Adult animals of many species often behave in a cannibalistic manner when encountering conspecific offspring. Kin discrimination is critical for avoiding the consumption of one’s own offspring or filial cannibalism. Some fishes cannibalize embryos when other nutritional sources are unavailable. We tested the hypotheses that (1) adult mangrove rivulus, Kryptolebias marmoratus, cannibalize conspecific offspring; (2) cannibalism of unrelated conspecifics is more prevalent than filial cannibalism and (3) the drive to cannibalize embryos is associated with nutritional status (‘energy-based hypothesis’). We examined cannibalistic behaviours of the self-fertilizing amphibious K. marmoratus in the laboratory using two isogenic strains. Adults recognized kinship of single embryos, cannibalizing unrelated embryos (28% of the time) but not their own. The ability to recognize kin differed between isogenic strains. Thus, genetic differences significantly influenced behaviour. Fasting had no significant effect on cannibalistic behaviours and thus nutritional state is not an important factor driving cannibalism in this species under these conditions. This is the first documented evidence that a fish species can recognize the kinship of an individual embryo.
Across the animal world, there are many examples of animals that eat their own offspring (filial cannibalism), but the outcome of such behaviour may be reproductively costly. Other animals may consume offspring belonging to other parents (non-kin cannibalism). The trick is to recognize the difference between your own versus someone else’s offspring to optimize reproductive success. Previous studies on fish have shown that parents can assess the relative ratio of kin to non-kin embryos in an entire nest, but the ability to recognize single embryos has not been demonstrated. We have shown that when a self-fertilizing mangrove fish was presented with a single embryo, it never ate its own but consumed unrelated embryos, suggesting that they have the ability to recognize solo relatives at very early stages of development.
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Abel DC, Koenig CC, Davis WP (1987) Emersion in the mangrove forest fish Rivulus marmoratus: a unique response to hydrogen sulfide. Environ Biol Fish 18:67–72
Bose APH, McClelland GB, Balshine S (2016) Cannibalism, competition, and costly care in the plainfin midshipman fish, Porichthys notatus. Behav Ecol 27:628–636
Brown GE, Brown JA (1996) Kin discrimination in salmonids. Rev Fish Biol Fisher 6:201–219
Courtenay SC, Quinn TP, Dupuis HMC, Groot C, Larkin PA (2001) Discrimination of family-specific odours by juvenile coho salmon: roles of learning and odour concentration. J Fish Biol 58:107–125
Culot L, Lledo-Ferrer Y, Hoelscher O, Munoz Lazo FJJ, Huynen MC, Heymann EW (2011) Reproductive failure, possible maternal infanticide, and cannibalism in wild moustached tamarins, Saguinus mystax. Primates 52:179–186
Edenbrow M, Croft DP (2012) Kin and familiarity influence association preferences and aggression in the mangrove killifish Kryptolebias marmoratus. J Fish Biol 44:503–518
Ellison A, Jones J, Inchley C, Consuegra S (2013) Choosy males could help explain androdioecy in a selfing fish. Am Nat 181:855–862
Elwood RW (1994) Temporal-based kinship recognition: a switch in time saves mine. Behav Process 33:15–24
Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967–971
Feuth-de Bruijn E, Sevenster P (1983) Parental reactions to young in sticklebacks (Gasterosteus aculeatus L.) Behaviour 83:186–203
Frick NT, Wright PA (2002) Nitrogen metabolism and excretion in the mangrove killifish Rivulus marmoratus. I The influence of environmental salinity and external ammonia J Exp Biol 205:79–89
