Advertisement

Hydrobiologia

, Volume 739, Issue 1, pp 145–153 | Cite as

Prey preferences in captivity of the freshwater crab Potamonautes lirrangensis from Lake Malawi with special emphasis on molluscivory

  • A. M. Weigand
  • The Volkswagen Foundation Lake Malawi Field School 2012 Consortium
  • M. Plath
SPECIATION IN ANCIENT LAKES 6

Abstract

Freshwater crabs play an important role for the diversification of shell morphologies in freshwater gastropods. For example, the radiation of the freshwater crab genus Platythelphusa in Lake Tanganyika is thought to have driven shell diversification of the lake’s snail fauna, promoting the evolution of thalassoid shells. No comparable thalassoid snails are known from Lake Malawi. Accordingly, it was hypothesized that the lake’s only freshwater crab, Potamonautes lirrangensis, is not a snail predator. We tested this hypothesis using feeding experiments with specimens caught in the southern part of Lake Malawi. Individual crabs were held in experimental containers offshore and were presented with various food items overnight, after which ingestion frequency was recorded. Potamonautes lirrangensis can be characterized as a scavenger that is opportunistically carnivorous. A preference for fish and snail flesh could be observed, indicating a bias toward carnivory. We observed occasional cracking of the shell in different snail species, with frequent ingestion of artificially crushed specimens, suggesting that crabs do attempt to feed on snails. However, the investigated Lake Malawi gastropods appear to be partly protected against crab predation through thick-walled and low-spired shells (especially Lanistes and Bellamya), obviating the evolution of thalassoid shells carrying rims, ridges, or spines.

Keywords

Feeding ecology Molluscivory Co-evolution Arms race Adaptation 

Notes

Acknowledgements

Authorities of the Lake Malawi National Park and the University of Malawi have approved and coauthored this study. Following the ‘Malawi National Parks and Wildlife Act’, permission to conduct this research was obtained from the Wildlife Officer Mr. Bryson Banda of the ‘Lake Malawi National Park’ site (paragraph 39). We acknowledge financial support for the present study by the Volkswagen Foundation in the frame of the field school “Evolution of Lake Malawi Biodiversity” (AZ 86 253). The field school ‘Evolution of Lake Malawi Biodiversity’ was dedicated to the investigation and understanding of aspects of evolutionary biology presented in hands-on experiments at the Mbuna Research Station in Cape Maclear. All participants of the field school were actively and passionately involved in the data collection process. We thank the local people from Chembe for their support during all phases of the experiment and two anonymous reviewers, and Thomas von Rintelen (editor) for their constructive and helpful comments.

The Members of Volkswagen Foundation Lake Malawi Field School 2012 Consortium

A. M. Weigand, M. Plath, A. Klussmann-Kolb, H. Schweyen (Institute for Ecology, Evolution & Diversity, J.W.-Goethe University Frankfurt am Main, Germany), J. J. Agaba, A. Kyakuwa, C. U. Tolo (Department of Biology, Faculty of Science, Mbarara University of Science & Technology, Uganda), C. Albrecht, C. Clewing (Department of Animal Ecology and Systematics, Justus Liebig University Giessen, Germany), A. Apio, J. D. Bariyanga, J. M. Mindje, D. Umutoni (Umutara Polytechnic, Faculty of Veterinary Medicine, Nyagatare, Rwanda), M. Babu (Department of Environmental Sciences, Faculty of Science, Islamic University in Uganda, Uganda), M. Bäuchle (Department of Paleoanthropology, Research Institute Senckenberg, Frankfurt am Main, Germany), B. Banda, (Lake Malawi National Park, Malawi), E. Bandason, B. C. Makina, D. F. Pemba (Biology Department, Chancellor College, University of Malawi, Zomba, Malawi), M. Chipyola (Department of Environmental Affairs, Chancellor College, University of Malawi, Zomba, Malawi), C. M. Githukia (Kenya Marine and Fisheries Research Institute, Kegati Aquaculture Station, Kenya), J. K. Kochey, C. N. Lange, E. N. Linus (National Museums of Kenya, Nairobi, Kenya), K. D. Makasi, M. M. Maombi, M. Malikwisha, O. W. Ndeo (Department of Environment, Faculty of Science, Ruwenzori State University U.O.R., DR Congo), A.-M. Oppold, A. Seeland (Department of Aquatic Ecotoxicology, J. W.-Goethe University Frankfurt am Main, Germany), S. Schmid (Centre for Interdisciplinary African Studies (ZIAF), J. W.-Goethe University Frankfurt am Main, Germany), R. Schultheiß (Division of Genetics and Physiology, Department of Biology, Pharmacity, 20014 University of Turku, Finland).

