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26. Crustacea

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Crustacea: Isopoda

Niel L. Bruce Marine Biodiversity and Biosecurity, National Institute of Water and Atmospheric Research, Private Bag 14901, Kilbirnie, Wellington, New Zealand (Email: [email protected])

INTRODUCTION Isopods are known by many as the small bug-like slaters that are found in damp spots around the house and in suburban gardens. They are relatives of the shrimps and crabs, and belong to the Peracarida, a group that includes, amongst others, the amphipods (sand hoppers). Most isopods are small, 3–10 mm long, and most species hide away during the day, emerging at night to feed. Many are robust and compact in form, but body shape can be worm-like, robust or scale-like, while many deep-sea species have highly ornamented and bizarre shapes. Freshwater isopods are most familiar to the casual observer as the so-called fish ‘lice’ familiar to marine fishers and anglers. Isopods are generally characterized as being dorso- ventrally compressed, lacking a carapace and having seven pairs of relatively uniform legs (the anterior first or second legs are not chelate as in amphipods or tanaids). The greatest diversity of aquatic isopods – more than 5700 species – is to be found in marine habitats. It is generally accepted that freshwater isopods are largely derived from marine ancestors. The greatest diversity of free-living freshwater isopods is probably to be found in cave waters (Botosaneanu 1986) although, as the greatest diversity of cave occurs in salty anchialine waters, it must be remembered that not all aquatic cave isopods are freshwater. The aquatic cave fauna of Southeast Asia remains little documented, and it is likely that many isopods will be found in such habitats

GENERAL BIOLOGY Isopods are the most morphologically diverse group of crustaceans. They inhabit all habitats, except perhaps the highest mountain peaks, having been taken at depths of 8 kilometres in the deep-sea trenches and through all marine and terrestrial habitats including deserts. Marine species are free-living for the most part, feeding on detritus, algae and also as predators and scavengers. Marine isopods are well-known as parasites of fishes and crustaceans and this mode of life is confirmed for the freshwater genus Tachaea. Note added in proof. Brandt and Poore (2003) published a new classification of the Isopoda, whereby the suborder is made redundant and replaced by four suborders: Cymothoida Wägele, 1989, Limnoriidea Brandt and Poore, 2002 and Sphaeromatidea, Wägele, 1989 and the monotypic Phoratopidea Brandt and Poore, 2003. Here the earlier classification is followed. Crustacea: Isopoda 299

Figure 1. Morphological features of an isopod. A – Alitropus typus (Aegidae) dorsal view showing major body regions; B – ventral side of head, Cirolanidae; C – antennule; D – antenna; E – mandible, Cirolanidae; F – mandible, Aegidae; G – ambulatory anterior leg, Cirolanidae; H – prehensile anterior leg, Cymothoidae. (Sources: A, F, Ho and Tonguthai 1992; B–E, Bruce and Iliffe 1993; G, Bruce 1986; H, Bruce and Harrison-Nelson 1988) 300 Freshwater Invertebrates of the Malaysian Region

Life cycle Isopods are mostly small , and are characterized by what is termed ‘direct development’. Unlike most crustaceans, which have a pelagic or larval stage, isopods keep their eggs in a brood pouch that is formed by overlapping plates under the abdomen. The young that emerge are miniature versions of the adult, but with the seventh pair of legs yet to develop.

REGIONAL TAXA Few isopods are restricted to freshwater habitats of Peninsular Malaysia or Borneo. However, there are more records of freshwater isopods from Southeast Asia, species of genera of which could reasonably expected to occur in the Malaysian region. A further consideration is that there are a number of genera that occur at least to the upper reaches of tidal rivers and are therefore at times in purely fresh water. Museum collections of isopods from Thailand, Indonesia and elsewhere in the region contain undocumented species of some of these genera. Several of those genera are included here. Freshwater isopods from open-water habitats principally belong to the flabelliferan families Aegidae, Cirolanidae and Corallanidae (the asellotan family Stenasellidae are found in wells, caves and springs). Most other records can be attributed to estuarine species. While diversity is low, on occasion these species can be found in large numbers. There is so little known about the freshwater isopods of Malaysia, only one species recorded to date, that this would indeed be an area for fruitful investigation and collecting. Limited data from the greater Indo-Malaysian region suggest that karst spring and cave habitats and open waters will produce a number of new species and these could provide valuable biogeographic information.

