Behavioral Ecology and Sociobiology

, Volume 66, Issue 12, pp 1639–1649 | Cite as

Carer provisioning rules in an obligate cooperative breeder: prey type, size and delivery rate

  • L. E. BrowningEmail author
  • C. M. Young
  • J. L. Savage
  • D. J. F. Russell
  • H. Barclay
  • S. C. Griffith
  • A. F. Russell
Original Paper


Providing food to developing offspring is beneficial for offspring but costly for carers. Understanding patterns of provisioning thus yields important insights into how selection shapes (allo-) parental care strategies. Broadly, offspring development will be influenced by three components of provisioning (prey type, size and delivery rate). However, all three variables are rarely considered simultaneously, leading to suggestions that the results of many studies are misleading. Additionally, few studies have examined the provisioning strategies of breeders and non-breeding helpers in obligate cooperative breeders, wherein reproduction without help is typically unsuccessful. We investigated these components of provisioning in obligately cooperative chestnut-crowned babblers (Pomatostomus ruficeps). Prey type was associated with size, and delivery rate was the best predictor of the overall amount of food provided by carers. As broods aged, breeders and helpers similarly modified the relative proportion of different prey provided and increased both prey size and delivery rate. Breeding females contributed less prey than male breeders and adult helpers, and were the only carers to load-lighten by reducing their provisioning rates in the presence of additional carers. While our results suggest that breeders and helpers follow broadly comparable provisioning rules, they are also consistent with the idea that, in obligately cooperative species, breeding females benefit more from conserving resources for future reproduction than do helpers which have a low probability of breeding independently.


Additive care Allo-parental care Costs of helping Helper effort Load-lightening 



We thank Dr. David Croft, Garry and Vicky Dowling and Zane Turner for logistical support at Fowlers Gap; UNSW for permission to work there; Elena Berg, Sam Patrick, Bec Rose and Beth Woodward for fieldwork; Clare Holleley and Lee Ann Rollins for molecular work; Stanislaw Zabramski and Michael Magrath for designing and making the PIT tag system; Tim Clutton-Brock, Nick Davies and Ben Hatchwell for helpful discussion; James Gilbert, Stuart Sharp, Sjouke Kingma and two anonymous referees for valuable comments on the manuscript; and James Gilbert for help with MCMCglmm. This work was funded by grants from the Natural Environment Research Council [studentship to University of Cambridge (LEB)] and New Investigator’s (AFR), Marmaduke Shield Fund (LEB), Australian Research Council Discovery Grant (AFR) and the Royal Society University Research Fellowship Scheme (AFR).

Ethical standards

Fieldwork was carried out under the approval of UNSW Animal Care and Ethics Committee (license no. 06/40A) and the authority of NSW National Parks and Wildlife Service and the Australian Bird and Bat Banding Scheme.