Supplementary material

10750_2013_1705_MOESM1_ESM.doc (138 kb)
Supplementary material 1 (DOC 139 kb)
10750_2013_1705_MOESM2_ESM.pdf (2.2 mb)
Fig. S1 Study organism and selected food items. a Potamonautes lirrangensis female dorsal view. b P. lirrangensis female ventral view. c P. lirrangensis male dorsal view. d P. lirrangensis male ventral view. e Eichhornia crassipes. f Ceratophyllum cf. demersum. g Coelatura sp. h Melanoides sp. i Lanistes solidus. j Lanistes nyassanus (PDF 2268 kb)
10750_2013_1705_MOESM3_ESM.pdf (803 kb)
Fig. S2 Handled food items and chela dentition. a Crack in the central part of the shell of Bellamya robertsoni. b Single cracked individual of Lanistes solidus. c Partially eaten Eichhornia crassipes. d Potamonautes lirrangensis chela with generalized dentition (PDF 803 kb)

References

  1. Barbaresi, S. & F. Gherardi, 1997. Italian freshwater decapods: exclusion between the crayfish Austropotamobius pallipes (Faxon) and the river crab Potamon fluviatile (Herbst). Bulletin française de la Pêche et de la Piscicolture 347: 731–747.CrossRefGoogle Scholar
  2. Berthold, T., 1990. Phylogenetic relationships, adaptations and biogeographic origin of the Ampullariidae endemic to Lake Malawi. Abhandlungen und Verhandlungen des Naturwissenschaftlichen Vereins zu Hamburg 31(32): 47–84.Google Scholar
  3. Bromage, T. G., F. Schrenk & Y. M. Juwayeyi, 1995. Paleobiogeography of the Malawi Rift: age and vertebrate paleontology of the Chiwondo Beds, Northern Malawi. Journal of Human Evolution 28: 37–57.CrossRefGoogle Scholar
  4. Cohen, A. S., M. 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
  5. Cohen, A. S., J. R. Stone, K. R. M. Beuning, L. E. Park, P. N. Reinthal, D. Dettman, C. A. Scholz, T. C. Johnson, J. W. King, M. R. Talbot, E. T. Brown & S. J. Ivory, 2007. Ecological consequences of early Late Pleistocene megadroughts in tropical Africa. Proceedings of the National Academy of Sciences 104: 16422–16427.CrossRefGoogle Scholar
  6. Covich, A. P., 2010. Winning the biodiversity arms race among freshwater gastropods: competition and coexistence through shell variability and predator avoidance. Hydrobiologia 653: 191–215.CrossRefGoogle Scholar
  7. Cumberlidge, N. & P. K. L. Ng, 2009. Systematics, evolution and biogeography of freshwater crabs. In Martin, J. W., K. A. Crandall & D. L. Felder (eds), Crustacean Issues: Decapod crustacean Phylogenetics. CRC Press, Leiden: 491–508.Google Scholar
  8. Cumberlidge, N., P. K. L. Ng, D. C. J. Yeo, C. Magalhaes, M. R. Campos, F. Alvarez, T. Naruse, S. R. Daniels, L. J. Esser, F. Y. K. Attipoe, F.-L. Clotilde-Ba, W. Darwalli, A. McIvor, J. E. M. Baillie, B. Collen & M. Ram, 2009. Freshwater crabs and the biodiversity crisis: importance, threats, status, and conservation challenges. Biological Conservation 142: 1665–1673.CrossRefGoogle Scholar
  9. Day, J. J., J. A. Cotton & T. G. Barraclough, 2008. Tempo and mode of diversification of Lake Tanganyika cichlid fishes. PLoS ONE 3: e1730.PubMedCrossRefPubMedCentralGoogle Scholar
  10. Diederich, S., 2006. High survival and growth rates of introduced Pacific oysters may cause restrictions on habitat use by native mussels in the Wadden Sea. Journal of Experimental Marine Biology and Ecology 328: 211–227.CrossRefGoogle Scholar
  11. Dobson, M. K., 2004. Freshwater crabs in Africa. Freshwater Forum 21: 3–26.Google Scholar
  12. Erpenbeck, J., 1970. Untersuchungen zur Ökologie und Biologie von Potamon potamios rhodium Parisi (Decapoda, Potamidae). Ph.D. Thesis, Westfälische Wilhelms-Universität, Münster.Google Scholar
