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Older can be better: physiological costs of paternal investment in the Florida scrub-jay

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Abstract

In species that undergo actuarial senescence, the value of current reproduction is predicted to increase relative to the value of future reproduction with age, as the probability of survival to another reproductive event is reduced. Therefore, life history theory predicts that aging animals should increase their investment in reproduction. However, an increase in reproductive investment may carry significant costs to the breeding individuals. We recorded provisioning rates of Florida scrub-jay male breeders, followed by their immediate capture to assess body condition and collect blood for an in vitro test of immunocompetence and an assay of baseline corticosterone for a measure of stress. Older males provisioned offspring and brooding mates at the highest rates. There was no evidence of any physiological deficits in males with high provisioning rates, independent of age. It appears that birds that survive to old age are high quality birds that maintain good physiological condition, which complements the value of experience and permits maximal investment in offspring.

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References

  • Ardia DR (2005) Individual quality mediates trade-offs between reproductive effort and immune function in tree swallows. J Anim Ecol 74:517–524. doi:10.1111/j.1365-2656.2005.00950.x

    Article  Google Scholar 

  • Bernis F (1966) Migración en aves. Sociedad Española de Ornitología, Madrid

    Google Scholar 

  • Boughton RK, Bridge ES, Schoech SJ (2007) Energetic trade-offs between immunity and reproduction in male Japanese quail (Coturnix coturnix). J Exper Zool A 307A:479–487. doi:10.1002/jez.402

    Article  CAS  Google Scholar 

  • Bryant DM, Tatner P (1991) Intraspecies variation in avian energy expenditure: correlations and constraints. Ibis 133:236–245

    Article  Google Scholar 

  • Clutton-Brock TH (1984) Reproductive effort and terminal investment in iteroparous animals. Am Nat 123:212–229

    Article  Google Scholar 

  • Coulson JC, Thomas C (1985) Differences in the breeding performance of individual kittiwake gulls, Rissa tridactyla. In: Sibley RM, Smith RH (eds) Behavioral ecology. Blackwell, Oxford, pp 489–503

    Google Scholar 

  • Daunt F, Monaghan P, Wanless S, Harris MP, Griffiths R (2001) Sons and daughters: age-specific differences in parental rearing capacities. Funct Ecol 15:211–216. doi:10.1046/j.1365-2435.2001.00515.x

    Article  Google Scholar 

  • Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252

    Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection. Dover, New York

    Google Scholar 

  • Fontaine JJ, Martin TE (2006) Parent birds assess nest predation risk and adjust their reproductive strategies. Ecol Lett 9:428–434. doi:10.1111/j.1461-0248.2006.00892.x

    Article  CAS  PubMed  Google Scholar 

  • Green AJ (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82:1473–1483. doi:10.1890/0012-9658(2001)082[1473:MLRMOB]2.0.CO;2

    Article  Google Scholar 

  • Gustafsson L, Sunderland WJ (1988) The costs of reproduction in the collared flycatcher Ficedula albicollis. Nature 375:311–313

    Article  Google Scholar 

  • Haussmann MF, Winkler DW, Huntington CE, Vleck D, Sanneman CE, Hanley D, Vleck CM (2005) Cell-mediated immunosenescence in birds. Oecologia 145:270–275. doi:10.1007/s00442-005-0123-3

    Article  PubMed  Google Scholar 

  • Ilmonen P, Taarna T, Hasselquist D (2002) Are incubation costs in female pied flycatchers expressed in humoral immune responsiveness or breeding success? Oecologia 130:199–204. doi:10.1007/s004420100804

    Google Scholar 

  • Ilmonen P, Hasselquist D, Langefors A, Wiehn J (2003) Stress, immunocompetence and leukocyte profiles of pied flycatchers in relation to brood size manipulation. Oecologia 136:148–154. doi:10.1007/s00442-003-1243-2

    Article  PubMed  Google Scholar 

  • Ketterson ED, Nolan V Jr (1992) Hormones and life histories: an integrative approach. Am Nat 140:533–562

    Article  Google Scholar 

  • Kokko H (1998) Good genes, old age and life-history trade-offs. Evol Ecol 12:739–750

    Article  Google Scholar 

  • Landau S, Everitt BS (2003) A handbook of statistical analysis using SPSS. Chapman & Hall/CRC, Boca Raton

    Book  Google Scholar 

  • Legge S (2000) Helper contributions in the cooperatively breeding laughing kookaburra: feeding young is no laughing matter. Anim Behav 59:1009–1018. doi:10.1046/j.1365-2656.2000.00429.x

    Article  PubMed  Google Scholar 

  • Love OP, Breuner CW, Vezina F, Williams TD (2004) Mediation of a corticosterone-induced reproductive conflict. Horm Behav 46:59–65. doi:10.1016/j.yhbeh.2004.02.001

