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Individual variation in workload during parental care: can we detect a physiological signature of quality or cost of reproduction?

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Abstract

How hard do birds work during parental care, chick rearing, or provisioning of their nestlings? And if birds do work hard, can we detect a physiological signature of individual variation in workload ability (perhaps related to ‘quality’) or costs associated with high workload? Here, we provide a broad conceptual perspective on these questions. Life-history theory predicts (or requires) that (1) parental care is hard work, (2) individuals that invest more in parental care benefit in terms of rearing more, larger, fitter offspring, but that (3) increased investment in parental care comes at a cost: decreased future fecundity and/or survival. However, we start by highlighting studies that are inconsistent with this conventional view, e.g., (1) females often do not pay a survival cost of increased workload (though males do), (2) some (high quality?) individuals appear to maximise numerous life-history traits, and (3) workload during parental care often does not predict productivity. We suggest that an “exercise physiology” perspective on parental care might be informative, but highlight the fact that existing models of exercise often involve conditions very different from that free-living animals experience while foraging (e.g., using forced exercise) and are often divorced from the critical relationship in free-living animals between exercise and acquisition of resources. We briefly review studies looking at physiological effects of workload during parental care in free-living birds, but again highlight our surprising lack of knowledge in this area especially where experimental manipulation of workload is coupled with comprehensive, physiological analysis. Finally, we make three recommendations for how can we advance the study of physiology of parental care in chick-rearing birds: (1) experimental manipulation of workload, (2) obtaining better measures of workload, for large numbers of known-individuals, and (3) better assessment of physiology of individual quality, and identification of specific metrics of workload-induced ‘wear and tear’.

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References

  • Adamo SA (2004) How should behavioral ecologists interpret measurements of immunity? Anim Behav 68:1443–1449

    Article  Google Scholar 

  • Bijleveld AI, Mullers RHE (2009) Reproductive effort in biparental care: an experimental study in long-lived Cape gannets. Behav Ecol 20:736–744. doi:10.1093/beheco/arp054

    Article  Google Scholar 

  • Borer KT (2003) Exercise endocrinology. Human Kinetics, Champagne

    Google Scholar 

  • Buehler DM, Vezina F, Goymann W, Schwabl I, Versteegh M, Tieleman BI, Piersma T (2012) Independence among physiological traits suggests flexibility in the face of ecological demands on phenotypes. J Evol Biol 25:1600–1613. doi:10.1111/j.1420-9101.2012.02543.x

    Article  PubMed  CAS  Google Scholar 

  • Burness GP, Ydenberg RC, Hochachka PW (1998) Interindividual variability in body composition and resting oxygen consumption rate in breeding tree swallows, Tachycineta bicolor. Physiol Zool 71:247–256

    Article  PubMed  CAS  Google Scholar 

  • Burnett NJ, Hinch SG, Braun DC, Casselman MT, Middleton CT, Wilson SM, Cooke SJ (2014) Burst swimming in areas of high flow: delayed consequences of anaerobiosis in wild adult sockeye salmon. Physiol Biochem Zool 87:587–598. doi:10.1086/677219

    PubMed  Google Scholar 

  • Clutton-Brock TH (1988) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago

    Google Scholar 

  • Daan S, Deerenberg C, Dijkstra C (1996) Increased daily work precipitates natural death in the kestrel. J Anim Ecol 65:539–544

    Article  Google Scholar 

  • Dawson RD, Bortolotti GR (2003) Parental effort of American kestrels: the role of variation in brood size. Can J Zool 81:852–860

    Article  Google Scholar 

  • Dijkstra C, Bult A, Bijlsma S, Daan S, Meijer T, Zijlstra M (1990) Brood size manipulations in the kestrel (falco tinnunculus)—effects on offspring and parent survival. J Anim Ecol 59:269–285

    Article  Google Scholar 

  • Dor R, Lotem A (2010) Parental effort and response to nestling begging in the house sparrow: repeatability, heritability and parent-offspring coevolution. J Evol Biol 23:1605–1612

    Article  PubMed  CAS  Google Scholar 

  • Drent R (2006) The timing of birds’ breeding seasons: the Perrin’s hypothesis revisited especially for migrants. Ardea 94:305–322

    Google Scholar 

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

    Google Scholar 

  • Duclos M (2008) A critical assessment of hormonal methods used in monitoring training status in athetes. Int Sports Med J 9:56–66

