Advertisement

Hydrobiologia

, Volume 592, Issue 1, pp 11–94 | Cite as

Ancient lakes as hotspots of diversity: a morphological review of an endemic species flock of Tylomelania (Gastropoda: Cerithioidea: Pachychilidae) in the Malili lake system on Sulawesi, Indonesia

  • Thomas von Rintelen
  • Philippe Bouchet
  • Matthias Glaubrecht
Primary Research Paper

Abstract

The viviparous freshwater gastropod Tylomelania (Caenogastropoda: Cerithioidea: Pachychilidae) endemic to the Indonesian island Sulawesi has radiated extensively in two ancient lake systems. We here present the first systematic species-level review of taxa in the five lakes of the Malili lake system, which contains the most diverse and best studied freshwater fauna on Sulawesi. Our results indicate a significantly higher diversity of Tylomelania in these lakes than previously perceived based on morphological evidence for delimiting the taxa. We describe nine new species, thus increasing the number of taxa known from the Malili lakes to 25. Tylomelania species are inhabiting all available substrates in the lakes, and the diversity of habitats is reflected in an unparalleled range of radula types in this closely related group. Several species show a high intraspecific variability in some characters, and their closer investigation will probably lead to the discovery of more cryptic species. As it is, this species flock on Sulawesi is among the largest freshwater mollusc radiations known. Since the Malili lake system also contains other large endemic species flocks of e.g. crustaceans and fishes, it is a major hotspot of freshwater biodiversity in Asia to become a conservation priority.

Keywords

Freshwater gastropods Adaptive radiation Taxonomy Morphology Ecology Biodiversity 

Notes

Acknowledgements

We are very grateful to Ristiyanti Marwoto (MZB) for the immense support in arranging the field trip of 1999, which yielded a considerable part of the material studied. We also thank LIPI (Indonesian Institute of Sciences) for the permit to conduct research in Indonesia. Invaluable support was experienced from INCO at Soroako, Lake Matano. Without their help in providing accommodation, transport and general logistics this study would not have yielded the same amount of results. Thanks are also due to Ambros Hänggi, Urs Wüest (NMB) and Robert Moolenbeck (ZMA) for their courtesy and generous help with the loan of material. Many thanks go to M. Drescher, V. Heinrich, I. Kilias, (ZMB) and A. Munandar (MZB) for technical assistence, and to N. Brinkmann (ZMB) for her help with radula preparation. This study was made possible through continuous funding from the Deutsche Forschungsgemeinschaft (DFG) through grants GL 297/1-1 and 1-2.

