Brood parasites have demanding needs of host resources. Brood parasitic offspring are highly competitive and frequently cause the failure of host broods and the survival of a single parasitic offspring. Accordingly, virulent brood parasites lay a single egg in the same host nest to avoid sibling competition. In the cuckoo catfish (Synodontis multipunctatus), which parasitize mouthbrooding cichlid fishes in Lake Tanganyika, the modes of host and parasite oviposition lead to frequent cases of multiple parasitism. We experimentally tested the prediction that multiple parasitism leads to frequent cannibalism among offspring. Cuckoo catfish embryos prey upon host offspring to obtain nourishment during their 3-week development in the host buccal cavity and may also consume conspecific embryos. The potential benefits of cannibalism in the system are, therefore, twofold; to decrease competition for limited resources (i.e., host brood with rich yolk sacs) and to directly obtain nourishment by consuming rivals. We found that cannibalism indeed provided measurable benefits in terms of increased growth of the cannibals, but cannibalism was rare and typically occurred once all host offspring had been consumed. This implies that cannibalism among cuckoo catfish embryos emerges to mitigate starvation rather than eliminate competition.

Department of Botany and Zoology Faculty of Science Masaryk University Kotlářská 2 611 37 Brno Czech Republic

Department of Ecology and Vertebrate Zoology University of Łódź 12 16 Banacha street 90 237 Łódź Poland

Helsinki Institute of Life Sciences University of Helsinki Yliopistonkatu 3 00014 Helsinki Finland

Institute of Vertebrate Biology Czech Academy of Sciences Květná 8 603 00 Brno Czech Republic

Zobrazit více v PubMed

Ahi EP, Singh P, Lecaudey LA, Gessl W, Sturmbauer C.. 2018. Maternal mRNA input of growth and stress-response-related genes in cichlids in relation to egg size and trophic specialization. Evodevo. 9(1):1–17. PubMed PMC

Antonson ND, Schelsky WM, Tolman D, Kilner RM, Hauber ME.. 2022. Niche construction through a Goldilocks principle maximizes fitness for a nest-sharing brood parasite. Proc R Soc B. 289(1982):20221223. doi:10.1098/RSPB.2022.1223. PubMed DOI PMC

Baba R. 1994. Timing of spawning and host-nest choice for brood parasitism by the Japanese Minnow, Pungtungia herzi, on the Japanese Aucha Perch, Siniperca kawamebari. Ethology. 98(1):50–59.

Balshine S, Sloman KA.. 2011. Parental care in fishes. In: Farrell AP, editor. Encyclopedia of Fish Physiology: From Genome to Environment. San Diego: Academic Press, pp. 670–677.

Bates D, Mächler M, Bolker B, Walker S.. 2015. Fitting linear mixed-effects models using lme4. J Stat Softw. 67(1):1–48.

Blažek R, Polačik M, Reichard M.. 2022. Group intrusions by a brood parasitic fish are not cooperative. Behav Ecol. 33(1):178–183.

Blažek R, Polačik M, Smith C, Honza M, Meyer A, Reichard M.. 2018. Success of cuckoo catfish brood parasitism reflects coevolutionary history and individual experience of their cichlid hosts. Sci Adv. 4(5):eaar4380. doi:10.1126/sciadv.aar4380 PubMed DOI PMC

Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Maechler M, Bolker BM.. 2017. {glmmTMB} Balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9(2):378–400.

Cohen MS, Hawkins MB, Stock DW, Cruz A.. 2019. Early life-history features associated with brood parasitism in the cuckoo catfish, Synodontis multipunctatus (Siluriformes: Mochokidae). Philos Trans R Soc B Biol Sci. 374(1769):20180205. doi:10.1098/rstb.2018.0205 PubMed DOI PMC

Davies N. 2015. Cuckoo: cheating by nature. London: Bloomsbury Publishing.

Gilmore RGJ, Putz O, Dodrill JW.. 2005. Oophagy, intrauterine cannibalism and reproductive strategy in lamnoid sharks. In: Hamlett WC, editor. Reproductive biology and phylogeny of chondrichthyes. Vol. 3. 1st ed. Boca Raton: CRC Press. p. 445–472.