    Google Scholar 

  • Eliason EJ et al (2011) Differences in thermal tolerance among sockeye salmon populations. Science 332:109–112. doi:10.1126/science.1199158

    Article  PubMed  CAS  Google Scholar 

  • Elliott KH, Le Vaillant M, Kato A, Speakman JR, Ropert-Coudert Y (2013) Accelerometry predicts daily energy expenditure in a bird with high activity levels. Biol Lett. doi:10.1098/rsbl.2012.0919

    PubMed  PubMed Central  Google Scholar 

  • Elliott KH et al (2014) Age-related variation in energy expenditure in a long-lived bird within the envelope of an energy ceiling. J Anim Ecol 83:136–146. doi:10.1111/1365-2656.12126

    Article  PubMed  Google Scholar 

  • Fonseca IAT et al (2014) Exercising for food: bringing the laboratory closer to nature. J Exp Biol 217:3274–3282. doi:10.1242/jeb.108191

    Article  PubMed  Google Scholar 

  • Frost PC, Song K, Wagner ND (2014) A beginner’s guide to nutritional profiling in physiology and ecology. Integr comp Biolo 54:873–879. doi:10.1093/icb/icu054

    Article  Google Scholar 

  • García-Navas V, Sanz JJ (2010) flexibility in the foraging behavior of blue tits in response to short-term manipulations of brood size. Ethology 116:744–754

    Google Scholar 

  • Garcia-Navas V, Ferrer ES, Sanz JJ (2012) Prey selectivity and parental feeding rates of Blue Tits (Cyanistes caeruleus) in relation to nestling age. Bird Study 59:236–242

    Article  Google Scholar 

  • Garland T et al (2011a) How to run far: multiple solutions and sex-specific responses to selective breeding for high voluntary activity levels. Proc R Soc Lond B 278:574–581. doi:10.1098/rspb.2010.1584

    Article  Google Scholar 

  • Garland T et al (2011b) The biological control of voluntary exercise, spontaneous physical activity and daily energy expenditure in relation to obesity: human and rodent perspectives. J Exp Biol 214:206–229

    Article  PubMed  PubMed Central  Google Scholar 

  • Girard I, Swallow JG, Carter PA, Koteja P, Rhodes JS, Garland T Jr (2002) Maternal-care behavior and life-history traits in house mice (Mus domesticus) artificially selected for high voluntary wheel-running activity. Behav Proc 57:37–50. doi:10.1016/S0376-6357(01)00206-6

    Article  Google Scholar 

  • Guindre-Parker S, Baldo S, Gilchrist HG, Macdonald CA, Harris CM, Love OP (2013) The oxidative costs of territory quality and offspring provisioning. J Evol Biol 26:2558–2565. doi:10.1111/jeb.12256

    Article  PubMed  CAS  Google Scholar 

  • Harshman LG, Zera AJ (2007) The cost of reproduction: the devil in the details. Trends Ecol Evol 22:80–88

    Article  PubMed  Google Scholar 

  • Hegemann A, Matson K, Flinks H, Tieleman B (2013) Offspring pay sooner, parents pay later: experimental manipulation of body mass reveals trade-offs between immune function, reproduction and survival. Front Zool 10:77

    Article  PubMed  PubMed Central  Google Scholar 

  • Horak P, Jenni-Eiermann S, Ots I (1999) Do great tits (Parus major) starve to reproduce? Oecologia 119:293–299

    Article  Google Scholar 

  • Horváthová T, Nakagawa S, Uller T (2012) Strategic female reproductive investment in response to male attractiveness in birds. Proc R Soc Lond B 279:163–170. doi:10.1098/rspb.2011.0663

    Article  Google Scholar 

  • Hug M, Mullis PE, Vogt M, Ventura N, Hoppeler H (2003) Training modalities: over-reaching and over-training in athletes, including a study of the role of hormones. Best Prac Res Clin Endocrinol Metab 17:191–209. doi:10.1016/S1521-690X(02)00104-5

    Article  CAS  Google Scholar 

  • Husak JF (2006) Does survival depend on how fast you can run or how fast you do run? Funct Ecol 20:1080–1086

    Article  Google Scholar 

  • Irschick DJ (2003) Studying performance in nature: implications for fitness variation within populations. Integr Comp Biol 43:396–407