References

  1. Albrecht, C. & M. Glaubrecht, 2006. Brood care among basommatophorans: a unique reproductive strategy in the freshwater limpet snail Protancylus (Heterobranchia: Protancylidae), endemic to ancient lakes on Sulawesi, Indonesia. Acta Zoologica 87: 49–58.CrossRefGoogle Scholar
  2. Benthem Jutting, W. S. S. v., 1934. Über den Bau der Radula und ihre Bedeutung fÜr die Nahrungsaufnahme bei einigen Javanischen SÜßwassergastropoden. Verhandlungen der Internationalen Vereinigung fÜr theoretische und angewandte Limnologie 6: 325–330.Google Scholar
  3. Boss, K. J., 1978. On the evolution of gastropods in ancient lakes. In Fretter V. & J. F. Peake (eds), Systematics, Evolution and Ecology, 2A. Academic Press, London: 385–428.Google Scholar
  4. Bouchet, P., 1995. A major new mollusc radiation discovered in the ancient lakes of Sulawesi. In Guerra A., E. Rolán & F. Rocha (eds), Abstracts 12th International Malacological Congress, Vigo 1995. UNITAS, Vigo: 14–15.Google Scholar
  5. Brooks, J. L., 1950. Speciation in ancient lakes. Quarterly Review of Biology 25: 30–60, 131–176.CrossRefGoogle Scholar
  6. Brown, D. S., 1994. Freshwater snails of Africa and their medical importance. Taylor and Francis, London.Google Scholar
  7. Cohen, A. S., M. J. Soreghan & C. A. Scholz, 1993. Estimating the age of formation of lakes: an example from Lake Tanganyika, East African Rift system. Geology 21: 511–514.CrossRefGoogle Scholar
  8. Coulter, G. W., 1994. Lake Tanganyika. In Martens K., B. Goddeeris & G. Coulter (eds), Speciation in ancient lakes. E.Schweizerbart’sche Verlagsbuchhandlung, Stuttgart: 13–18.Google Scholar
  9. Coyne, J. A. & H. A. Orr, 2004. Speciation. Sinauer, Sunderland, Mass.Google Scholar
  10. Davis, G. M., 1982. Historical and ecological factors in the evolution, adaptive radiation, and biogeography of freshwater mollusks. American Zoologist 22: 375–395.Google Scholar
  11. Dejoux, C., 1994. Lake Titicaca. In Martens K., B. Goddeeris & G. Coulter (eds), Speciation in ancient lakes. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart: 35–42.Google Scholar
  12. Dillon, R. T., 1984. What shall I measure on my snails? Allozyme data and multivariate analysis used to reduce the non-genetic component of morphological variance in Goniobasis proxima. Malacologia 25: 503–511.Google Scholar
  13. Funk, D. J. & K. E. Omland, 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with Insights from animal mitochondrial DNA. Annual Review of Ecology and Systematics 34: 397–423.CrossRefGoogle Scholar
  14. Genner, M. J., J. A. Todd, E. Michel, D. Erpenbeck, A. Jimoh, D. A. Joyce, A. Poechocki & J.-P. Pointier, 2007. Amassing diversity in an ancient lake: evolution of a morphologically diverse parthenogenetic gastropod assemblage in Lake Malawi. Molecular Ecology 16: 517–530.PubMedCrossRefGoogle Scholar
  15. Giesen, W., 1994. Indonesia’s major freshwater lakes: a review of current knowledge, development processes and threats. Mitteilungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 24: 115–128.Google Scholar
  16. Giesen, W., M. Baltzer & R. Baruadi, 1991. Integrating conservation with land-use development in wetlands of South Sulawesi. Directorate General of Forest Protection and Nature Conservation, Bogor.Google Scholar
  17. Glaubrecht, M., 1996. Evolutionsökologie und Systematik am Beispiel von Süß- und Brackwasserschnecken (Mollusca: Caenogastropoda: Cerithioidea): Ontogenese-Strategien, paläontologische Befunde und historische Zoogeographie. Backhuys, Leiden, 499 pp.Google Scholar
  18. Glaubrecht, M., 2004. Leopold von Buch’s legacy: treating species as dynamic natural entities, or why geography matters. American Malacological Bulletin 19: 111–134.Google Scholar
