Zebra finch nestlings, rather than parents, suffer from raising broods under low nutritional conditions

Abstract

In sexually reproducing species, parents and offspring have different optima in terms of the amount of parental investment. For offspring, higher investment than the parental optimum generally increases their fitness. However, such higher investment will, in theory, result in net parental fitness loss because increased benefits from current offspring will be more than offset by a potential decrease in parental survival or future reproduction. Whether and how parents respond to a shortfall in resources might therefore have important fitness consequences. Here, we manipulate the nutritional condition of captive zebra finch families to investigate how variation in environmental conditions influences parental resource allocation between themselves and their offspring. By allowing the same zebra finch pairs to raise one brood under high and another brood under low nutritional conditions, we found that parents lost more body mass and their offspring grew at slower rates under low nutritional conditions. Therefore, both parents and their offspring were affected by the nutritional treatments. Offspring incurred greater costs, because slower growth rates under low nutritional conditions resulted in an overall lower body mass of nestlings after reaching independence. Nutritional treatments had sex-specific effects on parental body mass, because, in contrast to fathers, only mothers recouped their losses under high nutritional conditions. Furthermore, both parents spent less time brooding their nestlings under low nutritional conditions. Parental strategies hence vary with the nutritional quality of their food, even in captivity, supporting the idea that parental resource allocation may be driven by the expected costs and benefits from current offspring.

Significance statement

Parental care is among the most influential traits affecting fitness in many sexually reproducing animals. The more care offspring receive, the higher their chances of survival and reproduction. However, caring for their young does not only provide benefits for parents: all costs of parental care are paid by them. Parental resource allocation is therefore expected to be optimised. But how should parents respond to changing environmental conditions when they are already breeding? By manipulating nutritional conditions in a captive population of zebra finches Taeniopygia guttata, we show that both parents and their offspring lose body mass under low nutritional conditions. The effect on offspring was more pronounced and long lasting, and parents also decreased their parental effort. Our results show plasticity in parental investment of zebra finches in response to nutritional conditions and reproductive value of their offspring.

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References

  1. AlRashidi M, Kosztolányi A, Küpper C, Cuthill IC, Javed S, Székely T (2010) The influence of a hot environment on parental cooperation of a ground-nesting shorebird, the Kentish plover Charadrius alexandrinus. Front Zool 7:1

    Article  PubMed  PubMed Central  Google Scholar 

  2. Amat JA (1995) Parent-offspring feeding relationship of coots (Fulica atra) in a varying environment. Behaviour 132:519–527

    Article  Google Scholar 

  3. Arnold KE, Blount JD, Metcalfe NB, Orr KJ, Adam A, Houston D, Monaghan P (2007) Sex-specific differences in compensation for poor neonatal nutrition in the zebra finch Taeniopygia guttata. J Avian Biol 38:356–366

    Article  Google Scholar 

  4. Boag PT (1987) Effects of nestling diet on growth and adult size of zebra finches (Poephila guttata). Auk 104:155–166

    Google Scholar 

  5. Bolund E, Schielzeth H, Forstmeier W (2009) Compensatory investment in zebra finches: females lay larger eggs when paired to sexually unattractive males. Proc R Soc Lond B 276:707–715

    Article  Google Scholar 

  6. Carlisle TR (1982) Brood success in variable environments—implications for parental care allocation. Anim Behav 30:824–836

    Article  Google Scholar 

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

    Google Scholar 

  8. Criscuolo F, Monaghan P, Nasir L, Metcalfe N (2008) Early nutrition and phenotypic development: ‘catch-up’ growth leads to elevated metabolic rate in adulthood. Proc R Soc Lond B 275:1565–1570

    Article  Google Scholar 

  9. Dawson RD, Bortolotti GR (2002) Experimental evidence for food limitation and sex-specific strategies of American kestrels (Falco sparverius) provisioning offspring. Behav Ecol Sociobiol 52:43–52

    Article  Google Scholar 

  10. Delia JRJ, Ramirez-Bautista A, Summers K (2013) Parents adjust care in response to weather conditions and egg dehydration in a Neotropical glassfrog. Behav Ecol Sociobiol 67:557–569

    Article  Google Scholar 

  11. Dingemanse NJ, Wolf M (2013) Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim Behav 85:1031–1039

    Article  Google Scholar 

  12. Eldegard K, Sonerud GA (2010) Experimental increase in food supply influences the outcome of within-family conflicts in Tengmalm’s owl. Behav Ecol Sociobiol 64:815–826

    Article  Google Scholar 

  13. Erikstad KE, Fauchald P, Tveraa T, Steen H (1998) On the cost of reproduction in long-lived birds: the influence of environmental variability. Ecology 79:1781–1788

