Skip to main content
SpringerLink
Log in

Temporal and sex-specific patterns of breeding territory defense in a color-polymorphic cichlid fish

  • ADVANCES IN CICHLID RESEARCH II
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

In biparental species, the costs and benefits of parental investment can vary between the sexes and shift over time. However, such sex-specific and temporal changes in territory defense are not well understood. Here, we experimentally investigated parental investment in breeding territory defense in a feral population of the color-polymorphic, biparental cichlid fish, the red devil (Amphilophus labiatus). We presented either gold- or dark-colored conspecific intruder models (i.e., dummy models) to A. labiatus pairs at three key stages during the breeding cycle (i.e., after pair formation, after eggs have been laid, and when fry were free-swimming). We found that males were more aggressive when the pair first formed, whereas females significantly increased their territory defense with time, and were most aggressive when fry were free-swimming. These results show that parental roles in territory defense can markedly shift over key stages of the breeding cycle. Our results demonstrate that parental behaviors may not only vary between the sexes, but can also shift dramatically over the course of the brood cycle.

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

Similar content being viewed by others

References

  • Amat, J. A., G. H. Visser, A. Pérez-Hurtado & G. M. Arroyo, 2000. Brood desertion by female shorebirds: a test of the differential parental capacity hypothesis on Kentish plovers. Proceedings of the Royal Society London B 267: 2171–2176.

    Article  CAS  Google Scholar 

  • Barlow, G. W., 1976. The Midas Cichlid In Nicaragua. In Thorson, T. B. (ed.), Investigation of the Ichthyofauna of Nicaraguan Lakes. University of Nebraska-Lincoln, Lincoln.

    Google Scholar 

  • Barlow, G. W., 1983. Do gold midas cichlid fish win fights because of their colour, or because they lack normal coloration? A logistic solution. Behavioral Ecology and Sociobiology 13: 197–204.

    Article  Google Scholar 

  • Barlow, G. W., 2000. The cichlid fishes: nature’s grand experiment in evolution. Perse us Publishing, Cambridge.

    Google Scholar 

  • Barlow, G. W. & P. Siri, 1994. Polychromatic midas cichlids respond to dummy opponents: color, contrast and context. Behaviour 130: 77–112.

    Article  Google Scholar 

  • Baylis, J. R., 1981. The evolution of parental care in fishes, with reference to Darwin’s rule of male sexual selection. Environmental Biology of Fishes 6: 223–251.

    Article  Google Scholar 

  • Blumer, L. S., 1979. Male parental care in the bony fishes. The Quarterly Review of Biology 54: 149–161.

    Article  Google Scholar 

  • Budaev, S. V., D. D. Zworykin & A. D. Mochek, 1999. Individual differences in parental care and behaviour profile in the convict cichlid: a correlation study. Animal Behaviour 58: 195–202.

    Article  CAS  PubMed  Google Scholar 

  • Carere, C. & E. Alleva, 1998. Sex differences in parental care in the common swift (Apus apus): effect of brood size and nestling age. Canadian Journal of Zoology 76: 1382–1387.

    Article  Google Scholar 

  • Chapman, T., G. Arnqvist, J. Bangham & L. Rowe, 2003. Sexual conflict. Trends in Ecology and Evolution 18: 41–47.

    Article  Google Scholar 

  • Chuang-Dobbs, H. C., M. S. Webster & R. T. Holmes, 2001. The effectiveness of mate guarding by male black-throated blue warblers. Behavioral Ecology 12: 541–546.

    Article  Google Scholar 

  • Clutton-Brock, T. H., 1991. The Evolution of Parental Care. Princeton University Press, Princeton.

    Google Scholar 

  • Colombo, M., E. T. Diepeveen, M. Muschick, M. E. Santos, A. Indermaur, N. Boileau, M. Barluenga & W. Salzburger, 2013. The ecological and genetic basis of convergent thick-lipped phenotypes in cichlid fishes. Molecular Ecology 22: 670–684.

