbean Wakatobi Marine National Park, Indonesia. Estuarine, Coastal island in relation to adjacent habitat types. Aquatic Botany, and Shelf Science, 72: 81–88. 87: 31–37. Young, P.C., 1981. Temporal changes in the vagile epibenthic fauna of 2 seagrass meadows Zostera capricorni and Posidonia australis. Marine Ecology Progress Series, 5: 91–102.

135

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FISHES OF THE MARINA BASIN, SINGAPORE, BEFORE THE ERECTION OF THE MARINA BARRAGE

Tan Heok Hui, Martyn E. Y. Low and Kelvin Lim Kok Peng Rafﬂ es Museum of Biodiversity Research, Department of Biological Sciences, National University of Singapore Block S6, Science Drive 2, #03-01, Singapore 117546, Republic of Singapore Email: [email protected] (THH; Corresponding author)

ABSTRACT. – A survey of the ﬁ sh diversity in the Marina Basin was conducted from March to October 2005 for the Public Utilities Board (PUB) to establish the pre-barrage baseline condition so that post-barrage changes in the ecosystem can be monitored and managed. A total of 139 ﬁ sh species from 57 families is recorded. A critical assessment of the potential occupants of the Marina basin was carried out, in anticipation of the change in salinity that will be caused by the erection of the Marina Barrage. The likely species loss and possible new ones to be settled in the new reservoir created by the barrage building are examined.

KEY WORDS. – Marina Bay, Singapore, Fish, pre-Barrage, biodiversity.

INTRODUCTION specimens were obtained by several methods: custom-made bubu/fi sh traps (about one metre in length, mesh 4 cm), The coastal areas of Singapore have been heavily modifi ed gill nets (mesh size 3” and 4”), cast net (10, 12 and 14 feet due to land reclamation and the damming of rivers to diameter), scoop net, hand net, 25 metre seine net (15 mm construct reservoirs (Chia et al., 1988). Despite these mesh size) and angling. Due to heavy boating traffi c, the fi sh activities, patches of mature secondary mangroves still traps were placed near the concrete or rock embankments remain along the northern coast, i.e. Sungei Buloh Wetland and bridge foundations. Gill nets were set parallel to shore Reserve (Bird et al., 2004) and the Mandai mangroves near and constantly monitored for three to four hours before the Woodlands causeway (Ng & Sivasothi, 1999). The Johor retrieval (with written permission from the Maritime and Straits still serve as a vital nursery ground for fi shes despite Port Authority of Singapore, MPA). Cast netting was only being heavily impacted (Hajisamae & Chou, 2003; Jaafar used along concrete or rock embankments, and sandy areas. et al., 2004). Less is known of the southern coast, although Seining was carried out parallel to shore only in areas with much of it has been heavily modifi ed for port facilities and sandy or silty bottom (e.g. Kallang Riverside Park). Visual reclaimed for land expansion. census was conducted during both low and high tides, using binoculars (8× magnifi cation power). Visual census was The Marina Bay area, which consists of reclaimed land and carried out mostly along banks of canals and drains within the estuaries of several natural drainage systems (namely the survey area. the Singapore River, Geylang River and Kallang River) is currently being converted into a freshwater reservoir by Fish specimens obtained were euthanized in ice (a protocol the erection of the Marina Barrage at the mouth of Marina approved by the Institutional Animal Care and Use Bay (Fig. 1). The following reports on a recent survey in Committee, IACUC, of the National University of Singapore, the Marina Basin, conducted over 8 months in 2005 for the NUS) and fi xed in 10% formalin solution for one to two Public Utilities Board (PUB), as part of the biodiversity weeks. They were subsequently placed in tap water to leach baseline data collation, done in partnership with the Tropical for one to two days before transfer to permanent storage in Marine Science Institute (TMSI). 75% ethanol. The specimens were catalogued and deposited in the Zoological Reference Collection of the Raffl es Museum of Biodiversity Research (RMBR), NUS. Fish species were MATERIALS AND METHODS identifi ed with reference to the following: Tan et al. (1982), Lim & Ng (1990), Kottelat et al. (1993), Carpenter & Niem The extent of the present survey covers the boat accessible (1998, 1999a, 1999b, 1999c, 1999d), Lim & Low (1998), areas of the Marina Basin, which includes visual surveys Kimura & Matsuura (2003) and Larson & Lim (2005). covering the open drain areas up to tidal infl uence. Fish

137 Tan et al: Fishes of Marina Basin, Singapore

Fish of local conservation status. – The conservation CONCLUSIONS status of the various species encountered follow those presented in the second edition of The Singapore Red Data A list of possible fishes that will survive in freshwater Book (Davison et al., 2008). Three categories are relevant: without access to the sea is as follows: Anabantidae Critically Endangered (CR), Endangered (EN) and Vulnerable – Anabas testudineus, Channidae – Channa striata, Cichlidae (VU). – Etroplus suratensis, Geophagus altifrons, Oreochromis mossambicus, Clariidae – Clarias batrachus, C. gariepinis, Cyprinidae – Carassius auratus, Cyclocheilichthys apogon, RESULTS Puntius banksi, P. lateristriga, P. semifasciolatus, Rasbora elegans, Rasborinus lineatus, Gobiidae – except Rhinogobius, A total of 138 fi sh species from 57 families is obtained from Glossogobius giuris, Gobiopterus and Oxyeleotris marmorata, the present survey (see Table 1). A search through museum Hemiramphidae - Dermogenys collettei, Hemirhamphodon catalogue records and the collection at the RMBR turned pogonognathus, Mastacembelidae – Macrognathus maculatus, up an additional 44 fi sh species (of which 16 are confi ned Osphronemidae – Betta splendens, Trichopodus pectoralis, to freshwater) and an additional 6 families. T. trichopterus, Trichopsis vittata, Poeciliidae – Poecilia sphenops, Xiphorus maculatus, Siluridae – Silurichthys hasseltii. DISCUSSION This next list of fi shes may survive but not breed if access The abundance of each fi sh trap was not noted, as the use to the marine environment is restricted, is as follows: of the traps were not standardized nor were the locations Adrianichthyidae – Oryzias javanicus, Ariidae – Arius sagor, of the traps fi xed. Each fi sh trap method targeted different Batrachiodidae – Batrachomoeus trispinosus, Centropomidae groups of fi sh. The fi sh traps/bubus were not baited and – Lates calcarifer, Eleotrididae – Butis humeralis, Ophiocara usually placed near a man-made structure (e.g. bridge porocephala, Gobiidae – all species listed (except those foundation) and these normally attracted species attracted mentioned above), Lutjanidae – Lutjanus johnii, L. to hard structures, i.e. Etroplus suratensis, Siganus javus, russellii, Megalopidae – Megalops cyprinoides, Muraenidae Epinephalus spp., Monacanthus chinensis. Cast netting – Gymnothorax tile, Plotosidae – Paraplotosus albilabrus, usually yielded pelagic species (e.g. Ambassis spp., clupeids Plotosus canius, Scatophagidae – Scatophagus argus, S. and engraulids, Atherinomorus duodecimalis, mugilids, cf. argus, Terapontidae – Terapon jarbua, Tetraodontidae gerrids and leiognathids) and benthic species (e.g. gobiids, – Tetraodon nigroviridis, Toxotidae – Toxotes chatareus, platycephalids and synodontids). Seine netting yielded the T. jaculator. highest diversity as the net is swept and dragged along a water column and substratum, usually with a mix of pelagic As there had been no previous studies or research into and benthic fauna, including invertebrates, e.g. crustaceans, freshwater adaptation of existing fi sh fauna of riverine habitats echinoderms, mollusks. Gill netting produced the least yield, being converted in freshwater reservoirs in Singapore, this as the net placement was restricted to being placed parallel study would serve as a good basis and baseline for future to shore, whereas the maximal output would have been studies and surveys. The postulations of the potential perpendicular to the shore. Nonetheless, a single specimen occupants of the Marina Barrage can be tested and should of wolf herring (Chirocentrus dorab) was obtained via prove to be an excellent case study for similar scenarios that this method. Usually, seine and scoop netting obtained the may occur in Asia and the region in the future. small species and juvenile specimens, as the mesh size is smaller. ACKNOWLEDGEMENTS The location of the fi shing site also plays a role in the yield. Sampling at the confl uence of two river systems or canals We are very grateful to PUB, who initiated this study and yields a larger catch. Sampling at the Marina channel yielded granted us permission to carry out the survey and to publish more marine species than at the estuarine areas (e.g. species this information. Invaluable help was rendered by MPA, for from Pomacanthidae, Chaetodontidae, Ephippidae, Labriidae permission to use a shallow draft powered boat within the and Pempheridae). confi nes of the Marina Bay; Kallang Water Sports Centre, for permission to dock at their premises and use of their The current results indicate that estuarine elements still exist facilities; Alvin Lok Siew Loon, Jeffrey Kwik Teik Beng, in the modifi ed habitats such as Kallang and Geylang Rivers, Eunice Tan Jing Mei and Reuben Clements Gopalasamy, but only in remnant populations. The Marina channel is for helping out in the fi eld; Zeehan bte Jafaar, for sourcing more reminiscent of a rocky shore marine habitat, because the literature and museum records; and Oung Hock Lim, of the rock bunds. the boatman for safely steering us around.

138 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. Distribution of coastal ﬁ sh from the Marina Bay and Channel area. Legend: (CR), critically endangered; (EN), endangered; (VU), vulnerable. °, denotes wholly freshwater species; *, denotes introduced species. Conservation status information are from Davison et al., 2008.

DISTRIBUTION FAMILY Singapore Rochor Kallang Geylang Marina SPECIES River Canal River River Channel Adrianichthyidae Oryzias javanicus + + + Ambassidae Ambassis interrupta + Ambassis kopsii + + + + + Ambassis nalua + Ambassis vachellii + + Anabantidae Anabas testudineus° + Apogonidae Apogon fraenatus + Apogon hyalosoma + + Apogon melas + Apogon quadrifasciatus + Chilodipterus singapurensis + Lepidamia kalosoma + Ariidae Arius nella + Arius sagor + + Atherinidae Atherinomorus duodecimalis + Batrachoididae Batrachomoeus trispinosus + + + Blennidae Omobranchus ferox + + Carangidae Alectis indicus + Alepes djedaba + Gnathanodon speciosus + Scomberoides commersonianus + Centropomidae Lates calcarifer + + Psammoperca waigiensis + Chaetodontidae Chaetodon octofasciatus + Chelmon rostratus + Parachaetodon ocellatus + Chanidae Chanos chanos + Channidae Channa striata° + Chirocentridae Chirocentrus dorab + Cichlidae Etroplus suratensis* + + + + + Geophagus surinamensis* + Oreochromis mossambicus* + + + +

139 Tan et al: Fishes of Marina Basin, Singapore

Table 1. Cont'd.

DISTRIBUTION FAMILY Singapore Rochor Kallang Geylang Marina SPECIES River Canal River River Channel Clariidae Clarias batrachus° + Clarias gariepinus°* + Clupeidae Anodontostoma chacunda + + Dussumieria acuta + Escualosa thoracata + + Herklotsichthys dispilonotus + Hilsa keele + + Sardinella albella + + + Sardinella ﬁ mbriata + Cyprinidae Carassius auratus°* + Cyclocheilichthys apogon° (EN) + Metzia lineatus°* + Puntius banksi° + Puntius lateristriga° + Puntius semifasciolatus°* + Rasbora elegans° + Dasyatidae Dasyatis zugei + Himantura gerrardi + Drepaneidae Drepane punctata + Eleotrididae Butis humeralis + Ophiocara porocephala + + + + Engraulididae Stolephorus indicus + + Stoelphorus sp. + + Thryssa hamiltonii + Thryssa setirostris Ephippidae Platax orbicularis + Gerreidae Gerres erythrourus + Gerres ﬁ lamentosus + + Gerres kapas + + + Gerres macracanthus + + Gerres oyena + + Gobiidae Acentrogobius caninus + + + Acentrogobius janthinopterus + Acentrogobius nebulosus + Acentrogobius viridipunctatus + Arcygobius baliurus + + Brachyamblyopus brachysoma + Callamiana illota + Drombus globiceps + + + Drombus ocyurus + Exyrias puntang + + Favonigobius reichei +

140 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. Cont'd.

DISTRIBUTION FAMILY Singapore Rochor Kallang Geylang Marina SPECIES River Canal River River Channel Glossogobius aureus + Glossogobius circumspectus + Gobiopsis macrostoma + Hemigobius hoeveni + + Istigobius dianema + Mugilogobius chulae + Oxyurichthys uronema + Periophthalmodon schlosseri + + + Periophthalmus argentilineatus + + + Periophthalmus variabilis + + Periophthalmus walailakae + Psammogobius biocellatus + Pseudogobiopsis oligactis + Pseudogobius javanicus + + + + Stigmatogobius pleurostigma + + Stigmatogobius sadanundio + Taenioides gracilis + Trypauchen vagina + Haemulidae Diagramma pictum + Plectorhinchus gibbosus + Pomadasys argenteus + Pomadasys kaakan + Pomadasys maculatum + + Hemiramphidae Dermogenys collettei° + Hemirhamphodon pogonognathus° + Zenarchopterus buffonis + + Zenarchopterus gilli + + + + Labridae Choerodon anchorago + Choerodon oligocanthus + Choerodon schoenleinii + Leiognathidae Deveximentum ruconis + Gazza minuta + Leiognathus equulus + + + + Nuchequula blochii + + + Lethrinidae Lethrinus lentjan + Lutjanidae Lutjanus carponotatus + Lutjanus erythropterus + Lutjanus fulviﬂ amma + Lutjanus johnii + Lutjanus monostigma + Lutjanus russellii + + + Mastacembelidae Macrognathus maculatus° (CR) + Megalopidae Megalops cyprinoides +

141 Tan et al: Fishes of Marina Basin, Singapore

Table 1. Cont'd.

