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Hydrobiologia

, Volume 748, Issue 1, pp 75–85 | Cite as

Sex and social status affect territorial defence in a cooperatively breeding cichlid fish, Neolamprologus savoryi

  • Kelly A. Garvy
  • Jennifer K. Hellmann
  • Isaac Y. Ligocki
  • Adam R. Reddon
  • Susan E. Marsh-Rollo
  • Ian M. Hamilton
  • Sigal Balshine
  • Constance M. O’Connor
ADVANCES IN CICHLID RESEARCH

Abstract

Members of social groups must defend their shared territory against both predators and competitors. However, individuals differ widely in their contributions to territorial defence. Assessing the variation in response to territorial intrusions provides insight into both the benefits and costs of group living for different group members. In this study, we assessed the response of wild Neolamprologus savoryi to experimentally staged territorial intrusions. Neolamprologus savoryi is an understudied cooperatively breeding cichlid fish endemic to Lake Tanganyika, East Africa. We found that dominant male and dominant female N. savoryi were both highly aggressive towards heterospecific predators and towards same-sex conspecific rivals. Both dominant males and females were less aggressive towards opposite-sex conspecific opponents, with the relative reduction in aggression being most pronounced in males. Subordinates provided low levels of defence against all intruder types, which suggests that subordinate N. savoryi rely on larger group members for protection. Collectively, our results provide insight into the structure and function of N. savoryi social groups, and highlights key costs and benefits of cooperation for individual social group members.

Keywords

Aggression Defence Cooperation Lake Tanganyika Neolamprologus pulcher 

Notes

Acknowledgements

The authors wish to thank Danny Sinyinza, Dr. Cyprian Katongo, Dr. Harris Phiri, Peter Sekazway, Clement Sichamba, Augustine Mwewa, Celestine Mwewa, Fernandez Mwewa, Gegwin Kapembwe, Damius Kapembwe, and all of the wonderful staff of the Tanganyika Science Lodge for their logistical support of the field research. The research was supported by a Natural Sciences and Engineering Research Council of Canada Discovery (NSERC) grant and equipment grant to SB, as well as Ontario Innovation Trust and Canadian Foundation for Innovation awards to SB. Further funding for the field research was provided by a Journal of Experimental Biology Travelling Fellowship to CMO, and Canadian Society of Zoologists and McMaster School of Graduate Studies research grants to ARR. CMO was supported by the E.B. Eastburn Postdoctoral Fellowship from the Hamilton Community Foundation, and is currently supported by an NSERC Postdoctoral Fellowship. ARR was supported by the Margo Wilson and Martin Daly Ontario Graduate Scholarship, and is currently supported by the Richard H. Tomlinson Postdoctoral Fellowship, and an NSERC Postdoctoral Fellowship. IYL and JKH are supported by the Department of Evolution, Ecology, and Organismal Biology at The Ohio State University, The Ohio State University Fish Systematics Endowment, and the SciFund Challenge. JKH is supported by the American Academy of Underwater Sciences. SB is supported by the Canada Research Chair Program and the NSERC Discovery Program.

