Skip to main content

Parental and alloparental investment in campo flickers (Colaptes campestris campestris): when relatedness comes first

Behavioral Ecology and Sociobiology volume 71, Article number: 139 (2017) Cite this article

Abstract

In cooperative species, parental investment may be shared with auxiliaries. Kin selection and other types of benefits have been proposed to explain the evolution of helping behavior. Auxiliaries are expected to be more helpful when closely related to the breeders. In this context, breeders may adjust parental investment in at least three ways: (a) reducing their effort and being compensated by the auxiliaries’ investment (compensatory effect); (b) maintaining their effort, with an increase in total investment (additive effect); or (c) partial compensation, i.e., a decrease in care by the parents but not by as much as the increase in care from the auxiliaries. We studied the cooperative species Colaptes campestris campestris and tested the following hypotheses: (1) partial compensation effect occurs, (2) parents modulate their investment relative to the auxiliaries’ investment, (3) auxiliaries adjust their investment according to their relationship to the offspring, and (4) groups whose members are in better physical condition fledge more young or these are in better condition. We determined relatedness within groups and monitored parental and alloparental behavior during breeding. Breeders in cooperative groups presented the same investment as unattended breeders. Restricting the analysis to cooperative groups revealed that the investment made by auxiliaries reflected their relatedness to the young and positively affected the investment by breeders. Results suggest that a partial compensation occurs in the species, with breeders reducing their effort despite the small increase in overall nest investment. Results highlight the importance of kin selection in the evolution of cooperative breeding in campo flickers.

Significance statement

Cooperatively breeding birds may have auxiliaries that help rear their brood. The evolution of helping behavior may derive from kin selection, where auxiliaries could gain a genetic benefit by helping to rear kin, which occurs when groups are composed of closely related individuals. However, it is often the case that some offspring may not be closely related to the auxiliaries due to the species’ mating system. We used the cooperatively breeding campo flickers to investigate whether and how the presence of auxiliaries might affect parental care patterns and nest productivity. We found that breeders did not reduce their investment in the presence of auxiliaries and that cooperative groups present the same overall investment when compared with unassisted pairs, indicating that the investment made by auxiliaries was not large enough to affect the total investment nor the breeders’ investment. Our results also show that auxiliaries increased their investment when they were more closely related to the brood.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

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

    Article  Google Scholar 

  • Brouwer L, van de Pol M, Cockburn A (2014) The role of social environment on parental care: offspring benefit more from the presence of female than male helpers. J Anim Ecol 83:491–503

    Article  PubMed  Google Scholar 

  • Brown JL (1987) Helping and communal breeding in birds. Princeton University Press, Princeton

    Book  Google Scholar 

  • Brown JL, Dow DD, Brown ER, Brown SD (1978) Effects of helpers on feeding on nestlings in the grey-crowned babbler (Pomatostomus temporalis). Behav Ecol Sociobiol 4:43–59

    Article  Google Scholar 

  • Burley N (1988) The differential-allocation hypothesis: an experimental test. Am Nat 132:611–628

    Article  Google Scholar 

  • Canestrari D, Marcos JM, Baglione V (2005) Effect of parentage and relatedness on the individual contributions to cooperative chick care in the carrion crow Corvus corone corone. Behav Ecol Sociobiol 57:422–428

    Article  Google Scholar 

  • Canestrari D, Marcos JM, Baglione V (2008) Reproductive success increases with group size in cooperative carrion crows, Corvus corone corone. Anim Behav 75:403–416

    Article  Google Scholar 

  • Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton

    Google Scholar 

  • Cockburn A (1998) Evolution of helping behavior in cooperatively breeding birds. Annu Rev Ecol Syst 29:141–177

    Article  Google Scholar 

  • Cornwallis C, West S, Griffin A (2009) Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal. J Evol Biol 22:2445–2457

    CAS  Article  PubMed  Google Scholar 

  • DeMory ML, Thompson CF, Sakaluk SK (2010) Male quality influences male provisioning in house wrens independent of attractiveness. Behav Ecol 21:1156–1164

    Article  Google Scholar 

  • de Lope F, Møller AP (1993) Female reproductive effort depends on the degree of ornamentation of their mates. Evolution 47:1152–1160

