Skip to main content
Log in

Consistent individual differences in paternal behavior: a field study of three-spined stickleback

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Consistent individual differences in parenting are widespread; however, we know little about why there is variation in parenting behavior among individuals within species. One possible explanation for consistent individual differences in parenting is that individuals invest in different aspects of parental care, such as provisioning or defense. In this field study, we measured consistent individual differences in parenting behavior and evaluated correlations between parenting and other behaviors in three-spined stickleback (Gasterosteus aculeatus). We repeatedly measured male parenting behavior and male behavior in the presence of three different types of live intruders: a female, a conspecific male, and a predator, meant to provoke courtship, aggressive, and antipredator behavior, respectively. While males plastically adjusted their reactions to different types of intruders, we found consistent individual differences in behavior (behavioral types) both within and across contexts, even after accounting for variation in body size and nest characteristics. Males that performed more parenting behavior responded faster to all types of intruders. These results suggest that in nature, individual male sticklebacks exhibit robust parental behavioral types, and highly parental males are more attentive to their surroundings. Future studies are needed to examine the potential causes of individual variation in parental behavior in the field.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Barnett CA, Thompson CF, Sakaluk SK (2012) Aggressiveness, boldness and parental food provisioning in male house wrens (Troglodytes aedon). Ethology 118:984–993

    Article  Google Scholar 

  • Bell AM (2005) Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J Evol Biol 18:464–473

    Article  CAS  PubMed  Google Scholar 

  • Bell AM (2013) Randomized or fixed order for studies of behavioral syndromes? Behav Ecol 24:16–20

    Article  Google Scholar 

  • Bell AM, Backstrom T, Huntingford FA, Pottinger TG, Winberg S (2007) Variable neuroendocrine responses to ecologically-relevant challenges in sticklebacks. Physiol Behav 91:15–25

    Article  CAS  PubMed  Google Scholar 

  • Betini GS, Norris DR (2012) The relationship between personality and plasticity in tree swallow aggression and the consequences for reproductive success. Anim Behav 83:137–143

    Article  Google Scholar 

  • Boughman JW (2007) Condition-dependent expression of red colour differs between stickleback species. J Evol Biol 20:1577–1590

    Article  CAS  PubMed  Google Scholar 

  • Budaev SV, Zworykin DD, Mochek AD (1999) Individual differences in parental care and behavior profile in the convict cichlid: a correlation study. Anim Behav 58:195–202

    Article  PubMed  Google Scholar 

  • Burtka JL, Grindstaff JL (2013) Repeatable nest defense behavior in a wild population of Eastern bluebirds (Sialia sialis) as evidence of personality. Acta Ethol 16:135–146

    Article  Google Scholar 

  • Candolin U (1998) Reproduction under predation risk and the trade-off between current and future reproduction in the threespine stickleback. Proc R Soc Lond B 265:1171–1175

    Article  Google Scholar 

  • Candolin U (2007) Changes in expression and honesty of sexual signalling over the reproductive lifetime of sticklebacks. Proc R Soc Lond B 267:2425–2430

    Article  Google Scholar 

  • Cole EF, Quinn JL (2014) Shy birds play it safe: personality in captivity predicts risk responsiveness during reproduction in the wild. Biol Lett 10:20140178

    Article  PubMed  Google Scholar 

  • Dingemanse NJ, Dochtermann N (2013) Quantifying individual variation in behavior: mixed-effect modelling approaches. J Anim Ecol 82:39–54

    Article  PubMed  Google Scholar 

  • Dingemanse NJ, Wright J, Kazem AJN, Thomas DK, Hickling R, Dawnay N (2007) Behavioral syndromes differ predictably between 12 populations of three-spined stickleback. J Anim Ecol 76:1128–1138

    Article  PubMed  Google Scholar 

  • Dochtermann NA, Dingemanse NJ (2013) Behavioral syndromes as evolutionary constraints. Behav Ecol 24:806–811

    Article  Google Scholar 

  • Duckworth RA (2006) Behavioral correlations across breeding contexts provide a mechanism for a cost of aggression. Behav Ecol 17:1011–1019