    Article  PubMed  Google Scholar 

  • Jacobs SR, Elliott KH, Gaston AJ (2013) parents are a drag: long-lived birds share the cost of increased foraging effort with their offspring, but males pass on more of the costs than females. PLoS ONE 8:e54594. doi:10.1371/journal.pone.0054594

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Joyner MJ, Coyle EF (2008) Endurance exercise performance: the physiology of champions. J Physiol 586:35–44. doi:10.1113/jphysiol.2007.143834

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Keil D, Lubke RW, Pruett SB (2001) Quantifying the relationship between multiple immunological parameters and host resistance: probing the limits of reductionism. J Immunol 167:4543–4552

    Article  PubMed  CAS  Google Scholar 

  • Kern M, Bacon W, Long D, Cowie RJ (2005) Blood metabolites and corticosterone levels in breeding adult pied flycatchers. Condor 107:665–677

    Article  Google Scholar 

  • Klomberg KF, Garland T Jr, Swallow JG, Carter PA (2002) Dominance, plasma testosterone levels, and testis size in house mice artificially selected for high activity levels. Physiol Behav 77:27–38. doi:10.1016/S0031-9384(02)00767-9

    Article  PubMed  CAS  Google Scholar 

  • Koetsier E, Verhulst S (2011) A simple technique to manipulate foraging costs in seed-eating birds. J Exp Biol 214:1225–1229. doi:10.1242/jeb.050336

    Article  PubMed  Google Scholar 

  • Lescroël A, Dugger KM, Ballard G, Ainley DG (2009) Effects of individual quality, reproductive success and environmental variability on survival of a long-lived seabird. J Anim Ecol 78:798–806

    Article  PubMed  Google Scholar 

  • Love OP, Williams TD (2008) The adaptive value of stress-induced phenotypes: effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness. Am Nat 172:E135–E149. doi:10.1086/590959

    Article  PubMed  Google Scholar 

  • Low M, Makan T, Castro I (2012) Food availability and offspring demand influence sex-specific patterns and repeatability of parental provisioning. Behav Ecol 23:25–34

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Malisch JL, Saltzman W, Gomes FR, Rezende EL, Jeske DR, Garland T Jr (2007) Baseline and stress-induced plasma corticosterone concentrations of mice selectively bred for high voluntary wheel running. Physiol Biochem Zool 80:146–156. doi:10.1086/508828

    Article  PubMed  CAS  Google Scholar 

  • Mariette MM, Pariser EC, Gilby AJ, Magrath MJL, Pryke SR, Griffith SC (2011) Using an electronic monitoring system to link offspring provisioning and foraging behavior of a wild passerine. Auk 128:26–35. doi:10.1525/auk.2011.10117

    Article  Google Scholar 

  • Metcalfe NB, Monaghan P (2013) Does reproduction cause oxidative stress? An open question. Trends Ecol Evol 28:347–350. doi:10.1016/j.tree.2013.01.015

    Article  PubMed  Google Scholar 

  • Mitchell GW, Newman AEM, Wikelski M, Ryan Norris D (2012) Timing of breeding carries over to influence migratory departure in a songbird: an automated radiotracking study. J Anim Ecol 81:1024–1033. doi:10.1111/j.1365-2656.2012.01978.x

    Article  PubMed  Google Scholar 

  • Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92

    Article  PubMed  Google Scholar 

  • Murray A, Costa R (2012) Born to run. Studying the limits of human performance. BMC Med 10:76

    Article  PubMed  PubMed Central  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. J Evol Biol 20:1674–1681

    Article  PubMed  CAS  Google Scholar 

  • Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci USA 105:19052–19059. doi:10.1073/pnas.0800375105

    Article  PubMed  PubMed Central  Google Scholar 

  • Neufer PD (1989) The effect of detraining and reduced training on the physiological adaptations to aerobic exercise training. Sports Med 8:302–320

    Article  PubMed  CAS  Google Scholar 

  • Newton I (1989) Lifetime reproduction in birds. Academic, London

    Google Scholar 

  • Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26

    Article  Google Scholar 

  • Norte AC, Ramos JA, Sampaio JP, Sousa JP, Sheldon BC (2010) Physiological condition and breeding performance of the great tit. Condor 112:79–86