  • Dias RI, Macedo RH, Goedert D, Webster MS (2013a) Cooperative breeding in the campo flicker II: patterns of reproduction and kinship. Condor 115:855–862

    Article  Google Scholar 

  • Dias RI, Webster MS, Goedert D, Macedo RH (2013b) Cooperative breeding in the campo flicker I: breeding ecology and social behavior. Condor 115:847–854

    Article  Google Scholar 

  • Dias RI, Webster MS, Macedo RH (2015) Helping enhances productivity in campo flicker (Colaptes campestris) cooperative groups. Sci Nat 102:31

    Article  Google Scholar 

  • Dickinson JL, Hatchwell BJ (2004) Fitness consequences of helping. In: Koenig WD, Dickinson JL (eds) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, pp 48–66

    Chapter  Google Scholar 

  • Dickinson JL, Koenig WD, Pitelka FA (1996) The fitness consequences of helping behavior in the western bluebird. Behav Ecol 7:168–177

    Article  Google Scholar 

  • Doerr ED, Doerr VAJ (2007) Positive effects of helpers on reproductive success in the brown treecreeper and the general importance of future benefits. J Anim Ecol 76:966–976

    Article  PubMed  Google Scholar 

  • Dunn PO, Cockburn A, Mulder RA (1995) Fairy-wren helpers often care for young to which they are unrelated. Proc R Soc Lond B 259:339–343

    Article  Google Scholar 

  • Eikenaar C, Berg ML, Komdeur J (2003) Experimental evidence for the influence of food availability on incubation attendance and hatching asynchrony in the Australian reed warbler Acrocephalus australis. J Avian Biol 34:419–427

    Article  Google Scholar 

  • Emlen ST (1997) Predicting family dynamics in social vertebrates. In: Krebs JR, Davies NB (eds) Behavioural ecology, an evolutionary approach, 4th edn. Blackwell Publishing, Oxford, pp 228–253

  • Emlen ST, Wrege PH (1991) Breeding biology of white-fronted bee-eaters at Nakuru: the influence of helpers on breeder fitness. J Anim Ecol 60:309–326

    Article  Google Scholar 

  • Griffin AS, West SA (2003) Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302:634–636

    CAS  Article  PubMed  Google Scholar 

  • Hamilton WD (1964) The genetical theory of social behavior, I and II. J Theor Biol 7:1–52

    CAS  Article  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hatchwell BJ (1999) Investment strategies of breeders in avian cooperative breeding systems. Am Nat 154:205–219

    Article  Google Scholar 

  • Hatchwell BJ, Russell AF (1996) Provisioning rules in cooperatively breeding long-tailed tits Aegithalos caudatus: an experimental study. Proc R Soc Lond B 263:83–88

    Article  Google Scholar 

  • Hatchwell BJ, Russell AF, MacColl ADC, Ross DJ, Fowlie MK, McGowan A (2004) Helpers increase long-term but not short-term productivity in cooperatively breeding long-tailed tits. Behav Ecol 15:1–10

    Article  Google Scholar 

  • Heinsohn RG (2004) Parental care, load-lightening, and costs. In: Koenig WD, Dickinson JL (eds) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, pp 67–80

    Chapter  Google Scholar 

  • Johnstone RA (2011) Load lightening and negotiation over offspring care in cooperative breeders. Behav Ecol 22:436–444

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Khan MZ, Walters JR (2002) Effects of helpers on breeder survival in the red-cockaded woodpecker (Picoides borealis). Behav Ecol Sociobiol 51:336–344

    Article  Google Scholar 

  • Kingma SA, Hall ML, Arriero E, Peters A (2010) Multiple benefits of cooperative breeding in purple-crowned fairy-wrens: a consequence of fidelity? J Anim Ecol 79:757–768

    PubMed  Google Scholar 

  • Koenig WD, Mumme RL (1987) Population ecology of the cooperatively breeding acorn woodpecker. Princeton University Press, Princeton

