Skip to main content

Advertisement

SpringerLink
Log in

Just below the surface, the pelagic haplochromine cichlids from the Lake Edward system

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The East African Great Lakes are inhabited by impressive radiations of cichlids that display a large variation in morphology, diet, colour pattern, and behaviour and have adapted to a large array of niches. Whilst most of these cichlids are bottom dwellers, a number of species have adapted to a pelagic environment and inhabit open waters. From the Lake Edward system, one pelagic species had been previously described, the zooplanktivorous Haplochromis pappenheimi. Our sampling revealed the Lake Edward system to be inhabited by two more pelagic species that were unknown to science and are formally described here, the zooplanktivorous Haplochromis pelagicus sp. nov. and the insectivorous H. aureus sp. nov. All three species seem mostly restricted to deepwater regions where the depth exceeds six metres in Lake Edward, except for H. pelagicus sp. nov., which also occurs in shallower regions of Lakes Edward and George and of the Kazinga Channel. Sexual dimorphism, mainly in head shape, was discovered in H. pappenheimi and H. pelagicus sp. nov. These differences suggest that females of these species have larger buccal cavities than males, which is most likely linked to female mouth brooding behaviour.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

Raw data of all catches generated during this study are provided in Supplementary information (Table S1). Summarised morphometric data are provided in Table 2 and Supplementary information (Table S12); raw morphometric data is available from the corresponding author on reasonable request.

References

  • 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 Cichlidae from Lake Victoria. Netherlands Journal of Zoology 27: 333–380. https://doi.org/10.1163/002829677X00199.

    Article  Google Scholar 

  • Barel, C. D. N., 1983. Towards a constructional morphology of cichlid fishes (Teleostei, Perciformes). Netherlands Journal of Zoology 33: 357–424.

    Article  Google Scholar 

  • Boulenger, G. A., 1914. Cichlidae In Pappenheim, P. & G. A. Boulenger (eds), Fishe. Wissenschaftliche ergebnisse der Deutschen Zentral-Africa-Expedition, 1907–1908. pp. 253–259.

  • Boulenger, G. A., 1915. Catalogue of the fresh-water fishes of Africa in the British Museum (Natural History). Volume III. Trustees of the BMNH, London.

  • Buris, M. J., J. P. E. C. Darlington, I. G. Dunn, G. G. Ganf, J. J. Gwahaba & L. M. McGowan, 1973. The biomass and distribution of organisms in Lake George, Uganda. Proceedings of the Royal Society of London Series b: Biological Sciences 184: 271–298. https://doi.org/10.1098/rspb.1973.0049.

    Article  Google Scholar 

  • de Zeeuw, M. P., I. Westbroek, M. J. P. Van Oijen & F. Witte, 2012. Two new species of zooplanktivorous haplochromine cichlids from Lake Victoria, Tanzania. ZooKeys 256: 1–34. https://doi.org/10.3897/zookeys.256.3871.

    Article  Google Scholar 

  • Decru, E., N. Vranken, P. H. N. Bragança, J. Snoeks & M. Van Steenberge, 2020. Where ichthyofaunal provinces meet: the fish fauna of the Lake Edward system, East Africa. Journal of Fish Biology 96: 1186–1201. https://doi.org/10.1111/jfb.13992.

    Article  PubMed  Google Scholar 

  • Decru, E., N. Vranken, H. Maetens, A. Mertens De Vry, A. Kayenbergh, J. Snoeks & M. Van Steenberge, 2022. DNA barcoding the Lake Edward basin: high taxonomic coverage of a tropical freshwater ichthyofauna. Hydrobiologia 849: 1743–1762. https://doi.org/10.1007/s10750-022-04812-0.

    Article  CAS  Google Scholar 

  • Dunn, I. G., 1975. Ecological notes on the Haplochromis (Pisces: Cichlidae) species-flock of Lake George, Uganda (East Africa). Journal of Fish Biology 7: 651–666. https://doi.org/10.1111/j.1095-8649.1975.tb04638.x.

    Article  Google Scholar 

  • Everson, I., A. Taabu-Munyaho & R. Kayanda, 2013. Acoustic estimates of commercial fish species in Lake Victoria: moving towards ecosystem-based fisheries management. Fisheries Research 139: 65–75. https://doi.org/10.1016/j.fishres.2012.09.019.

    Article  Google Scholar 

  • Feilich, K. L., 2016. Correlated evolution of body and fin morphology in the cichlid fishes. Evolution 70: 2247–2267. https://doi.org/10.1111/evo.13021.

