Advertisement

Male parental investment reflects the level of partner contributions and brood value in tree swallows

  • Ádám Z. Lendvai
  • Çağlar Akçay
  • Mark Stanback
  • Mark F. Haussmann
  • Ignacio T. Moore
  • Frances Bonier
Original Article

Abstract

Biparental care presents an interesting case of cooperation and conflict between unrelated individuals. Several models have been proposed to explain how parents should respond to changes in each other’s parental care to maximize their own fitness, predicting no change, partial compensation, or matching effort as a response. Here, we present an experiment in tree swallows (Tachycineta bicolor) in which we increased the offspring provisioning of females by presenting them, but not their mates, with additional nestling begging calls using automated playbacks. We performed this experiment in two populations differing in future breeding opportunities. We found that in response to a temporary increase in female parental effort, males in the northern population (with lower future breeding opportunities and thus higher brood value) matched the increased effort, whereas males in the southern population did not. We also found that increases in parental care during playbacks were driven by the females (i.e., females initiated the increased effort and their mates followed them) in the northern population but not the southern population. These results support the idea that with incomplete information about the brood value and need, cues or signals from the partner might become important in coordinating parental care.

Significance statement

Male tree swallows increase parental effort when their mates need to work harder. Using an automated system, we broadcast playback of hungry nestling calls only when the female parent was visiting the nest. In a population where the value of the current brood was high, males significantly increased their provisioning rate, much more than their partners did. Since only the females could hear the playbacks, and the begging of the nestlings did not change in response to the treatment, we suggest that either the males used their partner’s feeding rate as a cue or the females may have communicated to their mates that they should work harder. These results suggest that cues or signals from the partner may be important in coordinating parental care.

Keywords

Biparental care Parental effort Negotiation Sexual conflict Tree swallow 

Notes

Acknowledgments

We are grateful to Alice Domalik, Pria St. John (Queen’s University), and Drew Gill and Spencer Gill (Davidson College) for excellent help in the field and for Fruzsina Demcsák (University of Debrecen) for analyzing the begging recordings. We thank Katharina Mahr, the associate editor Marty Leonard, and anonymous reviewers for comments on previous versions of the manuscript.

Author contributions

ÇA and ÁZL designed and coordinated the study, collected field data, carried out data analysis, and drafted the manuscript; MS collected field data and helped draft the manuscript; MFH contributed to the design of the study and helped draft the manuscript; FB collected field data, contributed to the design of the study, and helped draft the manuscript; ITM contributed to the design of the study and helped draft the manuscript. All authors gave final approval for publication.

Funding

This work was supported by a U.S. National Science Foundation (NSF) grant (FB, ITM and MFH; IOS-1145625) and by the Natural Sciences and Engineering Research Council of Canada Discovery Grant (FB). During the preparation of the manuscript, ÁZL was supported by grants from the National Research Development and Innovation Office (OTKA K113108 and TÉT_15-1-2016-0044) and by the Romanian Ministry of Education (PN-III-P4-ID-PCE-2016-0572).

Compliance with ethical standards

Ethical approval

We confirm that the procedures used in the study followed the guidelines for animal care outlined by Animal Behaviour Society and Association for the Study of Animal Behaviour and were approved by approved by the Institutional Animal Care and Use Committee at Virginia Tech (#12–020) and Animal Care Committee of Queen’s University (#2013-019) and the Canadian Wildlife Service (#CA0211). The field research was conducted with a permit from US Geological Survey Bird Banding Laboratory to MS (#22742) and Canadian Wildlife Service permit to FB (#10771).