    Article  CAS  PubMed  Google Scholar 

  • Love OP, Salvante KG, Dale J, Williams TD (2008) Sex-specific variability in the immune system across life-history stages. Am Nat 172:E99–E112. doi:10.1086/589521

    Article  PubMed  Google Scholar 

  • Maigret JL, Murphy MT (1997) Costs and benefits of parental care in eastern kingbirds. Behav Ecol 8:250–259. doi:10.1093/beheco/8.3.250

    Article  Google Scholar 

  • Martin K (1995) Patterns and mechanisms for age-dependent reproduction and survival in birds. Am Zool 35:340–348

    Google Scholar 

  • Matson KD, Tieleman BI, Klasing KC (2006) Capture stress and the bactericidal competence of blood and plasma in five species of tropical birds. Phys Biochem Zool 79:556–564. doi:10.1086/501057

    Article  Google Scholar 

  • McDonald DB, Fitzpatrick JW, Woolfenden GE (1996) Actuarial senescence and demographic heterogeneity in the Florida scrub jay. Ecology 77:2373–2381. doi:10.2307/2265739

    Article  Google Scholar 

  • McGowan KJ, Woolfenden GE (1990) Contributions to fledgling feeding in the Florida scrub jay. J Anim Ecol 59:691–707

    Article  Google Scholar 

  • Millet S, Bennett J, Lee KA, Hau M, Klasing KC (2007) Quantifying and comparing constitutive immunity across avain species. Dev Comp Immun 31:188–201. doi:10.1016/j.dci.2006.05.013

    Article  CAS  Google Scholar 

  • Monaghan P, Charmantier A, Nussey DH, Ricklefs RE (2008) The evolutionary ecology of senescence. Funct Ecol 22:371–378. doi:10.1111/j.1365-2435.2008.01418.x

    Article  Google Scholar 

  • Mumme RL (1992) Do helpers increase reproductive success? Behav Ecol Sociobiol 31:319–328

    Article  Google Scholar 

  • Murphy MT, Armbrecht B, Vlamis E, Pierce A (2000) Is reproduction by tree swallows cost free? Auk 117:902–212. doi:10.1642/0004-8038(2000)117[0902:IRBTSC]2.0.CO;2

    Article  Google Scholar 

  • Orians GH (1969) Age and hunting success in the brown pelican (Pelicanus occidentalis). Anim Behav 17:316–319

    Article  Google Scholar 

  • Owens IPF, Bennett PM (1994) Mortality costs of parental care and sexual dimorphism in birds. Proc R Soc B 257:1–8. doi:10.1098/rspb.1994.0086

    Article  Google Scholar 

  • PASW Inc (2009) PASW advanced models 17.0. SPSS Inc, Chicago

    Google Scholar 

  • Quinn JS, Woolfenden GE, Fitzpatrick JW, White BN (1999) Multi-locus DNA fingerprinting supports genetic monogamy in Florida scrub-jays. Behav Ecol Sociobiol 45:1–10. doi:10.1007/s002650050534

    Article  Google Scholar 

  • Ratcliffe N, Furness RW, Hamer KC (1998) The interactive effects of age and food supply on the breeding ecology of great skuas. J Anim Ecol 67:853–862. doi:10.1046/j.1365-2656.1998.6760853.x

    Article  Google Scholar 

  • Reid WV (1987) The cost of reproduction in the glaucous-winged gull. Oecologia 74:458–467

    Article  Google Scholar 

  • Reid JM, Bignal EM, McCracken DJ, Monaghan P (2003) Age-specific reproductive performance in red-billed choughs Pyrrhocorax pyrrhocorax: patterns and processes in a natural population. J Anim Ecol 72:765–776. doi:10.1046/j.1365-2656.2003.00750.x

    Article  Google Scholar 

  • Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468. doi:10.1016/S0169-5347(02)02578-8

    Article  Google Scholar 

  • Sapolsky RM, Romero L, Munch A (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89. doi:10.0163-769X/00

    Article  CAS  PubMed  Google Scholar 

  • Schoech SJ (1996) The effect of supplemental food on body condition and the timing of reproduction in a cooperative breeder, the Florida scrub-jay (Aphelocoma coerulescens). Condor 98:234–244

    Article  Google Scholar 

  • Schoech SJ (2009) Food supplementation experiments: a tool to reveal mechanisms that mediate timing of breeding. Integr Comp Biol 49:480–492. doi:10.1093/icb/icp005

    Article  CAS  Google Scholar 

  • Schoech SJ, Mumme RL, Wingfield JC (1996) Prolactin and helping behavior in the cooperatively breeding Florida Scrub-Jay, Aphelocoma coerulescens. Anim Behav 52:445–456