  13. Fryer, G., 1959. The trophic interrelationships and ecology of some littoral communities of Lake Nyasa with especial reference to the fishes, and a discussion of the evolution of a group of rock-frequenting Cichlidae. Proceedings of the Zoological Society of London 132: 153–281.CrossRefGoogle Scholar
  14. Gavrilets, S. & J. B. Losos, 2009. Adaptive radiation: contrasting theory with data. Science 323: 732–737.PubMedCrossRefGoogle Scholar
  15. Genner, M. J., E. Michel, D. Erpenbeck, N. De Voogd, F. Witte & J.-P. Pointier, 2004. Camouflaged invasion of Lake Malawi by an Oriental gastropod. Molecular Ecology 13: 2135–2141.PubMedCrossRefGoogle Scholar
  16. Genner, M. J., J. A. Todd, E. Michel, D. Erpenbeck, A. Jimoh, D. A. Joyce, A. Piechocki & J.-P. Pointier, 2007a. Amassing diversity in an ancient lake: evolution of a morphologically diverse parthenogenetic gastropod assemblage in Lake Malawi. Molecular Ecology 16: 517–530.PubMedCrossRefGoogle Scholar
  17. Genner, M. J., O. Seehausen, D. H. Lunt, D. A. Joyce, P. W. Shaw PW, G. R. Carvalho & G. F. Turner, 2007b. Age of cichlids: new dates for ancient lake fish radiations. Molecular Biology and Evolution 24: 1269–1282.PubMedCrossRefGoogle Scholar
  18. Gherardi, F., G. Messana, A. Ugolini & M. Vannini, 1988. Studies on the locomotor activity of the freshwater crab, Potamon fluviatile. Hydrobiologia 169: 241–250.CrossRefGoogle Scholar
  19. Gherardi, F., F. Tarducci & F. Micheli, 1989. Energy maximization and foraging strategies in Potamon fluviatile (Decapoda, Brachyura). Freshwater Biology 22: 233–245.CrossRefGoogle Scholar
  20. Glaubrecht, M., 2008. Adaptive radiation of thalassoid gastropods in Lake Tanganyika, East Africa: morphology and systematization of a paludomid species flock in an ancient lake. Zoosystematics and Evolution 84: 71–122.CrossRefGoogle Scholar
  21. Greenwood, P. H., 1981. The Haplochromine Species of East African Lakes: Collected Papers on their Taxonomy, Biology and Evolution (With an Introduction and Species Index). Krause International Publications, Munich.Google Scholar
  22. Gurdebeke, P. R. & B. Van Bocxlaer, 2013. Conchological differentiation in an ongoing radiation of Lanistes gastropods from ancient Lake Malawi: how adaptive is shell morphology? Geologica Belgica 16: 118–119.Google Scholar
  23. Hill, M. P. & J. H. O’Keeffe, 1992. Some aspects of the ecology of the freshwater crab (Potamonautes perlatus Milne Edwards) in the upper reaches of the BuValo River, Eastern Cape Province, South Africa. Southern African Journal of Aquatic Science 18: 42–50.CrossRefGoogle Scholar
  24. Horstkotte, J. & M. Plath, 2008. Divergent evolution of feeding substrate preferences in a phylogenetically young species flock of pupfish (Cyprinodon spp.). Naturwissenschaften 95: 1175–1180.PubMedCrossRefGoogle Scholar
  25. Horstkotte, J. & U. Strecker, 2005. Trophic differentiation in the phylogenetically young Cyprinodon species flock (Cyprinodontidae teleostei) from Laguna Chichancanab (Mexico). Biological Journal of the Linnean Society 85: 125–134.CrossRefGoogle Scholar
  26. Huberndick, B., 1952. On the evolution of the so-called thalassoid molluscs of Lake Tanganyika. Arkiv för Zoologi 3: 319–323.Google Scholar
  27. Klaus, S. & M. Plath, 2011. Predation on a cave fish by the freshwater crab Avotrichodactylus bidens (Bott, 1969) (Brachyura: Trichodactylidae) in a Mexican sulfur cave. Crustaceana 84: 411–418.CrossRefGoogle Scholar
  28. Louda, S. M. & K. R. McKaye, 1982. Diurnal movements in populations of the prosobranch Lanistes nyassanus at Cape Maclear, Lake Malawi, Africa. Malacologia 23: 13–21.Google Scholar
