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A New Molluscivore Crab from Lake Poso Confirms Multiple Colonization of Ancient Lakes in Sulawesi by Freshwater Crabs (Decapoda: Brachyura)

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A New Molluscivore Crab from Lake Poso Confirms Multiple Colonization of Ancient Lakes in Sulawesi by Freshwater Crabs (Decapoda: Brachyura) Zoological Journal of the Linnean Society, 2008, 154, 211–221. With 5 figures A new molluscivore crab from Lake Poso confirms multiple colonization of ancient lakes in Sulawesi by freshwater crabs (Decapoda: Brachyura) CHRISTOPH D. SCHUBART1* and PETER K. L. NG2 1Fakultät für Biologie I, Universität Regensburg, D-93040 Regensburg, Germany 2Department of Biological Sciences, National University of Singapore, 10 Kent Ridge Crescent, Singapore 119260, Republic of Singapore Received 31 January 2006; accepted for publication 6 November 2007 Ancient lakes are among the most stable freshwater environments on our planet, with a species richness far exceeding that of younger and less stable limnic habitats. Compared with the African rift lakes, the ancient lakes of the Indonesian island Sulawesi have received less attention, and their fauna has not been satisfactorily explored. Here, we present results on the freshwater crabs from these lakes and their phylogenetic relationships. Comple- menting recent descriptions of new species and genera of freshwater crabs from the Parathelphusa complex endemic to the Malili lake system and Lake Poso, here we report on another new species belonging to the genus Sundathelphusa (Potamoidea Gecarcinucidae), so far only known from one locality in Lake Poso. The morphology of the chelae of this crab is indicative of a predatory lifestyle: it probably feeds on the rich gastropod and bivalve fauna of the lake. So far, no specialized molluscivore crab has been known from Lake Poso, whereas mollusc-feeding crabs had been described from all lakes belonging to the nearby Malili system. A phylogenetic reconstruction of all known freshwater crab species from the ancient lakes, based on 562 base pairs of mitochondrial DNA (large ribosomal subunit 16S rRNA), revealed that the crabs inhabiting these lakes are not monophyletic. The large number of endemic crab species in both lake systems is thus not the consequence of a single adaptive radiation, but is the outcome of at least two independent colonizations from nearby tributaries and the subsequent specialization to the stable freshwater environment. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154, 211–221. ADDITIONAL KEYWORDS: endemism – freshwater crabs – Gecarcinucidae – Indonesia – molecular systematics – phylogeny – species flocks – Sundathelphusa molluscivora. INTRODUCTION 1997). However, most ancient lakes also harbour one or several species flocks of invertebrates. These are Interest in the evolution of species flocks has directed often crustaceans and snails, as in Lake Tanganyika, a lot of attention to faunal studies of ancient lakes, Lake Baikal, and the Malili lakes of Sulawesi (see von with Lake Tanganyika, Lake Malawi, and Lake Rintelen et al., 2004). The available knowledge on the Baikal being among the best-known examples. To evolution of these invertebrate species flocks is more date, research on species flocks has mainly focused on than rudimentary in comparison with fishes. In most vertebrates, with cichlid fishes from the East African cases, the basic taxonomy still needs to be estab- lakes being probably the best known and best studied lished, and testing of evolutionary hypotheses can example (Meyer et al., 1990; Sturmbauer & Meyer, only be a long-term goal. However, hard-shelled inver- 1992; Schliewen, Tautz & Pääbo, 1994; Goldschmidt, tebrates with a rich fossil record, like crabs and snails, promise to be extremely useful models for *Corresponding author. in situ studies of adaptive radiation and formation of E-mail: [email protected] species flocks (e.g. see Glaubrecht, 1996). © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154, 211–221 211 212 C. D. SCHUBART and P. K. L. NG In most of the better studied ancient lake systems, separate lake, belonging to the Poso River and thus to the occurrence of crustacean species flocks has a different watershed draining to the north (see already been documented (e.g. Mashiko, Kawabata & Whitten, Mustafa & Henderson, 1987). The freshwa- Okino, 1991; Martens, 1994; Cumberlidge et al., 1999; ter fish fauna of these lakes has been relatively well Sherbakov, 1999; von Sternberg & Cumberlidge, studied in recent years. Three families of freshwater 1999; Mashiko, 2000). Species flock formation is not fishes with high endemism rates in Sulawesi deserve restricted to single taxonomic groups. In the temper- mention, viz. Adrianichthyidae, Oryziidae, and Tel- ate Lake Baikal, freshwater gammarids (Peracarida: matherinidae. The Adrianichthyidae and Oryziidae Amphipoda) have