KEY TO FRESHWATER ISOPODS OF MALAYSIA This key is presented using characters selected for ease of observation for those isopods known to occur in freshwater habitats in Southeast Asia. For that reason this key does not reflect phylogeny, does not include all suborders, and may not work for isopods in other regions where generic representation may differ. Comprehensive keys to place isopods into orders and families are to be found in Kensley and Schotte (1989). Bruce (1997) gives an illustrated guide to marine isopods of the Western Indian Ocean which can also be used to identify isopods to family. The world list of isopods (Kensley et al. 2002) and the Brusca et al. (2002) guide are useful Internet resources. This key borrows from many other keys, but is designed as far as possible to allow identification without dissection of the animals, particularly dissection of small mouthparts. Crustacea: Isopoda 301

1. Uropods positioned and articulating terminally (or sub-terminally) on pleotelson; uropods styli- form (slender) ...... Suborder Asellota: Stenasellus - Uropods positioned anterolaterally or anteroventrally on pleotelson; rami lamellar or robust, never styliform ...... 2 2. Body elongate, worm-like, usually more than 6 times as long as wide; uropodal exopod curving dorsally over pleotelson ...... Suborder Anthuridea: Stygocyathura - Body not markedly elongate, length usually less than 4 times as long as wide; uropodal exopod not curving over pleotelson ...... Suborder Flabellifera ..3 3. Pleon with 4 pleonites, variously fused; uropodal endopod fused to peduncle ...... - Pleon with 5 free pleonites, both uropods articulating ...... 4 4. All pereopods prehensile, with dactylus strongly recurved (hooked or claw-like – Fig 1H); obligate parasites of fishes ...... CYMOTHOIDAE - Pereopods 4–7 ambulatory, not prehensile (Fig 1G); free-living or micro-predators of fishes and crustaceans ...... 5 5. Pereopods 1–3 with hooked (claw-like) dactylus (Fig 1H); mouthparts forming a ventrally- directed cone ...... AEGIDAE: Alitropus typus - Pereopods 1–3 ambulatory (i.e. not hooked or claw-like)(Fig 1G); mouthparts not forming a ventrally directed cone ...... 6 6. Mandible incisor wide, tridentate (Fig 1E) ...... CIROLANIDAE ..7 - Mandible incisor narrow, uni- or bidentate (Fig 1F) ...... CORALLANIDAE ..10 7. Antenna 2 with massive peduncle and geniculate flagellum ...... Annina ..9 - Antenna 2 (Fig 1C) peduncle not massive, flagellum not geniculate ...... 8 8. Head with massive anteriorly-directed rostral process; frontal lamina strongly produced anteriorly, extending anterior to rostrum ...... Ceratolana - Head with small rostral process; frontal lamina not anteriorly produced beyond anterior margin of head ...... Anopsilana 9. Male pereonite 2 with two prominent anteriorly-directed process, head and pereonite 1 without processes ...... Annina fustis - Male head, pereonites 1 and 2 each with 2 dorsally-directed processes; pereonite 2 with median acute tubercle ...... Annina kumari 10. Maxilliped elongate, slender, palp with 5 distinct articles ...... Corallana - Maxilliped short, with 3–5 short articles, tending to fuse; commensal on fish and shrimps ...... Tachaea

FAMILIES AND GENERA Mangrove-dwelling and estuarine species are marked with an asterisk*. Species specifically recorded from Peninsular Malaysia, Singapore or Sabah and Sarawak are in bold. 302 Freshwater Invertebrates of the Malaysian Region

SUBORDER FLABELLIFERA FAMILY AEGIDAE Alitropus: A monotypic genus; Alitropus typus H. Milne Edwards, 1840 (Fig. 1A) is a commensal or micro-predator of freshwater fishes. Recorded from India, Sri Lanka, Thailand and Australia. Can be expected to occur in the Malaysian region.

FAMILY CIROLANIDAE Annina: *Annina fustis Bowman and Iliffe, 1991 (Fig. 2B) from streams in the vicinity of mangroves in south-western Thailand and from mangroves in Singapore. *Annina kumari (Bowman, 1971) (Fig. 2A) from mangroves at Port Swettenham, Malaysia. Anopsilana: This genus is known world-wide in rivers, estuaries and cave waters, so it is likely that the genus will be found in appropriate habitats in the region. Anopsilana conditoria Bruce and Iliffe, 1993 (Figs. 1C, D, 2E) is a cave-dwelling species from the Philippines. *Anopsilana willeyi (Stebbing, 1904) (Fig. 2D) has been reported from mangrove estuaries in Kenya, Sri Lanka and Australia (Bruce 1986). Ceratolana: The genus is monotypic. *Ceratolana papuae Bowman, 1977 (Fig. 2C), a large and distinctive species, has been recorded from mangroves at Kuantan, Pahang, Malaysia (Bruce 1995).

FAMILY CORALLANIDAE Corallana: This genus is primarily estuarine and marine, and it is probable that this species will be found within the region. Corallana grandiventra Ho and Tonguthai, 1992 (Fig. 3E) was reported from Chian Kong and Bangkok, Thailand; on the gills of Pangasianodon gigas (giant catfish) and Tilapia nilotica. Tachaea: Species of the genus are known to be commensal of fishes and freshwater ‘shrimps’ (e.g. Macrobrachium spp.); the genus is known from Australia, China, Indonesia, Thailand and India and can be expected to occur in the region (Delaney 1989). *Tachaea crassipes Schioedte and Meinert, 1879 is known only from an estuarine habitat in Singapore. Tachaea lacustris Weber, 1892 (Fig. 3C) has been reported from Sumatra, Java and Sulawesi (Bowman and Botosaneanu 1992).