Conflict of interest



  1. Arnold KE, Ramsay SL, Donaldson C, Adam A (2007) Parental prey selection affects risk-taking behaviour and spatial learning in avian offspring. Proc R Soc Lond B 274:2563–2569CrossRefGoogle Scholar
  2. Bañbura J, Lambrechts MM, Blondel J, Perret P, Cartan-Son M (1999) Food handling time of blue tit chicks: constraints and adaptation to different prey types. J Avian Biol 30:263–270CrossRefGoogle Scholar
  3. Bates D, Maechler M, Bolker BM (2011) lme4: linear mixed-effects models using S4 classes.
  4. Boland CRJ, Heinsohn R, Cockburn A (1997) Experimental manipulation of brood reduction and parental care in cooperatively breeding white-winged choughs. J Anim Ecol 66:683–691CrossRefGoogle Scholar
  5. Brown JL (1987) Helping and communal breeding in birds. Princeton University Press, PrincetonGoogle Scholar
  6. Browning LE, Patrick SC, Rollins LA, Griffith SC, Russell AF (2012) Kin selection, not group augmentation, predicts helping in an obligate cooperatively breeding bird. Proc R Soc Lond B 279:3861–3869CrossRefGoogle Scholar
  7. Canestrari D, Chiarati E, Marcos JM, Ekman J, Baglione V (2008) Helpers but not breeders adjust provisioning effort to year-round territory resource availability in carrion crows. Anim Behav 76:943–949CrossRefGoogle Scholar
  8. Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, PrincetonGoogle Scholar
  9. Clutton-Brock TH, Hodge SJ, Spong G, Russell AF, Jordan NR, Bennett NC, Sharpe LL, Manser MB (2006) Intrasexual competition and sexual selection in cooperative mammals. Nature 444:1065–1068PubMedCrossRefGoogle Scholar
  10. Clutton-Brock TH, Russell AF, Sharpe LL (2004) Behavioural tactics of breeders in cooperative meerkats. Anim Behav 68:1029–1040CrossRefGoogle Scholar
  11. Clutton-Brock TH, Russell AF, Sharpe LL, Young AJ, Balmforth Z, McIlrath GM (2002) Evolution and development of sex differences in cooperative behavior in meerkats. Science 297:253–297PubMedCrossRefGoogle Scholar
  12. Cornwallis CK, West SA, Griffin AS (2009) Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal. J Evol Biol 22:2445–2457PubMedCrossRefGoogle Scholar
  13. Cowie RJ, Hinsley SA (1988) Feeding ecology of great tits (Parus major) and blue tits (Parus caeruleus), breeding in suburban gardens. J Avian Biol 57:611–626Google Scholar
  14. Dickinson JL, Hatchwell BJ (2004) Fitness consequences of helping. In: Koenig WD, Dickinson JL (eds) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, pp 48–66CrossRefGoogle Scholar
  15. Emlen ST, Wrege PH (1991) Breeding biology of white-fronted bee-eaters at Nakuru: the influence of helpers on breeder fitness. J Anim Ecol 60:309–326CrossRefGoogle Scholar
  16. Gelman A (2008) Scaling regression inputs by dividing by two standard deviations. Stat Med 27:2865–2873PubMedCrossRefGoogle Scholar
  17. Gilchrist J, Russell AF (2007) Who cares? Individual contributions to pup care by breeders vs non-breeders in the cooperatively breeding banded mongoose (Mungos mungo). Behav Ecol Sociobiol 61:1053–1060CrossRefGoogle Scholar
  18. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075PubMedCrossRefGoogle Scholar
  19. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 32:1–22Google Scholar
  20. Hamilton WD (1964) The genetical evolution of social behaviour I & II. J Theor Biol 7:1–82PubMedCrossRefGoogle Scholar
  21. Hatchwell BJ (1999) Investment strategies of breeders in avian cooperative breeding systems. Am Nat 154:205–219CrossRefGoogle Scholar
  22. Hatchwell BJ (2009) The evolution of cooperative breeding in birds: kinship, dispersal and life history. Philos T Roy Soc B 364:3217–3227CrossRefGoogle Scholar
  23. 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 15:1–10CrossRefGoogle Scholar
  24. Heinsohn R (1991) Slow learning of foraging skills and extended parental care in cooperatively breeding white-winged choughs. Am Nat 137:864–881CrossRefGoogle Scholar
  25. Heinsohn R (2004) Parental care, load-lightening, and costs. In: Koenig WD, Dickinson JL (eds) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, pp 67–80CrossRefGoogle Scholar
  26. Higgins PJ, Peter JM (2002) Handbook of Australian, New Zealand and Antarctic Birds. Volume 6: Pardalotes to Shrike-thrushes. Oxford University Press, MelbourneGoogle Scholar
  27. Holleley CE, Russell AF, Griffith SC (2009) Isolation and characterization of polymorphic tetranucleotide microsatellite loci in the chestnut-crowned babbler (Pomatostomus ruficeps). Mol Ecol Res 9:993–995CrossRefGoogle Scholar
  28. Langen TA (1996) Skill acquisition and the timing of natal dispersal in the white-throated magpie-jay, Calocitta formosa. Anim Behav 51:575–588CrossRefGoogle Scholar
  29. Legge S (2000) Helper contributions in the cooperatively breeding laughing kookaburra: feeding young is no laughing matter. Anim Behav 59:1009–1018PubMedCrossRefGoogle Scholar
  30. Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348PubMedCrossRefGoogle Scholar
