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How do helpers help? Helper contributions throughout the nesting cycle in the cooperatively breeding brown-headed nuthatch

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Abstract

Breeder investment in offspring reflects a trade-off between the benefits realized from current reproductive efforts and the benefits expected from future reproductive opportunities. When assisted by nonbreeding helpers that provide care for offspring, breeders may modify reproductive investments to minimize the costs of producing offspring, or in ways that maximize productivity and offspring survival. How helpers assist breeders can vary with different stages of reproduction, and how breeders alter investment in response to helpers may change depending on the stage of reproduction. We assessed how helpers contribute to reproduction and how breeders alter their investment in response to helper contributions in the cooperatively breeding brown-headed nuthatch (Sitta pusilla). We assessed helper contributions across three stages of reproduction: (1) nest excavation, (2) maternal egg production, and (3) nestling care and development at days 8–12 post-hatching, a period of rapid nestling growth. We also investigated how breeders responded to helper contributions and the relationship of helper behavior with breeders’ reproductive success. Helpers contributed to offspring care but not nest excavation. Breeders assisted by helpers did not alter investments in nest excavation, offspring production, or offspring care. As a result, offspring raised by cooperative groups received more food and weighed more. Nests with helpers were more likely to fledge at least one offspring, even when considering variation in territory characteristics and breeder experience. Results indicate breeders likely benefit from the favorable breeding conditions helpers provided for current breeding efforts, which influenced the quality of offspring produced and their likelihood of fledging in this study.

Significance statement

Helpers may contribute to breeders’ reproductive effort during many stages of reproduction. The presence of nonbreeding helpers should therefore influence the investments made by breeders during different stages of breeding. Investment decisions in one stage should furthermore influence later investment decisions. We demonstrated that helpers assisted breeders primarily during the offspring rearing stage in brown-headed nuthatches (Sitta pusilla), a facultative cooperative breeder. Breeders with helpers maintained their level of investments in offspring similar to the investments documented for breeders without helpers. As a result, chicks in nests with helpers received more food and were heavier, and adults with helpers were more likely to fledge at least one young. Our results suggest that the combined effects of parental and helper investment provided benefits for current broods with potentially important survival consequences for offspring.

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References

  • Arnold TW (2010) Uninformative parameters and model selection using Akaike’s information criterion. J Wildlife Manag 74:1175–1178. https://doi.org/10.2193/2009-367

    Article  Google Scholar 

  • Balshine-Earn S, Neat FC, Reid H, Taborsky M (1998) Paying to stay or paying to breed? Field evidence for direct benefits of helping behavior in a cooperatively breeding fish. Behav Ecol 9:432–438. https://doi.org/10.1093/beheco/9.5.432

    Article  Google Scholar 

  • Baran NM, Adkins-Regan E (2014) Breeding experience, alternative reproductive strategies and reproductive success in a captive colony of zebra finches (Taeniopygia guttata). PLoS One 9:e89808. https://doi.org/10.1371/journal.pone.0089808

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bates D, Maechler M, Bolker BM, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R Package Version 11-7, http://cran.r-project.org/package=lme4

  • Becker RA, Chambers JM, Wilks AR (1988) The new S language: a programming environment for data analysis and graphics. Wadsworth & Brooks/Cole, Pacific Grove

    Google Scholar 

  • Bednekoff PA (1997) Mutualism among safe, selfish sentinels: a dynamic game. Am Nat 150:373–392

    Article  PubMed  CAS  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Burnham KP, Anderson DR, Huyvaert KP (2010) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35. https://doi.org/10.1007/s00265-010-1029-6

    Article  Google Scholar 

  • Canestrari D, Marcos JM, Baglione V (2011) Helpers at the nest compensate for reduced maternal investment in egg size in carrion crows. J Evol Biol 24:1870–1878. https://doi.org/10.1111/j.1420-9101.2011.02313.x

    Article  PubMed  CAS  Google Scholar 

  • Carranza J, Polo V, Valencia J, Mateo C, de la Cruz C (2008) How should breeders react when aided by helpers? Anim Behav 75:1535–1542

    Article  Google Scholar 

  • Clutton-Brock TH, Hodge SJ, Spong G, Russell AF, Jordan NR, Bennett NC, Sharpe LL, Manswer MB (2006) Intrasexual competition and sexual selection in cooperative mammals. Nature 444:1065–1068

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Cox JA, McCormic JK (2016) New insights from an attempt to reintroduce red-cockaded woodpeckers in northern Florida. J Field Ornithol 87:360–379

    Article  Google Scholar 

  • Cox JA, Slater GL (2007) Cooperative breeding in the brown-headed nuthatch. Wilson J Ornithol 119:1–8