    Article  PubMed  Google Scholar 

  • Fryer, G. & T. D. Iles, 1972. The cichlid fishes of the Great Lakes of Africa. Their biology and evolution. Oliver and Boyd, Edinburgh. https://doi.org/10.2307/1442393.

  • Genner, M. J., P. Nichols, G. R. Carvalho, R. L. Robinson, P. W. Shaw & G. F. Turner, 2007. Reproductive isolation among deep-water cichlid fishes of Lake Malawi differing in monochromatic male breeding dress. Molecular Ecology 16: 651–662. https://doi.org/10.1111/j.1365-294X.2006.03173.x.

    Article  PubMed  Google Scholar 

  • Goudswaard, K. P. C., F. Witte & E. F. B. Katunzi, 2008. The invasion of an introduced predator, Nile perch (Lates niloticus, L.) in Lake Victoria (East Africa): chronology and causes. Environmental Biology of Fishes 81: 127–139. https://doi.org/10.1007/s10641-006-9180-7.

    Article  Google Scholar 

  • 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. https://doi.org/10.5962/bhl.part.16340.

    Article  Google Scholar 

  • Greenwood, P. H. & J. M. Gee, 1969. A revision of the Lake Victoria Haplochromis species (Pisces, Cichlidae), part VII. Bulletin of the British Museum (natural History) Zoology 18: 1–65.

    Article  Google Scholar 

  • 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: 139–242.

  • 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 Supplement 6: 134. https://doi.org/10.5962/p.119071.

    Article  Google Scholar 

  • 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). 35: 265–322. https://doi.org/10.5962/bhl.part.20455.

    Article  Google Scholar 

  • Greenwood, P. H., 1980. Towards a phyletic classification of the “genus” Haplochromis (Pisces, Cichlidae) and related taxa, part II. Bulletin of the British Museum (natural History) Zoology 39: 1–101. https://doi.org/10.5962/bhl.part.13268.

    Article  Google Scholar 

  • Goldschmidt, T., F. Witte, & J. de Visser, 1990. Ecological Segregation in Zooplanktivorous Haplochromine Species (Pisces: Cichlidae) from Lake Victoria. Oikos 58: 343. https://doi.org/10.2307/3545226.

    Article  Google Scholar 

  • Kolding, J., P. van Zwieten, F. Marttin, S. Funge-Smith & F. Poulain, 2019. Freshwater small pelagic fish and their fisheries in the major African lakes and reservoirs in relation to food security and nutrition. FAO Fisheries and Aquaculture Technical Paper 642: 124. https://doi.org/10.4060/ca0843en.

  • Konings, A. F., 2016. Malawi Cichlids in Their Natural Habitat, Cichlid Press, El Paso:

    Google Scholar 

  • Lærdal, T. & M. R. Talbot, 2002. Basin neotectonics of lakes Edward and George, East African Rift. Palaeogeography, Palaeoclimatology, Palaeoecology 187: 213–232. https://doi.org/10.1016/S0031-0182(02)00478-9.

    Article  Google Scholar 

  • Levring, T. & G. R. Fish, 1956. The penetration of light in some tropical East African waters. Oikos 7: 98–109. https://doi.org/10.2307/3564986.

    Article  Google Scholar 

  • Malinsky, M., H. Svardal, A. M. Tyers, E. A. Miska, M. J. Genner, G. F. Turner & R. Durbin, 2018. Whole-genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow. Nature Ecology & Evolution 2: 1940–1955. https://doi.org/10.1038/s41559-018-0717-x.

    Article  Google Scholar 

  • McGee, M. D., S. R. Borstein, J. I. Meier, D. A. Marques, S. Mwaiko, A. Taabu, M. A. Kishe-Machumu, B. O’Meara, R. Bruggmann, L. Excoffier & O. Seehausen, 2020. The ecological and genomic basis of explosive adaptive radiation. Nature 586: 75–79. https://doi.org/10.1038/s41586-020-2652-7.

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1038/ncomms14363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moriarty, D. J. W., J. P. E. C. Darlington, I. G. Dunn, C. M. Moriarty & M. P. Tevlin, 1973. Feeding and grazing in Lake George, Uganda. Proceedings of the Royal Society b: Biological Sciences 184: 299–319. https://doi.org/10.1098/rspb.1973.0050.

    Article  Google Scholar 

  • Murrell, P., 2005. R Graphics, Chapman & Hall/CRC Press, New York:

    Book  Google Scholar 

  • Okuda, N., M. Miyazaki & Y. Yanagisawa, 2002. Sexual difference in buccal morphology of the paternal mouthbrooding cardinalfish Apogon doederleini. Zoological Science 19: 801–807. https://doi.org/10.2108/zsj.19.801.

