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
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
Borer KT (2003) Exercise endocrinology. Human Kinetics, Champagne
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
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
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
Clutton-Brock TH (1988) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago
Daan S, Deerenberg C, Dijkstra C (1996) Increased daily work precipitates natural death in the kestrel. J Anim Ecol 65:539–544
Dawson RD, Bortolotti GR (2003) Parental effort of American kestrels: the role of variation in brood size. Can J Zool 81:852–860
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
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
Drent R (2006) The timing of birds’ breeding seasons: the Perrin’s hypothesis revisited especially for migrants. Ardea 94:305–322
Drent R, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252
Duclos M (2008) A critical assessment of hormonal methods used in monitoring training status in athetes. Int Sports Med J 9:56–66
Eliason EJ et al (2011) Differences in thermal tolerance among sockeye salmon populations. Science 332:109–112. doi:10.1126/science.1199158
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
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
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
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
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
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
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
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
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
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
Harshman LG, Zera AJ (2007) The cost of reproduction: the devil in the details. Trends Ecol Evol 22:80–88
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
Horak P, Jenni-Eiermann S, Ots I (1999) Do great tits (Parus major) starve to reproduce? Oecologia 119:293–299
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
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
Husak JF (2006) Does survival depend on how fast you can run or how fast you do run? Funct Ecol 20:1080–1086
Irschick DJ (2003) Studying performance in nature: implications for fitness variation within populations. Integr Comp Biol 43:396–407
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
Joyner MJ, Coyle EF (2008) Endurance exercise performance: the physiology of champions. J Physiol 586:35–44. doi:10.1113/jphysiol.2007.143834
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
Kern M, Bacon W, Long D, Cowie RJ (2005) Blood metabolites and corticosterone levels in breeding adult pied flycatchers. Condor 107:665–677
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
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
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
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
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
MacColl ADC, Hatchwell BJ (2003) Heritability of parental effort in a passerine bird. Evolution 57:2191–2195
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
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
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
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
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
Murray A, Costa R (2012) Born to run. Studying the limits of human performance. BMC Med 10:76
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
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
Neufer PD (1989) The effect of detraining and reduced training on the physiological adaptations to aerobic exercise training. Sports Med 8:302–320
Newton I (1989) Lifetime reproduction in birds. Academic, London
Norris K, Evans MR (2000) Ecological immunology: life history trade-offs and immune defense in birds. Behav Ecol 11:19–26
Norte AC, Ramos JA, Sampaio JP, Sousa JP, Sheldon BC (2010) Physiological condition and breeding performance of the great tit. Condor 112:79–86
Nur N (1984) Feeding frequencies of nestling blue tits (Parus caeruleus): costs, benefits and a model of optimal feeding frequency. Oecologia 65:125–137
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
Piersma T, van Gils JA (2011) The flexible phenotype. A body-centred integration of ecology, physiology, and behaviour. Oxford University Press, Oxford
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
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
Salvante KG (2006) Techniques for studying integrated immune function in birds. Auk 123:575–586
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
Scantlebury DM et al (2014) Flexible energetics of cheetah hunting strategies provide resistance against kleptoparasitism. Science 346:79–81. doi:10.1126/science.1256424
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
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
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
Schwagmeyer PL, Mock DW (2008a) Parental provisioning and offspring fitness: size matters. Anim Behav 75:291–298
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
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
Sinclair ELE, de Souza CRN, Ward AJW, Seebacher F (2014) Exercise changes behaviour. Funct Ecol 28:652–659. doi:10.1111/1365-2435.12198
Slagsvold T, Lifjeld JT (1988) Ultimate adjustment of clutch size to parental feeding capacity in a passerine bird. Ecology 69:1918–1922
Speakman J (1997) Factors influencing the daily energy expenditure of small mammals. Proc Nutr Soc 56:1119–1136. doi:10.1079/PNS19970115
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
Stearns SC (1992) The evolution of life-histories. Oxford University Press, Oxford
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
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
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
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
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
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
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
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
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
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
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
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
Williams TD (2012) Physiological adaptations for breeding in birds. Princeton University Press, Princeton
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
Wilson AJ, Nussey DH (2010) What is individual quality? An evolutionary perspective. Trends Ecol Evol 25:207–214
Winkler DW, Allen PE (1995) Effects of handicapping on female condition and reproduction in tree swallows (Tachycineta bicolor). Auk 112:737–747
Wright J, Cuthill I (1989) Manipulation of sex differences in parental care. Behav Ecol Sociobiol 25:171–181
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
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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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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DOI: https://doi.org/10.1007/s10336-015-1213-6