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

265_2018_2594_MOESM1_ESM.docx (290 kb)
ESM 1 (DOCX 290 kb)
265_2018_2594_MOESM2_ESM.xlsx (33 kb)
ESM 2 (XLSX 32 kb)

References

  1. Akçay Ç, Lendvai ÁZ, Stanback MT, Haussmann MF, Moore IT, Bonier F (2016) Strategic adjustment of parental care in tree swallows: life-history trade-offs and the role of glucocorticoids. R Soc Open Sci 3:160740.  https://doi.org/10.1098/rsos.160740 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Akçay E, Roughgarden J (2009) The perfect family: decision making in biparental care. PLoS One 4:e7345.  https://doi.org/10.1371/journal.pone.0007345 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Ardia DR (2005) Tree swallows trade off immune function and reproductive effort differently across their range. Ecology 86:2040–2046.  https://doi.org/10.1890/04-1619 CrossRefGoogle Scholar
  4. Bebbington K, Hatchwell BJ (2016) Coordinated parental provisioning is related to feeding rate and reproductive success in a songbird. Behav Ecol 27:652–659.  https://doi.org/10.1093/beheco/arv198 CrossRefGoogle Scholar
  5. Bókony V, Lendvai ÁZ, Liker A, Angelier F, Wingfield JC, Chastel O (2009) Stress response and the value of reproduction: are birds prudent parents? Am Nat 173:589–598.  https://doi.org/10.1086/597610 CrossRefPubMedGoogle Scholar
  6. Boucaud IC, Mariette MM, Villain AS, Vignal C (2015) Vocal negotiation over parental care? Acoustic communication at the nest predicts partners’ incubation share. Biol J Linn Soc 117:322–336.  https://doi.org/10.1111/bij.12705 CrossRefGoogle Scholar
  7. Chase ID (1980) Cooperative and noncooperative behavior in animals. Am Nat 115:827–857.  https://doi.org/10.1086/283603 CrossRefGoogle Scholar
  8. Clark RG, Winkler DW, Dawson RD, Shutler D, Hussell DJT, Lombardo MP, Thorpe PA, Dunn PO, Whittingham LA (2018) Geographic variation and environmental correlates of apparent survival rates in adult tree swallows Tachycineta bicolor. J Avian Biol 49:jav-012514.  https://doi.org/10.1111/jav.01659 CrossRefGoogle Scholar
  9. Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton, NJGoogle Scholar
  10. Cockburn A (2006) Prevalence of different modes of parental care in birds. Proc R Soc B Biol Sci 273:1375–1383.  https://doi.org/10.1098/rspb.2005.3458 CrossRefGoogle Scholar
  11. Cox AR, Robertson RJ, Bradley FC, Wallace RB, Bonier F (2018) Demographic drivers of local population decline in Tree Swallows (Tachycineta bicolor) in Ontario, Canada. Condor (published online, doi:  https://doi.org/10.1650/CONDOR-18-42.1)  https://doi.org/10.1650/CONDOR-18-42.1)
  12. Dakin R, Ouyang JQ, Lendvai ÁZ, Haussmann MF, Moore IT, Bonier F (2016) Weather matters: begging calls are temperature- and size-dependent signals of offspring state. Behaviour 153:871–896.  https://doi.org/10.1163/1568539X-00003370 CrossRefGoogle Scholar
  13. Dunn PO, Robertson RJ, Michaud-Freeman D, Boag PT (1994) Extra-pair paternity in tree swallows: why do females mate with more than one male? Behav Ecol Sociobiol 35:273–281.  https://doi.org/10.1007/BF00170708 CrossRefGoogle Scholar
  14. Elie JE, Mariette MM, Soula HA, Griffith SC, Mathevon N, Vignal C (2010) Vocal communication at the nest between mates in wild zebra finches: a private vocal duet? Anim Behav 80:597–605.  https://doi.org/10.1016/j.anbehav.2010.06.003 CrossRefGoogle Scholar