    Google Scholar 

  • Koenig WD, Stacey PB (1990) Acorn woodpeckers: group-living and food storage under contrasting ecological conditions. In: Stacey PB, Koenig WD (eds) Cooperative breeding in birds: long-term studies of ecology and behavior. Cambridge University Press, Cambridge, pp 413–453

    Chapter  Google Scholar 

  • Koenig WD, Walters EL (2012) Brooding, provisioning, and compensatory care in the cooperatively breeding acorn woodpecker. Behav Ecol 23:181–190

    Article  Google Scholar 

  • Komdeur J (1994) The effect of kinship on helping in the co-operative breeding Seychelles warbler (Acrocephalus sechellensis). Proc R Soc Lond B 256:47–52

    Article  Google Scholar 

  • Kuhn S, Wiebe KL, Kempenaers B (2009) Isolation and characterization of polymorphic microsatellite loci for the northern flicker (Colaptes auratus). Mol Ecol Resour 9:845–848

    CAS  Article  PubMed  Google Scholar 

  • Legge S (2000a) The effect of helpers on reproductive success in the laughing kookaburra. J Anim Ecol 69:714–724

    Article  Google Scholar 

  • Legge S (2000b) Helper contributions in the cooperatively breeding laughing kookaburra: feeding young is no laughing matter. Anim Behav 59:1009–1018

    CAS  Article  PubMed  Google Scholar 

  • Liebl AL, Nomano FY, Browning LE, Russell AF (2016) Experimental evidence for fully additive care among male carers in the cooperatively breeding chestnut-crowned babbler. Anim Behav 115:47–53

    Article  Google Scholar 

  • Lloyd P, Taylor A, de Plessis MA, Martin TE (2009) Females increase reproductive investment in response to helper-mediated improvements in allo-feeding, nest survival, nestling provisioning and post-fledging survival in the Katoo scrub-robin Cercotrichas coryphaeus. J Avian Biol 40:400–411

    Article  Google Scholar 

  • Magrath RD, Yezerinac SM (1997) Facultative helping does not influence reproductive success or survival in cooperatively-breeding white-browed scrubwrens. J Anim Ecol 66:658–670

    Article  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    CAS  Article  PubMed  Google Scholar 

  • McDonald PG, Kazem AJN, Wright J (2009) Cooperative provisioning dynamics: fathers and unrelated helpers show similar responses to manipulations of begging. Anim Behav 77:369–376

    Article  Google Scholar 

  • Meade J, Nam K, Beckerman AP, Hatchwell BJ (2010) Consequences of ‘load-lightening’ for future indirect fitness gains by helpers in a cooperatively breeding bird. J Anim Ecol 79:529–537

    Article  PubMed  Google Scholar 

  • Mumme RL (1992) Do helpers increase reproductive success? An experimental analysis in the Florida scrub jay. Behav Ecol Sociobiol 31:319–328

    Article  Google Scholar 

  • Nam KB, Simeoni M, Sharp SP, Hatchwell BJ (2010) Kinship affects investment by helpers in a cooperatively breeding bird. Proc R Soc Lond B 277:3299–3306

    Article  Google Scholar 

  • Peig J, Green AJ (2009) New perspectives for estimating body condition from mass⁄ length data: the scaled mass index as an alternative method. Oikos 118:1883–1891

    Article  Google Scholar 

  • Queller DC, Goodnight K (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  PubMed  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, https://www.R-project.org/

  • Richardson DS, Burke T, Komdeur J (2003) Sex-specific associative learning cues and inclusive fitness benefits in the Seychelles warbler. J Evol Biol 16:854–861

    CAS  Article  PubMed  Google Scholar 

  • Russell AF, Hatchwell BJ (2001) Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate. Proc R Soc Lond B 268:2169–2174

    CAS  Article  Google Scholar 

  • Russell E, Rowley I (1988) Helper contributions to reproductive success in the splendid fairy-wren Malurus splendens. Behav Ecol Sociobiol 22:131–140

    Article  Google Scholar 

  • Russell AF, Langmore NE, Gardner JL, Kilner RM (2008) Maternal investment tactics in superb fairy-wrens. Proc R Soc Lond B 275:29–36

    CAS  Article  Google Scholar 

  • Savage JL, Russell AF, Johnstone RA (2013) Intra-group relatedness affects parental and helper investment rules in offspring care. Behav Ecol Sociobiol 67:1855–1865