    Article  Google Scholar 

  • Feliciano JB (2004) A study of the salmonid populations in the Navarro River Watershed: patterns of decline and tools for monitoring. Dissertation, University of California Davis

  • Foster SA (1988) Diversionary displays of paternal stickleback—defenses against cannibalistic groups. Behav Ecol Sociobiol 22:335–340

    Google Scholar 

  • Hadfield JD (2010) MCMC methods for multi-response generalised linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22

    Google Scholar 

  • Huntingford FA (1976) The relationship between anti-predator behavior and aggression among conspecifics in the three-spined stickleback, Gasterosteus aculeatus. Anim Behav 24:245–260

    Article  Google Scholar 

  • Kazama K, Niizuma Y, Watanuki Y (2012) Consistent individual variations in aggressiveness and a behavioral syndrome across breeding contexts in different environments in the black-tailed gull. J Ethol 30:279–288

    Article  Google Scholar 

  • Ketterson ED, Nolan V (1999) Adaptation, exaptation, and constraint: a hormonal perspective. Am Nat 154:S4–S25

    Article  Google Scholar 

  • Kontiainen P, Pietiainen H, Huttunen K, Karell P, Kolunen H, Brommer JE (2009) Aggressive Ural owl mothers recruit more offspring. Behav Ecol 20:789–796

    Article  Google Scholar 

  • Kraak SBM, Bakker TCM, Mundwiler B (1999a) Sexual selection in sticklebacks in the field: correlates of reproductive, mating, and paternal success. Behav Ecol 10:696–706

    Article  Google Scholar 

  • Kraak SBM, Bakker TCM, Mundwiler B (1999b) Correlates of the duration of the egg collecting phase in the three-spined stickleback. J Fish Biol 54:1038–1049

    Article  Google Scholar 

  • Künzler R, Bakker TCM (2000) Pectoral fins and paternal quality in sticklebacks. Proc R Soc Lond B 267:999–1004

    Article  Google Scholar 

  • Lissaker M, Kvarnemo C (2006) Ventilation or nest defense—parental care trade-offs in a fish with male care. Behav Ecol Sociobiol 60:864–873

    Article  Google Scholar 

  • MacColl ADC, Hatchwell BJ (2003) Heritability of parental effort in a passerine bird. Evolution 57:2191–2195

    Article  PubMed  Google Scholar 

  • Marshall DJ, Uller T (2007) When is a maternal effect adaptive? Oikos 116:1957–1963

    Article  Google Scholar 

  • McGhee KE, Pintor L, Suhr E, Bell AM (2012) A nonadaptive maternal effect in sticklebacks. Funct Ecol 26:932–940

    Article  PubMed Central  PubMed  Google Scholar 

  • Meaney MJ (2001) Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 24:1161–1192

    Article  CAS  PubMed  Google Scholar 

  • Moodie GEE (1972) Predation, natural selection and adaptation in an unusual 3 spine stickleback. Heredity 28:155–167

    Article  Google Scholar 

  • Mutzel A, Blom MPK, Spagopoulou F, Wright J, Dingemanse NJ, Kempenaers B (2013) Temporal trade-offs between nestling provisioning and defense against nest predators in blue tits. Anim Behav 85:1459–1469

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

    PubMed  Google Scholar 

  • Nakagawa S, Gillespie DOS, Hatchwell BJ, Burke T (2007) Predictable males and unpredictable females: sex difference in repeatability of parental care in a wild bird population. J Evol Biol 20:1674–1681

  • Patrick SC, Browning LE (2011) Exploration behaviour is not associated with chick provisioning in great tits. PLoS ONE 6:e26383

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pressley PH (1981) Parental effort and the evolution of nest-guarding tactics in the threespine stickleback, Gasterosteus aculeatus L. Evolution 35:282–295

    Article  Google Scholar 

  • Rangeley RW, Godin J-GJ (1992) The effects of a trade-off between foraging and brood defense on parental behavior in the convict cichlid fish, Cichlasoma nigrofasciatum. Behaviour 120:123–138