References

  1. Arnold, K. & I. P. F. Owens, 1998. Cooperative breeding in birds: comparative test of the life history hypothesis. Proceedings of Royal Society of London B: Biological Sciences 265: 739–745.CrossRefGoogle Scholar
  2. Awata, S. & M. Kohda, 2004. Parental roles and the amount of care in a bi-parental substrate brooding cichlid: the effect of size differences within pairs. Behaviour 141: 1135–1149.CrossRefGoogle Scholar
  3. Balshine, S., B. Leach, F. C. Neat, H. Reid, M. Taborsky & N. Werner, 2001. Correlates of group size in a cooperatively breeding cichlid fish (Neolamprologus pulcher). Behavioral Ecology and Sociobiology 50: 134–140.CrossRefGoogle Scholar
  4. Balshine-Earn, S., F. C. Neat, H. Reid & M. Taborsky, 1998. Paying to stay or paying to breed? Field evidence for direct benefits of helping behavior in a cooperatively breeding fish. Behavioral Ecology 9: 432–438.CrossRefGoogle Scholar
  5. Balsine, S. & P. M. Buston, 2008. Cooperation in fish. In Magnhagen, V., E. Forsgren & B. G. Kapoor (eds), Fish Behaviour. Science Publishers, Enfield, New Hampshire: 437–484.CrossRefGoogle Scholar
  6. Barclay, P., 2010. Altruism as a courtship display: some effects of third-party generosity on audience perceptions. British Journal of Psychology 10: 123–135.CrossRefGoogle Scholar
  7. Barclay, P. & H. K. Reeve, 2012. The varying relationship between helping and individual quality. Behavioral Ecology 23: 693–698.CrossRefGoogle Scholar
  8. Bates, D., M. Maechler, B. Bolker & S. Walker, 2013. lme4: Linear Mixed-Effects Models Using Eigen and S4. R package version 1.0-5. http://CRAN.R-project.org/package=lme4.
  9. Bergmüller, R., D. Heg & M. Taborsky, 2005. Helpers in a cooperatively breeding cichlid stay and pay or disperse and breed, depending on ecological constraints. Proceedings of the Royal Society B: Biological Sciences 272: 325–331.CrossRefPubMedCentralPubMedGoogle Scholar
  10. Bergmüller, R., R. A. Johnstone, A. F. Russell & R. Bshary, 2007. Integrating cooperative breeding into theoretical concepts of cooperation. Behavioural Processes 76: 61–72.CrossRefPubMedGoogle Scholar
  11. Bernasconi, G. & J. E. Strassmann, 1999. Cooperation among unrelated individuals: the ant foundress case. Trends in Ecology and Evolution 14: 477–482.CrossRefPubMedGoogle Scholar
  12. Bolker, B. M., 2008. Ecological Models and Data in R. Princeton University Press, Princeton, NJ.Google Scholar
  13. Brichard, P., 1989. Cichlids and all the other fishes of Lake Tanganyika. THF Publications, Neptune City, NJ.Google Scholar
  14. Brouwer, L., D. Heg & M. Taborsky, 2005. Experimental evidence for helper effects in a cooperatively breeding cichlid. Behavioral Ecology 16: 667–673.CrossRefGoogle Scholar
  15. Brown, J. L., 1987. Helping and Communal Breeding in Birds. Princeton University Press, Princeton, NJ.CrossRefGoogle Scholar
  16. Choe, J. C. & B. J. Crespi, 1997. The Evolution of Social Behaviour in Insects and Arachnids. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
  17. Clutton-Brock, T., 2002. Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296: 69–72.CrossRefPubMedGoogle Scholar
  18. Clutton-Brock, T., 2009. Cooperation between non-kin in animal societies. Nature 462: 51–57.CrossRefPubMedGoogle Scholar
  19. Clutton-Brock, T. & E. Huchard, 2013. Social competition and selection in males and females. Philosophical Transactions of the Royal Society B: Biological Sciences 368: 20130074.CrossRefGoogle Scholar
  20. Clutton-Brock, T. H., D. Gaynor, G. M. McIlrath, A. D. C. Maccoll, R. Kansky, P. Chadwick, M. Manser, J. D. Skinner & P. N. M. Brotherton, 1999. Predation, group size and mortality in a cooperative mongoose, Suricata suricatta. Journal of Animal Ecology 68: 672–683.CrossRefGoogle Scholar