  29. Louda, S. M., K. R. McKaye, T. D. Kocher & C. J. Stackhouse, 1984. Activity, dispersion, and size of Lanistes nyassanus and L. solidus (Gastropoda, Ampullariidae) over the depth gradient at Cape Maclear, Lake Malawi, Africa. The Veliger 26: 145–152.Google Scholar
  30. Marijnissen, S. A. E., E. Michel, S. R. Daniels, D. Erpenbeck, S. B. J. Menken & F. R. Schram, 2006. Molecular evidence for recent divergence of Lake Tanganyika endemic crabs (Decapoda: Platythelphusidae). Molecular Phylogenetics and Evolution 40: 628–634.PubMedCrossRefGoogle Scholar
  31. Marijnissen, S. A. E., E. Michel, K. Kamermans, K. Olaya-Bosch, M. Kars, D. F. R. Cleary, E. E. van Loon, P. G. R. Dolmen & S. B. J. Menken, 2008. Ecological correlates of species in the Lake Tanganyika crab radiation. Hydrobiologia 615: 81–94.CrossRefGoogle Scholar
  32. Marijnissen, S. A. E., E. Michel, D. F. R. Cleary & P. B. McIntyre, 2009. Ecology and conservation status of endemic freshwater crabs in Lake Tanganyika, Africa. Biodiversity and Conservation 18: 1555–1573.CrossRefGoogle Scholar
  33. McGlue, M. M., K. E. Lezzar, A. S. Cohen, J. M. Russell, J. J. Tiercelin, A. A. Felton, E. Mbede & H. H. Nkotagu, 2007. Seismic records of late Pleistocene aridity in Lake Tanganyika, tropical East Africa. Journal of Paleolimnology 40: 635–653.CrossRefGoogle Scholar
  34. McKaye, K. R., J. R. Stauffer & S. M. Louda, 1986. Fish predation as a factor in the distribution of Lake Malawi gastropods. Experimental Biology 45: 279–289.PubMedGoogle Scholar
  35. Michel, E., 1994. Why snails radiate: a review of gastropod evolution in long-lived lakes, both recent and fossil. Archiv für Hydrobiologie 44: 285–317.Google Scholar
  36. Ng, P. K. L., 1988. The Freshwater Crabs of Peninsular Malaysia and Singapore. National University of Singapore. Shinglee Press, Singapore.Google Scholar
  37. Plath, M., R. Riesch, Z. W. Culumber, B. Streit & M. Tobler, 2011. Giant water bug (Belostoma sp.) predation on a cave fish (Poecilia mexicana): effects of female body size and gestational state. Evolutionary Ecology Research 13: 133–144.Google Scholar
  38. Rathbun, M., 1904. Les Crabes d’Eau Douce (Potamonidae). Nouvelles Archives du Museum D’Histoire Naturelle De Paris 4: 225–312.Google Scholar
  39. Reed, S. K. & N. Cumberlidge, 2006. Taxonomy and biogeography of the freshwater crabs of Tanzania, East Africa (Brachyura: Potamoidea: Potamonautidae, Platythelphusidae, Deckeniidae). Zootaxa 1262: 1–139.Google Scholar
  40. Scalici, M. & G. Gibertini, 2007. Feeding habits of the cray-fish Austropotamobius pallipes (Decapoda, Astacidae) in a brook of Latium (central Italy). Italian Journal of Zoology 74: 157–168.CrossRefGoogle Scholar
  41. Schneider, P., 1971. Zur Biologie der afghanischen Flußkrabbe Potamon gedrosianum. 1. Lebensweise, Verbreitung, Morphologie und systematische Stellung. Bonner Zoologische Beiträge 22: 305–321.Google Scholar
  42. Scholz, C. A., T. C. Johnson, A. S. Cohen, J. W. King, J. A. Peck, J. T. Overpeck, M. R. Talbot, E. T. Brown, L. Kalindekafe, P. Y. O. Amoako, R. P. Lyons, T. M. Shanahan, I. S. Castaneda, C. W. Heil, S. L. Forman, L. R. McHargue, K. R. Beuning, J. Gomez & J. Pierson, 2007. East African megadroughts between 135 and 75 thousand years ago and bearing on early-modern human origins. Proceedings of the National Academy of Sciences 104: 16416–16421.CrossRefGoogle Scholar
  43. Schubart, C. D. & P. K. L. Ng, 2008. A new molluscivore crab from Lake Poso confirms multiple colonisation of ancient lakes in Sulawesi by freshwater crabs (Decapoda: Brachyura). Zoological Journal of the Linnean Society 154: 211–221.Google Scholar