  19. Glaubrecht, M. & F. Köhler, 2004. Radiating in a river: systematics, molecular genetics and morphological differentiation of viviparous freshwater gastropods endemic to the Kaek River, central Thailand (Cerithioidea, Pachychilidae). Biological Journal of the Linnean Society 82: 275–311.CrossRefGoogle Scholar
  20. Glaubrecht, M. & E. E. Strong, 2004. Spermatophores of thalassoid gastropods (Paludomidae) in Lake Tanganyika, East Africa, with a survey of their occurrence in Cerithioidea: functional and phylogenetic implications. Invertebrate Biology 123: 218–236.CrossRefGoogle Scholar
  21. Glaubrecht, M. & E. E. Strong, 2007. Ancestry to an endemic radiation in Lake Tanganyika? Evolution of the viviparous gastropod Potadomoides Leloup, 1953 in the Congo River system (Cerithioidea, Paludomidae). Biological Journal of the Linnean Society, in press.Google Scholar
  22. Gorthner, A., 1992. Bau, Funktion und Evolution komplexer Gastropodenschalen in Langzeit-Seen Mit einem Beitrag zur Paläobiologie von Gyraulus “multiformis” im Steinheimer Becken. Stuttgarter Beiträge zur Naturkunde, Ser. B. 190, 1–173.Google Scholar
  23. Haase, M. & P. Bouchet, 2006. The species flock of hydrobioid gastropods (Caenogastropoda, Rissooidea) in ancient Lake Poso, Sulawesi. Hydrobiologia 556: 17–46.CrossRefGoogle Scholar
  24. Haffner, G. D., P. E. Hehanussa & D. Hartoto, 2001. The biology and physical processes of large lakes of Indonesia: Lakes Matano and Towuti. In Munawar, M. & R. E. Hecky (eds), The Great Lakes of the World (GLOW): Food-web, Health and Integrity. Backhuys Publishers, Leiden: 183–192.Google Scholar
  25. Harrison, R. G., 1998. Linking evolutionary pattern and process. The relevance of species concepts for the study of speciation. In Howard D. J. & S. H. Berlocher (eds), Endless forms. Species and speciation. Oxford University press, New York: 19–31.Google Scholar
  26. Harvey, P. H. & M. D. Pagel, 1991. The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.Google Scholar
  27. Herder, F., A. W. Nolte, J. Pfänder, J. Schwarzer, R. K. Hadiaty & U. K. Schliewen, 2006. Adaptive radiation and hybridization in Wallace’s dreamponds: evidence from sailfin silversides in the Malili lakes of Sulawesi. Proceedings of the Royal Society London B 273, 2209–2217.CrossRefGoogle Scholar
  28. Herder, F., J. Schwarzer, J. Pfänder, R. K. Hadiaty & U. K. Schliewen, 2006. Preliminary checklist of sailfin silversides (Telostei: Telmatherinidae) in the Malili Lakes of Sulawesi (Indonesia), with a synopsis of systematics and threats. Verhandlungen der Gesellschaft für Ichthyologie 5: 139–163.Google Scholar
  29. Hershler, R. & F. G. Thompson, 1992. A review of the aquatic gastropod subfamily Cochliopinae (Prosobranchia: Hydrobiidae). Malacological Review Suppl. 5: 1–140.Google Scholar
  30. Hey, J., 2006. On the failure of modern species concepts. Trends in Ecology and Evolution 21: 447–450.PubMedCrossRefGoogle Scholar
  31. Hey, J., R. S. Waples, M. L. Arnold, R. K. Butlin & R. G. Harrison, 2003. Understanding and confronting species uncertainty in biology and conservation. Trends in Ecology and Evolution 18: 597–603.CrossRefGoogle Scholar
  32. Holznagel, W. E., 1998. A nondestructive method for cleaning gastropod radulae from frozen, alcohol-fixed, or dried material. American Malacological Bulletin 14: 181–183.Google Scholar
  33. Hutchinson, G. E., 1957. A Treatise on Limnology. John Wiley & Sons, New York.Google Scholar
  34. Ihering, H. v., 1885. Zur Verständigung über Beschreibung und Abbildung von Radula-Zähnen. Nachrichtsblatt der Deutschen Malakozoologischen Gesellschaft 17: 1–7.Google Scholar