  21. Day, J. J., S. Santini & J. Garcia-Moreno, 2007. Phylogenetic relationships of the Lake Tanganyika cichlid tribe Lamprologini: the story from mitochondrial DNA. Molecular Phylogenetics and Evolution 45: 629–642.CrossRefPubMedGoogle Scholar
  22. De Rosario-Martinez, H., 2013. phia: Post-Hoc Interaction Analysis. R package version 0.1-5. http://CRAN.R-project.org/package=phia.
  23. Desjardins, J. K., K. A. Stiver, J. L. Fitzpatrick & S. Balshine, 2008. Differential responses to territory intrusions in cooperatively breeding fish. Animal Behaviour 75: 595–604.CrossRefGoogle Scholar
  24. Dierkes, P., D. Heg, M. Taborsky, E. Skubic & R. Achmann, 2005. Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid. Ecology Letters 8: 968–975.CrossRefGoogle Scholar
  25. Duffy, E. J., C. L. Morrison & K. S. Macdonald, 2002. Colony defense and behavioral differentiation in the eusocial shrimp Synalpheus regalis. Behavioral Ecology and Sociobiology 51: 488–495.CrossRefGoogle Scholar
  26. Dugatkin, L., 2002. Animal cooperation among unrelated individuals. Naturwissenschaften 89: 533–541.PubMedGoogle Scholar
  27. Emlen, S. T., 1997. Predicting family dynamics in social vertebrates. In Krebs, J. R. & N. B. Davies (eds), Behavioural Ecology: An Evolutionary Approach. Wiley Publishers, Hoboken, NJ: 228–253.Google Scholar
  28. Emlen, S. T., H. K. Reeve, P. W. Sherman, P. H. Wrege & J. Shellman-Reeve, 1991. Adaptive versus nonadaptive explanations of behavior: the case of alloparental helping. The American Naturalist 138: 259–270.CrossRefGoogle Scholar
  29. Gaston, A. J., 1978. The evolution of group territorial behavior and cooperative breeding. The American Naturalist 112: 1091–1100.CrossRefGoogle Scholar
  30. Godin, J.-G. J., 1997. Behavioural ecology of fishes: adaptations for survival and reproduction. In Godin, J.-G. J. (ed.), Behavioural Ecology of Teleost Fishes. Oxford University Press, Oxford, UK: 1–9.Google Scholar
  31. Goodwin, N. B., S. Balshine-Earn & J. D. Reynolds, 1998. Evolutionary transitions in parental care in cichlid fish. Proceedings of the Royal Society of London B: Biological Sciences 265: 2265–2272.CrossRefGoogle Scholar
  32. Griffin, A. S. & S. A. West, 2003. Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302: 634–636.CrossRefPubMedGoogle Scholar
  33. Hamilton, W. D., 1964a. The genetical evolution of social behaviour I. Journal of Theoretical Biology 7: 1–16.CrossRefPubMedGoogle Scholar
  34. Hamilton, W. D., 1964b. The genetical evolution of social behaviour II. Journal of Theoretical Biology 7: 17–52.CrossRefPubMedGoogle Scholar
  35. Hatchwell, B. J. & J. Komdeur, 2000. Ecological constraints, life history traits and the evolution of cooperative breeding. Animal Behaviour 59: 1079–1086.CrossRefPubMedGoogle Scholar
  36. Heg, D. & Z. Bachar, 2006. Cooperative breeding in the Lake Tanganyika cichlid Julidochromis ornatus. Environmental Biology of Fishes 76: 265–281.CrossRefGoogle Scholar
  37. Heg, D. & M. Taborsky, 2010. Helper response to experimentally manipulated predation risk in the cooperatively breeding cichlid Neolamprologus pulcher. PLoS One 5: e10784.CrossRefPubMedCentralPubMedGoogle Scholar
  38. Heg, D., Z. Bachar & M. Taborsky, 2005a. Cooperative breeding and group structure in the Lake Tanganyika cichlid Neolamprologus savoryi. Ethology 111: 1017–1043.CrossRefGoogle Scholar
  39. Heg, D., L. Brouwer, Z. Bachar & M. Taborsky, 2005b. Large group size yields group stability in the cooperatively breeding cichlid Neolamprologus pulcher. Behaviour 142: 11–12.CrossRefGoogle Scholar
  40. Heg, D., Z. Heg-Bachar, L. Brouwer & M. Taborsky, 2008. Experimentally induced helper dispersal in colonially breeding cooperative cichlids. Environmental Biology of Fishes 83: 191–206.CrossRefGoogle Scholar
  41. Heg, D., E. Jutzeler, J. S. Mitchell & I. M. Hamilton, 2009. Helpful female subordinate cichlids are more likely to reproduce. PLoS One 4: e5458.CrossRefPubMedCentralPubMedGoogle Scholar