DISTRIBUTION FAMILY Singapore Rochor Kallang Geylang Marina SPECIES River Canal River River Channel Monacanthidae Acreichthys tomentosum + Monacanthus chinensis + + Mugilidae Ellochelon vaigiensis + Liza sp. 1 + + + + + Liza sp. 2 + + + Mulidae Paruepeneus cyclostomus + Muraenidae Gymnothorax reevesi + Gymnothorax tile + Nemipteridae Scolopsis vosmeri + Ophichthidae Pisodonophis cancrivorus + Osphronemidae Betta splendens°* + Trichopodus pectoralis°* + Trichopodus trichopterus° + Trichopsis vittata° + Ostraciidae Ostracion nasus + Paralichthyidae Pseudorhombus malayanus + Pempheridae Pempheris oualensis + Platycephalidae Cymbacephalus nematophthalmus + Eurycephalus carbunculus + Grammoplites knappi + Inegocia japonica + Platycephalus indicus + + Plotosidae Paraplotosus albilabris + Plotosus canius + + Plotosus lineatus + + Poeciliidae Poecilia sphenops* + + + + + Xiphophorus maculatus* + Pomacanthidae Chaetodontoplus mesoleucus + Pomacanthus imperator + Scatophagidae Scatophagus argus + + + + + Scatophagus cf. argus + Sciaenidae Dendrophysa russelli +

142 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. Cont'd.

DISTRIBUTION FAMILY Singapore Rochor Kallang Geylang Marina SPECIES River Canal River River Channel Scorpaenidae Minous monodactylus + Scorpaeniopsis oxycephala + Synanceia horrida + Serranidae Diploprion bifasciatum + Epinephelus coioides + Epinephelus fuscoguttatus + Epinephelus malabaricus + + Plectropomus leopardus + Siganidae Siganus canaliculatus + + Siganus guttatus + + + Siganus javus + + + + Sillaginidae Sillago sihama + Siluridae Silurichthys hasseltii° + Soleidae Pardachirus pavoninus + Sphyraenidae Sphyraena jello + Synbranchidae Opisternon bengalense + Syngnathidae Hippichthys cyanospilos + Hippocampus comes (VU) + Hippocampus kuda (VU) + Synodontidae Saurida tumbil + Terapontidae Terapon jarbua + + Terapon puta + Terapon theraps + Tetraodontidae Arothron immaculatus + + Arothron mappa + Arothron reticularis + + Lagocephalus lunaris + Takifugu oblongus + Tetraodon nigroviridis + + Toxotidae Toxotes chatareus + + Toxotes jaculator + + + + Triacanthidae Tripodichthys blochi + + Trichiuridae Trichiurus lepturus + TOTAL NUMBER OF SPECIES 49 30 47 30 123

143 Tan et al: Fishes of Marina Basin, Singapore

LITERATURE CITED Hajisamae, S. & L. M. Chou, 2003. Do shallow water habitats of an impacted coastal strait serve as nursery grounds for fi sh? Bird, M., S. Chua, L. K. Fifi eld, T. S. Teh & J. Lai, 2004. Evolution Estuarine, Coastal and Shelf Science, 56: 281–290. of the Sungei Buloh-Kranji mangrove coast, Singapore. Applied Jaafar, Z., S. Hajisamae, L. M. Chou & Y. Yatiman, 2004. Geography, 24: 181–198. Community structure of coastal fi shes in relation to heavily Carpenter, K. E. & V. H. Niem (Eds.), 1998. FAO species impacted human modified habitats. Hydrobiologia, 511: identifi cation guide for fi shery purposes. The living marine 113–123. resources of the Western Central Pacifi c. Volume 2. Cephalopods, Kimura, S. & K. Matsuura (eds.), 2003. Fishes of Bitung. Northern crustaceans, holothurians and sharks. Food and Agriculture tip of Sulawesi, Indonesia. Ocean Research Institute, The Organization of the United Nations, Rome: 687–1396. University of Tokyo. 244 pp. Carpenter, K. E. & V. H. Niem (Eds.), 1999a. FAO species Kottelat, M., A. J. Whitten, S. N. Kartikasari & S. Wirjoatmodjo, identifi cation guide for fi shery purposes. The living marine 1993. Freshwater fi shes of western Indonesia and Sulawesi. resources of the Western Central Pacifi c. Volume 3. Batoid fi shes, Periplus Editions, Hong Kong. 221 pp. + 84 pls. chimaeras and bony fi shes part 1 (Elopidae to Linophrynidae). Larson, H. K. & K. K. P. Lim, 2005. A guide to Gobies of Singapore. Food and Agriculture Organization of the United Nations, Singapore Science Centre, 164 pp. Rome: 1397–2068. Lim, K. K. P. & J. K. Y. Low, 1998. A guide to common marine Carpenter, K. E. & V. H. Niem (Eds.), 1999b. FAO species fi shes of Singapore. Singapore Science Centre, 163 pp. identifi cation guide for fi shery purposes. The living marine resources of the Western Central Pacific. Volume 4. Bony Lim, K. K. P. & P. K. L. Ng, 1990. A guide to the freshwater fi shes fi shes part 2 (Mugilidae to Carangidae). Food and Agriculture of Singapore. Singapore Science Centre, 160 pp. Organization of the United Nations, Rome: 2069–2790. Ng, P. K. L., J. Low & K. K. P. Lim, 1994. Fish, species accounts: Carpenter, K. E. & V. H. Niem (Eds.), 1999c. FAO species In: P. K. L. Ng & Y. C. Wee (eds.), The Singapore Red Data identifi cation guide for fi shery purposes. The living marine Book. Threatened Plants and Animals of Singapore. The Nature resources of the Western Central Pacifi c. Volume 5. Bony fi shes Society (Singapore): 184–208, 326–330 (list). part 3 (Menidae to Pomacentridae). Food and Agriculture Ng, P. K. L. & N. Sivasothi, 1999. A Guide to the Mangroves Organization of the United Nations, Rome: 2791–3380. of Singapore I: The ecosystem and plant diversity. Singapore Carpenter, K. E. & V. H. Niem (Eds.), 1999d. FAO species Science Centre, Singapore, 160 pp. identifi cation guide for fi shery purposes. The living marine Tan, S. M., P. Y. Lim, T. Senta, K. K. Hooi, R. S. H. Lim, N. W. resources of the Western Central Pacific. Volume 6. Bony Loy, S. S. F. Lee, B. N. Ng, C. S. Gwee, A. C. H. Lee & P. H. fi shes part 4 (Labridae to Latimeriidae). Food and Agriculture Wong, 1982. A colour guide to the fi shes of the South China Sea Organization of the United Nations, Rome: 3381–4218. and the Andaman Sea. Primary Production Department/Marine Chia, L. S., H. Khan & L. M. Chou, 1988. The coastal environmental Fisheries Research Department, SEAFDEC, Singapore, 55 pp., profile of Singapore. ICLARM Technical Reports 21, revised October, 1996. International Centre for Living Aquatic Resources Management, Manila, Philippines. 92 pp. Davison, G. W. H., P. K. L. Ng & H. H. Chew. (eds.), The Singapore Red Data Book: Threatened plants & Animals of Singapore. 2nd Edition. The Nature Society (Singapore), Singapore. 285 pp.

144 THE RAFFLES BULLETIN OF ZOOLOGY 2010

MAMMAL DIVERSITY AND CONSERVATION IN A SMALL ISOLATED FOREST OF SOUTHERN THAILAND

S. Kitamura Laboratory of Animal Ecology, Department of Life Sciences, Faculty of Science, Rikkyo University, Tokyo 171-8501, Japan; Thailand Hornbill Project, Department of Microbiology, Faculty of Science, Mahidol University, Rama 6 Rd., Bangkok 10400, Thailand Present address: Division of Nature and Environmental Management, The Museum of Nature and Human Activities, Hyogo, Yayoigaoka 6, Sanda, Hyogo, 669-1546, Japan Email: [email protected] (Corresponding author)

S. Thong-Aree and S. Madsri National Park, Wildlife and Plant Conservation Department, 61 Phahonyothin Rd., Chatuchak, Bangkok 10900 Thailand

P. Poonswad Department of Microbiology, Faculty of Science, Mahidol University, Rama 6 Rd., Bangkok 10400, Thailand Email: [email protected]

ABSTRACT. – Knowledge of the presence and distribution of species is crucial for designing and evaluating conservation strategies within a region. We conducted a camera-trapping survey of terrestrial mammal and bird diversity in a small isolated forest of southern Thailand over 3 yr. A total of 15 camera traps, which accumulated 11,106 camera-days, were set in three forest types: primary, logged, and hill forests. Despite its small size, isolation, and surrounding agricultural areas, a total of 35 mammal species, eight bird species, and one reptile species were recorded in the forest system. The total number of species photographed was similar among forest types (26-30 species), and rarefaction curves of each forest did not indicate any differences in the relationship between sampling effort and recorded species richness. As the activity period of these animals does not appear to be affected by human activities, we believe that the effect of direct poaching on large mammals in the study area is negligible. Although we did not observe any previously unrecorded animals in our study site, our ﬁ ndings are very valuable and point to the importance of biodiversity conservation efforts in these small fragmented and human-modiﬁ ed forest landscapes.

KEY WORDS. – Camera trapping, dipterocarp forest, Hala-Bala Wildlife Sanctuary, rarefaction curve.

INTRODUCTION Research into the presence and distribution of species is crucial for planning and evaluating conservation strategies Tropical forests are becoming increasingly fragmented, which within a region (Tobler et al., 2008). Even though studies in turn threatens the survival of their resident species (Sodhi on mammals in tropical forests are often diffi cult, a great et al., 2004b; Primack & Corlett, 2005; Laurance, 2007). deal of comprehensive work has focused on mammals in Changes in the size, shape, or confi guration of habitat that Southeast Asia (Carbone et al., 2001; Lynam et al., 2001; result from human disturbances strongly affect populations Fernando et al., 2003; Kinnaird et al., 2003; O’Brien et al., of various animals. Species extirpation is driven by the 2003; Wong et al., 2004; Fredriksson et al., 2006; Wilting direct effects of hunting and illegal trading, by the indirect et al., 2006; Meijaard & Sheil, 2008). Many of these species effects of habitat loss (deforestation and fragmentation), and are charismatic and/or fl agship species for the conservation by interactions among these factors (Peres, 2001; Dirzo et of habitats or ecosystems. al., 2007; Wright et al., 2007). No tropical forests are more threatened and no tropical fauna are more endangered than Studies of large mammals in tropical forests have benefi ted those of Southeast Asia (Sodhi et al., 2004a; Corlett, 2007; greatly from recent technological improvements that provide Laurance, 2007). various ready-made camera traps with tiny infrared-motion sensors, built-in-fl ashes, and data packs at a reasonable cost (Swann et al., 2004; Yasuda, 2004). In fact, infrared-triggered

145 Kitamura et al.: Mammal diversity of a Thai forest camera systems are now widely used in vertebrate ecology, MATERIALS AND METHODS with applications to nest ecology, population estimation, behavioural ecology, mammal inventories, and studies of Study site. – The Bala forest is part of the Hala-Bala Wildlife animal damage (Carthew & Slater, 1991; Cutler & Swann, Sanctuary (hereafter, Bala), on the Thai-Malaysian border 1999). Even in tropical forests, recent studies have determined (5°44'N 101°46'E–5°57'N 101°51'E; Fig. 1). The Bala that sampling medium- to large-sized mammals using camera portion of the sanctuary is 111.5 km2 in area and is isolated traps is a practical, non-invasive method that requires little from other forests by agricultural lands on the Thai side of effort and is particularly useful when compared to alternative the border (the 314 km2 Hala portion of the sanctuary lies methods, such as line transects, direct observations, track and approximately 22 km to the west) and a mix of forest and faeces identifi cation, trapping, and interviews of local people agriculture on the Malaysian side. Bala ranges in elevation (Silveira et al., 2003; Srbek-Araujo & Chiarello, 2005). from 50 to 960 m above sea level and is broadly classifi ed as tropical lowland evergreen forest (Bird Conservation Society In Southeast Asia, camera traps have been used in a number of Thailand, 2004). The forests primarily comprise species of studies for a variety of research purposes, e.g., mammal typical of the Sundaic or Malesian region (Malay Peninsula, inventories of specifi c areas (Numata et al., 2005; Mohd- Borneo, Sumatra, Java), many of which are uncommon in Azlan & Engkamat, 2006; Giman et al., 2007; Dinata et al., Thailand and have their primary home ranges farther south 2008); monitoring animals visiting a particular site, such as on the Malay Peninsula. During 1987–1992, Bala was partly natural licks (Matsubayashi et al., 2007a; Matsubayashi et logged along the paved road that bisects the lower one-third of al., 2007b), natal dens (Lim & Ng, 2008), or fruiting trees the site and was sporadically (and illegally) logged elsewhere (Miura et al., 1997; Kitamura et al., 2004; Kitamura et al., in the sanctuary. 2006; Suzuki et al., 2007; Yasuda et al., 2007; Van der Meer et al., 2008; Kitamura et al., 2009); recording animal Bala forest receives an average annual rainfall of 3,500 mm activity periods (Griffi ths & van Schaik, 1993b; van Schaik (in some years nearly 5,000 mm), mostly from southeast & Griffi ths, 1996; Grassman et al., 2005a; Grassman et al., monsoons between October and January. The clear, dry 2005b; Grassman et al., 2006; Mohd-Azlan, 2006; Mohd- season lasts from February to April, and the mean monthly Azlan & Sharma, 2006; Suzuki et al., 2006; Kawanishi temperature is 23°C. Fruit production is highly seasonal, and & Sunquist, 2008); identifying seed dispersers/predators an abundance of ripe fruits peaks during July and September, (Yasuda et al., 2000; Kitamura et al., 2004; Kitamura et al., while periods of fruit scarcity strongly differ across years (S. 2006; Kitamura et al., 2008); and estimating the relative Kitamura, unpublished data). Most fi eld studies conducted in and absolute abundance of a particular species, such as the Bala forest have focused on describing specifi c taxa, such tigers (Mohd-Azlan & Sharma, 2003; O’Brien et al., 2003; as fi gs (Chantarasuwan & Thong-Aree, 2006), ants (Noon- Kawanishi & Sunquist, 2004; Linkie et al., 2006; Mohd- Anant, 2003), and bats (Bumrungsri et al., 2006), with the Azlan & Sharma, 2006; Lynam et al., 2007; Simcharoen et exception of several ecological studies on hornbills (Gale & al., 2007), leopards (Ngoprasert et al., 2007), Malayan sun Thong-Aree, 2006; Kemp et al., 2007; Thong-Aree, 2007). bears (Wong et al., 2004; Linkie et al., 2007), or Malayan tapirs (Holden et al., 2003). Camera trapping. – Each remote camera was equipped with a built-in infrared motion sensor, a built-in fl ash, and a data Relatively undisturbed lowland forest is now rare in the pack that stamped each photograph with the time and date of Sundaic region (Lambert & Collar, 2002), particularly in southern Thailand, where more than 95% of the natural forest has been destroyed (Round, 1988). Most of the remaining forests in southern Thailand are highly fragmented and isolated as a result of human activities, including illegal logging, rubber plantations, and fruit orchards (Bird Conservation Society of Thailand, 2004). With such a rapid destruction of natural habitats, it is important to document the presence, diversity, and distribution of large mammals occurring in various forest patches in southern Thailand and to study mammal species that may not be able to survive in small isolated forests. Such research will provide essential information for conservation and management efforts. Moreover, the data can be used to assess loss of diversity elsewhere if isolation/fragmentation occurs in a similar manner. Here, we present data on mammalian fauna obtained from a 3-year camera-trap study in an isolated forest of southern Thailand.