    Article  Google Scholar 

  • Schoech SJ, Bowman R, Bridge ES, Boughton RK (2007) Baseline and acute levels of corticosterone in Florida scrub-jays (Aphelocoma coerulescens): effects of food supplementation, suburban habitat, and year. Gen Comp Endocr 154:150–160. doi:10.1016/j.ygcen.2007.05.027

    Article  CAS  PubMed  Google Scholar 

  • Silverin B (1982) Endocrine correlates of brood size in pied flycatchers Ficedula hypoleuca. Gen Comp Endocr 47:18–23

    Article  CAS  PubMed  Google Scholar 

  • Silverin B (1986) Corticosterone-binding proteins and behavior effects of high plasma levels of corticosterone during the breeding period in the pied flycatcher. Gen Comp Endocr 64:67–74

    Article  CAS  PubMed  Google Scholar 

  • Smith HG, Kallander H, Nilsson JA (1989) The trade-off between offspring number and quality in the great tit Parus major. J Anim Ecol 58:383–401

    Article  Google Scholar 

  • Stallcup JA, Woolfenden GE (1978) Family status and contribution to breeding by Florida scrub-jays. Anim Behav 26:1144–1156

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • 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. doi:10.1016/j.anbehav.2005.06.021

    Article  Google Scholar 

  • Velando A, Drummond H, Torres R (2006) Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis. Proc R Soc B 273:1443–1448. doi:10.1098/rspb.2006.3480

    Article  PubMed  Google Scholar 

  • Viney ME, Riley EM, Buchanan KL (2005) Optimal immune responses: immunocompetence revisited. Trends Ecol Evol 20:665–669. doi:10.1016/j.tree.2005.10.003

    Article  PubMed  Google Scholar 

  • Wilcoxen TE, Boughton RK, Schoech SJ (2010) Selection on innate immunity and body condition in Florida scrub-jays throughout an epidemic. Biol Lett. doi: 10.1098/rsbl.2009.1078

  • Williams GC (1966) Natural selection, the costs of reproduction and a refinement of Lack’s principle. Am Nat 100:687–692

    Article  Google Scholar 

  • Williams TD (2005) Mechanisms underlying costs of egg production. Bioscience 55:39–48. doi:10.1641/0006-3568(2005)055[0039:MUTCOEJ2.0.CO;2

    Article  Google Scholar 

  • Wingfield JC (1994) Modulation of the adrenocortical response to stress in birds. In: Davey KG, Peter RE, Tobe SS (eds) Perspective in comparative endocrinology. Springer, Ottawa, pp 520–528

    Google Scholar 

  • Wingfield JC, Farner DS (1976) Avian endocrinology—field investigations and methods. Condor 78:570–573

    Article  Google Scholar 

  • Woolfenden GE, Fitzpatrick JW (1984) The Florida scrub jay: demography of a cooperatively-breeding bird. Princeton University Press, Princeton

    Google Scholar 

  • Woolfenden GE, Fitzpatrick JW (1996) Florida scrub-jay (Aphelocoma coerulescens). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca. doi:10.2173/bna.228

    Google Scholar 

  • Woolfenden GE, Fitzpatrick JW (1998) Bird Research. Archbold Biological Station Biennial Report, 1997–1998

  • Wunderle JM Jr (1991) Age-specific foraging proficiency in birds. Curr Ornithol 8:273–324

    Google Scholar 

  • Zera AJ, Potts J, Kobus K (1998) The physiology of life-history trade-offs: experimental analysis of a hormonally induced life-history trade-off in Gryllus assimilis. Am Nat 152:7–23. doi:10.1086/286146

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank everyone at Archbold Biological Station for continued hospitality and support, particularly R Bowman. We are greatly indebted to MA Rensel and ES Bridge for their leadership and numerous contributions throughout the long field seasons. Furthermore, we thank GM Morgan, MA Desrosiers, and ZD Seilo for their hard work in the field and MD Venesky for cooking breakfast. This work was supported by the National Science Foundation (IBN-034632 to SJS, IBN-0508418 to RKB and SJS, and IOS-0909620, to TEW and SJS), Sigma Xi (Grant-in-Aid of Research to TEW), the American Ornithologists’ Union (Josselyn Van Tyne Student Research Award to TEW), and the Florida Ornithological Society (Cruickshank Research Award to TEW). TEW was also supported by a Van Vleet Memorial Fellowship from the College of Arts and Sciences at the University of Memphis during the course of this research. The experiments in this work comply with the current laws of the United States of America and all methods were approved by the University of Memphis Institutional Animal Care and Use Committee.

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The authors declare that they have no conflict of interest.

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Correspondence to Travis E. Wilcoxen.

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Communicated by C. Brown

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Wilcoxen, T.E., Boughton, R.K. & Schoech, S.J. Older can be better: physiological costs of paternal investment in the Florida scrub-jay. Behav Ecol Sociobiol 64, 1527–1535 (2010). https://doi.org/10.1007/s00265-010-0966-4

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