  44. Schultheiß, R., B. Van Bocxlaer, T. Wilke & C. Albrecht, 2009. Old fossils—young species: evolutionary history of an endemic gastropod assemblage in Lake Malawi. Proceedings of the Royal Society B 276: 2837–2846.PubMedCrossRefPubMedCentralGoogle Scholar
  45. Schultheiß, R., T. Wilke, A. Jørgensen & C. Albrecht, 2011. The birth of an endemic species flock: demographic history of the Bellamya group (Gastropoda, Viviparidae) in Lake Malawi. Biological Journal of the Linnean Society 102: 130–143.CrossRefGoogle Scholar
  46. Seehausen, O., 2006. African cichlid fish: a model system in adaptive radiation research. Proceedings of the Royal Society B 273: 1987–1998.PubMedCrossRefPubMedCentralGoogle Scholar
  47. Somers, M. J. & J. A. J. Nel, 1998. Dominance and population structure of freshwater crabs (Potamonautes perlatus Milne Edwards). South African Journal of Zoology 33: 31–36.Google Scholar
  48. Turkheimer, F. E., R. Hinz & V. J. Cunningham, 2003. On the undecidability among kinetic models: from model selection to model averaging. Journal of Cerebral Blood Flow and Metabolism 23: 490–498.PubMedCrossRefGoogle Scholar
  49. Van Damme, D. & A. Gautier, 2012. Lacustrine mollusc radiations in the Malawi Basin: experiments in a natural laboratory for evolution. Biogeosciences Discussions 9: 18519–18544.CrossRefGoogle Scholar
  50. Verheyen, E., W. Salzburger, J. Snoeks & A. Meyer, 2003. Origin of the superflock of cichlid fishes from Lake Victoria, East Africa. Science 300: 325–329.PubMedCrossRefGoogle Scholar
  51. Vermeij, G. J., 1974. Marine faunal dominance and molluscan shell form. Evolution 28: 656–664.CrossRefGoogle Scholar
  52. Vermeij, G. J. & A. P. Covich, 1978. Coevolution of freshwater gastropods and their predators. American Naturalist 112: 833–843.CrossRefGoogle Scholar
  53. von Rintelen, T., A. B. Wilson, A. Meyer & M. Glaubrecht, 2004. Escalation and trophic specialization drive adaptive radiation of freshwater gastropods in ancient lakes on Sulawesi, Indonesia. Proceedings of the Royal Society B 271: 2541–2549.CrossRefGoogle Scholar
  54. West, K. & A. Cohen, 1994. Predator-prey coevolution as a model for the unusual morphologies of the crabs and gastropods of Lake Tanganyika. Archiv für Hydrobiologie 44: 267–283.Google Scholar
  55. West, K. & A. Cohen, 1996. Shell microstructure of gastropods from Lake Tanganyika, Africa: adaptation, convergent evolution, and escalation. Evolution 50: 672–681.CrossRefGoogle Scholar
  56. West, K., A. Cohen & M. Baron, 1991. Morphology and behavior of crabs and gastropods from Lake Tanganyika, Africa: Implications for lacustrine predator–prey coevolution. Evolution 45: 589–607.CrossRefGoogle Scholar
  57. Williams, T. R., 1961. The diet of freshwater crabs associated with Simulium neavei in East Africa. I. Crabs from West and East Uganda collected by the Cambridge East African Expedition 1959. Annals of Tropical Medicine and Parasitology 55: 128–131.PubMedGoogle Scholar
  58. Yeo, D. C. J., P. K. L. Ng, N. Cumberlidge, C. Magalhaes, S. R. Daniels & M. R. Campos, 2008. Global diversity of crabs (Crustacea: Decapoda: Brachyura) in freshwater. Hydrobiologia 595: 275–286.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • A. M. Weigand
    • 1
  • The Volkswagen Foundation Lake Malawi Field School 2012 Consortium
  • M. Plath
    • 1
  1. 1.Institute for Ecology, Evolution & DiversityJ.W.-Goethe University Frankfurt am MainFrankfurtGermany

Personalised recommendations