Abstract
The Lake Edward system in Eastern Central Africa, including Lakes Edward and George and their associated rivers, is home to a species assemblage of endemic haplochromine cichlids. Currently, 36 of these species have been formally described, while it is estimated that the system may harbour a total of 60 species. Species flocks of haplochromine cichlids are morphologically and ecologically very diverse and have radiated into many specialised trophic niches. Paedophagy is the feeding on eggs and larvae. In Haplochromis, most paedophages steal fry and eggs from the buccal cavities of mouthbrooding female cichlids. Hitherto, one formally described species with this diet is known from the Lake Edward system: Haplochromis taurinus. We performed a morphometrical revision of all species of Haplochromis from this system with a morphology that suggests a paedophagous diet: long oral jaws set with small teeth. Sixty-eight specimens were studied by taking 28 measurements and 20 counts and by performing stomach content observations. We discovered that H. paradoxus also had a paedophagous diet. Our analyses further revealed the presence of three new species: H. gracilifur sp. nov., H. molossus sp. nov., and H. relictidens sp. nov. All five of these species were described or redescribed.
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References
Barel, C. D. N., F. Witte & M. J. P. van Oijen, 1976. The shape of the skeletal elements in the head of a generalized Haplochromis species: H. elegans Trewavas 1933 (Pisces, Cichlidae). Netherlands Journal of Zoology 26: 163–265.
Barel, C. D. N., M. J. P. van Oijen, F. Witte & E. L. M. Witte-Maas, 1977. An introduction to the taxonomy and morphology of the haplochromine cichlids from Lake Victoria. Netherlands Journal of Zoology 27: 333–389.
Boulenger, G. A., 1906. Descriptions of new fishes discovered by Mr. E. Degen in Lake Victoria. Annals and Magazine of Natural History 17: 433–452.
Boulenger, G. A., 1911. On a third collection of fishes made by Dr. E. Bayon in Uganda, 1909–1910. (Collezioni zoologiche fatte nell-Uganda dal Dott. E. Bayon. XII.). Annali del Museo Civico di Storia Naturale de Genova 5: 64–78.
Boulenger, G. A., 1914. Fische. In Wissenschaftlichen ergebnisse der Deutschen Zentral-Afrika Expedition, 1907–1908, Zoologie,Vol. 3: 354.
de Zeeuw, M. P., M. Mietes, P. Niemantsverdriet, S. ter Huurne & F. Witte, 2010. Seven new species of detritivorous and phytoplanktivorous haplochromines from Lake Victoria. Zoologische Mededelingen Leiden 84: 201–250.
Froese, R. & D. Pauly (eds), 2018. Fishbase. www.fishbase.org, version 02/2018. Accessed June 2018.
Fryer, G. & T. D. Iles, 1972. The cichlid fishes of the Great Lakes of Africa: their biology and evolution. Oliver & Boyd, Edinburgh.
Givnish, T. J., 2015. Adaptive radiation versus ‘radiation’ and ‘explosive diversification’: why conceptual distinctions are fundamental to understanding evolution. New Phytologist 207: 297–303.
Goldschmidt, T., 2004. Darwins Hofvijver: Een Drama in Het Victoriameer. Uitgeverij Bert Bakker, Amsterdam.
Greenwood, P. H., 1959. A revision of the Lake Victoria Haplochromis species (Pisces, Cichlidae), Part III. Bulletin British Museum (Natural History) Zoology 5: 179–218.
Greenwood, P. H., 1962. A revision of the Lake Victoria Haplochromis species (Pisces, Cichlidae). Part V. Bulletin of the British Museum (Natural History) Zoology 9: 139–214.
Greenwood, P. H., 1967. A revision of the Lake Victoria Haplochromis species (Pisces, Cichlidae). Part VI. Bulletin of the British Museum (Natural History) Zoology 15: 31–119.
Greenwood, P. H., 1973. A revision of the Haplochromis and related species (Pisces: Cichlidae) from Lake George, Uganda. Bulletin of the British Museum (Natural History) Zoology 25: 141–242.
Greenwood, P. H., 1974. The cichlid fishes of Lake Victoria, East Africa: the biology and evolution of a species flock. Bulletin of the British Museum (Natural History) Zoology 25: 1–134.
Greenwood, P. H., 1979. Towards a phyletic classification of the ‘genus’ Haplochromis (Pisces, Cichlidae) and related taxa. Part 1. Bulletin of the British Museum (Natural History) Zoology 35: 265–322.
Greenwood, P. H., 1980. Towards a phyletic classification of the ‘genus’ Haplochromis (Pisces, Cichlidae) and related taxa. Part II; the species from lakes Victoria, Nabugabo, Edward, George and Kivu. Bulletin of the British Museum (Natural History) Zoology 39: 1–101.
Greenwood, P. H., 1991. Speciation. In Keenleyside, M. H. (ed.), Cichlid Fishes: Behaviour, ecology and Evolution. Springer, Netherlands: 86–102.