Fig. 1. Hala-Bala Wildlife Sanctuary (Bala forest) in southern Thailand, and the road cutting through the forest and associated trails on either side, as used by Gale and Thong-Aree (2006).

146 THE RAFFLES BULLETIN OF ZOOLOGY 2010 the event (Sensor Camera Fieldnote, Marif Co., Ltd., Iwakuni, Data analysis. – Camera-trapping data are often diffi cult to Yamaguchi, Japan). Power was supplied by a CR123A interpret when a series of photographs depict the same species, lithium battery, which lasted approximately three months. which leads to issues of self-dependence and unsuitability Colour print fi lm (ISO 400) was used in each camera, and for statistical analysis (O’Brien et al., 2003; Yasuda, 2004). no photographic delay interval was available for the model One way to minimise self-dependence in camera-trapping used. If an animal or a group of animals remained at the results is to consider a series of photographs of the same site, the camera was triggered every 10–15 sec. Each camera species taken within a certain period of time as a single event was wrapped tightly in a transparent polypropylene bag and (Otani, 2001; O’Brien et al., 2003). In this study, we treated encased in an unsealed plastic box for waterproofi ng. a picture as indicating a single visit by a given species if that picture was taken >30 min after the previous picture of that Cameras were deployed at 15 locations in three different species (O’Brien et al., 2003; Yasuda, 2004). forest types (Fig. 1). In each forest type, cameras were deployed 300–500 m apart along an existing trail: primary Researchers and conservation planners are often interested forest (trail #4, southern part of the paved road, P1-5: 323 in the number of species supported by a particular habitat, ± 11 m a.s.l., mean ± SD), logged forest (trail #8, northern region, or protected area. In our study, unequal sampling part of the paved road, L1-5: 301 ± 44 m a.s.l.), and hill effort (36 mo for both primary and logged forests versus 18 forest (trail #12, western part of Bala, H1-5: 715 ± 95 m mo for the hill forest) limited our ability to compare species a.s.l.). The sampling effort varied among forests. In the richness among habitat types. When animal abundance varies primary and logged forests, the same camera locations were between sites, comparisons of diversity will favour the more maintained for 36 months (Oct.2004 to Oct.2007), whereas abundant site with more animals because of higher species those in the hill forest were maintained for 18 months (May detection rates (Gotelli & Colwell, 2001). To control for 2006 to Sep.2007). this issue, we implemented the rarefaction approach with EstimateS Win 8.0.0 (Colwell, 2005), and we used species In the primary and logged forests, several cameras were accumulation curves to compare richness levels among also set up along animal trails and around common fruiting habitats. trees, such as Anisophyllea cornei (Anisophylleaceae), Baccaurea parvifl ora (Euphorbiaceae), Canarium littorale In our study area, sunrise annually varies between 0557 (Burseraceae), Cheilosa malayana (Euphorbiaceae), and 0629 hrs and sunset varies between 1756 and 1834 Elaeocarpus stipularis (Elaeocarpaceae), Garcinia sp.1 hrs. According to the standard time near Bala, we divided (Guttiferae), Irvingia malayana (Irvingiaceae), Palaquium the day into two time zones, i.e., daytime (0600 to 1800 impressinervium (Sapotaceae), and Sterculia macrophylla hrs) and nighttime (1800 to 0600 hrs). Time periods were (Sterculiaceae). Ten fruits were collected from the ground pooled in 1-hour intervals. We assumed that the numbers around fruiting trees and were placed at the base of the same of photographs taken were correlated with animal activity, trees as animal bait. Cameras were set approximately 2 m and we classifi ed the activity patterns of captured animals away from the bait. When fruits were consumed by animals based on previous studies in Southeast Asia (van Schaik & or damaged by insects, they were replaced with new samples. Griffi ths, 1996; Grassman et al., 2005a; Grassman et al., Although the photographing duration was limited by the 2006). For species with > 10 captures, we defi ned diurnally length of fruit availability, each session continued for at active species as those with < 10 percent of captures at night, least one month. All camera-trapping stations were marked and nocturnally active species as those that had > 90 percent using a global positioning system (GPS; GARMIN eTrex). captures at night. We considered species with between 10 and Cameras were checked every month to reload new fi lm. In 90 percent nocturnal captures as arrhythmic, i.e. they showed several instances, the fi lm had fi nished prior to checking; no clear activity pattern (Grassman et al., 2006). therefore, some records may have been missed.

Species identification and their conservation status in RESULTS Thailand. – After the fi lm was developed, the photographs were examined for images of animals. Animal nomenclature Species diversity of photographed animals in Bala. – The follows (Lekagul & Round, 1991) for birds, and (Corbet & total number of camera-days was 11,106 over 36 months Hill, 1992) for mammals. The identifi cation of some small (4,428 camera-days in the primary forest, 3,965 in the logged mammals was diffi cult when based solely on photographs. In forest, 1,891 in the hill forest, 613 along animal trails, and addition to photographing, we also conducted live trapping of 389 around fruiting trees). In total, 8,414 photographs were small mammals in the primary and logged forests of Bala (S. exposed, 3,750 of which (44.6%) contained no animal image. Kitamura, unpublished data). Thus, we were able to identify The remaining 4,664 photographs (55.4%) showed images of small mammals by comparing body sizes and colours of those 44 species, including 35 mammal species, eight bird species, in the pictures to those that had been trapped. Based on the and one reptile species (Table 1). Of these, 2,087 photographs Thailand Red Data Book (Nabhitabhata & Chan-Ard, 2005; (44.7%) were considered independent visits and were used Sanguansombat, 2005), we determined the conservation status for further analysis. in Thailand of the photographed animals. Some species of bats and birds were photographed several times but could not be identifi ed from the photographs.

147 Kitamura et al.: Mammal diversity of a Thai forest

Table 1. Summary of animals recorded in the Hala-Bala Wildlife Sanctuary, Thailand, from November 2004 to October 2007. Species with > 10 photo-captures are underlined. Site abbreviations: P: primary forest; L: logged forest; H: hill forest; A: animal trail; and F: fruiting tree. TRD: Thailand Red Data (Nabhitabhata & Chan-Ard, 2005; Sanguansombat, 2005), EN: endangered, VU: vulnerable, NT: near threatened, LC: least concern.

Family Scientiﬁ c name English name N Site TRD Mammalia Tupaiidae Ptilocercus lowii Feather-tailed treeshrew 2 F VU Tupaia glis Common treeshrew 55 P, L, A, F Erinaceidae Echinosorex gymnurus Moonrat 47 P, L, F VU Cercopithicidae Macaca nemestrina Pig-tailed macaque 237 P, L, H, A, F NT Trachypithecus obscurus Dusky langur 12 P, L, H VU Manidae Manis javanica Sunda pangolin 5 P, L, F NT Sciuridae Callosciurus caniceps Grey-bellied squirrel 1 L C. notatus Palntain squirrel 5 P, L, H, F Lariscus insignis Three-striped ground squirrel 9 P, L, F VU Rhinosciurus laticaudatus Shrew-faced ground squirrel 1 F VU Muridae Leopoldamys sabanus Noisy rat 83 P, L, F Maxomys surifer Red spiny rat 293 P, L, H, A, F M. whiteheadi Whitehead’s rat 6 P, L, F VU Sundamys muelleri Muller’s rat 1 P Hystricidae Atherurus macrourus Bush-tailed porcupine 5 L, H, A LC Hystrix brachyura Malayan porcupine 160 P, L, H, A, F LC Mustelidae Martes ﬂ avigula Yellow-throated marten 17 P, L, H, F Viverridae Arctictis binturong Binturong 7 P, L, H Hemigalus derbyanus Banded palm civet 13 P, L, H, A, F EN Paguma larvata Masked palm civet 21 P, L, H, A Paradoxurus hermaphroditus Common palm civet 1 L Prionodon linsang Banded linsang 7 P, L, H, A VU Herpestidae Herpestes javanicus Javan mongoose 1 H Felidae Catopuma temminckii Asian golden cat 43 P, L, H, A, F VU Panthera pardus Leopard 2 P, L VU P. tigris Tiger 5 P, H EN Pardofelis nebulosa Clouded leopard 4 H VU Prionailurus bengalensis Leopard cat 13 P, L, H, A Tapiridae Tapirus indicus Malayan tapir 99 P, L, H, A EN Suidae Sus scrofa Common wild pig 426 P, L, H, A, F Tragulidae Tragulus kanchil Lesser mouse deer 58 P, L, A, F T. napu Greater mouse deer 12 P, L, F EN Cervidae Muntiacus muntjak Common barking deer 396 P, L, H, A, F Bovidae Naemorhedus sumatraensis Southern serow 1 H NT Bat spp. Bat spp. 5 L, H, A Mammal total 35 spp. 2,053 Aves Accipitridae Spilornis cheela Crested serpent eagle 1 H Phasianidae Argusianus argus Great argus 18 L, H VU Gallus gallus Red junglefowl 1 A Columbidae Chalcophaps indica Emerald dove 2 F Bucerotidae Anorrhinus galeritus Bushy-crested hornbill 1 H NT Turdidae Zoothera citrina Orange-headed thrush 1 P Copsychus malabaricus White-rumped shama 1 F Bird spp. Bird spp. 3 P, H Bird total 8 spp. 28 Reptilia Varinidae Varanus sp.1 Monitor lizard 6 L, H, A, F Reptile total 1 spp. 6 2,087

148 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Mammals accounted for 98.3 percent of all animals identifi ed fi rst year than during the second or third years (Fig. 3). In from the photographs. Of the identifi ed species, wild boar, contrast, the number of species photographed during the Sus scrofa, was the most frequently photographed (426 second compared to the third year did not significantly times, 20.4% of the total), followed by common barking differ in either the primary or logged forest. Most animal deer, Muntiacus muntjak (396 times), red spiny rat, Maxomys species were photographed in the fi rst year (93% of recorded surifer (293 times), pig-tailed macaque, Macaca nemestrina species in both the primary and logged forests). Similarly, (237 times), and Malayan porcupine, Hystrix brachyura (160 the number of species photographed within the fi rst 12 mo times). These fi ve species accounted for 72.5 percent of all accounted for 85% of the total species recorded for 18 mo identifi ed photographs. In contrast, six species of mammals in the hill forest. and fi ve species of birds were photographed only once during the study (Table 1). Most animals were photographed alone Activity period. – The activity periods were based on fi ltered or in pairs, except for the Malayan porcupine (up to three data and were determined for only 18 species (Fig. 4). Six individuals), pig-tailed macaque (up to six individuals), and species of mammals (Echinosorex gymnurus, Leopoldamys wild boar (up to 17 individuals). Of the 44 animal species sabanus, Maxomys surifer, Hystrix brachyura, Hemigalus photographed, 21 are listed in the Thailand Red Data derbyanus, and Prionailurus bengalensis) were classifi ed as Book, including four endangered, 11 vulnerable, four near nocturnal, whereas three mammal species and one bird species threatened, and two species of least concern (Table 1). (Macaca nemestrina, Trachypithecus obscurus, Tupaia glis, and Argusianus argus) were considered diurnal. Species accumulation curves. – In total, 30, 28, and 26 species were photographed in the primary, logged, and hill forests, respectively. The identity of species substantially overlapped in the primary and logged forests (24 species in common) but overlapped to a lesser extent in the logged and hill forests (19 species) and the hill and primary forests (17 species). Rarefaction of the source pool of species sampled in each forest indicated no differences among forests in the relationship between sampling effort and recorded species richness (Fig. 2). The number of photographs per 100 camera-days also did not differ among forest types: 20.2 ± 4.3 (mean ± SD) in the primary forest, 17.1 ± 14.4 in the logged forest, and 16.6 ± 11.4 in the hill forest. Similarly, the number of photographed species per 100 camera-days Fig. 3. Rarefaction curves for photo-captured animal assemblages did not substantially differ among forests: 1.9 ± 0.6 in the in primary and logged forests over 3 years (thick line: fi rst year; primary forest, 2.1 ± 0.9 in the logged forest, and 3.1 ± 1.7 open circles: second year; solid circles: third year) in the Hala-Bala in the hill forest. Wildlife Sanctuary, Thailand. The dotted line represents the 95% CI for the fi rst year. For clarity, the 95% CI for the second and In both the primary and logged forests, the number of third years are not presented. photographed species was signifi cantly higher during the

Fig. 2. Rarefaction curves for photo-captured animal assemblages in three forest types (thick line: primary forest; open circles: logged forest; solid circles: hill forest) in the Hala-Bala Wildlife Sanctuary, Fig. 4. Activity periods of photo-captured animals (N>10) in Thailand, from Nov.2004 to Oct.2007. The dotted line represents the Hala-Bala Wildlife Sanctuary, Thailand, from Nov.2004 to the 95% CI for the primary forest. For clarity, the 95% CI for the Oct.2007. Species are listed in order of decreasing frequency of logged and hill forests are not presented. diurnal activity. Numbers in parentheses indicate sample size.