  42. Hellmann, J. K. & I. M. Hamilton, 2014. The presence of neighbors influences defense against predators in a cooperatively breeding cichlid. Behavioral Ecology 25: 386–391.CrossRefGoogle Scholar
  43. Hick, K., A. R. Reddon, C. M. O’Connor & S. Balshine, 2014. Strategic and tactical fighting decisions in cichlid fishes with divergent social systems. Behaviour 151: 47–71.CrossRefGoogle Scholar
  44. 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: 237–245.CrossRefGoogle Scholar
  45. Itzkowitz, M., N. Santangelo & M. Richter, 2002. How similar is the coordination of parental roles among different pairs? An examination of a monogamous fish. Ethology 108: 727–738.CrossRefGoogle Scholar
  46. 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.CrossRefGoogle Scholar
  47. Jetz, W. & D. R. Rubenstein, 2011. Environmental uncertainty and the global biogeography of cooperative breeding in birds. Current Biology 21: 72–78.CrossRefPubMedGoogle Scholar
  48. Johnsson, J. I., F. Nöbbelin & T. Bohlin, 1999. Territorial competition among wild brown trout fry: effects of ownership and body size. Journal of Fish Biology 54: 469–472.CrossRefGoogle Scholar
  49. Katoh, R., H. Munehara & M. Kohda, 2005. Alternative male mating tactics of the substrate brooding cichlid Telmatochromis temporalis in Lake Tanganyika. Zoological Science 22: 555–561.CrossRefPubMedGoogle Scholar
  50. Kawanabe, H., M. Hori & M. Nagoshi, 1997. Fish Communities in Lake Tanganyika. Kyoto University Press, Kyoto, Japan.Google Scholar
  51. Kleiber, C. & A. Zeileis, 2008. AER: Applied Econometrics with R. R package version 1.2-2. http://CRAN.R-project.org/package=AER.
  52. Koenig, W. D. & J. L. Dickinson, 2004. Ecology and Evolution of Cooperative Breeding in Birds. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
  53. Kokko, H., R. A. Johnstone & T. H. Clutton-Brock, 2001. The evolution of cooperative breeding through group augmentation. Proceedings of the Royal Society of London B: Biological Sciences 268: 187–196.CrossRefGoogle Scholar
  54. Kokko, H., R. A. Johnstone & J. Wright, 2002. The evolution of parental and alloparental effort in cooperatively breeding groups: when should helpers pay to stay? Behavioral Ecology 13: 291–300.CrossRefGoogle Scholar
  55. Komdeur, J., 2006. Variation in individual investment strategies among social animals. Ethology 112: 729–747.Google Scholar
  56. Kondo, T., 1986. Feeding habits of Lamprologus savoryi (Teleostei: Cichlidae) with reference to its social behaviour. Physiology & Ecology Japan 23: 1–15.Google Scholar
  57. Konings, A., 1998. Tanganyika Cichlids in Their Natural Habitat. Cichlid Press, El Paso, TX.Google Scholar
  58. Konings, A., 2005. Back to Nature Guide to Tanganyika cichlids. Cichlid Press, El Paso, TX.Google Scholar
  59. Krause, J. & G. D. Ruxton, 2002. Living in Groups. Oxford University Press, Oxford, UK.Google Scholar
  60. Lehtonen, T. K., J. K. McCrary & A. Meyer, 2010. Territorial aggression can be sensitive to the status of heterospecific intruders. Behavioral Processes 84: 598–601.CrossRefGoogle Scholar
  61. Lukas, D. & T. Clutton-Brock, 2012. Cooperative breeding and monogamy in mammalian societies. Proceedings of the Royal Society B: Biological Sciences 279: 2151–2156.CrossRefPubMedCentralPubMedGoogle Scholar
  62. Magrath, R. D., 2001. Group breeding dramatically increases reproductive success of yearling but not older female scrubwrens: a model for cooperatively breeding birds? Journal of Animal Ecology 70: 370–385.CrossRefGoogle Scholar
  63. Maklakov, A. A., 2002. Snake-directed mobbing in a cooperative breeder: anti-predator behaviour or self-advertisement for the formation of dispersal coalitions? Behavioral Ecology and Sociobiology 52: 372–378.CrossRefGoogle Scholar