    Article  Google Scholar 

  14. Ferrer M (1992) Regulation of the period of postfledging dependence in the Spanish imperial eagle Aquila adalberti. Ibis 134:128–133

    Article  Google Scholar 

  15. Fisher MO, Nager RG, Monaghan P (2006) Compensatory growth impairs adult cognitive performance. PLoS Biol 4:e251

    Article  PubMed  PubMed Central  Google Scholar 

  16. Forstmeier W, Segelbacher G, Mueller JC, Kempenaers B (2007) Genetic variation and differentiation in captive and wild zebra finches (Taeniopygia guttata). Mol Ecol 16:4039–4050

    CAS  Article  PubMed  Google Scholar 

  17. Gilby A, Mainwaring M, Rollins L, Griffith S (2011) Parental care in wild and captive zebra finches: measuring food delivery to quantify parental effort. Anim Behav 81:289–295

    Article  Google Scholar 

  18. Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546

    CAS  Article  PubMed  Google Scholar 

  19. Griffith SC, Crino OL, Andrew SC et al (2017) Variation in reproductive success across captive populations: methodological differences, potential biases and opportunities. Ethology 123:1–29

    Article  Google Scholar 

  20. Hale RE, St Mary CM, Lindström K (2003) Parental responses to changes in costs and benefits along an environmental gradient. Environ Biol Fish 67:107–116

    Article  Google Scholar 

  21. Hill DL, Lindström J, McCafferty DJ, Nager RG (2014) Female but not male zebra finches adjust heat output in response to increased incubation demand. J Exp Biol 217:1326–1332

    Article  PubMed  Google Scholar 

  22. Hinde CA, Kilner RM (2007) Negotiations within the family over the supply of parental care. Proc R Soc Lond B 274:53–60

    Article  Google Scholar 

  23. Hoffman JI, Krause ET, Lehmann K, Krüger O (2014) MC1R genotype and plumage colouration in the zebra finch (Taeniopygia guttata): population structure generates artefactual associations. PLoS One 9:e86519

    Article  PubMed  PubMed Central  Google Scholar 

  24. Honarmand M, Goymann W, Naguib M (2010) Stressful dieting: nutritional conditions but not compensatory growth elevate corticosterone levels in zebra finch nestlings and fledglings. PLoS One 5:e12930

    Article  PubMed  PubMed Central  Google Scholar 

  25. Horak P (2003) When to pay the cost of reproduction? A brood size manipulation experiment in great tits (Parus major). Behav Ecol Sociobiol 54:105–112

    Google Scholar 

  26. Hussell DJT (1988) Supply and demand in tree swallow broods—a model of parent-offspring food-provisioning interactions in birds. Am Nat 131:175–202

    Article  Google Scholar 

  27. Immelmann K (1965) Versuch einer ökologischen Verbreitungsanalyse beim australischen Zebrafinken, Taeniopygia guttata castanotis (Gould). J Ornithol 106:415–430

    Article  Google Scholar 

  28. Jennions MD, Polakow DA (2001) The effect of partial brood loss on male desertion in a cichlid fish: an experimental test. Behav Ecol 12:84–92

    Article  Google Scholar 

  29. Jodice PGR, Roby DD, Hatch SA, Gill VA, Lanctot RB, Visser GH (2002) Does food availability affect energy expenditure rates of nesting seabirds? A supplemental-feeding experiment with black-legged kittiwakes (Rissa tridactyla). Can J Zool 80:214–222

    Article  Google Scholar 

  30. Kilner RM, Hinde CA (2008) Information warfare and parent-offspring conflict. Adv Stud Behav 38:283–336

    Article  Google Scholar 

  31. Kölliker M, Brodie ED III, Moore AJ (2005) The coadaptation of parental supply and offspring demand. Am Nat 166:506–516

    Article  PubMed  Google Scholar 

  32. Krause ET, Naguib M (2011) Compensatory growth affects exploratory behaviour in zebra finches, Taeniopygia guttata. Anim Behav 81:1295–1300

    Article  Google Scholar 

  33. Krause ET, Naguib M (2014) Effects of parental and own early developmental conditions on the phenotype in zebra finches (Taeniopygia guttata). Evol Ecol 28:263–275

    Article  Google Scholar 

  34. Krause ET, Naguib M (2015) Zebra finch males compensate in plumage ornaments at sexual maturation for a bad start in life. Front Zool 12:S11

    Article  PubMed  PubMed Central  Google Scholar 

  35. Krause ET, Honarmand M, Wetzel J, Naguib M (2009) Early fasting is long lasting: differences in early nutritional conditions reappear under stressful conditions in adult female zebra finches. PLoS One 4:e5015