Gomagano D, Kohda M (2008) Partial filial cannibalism enhances initial body condition and size in paternal care fish with strong male-male competition. Ann Zool Fenn 45:55–65
Grageda MVC, Sakakura Y, Minamimoto M, Hagiwara A (2005) Differences in life-history traits in two clonal strains of the self-fertilizing fish, Rivulus marmoratus. Environ Biol Fish 73:427–436
Harrington RW Jr (1961) Oviparous hermaphroditic fish with internal self-fertilization. Science 134:1749–1750
Harrington RW Jr (1963) Twenty-four-hour rhythms of internal self-fertilization and of oviposition by hermaphrodites of Rivulus marmoratus. Physiol Zool 36:325–341
Hoelzer G (1988) Filial cannibalism in a non-brood cycling marine fish. Environ Biol Fish 21:309–313
Hoelzer GA (1992) The ecology and evolution of partial-clutch cannibalism by paternal Cortez damselfish. Oikos 65:113–120
Hrdy SB (1979) Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol Sociobiol 1:13–40
Huber JH (1992) Review of Rivulus: ecobiogeography, relationships. Société Française D'ichtyologie, Paris
Johns LS, Liley NR (1970) The effects of gonadectomy and testosterone treatment on the reproductive behavior of the male blue gourami Trichogaster trichopterus. Can J Zool 48:977–987
Klug H, Bonsall MB (2007) When to care for, abandon, or eat your offspring: the evolution of parental care and filial cannibalism. Am Nat 170:886–901
Klug H, St. Mary CM (2005) Reproductive fitness consequences of filial cannibalism in the flagfish, Jordanella floridae. Anim Behav 70:685–691
Kraak SBM (1996) Female preference and filial cannibalism in Aidablennius sphinx (Teleostei, Blennidae); a combined field and laboratory study. Behav Process 36:85–98
Kristensen I (1970) Competition in three cyprinodont fish species in the Netherlands Antilles. Stud Fauna Curaçao Caribbean Isl 32:82–101
Kvarnemo C, Svensson O, Forsgren E (1998) Parental behaviour in relation to food availability in the common goby. Anim Behav 56:1285–1290
Li S, Mathias JA (1982) Causes of high mortality among cultured larval walleyes. T Am Fish Soc 11:710–721
Li SK, Owings DH (1978) Sexual selection in the three-spined stickleback: II. Nest raiding during the courtship phase Behaviour 64:298–304
Mackiewicz M, Tatorenkov A, Taylor DS, Turner BJ, Avise J (2006) Extensive outcrossing and androdioecy in a vertebrate species that otherwise reproduces as a self-fertilizing hermaphrodite. P Natl Acad Sci USA 103:9924–9928
Manica A (2002) Filial cannibalism in teleost fish. Biol Rev 77:261–277
Manica A (2004) Parental fish change their cannibalistic behaviour in response to the cost-to-benefit ratio of parental care. Anim Behav 67:1015–1021
Mehlis M, Bakker TCM, Engqvist L, Frommen JG (2010) To eat or not to eat: egg-based assessment of paternity triggers fine-tuned decisions about filial cannibalism. Proc R Soc Lond B 277:2627–2635
Mehlis M, Bakker TCM, Frommen JG (2009) Nutritional benefits of filial cannibalism in three-spined sticklebacks (Gasterosteus aculeatus). Naturwissenschaften 96:399–403
Mociño-Deloya E, Setser K, Pleguezuelos JM, Kardon A, Lazcano D (2009) Cannibalism of nonviable offspring by postparturient Mexican lance-headed rattlesnakes, Crotalus polystictus. Anim Behav 77:145–150
Mourabit S, Edenbrow M, Croft DP, Kudoh T (2011) Embryonic development of the self-fertilizing mangrove killifish Kryptolebias marmoratus. Dev Dynam 240:1694–1704
Myrberg AA (1975) The role of chemical and visual stimuli in the preferential discrimination of young by the cichlid fish Cichlasoma nigrofasciatum (Günther). Z Tierpsychol 37:274–297
Neff BD (2003) Paternity and condition affect cannibalistic behaviour in nest-tending bluegill sunfish. Behav Ecol Sociobiol 54:377–384
Neff BD, Gross MR (2001) Dynamic adjustment of parental care in response to perceived paternity. Proc R Soc Lond B 268:1559–1565