  35. International Commission on Zoological Nomenclature, 1999. International Code of Zoological Nomenclature, The International Trust for Zoological Nomenclature, London.Google Scholar
  36. Köhler, F. & M. Glaubrecht, 2003. Morphology, reproductive biology and molecular genetics of ovoviviparous freshwater gastropods (Cerithioidea, Pachychilidae) from the Philippines, with description of a new genus Jagora. Zoologica Scripta 32: 35–59.CrossRefGoogle Scholar
  37. Köhler, F. & M. Glaubrecht, 2006. A systematic revision of the Southeast Asian freshwater gastropod Brotia (Cerithioidea: Pachychilidae). Malacologia 48: 159–251.Google Scholar
  38. Kottelat, M., 1990. Sailfin silversides (Pisces: Telmatherinidae) of Lakes Towuti, Mahalona and Wawontoa (Sulawesi, Indonesia) with descriptions of two new genera and two new species. Ichthyological Exploration of Freshwaters 1: 227–246.Google Scholar
  39. Kottelat, M., 1991. Sailfin silversides (Pisces: Telmatherinidae) of Lake Matano, Sulawesi, Indonesia, with descriptions of six new species. Ichthyological Exploration of Freshwaters 1: 321–344.Google Scholar
  40. Kottelat, M., A. J. Whitten, S. N. Kartikasari & S. Wirjoatmodjo, 1993. Freshwater Fishes of Western Indonesia and Sulawesi. Periplus, Jakarta.Google Scholar
  41. Kruimel, J. H., 1913. Verzeichnis der von Herrn E. C. Abendanon in Celebes gesammelten Süsswasser-Mollusken. Bijdragen tot de Dierkunde 19: 217–235.Google Scholar
  42. Martens, E. v., 1883. Die Weich- und Schaltiere gemeingefaßlich dargestellt. G. Freytag, Leipzig.Google Scholar
  43. Martin, P., 1994. Lake Baikal. In Martens, K., B. Goddeeris & G. Coulter (eds), Speciation in ancient lakes. E.Schweizerbart’sche Verlagsbuchhandlung, Stuttgart: 3–11.Google Scholar
  44. Marwoto, R., 1997. A preliminary study of the biodiversity of the freshwater snail family Thiaridae from Indonesia (Mollusca: Prosobranchia). In Ulrich, H. (ed), Tropical Biodiversity and Systematics. Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn: 109–112.Google Scholar
  45. Mayr, E., 1942. Systematics and the Origin of Species. Columbia University Press, New York.Google Scholar
  46. Mayr, E., 1963. Animal Species and Evolution. Belknap Press of Harvard University Press, Cambridge, Mass. Google Scholar
  47. Mayr, E., 2000. The biological species concept. In Wheeler, Q. D. & R. Meier (eds), Species Concepts and Phylogenetic Theory. A Debate. Columbia University Press, New York: 17–29.Google Scholar
  48. McLean, J. H., 1971. Archaeogastropoda. In Keen, A. M. (ed), Seashells of Tropical West America. Stanford University Press, Stanford: 307–363.Google Scholar
  49. Michel, E., 1994. Why snails radiate: a review of gastropod evolution in long-lived lakes, both recent and fossil. In Martens, K., B. Goddeeris & G. Coulter (eds), Speciation in Ancient Lakes. E.Schweitzerbart’sche Verlagsbuchhandlung, Stuttgart: 285–317.Google Scholar
  50. Michel, E., 2004. Vinundu, a new genus of gastropod (Cerithioidea: ‘Thiaridae’) with two species from Lake Tanganyika, East Africa, and its molecular pyhlogenetic relationships. Journal of Molluscan Studies 70: 1–19.CrossRefGoogle Scholar
  51. Nakajima, T. & K. Nakai, 1994. Lake Biwa. In Martens, K., B. Goddeeris & G. Coulter (eds), Speciation in Ancient Lakes. E.Schweizerbart’sche Verlagsbuchhandlung, Stuttgart: 43–54.Google Scholar
  52. Nishino, M. & N. C. Watanabe, 2000. Evolution and endemism in Lake Biwa, with special reference to its gastropod mollusc fauna. In Rossiter, A. & H. Kawanabe (eds), Ancient Lakes: Biodiversity, Ecology and Evolution. Academic Press, San Diego: 151–180.CrossRefGoogle Scholar
  53. Padilla, D. K., 1998. Inducible phenotypic plasticity of the radula in Lacuna (Gastropoda: Littorinidae). Veliger 4: 201–204.Google Scholar