Gloag R, Beekman M.. 2019. The brood parasite’s guide to inclusive fitness theory. Philos Trans R Soc B Biol Sci. 374(1769):20180198. doi:10.1098/rstb.2018.0198 PubMed DOI PMC

Gloag R, Fiorini VD, Reboreda JC, Kacelnik A.. 2012. Brood parasite eggs enhance egg survivorship in a multiply parasitized host. Proc R Soc B Biol Sci. 279(1734):1831–1839. PubMed PMC

Gloag R, Tuero DT, Fiorini VD, Reboreda JC, Kacelnik A.. 2012. The economics of nestmate killing in avian brood parasites: a provisions trade-off. Behav Ecol. 23(1):132–140.

Goguen CB, Curson DR, Mathews NE.. 2011. Costs of multiple parasitism for an avian brood parasite, the Brown-headed Cowbird (Molothrus ater). Can J Zool. 89(12):1237–1248.

Hartig F. 2021. DHARMa: residual diagnostics for hierarchical (multi-level/ mixed) regression models. https://cran.r-project.org/web/packages/DHARMa/vignettes/DHARMa.html. Accessed on 3 January 2022.

Honza M, Koleček J, Piálek L, Piálková R, Požgayová M, Procházka P, Štětková G, Jelínek V, Hughes AE, Šulc M.. 2022. Multiple parasitism in an evictor brood parasite: patterns revealed by long-term monitoring, continuous video recording, and genetic analyses. Behav Ecol Sociobiol. 76(12):161. doi:10.1007/S00265-022-03270-X DOI

Honza M, Vošlajerová K, Moskát C.. 2007. Eviction behaviour of the common cuckoo Cuculus canorus chicks. J Avian Biol. 38(3):385–389.

Kilner RM. 2005. The evolution of virulence in brood parasites. Ornithol Sci. 4(1):55–64.

Kilner RM, Madden JR, Hauber ME.. 2004. Broad parasitic cowbird nestlings use host young to procure resources. Science. 305(5685):877–879. PubMed

Koller M. 2016. robustlmm: an R package for robust estimation of linear mixed-effects models. J Stat Softw. 75(1):1–24. PubMed PMC

Liu X, Xia J, Pang H, Yue G.. 2017. Who eats whom, when and why? Juvenile cannibalism in fish Asian seabass. Aquac Fish. 2(1):1–9.

Martínez JG, Soler JJ, Soler M, Burke T.. 1998. Spatial patterns of egg laying and multiple parasitism in a brood parasite: a non-territorial system in the great spotted cuckoo (Clamator glandarius). Oecologia. 117(1–2):286–294. PubMed

Marton A. 2021. Quintuple parasitism of a great reed warbler nest by common cuckoos. Ecol Evol. 11(13):8420–8423. PubMed PMC

Miller E, Wails CN, Sulikowski J.. 2022. It’s a shark-eat-shark world, but does that make for bigger pups? A comparison between oophagous and non-oophagous viviparous sharks. Rev Fish Biol Fish. 32(4):1019–1033.

Mock DW, Parker GA.. 1998. Siblicide, conflict and the evolutionary limits of selfishness. Anim Behav. 56(1):1–10. PubMed

Morandini V, Ferrer M.. 2015. Sibling aggression and brood reduction: a review. Ethol Ecol Evol. 27(1):2–16.

Moskát C, Honza M.. 2002. European Cuckoo Cuculus canorus parasitism and host’s rejection behaviour in a heavily parasitized Great Reed Warbler Acrocephalus arundinaceus population. Ibis (Lond 1859). 144(4):614–622.

Neff BD. 2003. Decisions about parental care in response to perceived paternity. Nature. 422(April):716–719. PubMed

Olsén KH. 1992. Kin recognition in fish mediated by chemical cues. Fish Chemorecept. 1992:229–248.