  64. Mares, R., A. J. Young & T. H. Clutton-Brock, 2012. Individual contributions to territory defence in a cooperative breeder: weighing up the benefits and costs. Proceedings of the Royal Society B: Biological Sciences 279: 3989–3995.CrossRefPubMedCentralPubMedGoogle Scholar
  65. Mathis, A., 1991. Territories of male and female terrestrial salamanders: costs, benefits and intersexual spatial associations. Oecologica 86: 433–440.CrossRefGoogle Scholar
  66. Mboko, S. K. & M. Kohda, 1999. Piracy mating by large males in a monogamous substrate-breeding cichlid in Lake Tanganyika. Journal of Ethology 17: 51–55.CrossRefGoogle Scholar
  67. 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.Google Scholar
  68. Morley, J. I. & S. Balshine, 2003. Faithful fish: territory and mate defence favour monogamy in an African cichlid fish. Environmental Biology of Fishes 66: 169–179.CrossRefGoogle Scholar
  69. Nelson, J. S., 2006. Fishes of the World. Wiley Publishers, Hoboken, NJ.Google Scholar
  70. Ota, K. & M. Kohda, 2006. Description of alternative male reproductive tactics in a shell-brooding cichlid, Telmatochromis vittatus, in Lake Tanganyika. Journal of Ethology 24: 9–15.CrossRefGoogle Scholar
  71. Ota, K., M. Aibara, M. Morita, S. Awata, M. Hori & M. Kohda, 2012. Alternative reproductive tactics in the shell-brooding Lake Tanganyika cichlid Neolamprologus brevis. International Journal of Evolutionary Biology 2012: 193235.CrossRefPubMedCentralPubMedGoogle Scholar
  72. Queller, D. C. & J. E. Strassmann, 1998. Kin selection and social insects. Bioscience 48: 165–175.CrossRefGoogle Scholar
  73. Queller, D. C., F. Zacchi, R. Cervo, S. Turillazzi, M. Henshaw, L. Santorelli & J. E. Strassmann, 2000. Unrelated helpers in a social insect. Nature 405: 784–787.CrossRefPubMedGoogle Scholar
  74. R Development Core Team, 2008. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.
  75. Rasa, O. A. E., 1987. The dwarf mongoose: a study of behavior and social structure in relation to ecology in a small, social carnivore. Advances in the Study of Behaviour 17: 121–163.CrossRefGoogle Scholar
  76. Rasa, O. A. E., 1989. The costs and effectiveness of vigilance behaviour in the dwarf mongoose: implications for fitness and optimal group size. Ethology Ecology and Evolution 1: 265–282.CrossRefGoogle Scholar
  77. Ripley, B., B. Venables, D. M. Bates, K. Hornik, A. Gebhardt & D. Firth, 2014. MASS: Support Functions and Datasets for Venables and Ripley’s MASS. R Package Version 7.3-31. http://CRAN.R-project.org/package=MASS.
  78. Rogers, W., 1988. Parental investment and division of labor in the Midas cichlid (Cichlasoma citrinellum). Ethology 79: 126–142.CrossRefGoogle Scholar
  79. Rossiter, A., 1995. The cichlid fish assemblages of Lake Tanganyika: ecology, behaviour and evolution of its species flocks. Advances in Ecological Research 26: 187–252.CrossRefGoogle Scholar
  80. Sato, T. & M. M. Gashagaza, 1997. Shell-brooding cichlids of Lake Tanganyika: their habits and maing systems. In Kawanabe, H., M. Hori & M. Nagoshi (eds), Fish Communities in Lake Tanganyika. Kyoto University Press, Kyoto: 221–240.Google Scholar
  81. Schradin, C., 2004. Territorial defense in a group-living solitary forager: who, where, against whom? Behavioral Ecology and Sociobiology 55: 439–446.CrossRefGoogle Scholar
  82. Schradin, C. & J. Lamprecht, 2002. Causes of female emigration in the group-living cichlid fish Neolamprologus multifasciatus. Ethology 108: 237–248.CrossRefGoogle Scholar
  83. Sopinka, N. M., J. L. Fitzpatrick, J. K. Desjardins, K. A. Stiver, S. E. Marsh-Rollo & S. Balshine, 2009. Liver size reveals social status in the African cichlid Neolamprologus pulcher. Journal of Fish Biology 75: 1–16.Google Scholar
  84. Stacey, P. B. & W. D. Koenig, 1990. Cooperative Breeding in Birds: Long-term Studies of Ecology and Behaviour. Cambridge University Press, Cambridge, UK.CrossRefGoogle Scholar