  54. Palmer, A. R., 1990. Effect of crab effluent and scent of damaged conspecifics on feeding, growth, and shell morphology of the Atlantic dogwhelk Nucella lapillus (L.). Hydrobiologia 193: 155–182.CrossRefGoogle Scholar
  55. Radoman, P., 1985. Hydrobioidea, a superfamily of Prosobranchia (Gastropoda). II. Origin, zoogeography, evolution in the Balkans and Asia Minor. Belgrade.Google Scholar
  56. Reid, D. G., 2000. The use of the radula in the taxonomy and phylogeny of gastropods: cautionary cases of convergence, intraspecific variation and plasticity. Phuket Marine Biological Center Special Publication 21: 329–345.Google Scholar
  57. Reid, D. G. & Y. M. Mak, 1999. Indirect evidence for ecophenotypic plasticity in radular dentition of Littoraria species (Gastropoda: Littorinidae). Journal of Molluscan Studies 65: 355–370.CrossRefGoogle Scholar
  58. Ribbink, A. J., 1994. Lake Malawi. In Martens, K., B. Goddeeris & G. Coulter (eds), Speciation in ancient lakes. E.Schweizerbart’sche Verlagsbuchhandlung, Stuttgart: 27–33.Google Scholar
  59. Rintelen, T. v. & M. Glaubrecht, 2003. New discoveries in old lakes: three new species of Tylomelania Sarasin & Sarasin, 1897 (Gastropoda: Cerithioidea: Pachychilidae) from the Malili lake system on Sulawesi, Indonesia. Journal of Molluscan Studies 69: 3–17.CrossRefGoogle Scholar
  60. Rintelen, T. v. & M. Glaubrecht, 2005. Anatomy of an adaptive radiation: a unique reproductive strategy in the endemic freshwater gastropod Tylomelania (Cerithioidea: Pachychilidae) on Sulawesi, Indonesia, and its biogeographic implications. Biological Journal of the Linnean Society 85: 513–542.CrossRefGoogle Scholar
  61. Rintelen, T. v. & M. Glaubrecht, 2006. Rapid evolution of sessility in an endemic species flock of the freshwater bivalve Corbicula from ancient lakes on Sulawesi, Indonesia. Biology Letters 2: 73–77.CrossRefGoogle Scholar
  62. Rintelen, T. v., A. B. Wilson, A. Meyer & M. Glaubrecht, 2004. Escalation and trophic specialization drive adaptive radiation of viviparous freshwater gastropods in the ancient lakes on Sulawesi, Indonesia. Proceedings of the Royal Society London B 271: 2541–2549.CrossRefGoogle Scholar
  63. Salemaa, H., 1994. Lake Ohrid. In Martens, K., B. Goddeeris & G. Coulter (eds), Speciation in ancient lakes. E.Schweizerbart’sche Verlagsbuchhandlung, Stuttgart: 55–64.Google Scholar
  64. Sarasin, P. & F. Sarasin, 1897. Über die Molluskenfauna der großen SÜßwasser-Seen von Central-Celebes. Zoologischer Anzeiger 539/540: 308–320.Google Scholar
  65. Sarasin, P. & F. Sarasin, 1898. Die Süßwassermollusken von Celebes. Kreidel, Wiesbaden.Google Scholar
  66. Sarasin, P. & F. Sarasin, 1905. Reisen in Celebes ausgeführt in den Jahren 1893–1896 und 1902–1903. Kreidel, Wiesbaden.Google Scholar
  67. Schlichting, C. D. & M. Pigliucci, 1998. Phenotypic Evolution. A Reaction Norm Perspective. Sinauer Associates, Sunderland, MA.Google Scholar
  68. Schluter, D., 2000. The Ecology of Adaptive Radiation. Oxford University Press, Oxford.Google Scholar
  69. Simison, W. B. & D. R. Lindberg, 1999. Morphological and molecular resolution of a putative cryptic species complex: a case study of Notoacmea fascicularis (Menke, 1851) (Gastropoda: Patellogastropoda). Journal of Molluscan Studies 65: 99–109.CrossRefGoogle Scholar
  70. Sites, J. W. & J. C. Marshall, 2004. Operational criteria for delimiting species. Annual Review of Ecology and Systematics 35: 199–227.CrossRefGoogle Scholar
  71. Sitnikova, T., 1994. Recent views on the history and diversity of the Baikalian malacofauna. In Martens, K., B. Goddeeris & G. Coulter (eds), Speciation in Ancient Lakes. E.Schweizerbart’sche Verlagsbuchhandlung, Stuttgart: 319–326.Google Scholar
