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A laboratory study of host use by the cuckoo catfish Synodontis multipunctatus

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Abstract

The only known non-avian vertebrate obligate brood parasite is the cuckoo catfish (Synodontis multipunctatus), a Lake Tanganyikan endemic. The cuckoo catfish parasitizes Tanganyikan mouthbrooding cichlids, and under captive conditions, will also parasitize cichlids from other Rift Valley lakes. Here we examine the frequency of parasitism by the cuckoo catfish of Ctenochromis horei from Lake Tanganyika and three species from Lake Malawi and the greater Lake Victorian system in a laboratory setting. C. horei was parasitized significantly less (17%) than the allopatric species Haplochromis latifasciatus, Haplochromis nubilus, and Metriaclima estherae (combined parasitism rate of 28%). The lower rates of parasitism in C. horei may be due to differences in the mating ritual, oviposition (e.g., long periods of pseudo-spawning before actual oviposition), and behavioral adaptations (e.g., increased aggression towards the cuckoo catfish). The number of catfish eggs per parasitized brood was similar between C. horei, H. latifasciatus, H. nubilus, and M. estherae. Our results are comparable to findings from the field for C. horei parasitism frequency and number of cuckoo catfish per brood. We also analyzed the parasitism rate of the albino morph of Metriaclima zebra, a domestic strain. Parasitism rates and number of catfish per brood were the highest in the albino morphotype suggesting that the higher levels of parasitism may be related to lower aggressive behavior, lower visual acuity, or captive influence. Cuckoo catfish and mouthbrooding cichlids provide a model system for testing brood parasitism in a laboratory setting.

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References

  • Abadi RV, Pascal E (1991) Visual resolution limits in human albinism. Vis Res 31(7):1445–1447

    Article  PubMed  CAS  Google Scholar 

  • Barlow GW (2000) The cichlid fishes: Nature's grand experiment in evolution. Perseus Publishing, Cambridge, MA

    Google Scholar 

  • Boulenger GA (1898) Report on the fishes recently obtained by Mr. J.E.S. Moore in Lake Tanganyika. Proc Zool Soc London 1898(pt 3):494–497

    Google Scholar 

  • Boulenger GA (1899) A revision of the African and Syrian fishes of the family Cichlida.–part II.1. Proc Zool Soc London 67(1):98–144. https://doi.org/10.1111/j.1469-7998.1899.tb06852.x

    Article  Google Scholar 

  • Boulenger GA (1906) Descriptions of new fishes discovered by Mr. E. Degen in Lake Victoria. Annals and Magazine of Natural History. Vol (series 7) vol. 17 (no. 101) p(Art 49): 433–452

  • Brichard P (1979) Unusual breeding behavior in Lake Tanganyika cichlids Buntbarshe. Bulletin 74:10–12

    Google Scholar 

  • Cervo R, Macinai V, Dechigi F, Turillazzi S (2004) Fast growth of immature brood in a social parasite wasp: a convergent evolution between avian and insect cuckoos. Am Nat 164(6):814–820

    Article  PubMed  Google Scholar 

  • Cruz A, Knox J, Pawlowski S (2004) Caregiving-brood parasitism in freshwater fish. In: Bekoff M (ed) Encyclopedia of animal behavior. Vol 1. Greenwood Press, pp 180–182

  • Danley PD, Kocher TD (2001) Speciation in rapidly diverging systems: lessons from Lake Malawi. Mol Ecol 10:1075–1086

    Article  PubMed  CAS  Google Scholar 

  • Davies N (2000) Cuckoos, cowbirds and other cheats. T & a. D. Poyser Ltd, London

    Google Scholar 

  • Davies NB, Brooke ML (1989) An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. I. Host egg discrimination. J Anim Ecol 58(1):207–224. https://doi.org/10.2307/4995

    Article  Google Scholar 

  • Davies NB, Bourke AFG, Brooke ML (1989) Cuckoos and parasitic ants: interspecific brood parasitism as an evolutionary arms race. Trends Ecol Evol 4(9):274–278. https://doi.org/10.1016/0169-5347(89)90202-4

    Article  PubMed  CAS  Google Scholar 

  • Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc B Biol Sci 205(1161):489–511. https://doi.org/10.1098/rspb.1979.0081

    Article  CAS  Google Scholar 

  • Duckworth J (1991) Responses of breeding reed warblers Acrocephalus scirpaceus to mounts of sparrowhawk Accipiter nisus, cuckoo Cuculus canorus and jay Garrulus glandarius. Ibis 133(1):68–74

    Article  Google Scholar 

  • Ducrest AL, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23(9):502–510. https://doi.org/10.1016/j.tree.2008.06.001

    Article  PubMed  Google Scholar 

  • Eccles DH (1992) FAO species identification sheets for fishery purposes. Field guide to the freshwater fishes of Tanzania. Food and Agriculture Organization of the United Nations, Rome:145 p