Neff BD, Sherman PW (2003) Nestling recognition via direct cues by parental male bluegill sunfish (Lepomis macrochirus). Anim Cogn 6:87–92
Nelson CT, Elwood RW (1997) Parental state and offspring recognition in the biparental cichlid fish Pelvicachromis pulcher. Anim Behav 54:803–809
Pereira LS, Agostinho AA, Winemiller KO (2017) Revisiting cannibalism in fishes. Rev Fish Biol Fisher 27:1–15
Pfennig DW, Reeve H, Sherman PW (1993) Kin recognition and cannibalism in spadefoot toad tadpoles. Anim Behav 46:87–94
Reeve HK (1989) The evolution of conspecific acceptance thresholds. Am Nat 133:407–435
Rohwer S (1978) Parent cannibalism of offspring and egg raiding as a courtship strategy. Am Nat 112:429–440
Sakakura Y, Noakes DLG (2000) Age, growth, and sexual development in the self-fertilizing hermaphroditic fish Rivulus marmoratus. Environ Biol Fish 59:309–317
Smith C, Reay P (1991) Cannibalism in teleost fish. Rev Fish Biol Fisher 1:41–64
Tatarenkov A, Ring BC, Elder JF, Bechler DL, Avise JC (2010) Genetic composition of laboratory stocks of the self-fertilizing fish Kryptolebias marmoratus: a valuable resource for experimental research. PLoS One 5:e12863
Taylor DS (1988) Observations of the ecology of the killifish Rivulus marmoratus (Cyprinodontidae) in an infrequently flooded mangrove swamp. NE Gulf Sci 10:63–68
Taylor DS (2012) Twenty-four years in the mud: what have we learned about the natural history and ecology of the mangrove rivulus, Kryptolebias marmoratus? Integr Comp Biol 52:724–736
Taylor DS, Turner BJ, Davis WP, Chapman BB (2008) A novel terrestrial fish habitat inside emergent logs. Am Nat 171:263–266
Turko AJ, Earley RL, Wright PA (2011) Behaviour drives morphology: voluntary emersion patterns shape gill structure in genetically identical mangrove rivulus. Anim Behav 82:39–47
Turner BJ, William PD, Taylor DS (1992) Abundant males in populations of a selfing hermaphrodite fish, Rivulus marmoratus, from some Belize cays. J Fish Biol 40:307–310
Ward AJ, Hart PJ (2003) The effects of kin and familiarity on interactions between fish. Fish Fish 4:348–358
Wells MW, Turko AK, Wright PA (2015) Fish embryos on land: terrestrial embryo deposition lowers oxygen uptake without altering growth or survival in the amphibious fish Kryptolebias marmoratus. J Exp Biol 218:3249–3256
Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle River, NJ
The authors wish to thank anonymous reviewers for excellent suggestions. Thanks also to Drs. F. Laberge and A. Heyland for the advice on experimental design; D. Eisner for the help with data collection; Drs. A. Gibb, B. Robinson, D.S. Taylor and R. Earley for the discussions and a special thanks to Drs. A. McAdam and B. Allen for sound statistical advice. A. Turko provided very useful advice on several aspects of this project. Thanks to K. Levesque and H. Ferguson for providing the typographical help. Thank you to B. Frank, M. Cornish, M. Davies and several volunteers for their help with fish maintenance. Funding was by NSERC Discovery grants program to PAW and an OGS grant to MWW.
Our experiments were conducted in Canada and comply with the current laws of the country in which they were performed. All experiments were carried out under the Animal Utilization Protocol 10R068 at the University of Guelph.
Conflict of interest
The authors declare that they have no conflict of interest.
The datasets analysed during the current study are available from the corresponding author on reasonable request.
Communicated by J. Frommen
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Wells, M.W., Wright, P.A. Do not eat your kids: embryonic kin recognition in an amphibious fish. Behav Ecol Sociobiol 71, 140 (2017). https://doi.org/10.1007/s00265-017-2360-y
- Filial cannibalism
- Energy-based hypothesis
- Mangrove rivulus
- Kryptolebias marmoratus