  72. Sodhi, N. S., L. P. Koh, B. W. Brook & P. K. L. Ng, 2004. Southeast Asian biodiversity: an impending disaster. Trends in Ecology and Evolution 19: 654–660.PubMedCrossRefGoogle Scholar
  73. Streelman, J. T. & P. D. Danley, 2003. The stages of vertebrate evolutionary radiation. Trends in Ecology and Evolution, 18: 126–131.CrossRefGoogle Scholar
  74. Strong, E. E. & M. Glaubrecht, 2002. Evidence for convergent evolution of brooding in a unique gastropod from Lake Tanganyika: anatomy and affinity of Tanganyicia rufofilosa (Caenogastropod, Cerithioidea, Paludomidae). Zoologica Scripta 31: 167–184.CrossRefGoogle Scholar
  75. Strong, E. E. & M. Glaubrecht, 2003. Anatomy and systematic affinity of Stanleya neritinoides (Smith, 1880), an enigmatic member of the thalassoid gastropod species flock in Lake Tanganyika, East Africa (Cerithioidea, Paludomidae). Acta Zoologica 84: 249–265.CrossRefGoogle Scholar
  76. Troschel, F. H., 1857. Das Gebiss der Schnecken zur Begründung einer natürlichen Classification. Nicolaische Verlagsbuchhandlung, Berlin.Google Scholar
  77. van Oosterzee, P., 1997. Where Worlds Collide. The Wallace Line. Cornell University Press, Ithaca.Google Scholar
  78. Wesenberg-Lund, C., 1939. Biologie der Süsswassertiere. Wirbellose Tiere. Julius Springer, Wien.Google Scholar
  79. West, K. & E. Michel, 2000. The dynamics of endemic diversification: Molecular phylogeny suggests an explosive origin of the thiarid gastropods of Lake Tanganyika. In Rossiter, A. & H. Kawanabe (eds), Ancient Lakes: Biodiversity, Ecology and Evolution. Academic Press, San Diego: 331–354.CrossRefGoogle Scholar
  80. West, K., E. Michel, J. Todd, D. Brown & J. Clabaugh, 2003. The gastropods of Lake Tanganyika. International Association of Theoretical and Applied Limnology, Chapel Hill, NC.Google Scholar
  81. Westerlund, C. A., 1892. Fundamenta Malacologia. Håkan Ohlsson, Lund.Google Scholar
  82. Wheeler, Q. D. & R. Meier, 2000. Species Concepts and Phylogenetic Theory. A Debate. Columbia University Press, New York.Google Scholar
  83. Whitten, A. J., M. Mustafa & G. S. Henderson, 2002. The Ecology of Sulawesi. Periplus, Singapore.Google Scholar
  84. Wilson, A. B., M. Glaubrecht & A. Meyer, 2004. Ancient lakes as evolutionary reservoirs: evidence from the thalassoid gastropods of Lake Tanganyika. Proceedings of the Royal Society London B 271: 529–536.CrossRefGoogle Scholar
  85. Wilson, M. E. J. & S. J. Moss, 1999. Cenozoic palaeogeographic evolution of Sulawesi and Borneo. Palaeogeography, Palaeoclimatology, Palaeoecology 145: 303–337.CrossRefGoogle Scholar
  86. Woltereck, E., 1937a. Systematisch-variationsanalytische Untersuchungen über die Rassen- und Artbildung bei Süßwassergarnelen aus der Gattung Caridina (Decapoda, Atyidae). Internationale Revue der gesamten Hydrobiologie und Hydrographie 34: 208–262.CrossRefGoogle Scholar
  87. Woltereck, E., 1937b. Zur Systematik und geographischen Verbreitung der Caridinen. Internationale Revue der gesamten Hydrobiologie und Hydrographie 34: 294–330.CrossRefGoogle Scholar
  88. Woltereck, R., 1931. Beobachtungen und Versuche zum Fragenkomplex der Artbildung. I. Wie entsteht eine endemische Rasse oder Art? Biologisches Zentralblatt 51: 231–253.Google Scholar
  89. Woltereck, R., 1941. Die Seen und Inseln der “Wallacea”-Zwischenregion und ihre endemische Tierwelt. Erster Teil: Vorgeschichte und Aufgabe der Forschungsreise. Internationale Revue der gesamten Hydrobiologie und Hydrographie 41: 1–36.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Thomas von Rintelen
    • 1
  • Philippe Bouchet
    • 2
  • Matthias Glaubrecht
    • 1
  1. 1.Museum of Natural History, Humboldt University BerlinBerlinGermany
  2. 2.Muséum National d’Histoire NaturelleParis cedex 05France

Personalised recommendations