  • Feeney WE, Welbergen JA, Langmore NE (2014) Advances in the study of coevolution between avian brood parasites and their hosts. In: Futuyma DJ (ed) Annu Rev Ecol Evol Syst, Vol 45. Annual Review of Ecology Evolution and Systematics, vol 45. Annual Reviews, Palo Alto, p 227–246

  • Ferguson J (1983) Observations of a spawning of Synodontis multipunctatus among rift Lake cichlids Buntbarshe. Bulletin 98:13–16

    Google Scholar 

  • Finley L (1983) Synodontis multipunctatus, reproduction and maternal Mouthbrooding cichlids - a cuckoo relationship? Buntbarshe Bulletin 98:13–16

    Google Scholar 

  • Finley L (1984) Reproduction in Synodontis multipunctatus Freshw Mar Aquar vol 7, p 22–25, 63, 66–75,

  • Fossøy F et al (2011) Genetic differentiation among sympatric cuckoo host races: males matter. Proc R Soc B Biol Sci 278(1712):1639–1645

    Article  Google Scholar 

  • Friedmann H (1929) The cowbirds: a study in the biology of social parasitism (Charles C. Thomas, Springfield, Ill.). 1963. Host relations of the parasitic cowbirds. US Nat Mus Bull(223)

  • Friel JP, Vigliotta TR (2006) Synodontis acanthoperca, a new species from the Ogooue River system, Gabon with comments on spiny ornamentation and sexual dimorphism in mochokid catfishes (Siluriformes : Mochokidae). Zootaxa(1125):45–56

  • Fryer G, Iles TD (1972) The cichlid fishes of the Great Lakes of Africa: their biology and evolution. Oliver and Boyd, Edinburgh

    Google Scholar 

  • Günther A (1894) Descriptions of the reptiles and fishes collected by Mr. E Coode-Hore on Lake Tanganyika. Proc Zool Soc London 1893(pt4):628–632

    Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50(3):346–363

    Article  PubMed  Google Scholar 

  • Kaufman L (1996) Haplochromis latifasciatus. The IUCN Red List of Threatened Species 1996: e.T2195A9341435 In. http://www.iucnredlist.org/details/2195/0 Accessed October 2017

  • Keenleyside MHA (1991) Parental Care. In: Keenleyside MHA (ed) Cichlid fishes: behavior, ecology, and evolution. Chapman and Hall, London, pp 191–208

    Google Scholar 

  • Kilner RM, Langmore NE (2011) Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol Rev 86(4):836–852

    Article  PubMed  Google Scholar 

  • Koblmuller S, Sturmbauer C, Verheyen E, Meyer A, Salzburger W (2006) Mitochondrial phylogeny and phylogeography of east African squeaker catfishes (Siluriformes: Synodontis). BMC Evol Biol 6(1):49

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nat Rev Genet 5:288–298

    Article  PubMed  CAS  Google Scholar 

  • Konings A (1995) Description of Pseudotropheus estherae sp. nov., the well-known red zebra cichlid from Lake Malawi. Tropical fish hobbyist (may 1995). p 206–210,

  • Lande R, Seehausen O, van Alphen JJM (2001) Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in cichlid fish. Genetica 112-113(1):435–443

  • Lashley KS (1930) The mechanism of vision: III. The comparative visual acuity of pigmented and albino rats. Pedagogical Seminary and Journal of Genetic Psychology 37(4):481–484

    Article  Google Scholar 

  • Loiselle PV (1998) Egg holders: how Synodontis catfish can use cichlids from two continents to hatch their young. Aquarium Fish Magazine 10:5–6

    Google Scholar 

  • Molina-Morales M, Martinez JG, Martin-Galvez D, Dawson DA, Burke T, Aviles JM (2014) Cuckoo hosts shift from accepting to rejecting parasitic eggs across their lifetime. Evolution 68(10):3020–3029. https://doi.org/10.1111/evo.12471

    Article  PubMed  Google Scholar 

  • Ochi H (1993) Mate monopolization by a dominant male in a multi-male social group of a mouthbrooding cichlid, Ctenochromis horei. Japanese Journal of Ichthyology 40(2):209–218

    Google Scholar 

  • Ortega CP (1998) Cowbirds and other brood parasites. University of Arizona Press

  • Payne RB (1977) The ecology of brood parasitism in birds. Annual Review of Ecology and Systematics 8:1–28

    Article  Google Scholar 

  • Peer BD, Rothstein SI (2010) Phenotypic Plasticity in Common Grackles (Quiscalus quiscula) in Response to Repeated Brood Parasitism. The Auk 127(2):293–299. https://doi.org/10.1525/auk.2009.09063

    Article  Google Scholar 

  • Poll M (1971) Revision des Synodontis africains (famille Mochocidae). Musée royal de l’Afrique centrale.

  • Questar-Inc. (2000) “National Geographic’s Lake Tanganyika - Jewel of the Rift” (VHS), Alexander Grasshoff and Al Giddings (Producers).