    Article  Google Scholar 

  • Crawford RL, Brueckheimer WR (2012) The legacy of a red hills hunting plantation: Tall Timbers Research Station and Land Conservancy. University Press of Florida, Gainesville

    Google Scholar 

  • Cunningham EJA, Russell AF (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–77

    Article  PubMed  CAS  Google Scholar 

  • Dias RI, Webster MS, Macedo RH (2015) Helping enhances productivity in campo flicker (Colaptes campestris) cooperative groups. Naturwissenschaften 102:31. https://doi.org/10.1007/s00114-015-1281-8

    Article  PubMed  CAS  Google Scholar 

  • Dornak LL, Burt DB, Coble DW, Connor RN (2004) Relationships between habitat and snag characteristics and the reproductive success of the brown-headed nuthatch (Sitta pusilla) in eastern Texas. Southeast Nat 3:683–694

    Article  Google Scholar 

  • Engstrom RT (1992) Characteristic birds and mammals of longleaf pine forests. Proc Tall Timbers Fire Ecol Conf 18:127–138

    Google Scholar 

  • Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder MN, Nielsen A, Sibert J (2012) AD model builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249

    Article  Google Scholar 

  • Fox C, Thaker M, Mousseau T (1997) Egg size plasticity in a seed beetle: an adaptive maternal effect. Am Nat 149:149–163

    Article  Google Scholar 

  • Fridolfsson A, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121

    Article  Google Scholar 

  • Germain RR, Arcese P (2014) Distinguishing individual quality from habitat preference and quality in a territorial passerine. Ecology 95:436–445

    Article  PubMed  Google Scholar 

  • Gotmark F (2002) Predation by sparrowhawks favours early breeding and small broods in great tits. Oecologia 130:25–32. https://doi.org/10.1007/s004420100769

    Article  PubMed  Google Scholar 

  • Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711. https://doi.org/10.1111/j.1420-9101.2010.02210.x

    Article  PubMed  CAS  Google Scholar 

  • Haas SE, Cox JA, Smith JV, Kimball RT (2010) Fine-scale spatial genetic structure in the cooperatively breeding brown-headed nuthatch (Sitta pusilla). Southeast Nat 9:743–756. https://doi.org/10.1656/058.009.0409

    Article  Google Scholar 

  • Han K, Cox JA, Kimball RT (2015) Uncommon levels of relatedness and parentage in a cooperatively breeding bird, the brown-headed nuthatch (Sitta pusilla). Wilson J Ornithol 127:593–600

    Article  Google Scholar 

  • Hannah TI, Tirpak JM, Walthen G, Loman ZG, Evans DL, Rush SA (2017) Influence of landscape- and stand-scale factors on avian communities to aid in open pine restoration. For Ecol Manag 384:389–399

    Article  Google Scholar 

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

    Article  PubMed  CAS  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 

  • Herenyi M, Garamszegi LZ, Hargitai R, Hegyi G, Rosivall B, Szollosi E, Torok J (2014) Laying date and polygyny as determinants of annual reproductive success in male collared flycatchers (Ficedula albicollis): a long-term study. Naturwissenschaften 101:305–312. https://doi.org/10.1007/s00114-014-1157-3

    Article  PubMed  CAS  Google Scholar 

  • Hoyt DF (1979) Practical methods of estimating volume and fresh weight of bird eggs. Auk 96:73–77

    Google Scholar 

  • Ibarzabal J, Tremblay JA (2006) The hole saw method for accessing woodpecker nestlings during developmental studies. Ann Zool Fenn 43:235–238. https://doi.org/10.2307/23735934

    Article  Google Scholar 

  • Innes KE, Johnston RE (1996) Cooperative breeding in the white-throated magpie-jay. How do auxiliaries influence nesting success? Anim Behav 51:519–533. https://doi.org/10.1006/anbe.1996.0057

    Article  Google Scholar 

  • Jones JA, Harris MR, Siefferman L (2014) Physical habitat quality and interspecific competition interact to influence territory settlement and reproductive success in a cavity nesting bird. Front Ecol Evol 2:71. https://doi.org/10.3389/fevo.2014.00071

    Article  Google Scholar 

  • Langen TA, Vehrencamp SL (1999) How white-throated magpie-jay helpers contribute during breeding. Auk 116:131–140. https://doi.org/10.2307/4089460

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JD, Slater GL (2007) Environmental factors affecting productivity of brown-headed nuthatches. J Wildlife Manag 71:1968–1975. https://doi.org/10.2193/2006-384

    Article  Google Scholar 

  • Lloyd JD, Slater GL, Snow S (2009) Demography of reintroduced eastern bluebirds and brown-headed nuthatches. J Wildlife Manag 73:955–964. https://doi.org/10.2193/2008-009