149 Kitamura et al.: Mammal diversity of a Thai forest

DISCUSSION Davison, 2006; Dinata et al., 2008). In Bala, the call of this species is also the most commonly heard birdsong; Species diversity of mammals and birds photographed in thus, camera trapping would not be necessary for a general Bala. – Our study revealed that at least 44 species of animals, survey. Although camera trapping provides some baseline of which 21 (47.7%) are listed in the Thailand Red Data information for species records (Mohd-Azlan & Davison, Book, were found in an isolated forest of Bala in southern 2006) and can sometimes detect very rare species (Dinata Thailand. One method of assessing the relative conservation et al., 2008), we did not record any new birds for the Bala value of Bala is to compare its species richness as assessed forest. For certain mammal species, camera trapping is by photography to that evaluated by photography elsewhere, a promising survey technique that generates useful data; assuming that higher species richness implies higher quality however, camera trapping used solely for the study of birds habitat. The species richness of large- and medium-sized is impractical in Bala. mammals photographed in the Jerangau Forest Reserve, Peninsular Malaysia, was 27 species over 5,972 camera-days Activity periods of mammals. – Research into animal activity (Mohd-Azlan, 2006), and that of three study sites in Taman periods using camera trapping in tropical forests in Southeast Negara National Park, Peninsular Malaysia, was 27 species Asia is increasing (Griffi ths & van Schaik, 1993a; b; van over 4,336 camera-days, 25 over 4,847 camera-days, and 26 Schaik & Griffi ths, 1996; Miura et al., 1997; Mohd-Azlan over 4,871 camera-days (Kawanishi, 2002). Compared to & Sharma, 2003; Grassman et al., 2005a; Grassman et al., these studies, the species richness of large- and medium-sized 2006; Mohd-Azlan, 2006; Mohd-Azlan & Engkamat, 2006; mammals (not including that of small mammals belonging Mohd-Azlan & Sharma, 2006; Suzuki et al., 2006; 2007). to Tupaiidae, Erinaceidae, Sciuridae, Muridae, and bats) in For 11 animal species, we found documentation of activity Bala was relatively low (21 species). periods for the same species in previous studies from the Phu Kheio Wildlife Sanctuary (Grassman et al., 2005a; Grassman Despite the huge sampling effort in our study, we did et al., 2006) and Khao Yai National Park (Suzuki et al., 2006; encounter certain limitations that deterred us from examining 2007) in Thailand and Jerangau Forest Reserve (Mohd-Azlan, the relative importance of the Bala forest in greater depth. 2006), Taman Negara National Park (Kawanishi & Sunquist, Because we continuously maintained our camera trappings at 2004), and Pasoh Forest Reserve (Miura et al., 1997) in the same locations for three years, and the minimum distance Peninsular Malaysia (Table 2). There were no differences between each camera location was short (300–500 m), the between the activity periods determined in our study and effective sampling area in our study was rather limited. those reported in the previous studies, with the exception of Although the rarefaction curve for photo-captured animal the leopard cat, which we classifi ed as nocturnal but others assemblages continued to increase throughout the study categorised as arrhythmic (Table 2). The activity periods period (Fig. 2), the number of species photographed in the fi rst of mammals common to Bala generally do not differ from year included most of the photographed species. Some species those at other study sites, despite its small isolated habitat may actually be more abundant or even restricted to one surrounded by agricultural areas, such as fruit orchards and habitat type. To increase the probability of capturing species rubber plantations. In areas severely disturbed by humans, that rarely use trails or are habitat specialists, it is important some large game mammals shift their activity periods from to ensure that all major habitat types are sampled. Indeed, diurnal to nocturnal (Griffi ths & van Schaik, 1993a; b; van clouded leopard and southern serow were not recorded in Schaik & Griffi ths, 1996). We did not observe this trend at the primary or logged forests over the three study years but our sites, nor did we record any hunting of large animals were observed in the hill forest during one year. Even in the during our study, although we did witness the collection of primary and logged forests, several rare species in Bala, such non-forest timber products (e.g., wild fruits and mushrooms) as the Asian elephant Elephas maximus and the Malayan and the trapping of small passerines (e.g., bulbuls and leaf sun bear Ursus malayanus went undetected by our camera birds) by local peoples. Thus, we believe that the effect of trappings. To prevent camera malfunction, no cameras were direct poaching on large mammals in Bala is negligible, and deployed near streams due to fl ooding or near steep rocky the activity period of these animals is likely not affected by slopes. Together, these factors indicate that a comprehensive such human activities. mammal list has yet to be compiled for this area, particularly for secretive animals that are strictly arboreal or associated The protected area of Bala is only 111.5 km2, a threshold with aquatic habitats. To obtain a complete list of the below which tigers and some other large mammals may mammals of Bala, other methods of observation must be rapidly become extirpated from this region (Laidlaw, 2000). combined with camera-trapping studies. Most large mammals photographed in this study have large home ranges (Table 3) and require large areas of contiguous In our photographs, bird species accounted for only 1.7 forest for their long-term survival (Karanth & Nichols, 2002). percent of all animals identifi ed. In general, the frequency Habitats for large mammals are highly fragmented and are of photographed mammals is much greater than that of lost through the construction of roads, power networks, birds in tropical forests of Southeast Asia (Miura et al., plantations, urban expansion, dams, irrigation, and other 1997; Mohd-Azlan & Davison, 2006; Dinata et al., 2008). development in this region (Bird Conservation Society The great argus Argusianus argus, a true ground dweller, of Thailand, 2004; Lynam et al., 2007). Although we did was the most commonly photographed bird species (Table not record any animals that were previously unknown to 1), as previously reported in this region (Mohd-Azlan & Bala, we did confi rm the existence of some endangered

150 THE RAFFLES BULLETIN OF ZOOLOGY 2010 ve different sites in Thailand and Peninsular Malaysia. Activity abbreviations: D: diurnal; N: This study (Grassman et al., (Suzuki et al., (Mohd-Azlan, 2006) (Kawanishi & (Miura et al., 1997) Thailand Peninsular Malaysia Peninsular D D D Thailand treeshrew N rat N N nocturnal; A: arrhythmic. Species Common Pig-tailed macaque Noisy Red spiny rat Malayan porcupine Asian golden cat D Leopard cat Malayan tapir Common wild pig N Lesser mouse deer N Common barking deer A D N A A 2005a; 2006) A A N 2006; 2007) D A A A A N N D A A A A N Sunquist, 2004) A A A A A A D A A A A N A A Table 2. Comparison of activity periods 11 mammal species photographed in this study at ﬁ

151 Kitamura et al.: Mammal diversity of a Thai forest in tropical Asia are cited. NA: not available. 1.9–6.4 (Emmons, 2000) 1986) 1980) 1.9–6.4 (Emmons, 0.33 NA 62–828 (Caldecott, 17–33 (Curtin, 5.6–7.0 0.7–2.4 0.7–1.8 0.2–3.7 1991) NA 1991) 0.25–0.32 0.12–0.84 0.02–0.14 (Walker & Rabinowitz, 1992) NA NA NA (Lim & Ng, 2008) 350–1180 (Saiful et al., 2001) 1978) 470–650 (Saiful et al., 2001) NA (Saiful et al., 2001) 60–145 (Rabinowitz, (Wells et al., 2008) 210–630 (Rabinowitz, (Walker & Rabinowitz, 1992) NA 1994) (Nakagawa et al., 2007) NA 3260–4770 500–4800 7800 (Grassman et al., 2005c) 2290–4510 220–3710 (Grassman et al., 2005c) 1275 (Williams, NA 3.5–6.2 NA 647–592 (Heydon, (Grassman et al., 2005e) NA (Odden & Wegge, 2005) (Grassman et al., 2005e) (Lynam et al., 2001) (Grassman et al., 2005d) (Matsubayashi et al., 2003) avigula c name Home range (ha) References Tupaia glis Tupaia gymnurus Echinosorex Macaca nemestrina obscurus Trachypithecus Manis javanica Callosciurus caniceps C. notatus Lariscus insignis Rhinosciurus laticaudatus Leopoldamys sabanus Maxomys surifer M. whiteheadi Sundamys muelleri Atherurus macrourus Hystrix brachyura Martes ﬂ binturong Arctictis Hemigalus derbyanus Paguma larvata Paradoxurus hermaphroditus Prionodon linsang Herpestes javanicus Catopuma temminckii Panthera pardus tigris P. nebulosa Pardofelis Prionailurus bengalensis indicus Tapirus Sus scrofa kanchil Tragulus napu T. Muntiacus muntjak sumatraensis Naemorhedus Ptilocercus lowii Ptilocercus Erinaceidae Cercopithicidae Manidae Sciuridae Muridae Hystricidae Mustelidae Viverridae Herpestidae Felidae Tapiridae Suidae Tragulidae Cervidae Bovidae Table 3. Home-range sizes of various mammals photographed in the Hala-Bala Wildlife Sanctuary, Thailand. Only studies conducted Family Scientiﬁ Mammalia Tupaiidae

152 THE RAFFLES BULLETIN OF ZOOLOGY 2010 species in Thailand (Table 1). Therefore, our fi ndings are richness and shared species from samples. Version 8.0.0. crucial for the development of biodiversity conservation in User’s Guide and application published at: http://purl.oclc. this small fragmented forest that is largely surrounded by org/estimates. human-modifi ed landscapes. Because we are interested in Corbet, G. B. & J. E. Hill. 1992. The mammals of the Indomalayan the long-term management of relatively rare or threatened region: a systematic review. Natural History Museum species, unbiased estimates of density, which incorporate Publications, Oxford University Press, Oxford. some estimates of detectability, are more valuable than the Corlett, R. T. 2007. The impact of hunting on the mammalian fauna presence/absence or relative abundance data presented in of tropical Asian forests. Biotropica, 39: 292–303. this study. Measurements of density provide managers with Curtin, S. H. 1980. Dusky and banded leaf monkeys. In: Chivers, survey results that are comparable over time and space and D. J. (ed.). Malayan forest primates: ten years’ study in tropical are thus more accurate assessments of habitat suitability rain forest. Plenum Press, New York, USA. Pp. 107–145. in relation to different degrees of human disturbance. Cutler, T. L. & D. E. Swann. 1999. Using remote photography Thus, density estimates are the primary dataset necessary in wildlife ecology: a review. Wildlife Society Bulletin, 27: for monitoring populations and for assessing the success 571–581. or failure of conservation and management efforts. Such Dinata, Y., A. Nugroho, I. A. Haidir & M. Linkie. 2008. Camera studies have been conducted for hornbills in Bala (Gale & trapping rare and threatened avifauna in west-central Sumatra. Thong-Aree, 2006; Kemp et al., 2007), and further studies Bird Conservation International, 18: 30–37. of large- and medium-sized mammals in this highly valuable Dirzo, R., E. Mendoza & E. Ortiz. 2007. Size-related differential forest are warranted. seed predation in a heavily defaunated Neotropical rain forest. Biotropica, 39: 355–362. Emmons, L. H. 2000. Tupai: a fi eld study of Bornean treeshrews. ACKNOWLEDGMENTS University of California Press, London, UK. Fernando, P., T. N. C. Vidya, J. Payne, M. Stuewe, G. W. H. We thank the National Research Council of Thailand and Davidson, R. J. Alfred, P. Andau, E. Bosi, A. M. Kilbourn the Thailand Department of National Park, Wildlife and & D. J. Melnick. 2003. DNA analysis indicates that Asian Plant Conservation for collaboration and granting of permits. elephants are native to Borneo and are therefore a high priority We are indebted to staff of Thailand Hornbill Project and for conservation. PLOS Biology, 1: 110–115. 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156 THE RAFFLES BULLETIN OF ZOOLOGY 2010

POPULATION ASSESSMENT METHODS FOR THE SUNDA COLUGO GALEOPTERUS VARIEGATUS (MAMMALIA: DERMOPTERA) IN TROPICAL FORESTS AND THEIR VIABILITY IN SINGAPORE

Norman T-L. Lim Department of Biological Sciences, National University of Singapore, 14 Science Dr. 4, Republic of Singapore 117543 Current address: Department of Wildlife, Fish & Conservation Biology, University of California, Davis, One Shields Avenue. Davis, CA 95616, U.S.A. Email: [email protected] (Corresponding author)

Peter K. L. Ng Department of Biological Sciences, National University of Singapore, 14 Science Dr. 4, Republic of Singapore 117543 Email: [email protected]

ABSTRACT. – Colugos are arboreal folivores and are found in tropical rainforests of Southeast Asia. Despite their discovery roughly 200 years ago, colugos attracted relatively little scientifi c attention. Given the importance of population estimates in conservation decision-making, it is surprising that no colugo has been surveyed in tropical forest habitats. In this study, we assessed the possibility of using distance- sampling for estimating population size of Sunda Colugo (Galeopterus variegatus) in the protected forests of Singapore, and also compared this method with estimates from fi xed-width strip transect. We found that key assumptions of distance-sampling were not violated and the method provided relatively more precise estimates than fi xed-width strip transect. The population density estimate obtained was 0.535 (± 0.104) individuals per ha, and this translates to an estimated 1,074 ± 209 individuals within the 2,007 ha of protected forests in Singapore. We recommend the use of distance-sampling for the long-term monitoring of colugo populations and also discuss the viability of the species in Singapore.

KEY WORDS. – Flying lemur, distance-sampling, population estimate, ﬁ xed-width transect, conservation.