    Article  CAS  PubMed  Google Scholar 

  • Elmer, K. R., T. K. Lehtonen & A. Meyer, 2009. Color assortative mating contributes to sympatric divergence of neotropical cichlid fish. Evolution 63: 2750–2757.

    Article  PubMed  Google Scholar 

  • Elmer, K. R., H. Kusche, T. K. Lehtonen & A. Meyer, 2010. Local variation and parallel evolution: morphological and genetic diversity across a species complex of neotropical crater lake cichlid fishes. Proceedings of the Royal Society London B 365: 1763–1782.

    Article  Google Scholar 

  • Ercit, K., A. Martinez-Novoa & D. T. Gwynne, 2014. Egg load decreases mobility and increases predation risk in female black-horned tree crickets (Oecanthus nigricornis). PLoS One 9: e110298.

    Article  PubMed  PubMed Central  Google Scholar 

  • Goodwin, N. B., S. Balshine-Earn & J. D. Reynolds, 1998. Evolutionary transitions in parental care in cichlid fish. Proceedings of the Royal Society London B 265: 2265–2272.

    Article  Google Scholar 

  • Gross, M. R. & R. C. Sargent, 1985. The evolution of male and female parental care in fishes. American Zoologist 25: 807–822.

    Article  Google Scholar 

  • Haller, J., 1996. Biochemical background for an analysis of cost-benefit interrelations in aggression. Neuroscience & Biobehavioral Reviews 19: 599–604.

    Article  Google Scholar 

  • Hammerstein, P. & G. A. Parker, 1987. Sexual selection: games between the sexes. In Bradbury, J. W. & M. B. Andersson (eds), Sexual selection: testing the alternatives. Wiley, Chichester: 119–142.

    Google Scholar 

  • Harrison, F., Z. Barta, I. Cuthill & T. Székely, 2009. How is sexual conflict over parental care resolved? A meta-analysis. Journal of Evolutionary Biology 22: 1800–1812.

    Article  CAS  PubMed  Google Scholar 

  • Holder, J. L., G. W. Barlow & R. C. Francis, 1991. Differences in aggressiveness in the Midas cichlid (Cichlasoma citrinellum) in relation to sex, reproductive state and the individual. Ethology 88: 297–306.

    Article  Google Scholar 

  • Houston, A. I., T. Székely & J. M. McNamara, 2005. Conflict between parents over care. Trends in Ecology and Evolution 20: 33–38.

    Article  PubMed  Google Scholar 

  • Itzkowitz, M., 1984. Parental division of labor in a monogamous fish. Behaviour 89: 251–260.

    Article  Google Scholar 

  • Itzkowitz, M., 1985. Sexual differences in offspring defense in a monogamous cichlid fish. Zeitschrift für Tierpsychologie 70: 247–255.

    Article  Google Scholar 

  • Itzkowitz, M., N. Santangelo & M. Richter, 2001. Parental division of labour and the shift from minimal to maximal role specializations: an examination using a biparental fish. Animal Behaviour 61: 1237–1245.

    Article  Google Scholar 

  • Itzkowitz, M., N. Santangelo, A. Cleveland, A. Bockelman & M. Richter, 2005. Is the selection of sex-typical parental roles based on an assessment process? A test in the monogamous convict cichlid fish. Animal Behaviour 69: 95–105.

    Article  Google Scholar 

  • Jaroensutasinee, M. & K. Jaroensutasinee, 2003. Type of intruder and reproductive phase influence male territorial defence in wild-caught Siamese fighting fish. Behavioural Processes 64: 23–29.

    Article  PubMed  Google Scholar 

  • Jennions, M. D. & D. A. Polakow, 2001. The effect of partial brood loss on male desertion in a cichlid fish: an experimental test. Behavioral Ecology 12: 84–92.

    Article  Google Scholar 

  • Jennions, M. D. & S. Telford, 2002. Life-history phenotypes in populations of Brachyrhaphis episcopi (Poeciliidae) with different predator communities. Oecologia 132: 44–50.