Hammer, Ø., D. A. T. Harper & P. D. Ryan, 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: 9.
Hoogerhoud, R. J. C., 1984. A taxonomic reconsideration of the haplochromine genera Gaurochromis Greenwood, 1980 and Labrochromis Regan, 1920 (Pisces, Cichlidae). Netherlands Journal of Zoology 34: 539–656.
Hulot, A., 1956. Aperçu sur la question de la pêche industrielle aux lacs Kivu, Edouard et Albert. Bulletin Agricole du Congo Belge 47: 1–68.
Kocher, T. D., 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nature Reviews Genetics 5: 288–298.
Konings, A., 2013. Tropheus in their Natural Habitat. Cichlid press, El Paso.
Linnaeus, C., 1758. Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata. Holmiae: Laurentii Salvii.
Lippitsch, E., 2003. Redescription of ‘Haplochromis’ nubilus (Teleostei: Cichlidae), with description of two new species. Ichthyological Exploration of Freshwaters 14: 85–95.
Lippitsch, E. & L. Kaufman, 2003. Pyxichromis paradoxus (Perciformes: Cichlidae), a new haplochromine species from Lake Edward, East Africa, and reassessment of the genus Pyxichromis Greenwood, 1980. Zeitschrift für Fischkunde 6: 87–98.
Machado-Schiaffino, G., A. F. Kautt, H. Kusche & A. Meyer, 2015. Parallel evolution in Ugandan crater lakes: repeated evolution of limnetic body shapes in haplochromine cichlid fish. BMC Evolutionary Biology 15: 9.
McKaye, K. R. & T. D. Kocher, 1983. Head ramming behaviour by three paedophagous cichlids in Lake Malawi, Africa. Animal Behaviour 31: 206–210.
McKaye, K. R., & C. Mackenzie, 1982. Cyrtocara liemi, a previously undescribed paedophagous cichlid fish (Teleostei: Cichlidae) from Lake Malawi, Africa. Proceedings of the Biological Society of Washington 95: 398–402.
Meier, J. I., D. A. Marques, S. Mwaiko, C. E. Wagner, L. Excoffier & O. Seehausen, 2017. Ancient hybridization fuels rapid cichlid fish adaptive radiations. Nature Communications 8: 14363.
Meyer, A., T. D. Kocher, P. Basasibwaki & A. C. Wilson, 1990. Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 374: 550–553.
Nagl, S., H. Tichy, W. E. Mayer, N. Takezaki, N. Takahata & J. Klein, 2000. The origin and age of haplochromine fishes in Lake Victoria, East Africa. Proceedings of The Royal Society B 267: 1049–1061.
Pellegrin, J., 1904. Diagnoses préliminaires de Poissons nouveaux du Lac Victoria, recueillis par M. Allaud. Bulletin de la Société Zoologique de France 29: 184–186.
Pfeffer, G. J., 1896. Die Thierwelt Ost-Afrikas und der Nachbargebiete, Lieferung V. Geographische Verlagshandlung Dietrich Reimer, Berlin.
Poll, M., 1939a. Poissons. In Exploration du Parc National Albert Mission G. F. de Witte (1933–1935). Institut des Parcs Nationaux du Congo Belge 24, Bruxelles.
Poll, M., 1939b. Poissons. In Exploration du Parc National Albert Mission H. Damas (1935–1936). Institut des Parcs Nationaux du Congo Belge 6, Bruxelles.
Regan, C. T., 1920. The classification of the fishes of the family Cichlidae–I. The Tanganyika genera. Annals and Magazine of Natural History 5: 33–53.
Regan, C. T., 1921. The cichlid fishes of lakes Albert, Edward and Kivu. Annals and Magazine of Natural History 9: 632–639.
Regan, C. T., 1922. The cichlid fishes of Lake Nyassa. Proceedings of the Zoological Society of London 1921: 675–727.
Ribbink, A. J. & A. C. Ribbink, 1997. Paedophagia among cichlid fishes of Lake Victoria and Lake Malawi/Nyasa. South African Journal of Science 93: 509–512.
Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.
Salzburger, W., A. Meyer, S. Baric, E. Verheyen & C. Sturmbauer, 2002. Phylogeny of the Lake Tanganyika cichlid species flock and its relationship to the central and East African haplochromine cichlid fish faunas. Systematic Biology 51: 113–135.
Salzburger, W., T. Mack, E. Verheyen & A. Meyer, 2005. Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC evolutionary biology 5: 17.
Schluter, D. & L. M. Nagel, 1995. Parallel speciation by natural selection. The American Naturalist 146: 292–301.
Seehausen, O., 1996. Lake Victoria Rock Cichlids: Taxonomy, Ecology, and Distribution. Verduyn Cichlids, Zevenhuizen.
Seehausen, O., 2006. African cichlid fish: a model system in adaptive radiation research. Proceedings of The Royal Society B 273: 1987–1998.