    Article  Google Scholar 

  • Sharp SP, McGowan A, Wood MJ, Hatchwell BJ (2005) Learned kin recognition cues in a social bird. Nature 434:1127–1130

    CAS  Article  PubMed  Google Scholar 

  • Short LL (1972) Systematics and behavior of South American flickers (Aves: Colaptes). Bull Am Mus Nat Hist 149:1–110

    Google Scholar 

  • Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man 1871–1971. Aldine Press, Chicago, pp 136–179

    Google Scholar 

  • Whittingham LA, Robertson RJ (1994) Food availability, male parental care and mating success in red-winged blackbirds (Agelaius phoeniceus). J Anim Ecol 63:139–150

    Article  Google Scholar 

  • Wiebe KL, Elchuk CE (2003) Correlates of parental care in northern flickers: do the sexes contribute equally while provisioning young? Ardea 91:91–101

    Google Scholar 

  • Woxvold IA, Magrath MJL (2005) Helping enhances multiple components of reproductive success in the cooperatively breeding apostlebird. J Anim Ecol 74:1039–1050

    Article  Google Scholar 

  • Wright J, Dingemanse N (1999) Parents and helpers compensate for experimental changes in the provisioning effort of others in the Arabian babbler. Anim Behav 58:345–350

    CAS  Article  PubMed  Google Scholar 

  • Wright J, McDonald PG, te Marvelde L, Kazem AJN, Bishop CM (2010) Helping effort increases with relatedness in bell miners, but ‘unrelated’ helpers of both sexes still provide substantial care. Proc R Soc Lond B 277:437–445

    Article  Google Scholar 

  • Zöttl M, Fischer S, Taborsky M (2013) Partial brood care compensation by female breeders in response to experimental manipulation of alloparental care. Anim Behav 85:1471–1478

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to Debora Goedert, Marcelo Kuhlmann, Jonas Maravalhas, Isadora Oliveira, João V. Caetano, and Paula Sicsú for help with fieldwork. We thank Irby Lovette for allowing access to his lab and especially Laura Stenzler for all the support during lab work. We also thank two anonymous reviewers for their suggestions in an earlier version of the manuscript.

Funding

This study was supported by the François Vuilleumier Fund and the University of Brasília. RID was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior and the Conselho Nacional de Desenvolvimento Científico e Tecnológico through student scholarships, and RHM was supported through a CNPq research fellowship.

Author information

Authors and Affiliations

  1. Programa de Pós-Graduação em Ecologia, Universidade de Brasília, Brasília, DF, 70910-900, Brazil

    Raphael Igor Dias

  2. Faculdade de Ciências da Educação e Saúde, Centro Universitário de Brasília, Brasília, DF, 70790-075, Brazil

    Raphael Igor Dias

  3. Department of Neurobiology and Behavior and Cornell Laboratory of Ornithology, Cornell University, Ithaca, NY, 14853, USA

    Michael S. Webster

  4. Departamento de Zoologia, Universidade de Brasília, Brasília, DF, 70910-900, Brazil

    Regina H. Macedo

Authors
  1. Raphael Igor Dias
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael S. Webster
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Regina H. Macedo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Raphael Igor Dias.

Ethics declarations

All applicable international, national, and institutional guidelines for the use and capture of animals were followed. The study complied with the current laws of Brazil under permits 14368 and 2056 from Instituto Brasileiro de Recursos Renováveis.

Conflict of interest

The authors declare that they have no conflicts of interest.

Data availability

The datasets analyzed during the current study are available from the corresponding author on reasonable request.

Additional information

Communicated by J. Komdeur

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dias, R.I., Webster, M.S. & Macedo, R.H. Parental and alloparental investment in campo flickers (Colaptes campestris campestris): when relatedness comes first. Behav Ecol Sociobiol 71, 139 (2017). https://doi.org/10.1007/s00265-017-2368-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-017-2368-3

Keywords

  • Additive effect
  • Compensatory effect
  • Cooperative breeding
  • Kin selection
  • Parental care
  • Relatedness
  • Sociality