    Article  Google Scholar 

  • Keenleyside, M. H., 1983. Mate desertion in relation to adult sex ratio in the biparental cichlid fish (Herotilapia multispinosa). Animal Behaviour 31: 683–688.

    Article  Google Scholar 

  • Keenleyside, M. H. (ed.), 1991. Cichlid Fishes: Behaviour, Ecology and Evolution, 2nd ed. Springer, Netherlands.

    Google Scholar 

  • Keenleyside, M. H., R. C. Bailey & V. H. Young, 1990. Variations in the mating system and associated parental behaviour of captive and free-living Cichlasoma nigrofasciatum (Pisces, Cichlidae). Behaviour 112: 202–221.

    Article  Google Scholar 

  • Komdeur, J., F. Kraaijeveld-Smit, K. Kraaijeveld & P. Edelaar, 1999. Explicit experimental evidence for the role of mate guarding in minimizing loss of paternity in the Seychelles warbler. Proceedings of the Royal Society London B 266: 2075.

    Article  Google Scholar 

  • Lappin, A. K. & J. F. Husak, 2005. Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris). The American Naturalist 166: 426–436.

    Article  PubMed  Google Scholar 

  • Lehtonen, T. K., 2014. Colour biases in territorial aggression in a Neotropical cichlid fish. Oecologia 175: 85–93.

    Article  PubMed  Google Scholar 

  • Lehtonen, T. K., B. B. M. Wong, K. Lindström & A. Meyer, 2011. Species divergence and seasonal succession in rates of mate desertion in closely related Neotropical cichlid fishes. Behavioral Ecology and Sociobiology 65: 607–612.

    Article  Google Scholar 

  • Lehtonen, T. K., J. K. McCrary & A. Meyer, 2012. Introduced predator elicits deficient brood defence behaviour in a crater lake fish. PLoS One 7: e30064.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehtonen, T. K., W. Sowersby, K. Gagnon & B. B. M. Wong, 2015a. Cichlid fish use color as a cue to assess the threat status of heterospecific intruders. The American Naturalist 186: 547–552.

    Article  PubMed  Google Scholar 

  • Lehtonen, T. K., W. Sowersby & B. B. M. Wong, 2015b. Heterospecific aggression bias towards a rarer colour morph. Proceedings of the Royal Society London B 282: 20151551.

    Article  Google Scholar 

  • Lessells, K. 1999. Sexual conflict. Wiley Online Library, eLS.

  • Marler, C. & M. Moore, 1988. Evolutionary costs of aggression revealed by testosterone manipulations in free-living male lizards. Behavioral Ecology and Sociobiology 23: 21–26.

    Article  Google Scholar 

  • Meek, S. E. 1907. Synopsis of the fishes of the great lakes of Nicaragua. Field Columbian Museum, 121, Zoological Series 7: 97–132

  • McKaye, K. R., 1977. Competition for breeding sites between the cichlid fishes of Lake Jiloa, Nicaragua. Ecology 58: 291–302.

    Article  Google Scholar 

  • McKaye, K. R., 1986. Mate choice and size assortative pairing by the cichlid fishes of Lake Jiloá, Nicaragua. Journal of Fish Biology 29: s135–s150.

    Article  Google Scholar 

  • McKaye, K. R. & G. W. Barlow, 1976. Competition between color morphs of the Midas cichlid, Cichlasoma citrinellum, in Lake Jiloa, Nicaragua. In Thorson, T. B. (ed.), Investigation of the Ichthyofauna of Nicaraguan Lakes. University of Nebraska-Lincoln, Lincoln.

    Google Scholar 

  • McKaye, K. R. & B. A. Murry, 2008. Sex role differentiation in brood defense by a Nicaraguan cichlid fish, Amphilophus xiloanensis. Caribbean Journal of Science 44: 13–20.

    Article  Google Scholar 

  • McNamara, J. M., A. I. Houston, T. Székely & J. N. Webb, 2002. Do parents make independent decisions about desertion? Animal Behaviour 64: 147–149.