    Article  PubMed  Google Scholar 

  • Rasband, W. S., 2018. ImageJ, version 1.52a. National Institutes of Health, Bethesda, Maryland, USA.

  • Regan, C. T., 1921. The Cichlid fishes of lakes albert Edward and Kivu. Annals and Magazine of Natural History Series 9: 632–639. https://doi.org/10.1080/00222932108632633.

    Article  Google Scholar 

  • Rice, W. R., 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.

    Article  PubMed  Google Scholar 

  • Ronco, F., M. Roesti & W. Salzburger, 2019. A functional trade-off between trophic adaptation and parental care predicts sexual dimorphism in cichlid fish. Proceedings of the Royal Society b: Biological Sciences 286: 20191050. https://doi.org/10.1098/rspb.2019.1050.

    Article  PubMed Central  Google Scholar 

  • Ronco, F., M. Matschiner, A. Böhne, A. Boila, H. H. Büscher, A. Indermaur, A. El Taher, M. Malinsky, V. Ricci, A. Kahmen, S. Jentoft & W. Salzburger, 2021. Drivers and dynamics of a massive adaptive radiation in African cichlid fish. Nature 589: 76–81. https://doi.org/10.1038/s41586-020-2930-4.

    Article  CAS  PubMed  Google Scholar 

  • Seehausen, O., 1996. Lake Victoria Rock Cichlids: Taxonomy, Ecology, and Distribution. Verduyn Cichlids.

  • 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-Africa, Tervuren, Belgium.

  • Trewavas, E., 1933. Scientific results of the Cambridge expedition to the East African Lakes, 1930-1. The cichlid fishes. Zoological Journal of the Linnean Society Blackwell Publishing Ltd 38: 309–341.

    Google Scholar 

  • tkint, T., E. Verheyen, B. De Kegel, P. Helsen & D. Adriaens, 2012. Dealing with food and eggs in mouthbrooding cichlids: structural and functional trade-offs in fitness related traits. PLoS ONE 7: e31117. https://doi.org/10.1371/journal.pone.0031117.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Oijen, M. J. P., 1996. The generic classification of the haplochromine cichlids of Lake Victoria, East Africa. Zoologische Verhandelingen 302: 57–110.

    Google Scholar 

  • van Oijen, M. J. P. & F. Witte, 1996. Taxonomical and ecological description of a species complex of zooplanktivorous and insectivorous cichlids from Lake Victoria. Zoologische Verhandelingen 3–56.

  • van Rijssel, J. C. & F. Witte, 2013. Adaptive responses in resurgent Lake Victoria cichlids over the past 30 years. Evolutionary Ecology 27: 253–267. https://doi.org/10.1007/s10682-012-9596-9.

    Article  Google Scholar 

  • van Rijssel, J. C., E. S. Hoogwater, M. A. Kishe-Machumu, E. van Reenen, K. V. Spits, R. C. van der Stelt, J. H. Wanink & F. Witte, 2015. Fast adaptive responses in the oral jaw of Lake Victoria cichlids. Evolution 69: 179–189. https://doi.org/10.1111/evo.12561.

    Article  PubMed  Google Scholar 

  • 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. https://doi.org/10.1126/science.1080699.

    Article  CAS  PubMed  Google Scholar 

  • Vranken, N., M. Van Steenberge & J. Snoeks, 2019. Grasping ecological opportunities: not one but five paedophagous species of Haplochromis (Teleostei: Cichlidae) in the Lake Edward system. Hydrobiologia 832: 105–134. https://doi.org/10.1007/s10750-018-3742-5.

    Article  CAS  Google Scholar 

  • Vranken, N., M. Van Steenberge, A. Balagizi & J. Snoeks, 2020a. The synonymy of Haplochromis pharyngalis and Haplochromis petronius (Cichlidae). Journal of Fish Biology 97: 1554–1559. https://doi.org/10.1111/jfb.14455.

    Article  PubMed  Google Scholar 

  • Vranken, N., M. Van Steenberge, A. Kayenbergh & J. Snoeks, 2020b. The lobed-lipped species of Haplochromis (Teleostei, Cichlidae) from Lake Edward, two instead of one. Journal of Great Lakes Research 46: 1079–1089. https://doi.org/10.1016/j.jglr.2019.05.005.

    Article  Google Scholar 

  • Vranken, N., M. Van Steenberge & J. Snoeks, 2020c. Similar ecology, different morphology: three new species of oral-mollusc shellers from Lake Edward. Journal of Fish Biology 96: 1202–1217. https://doi.org/10.1111/jfb.14107.