FAMILY CYMOTHOIDAE Ichthyoxenus: Parasites of marine and freshwater fishes, known from Asia and Australia with, for example, Ichthyoxenus formosanus Harada, 1930 and Ichthyoxenus fushanensis Tsai and Dai, 1999, both from Taiwan. Nerocila: Primarily a marine and estuarine genus of fish parasites that occasionally ventures into the freshwater rivers. *Nerocila depressa Milne Edwards, 1840 (Fig. 3D); Choa Phya River, Thailand (Bruce and Harrison-Nelson 1988). *Nerocila phaiopleura Bleeker, 1857; Crustacea: Isopoda 303

Figure 2. Freshwater and estuarine isopods. A – Annina kumari (Cirolanidae); B – Annina fustis (Cirolanidae); C – Ceratolana papuae (Cirolanidae); D – Anopsilana willeyi (Cirolanidae); E – Anopsilana conditoria (Cirolanidae); F – Sphaeroma terebrans (Sphaeromatidae). (Sources: A, Bowman 1971; B, Bowman and Iliffe 1991; C, Bowman 1977; D, Bruce 1986; E, Bruce and Iliffe 1993; F, Harrison and Holdich 1984) 304 Freshwater Invertebrates of the Malaysian Region

Figure 3. Freshwater and estuarine isopods. A – Stygocyathura chapmani (Anthuridea); B – Stenasellus chapmani (Asellota); C – Tachaea lacustris (and maxilliped) (Corallanidae); D – Nerocila depressa (Cymothoidae); E – Corallana grandiventra (and maxilliped) (Corallanidae). (Sources: A, Andreev 1982; B, Magniez 1993; C, Delaney 1989; D, Bruce and Harrison-Nelson 1988; E, Delaney 1989) Crustacea: Isopoda 305 estuarine; Chantabun River, Thailand (Bruce and Harrison-Nelson 1988). *Nerocila serra Schioedte and Meinert,1881; estuarine and marine; Chantabun River, Thai- land (Bruce and Harrison-Nelson 1988).

FAMILY SPHAEROMATIDAE Sphaeroma: Species of Sphaeroma (Fig. 2F) are well known from estuarine wood, including mangroves, and may range into the upper tidal reaches (see Harrison and Holdich 1984). Numerous other sphaeromatid genera have been recorded from estuaries, but few are known from freshwater. Truly freshwater sphaeromatids are known from hot springs in North America and caves in Europe (Botosaneanu 1986) while one species, Cymodetta gambosa is known from locations upstream of the upper tidal limit in eastern Australia (unpublished Queensland Museum records). No freshwater sphaeromatids have been recorded from Malaysia or Singapore.

SUBORDER ASELLOTA FAMILY STENASELLIDAE Stenasellus: All species of Stenasellus are recorded from karst (limestone) waters, and the genus is well represented in Asia with at least nine species recorded, mostly from Thailand and Cambodia (Magniez 1993). Stenasellus brignolii Pesce and Argano, 1981 is from a freshwater well in Phuket, Thailand. Stenasellus chapmani Magniez, 1982 (Fig. 3B) is from cave waters in Borneo.

SUBORDER ANTHURIDEA FAMILY ANTHURIDAE Stygocyathura: A genus that occurs in cave waters world-wide. Stygocyathura chapmani (Andreev, 1982) (Fig. 3A); Kalimantan, Indonesia (caves). Stygocyathura filipinica (Botosaneanu and Sket, 1999); Bohol Is., Philippines (caves).

REFERENCES Andreev S. (1982) Une Cyathura cavernicole nouvelle de Sarawak–Kalimantan du Nord (Isopoda, Anthuridae). Bulletin Zoölogisch Museum, Universiteit van Amsterdam 8: 149–199. Botosaneanu L. (Ed.) (1986) Stygiofauna Mundi. A Faunistic, Distributional, and Ecological Synthesis of the World Fauna Inhabiting Subterranean Waters (Including the Marine Interstitial). Leiden: E.J. Brill. Botosaneanu L. and Sket B. (1999) A new freshwater stygobiotic species of Cyathura (Isopoda: Anthuridae) from Bohol Island, the Philippines. Acta Biologica Slovenica, Ljubljana 42: 27–33. Bowman T.E. (1971) Excirolana kumari, a new tubiculous isopod from Malaysia. Crustaceana 20: 70–76. Bowman T.E. (1977) Ceratolana papuae, a new genus and species of mangrove-boring cirolanid isopod from Papua New Guinea. Proceedings of the Biological Society of Washington 90: 819–825. Bowman T.E. and Iliffe T.M. (1991) Annina fustis, a new isopod from Phang Nga, Thailand (Crustacea: Isopoda: Cirolanidae). Proceedings of the Biological Society of Washington 104: 247–252. Bowman T.E. and Botosaneanu L. (1992) First record of a Tachaea species from Sulawesi (Indonesia) with description of its manca stage (Isopoda, Flabellifera, Corallanidae). Bijdragen tot de Dierkunde 62: 111–115. 306 Freshwater Invertebrates of the Malaysian Region

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