  31. MacColl ADC, Hatchwell BJ (2003) Sharing of caring: nestling provisioning behaviour of long-tailed tit, Aegithalos caudatus, parents and helpers. Anim Behav 66:955–964CrossRefGoogle Scholar
  32. Maynard Smith J (1964) Group selection and kin selection. Nature 201:1145–1147CrossRefGoogle Scholar
  33. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260PubMedCrossRefGoogle Scholar
  34. Monaghan P, Nager RG (1997) Why don’t birds lay more eggs? Trends Ecol Evol 12:270–274PubMedCrossRefGoogle Scholar
  35. Nam K-B, Meade J, Hatchwell BJ (2011) Do parents and helpers adjust their provisioning effort in relation to nestling sex in a cooperatively breeding bird? Anim Behav 82:303–309CrossRefGoogle Scholar
  36. Portelli DJ, Barclay H, Russell DJF, Griffith SC, Russell AF (2009) Social organisation and foraging ecology of the cooperatively breeding chestnut-crowned babbler (Pomatostomus ruficeps). Emu 109:153–162CrossRefGoogle Scholar
  37. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  38. Rabenold KN (1985) Cooperation in breeding by nonreproductive wrens: kinship, reciprocity, and demography. Behav Ecol Sociobiol 17:1–17CrossRefGoogle Scholar
  39. Radford AN (2008) Age-related changes in nestling diet of the cooperatively breeding green woodhoopoe. Ethology 114:907–915CrossRefGoogle Scholar
  40. Ramsay SL, Houston DC (2003) Amino acid composition of some woodland arthropods and its implications for breeding tits and other passerines. Ibis 145:227–232CrossRefGoogle Scholar
  41. Rollins LA, Browning LE, Hollely CE, Savage JL, Russell AF, Griffith SC (2012) Building genetic networks using relatedness information: a novel approach for the estimation of dispersal and characterization of group structure in social animals. Mol Ecol 21:1727–1740PubMedCrossRefGoogle Scholar
  42. Royama T (1970) Factors governing the hunting behaviour and selection of food by the great tit (Parus major L.). J Anim Ecol 39:619–668CrossRefGoogle Scholar
  43. Russell AF, Langmore NE, Gardner JL, Kilner RM (2008) Maternal investment tactics in superb fairy-wrens. Proc R Soc Lond B 275:29–36CrossRefGoogle Scholar
  44. Russell AF, Portelli DJ, Russell DJF, Barclay H (2010) Breeding ecology of the chestnut-crowned babbler: a cooperative breeder in the desert. Emu 110:324–331CrossRefGoogle Scholar
  45. Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113CrossRefGoogle Scholar
  46. Sheldon BC (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402PubMedCrossRefGoogle Scholar
  47. Solomon NG, French JA (1997) Cooperative breeding in mammals. Cambridge University Press, CambridgeGoogle Scholar
  48. Sorato E, Gullett PR, Griffith SC, Russell AF (2012) Effects of predation risk on foraging behaviour and group size: adaptations in a social cooperative species. Anim Behav 84(4):823–834CrossRefGoogle Scholar
  49. Stacey PB, Koenig WD (1990) Cooperative breeding in birds: long-term studies of ecology and behavior. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  50. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  51. te Marvelde L, McDonald PG, 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 77:727–735CrossRefGoogle Scholar
  52. Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am Nat 100:687–690CrossRefGoogle Scholar
  53. Woxvold IA, Mulder RA, Magrath MJL (2006) Contributions to care vary with age, sex, breeding status and group size in the cooperatively breeding apostlebird. Anim Behav 72:63–73CrossRefGoogle Scholar
  54. Wright J (1998) Helpers-at-the-nest have the same provisioning rule as parents: experimental evidence from play-backs of chick begging. Behav Ecol Sociobiol 42:423–429CrossRefGoogle Scholar
  55. Wright J, McDonald PG, te Marvelde L, Kazem AJN, Bishop CM (2010) Helping effort increases with relatedness in bell miners, but “unrelated” helpers of both sexes still provide substantial care. Proc R Soc Lond B 277:437CrossRefGoogle Scholar
  56. Young CM, Browning LE, Savage JL, Griffith SC, Russell AF (2012) No evidence for deception over allocation to brood care in a cooperative bird. Behav Ecol. doi: 10.1093/beheco/ars137
  57. Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • L. E. Browning
    • 1
    • 2
    Email author
  • C. M. Young
    • 3
  • J. L. Savage
    • 2
  • D. J. F. Russell
    • 4
    • 5
  • H. Barclay
    • 2
  • S. C. Griffith
    • 3
  • A. F. Russell
    • 6
    • 7
  1. 1.Fowlers Gap Arid Zone Research Station, School of Biological, Earth & Environmental SciencesUniversity of New South WalesSydneyAustralia
  2. 2.Department of ZoologyUniversity of CambridgeCambridgeUK
  3. 3.Department of Biological SciencesMacquarie UniversitySydneyAustralia
  4. 4.Department of Animal & Plant SciencesUniversity of SheffieldSheffieldUK
  5. 5.Sea Mammal Research UnitUniversity of St AndrewsFifeUK
  6. 6.Centre for Ecology & Conservation, College of Life & Environmental SciencesUniversity of ExeterPenrynUK
  7. 7.Station d’Ecologie Expérimentale du CNRSMoulisFrance

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