    Article  PubMed  PubMed Central  Google Scholar 

  36. Krause ET, Honarmand M, Naguib M (2011) Zebra finch nestlings beg more under better nutritional conditions. Behaviour 148:1239–1255

    Google Scholar 

  37. Krause ET, Krüger O, Schielzeth H (2017) Long-term effects of early nutrition and environmental matching on developmental and personality traits in zebra finches. Anim Behav 128:103–115

    Article  Google Scholar 

  38. Kriengwatana B, Farrell TM, Aitken SDT, Garcia L, MacDougall-Shackleton SA (2014) Early-life nutritional stress affects associative learning and spatial memory but not performance on a novel object test. Behaviour 152:195–218

    Article  Google Scholar 

  39. Lessells CM (2002) Parentally biased favouritism: why should parents specialize in caring for different offspring? Philos T Roy Soc B 357:381–403

    CAS  Article  Google Scholar 

  40. Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348

    Article  PubMed  Google Scholar 

  41. Lycett JE, Henzi SP, Barrett L (1998) Maternal investment in mountain baboons and the hypothesis of reduced care. Behav Ecol Sociobiol 42:49–56

    Article  Google Scholar 

  42. Mariette MM, Griffith SC (2012) Nest visit synchrony is high and correlates with reproductive success in the wild zebra finch Taeniopygia guttata. J Avian Biol 43:131–140

    Article  Google Scholar 

  43. Mas F, Haynes KF, Kölliker M (2009) A chemical signal of offspring quality affects maternal care in a social insect. Proc R Soc Lond B 276:2847–2853

    Article  Google Scholar 

  44. McNamara JM, Gasson CE, Houston AI (1999) Incorporating rules for responding into evolutionary games. Nature 401:368–371

    CAS  PubMed  Google Scholar 

  45. Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, Oxford

    Google Scholar 

  46. Morvai B, Nanuru S, Mul D, Kusche N, Milne G, Szekely T, Komdeur J, Miklosi A, Pogany A (2016) Diurnal and reproductive stage-dependent variation of parental behaviour in captive zebra finches. PLoS One 11:e0167368

    Article  PubMed  PubMed Central  Google Scholar 

  47. Naguib M, Gil D (2005) Transgenerational effects on body size caused by early developmental stress in zebra finches. Biol Lett 1:95–97

    Article  PubMed  PubMed Central  Google Scholar 

  48. Parker GA, Macnair MR (1978) Models of parent-offspring conflict.1. Monogamy. Anim Behav 26:97–110

    CAS  Article  PubMed  Google Scholar 

  49. Parker GA, Royle NJ, Hartley IR (2002) Intrafamilial conflict and parental investment: a synthesis. Philos T Roy Soc B 357:295–307

    Article  Google Scholar 

  50. Pinheiro J, Bates D, DebRoy S, Sarkar D, Core Team R (2017) nlme: linear and nonlinear mixed effects models. R package version 3:1–131 https://CRAN.R-project.org/package=nlme

    Google Scholar 

  51. Pogány Á, van Dijk RE, Horváth P, Székely T (2012) Parental behavior and reproductive output in male-only cared and female-only cared clutches in the Eurasian penduline tit (Remiz pendulinus). Auk 129:773–781

    Article  Google Scholar 

  52. R Core Team (2015) R: A language and environment for statistical computing, version 3.2.3. R Foundation for Statistical Computing, Vienna http://www.R-project.org

    Google Scholar 

  53. Rehling A, Spiller I, Krause ET, Nager RG, Monaghan P, Trillmich F (2012) Flexibility in the duration of parental care: zebra finch parents respond to offspring needs. Anim Behav 83:35–39

    Article  Google Scholar 

  54. Royle NJ, Surai PF, Hartley IR (2003) The effect of variation in dietary intake on maternal deposition of antioxidants in zebra finch eggs. Funct Ecol 17:472–481

    Article  Google Scholar 

  55. Royle NJ, Smiseth PT, Kölliker M (eds) (2012) The evolution of parental care. Oxford University Press, Oxford

    Google Scholar 

  56. Royle NJ, Russell AF, Wilson AJ (2014) The evolution of flexible parenting. Science 345:776–781

    CAS  Article  PubMed  Google Scholar 

  57. Rutstein A, Slater P, Graves J (2004) Diet quality and resource allocation in the zebra finch. Proc R Soc Lond B 271:S286–S289

    Article  Google Scholar 

  58. Rytkonen S (2002) Nest defence in great tits Parus major: support for parental investment theory. Behav Ecol Sociobiol 52:379–384

    Article  Google Scholar 

  59. Rytkonen S, Orell M, Koivula K, Soppela M (1995) Correlation between 2 components of parental investment—nest defense intensity and nestling provisioning effort of willow tits. Oecologia 104:386–393