INTRODUCTION their life history and behaviour has been based on sporadic fi eld observations, and are mostly anecdotal (e.g. Medway, The mammal order Dermoptera comprises two species of 1978, Lekagul et al., 1988, Mendoza et al., 2001). Only colugos (or fl ying lemurs). These include the Sunda Colugo a handful of studies have focused on the behaviour and (Galeopterus variegatus) which resides in Java, Sumatra, ecology of colugos. The fi rst was an unpublished Honours Borneo, Malay Peninsula, Southeast Asian mainland year thesis (Tan, 1972), which reported on the behaviour (Medway, 1978; but see Jane ka et al., 2008) and recently of Malaysian G. variegatus in captivity. Unfortunately, documented from northern Laos (Ruggeri et al., 1998), and this was never published and remains unavailable to most the Philippine Colugo (Cynocephalus volans; known locally workers. The other was a Ph.D. dissertation on C. volans (see as kagwang) which occurs only in the southern islands of Wischusen 1990; Wischusen et al., 1989, 1992, 1998) which the Philippines (Mendoza et al., 2001). Colugos are arboreal investigated various aspects of foraging behaviour and social folivores and are found in tropical rainforests (Lim, 2007). behaviour. The fi nal study was a report on population size Their most striking feature is the extensive gliding membrane and diet of G. variegatus in a managed landscape of ca. 68 (or patagium) which enables them to travel up to 136 m in a ha in Singapore (Agoramoorthy et al., 2005). These studies single glide, and a corresponding decline in vertical height yielded some results contrary to information mentioned in of 10.5 to 12 m (Walker, 1983). older literature. For instance, most older records suggest a gestation period of 60 days but failed to present methods However, perhaps because of their nocturnal habits, cryptic employed or concrete evidence (see Kenneth et al., 1953); a coloration and that they seldom vocalise, colugos attracted much longer duration (150 days) was suggested by Wischusen relatively little scientifi c attention. Despite their discovery et al. (1992) for C. volans and even longer (180 days) by roughly 200 years ago, much of the available literature on Tan (1972) for G. variegatus.

157 Lim & Ng: Population assessment of colugo

Surprisingly, no colugo has been rigorously surveyed in We assessed the possibility of using distance-sampling their natural habitat of tropical forests. Even the study by (Burnham et al., 1985, Buckland et al., 1993) for estimating Agoramoorthy et al. (2005) was undertaken in a largely population size of the Sunda Colugo (G. variegatus landscaped environment at the Singapore Zoo. Many peninsulae) in the tropical forests in Singapore, and also biological studies require estimates (or absolute number) of compare this method with estimates from fi xed-width strip population size or rate of population change, and land-use transect. We provide an estimate for the population density managers require such baseline data to understand specifi c in Singapore and also discuss the viability of the species in habitat requirements, to justify conservation actions, and to Singapore. assess the success or failure of any such actions. Various census techniques exist (e.g. total counts, mark-recapture methods, point and line transects; Sutherland, 1996) and METHODS AND MATERIALS the technique should be selected based on the habitat, resource limitations and the species of interest. Even with Study Site. – We studied colugos in mainland Singapore the multitude of census techniques for different species, (1°16'N 103°51'E), an island state 699 km2 in area and situated most are mathematical models and thus require assumptions at the southern tip of the Malay Peninsula. The climate is which may be diffi cult or impossible to fulfi ll in the fi eld characterised by high relative humidity, temperature (daily (Seber, 1982). In addition, the extent to which individuals mean: 84.3% and 26.8°C respectively) and rainfall (annual vocalise, variation in the likelihood of being seen or caught, rainfall approximately 2,344 mm) (Tan et al., 2007). and their movement patterns all influence the accuracy of census techniques (Greenwood, 1996). Therefore, it is The primeval vegetation of Singapore was primarily lowland important for workers to be aware of these limitations and evergreen rainforest, which occupied about 82% of the area plan their methodology carefully. Census of arboreal species in the 1800s (Chou et al., 2006). Urbanisation and population is especially diffi cult and can often yield highly variable growth (currently about 4 million), these forest have been data (e.g. Carlos, 1996, Lindenmayer et al., 2003). This is reduced to just 279 ha, with a further 1,560 ha covered in especially true for cryptic and nocturnal arboreal species, tall secondary forest (Corlett, 1997, Tan et al., 2007). The and is perhaps a key reason behind the lack of ecological Central Catchment Nature Reserve possesses the largest studies on colugos. continuous tracts of old secondary forest in Singapore; this vegetation can be distinguished from primary forests by a Wischusen (1990) suggested that the highest priority for lower canopy and the absence of emergent species such as further research on colugos is to estimate population sizes the dipterocarps (Chou et al., 2006). The prominent species of these species, but he also recognised the diffi culties of in such forests include Rhodamina cinerea, Calophyllum conducting census in the tropical rainforest habitat. Perhaps species, Macaranga species and Archidendron clyperia (see due to the cryptic and inconspicuous nature of colugos, Tan et al., 2007). The Central Catchment Nature Reserve also they were often perceived to be rare and/or endangered. includes 168 ha of young regenerating forests that typically For example, Ho et al. (1994) gave a conservative estimate have lower and incomplete canopy cover. of 200 individuals in Singapore based on what their group observed, and as such, the species was regarded as highly Transect survey. – We conducted 61 variable-width transects endangered. Nevertheless, based on personal sightings of the (each 200 m long) within the protected forests of Bukit Timah fl ying lemurs over the past years and recorded sightings in Nature Reserve and Central Catchment Nature Reserve. To various places of Singapore (e.g. Yeo, 1991, Yeo et al., 1992, reduce the infl uence of edge effects, we restricted the censuses Subaraj et al., 1995), the population of Singapore colugos to small footpaths or trails (< 2 m wide) which were under almost certainly exceeds the conservative estimate of Ho et continuous canopy cover of the rain forest. To minimise al. (1994), and in the latest assessment of Singapore mammal stochastic infl uences, we surveyed each transect three times fauna, the species has been removed from the threatened list throughout the sampling period of February to June 2006. (see Davison et al., 2008). We only recorded sightings by the fi rst author; this eliminated Censuses typically employ fixed-width strip transects, observer differences (e.g. height differences and search image which assume that all subjects within the strip transect are of the observer) which can lead to problematic estimates detected (Greenwood, 1996). Unfortunately, this method has (Buckland et al., 1993). We walked each transect between limited applications for arboreal cryptic species in complex 2000 and 2359 hours, on nights without strong winds or rain. environment like closed forest, because the probability of This is known to be the active period of the Philippine Colugo detecting the subject falls rapidly with increasing distance (Wischusen & Richmond, 1998), and the authors have also from the observer. Distance-sampling (also known as observed most activity during this period for G. variegatus. variable-width transect), on the other hand, models the Surveys were conducted at a speed of about 1 km h-1, similar detection function based on the decline in observations with to velocities reported in other closed terrain transects (e.g. increasing distance (x) and requires only that all objects on Carlos, 1997, Chiarello et al., 2001). We employed small the transect line are detected (i.e. x = 0; Buckland et al., spotlights (3-watt L.E.D. fl ashlights) whenever visibility 1993). Additionally, distance-sampling requires objects to be allowed. Scanning at further distances and confi rmation of detected at their initial location and assumes that distances sightings was done with a 1,000,000 candlepower spotlight are measured accurately (Buckland et al., 1993). and Leitz 10 × 40 BA Trinovid binoculars. Extra care and

158 THE RAFFLES BULLETIN OF ZOOLOGY 2010 effort was concentrated on the scanning of trees near the RESULTS transect line. This was because the most important assumption for distance-sampling is that all animals on the line must be The sampling regime yielded 34 observations of Galeopterus detected (Buckland et al., 1993). variegatus. The furthest observer-object distance was 21 m. We recorded the perpendicular distance of the animal from the centre of the footpath using a measuring tape (< 14 Fixed-width strip transect. – When constraining observations m) or laser rangefi nder (> 14 m; Bushnell Yardage Pro, to 10 m wide strip transects, 61.8% of the observations (n = Bushnell Corporation, USA). Only independent colugos 21) were included and population density was estimated at were recorded for calculation of population density (i.e. we 0.574 (± 0.145) ind/ha. Broader transects encompassed 85.3% excluded dependent young clinging to their mothers). Any and 100% of observations (20 and 40 m respectively; n = unweaned young normally are hidden within the patagium, 29 and 34), and yielded density estimates of 0.396 (± 0.079) rendering it almost impossible to ascertain their presence and 0.232 (± 0.050) ind/ha. From these transects, population on every occasion. Additionally, independent animals are of estimates of colugo in the 2007 ha of forests in Singapore greater ecological signifi cance since they are the essential ranged from 466 to 1152 (Table 1). consumers of resources. Distance-sampling. – As indicated above, we removed the Distance-sampling analysis. – We pooled all sightings and furthest 5% of the sightings to truncate our data. This resulted analysed them using software DISTANCE (version 5.0; in a reduction from 34 sightings to 32. Buckland et al., 1993). Before model fi tting, we truncated the furthest 5% of observations because they are diffi cult The uniform key function adjusted with cosine series to model and provided little information for estimating the expansion (also known as the Fourier series model) possessed density function at zero distance, the most crucial part of the lowest AIC score and produced a population density the curve. In addition, truncation often reduces bias and/or estimate of 0.535 (± 0.104), with an effective strip width of improves precision in density estimates (Buckland et al., 8.17 m (see Table 2). Additionally, the coeffi cient of variation 1993). In the exploratory phase, the following fi ve models for this model was < 20% and therefore was deemed to be were utilised to generate the density estimate: a uniform reasonably precise, as suggested by Buckland et al. (1993). key function adjusted with either a cosine series expansion The detection probability function of the Fourier series model or simple polynomial series expansion, a half-normal key (Fig. 1) showed a “shoulder” and implied that there was function adjusted with cosine series expansion or Hermite no evasive behaviour exhibited by the subject. It was also polynomials, and a hazard-rate key function adjusted with noteworthy that the density estimates obtained by the other cosine series expansion. models were very similar to that by the Fourier series model, differing by less than 5%. Using the most parsimonious The criterion for selecting the best-fi t model was minimum model, we estimated that the colugo population was 1074 (± Akaike’s Information Criterion (AIC); AIC provides a 209) individuals in the 2007 ha of protected lowland forest quantitative method of model selection (Akaike, 1985) and of Singapore. is an integral part of DISTANCE software (Buckland et al., 1993). The best-fi t model was also checked for fi t near zero distance in the detection histogram (to investigate whether DISCUSSION the most important assumption, full detection on the line, has been met) and a presence of a “shoulder” in the histogram To the best of our knowledge, this is the first study to meeting the shape criterion mentioned by Buckland et al. investigate the suitability of various forms of line transect (1993). methods for assessing population density of G. variegatus in tropical forests. Fixed-width strip transect analysis. – To evaluate the effectiveness of strip-transects with varying cutoff distance, Fixed-width strip transect. – As no other studies have compared methods for estimating the population density of we calculated three density estimates using = , colugos, the appropriate strip width that should be used is not where is the density estimate, n the number of individuals clear. Because use of an incorrect cutoff distance can lead to sighted, L the length of the transect (i.e. 200 m) and 2W the gross deviation from the true population density, we provided width of the transect. Due to the limited visibility in the a range of cut-off distances for the analysis of fi xed-width forest environment, the three cutoff distances from the line strip transect (see National Research Council, 1981). of observation were 5 m, 10 m and 20 m (i.e. strip-transect with width 10, 20 and 40 m respectively). From the results, it was evident that with each doubling of the area covered by the strip transect (i.e. from 10 m width Throughout this paper, population density is reported as to 20 m, and from 20 m width to 40 m), the number of number of individuals per ha (± SE), and only applies for observations did not increase correspondingly (i.e. from 21 independent colugos. to 29 to 34, respectively). This likely refl ects rapid reduction

159 Lim & Ng: Population assessment of colugo

Table 1. Estimated population density ( ) of Sunda Colugos (Galeopterus variegatus) and total population size in Singapore (2007 ha) using ﬁ xed-width strip transects.

Width of Fixed Transect Parameters 10 m 20 m 40 m Number of observations 21 29 34 (+/- S.E.) 0.574 (± 0.145) 0.396 (± 0.079) 0.232 (± 0.050) Estimated population size 1,152 (± 291) 795 (± 159) 466 (± 100) C.V. 25.3% 19.9% 21.6%

in visibility with distance. As colugos are cryptic species from distances up to 43 m (unpublished data). Despite these and rarely vocalise, the only mode of detection is by visual arguments in favour of our sampling, density estimates cues, especially the strong eye-shine during spotlighting. provided here should be treated conservatively, as numbers Thus, within the complex three-dimensional space of tropical may be higher than we were able to document. forests, it is expected that visibility is reduced drastically with increasing distance, leading to disproportional decrease Although Buckland et al. (1993) recommended a minimum in detection probability. of 40 sightings for the calculation of reliable population densities, the selected model produced from distance- As a result, it is most likely that the density estimates from sampling of 32 sightings (i.e. the Fourier series model) the larger fi xed-width strip transects under-estimated colugo possessed a coeffi cient of variation lower than 20% and numbers. Consequently, we argue that the most appropriate was thus deemed to be reasonably precise, as suggested by strip transect used here was the narrowest, 10 m. This was Buckland et al. (1993). In addition, the other models possessed supported by distance-sampling procedures, which indicated a coeffi cient of variation slighter greater than 20% (Table 2) that the effective width of variable-width methods was but also yielded density estimates with a difference of less approximately 8 m (see below). than 5%. We therefore felt confi dent that the data presented here yielded consistent and reasonably precise estimates with Distance-sampling. – The presence of a “shoulder” in the the various options of modeling. detection probability function (Fig. 1) indicates that the Sunda Colugo was not exhibiting evasive behaviour (characterised Comparison of the two methods. – When comparing results by a peak in observations away from the line transect). These of the two methods, the 10m-wide strip transect produced an data agree with our observations that colugos normally do estimate that is 7.3% greater than that by the best distance- not behave adversely to human presence, regardless of sampling model. Even though both approaches utilised the day or night. Even though colugos are capable of gliding same dataset in this study, the former disregarded observations away from approaching humans, they often continued with beyond the transect boundary while the latter incorporated their activities and tolerated further approach and visual 95% of the sightings after truncation for the modeling of observation, provided that a weaker fl ashlight was used for illumination after the initial encounter. This absence of evasive behaviour may be attributed to the apparent lack of hunting in Singapore. Thus, it is probable that observations made during this study were at their initial positions, thus meeting a key assumption.