Parker GA, Mock DW, Lamey TC.. 1989. How selfish should stronger sibs be? Am Nat. 133(6):846–868.

Penn DJ, Frommen JG.. 2010. Kin recognition: an overview of conceptual issues, mechanisms and evolutionary theory. In: Animal behaviour: evolution and mechanisms. Berlin, Heidelberg: Springer Berlin Heidelberg. p. 55–85.

Pereira LS, Agostinho AA, Winemiller KO.. 2017. Revisiting cannibalism in fishes. Rev Fish Biol Fish. 27(3):499–513.

Pfennig DW. 1997. Kinship and cannibalism. Bioscience. 47(10):667–675.

Polis GA. 1981. The evolution and dynamics of intraspecific predation. Annu Rev Ecol Syst. 12(1):225–251.

R Studio Team. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing. R Core Team. http://www.r-project.org/. Accessed on 3 November 2022.

Rivers JW, Young S, Gonzalez EG, Horton B, Lock J, Fleischer RC.. 2012. High levels of relatedness between Brown-Headed Cowbird (Molothrus ater) nestmates in a heavily parasitized host community. Auk. 129(4):623–631.

Roulin A, Dreiss AN.. 2012. Sibling competition and cooperation over parental care. In: Royle NJ, Smiseth PT, Kölliker M, editors. The evolution of parental care. Oxford: Oxford University Press Oxford. p. 133–149.

Sato T. 1986. A brood parasitic catfish Synodontis multipunctatus of mouthbreeding cichlid fishes in Lake Tanganyika. Nature. 323:58–59. PubMed

Smith C, Reay P.. 1991. Cannibalism in teleost fish. Rev Fish Biol Fish. 1(1):41–64.

Smith C, Wootton RJ.. 1995. The cost of parental care in teleost fishes. Rev Fish Biol Fish. 5:7–22.

Soler M. 2017. Avian brood parasitism: behaviour, ecology, evolution and coevolution. 1st ed. Soler M, editor. Cham: Springer.

Sousa-Ferreira I, Abreu AM.. 2019. A review of Cox’s model extensions for multiple events. iJRDO - J Appl Sci 5(2):47–62.

Spottiswoode CN. 2013. A brood parasite selects for its own egg traits. Biol Lett. 9(5):20130573. doi:10.1098/rsbl.2013.0573 PubMed DOI PMC

Spottiswoode CN, Koorevaar J.. 2012. A stab in the dark: chick killing by brood parasitic honeyguides. Biol Lett. 8(2):241–244. PubMed PMC

Takahashi T, Koblmüller S.. 2020. Brood parasitism of an open‐water spawning cichlid by the cuckoo catfish. J Fish Biol. 96(6):1538–1542. PubMed

Therneau TM, Grambsch PM.. 2000. Modeling survival data: extending the cox model. New York: Springer (Statistics for Biology and Health).

Tuero DT, Fiorini VD, Reboreda JC.. 2007. Effects of Shiny Cowbird Molothrus bonariensis parasitism on different components of House Wren Troglodytes aedon reproductive success. Ibis (Lond 1859). 149(3):521–529.

Yanagisawa Y, Sato T.. 1990. Active browsing by mouthbrooding females of Tropheus duboisi and Tropheus moorii (Cichlidae) to feed the young and/or themselves. Environ Biol Fishes. 27(1):43–50.

Zimmermann H, Blažek R, Polačik M, Reichard M.. 2022. Individual experience as a key to success for the cuckoo catfish brood parasitism. Nat Commun. 13(1):1723. doi:10.1038/s41467-022-29417-y PubMed DOI PMC

Zimmermann H, Tolman D, Reichard M.. 2023. Low incidence of sibling cannibalism among brood parasitic cuckoo catfish embryos. Behav Ecol. doi:10.5061/dryad.6wwpzgn3g PubMed DOI PMC

Mixed Parentage Broods Indicate Group Spawning in the Brood Parasitic Cuckoo Catfish

Low incidence of cannibalism among brood parasitic cuckoo catfish embryos