  15. Gill LF, Goymann W, Ter Maat A, Gahr M (2015) Patterns of call communication between group-housed zebra finches change during the breeding cycle. Elife 4:e07770CrossRefGoogle Scholar
  16. Griggio M, Matessi G, Pilastro A (2005) Should I stay or should I go? Female brood desertion and male counterstrategy in rock sparrows. Behav Ecol 16:435–441.  https://doi.org/10.1093/beheco/ari009 CrossRefGoogle Scholar
  17. Harrison F, Barta Z, Cuthill I, Székely T (2009) How is sexual conflict over parental care resolved? A meta-analysis. J Evol Biol 22:1800–1812.  https://doi.org/10.1111/j.1420-9101.2009.01792.x CrossRefPubMedGoogle Scholar
  18. Hinde CA (2006) Negotiation over offspring care?—a positive response to partner-provisioning rate in great tits. Behav Ecol 17:6–12.  https://doi.org/10.1093/beheco/ari092 CrossRefGoogle Scholar
  19. Hinde CA, Kilner RM (2007) Negotiations within the family over the supply of parental care. Proc R Soc B Biol Sci 274:53–60.  https://doi.org/10.1098/rspb.2006.3692 CrossRefGoogle Scholar
  20. Horn AG, Leonard ML (2008) Acoustic interactions in broods of nestling birds (Tachycineta bicolor). J Comp Psychol 122:298–304.  https://doi.org/10.1037/0735-7036.122.3.298
  21. Houston AI, Davies NB (1985) The evolution of co-operation and life history in the dunnock, Prunella modularis. In: Sibly RM, Smith RH (eds) Behavioural ecology: ecological consequences of adaptive behaviour. Blackwell, Oxford, pp 471–487Google Scholar
  22. Houston AI, Székely T, McNamara JM (2005) Conflict between parents over care. Trends Ecol Evol 20:33–38.  https://doi.org/10.1016/j.tree.2004.10.008
  23. Johnstone RA, Hinde CA (2006) Negotiation over offspring care—how should parents respond to each other’s efforts? Behav Ecol 17:818–827.  https://doi.org/10.1093/beheco/arl009 CrossRefGoogle Scholar
  24. Johnstone RA, Manica A, Fayet AL, Stoddard MC, Rodriguez-Gironés MA, Hinde CA (2014) Reciprocity and conditional cooperation between great tit parents. Behav Ecol 25:216–222.  https://doi.org/10.1093/beheco/art109 CrossRefGoogle Scholar
  25. Kosztolányi A, Cuthill IC, Székely T (2009) Negotiation between parents over care: reversible compensation during incubation. Behav Ecol 20:446–452.  https://doi.org/10.1093/beheco/arn140 CrossRefGoogle Scholar
  26. Lendvai ÁZ, Akçay Ç, Ouyang JQ, Dakin R, Domalik AD, St John PS, Stanback M, Moore IT, Bonier F (2015a) Analysis of the optimal duration of behavioral observations based on an automated continuous monitoring system in tree swallows (Tachycineta bicolor): is one hour good enough? PLoS One 10:e0141194.  https://doi.org/10.1371/journal.pone.0141194
  27. Lendvai ÁZ, Akçay Ç, Weiss T, Haussmann MF, Moore IT, Bonier F (2015b) Low cost audiovisual playback and recording triggered by radio frequency identification using raspberry pi. PeerJ 3:e877.  https://doi.org/10.7717/peerj.877 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lendvai ÁZ, Barta Z, Chastel O (2009) Conflict over parental care in house sparrows: do females use a negotiation rule? Behav Ecol 20:651–656.  https://doi.org/10.1093/beheco/arp047 CrossRefGoogle Scholar
  29. Leonard ML, Horn AG (2001) Begging calls and parental feeding decisions in tree swallows (Tachycineta bicolor). Behav Ecol Sociobiol 49:170–175.  https://doi.org/10.1007/s002650000290
  30. Leonard ML, Horn AG (2006) Age-related changes in signalling of need by nestling tree swallows (Tachycineta bicolor). Ethology 112:1020–1026.  https://doi.org/10.1111/j.1439-0310.2006.01259.x