    Article  Google Scholar 

  • Magrath RD (1991) Nestling weight and juvenile survival in the blackbird (Turdus merula). J Anim Ecol 60:335–351

    Article  Google Scholar 

  • Magrath RD (2001) Group breeding dramatically increases reproductive success of yearlings but not older female scrubwrens: a model for cooperatively breeding birds? J Anim Ecol 70:370–385

    Article  Google Scholar 

  • Martin TE (1993) Evolutionary determinants of clutch size in cavity-nesting birds: nest predation or limited breeding opportunities. Am Nat 142:937–946

    Article  PubMed  CAS  Google Scholar 

  • Martin TE, Scott J, Menge C (2000) Nest predation increases with parental activity: separating nest site and parental activity effects. Proc R Soc Lond B 267:2287–2293. https://doi.org/10.1098/rspb.2000.1281

    Article  CAS  Google Scholar 

  • Marvelde LT, McDonald PGM, Kazem AJN, Wright J (2009) Do helpers really help? Provisioning biomass and prey type effects on nestling growth in the cooperative bell miner. Anim Behav 77:727–735. https://doi.org/10.1016/j.anbehav.20

    Article  Google Scholar 

  • Mullin SJ, Cooper RJ (1998) The foraging ecology of the gray rat snake (Elaphe obsoleta spiloides)—visual stimuli facilitate location of arboreal prey. Am Midl Nat 140:397–401

    Article  Google Scholar 

  • Mumme RL, Koenig WD, Pitelka FA (1990) Individual contributions to cooperative nest care in the acorn woodpecker. Condor 92:360–368

    Article  Google Scholar 

  • Mumme RL, Bowman R, Pruett MS, Fitzpatrick JW (2015) Natal territory size, group size, and body mass affect lifetime fitness in the cooperatively breeding Florida scrub-jay. Auk 132:634–646. https://doi.org/10.1642/auk-14-258.1

    Article  Google Scholar 

  • Nakagawa S, Freckleton RP (2010) Model averaging, missing data and multiple imputation: a case study for behavioural ecology. Behav Ecol Sociobiol 65:103–116

    Article  Google Scholar 

  • Nol E, James NMS (1987) Effects of age and breeding experience on seasonal reproductive success in the song sparrow. J Anim Ecol 56:301–313. https://doi.org/10.2307/4816

    Article  Google Scholar 

  • Norris RA (1958) Comparative biosystematics and life history of the nuthathes, Sitta pygmaea and Sitta pusilla. Univ Calif Publ Zool 56:119–300

    Google Scholar 

  • Paquet M, Covas R, Chastel O, Parenteau C, Doutrelant C (2013) Maternal effects in relation to helper presence in the cooperatively breeding sociable weaver. PLoS One 8:e59336. https://doi.org/10.1371/journal.pone.0059336

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Paquet M, Doutrelant C, Hatchwell BJ, Spottiswoode CN, Covas R (2015) Antagonistic effect of helpers on breeding male and female survival in a cooperatively breeding bird. J Anim Ecol 84:1354–1362. https://doi.org/10.1111/1365-2656.12377

    Article  PubMed  PubMed Central  Google Scholar 

  • Perrins CM (1970) The timing of birds’ breeding seasons. Ibis 112:242–255. https://doi.org/10.1111/j.1474-919X.1970.tb00096.x

    Article  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/

  • Russell AF, Lummaa V (2009) Maternal effects in cooperative breeders: from hymenopterans to humans. Philos Trans R Soc Lond B Biol Sci 364:1143–1167. https://doi.org/10.1098/rstb.2008.0298

    Article  PubMed  PubMed Central  Google Scholar 

  • Russell AF, Langmore NE, Cockbur AP, Astheimer LB, Kilner RM (2007) Reduced egg investment can conceal helper effects in cooperatively breeding birds. Science 317:941–944

    Article  PubMed  CAS  Google Scholar 

  • Saino N, Romano M, Ambrosini R, Rubolini D, Boncoraglio G, Caprioli M, Romano A (2012) Longevity and lifetime reproductive success of barn swallow offspring are predicted by their hatching date and phenotypic quality. J Anim Ecol 81:1004–1012. https://doi.org/10.1111/j.1365-2656.2012.01989.x

    Article  PubMed  Google Scholar 

  • Santos SA, Macedo RH (2011) Load lightening in southern lapwings: group-living mothers lay smaller eggs than pair-living mothers. Ethology 117:547–555. https://doi.org/10.1111/j.1439-0310.2011.01905.x

  • Savage JL, Russell AF, Johnstone RA (2012) Maternal costs in offspring production affect investment rules in joint rearing. Behav Ecol 24:750–758. https://doi.org/10.1093/beheco/ars203