    Article  Google Scholar 

  • Murry, B. A., E. P. Van Den Berghe & K. R. McKaye, 2001. Brood defense behavior of three sibling species in the Amphilophus citrinellus species complex in Lake Xiloá, Nicaragua. Journal of Aquariculture and Aquatic Science 9: 134–149.

    Google Scholar 

  • Newton, I., 1979. Population Ecology of Raptors. T and AD Poyser, Berkhamsted.

    Google Scholar 

  • NIWA, 2008. Review of the impacts of introduced ornamental fish species that have established wild populations in Australia. Department of the Environment, Water, Heritage and the Arts, Canberra

  • Oldfield, R., K. Mandrekar, M. X. Nieves, D. A. Hendrickson, P. Chakrabarty, B. O. Swanson & H. A. Hofmann, 2015. Parental care in the Cuatro Ciénegas cichlid, Herichthys minckleyi (Teleostei: Cichlidae). Hydrobiologia 48: 233–257.

    Article  Google Scholar 

  • Perrone Jr., M. & T. M. Zaret, 1979. Parental care patterns of fishes. The American Naturalist 113: 351–361.

    Article  Google Scholar 

  • Pinheiro, J. C. & D. M. Bates, 2000. Mixed-Effects Models in S and S-PLUS, Statistics and Computing Series. Springer, New York.

    Book  Google Scholar 

  • Pryke, S. R., 2007. Fiery red heads: female dominance among head color morphs in the Gouldian finch. Behavioral Ecology 18: 621–627.

    Article  Google Scholar 

  • Redondo, T. & J. Carranza, 1989. Offspring reproductive value and nest defense in the magpie (Pica pica). Behavioral Ecology and Sociobiology 25: 369–378.

    Article  Google Scholar 

  • Requena, G. S., B. A. Buzatto, E. G. Martins & G. Machado, 2012. Paternal care decreases foraging activity and body condition, but does not impose survival costs to caring males in a Neotropical arachnid. PLoS One 7: e46701.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds, J. D., 1996. Animal breeding systems. Trends in Ecology and Evolution 11: 68–72.

    Article  CAS  PubMed  Google Scholar 

  • Ridley, M., 1978. Paternal care. Animal Behaviour 26: 904–932.

    Article  Google Scholar 

  • Rogers, W., 1987. Sex ratio, monogamy and breeding success in the Midas cichlid (Cichlasoma citrinellum). Behavioral Ecology Sociobiology 21: 47–51.

    Article  Google Scholar 

  • Rogers, W., 1988. Parental investment and division of labor in the Midas cichlid (Cichlasoma citrinellum). Ethology 79: 126–142.

    Article  Google Scholar 

  • Rowland W. J., 1999. Studying visual cues in fish behavior: A review of ethological techniques. Environmental Biology of Fishes 56: 285–305.

    Article  Google Scholar 

  • Rytkönen, S., M. Orell, K. Koivula & M. Soppela, 1995. Correlation between two components of parental investment: nest defence intensity and nestling provisioning effort of willow tits. Oecologia 104: 386–393.

    Article  Google Scholar 

  • Saino, N., C. R. Primmer, H. Ellegren & A. P. Møller, 1999. Breeding synchrony and paternity in the barn swallow (Hirundo rustica). Behavioral Ecology and Sociobiology 45: 211–218.

    Article  Google Scholar 

  • Salfert, I. G. & G. E. E. Moodie, 1985. Filial egg-cannibalism in the brook stickleback, Culaea inconstans (Kirtland). Behaviour 93: 82–100.

    Article  Google Scholar 

  • Sinervo, B., D. B. Miles, W. A. Frankino, M. Klukowski & D. F. DeNardo, 2000. Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Hormones and Behavior 38: 222–233.

    Article  CAS  PubMed  Google Scholar 

  • Schipper, W. J. A., 1973. A Comparison of Prey Selection in Sympatric Harriers, Circus, in Western Europe. Institut Royal des Sciences naturelles de Belgique, Brussels.

    Google Scholar 

  • Székely, T. & I. C. Cuthill, 1999. Brood desertion in Kentish plover: the value of parental care. Behavioral Ecology 10: 191–197.