We made extra effort to scan for colugos near the line transect. However, we could not confi rm full detection along the line transect in this study, which is another assumption in distance-sampling method (and also for the fi xed-width line transect method; see below). We believe that in the three-dimensional space and density of tropical rainforests, full detection of arboreal species can be attained only by sampling at all possible heights (up to 45 m in tropical lowland rainforests) and is practically impossible for most studies. Nevertheless, we are confi dent that we detected most, if not all, colugos near the transect line because during their active period (from 2000 to 2359 hours), colugos exhibit increased activity (e.g. foraging along tree branches) which aid in the detection of their presence. Additionally, spotlighting during the night also enhanced the detection of colugos by making Fig. 1. The detection probability function of the Fourier series use of their eye-shine, an additional cue of their presence, model after removing the extreme 5% of observations.

160 THE RAFFLES BULLETIN OF ZOOLOGY 2010 AIC C.V. Δ cient of variation (C.V.) and AIC values. ) in Singapore using distance-sampling analysis. Estimates determined program DISTANCE. Presented Galeopterus variegatus dence interval (95% C.I.), coefﬁ (± S.E.) ESW 95% C.I. AIC

) of Sunda Colugos ( Uniform + cosine series Half-normal + cosine series Half-normal + Hermite Hazard-rate + cosine series Uniform + simple polynomials * denotes lowest AIC values; ** C.V. < 0.200. 0.535 (± 0.104) 0.541 (± 0.115) 0.541 (± 0.115) 0.554 (± 0.150) 0.535 (± 0.116) 8.17 8.08 8.08 7.89 8.17 0.366-0.783 0.357-0.820 0.357-0.820 0.326-0.942 0.350-0.819 160.95 * 161.51 161.51 161.89 162.74 0 0.56 0.56 0.91 1.79 0.194 ** 0.212 0.212 0.270 0.217 Parameters are density estimates, effective strip width (ESW), 95% conﬁ Table 2. Estimated population density (

161 Lim & Ng: Population assessment of colugo the detection probability function. Thus, the fi xed-width contrast, the Night Safari consists of secondary rainforest strip transect method excludes data which are potentially vegetation of the Central Catchment Nature Reserve with informative, possibly resulting in the slight difference in minimal landscaping. Although the observers performing density estimates obtained. the sampling were different in these two studies, distance- sampling still yielded similar population density estimates Importantly, the coeffi cient of variation of the 10 m fi xed- for the two small plots of semi-artifi cial landscape that are width strip transect was much greater than that of the nested within the study site of this study (i.e. the Central variable-width model. Thus, by making use of the additional Catchment Nature Reserve). sightings to model the detection probability function, distance-sampling is likely to be more precise and thus more Therefore, we are confi dent that our study provided suffi cient sensitive to changes in population densities. This advantage evidence that distance-sampling is a suitable technique for in greater precision is not the result of additional sampling as the long-term monitoring of Sunda Colugo in the complex similar effort was invested for both methods (i.e. the same three-dimensional space of tropical rainforests. amount of time and distance covered), with the exception that sightings further than 5m from transect line were disregarded Future of Galeopterus variegatus in Singapore. – We for the fi xed-width strip transect. As such, we believe that estimated that 1,074 ± 209 individuals exist within the 2007 distance-sampling is a more appropriate method for long- ha of protected forests in Singapore (i.e. Bukit Timah Nature term monitoring of colugo populations in forested habitats. Reserve and Central Catchment Nature Reserve). Boinski et al. (1998) argued that local extinction of similar-sized General discussion. – Most transect surveys of arboreal and arboreal neotropical squirrel monkeys (Saimiri spp.) mammals have been of primates (e.g. Nijman et al., 2005), was almost certain when group size dropped to less than 15 and were not without criticisms. First, there are few sites members and had less than about 30 hectares of available whereby primates are not disturbed or hunted by humans. As habitat. If this is a valid comparison, it suggests that colugos such, most primates are wary of human presence and exhibit in Singapore constitute a healthy and almost certainly viable evasive behaviour upon contact, thereby violating one of population, both in terms of population numbers and amount the important assumptions in distance-sampling (Marshall of available habitat. Nevertheless, we stress that proper et al., 2008). Additionally, most primates are gregarious baseline data (e.g. lifespan and fecundity) for a detailed and occur in social groups of several to as many as a few population viability analysis (White, 2000) is currently not hundred individuals (Barton et al., 1992, Swindler, 1998). available for the colugos. Therefore, it may be diffi cult to ascertain the group spread and thus measure the exact distance from transect to the In Singapore, colugos can be reliably found only from the centre of the group, violating another important assumption Central Catchment Nature Reserve and Bukit Timah Nature (Marshall et al., 2008). Reserve thus far. While there were unsubstantiated sightings from Khatib Bongsu (S. Rajathurai, pers. comm.) and small The above-mentioned issues do not seem to be relevant peripheral populations outside the central catchment area to colugos. As discussed earlier, evasive behaviour likely (e.g. the German European School at Bukit Tinggi; Yeo was absent in this study, probably because of the lack of & Lim, 1992), these sites have been surveyed and there hunting in Singapore. Furthermore, colugos are normally is no indication that colugos are present in any substantial encountered singly (with the exceptions of female colugos numbers. with their young on their undersides) and the distance to the individuals, rather than group centroids, was used for the In the recent years, however, there have also been confi rmed distance-sampling. As a result, although the Sunda Colugo, sightings of colugos at the Bukit Batok Nature Park (T. T. like most primates, is arboreal, there is no clear violation of the assumptions in distance-sampling.

Density estimates reported here compare well with those obtained at the Singapore Zoo and Night Safari, where Agoramoorthy et al. (2005) reported 0.550 ± 0.078 and 0.601 ± 0.078 ind/ha respectively. The Singapore Zoo (about 28 ha) and the Night Safari (about 40 ha) are located within the Central Catchment Nature Reserves and there is contiguous vegetation connecting the localities. Although vegetation at the Singapore Zoo was landscaped to a large extent, the high density of mature trees constitutes a semi- open landscape which resembles the structure of a tropical secondary forest. Furthermore, the great diversity of native and non-native trees planted within the compound might also prove to be attractive for colugos, as colugos are generalists Fig. 2. Map showing the separation between Bukit Timah Nature and feeds on leaves from a large variety of plant species Reserve and Bukit Batok Nature Park (location with new sightings (Wischusen et al., 1998, Agoramoorthy et al., 2005). In of Sunda Colugo).

162 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Guttensohn, Y. Cai, pers. comm.). This park is 36 ha and has Carlos, A. P., 1996. Population status of white-lipped Tayassu remnant forests which are separated from the edge of Bukit pecari and collared peccaries T. tajacu in hunted and unhunted Timah Nature Reserve by a road (Fig. 2). Given the colugo’s Amazonian forests. Biological Conservation, 77: 115–123. ability to glide up to 136 metres, even crossing roads (Lim, Carlos, A. P., 1997. Effects of habitat quality and hunting pressure 2007), expansion to the latter reserve is reasonable and is a on arboreal folivore densities in Neotropical forests: A case piece of positive evidence that the colugo is likely to persist study of howler monkeys (Alouatta spp.). Folio Primatologica, in the remaining forests of Singapore. 68: 199–222. Chiarello, A. G. & F. R. de Melo, 2001. Primate population Conclusion. – The present study focuses on the tropical densities and sizes in Atlantic forest remnants of northern forests in Singapore — which is a heterogeneous matrix of Espírito Santo, Brazil. International Journal of Primatology, different forest types, with mature secondary forest being 22(3): 379–396. the biggest component (ca. 77%). Although the population Chou, L. M., H. T. W. Tan & D. C. J. Yeo, 2006. The Natural density obtained in this study may not be applicable to Heritage of Singapore. Prentice Hall, Singapore. 244 pp. other pristine sites in the animal’s range, we are confi dent Corlett, R. T., 1997. The vegetation in the nature reserves of that distance-sampling has the potential to be a standard Singapore. The Garden’s Bulletin, Singapore, 49(2): 147– protocol for colugo population estimation. While colugos 160. are likely to persist in Singapore, this scenario is contingent Davison, G. W. H., P. K. L. Ng & H. C. Ho (eds.), 2008. The on the continued existence of tropical forests in land-scarce Singapore Red Data Book. Threatened Plants and Animals of Singapore as current knowledge about its ecology suggests Singapore. Second Edition. Nature Society, Singapore, 285 that it is strictly a forest-dwelling animal. With many of pp. the large- and medium-sized mammals extirpated from the Greenwood, J. J. D., 1996. Basic techniques. In: Sutherland, W. J. forests of Singapore, the charismatic but enigmatic Sunda (ed.). Ecological Census Techniques: A Handbook, Cambridge Colugo has the clear potential to be a fl agship species for University Press, Cambridge. Pp. 11–110. the conservation scene in Singapore. Ho, H. C., R. Subaraj, S. L. Yeo & C. M. Yang, 1994. Checklist of threatened species: mammals. In: Ng, P. K. L. & Y. C. Wee (eds.). The Singapore Red Data Book, Nature Society, ACKNOWLEDGEMENTS Singapore. Pp. 248–267. Jane ka, J. E., K. M. Helgen, N. T-L. Lim, M. Baba, M. Izawa, We thank the National Parks Board for permission to conduct Boeadi & W. J. Murphy, 2008. Evidence for multiple species fi eldwork in the Nature Reserve of Singapore. Special thanks of Sunda colugo. Current Biology, 18(21): R1001–R1002. to: Benjamin Lee, Rachel Lim, Ping Ting Chew and many Kenneth, J. H. & G. R. Ritchie, 1953. Gestation periods. 3rd other staff at National Parks Board; Douglas Kelt, Sara edition. Commonwealth Bureau Animal Breeding and Genetics, Krause, Kelvin Lim, Jaya Smith for constructive discussions; Technical Communication, 5: 1–39. and all the volunteers, especially Kwok Wai Chan, Lena Lim Lekagul, B. & J. A. McNeely, 1988. Mammals of Thailand. and Alan Yeo. We also thank Yixiong Cai, Teresa Guttensohn Association for the Conservation of Wildlife, Bangkok. 758 and Subaraj Rajathurai for the additional sightings, and pp. are grateful for the fi nancial support provided by National Lim, N. T-L., 2007. Colugo: The Flying Lemur of South-east Asia. University of Singapore. Draco Publishing, Singapore. 80 pp. Lindenmayer, D. B., R. B. Cunningham, C. MacGregor, R. D. Incoll & D. Micheal, 2003. A survey design for monitoring the LITERATURE CITED abundance of arboreal marsupials in the Central Highlands of Victoria. Biological Conservation, 110: 161–167. Agoramoorthy, G., C. M. Sha & M. J. Hsu, 2005. Population, Marshall, A. R., J. C. Lovett & P. C. L. White, 2008. Selection diet and conservation of Malayan fl ying lemurs in altered of line-transect methods for estimating the density of group- and fragmented habitats in Singapore. Biodiversity and living animals: lessons from the primates. American Journal Conservation, 15(7): 2177–2185. of Primatology, 70(5): 452–462. Akaike, H., 1985. Prediction and entropy. In: Atkinson, A. C. & S. Medway, L., 1978. The Wild Mammals of Malay Peninsula and E. Fienburg (eds.). A Celebration of Statistics, Springer-Verlag, Singapore. Oxford University Press, Kuala Lumpur. 128 pp. Berlin. Pp. 1–24. Mendoza, M. M. & C. C. Custodio, 2001. Field observations on the Barton, R. A., A. Whiten, S. C. Strum, R. W. Byrne & A. J. Simpson, Philippine fl ying lemur (Cynocephalus volans). In: Goldingay, 1992. Habitat use and resource availability in baboons. Animal R. L. & J. Scheibe (eds.). Biology of Gliding Mammals, Filander Behaviour, 43(5): 831–844. Press, Fürth. Pp. 273–280. Buckland, S. T., D. R. Anderson, K. P. Burnham & J. L. Laake, National Research Council, 1981. Techniques for the Study 1993. Distance Sampling: Estimating Abundance of Biological of Primate Population Ecology. National Academy Press, Populations. Chapman & Hall, London. 446 pp. Washington DC. 233 pp. Burnham, K. P., D. R. Anderson & J. L. Laake, 1985. Effi ciency Nijman, V. & S. B. J. Menken, 2005. Assessment of census and bias in strip and line transect sampling. Journal of Wildlife techniques for estimating density and biomass of gibbons Management, 49: 1012–1018. (Primates: Hylobatidae). 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Ruggeri, N. & M. Etterson, 1998. The fi rst records of colugo White, G. C., 2000. Population viability analysis: data requirements (Cynocephalus variegatus) from the Lao P.D.R. Mammalia, and essential analyses. In: Boitani, L. & T. K. Fuller (eds.). 62(3): 450–451. Research Techniques in Animal Ecology: Controversies and Seber, G. A. F., 1982. The Estimation of Animal Abundance and Consequences, Columbia University Press, New York. Pp. Related Parameters. Charles Griffi n, London. 654 pp. 288–331. Subaraj, R., K. K. P. Lim & R. Teo, 1995. Mammals. The Pangolin: Wischusen, E. W., 1990. The foraging ecology and natural history a bulletin on vertebrates of Singapore and the surrounding of the Philippine fl ying lemur (Cynocephalus volans). Cornell area, 8: 1. University, Ithaca. 123 pp. Sutherland, W. J., 1996. Why census? In: Sutherland, W. J. (ed.). Wischusen, E. W., N. R. Ingle & M. E. Richmond, 1992. Ecological Census Techniques: A Handbook, Cambridge Observations on the reproductive biology and social behaviour University Press, Cambridge. Pp. 1–10. of the Philippine fl ying lemur (Cynocephalus volans). Malayan Nature Journal, 46: 65–71. Swindler, D. R., 1998. Introduction to the Primates. University of Washington Press, Seattle. 284 pp. Wischusen, E. W. & M. E. Richmond, 1989. Techniques for capturing and marking Philippine fl ying lemur (Cynocephalus Tan, H. T. W., L. M. Chou, D. C. J. Yeo & P. K. L. Ng, 2007. volans). Malayan Nature Journal, 43: 100–105. The Natural Heritage of Singapore. Prentice Hall, Singapore. 271 pp. Wischusen, E. W. & M. E. Richmond, 1998. Foraging ecology of the Philippine fl ying lemur (Cynocephalus volans). Journal of Tan, W. C., 1972. Field work and laboratory studies of the mammal Mammalogy, 79(4): 1288–1295. Cynocephalus variegatus. National University of Singapore, Singapore. 105 pp. Yeo, S. H., 1991. Mammals. The Pangolin: a bulletin on vertebrates of Singapore and the surrounding area, 4: 3. Walker, E. P., 1983. Mammals of the World. John Hopkins University Press, Baltimore. 1362 pp. Yeo, S. H. & K. K. P. Lim, 1992. Mammals. The Pangolin: a bulletin on vertebrates of Singapore and the surrounding area, 5: 1.