    Article  Google Scholar 

  • Reznick D, Nunney L, Tessier A (2000) Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol Evol 15:421–425

  • Rytkonen S, Orell M, Koivula K, Soppela M (1995) Correlation between 2 components of parental investment—nest defense intensity and nestling provisioning effort of willow tits. Oecologia 104:386–393

    Article  Google Scholar 

  • Sabat AM (1994) Costs and benefits of parental effort in a brood-guarding fish (Ambloplites rupestris, Centrarchidae). Behav Ecol 5:195–201

    Article  Google Scholar 

  • Schwagmeyer PL, Mock DW (2003) How consistently are good parents good parents? Repeatability of parental care in the house sparrow, Passer domesticus. Ethology 109:303–313

    Article  Google Scholar 

  • Sparkes TC, Rush V, Foster SA (2008) Reproductive costs, condition and carotenoid-based colour in natural populations of threespine stickleback (Gasterosteus aculeatus). Ecol Freshw Fish 17:292–302

    Article  Google Scholar 

  • Stein LR, Bell AM (2012) Consistent individual differences in fathering in threespine stickleback Gasterosteus aculeatus. Curr Zool 58:45–52

    PubMed Central  PubMed  Google Scholar 

  • Stein LR, Bell AM (2014) Paternal programming in sticklebacks. Anim Behav 95:161–175

    Article  Google Scholar 

  • Stiver KA, Alonzo SH (2009) Parental and mating effort: is there necessarily a trade-off? Ethology 115:1101–1126

    Article  Google Scholar 

  • Tinbergen N, van Iersel JJA (1947) “Displacement reactions” in the three-spined stickleback. Behaviour 1:56–63

    Article  Google Scholar 

  • van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources—their influence on variation in life-history tactics. Am Nat 128:137–142

    Article  Google Scholar 

  • von Hippel FA (2000) Vigorously courting male sticklebacks are poor fathers. Acta Ethol 2:83–89

    Article  Google Scholar 

  • Westneat DF, Hatch MI, Wetzel DP, Ensminger AL (2011) Individual variation in parental care reaction norms: integration of personality and plasticity. Am Nat 178:652–667

    Article  PubMed  Google Scholar 

  • Wetzel DP, Westneat DF (2014) Parental care syndromes in house sparrows: positive covariance between provisioning and defense linked to parent identity. Ethology 10:249–257

    Article  Google Scholar 

  • Wingfield JC, Hegner RE, Dufty AM, Ball GF (1990) The challenge hypothesis—theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846

    Article  Google Scholar 

  • Wootton RJ (1984) A functional biology of sticklebacks. University of California Press, Berkeley

    Book  Google Scholar 

Download references

Acknowledgments

We are grateful to A. Fritzsche, L. Hostert, and M. Grobis for their help in the field. We also thank K. Laskowski, G. Kozak, K. McGhee, members of the Bell lab, and three reviewers for valuable comments on the manuscript. This project was supported by the University of Illinois, National Science Foundation Doctoral Dissertation Improvement Grant (IOS 1210696) and an NSF Graduate Research Fellowship to LRS, and NSF IOS 1121980 and National Institutes of Health R01 GM082937 to AMB.

Ethical note

All focal males resumed parenting behavior following measurements and observations. Intruders were placed in a wire cage with openings too small for either the focal male or the intruder to injure each other. All intruder individuals were held for less than 5 h and released at their point of capture following observations; all intruders resumed normal behavior upon release. This study was conducted under California Fish and Game Permit SC-11131 and approved by the Institutional Animal Care and Use Committee at the University of Illinois at Urbana-Champaign (protocol #09204).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laura R. Stein.

Additional information

Communicated by N. Dingemanse

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 24 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stein, L.R., Bell, A.M. Consistent individual differences in paternal behavior: a field study of three-spined stickleback. Behav Ecol Sociobiol 69, 227–236 (2015). https://doi.org/10.1007/s00265-014-1835-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-014-1835-3

Keywords

Navigation