experienced a huge radiation with dominate the Poso fauna, whereas the Telmatherin- more than 250 recognized species (Sherbakov, 1999). idae only occurs in the Malili lakes. No endemic Species flocks in tropical lakes typically consist of species are shared by Matano (seven telmatherinids freshwater crabs (Brachyura: Potamoidea) and and one oryziid) and Towuti, Mahalona, and Wawan- shrimps (Caridea: Atyidae), as for example in Lake toa (seven telmatherinids and two oryziids) (Kottelat, Tanganyika (Mashiko et al., 1991; Cumberlidge et al., 1991; Kottelat et al., 1993; Herder et al., 2006). Poso 1999). The ancient lakes of Sulawesi have been rela- has its own fish fauna, with five endemic species tively poorly studied in terms of their crustacean (three adrianichthyids and two oryziids). fauna, and the most recent reports previous to our In this paper, we describe a new molluscivorous present study were from Schenkel (1902) and Wolter- species of Sundathelphusa from Lake Poso, and eck (1937), with the latter dealing only with shrimps discuss the evolution of feeding guilds in the fresh- of the genus Caridina (Atyidae). Until recently, the water crabs of the ancient lakes. The specimens published literature records only one endemic crab examined are deposited in the Museum Zoologicum species in Lake Poso, Parathelphusa sarasinorum Bogoriense (MZB), Cibinong, Java, Indonesia, and the (Schenkel, 1902), and three in the Malili lake system, Zoological Reference Collection (ZRC) of the Raffles Parathelphusa pantherina (Schenkel, 1902), Parath- Museum, National University of Singapore. The elphusa matannensis (Schenkel, 1902), and Nau- abbreviations G1 and G2 are used for the male first tilothelphusa zimmeri (Balss, 1933) (Roux, 1915; Bott, and second pleopods, respectively. Measurements pro- 1970). However, a reappraisal of all extant specimens vided in millimetres are of the carapace width and as well as recently collected material from Sulawesi length, respectively. The classification used here has revealed a higher decapod crustacean species follows that proposed by Ng & Sket (1996), in which richness in these lakes than was previously known Sundathelphusa Bott, 1969, is regarded as a senior (Table 1; Chia & Ng, 2006; von Rintelen, 2008). subjective synonym of Archipelothelphusa Bott, 1969, Chia & Ng (2006) recently revised the taxonomy of and Sundathelphusidae Bott, 1969 is a junior all of the species belonging to the genera Para- synonym of Gecarcinucidae Alcock, 1910 (see also Ng, thelphusa and Nautilothelphusa from Sulawesi, 1988; Klaus et al., 2006). describing two new genera and three new species from these ancient lakes. Consequently, five genera of MATERIAL AND METHODS freshwater crabs are now known from Sulawesi, three of which are restricted to the ancient lakes: Nau- Most specimens used for the morphological and genetic tilothelphusa, Migmathelphusa, and Syntripsa.The comparisons in this study were collected during a field other two genera, Parathelphusa and Sundathel- trip to the lakes of Sulawesi in January 2000. The phusa, are also known from other Sundaic and molecular studies were carried out at the University of Sahulian islands, the Malay Peninsula, and the Phil- Regensburg. The genomic DNA of freshwater crabs ippines. They typically inhabit streams, swamps, rice was isolated from the muscle tissue of one walking leg fields, and caves (see Ng, 1988, 1991; Ng & Stuebing, using the Puregene kit (Gentra Systems). Selective 1989; Ng & Takeda, 1993; Ng & Sket, 1996). In amplification of a 560-base-pair (560-bp) region from Sulawesi, nine species of Parathelphusa and three the mitochondrial large subunit rRNA gene (16S species of Sundathelphusa are currently known from mtDNA) was carried out by polymerase chain reaction outside of the lakes (streams and caves) (Bott, 1970; (PCR) (40 cycles; with 45 s at 94 °C/1 min at 48 °C/ Chia & Ng, 2006). They represent the potential colo- 1 min at 72 °C denaturing/annealing/extension tem- nizers of the freshwater lake habitats. peratures, respectively) with the primer combination The ancient lakes of Sulawesi consist of two hydro- 16L2 (5′-TGCCTGTTTATCAAAAACAT-3′) and 1472 graphically isolated freshwater systems. The Malili (5′-AGATAGAAACCAACCTGG-3′)(~580 bp) or 16H37 lake system of Sulawesi is composed of five partially (5′-CCGGTyTGAACTCAAATCATGT-3′)(~560 bp) connected lakes, viz. Towuti, Mahalona, Wawantoa, (see Schubart, Cuesta & Felder, 2002; Klaus et al., Masapi, and Matano, and belongs to the Larona River 2006). PCR products were purified and sequenced in basin, which drains to the south. Lake Poso is a an ABI Prism 310 Genetic Analyzer. Sequences were © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154, 211–221 © 2008 The Linnean Society of London, Table 1. Gecarcinucid crabs used for DNA sequencing and subsequent phylogenetic reconstruction, including taxonomic
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