164 THE RAFFLES BULLETIN OF ZOOLOGY 2010

MORPHOMETRIC ANALYSIS OF TRIANCHORATUS PRICE & BERRY, 1966 (MONOGENEA: HETERONCHOCLEIDINAE) FROM CHANNA SPP. (OSTEICHTHYES: CHANNIDAE) OF PENINSULAR MALAYSIA

W. B. Tan Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia

T. F. Khang Department of Statistics & Applied Probability, Faculty of Science, National University of Singapore, Singapore (Current address: Institute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, Malaysia)

L. H. S Lim Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia Phone: +603 7967 4368; Fax: +603 7967 4178/4173; Email: [email protected] (Corresponding author)

ABSTRACT. – The morphometric data of anchors of 448 specimens belonging to four species of Trianchoratus Price & Berry, 1966, from Channa lucius (Cuvier) and C. striata (Bloch) were statistically analysed using principal components analysis (PCA) and Fisher’s linear discriminant (LD) analysis. Both methods were able to differentiate the 448 specimens into four groups which correspond to the four species of Trianchoratus viz. T. malayensis Lim, 1986, T. pahangensis Lim, 1986, T. longianchoratus Tan & Lim, 2009, and T. ophicephali Lim, 1986, based on the over all size of the three developed anchors and the two main morphometric descriptors are the inner length and outer length of the dorsal anchor. PCA and one-way multivariate analysis of variance (MANOVA) of the individuals within each species indicated the presence of groups or intraspeciﬁ c morphometric variants within T. malayensis, T. pahangensis and T. ophicephali. There are indications of morphovariants within T. longianchoratus, but more specimens are needed to verify the number of the morphometric variants. Preliminary analyses suggest that the intraspeciﬁ c morphometric variants could be locality-dependent as in T. malayensis and T. ophicephali, and partially host-dependent as in T. pahangensis. The distinguishing morphometric characters for the four Trianchoratus species and for each existing morphometric variants of the three species are presented.

KEY WORDS. – Trianchoratus, Heteronchocleidinae, Intraspeciﬁ c variation, Morphometric variant, Channa lucius, Channa striata.

INTRODUCTION of variance (ANOVA), multivariate analysis of variance (MANOVA) and factor analysis, have been used by various Morphometric data are used extensively in taxonomy for authors to reveal interspecifi c and intraspecifi c morphometric species differentiation. The wide ranges in morphometric data variations in monogeneans (Geets et al., 1999; Mariniello et in species descriptions indicate the presence of morphometric al., 2004; Dmitrieva et al., 2007; Jackson & Tinsley, 2007; variations in nature. Morphologically similar congeneric Olstad et al., 2007). PCA is a useful exploratory method species that exhibit substantial morphometric variations that reduces the dimension of a data set, allowing important within their populations may cause diffi culties in taxonomy, features to be summarized as two-dimensional PCA plots raising questions as to whether the observed variations are (Jolliffe, 2002). intraspecifi c or interspecifi c. Morphometric variations within monogenean populations have been shown by a number of In a recent taxonomic investigation on Trianchoratus Price & researchers including Lim (1987), Ergens (1991), Jackson & Berry, 1966 (Monogenea: Ancyrocephalidae) from Channa Tinsley (1995), Geets et al. (1999), Davidova et al. (2005), lucius (Cuvier) and C. striata (Bloch), we noted the presence Huyse et al. (2006), and Simkova et al. (2007). of groups with small but distinct morphometric differences within some Trianchoratus species. Briefl y, Trianchoratus Several statistical methods, for example, principal component spp. possess three well-developed anchors (two ventral analysis (PCA), discriminant analysis (DA), one-way analysis anchors and one dorsal anchor), one comma-shaped vestigial

165 Tan et al: Trianchoratus in Malaysian Channa dorsal anchor and 14 marginal hooks. The presence of multivariate means are suffi ciently small in all four species, these small but distinct morphometric groups within the the multivariate means were represented simultaneously as Trianchoratus species gives rise to questions as to whether Chernoff faces (Chernoff 1973, Johnson and Wichern 2002). these observed differences are interspecifi c or intraspecifi c The latter provide quick, visual assessment of similarities and variations especially since many of the Trianchoratus spp. differences among the four Trianchoratus species. To assess possess morphologically similar anchors (Lim, 1986; Tan & the strength of the current set of morphometric characters Lim, 2009). This issue prompted this present study to analyse in species classifi cation, Fisher’s linear discriminant (LD) morphometric data of Trianchoratus spp. In this study, PCA, analysis was performed on the total data set, with equal prior Fisher’s linear discriminant (LD) analysis, MANOVA and probabilities for all four species. The classifi cation error other related analyses are used fi rst to group the different rate was estimated using Lachenbruch’s method (Johnson individuals of Trianchoratus from the channids based on & Wichern, 2002). their morphometric data with analyses also performed on the individuals within each of the groups formed to determine In addition to these standard analyses, we also explored if morphometric variants are present. locality and host factors on the distribution patterns of the intraspecifi c variants, although this study was not designed for this purpose. Except for the T. longianchoratus data set, MATERIALS AND METHODS one-way multivariate analysis of variance (MANOVA) on the fi rst two PC scores were done to check if there are any The morphometric data for this study were from the type signifi cant differences in the PC means between different and voucher specimens of four species of Trianchoratus morphometric groups in terms of locality. To see the effect deposited in the Parasite Collection at the Zoological Museum of host factors on morphometric variations, MANOVA was of University of Malaya. The four species are Trianchoratus done using 102 T. pahangensis from two C. lucius from viz. T. malayensis Lim, 1986, T. pahangensis Lim, 1986 the same locality, Bukit Merah, and possessing almost and T. longianchoratus Tan & Lim, 2009, from C. lucius similar numbers (54 and 48) of T. pahangensis. To ensure and T. ophicephali Lim, 1986, from C. striata. The two that results of the statistical analyses could be interpreted host species were collected from the riverine swamp-lake confi dently checks on assumptions that are associated with Tasik Bera, Endau-Rompin and Bukit Merah Reservoirs each test were performed (Figures not shown but available (Table 1). The monogeneans were collected and prepared on request). For MANOVA, chi-square plots were used to as in Lim (1986). confi rm multivariate normality of the PC scores (Johnson & Wichern, 2002), while the assumption of equal covariance Although the Trianchoratus species have morphologically matrix (for the PC scores in MANOVA; and for the original similar copulatory organs which are different in terms of variables in LD analysis) was checked using Box’s test (see size they are subjected to distortions due to orientations Timm, 2002). and are hence diffi cult to measure. They are therefore not included in the analysis. The vestigial anchor and marginal hooks are also not considered in this analysis because they RESULTS are either obscured by the larger well-developed anchors or are not disposed properly to be measured. In this study fi ve Total dataset. – The PCA scatterplot of all 448 individuals parameters were taken: inner root (IR), outer root (OR), shows four distinct clusters which correspond to the four inner length (IL), outer length (OL) and point (pt), for each of the three well-developed anchors (Fig. 1) using Leica image analysis software (QWin Plus) resulting in a total of 15 variables per monogenean (the numbers attached to the parameters denote the position of the anchors, 1 and 2 for the two ventral anchors and 3 for the dorsal anchor). The measurements of the two ventral anchors are treated as separate datasets. All the measurements were taken by the fi rst author. A total of 448 Trianchoratus specimens were measured and identifi ed.

Statistical analyses. – All computations were conducted using R (Version 2.8.1; R Core Development Team 2008), and the scripts used are available upon request. The total data set consisting of 448 individuals were analysed ﬁ rst using PCA. Data sets for each of the four species were then analysed separately to detect if there are any morphometric variants. Biplots were used to aid interpretation of the principal component (PC) axes (to reduce the number of Figures in this paper not all biplots are shown but they Fig. 1. A well-developed anchor of Trianchoratus species showing are available on request). Since the standard errors of the the basic measurements taken for morphometric analysis.

166 THE RAFFLES BULLETIN OF ZOOLOGY 2010

Table 1. The host and locality distribution patterns of the 448 individuals of Trianchoratus spp. used in the morphometric analysis.

Trianchoratus spp. Host species Locality No. of individuals used in this study T. malayensis Channa lucius Bukit Merah 58 Endau-Rompin 36 Tasik Bera 25 Total 119 T. pahangensis Channa lucius Bukit Merah 113 Endau-Rompin 4 Tasik Bera 42 Total 159 T. longianchoratus Channa lucius Bukit Merah 25 T. ophicephali Channa striata Bukit Merah 95 Tasik Bera 50 Total 145 Grand total 448

Trianchoratus species, essentially clustering 119 specimens and PC2 resolve the 448 individuals into four groups. The as T. malayensis, 159 as T. pahangensis, 145 as T. ophicephali Chernoff faces also show the distinctive features of these and 25 as T. longianchoratus (Fig. 2). The biplot shows that four species (Fig. 4), which indicate T. malayensis and T. inner length and outer length of the well-developed dorsal ophicephali are most similar. anchor (IL3 and OL3) are the main distinguishing characters for the four species of Trianchoratus (Fig. 3). The fi rst PC Fisher’s LD analysis verifi es results of the PCA (Fig. 5). axis (PC1, x-axis), which accounts for 65% of total variation, The fi rst LD function (LD1) provides clear separation of is an index of the overall size of the three well-developed T. longianchoratus from the three other Trianchoratus anchors; it separates the 448 individuals into two groups species (65% of total variation), the second LD function as shown by the horizontal bar plot in Fig. 2. The second (LD2) separates T. pahangensis from the T. malayensis – T. principal component (PC2, y-axis), which explains 20% of ophicephali cluster (21% of total variation) and the third total variance, is an index that contrasts the inner lengths LD function (LD3) differentiates between T. malayensis (IL1, IL2), inner roots (IR1, IR2) and outer roots (OR1, and T. ophicephali (14% of total variations) (Table 2). OR2) of the ventral anchors against the other variables; it Lachenbruch’s method verifi es that benchmarking the present separates the Trianchoratus specimens into three groups as data set affords 100% correct classifi cation. shown by the vertical bar plot in Fig. 2. Taken together, PC1

Fig. 3. Biplot of the ﬁ rst two principal components for the four Fig. 2. PCA plot of four species of Trianchoratus. The horizontal species of Trianchoratus, with mean coordinates of the species and vertical barplots indicate one-dimensional summary of the indicated. Only vectors (IL1, OL1, IR1, OR1 and pt1) from one PC axes. ventral anchor are shown.

167 Tan et al: Trianchoratus in Malaysian Channa

Table 2. Diagnostic morphometric characters of the four Trianchoratus species from channid hosts based on Fisher’s Linear Discriminant analysis. (IR3, inner root of dorsal anchor; OR3, outer root of dorsal anchor; OL1, outer length of ventral anchor; OL3, outer length of dorsal anchor, the numbers attached to the parameters denote the anchors, 1 and 2 for the two ventral anchors and 3 for the dorsal anchor).

Linear Contribution to LD index Character traits with Species distinguished discriminant total variation large loading magnitude functions (LD) (in µm) LD1 65% LD1 > 5 IR3 ≥ 30 T. longianchoratus OR3 = 0 LD1 < 5 IR3 ≤ 30 other 3 spp. OR3 > 0 LD2 21% LD2 < −1.5 IR3 < 20 T. pahangensis OL1 < 30 LD2 > −1.5 IR3 > 20 other 2 spp. OL1 > 30 LD3 14% LD3 < 0 OL3 > 35 T. malayensis LD3 > 0 OL3 < 35 T. ophicephali

Morphometric variations within each Trianchoratus spp. three well-developed anchors, followed by T. malayensis from – The results of the PCA and MANOVA for the different Tasik Bera with medium size anchors and T. malayensis from individuals of the four species are provided below. Endau-Rompin, which has the smallest size anchors. The distinguishing character for these three locality-dependent Trianchoratus malayensis. – The PCA scatterplots show groups is the inner length of the well-developed dorsal anchor that the 119 T. malayensis could be separated into 3 groups (IL3) (Table 3). along the PC1 axis with no separation along PC2 (Fig. 6). The scatterplot result is conﬁ rmed by the MANOVA which Trianchoratus pahangensis. – The 159 individuals of shows all three groups have signiﬁ cantly different mean PC1 T. pahangensis are separated into three groups in the scores (p-value < 10−13; Box’s test p-value = 0.01), but not for PCA scatterplot (Fig. 7). Along the PC1 axis, the 159 T. PC2 scores. PC1 accounts for 63% of the total variation. pahangensis are divided into two groups. PC1 accounts for 72% of the total variation and separates the monogeneans Locality labels account for slightly over half of the total with large anchors from those with smaller anchors. The variations in PC1 (R2 = 52%), but contribute almost nothing group with smaller size anchors is further sub-divided into to PC2 (R2 = 0.6%). In other words the size of the anchors are different in three localities: T. malayensis from Bukit Merah has the largest overall size (negative scores) of the

Fig. 5. Fisher’s linear discriminant analysis plots of the ﬁ rst three Fig. 4. Chernoff faces: graphical summary of the mean of each of LD functions, which account for 65%, 21% and 14% of the total the 15 variables in the four Trianchoratus species represented as variation, respectively. Indicators: Trianchoratus malayensis (-); T. different facial features. pahangensis (+); T. ophicephali (o); T. longianchoratus (l).