    Article  PubMed  Google Scholar 

  • Vranken, N., M. Van Steenberge, A. Heylen, E. Decru & J. Snoeks, 2022. From a pair to a dozen: the piscivorous species of Haplochromis (Cichlidae) from the Lake Edward system. European Journal of Taxonomy 815: 1–94. https://doi.org/10.5852/ejt.2022.815.1749.

    Article  Google Scholar 

  • Witte, F. & M. J. P. van Oijen, 1990. Taxonomy, ecology and fishery of Lake Victoria haplochromine trophic groups. Zoologische Verhandelingen 262: 1–47.

    Google Scholar 

  • Witte, F. & E. L. M. Witte-Maas, 1987. Implications for taxonomy and morphology of intra-specific variation in haplochromine cichlids of Lake Victoria, with descriptions of five zooplanktivorous species. From form to fishery, PhD thesis, Rijksuniversiteit Leiden.

  • Witte, F., T. Goldschmidt, J. H. Wanink, M. J. P. van Oijen, K. Goudswaard, E. L. M. Witte-Maas & N. Bouton, 1992. The destruction of an endemic species flock: quantitative data on the decline of the haplochromine cichlids of Lake Victoria. Environmental Biology of Fishes 34: 1–28. https://doi.org/10.1007/BF00004782.

    Article  Google Scholar 

  • Zelditch, M. L., D. L. Swiderski, H. D. Sheets & W. L. Fink, 2004. Geometric Morphometrics for Biologists: A Primer. Elsevier Academic Press, London, UK.

    Google Scholar 

Download references

Acknowledgements

This research was conducted within the framework of the BELSPO (Belgian Science Policy Office) funded BRAIN projects HIPE (Human impacts on ecosystem health and resources of Lake Edward) and KEAFish (The biodiversity, biogeography and evolutionary history of the northern basins of the Great African Lakes: the enigmatic fish faunas of Lakes Kivu, Edward and Albert revisited) and an FWO (Research Foundation Flanders) funded PhD fellowship to NV (11E0520N). MM benefitted from a FishBase and Fish taxonomy training (2016) through the framework agreement of the RMCA with the Directorate-General for Development Cooperation and Humanitarian Aid. The fieldwork by NV, MVS, and ED was supported by the FWO and fieldwork by MVS by the King Leopold III Fund for Nature Exploration and Conservation. We thank L. Wasswa (Ugandan Fisheries Department) and M. Bifamengo (NaFIRRI, Uganda) for their help in collecting specimens, and W. Okello (NaFIRRI, Uganda) for valuable logistic support. We are grateful to M. Parrent (RMCA), O. Pauwels (IRSNB), J. Maclaine (NHMUK), and E. Aßel (ZMB) for curatorial services, E. Aßel for the provided photograph and X-ray image of the lectotype of H. pappenheimi, and support from the SYNTHESYS+ Project, http://www.synthesys.info/, which is financed by European Community Research Infrastructure Action under the H2020 Integrating Activities Programme, Project number 823827.

Author information

Authors and Affiliations

  1. Department of Biology, Fish Diversity and Conservation, KU Leuven, Charles Deberiotstraat 32, 3000, Leuven, Belgium

    Nathan Vranken & Jos Snoeks

  2. Section Vertebrates, Biology Department, Royal Museum for Central Africa, Leuvensesteenweg 13, 3080, Tervuren, Belgium

    Nathan Vranken & Jos Snoeks

  3. Operational Directorate Taxonomy and Phylogeny, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, 1000, Brussels, Belgium

    Maarten Van Steenberge

  4. Research Group Zoology, Biodiversity and Toxicology, Centre for Environmental Sciences, Hasselt University, Agoralaan Gebouw D, 3590, Diepenbeek, Belgium

    Maarten Van Steenberge

  5. Department of Environmental Management, Makerere University College of Agricultural and Environmental Sciences, Kampala, Uganda

    Mulongaibalu Mbalassa

  6. Section Hydrobiologie, Département de Biologie, Faculté des Sciences et Sciences Appliquées, Université Officielle de Bukavu, Bukavu, Democratic Republic of the Congo

    Mulongaibalu Mbalassa

Authors
  1. Nathan Vranken
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maarten Van Steenberge
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mulongaibalu Mbalassa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jos Snoeks
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nathan Vranken.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Additional information

Handling editor: Louise Chavarie

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 15 kb)

Supplementary file2 (DOCX 631 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vranken, N., Van Steenberge, M., Mbalassa, M. et al. Just below the surface, the pelagic haplochromine cichlids from the Lake Edward system. Hydrobiologia 850, 3173–3195 (2023). https://doi.org/10.1007/s10750-023-05246-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-023-05246-y

Keywords

Search

Navigation