    Article  Google Scholar 

  • Nur N (1984) Feeding frequencies of nestling blue tits (Parus caeruleus): costs, benefits and a model of optimal feeding frequency. Oecologia 65:125–137

    Article  Google Scholar 

  • Piersma T (2011) Why marathon migrants get away with high metabolic ceilings: towards an ecology of physiological restraint. J Exp Biol 214:295–302. doi:10.1242/jeb.046748

    Article  PubMed  Google Scholar 

  • Piersma T, van Gils JA (2011) The flexible phenotype. A body-centred integration of ecology, physiology, and behaviour. Oxford University Press, Oxford

    Google Scholar 

  • Ringsby T, Berge T, Saether B-E, Jensen H (2009) Reproductive success and individual variation in feeding frequency of House Sparrows (Passer domesticus). J Ornithol 150:469–481. doi:10.1007/s10336-008-0365-z

    Article  Google Scholar 

  • Ryder TB, Horton BM, van den Tillaart M, Morales JDD, Moore IT (2012) Proximity data-loggers increase the quantity and quality of social network data. Biol Lett 8:917–920. doi:10.1098/rsbl.2012.0536

    Article  PubMed  PubMed Central  Google Scholar 

  • Salvante KG (2006) Techniques for studying integrated immune function in birds. Auk 123:575–586

    Article  Google Scholar 

  • Santos ESA, Nakagawa S (2012) The costs of parental care: a meta-analysis of the trade-off between parental effort and survival in birds. J Evol Biol 25:1911–1917. doi:10.1111/j.1420-9101.2012.02569.x

    Article  PubMed  CAS  Google Scholar 

  • Scantlebury DM et al (2014) Flexible energetics of cheetah hunting strategies provide resistance against kleptoparasitism. Science 346:79–81. doi:10.1126/science.1256424

    Article  PubMed  CAS  Google Scholar 

  • Schroeder J, Burke T, Mannarelli ME, Dawson DA, Nakagawa S (2012) Maternal effects and heritability of annual productivity. J Evol Biol 25:149–156. doi:10.1111/j.1420-9101.2011.02412.x

    Article  PubMed  Google Scholar 

  • Schroeder J, Cleasby I, Dugdale HL, Nakagawa S, Burke T (2013) Social and genetic benefits of parental investment suggest sex differences in selection pressures. J Avian Biol 44:133–140. doi:10.1111/j.1600-048X.2012.00010.x

    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 

  • Schwagmeyer PL, Mock DW (2008a) Parental provisioning and offspring fitness: size matters. Anim Behav 75:291–298

    Article  Google Scholar 

  • Schwagmeyer PL, Mock DW (2008b) Parental provisioning and offspring fitness: size matters. Anim Behav 75:291–298. doi:10.1016/j.anbehav.2007.05.023

    Article  Google Scholar 

  • Simons MJP, Briga M, Leenknegt B, Verhulst S (2014) Context-dependent effects of carotenoid supplementation on reproduction in zebra finches. Behav Ecol 25:945–950. doi:10.1093/beheco/aru062

    Article  Google Scholar 

  • Sinclair ELE, de Souza CRN, Ward AJW, Seebacher F (2014) Exercise changes behaviour. Funct Ecol 28:652–659. doi:10.1111/1365-2435.12198

    Article  Google Scholar 

  • Slagsvold T, Lifjeld JT (1988) Ultimate adjustment of clutch size to parental feeding capacity in a passerine bird. Ecology 69:1918–1922

    Article  Google Scholar 

  • Speakman J (1997) Factors influencing the daily energy expenditure of small mammals. Proc Nutr Soc 56:1119–1136. doi:10.1079/PNS19970115

    Article  PubMed  CAS  Google Scholar 

  • Spivey RJ, Bishop CM (2013) Interpretation of body-mounted accelerometry in flying animals and estimation of biomechanical power. J R Soc Interface. doi:10.1098/rsif.2013.0404

    PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Stodola KW, Linder ET, Buehler DA, Franzreb KE, Kim DH, Cooper RJ (2010) Relative influence of male and female care in determining nestling mass in a migratory songbird. J Avian Biol 41:515–522

    Article  Google Scholar 

  • Swallow J, Carter P, Garland T Jr (1998) Artificial selection for increased wheel-running behavior in house mice. Behav Genet 28:227–237. doi:10.1023/A:1021479331779