168 THE RAFFLES BULLETIN OF ZOOLOGY 2010 two groups based on the inner length (IL1 and IL2) and inner MANOVA result indicates that the Tasik Bera and Bukit root (IR1 and IR2) of the ventral anchors along the PC2 axis. Merah populations have signifi cant differences in mean PC1 The biplot indicates that the outer length and inner root of the scores (p-value < 0.001), but not in the mean PC2 scores. ventral anchors (OL1 and IR1) (Table 3) are the characters Locality labels account for about one-fi fth of total variations which strongly infl uence the PC1 and PC2 coordinates of (R2 = 21%) on PC1 indicating some degree of locality one individual on the PCA scatterplot. infl uence. The morphometric variants of T. ophicephali in the two localities are distinguished by two main traits: IL1 The locality labels only explain a very small fraction of and IL3 (Table 3). total variations in PC1 (R2 = 2%) and PC2 (R2 = 0.2%). This indicates that differences in the multivariate means of PC1 Trianchoratus longianchoratus. – The PCA scatterplot for and PC2 scores in populations from the different localities the 25 individuals of T. longianchoratus (Fig. 9) indicates are unlikely to be biologically signifi cant, even though the the presence of two clusters along PC1 axis, one in the MANOVA result is statistically signifi cant (p-value = 0.02). direction of negative PC1, and another in the opposite In fact the latter needs to be cautiously interpreted since the direction. The cluster in the direction of the negative PC1 equal covariance assumption in MANOVA is violated (Box’s has more individuals which are further separated into two test result: p-value = 0.03) This suggests that the variants clusters by PC2. Biplot indicates that IR1 is the important are not dependent on locality and this is supported by the distinguishing character for the 25 individuals. Although presence of individuals from different localities in the three there appears to be three clusters in the PCA scatterplot of groups generated (Fig. 7). T. longianchoratus (Fig. 9), it would be premature to declare the number of intraspecifi c morphometric variants present It should be noted that in Fig. 7 we have colour-coded all the until more samples of T. longianchoratus are analysed. monogeneans belonging to two C. lucius (Host 1 and Host 2) from the Bukit Merah. The scatterplot (Fig. 7) shows that Host 1 possesses variant 1 and variant 3 while Host 2 has variant DISCUSSION 2 and variant 3. The MANOVA results (p-value < 0.001; Box’s test p-value = 0.06) indicate signifi cant differences in Both PCA and Fisher’s LD analysis are able to separate the mean of PC1 and PC2 scores of T. pahangensis from Host the 448 individuals of Trianchoratus into groups which 1 and Host 2. The above analyses suggest that intraspecifi c correspond to their respective species, 119 T. malayensis, 159 morphometric variants appear to be only partially dependent T. pahangensis, 145 T. ophicephali and 25 T. longianchoratus on host factors. (Fig. 2) based on morphometric differences of their anchors, particularly the overall size of three well-developed anchors. Trianchoratus ophicephali. – The PCA scatterplot of the Fisher’s LD provides diagnostic morphometric characters for 145 individuals of T. ophicephali (Fig. 8) does not show the four Trianchoratus spp., which are summarised in Table obvious separations, although PC1 and PC2 account for 2. These analyses indicate the suitability and effectiveness 51% and 10% of total variation, respectively. However, the of using the present set of morphometric variables for

Fig. 6. PCA plot of Trianchoratus malayensis, with geographical Fig. 7. PCA plot of Trianchoratus pahangensis. The horizontal origin of data indicated. The horizontal and vertical barplots indicate and vertical barplots indicate one-dimensional summary of the PC one-dimensional summary of the PC axes. axes. (Black dots = Host 1; Grey dots = Host 2).

169 Tan et al: Trianchoratus in Malaysian Channa

Table 3. Distinguishing morphometric traits of the intraspeciﬁ c variants of the four Trianchoratus species from channid hosts. (The abbreviations for the measured parameters are as in the text).

Trianchoratus spp. Channa spp. Intraspeciﬁ c Mean (standard Possible Factors variants deviation) of major variables (in µm) T. pahangensis (n = 159) C. lucius 1 OL1 = 24.3 (0.1) Host-dependent PC1 index = overall size of 3 IR1 = 26.1 (0.2) (Partial) anchors 2 OL1 = 22.6(0.1) PC2 index = IL1 + IL2 + IR1 IR1 = 23.1(0.2) + IR2 3 OL1 = 24.4(0.2) IR1 = 20.4(0.2) T. malayensis (n = 119) C. lucius 1 IL3 = 50.9 (2.9) Locality-dependent PC1 index = overall size of 3 (Bukit Merah) anchors 2 IL3 = 47.3 (3.0) Locality-dependent PC2 index = no separation on (Endau-Rompin) PC2 3 IL3 = 43.8 (2.5) Locality-dependent (Tasik Bera) T. ophicephali (n = 145) C. striata 1 IL1 = 49.5 (0.2) Locality-dependent PC1 index = overall size of 3 IL3 = 43.6 (0.2) (Bukit Merah) anchors PC2 index = IL1 + OL1 + IR1 + 2 IL1 = 52.3 (0.3) Locality-dependent OR1 against IL3 + OL3 + IR3 IL3 = 45.2 (0.3) (Tasik Bera) T. longianchoratus (n=25) C. lucius 3* (needs conﬁ rmation) PC1 index = IR1 + IR2 + OL3 + IR3 + OR3 + pt3 against other variables PC2 index = OL3 + OR3 against other variables

discriminating species of Trianchoratus (see Lim, 1986; Tan thus providing a powerful species classiﬁ cation tool for the & Lim, 2009). Fisher’s LD analysis (Fig. 5) using the current future. The automated assignments of unknown specimens dataset gives excellent classiﬁ cation results as indicated by of Trianchoratus can be directly done using Fisher’s LD the 0% estimated actual error rate by Lachenbruch’s method, analysis with the current data set as reference.

Fig. 8. PCA plot of Trianchoratus ophicephali with geographical Fig. 9. PCA plot of Trianchoratus longianchoratus. The horizontal origin of data indicated. The horizontal and vertical barplots indicate and vertical barplots indicate one-dimensional summary of the one-dimensional summary of the PC axes. PC axes.

170 THE RAFFLES BULLETIN OF ZOOLOGY 2010

For the present study, PCA has been successful in detecting LITERATURE CITED the presence of groupings or intraspecifi c morphometric variants within T. malayensis, T. pahangensis and T. Chernoff, H., 1973. Using faces to represent points in K-dimensional ophicephali and possibly in T. longianchoratus (Figs. 6, 7, 8 space graphically. Journal of American Statistical Association, & 9) and the numbers of groups vary according to the species. 68: 361–368. The morphometric characters defi ning these intraspecifi c Davidova, M., J. Jarkovsky, I. Matejusova & M. Gelnar, 2005. morphometric variants are also different among the four Seasonal occurrence and metrical variability of Gyrodactylus Trianchoratus species (Table 3). Our preliminary analyses rhodei Zitnan 1964 (Monogenea, Gyrodactylidae). Parasitology indicate that the factors affecting intraspecifi c morphometric Research, 95(6): 398–405. variations vary according to species: T. malayensis and Dmitrieva, E. V., P. I. Gerasev & N. V. Pron’kina, 2007. Ligophorus T. ophicephali are affected by locality differences while llewellyni n. sp. (Monogenea: Ancyrocephalidae) from the T. pahangensis is infl uenced by host factors. It should be redlip mullet Liza haematocheilus (Temminck & Schlegel) Systematic noted, however, that the locality labels explains only 21 % introduced into the Black Sea from the Far East. Parasitology, 67: 51–64. of the variations in T. ophicephali (R2 = 21%) compared to 52% in T. malayensis (R2 = 52%). Host and locality Ergens, R., 1991. Variability of the hard parts of opisthaptor of factors are common explanations for observed intraspectifi c Gyrodactylus leucisci Zitnan, 1964 (Monogenea, Gyrodactylidae). Folia Parasitologica, 38(1): 23–28. morphometric variations in other investigations (Rohde, 1991; Ergens, 1991; Shinn et al., 2001), but it is diffi cult to explain Geets, A. & C. Appleby & F. Ollevier, 1999. Host-dependent and why intraspecific morphometric variants of congeneric seasonal variation in opisthaptoral hard parts of Gyrodactylus cf. arcuatus from three Pomatoschistus spp. and G. arcuatus from species (T. malayensis and T. pahangensis) are infl uenced Gasterosteus aculeatus: a multivariate approach. Parasitology, by different factors, viz. locality and hosts, respectively. 119: 27–40. One explanation is that the inherent genotypic variations in Huyse, T., C. Pampoulie, V. Audenaert & F. A. M. Volckaert, 2006. the cross-fertilising hermaphroditic monogeneans (see Lim, First report of Gyrodactylus spp. (Platyhelminthes: Monogenea) 2002) respond differently to different factors or interactions in the Western Mediterranean sea: molecular and morphological of factors. descriptions. Journal of Parasitology, 92(4): 682–690. Jackson, J. A. & R. C. Tinsley, 1995. Sclerite growth and T. ophicephali The morphometric variants in are less obvious morphometric variation in Gyrdicotylus gallieni Vercammen- compared to those in T. malayensis which could be due to Grandjean, 1960 (Monogenea, Gyrodactylidae) from Xenopus the lack of congeneric competitors in T. ophicephali and laevis laevis (Anura). Systematic Parasitology, 31(1): 1–9. hence a lack of impetus to change. Even though intraspecifi c Jackson, J. A. & R. C. Tinsley, 2007. Evolutionary diversity in morphometric variants appear to be present within the polystomatids infecting tetraploid and octoploid Xenopus in scatterplot for T. longianchoratus, it is diffi cult to defi ne the East African highlands: biological and molecular evidence. variants due to small sample size (25 specimens) (Fig. 9). Parasitology, 134: 1223–1235. Larger sample size is a necessary requirement to statistically Johnson, R. A. & D. W. Wichern, 2002. Applied multivariate defi ne intraspecifi c morphometric variants within species statistical analysis. Pearson Education, Upper Saddle River, populations. N.J. 767 pp. Jolliffe, I. T., 2002. Principal component analysis. 2nd ed. Springer- Improved sampling designs are needed to ascertain the Verlag, New York. 487 pp. factors (environmental conditions, host factors and inherent Lim, L. H. S., 1986. New species of Trianchorathus Price et Berry, genotypic variations) responsible for the intraspecific 1966 (Ancyrocephalidae) from Malayan anabantoid fi shes. morphometric variations observed here. Adequate samples Parasitologia Hungarica, 19: 31–42. from more localities with similar and different environmental Lim, L. H. S., 1987. Distribution and diversity of monogeneans in conditions as well as hosts of different sizes (age groups) freshwater fi shes of Peninsular Malaysia. Unpublished Ph.D. are needed. Locality-dependent intraspecifi c morphometric Thesis, University of Malaya, Kuala Lumpur. 381 pp. variants could be used as potential locality indicators to Pseudohaliotrema determine the geographical origin of their fi sh hosts, but Lim, L. H. S., 2002. Three new species of Yamaguti, 1953 (Monogenea: Ancyrocephalidae) from Siganus should be used with caution since this requires understanding species (Siganidae) and the description of a mechanism of the role of each species within its community. for cross-insemination. Journal of Natural History, 36(14): 1639–1660. Mariniello, L., M. Ortis, S. D’Amelio & V. Petrarca, 2004. ACKNOWLEDGEMENTS Morphometric variability between and within species of Ligophorus Euzet & Suriano, 1977 (Monogenea: The authors would like to thank Mr. K. S. Liew for collecting Ancyrocephalidae) in the Mediterranean Sea. Systematic the fi sh hosts, recovering and preparing the monogeneans for Parasitology, 57: 183–190. analyses and Dr. David Gibson for help in procuring relevant Olstad, K., A. P. Shinn, L. Bachmann & T. A. Bakke, 2007. papers. This paper forms part of the PhD programme of the Host-based identifi cation is not supported by morphometrics fi rst author and is supported by various research grants (Vote in natural populations of Gyrodactylus salaris and G. F, FRGS, e-Science) from the University of Malaya, Kuala thymalli (Platyhelminthes, Monogenea). Parasitology, 134: Lumpur to the corresponding author. 2041–2052.

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R Development Core Team, 2008. R: a language and environment Tan, W. B. & L. H. S. Lim, 2009. Trianchoratus longianchoratus for statistical computing. Vienna: R Foundation for Statistical sp. n. (Monogenea: Ancyrocephalidae: Heteronchocleidinae) Computing. Available from: http://www.r-project.org. from Channa lucius (Osteichthyes: Channidae) in Peninsular Rohde, K., 1991. Size differences in hamuli of Kuhnia scombri Malaysia. Folia Parasitologica, 56(3): 180–184. (Monogenea: Polyopisthocotylea) from different geographical Timm, N. H., 2002. Applied multivariate analysis. Springer-Verlag, areas not due to differences in host size. International Journal New York. 720 pp. for Parasitology, 21(1): 113–114. Simkova, A., M. Pecinkova, E. Rehulkova, M. Vyskocilova & M. Ondrackova, 2007. Dactylogyrus species parasitizing European Barbus species: morphometric and molecular variability. Parasitology, 134: 1751–1765.

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