    Article  PubMed  Google Scholar 

  60. Saino N, Ninni P, Calza S, Martinelli R, De Bernardi F, Møller AP (2000) Better red than dead: carotenoid-based mouth coloration reveals infection in barn swallow nestlings. Proc R Soc Lond B 267:57–61

    CAS  Article  Google Scholar 

  61. Skagen SK (1988) Asynchronous hatching and food limitation—a test of lacks hypothesis. Auk 105:78–88

    Google Scholar 

  62. Spencer KA, Buchanan KL, Goldsmith AR, Catchpole CK (2003) Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm Behav 44:132–139

    CAS  Article  PubMed  Google Scholar 

  63. Spencer KA, Heidinger BJ, D’Alba LB, Evans NP, Monaghan P (2010) Then versus now: effect of developmental and current environmental conditions on incubation effort in birds. Behav Ecol 21:999–1004

    Article  Google Scholar 

  64. Thünken T, Meuthen D, Bakker TCM, Kullmann H (2010) Parental investment in relation to offspring quality in the biparental cichlid fish Pelvicachromis taeniatus. Anim Behav 80:69–74

    Article  Google Scholar 

  65. Tilgar V, Kikas K (2009) Is parental risk taking negatively related to the level of brood reduction? An experiment with pied flycatchers. Anim Behav 77:43–47

    Article  Google Scholar 

  66. Trillmich F, Spiller I, Naguib M, Krause ET (2016) Patient parents: do offspring decide on the timing of fledging in zebra finches? Ethology 122:411–418

    Article  Google Scholar 

  67. Trivers RL (1974) Parent-offspring conflict. Am Zool 14:249–264

    Article  Google Scholar 

  68. Vleck CM (1981) Energetic cost of incubation in the zebra finch. Condor 83:229–237

    Article  Google Scholar 

  69. Ward RJS, Cotter SC, Kilner RM (2009) Current brood size and residual reproductive value predict offspring desertion in the burying beetle Nicrophorus vespilloides. Behav Ecol 20:1274–1281

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  72. Winkler DW (1987) A general-model for parental care. Am Nat 130:526–543

    Article  Google Scholar 

  73. Zann RA (1996) The zebra finch: a synthesis of field and laboratory studies. Oxford University Press, Oxford

    Google Scholar 

  74. Zann RA, Rossetto M (1991) Zebra finch incubation—brood patch, egg temperature and thermal-properties of the nest. Emu 91:107–120

    Article  Google Scholar 

  75. Zarybnicka M (2009) Parental investment of female Tengmalm’s owls Aegolius funereus: correlation with varying food abundance and reproductive success. Acta Ornithol 44:81–88

    Article  Google Scholar 

  76. Zuckerman ZC, Philipp DP, Suski CD (2014) The influence of brood loss on nest abandonment decisions in largemouth bass Micropterus salmoides. J Fish Biol 84:1863–1875

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

We thank Fritz Trillmich, Kate Lessells and two anonymous reviewers for providing helpful comments on earlier versions of the manuscript. We also thank the animal care takers at the Department of Animal Behaviour, Bielefeld University, especially Ulla Kodytek and Gitta Otte.

Funding

ETK was supported by a fellowship of the Volkswagen Foundation under its Evolutionary Biology Initiative (85994) while writing the manuscript. AP was supported by the Hungarian Scientific Research Fund (OTKA K109337), an Eötvös postdoctoral grant by the Hungarian Scholarship Board, Balassi Institute (32078) and by the János Bolyai Research Scholarship of the Hungarian Academy of Sciences. OK was supported by a Heisenberg Professorship of the German Research Foundation (KR 2089/3-1).

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Correspondence to E. Tobias Krause or Ákos Pogány.

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Ethical approval

The study was carried out according to the German Laws for the experimentation with animals at that time and with permission of the LANUV NRW (# 8.87.51.05.20.11.011). Breeding and housing of the birds were done under the permission of the Veterinäramt Bielefeld (# 530.421630-1, 18.4.2002 and #530.4, 27.07.2014). All birds used in the experiments remained for their entire life at the Department of Animal Behaviour, Bielefeld University, Germany. All birds were visually monitored for health status on a daily basis.

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The authors declare that they have no conflict of interest.

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All data analysed during this study are included in the supplementary information files.

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Communicated by M. Leonard

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Krause, E.T., Krüger, O. & Pogány, Á. Zebra finch nestlings, rather than parents, suffer from raising broods under low nutritional conditions. Behav Ecol Sociobiol 71, 152 (2017). https://doi.org/10.1007/s00265-017-2382-5

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Keywords

  • Parental care
  • Resource allocation
  • Parent-offspring conflict
  • Environmental condition
  • Nutritional stress
  • Offspring reproductive value