Snoeks, J., 1988. Redescription d’Haplochromis paucidens Regan, 1921 et description d’Haplochromis occultidens sp. n. (Pisces, Cichlidae) du Lac Kivu en Afrique. Cybium 12: 203–218.
Snoeks, J., 1994. The haplochromine fishes (Teleostei, Cichlidae) of Lake Kivu, East Africa: a taxonomic revision with notes on their ecology. Koninklijk Museum voor Midden-Afrika, Tervuren, Belgium.
Snoeks, J., 2000. How well known is the ichthyodiversity of the large East African lakes? In Rossiter, A. & H. Kawanabe (eds), Advances in Ecological Research, Vol. 31. Academic Press, London: 17–38.
Snoeks, J., 2001. Cichlid diversity, speciation and systematics: examples for the Great African Lakes. Journal of Aquariculture and Aquatic Sciences 9: 150–166.
Snoeks, J., 2004. The Cichlid Diversity of Lake Malawi/Nyasa/Niassa: Identification, Distribution and Taxonomy. Cichlid Press, El Paso.
Stiassny, M. L. J. & A. Meyer, 1999. Cichlids of the Rift Lakes. Scientific American 280: 64–69.
Trewavas, E., 1933. Scientific results of the Cambridge expedition to the East African Lakes, 1930-1.–11.: the cichlid fishes. Journal of the Linnean Society of London, Zoology 38: 309–341.
Trewavas, E., 1935. A synopsis of the cichlid fishes of Lake Nyasa. Annals and Magazine of Natural History 10: 65–118.
Turner, G. F., 1996. Offshore cichlids of Lake Malawi. Cichlid Press, Lauenau, Germany.
van Oijen, M. J. P., 1991. A systematic revision of the piscivorous haplochromine Cichlidae (Pisces: Teleostei) of Lake Victoria (East Africa). Part I. Zoologische Verhandelingen 272: 1–95.
van Oijen, M. J. P., 1996. The generic classification of the haplochromine cichlids of Lake Victoria, East Africa. Zoologische Verhandelingen 302: 57–110.
Verbeke, J., 1957. Exploration hydrobiologique des lacs Kivu, Edouard et Albert. Institut Royal des Sciences Naturelles de Belgique, Bruxelles.
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.
Wagner, C. E., I. Keller, S. Wittwer, O. M. Selz, S. Mwaiko, L. Greuter, A. Sivasundar & O. Seehausen, 2013. Genome-wide RAD sequence data provide unprecedented resolution of species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Molecular Ecology 22: 787–798.
Wilhelm, W., 1980. The disputed feeding behaviour of a paedophagous haplochromine cichlids (Pisces) observed and discussed. Behaviour 74: 310–323.
Witte-Maas, E. L. M., 1981. Eggsnatching: an observation on the feeding behaviour of Haplochromis Barbarae Greenwood, 1967 (Pisces, Cichlidae). Netherlands journal of zoology 31: 786–789.
Witte, F. & M. J. P. van Oijen, 1990. Taxonomy, ecology and fishery of Lake Victoria haplochromine trophic groups. Zoologische Verhandelingen 262: 1–47.
Witte, F. & M. J. P. van Oijen, 1995. Biology of haplochromine trophic groups. In van Densen, W. L. T. (ed.), Fish Stocks and Fisheries of Lake Victoria. A handbook for field observations. Samara Publishing Limited, Cardigan: 321–335.
Zelditch, M. L., D. L. Swiderski, H. D. Sheets & W. L. Fink, 2004. Geometric Morphometrics for Biologists: A Primer. Elsevier Academic Press, London.
Acknowledgements
This research is part of the BELSPO (Belgian Science Policy) funded BRAIN project “HIPE”: Human impacts on ecosystem health and resources of Lake Edward. Fieldwork of M. Van Steenberge was supported by the research foundation Flanders (FWO, V435116 N) and the King Leopold III Fund for Nature Exploration and Conservation. We thank M. Mulongaibalu (UoB) and L. Mwaiswa for their help in collecting specimens and E. Decru (RMCA) for her contributions to the research and her helpful comments. We are grateful to A. Reygel (RMCA) for drawing the figures of all specimens, to J. Brecko (RMCA) for taking pictures of the pharyngeal jaws in the framework of the DIGIT03 project, and to M. Parrent (RMCA) for curatorial services.
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Guest editors: S. Koblmüller, R. C. Albertson, M. J. Genner, K. M. Sefc & T. Takahashi / Advances in Cichlid Research III: Behavior, Ecology and Evolutionary Biology
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Vranken, N., Van Steenberge, M. & Snoeks, J. Grasping ecological opportunities: not one but five paedophagous species of Haplochromis (Teleostei: Cichlidae) in the Lake Edward system. Hydrobiologia 832, 105–134 (2019). https://doi.org/10.1007/s10750-018-3742-5
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DOI: https://doi.org/10.1007/s10750-018-3742-5