    Article  Google Scholar 

  • Savage JL, Russell AF, Johnstone RA (2015) Maternal allocation in cooperative breeders: should mothers match or compensate for expected helper contributions? Anim Behav 102:189–197. https://doi.org/10.1016/j.anbehav.2015.01.015

    Article  Google Scholar 

  • Schiegg K, Pasinelli G, Walters JR, Daniels SJ (2002) Inbreeding and experience affect response to climate change by endangered woodpeckers. Proc R Soc Lond B 269:1153–1159. https://doi.org/10.1098/rspb.2002.1966

    Article  Google Scholar 

  • Siikamäki P (1998) Limitation of reproductive success by food availability and breeding time in pied flycatchers. Ecology 79:1789–1796. https://doi.org/10.1890/0012-9658(1998)079[1789:LORSBF]2.0.CO;2

  • Skaug HJ, Fournier DA, Bolker BM, Magnusson A, Nielsen A (2015) Generalized linear mixed models using AD model builder. R Package Version 0.81, http://glmmadmb.r-forge.r-project.org, http://admb-project.org

  • Slater GL (1997) Brown-headed nuthatches and eastern bluebirds in southern Florida pinelands: breeding biology, nest-site selection, and the influence of habitat on nesting success. MSc thesis, University of Florida

  • Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21. https://doi.org/10.1007/s00265-010-1037-6

    Article  Google Scholar 

  • Taborsky B, Skubic E, Bruintjes R (2007) Mothers adjust egg size to helper number in a cooperatively breeding cichlid. Behav Ecol 18:652–657. https://doi.org/10.1093/beheco/arm026

    Article  Google Scholar 

  • Thompson TK (2000) Breeding biology and the nature and importance of helper contributions in the cooperative breeding brown-headed nuthatch in a Texas urban population. MSc thesis, Stephen F. Austin State University

  • Valencia J, De La Cruz C, Carranza J, Mateos C (2006) Parents increase their parental effort when aided by helpers in a cooperatively breeding bird. Anim Behav 71:1021–1028. https://doi.org/10.1016/j.anbehav.2005.06.021

    Article  Google Scholar 

  • Valencia J, Mateos C, De La Cruz C, Carranza J (2017) Maternal allocation in eggs when counting on helpers in a cooperatively breeding bird. J Avian Biol 48:536–543

    Article  Google Scholar 

  • Williams G (1966) Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am Nat 100:687–690

    Article  Google Scholar 

  • Yasukawa K, Cockburn A (2009) Antipredator vigilance in cooperatively breeding superb fairy-wrens (Malurus cyaneus). Auk 126:147–154. https://doi.org/10.1525/auk.2009.08074

    Article  Google Scholar 

  • Zuur AF, Leno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R, statistics for biology and health. Springer-Verlag, New York

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Acknowledgments

Many volunteers and field assistants contributed to the fieldwork for this long-term study. Special thanks to A. Janik, A. Kreuser, J. Botero, D. McElveen, M. Gray, E. Schunke, A. Doyle, D. Pavlik, B. Williams, D. Smith, and H. Levy for exceptional fieldwork. The authors thank the editor and anonymous reviewers for their helpful suggestions and comments on the manuscript.

Funding

Funding was provided by the Florida State University Brenda Weems Bennison Endowment, the Florida State University Robert B. Short Zoology Scholarship, and the Wildlife Research Endowment at Tall Timbers Research Station. JAC was supported in part by a fellowship from Tall Timbers Research Station. EHD was supported in part by NSF grant 1453408.

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Authors and Affiliations

  1. Department of Biological Science, Florida State University, 319 Stadium Drive, Tallahassee, FL, 32306, USA

    Jessica A. Cusick, Miguel de Villa & Emily H. DuVal

  2. Tall Timbers Research Station and Land Conservancy, 13093 Henry Beadel Dr., Tallahassee, FL, 32312, USA

    Jessica A. Cusick & James A. Cox

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  1. Jessica A. Cusick
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  2. Miguel de Villa
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Correspondence to Jessica A. Cusick.

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Ethical statement

All applicable national and institutional guidelines for the care and use of animals were followed. All procedures performed were in accordance with the ethical standards approved by the Florida State University Animal Care and Use Committee (protocol 1505) and by the Tall Timbers Institutional Animal Care and Use Committee (protocol 1042). There has been no evidence of any effects of marking, handling, nest monitoring, or methodology on the behavior and survival of individuals in the study population.

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Communicated by S. Pruett-Jones

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Cusick, J.A., de Villa, M., DuVal, E.H. et al. How do helpers help? Helper contributions throughout the nesting cycle in the cooperatively breeding brown-headed nuthatch. Behav Ecol Sociobiol 72, 43 (2018). https://doi.org/10.1007/s00265-018-2470-1

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