  • R Core Team (2018) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org

  • Regan CT (1929) New cichlid fishes from lakes Victoria, Kioga, and Albert. Annals and Magazine of Natural History. vol (Series 10) vol. 3 (no.16), p 388–392,

  • Ren JQ, McCarthy WR, Zhang H, Adolph AR, Li L (2002) Behavioral visual responses of wild-type and hypopigmented zebrafish. Vis Res 42(3):293–299

    Article  PubMed  Google Scholar 

  • Ribbink A (1990) Alternative life-history styles of some African cichlid fishes. Environ Biol Fishes 28(1–4):87–100. https://doi.org/10.1007/BF00751029

    Article  Google Scholar 

  • Robertson RJ, Norman RF (1976) Behavioral Defenses to Brood Parasitism by Potential Hosts of the Brown-Headed Cowbird. The Condor 78(2):166–173. https://doi.org/10.2307/1366851

    Article  Google Scholar 

  • Robertson RJ, Norman RF (1977) The function and evolution of aggressive host behavior towards the brown-headed cowbird (Molothrus ater). Can J Zool 55(3):508–518. https://doi.org/10.1139/z77-066

    Article  Google Scholar 

  • Rothstein SI (1975) An experimental and teleonomic investigation of avian brood parasitism. The Condor 77(3):250–271

    Article  Google Scholar 

  • Rothstein SI (1990) A Model System for Coevolution: Avian Brood Parasitism. Annual Review of Ecology and Systematics 21(ArticleType: research-article / Full publication date: 1990 / Copyright ¬© 1990 Annual Reviews):481–508.

  • Sato T (1986) A brood parasitic catfish of mouthbrooding cichlid fishes in Lake Tanganyika. Nature 323:58–59

    Article  PubMed  CAS  Google Scholar 

  • Slavík O, Horký P, Wackermannová M (2016) How does agonistic behaviour differ in albino and pigmented fish? PeerJ 4:e1937.

  • Snoeks J (2000) How well known is the ichthodiversity of the large East African lakes? In: Rossiter A, Kawanabe H (eds) Advances in Ecological Research - Ancient Lakes: Biodiversity, Ecology, and Evolution. vol 31. Academic Press, p 17–38.

  • Sturmbauer C et al (2008) Abundance, distribution, and territory areas of rock-dwelling Lake Tanganyika cichlid fish species. Hydrobiologia 615(1):57–68. https://doi.org/10.1007/s10750-008-9557-z

    Article  Google Scholar 

  • Sturmbauer C, Husemann M, Danley P (2011) Explosive Speciation and Adaptive Radiation of East African Cichlid Fishes. In: Zachos FE, Habel JC (eds) Biodiversity Hotspots. Springer, Berlin Heidelberg, pp 333–362

    Chapter  Google Scholar 

  • Thorogood R, Davies NB (2013) Reed warbler hosts fine-tune their defenses to track three decades of cuckoo decline. Evolution 67(12):3545–3555. https://doi.org/10.1111/evo.12213

    Article  PubMed  PubMed Central  Google Scholar 

  • Van Oijen M, Snoeks J, Skelton P, Maréchal C, Teugels G (1991) Haplochromis. In: Daget J, Gosse JP, Teugels GG, Audenaerde DFETvd (eds) Check-list of the freshwater fishes of Africa (CLOFFA). vol 4. ISNB, Brussels; MRAC, Tervuren; and ORSTOM, Paris, p 100–184.

  • Wahlsten D (1972) Genetic experiments with animal learning: A critical review. Behav Biol 7(2):143–182. https://doi.org/10.1016/s0091-6773(72)80197-4

    Article  PubMed  CAS  Google Scholar 

  • Wilson HR, Mets MB, Nagy SE, Kressel AB (1988) Albino spatial vision as an instance of arrested visual development. Vis Res 28(9):979–990

    Article  PubMed  CAS  Google Scholar 

  • Wisenden BD (1999) Alloparental care in fishes. Rev Fish Biol Fish 9:45–70

    Article  Google Scholar 

  • Wright JJ, Page LM (2006) Taxonomic revision of Lake Tanganyikan Synodontis (Siluriformes: Mochokidae). Florida Museum of Natural History Bulletin 46:99–154

    Google Scholar 

  • Yom-Tov Y, Geffen E (2006) On the origin of brood parasitism in altricial birds. Behav Ecol 17(2):196–205. https://doi.org/10.1093/beheco/arj013

    Article  Google Scholar 

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Acknowledgements

We are grateful to our many research assistants for all of their hard work and to everyone dedicated to helping maintain the fish populations over the years. We would also like to recognize the significant contributions made by Cliff Bueno de Mesquita in performing our statistical analyses and helping revise our manuscript. Lastly we would like to thank the University of Colorado for the numerous funding opportunities available to support undergraduate research.

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  1. Alexander Cruz is deceased. This paper is dedicated to his memory.

    • Alexander Cruz
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Correspondence to Marcus S. Cohen.

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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

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Cohen, M.S., Hawkins, M.B., Knox-Hayes, J. et al. A laboratory study of host use by the cuckoo catfish Synodontis multipunctatus. Environ Biol Fish 101, 1417–1425 (2018). https://doi.org/10.1007/s10641-018-0788-1

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