    Article  PubMed  CAS  Google Scholar 

  • Swallow JG, Koteja P, Carter PA, Garland T (1999) Artificial selection for increased wheel-running activity in house mice results in decreased body mass at maturity. J Exp Biol 202:2513–2520

    PubMed  CAS  Google Scholar 

  • Tieleman BI, Dijkstra TH, Klasing KC, Visser GH, Williams JB (2008) Effects of experimentally increased costs of activity during reproduction on parental investment and self-maintenance in tropical house wrens. Behav Ecol 19:949–959. doi:10.1093/beheco/arn051

    Article  Google Scholar 

  • Tieleman BI, Croese E, Helm B, Versteegh MA (2010) Repeatability and individual correlates of microbicidal capacity of bird blood. Comp Biochem Physiol A 156:537–540

    Article  CAS  Google Scholar 

  • Tinbergen JM, Dietz MW (1994) Parental energy expenditure during brood rearing in the Great Tit (Parus major) in relation to body mass, temperature, food availability and clutch size. Funct Ecol 8:563–572

    Article  Google Scholar 

  • Toïgo C, Gaillard J-M, Loison A (2013) Alpine ibex males grow large horns at no survival cost for most of their lifetime. Oecologia 173:1261–1269. doi:10.1007/s00442-013-2700-1

    Article  PubMed  Google Scholar 

  • Travers M, Clinchy ML, Boonstra R, Zanette L, Williams TD (2010) Indirect predator effects on clutch size and the cost of egg production. Ecol Lett 13:980–988

    PubMed  Google Scholar 

  • Tremblay I, Thomas DW, Lambrechts MM, Blondel J, Perret P (2003) Variation in blue tit breeding performance across gradients in habitat richness. Ecology 84:3033–3043

    Article  Google Scholar 

  • Versteegh MA, Helm B, Kleynhans EJ, Gwinner E, Tieleman BI (2014) Genetic and phenotypically flexible components of seasonal variation in immune function. J Exp Biol 217:1510–1518. doi:10.1242/jeb.097105

    Article  PubMed  CAS  Google Scholar 

  • Wikelski M, Tarlow EM, Raim A, Diehl RH, Larkin RP, Visser GH (2003) Avian metabolism: costs of migration in free-flying songbirds. Nature 423:704

    Article  PubMed  CAS  Google Scholar 

  • Williams TD (2008) Individual variation in endocrine systems: moving beyond the “tyranny of the Golden Mean”. Philos Trans R Soc Lond B 363:1687–1698

    Article  CAS  Google Scholar 

  • Williams TD (2012) Physiological adaptations for breeding in birds. Princeton University Press, Princeton

    Google Scholar 

  • Williams TM et al (2014) Instantaneous energetics of puma kills reveal advantage of felid sneak attacks. Science 346:81–85. doi:10.1126/science.1254885

    Article  PubMed  CAS  Google Scholar 

  • Wilson AJ, Nussey DH (2010) What is individual quality? An evolutionary perspective. Trends Ecol Evol 25:207–214

    Article  PubMed  Google Scholar 

  • Winkler DW, Allen PE (1995) Effects of handicapping on female condition and reproduction in tree swallows (Tachycineta bicolor). Auk 112:737–747

    Google Scholar 

  • Wright J, Cuthill I (1989) Manipulation of sex differences in parental care. Behav Ecol Sociobiol 25:171–181

    Article  Google Scholar 

  • Wright J, Both C, Cotton PA, Bryant DM (1998) Quality vs. quantity: energetic and nutritional trade-offs in parental provisioning strategies. J Anim Ecol 67:620–634

    Article  Google Scholar 

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Acknowledgments

This work was funded by NSERC Discovery Grant and Accelerator funding to T.D.W. We thank Allison Cornell, Megan Rogers, James Hou, and Jessica Leung for help with fieldwork and laboratory analysis; this MS benefited greatly from discussions T.D.W. had with Jeff Yap and Mitchell Serota during a Directed Readings course on the “Physiology of exercise”.

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Communicated by E. Matthysen.

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Williams, T.D., Fowler, M.A. Individual variation in workload during parental care: can we detect a physiological signature of quality or cost of reproduction?. J Ornithol 156 (Suppl 1), 441–451 (2015). https://doi.org/10.1007/s10336-015-1213-6

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