    Article  Google Scholar 

  • Székely, T. & I. C. Cuthill, 2000. Trade-off between mating opportunities and parental care: brood desertion by female Kentish plovers. Proceedings of the Royal Society London B 267: 2087–2092.

    Article  Google Scholar 

  • Townshend, T. J. & R. J. Wootton, 1985. Variation in the mating system of a biparental cichlid fish, Cichlasoma panamense. Behaviour 95: 181–197.

    Article  Google Scholar 

  • Trivers, R., 1972. Parental investment and sexual selection. In Campbell, B. (ed.), Sexual Selection and the Descent of Man 1871–1971. Aldine Publication, Chicago.

    Google Scholar 

  • Trnka, A. & T. Grim, 2012. To compensate or not to compensate: testing the negotiation model in the context of nest defense. Behavioral Ecology 24: 223–228.

    Article  Google Scholar 

  • Tryjanowski, P. & A. Goławski, 2004. Sex differences in nest defence by the red-backed shrike Lanius collurio: effects of offspring age, brood size, and stage of breeding season. Journal of Ethology 22: 13–16.

    Article  Google Scholar 

  • Vélez, M. J., M. D. Jennions & S. R. Telford, 2002. The effect of an experimental brood reduction on male desertion in the Panamanian blue acara cichlid Aequidens coeruleopunctatus. Ethology 108: 331–340.

    Article  Google Scholar 

  • Watts, S. H., 2014. A study of nesting sparrowhawks Accipiter nisus using video analysis. Bird Study 61: 428–437.

    Article  Google Scholar 

  • Wisenden, B. D., 1994. Factors affecting mate desertion by males in free-ranging convict cichlids (Cichlasoma nigrofasciatum). Behavioral Ecology 5: 439–447.

    Article  Google Scholar 

  • Wisenden, B. D., J. L. Snekser, A. D. Stumbo & J. M. Leese, 2008. Parental defence of an empty nest after catastrophic brood loss. Animal Behaviour 76: 2059–2067.

    Article  Google Scholar 

  • Wynne-Edwards, K. E., 1995. Biparental care in Djungarian but not Siberian dwarf hamsters (Phodopus). Animal Behaviour 50: 1571–1585.

    Article  Google Scholar 

Download references

Acknowledgments

We thank Fiona Kang, Rowan Jacques-Hamilton, Nicholas Deal, Rachel Fetherston, Eeling Ng, Ruby Albury, Andrej Hohmann and Matthew Simpson for logistic support and animal collection. We also thank members of the Wong and Chapple Labs at Monash University, who assisted with animal husbandry. Lastly, we thank Professor Sefc and two anonymous reviewers for their helpful suggestions to improve the manuscript. Funding was provided by the Holsworth Wildlife Endowment Fund, and the Linnean Society of New South Wales.

Author information

Authors and Affiliations

  1. School of Biological Sciences, Monash University, Clayton, Australia

    Will Sowersby, Topi K. Lehtonen & Bob B. M. Wong

  2. Department of Zoology, Stockholm University, Universitetsvägen 10, 114 18, Stockholm, Sweden

    Will Sowersby

  3. Department of Biology, University of Turku, Turku, Finland

    Topi K. Lehtonen

Authors
  1. Will Sowersby
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Topi K. Lehtonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bob B. M. Wong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Will Sowersby.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Research Involving in Human and animal rights

All applicable national and 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 (Animal Ethics Committee of Monash University, Australia, BSCI/2012/23).

Additional information

Guest editors: S. Koblmüller, R. C. Albertson, M. J. Genner, K. M. Sefc & T. Takahashi / Advances in Cichlid Research II: Behavior, Ecology and Evolutionary Biology

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sowersby, W., Lehtonen, T.K. & Wong, B.B.M. Temporal and sex-specific patterns of breeding territory defense in a color-polymorphic cichlid fish. Hydrobiologia 791, 237–245 (2017). https://doi.org/10.1007/s10750-016-2889-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-2889-1

Keywords

Search

Navigation