  85. Stiver, K. A., P. Dierkes, M. Taborsky & S. Balshine, 2004. Dispersal patterns and status change in a co-operatively breeding cichlid Neolamprologus pulcher: evidence from microsatellite analyses and behavioural observations. Journal of Fish Biology 65: 91–105.CrossRefGoogle Scholar
  86. Stiver, K. A., P. Dierkes, M. Taborsky, H. L. Gibbs & S. Balshine, 2005. Relatedness and helping in fish: examining the theoretical predictions. Proceedings of the Royal Society B: Biological Sciences 272: 1593–1599.CrossRefPubMedCentralPubMedGoogle Scholar
  87. Sturmbauer, C., W. Salzburger, N. Duftner, R. Schelly & S. Koblmüller, 2010. Evolutionary history of the Lake Tanganyika cichlid tribe Lamprologini (Teleostei: Perciformes) derived from mitochondrial and nuclear DNA data. Molecular Phylogenetics and Evolution 57: 266–284.CrossRefPubMedCentralPubMedGoogle Scholar
  88. Taborsky, M., 1984. Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. Animal Behaviour 32: 1236–1252.CrossRefGoogle Scholar
  89. Taborsky, M., 1987. Cooperative behaviour in fish: coalitions, kin groups and reciprocity. In Brown, J. L. & I. Kikkawa (eds), Animal Societies: Theories and Facts. Japan Scientific Society Press, Tokyo, Japan: 229–237.Google Scholar
  90. Taborsky, M., 1994. Sneakers, satellites and helpers: parasitic and cooperative behaviour in fish reproduction. Advances in the Study of Behavior 23: 1–100.CrossRefGoogle Scholar
  91. Taborsky, M., 2001. The evolution of bourgeois, parasitic and cooperative reproductive behaviors in fishes. Journal of Heredity 92: 100–110.CrossRefPubMedGoogle Scholar
  92. Trewavas, E. & M. Poll, 1952. Three new species and two new subspecies of the genus Lamprologus, cichlid fishes of Lake Tanganyika. Proceedings of the Royal Society of London B: Biological Sciences 116: 240–246.Google Scholar
  93. Wisenden, B. D., 1999. Alloparental care in fishes. Reviews in Fish Biology and Fisheries 9: 45–70.CrossRefGoogle Scholar
  94. Wong, M. Y. L. & S. Balshine, 2011. The evolution of cooperative breeding in the African cichlid fish, Neolamprologus pulcher. Biological Reviews 86: 511–530.CrossRefPubMedGoogle Scholar
  95. Wong, M. Y. L., L. A. Jordan, S. Marsh-Rollo, S. St-Cyr, J. O. Reynolds, K. A. Stiver, J. K. Desjardins, J. L. Fitzpatrick & S. Balshine, 2012. Mating systems in cooperative breeders: the roles of resource dispersion and conflict mitigation. Behavioral Ecology 23: 521–530.CrossRefGoogle Scholar
  96. Yamagishi, S. & M. Kohda, 1996. Is the cichlid fish Julidochromis marlieri polyandrous? Ichthyological Research 43: 469–471.CrossRefGoogle Scholar
  97. Zahavi, A., 1995. Altruism as a handicap—the limitations of kin selection and reciprocity. Avian Biology 26: 1–3.CrossRefGoogle Scholar
  98. Zahavi, A. & A. Zahavi, 1997. The Handicap Principle: A Missing Piece of Darwin ‘s Puzzle. Oxford University Press, Oxford, UK.Google Scholar
  99. Zuur, A. F., J. M. Hilbe & E. N. Ieno, 2013. Beginner’s Guide to GLM and GLMM with R. Highland Statistics Ltd., Newburgh, UK.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Kelly A. Garvy
    • 1
  • Jennifer K. Hellmann
    • 2
  • Isaac Y. Ligocki
    • 2
  • Adam R. Reddon
    • 3
    • 5
  • Susan E. Marsh-Rollo
    • 3
  • Ian M. Hamilton
    • 2
    • 4
  • Sigal Balshine
    • 3
  • Constance M. O’Connor
    • 3
  1. 1.Nicholas School of the EnvironmentDuke UniversityDurhamUSA
  2. 2.Department of Evolution, Ecology and Organismal BiologyThe Ohio State UniversityColumbusUSA
  3. 3.Aquatic Behavioural Ecology Lab, Department of Psychology, Neuroscience, and BehaviourMcMaster UniversityHamiltonCanada
  4. 4.Department of MathematicsThe Ohio State UniversityColumbusUSA
  5. 5.Department of BiologyMcGill UniversityMontrealCanada

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