  31. Leonard ML, Horn AG, Brown CR, Fernandez NJ (1997) Parent–offspring recognition in tree swallows, Tachycineta bicolor. Anim Behav 54:1107–1116.  https://doi.org/10.1006/anbe.1997.0559
  32. Leonard ML, Horn AG, Gozna A, Ramen S (2000) Brood size and begging intensity in nestling birds. Behav Ecol 11:196–201.  https://doi.org/10.1093/beheco/11.2.196 CrossRefGoogle Scholar
  33. McCarty JP (2002) The number of visits to the nest by parents is an accurate measure of food delivered to nestlings in tree swallows. J Field Ornithol 73:9–14.  https://doi.org/10.2307/4131060 CrossRefGoogle Scholar
  34. McNamara JM, Gasson CE, Houston AI (1999) Incorporating rules for responding into evolutionary games. Nature 401:368–371.  https://doi.org/10.1038/43869 CrossRefPubMedGoogle Scholar
  35. McNamara JM, Houston AI, Barta Z, Osorno J-L (2003) Should young ever be better off with one parent than with two? Behav Ecol 14:301–310.  https://doi.org/10.1093/beheco/14.3.301 CrossRefGoogle Scholar
  36. Meade J, Nam K-B, Lee J-W, Hatchwell BJ (2011) An experimental test of the information model for negotiation of biparental care. PLoS One 6:e19684.  https://doi.org/10.1371/journal.pone.0019684 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Royle NJ, Hartley IR, Parker GA (2002) Sexual conflict reduces offspring fitness in zebra finches. Nature 416:733–736.  https://doi.org/10.1038/416733a CrossRefPubMedGoogle Scholar
  38. Sandercock BK (2003) Estimation of survival rates for wader populations: a review of mark-recapture methods. Wader Study Group Bull 100:163–174Google Scholar
  39. Schwagmeyer P, Mock DW, Parker GA (2002) Biparental care in house sparrows: negotiation or sealed bid? Behav Ecol 13:713–721CrossRefGoogle Scholar
  40. Sol D, Maspons J, Vall-llosera M, Bartomeus I, García-Peña GE, Piñol J, Freckleton RP (2012) Unraveling the life history of successful invaders. Science 337:580–583.  https://doi.org/10.1126/science.1221523 CrossRefPubMedGoogle Scholar
  41. Trivers RL (1972) Parental investment and sexual selection. In: Campbell BG (ed) Sexual selection and the descent of man, 1871-1971. Aldine, Chicago, pp 136–179Google Scholar
  42. Whittingham LA, Dunn PO, Robertson RJ (1994) Female response to reduced male parental care in birds: an experiment in tree swallows. Ethology 96:260–269.  https://doi.org/10.1111/j.1439-0310.1994.tb01014.x CrossRefGoogle Scholar
  43. Winkler DW, Wrege PH, Allen PE, Kast TL, Senesac P, Wasson MF, Llambías PE, Ferretti V, Sullivan PJ (2004) Breeding dispersal and philopatry in the tree swallow. Condor 106:768–776CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ádám Z. Lendvai
    • 1
    • 2
    • 3
  • Çağlar Akçay
    • 1
    • 4
  • Mark Stanback
    • 5
  • Mark F. Haussmann
    • 6
  • Ignacio T. Moore
    • 1
  • Frances Bonier
    • 1
    • 7
  1. 1.Department of Biological SciencesVirginia TechBlacksburgUSA
  2. 2.Department of Evolutionary Zoology and Human BiologyUniversity of DebrecenDebrecenHungary
  3. 3.Department of GeologyBabeş-Bolyai UniversityCluj-NapocaRomania
  4. 4.Department of PsychologyKoç UniversityİstanbulTurkey
  5. 5.Department of BiologyDavidson CollegeDavidsonUSA
  6. 6.Department of BiologyBucknell UniversityLewisburgUSA
  7. 7.Department of BiologyQueen’s UniversityKingstonCanada

Personalised recommendations