Advertisement

Behavioral Ecology and Sociobiology

, Volume 70, Issue 1, pp 171–178 | Cite as

Barn swallows (Hirundo rustica) differentiate between common cuckoo and sparrowhawk in China: alarm calls convey information on threat

  • Jiangping Yu
  • Longwu Wang
  • Xiaoying Xing
  • Canchao Yang
  • Jianhua Ma
  • Anders Pape Møller
  • Haitao Wang
  • Wei Liang
Original Article

Abstract

Morphological mimicry of sparrowhawks Accipiter spp. by cuckoos acts to deceive hosts and thus promotes parasitism by cuckoos. Recent studies have suggested that common hosts are able to identify parasites and make special alarm calls as the result of co-evolution between hosts and brood parasites. Previous studies showed that barn swallows Hirundo rustica could distinguish between common cuckoo Cuculus canorus and sparrowhawk Accipiter nisus in Denmark, but seemed unable to make this distinction in China. However, these previous studies did not investigate vocal responses in terms of alarm calls. We tested whether barn swallows, which are regular hosts of the common cuckoo in China, could distinguish between the common cuckoo and sparrowhawk in China. In Heilongjiang, in the presence of the cuckoo and, in Hainan, in its absence, we used dummies of common cuckoo, sparrowhawk, and Oriental turtle dove Streptopelia orientalis (neutral control) to induce and record alarm calls that were used to estimate response to playbacks. Barn swallows responded more strongly to playbacks of swallow hawk alarm calls than in response to swallow cuckoo or swallow dove alarm calls. Given that alarm calls conveyed information about the presence of potential threats, our study showed that barn swallows from both study regions in China were able to distinguish between common cuckoo and sparrowhawk and respond accordingly in their vocal behavior.

Keywords

Accipiter virgatus Alarm call playback Barn swallow Brood parasitism Cuculus canorus 

Notes

Acknowledgments

We would like to thank Prof. Manuel Soler and the two anonymous reviewers for their constructive and helpful comments on our manuscript. We are grateful to Wenfeng Wang from the Zhalong National Nature Reserve and to Tongping Su and Yiping Hu for their assistance in fieldwork. We also thank the Baomeiling Nature Reserve, Changjiang, Hainan, and the Zhalong National Nature Reserve, Heilongjiang, for their support and permission to carry out this study. This work was supported by the National Natural Science Foundation of China (31272331 to HW, 31272328 and 31472013 to WL, and 31260514 to CY) and the Program for New Century Excellent Talents in University (NCET-13-0761 to CY).

Compliance with ethical standards

The experiments comply with the current laws of China, where they were performed. Fieldwork was carried out under the permission from Zhalong National Nature Reserves and Baomeiling Nature Reserve, China. Experimental procedures were in agreement with the Animal Research Ethics Committee of Hainan Provincial Education Centre for Ecology and Environment, Hainan Normal University.

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B 57:289–300Google Scholar
  2. Beránková J, Veselý P, Sýkorová J, Fuchs R (2014) The role of key features in predator recognition by untrained birds. Anim Cogn 17:963–971PubMedCrossRefGoogle Scholar
  3. Campobello D, Sealy SG (2010) Enemy recognition of reed warblers (Acrocephalus scirpaceus): threats and reproductive value act independently in nest defence modulation. Ethology 116:498–508CrossRefGoogle Scholar
  4. Campobello D, Sealy SG (2011) Use of social over personal information enhances nest defense against avian brood parasitism. Behav Ecol 22:422–428CrossRefGoogle Scholar
  5. Courter JR, Ritchison G (2010) Alarm calls of tufted titmice convey information about predator size and threat. Behav Ecol 21:936–942CrossRefGoogle Scholar
  6. Craib J (1994) Why do common cuckoos resemble raptors? Br Birds 87:78–79Google Scholar
  7. Curio E (1978) The adaptive significance of avian mobbing: I. Teleonomic hypotheses and predictions. Z Tierpsychol 48:175–183Google Scholar
  8. Davies NB (2000) Cuckoos, cowbirds and other cheats. T & A D Poyser, LondonGoogle Scholar
  9. Davies NB (2011) Cuckoo adaptations: trickery and tuning. J Zool 284:1–14CrossRefGoogle Scholar
  10. Davies NB, Welbergen JA (2008) Cuckoo-hawk mimicry? An experimental test. Proc R Soc Lond B 275:1817–1822CrossRefGoogle Scholar
  11. Evans CS (1997) Referential signals. In: Owings DH, Beecher MD, Thompson NS (eds) Perspectives in ethology: communication, vol 12. Plenum, New York, pp 99–143Google Scholar
  12. Evans CS, Evans E, Marler P (1993) On the meaning of alarm calls: functional reference in an avian vocal system. Anim Behav 46:23–38CrossRefGoogle Scholar
  13. Feeney WE, Medina I, Somveille M, Heinsohn R, Hall ML, Mulder RA, Stein JA, Kilner RM, Langmore NE (2013) Brood parasitism and the evolution of cooperative breeding in birds. Science 342:1506–1508PubMedCrossRefGoogle Scholar
  14. Gill SA, Sealy SG (1996) Nest defence by yellow warblers: recognition of a brood parasite and an avian nest predator. Behaviour 133:263–282CrossRefGoogle Scholar
  15. Gill SA, Sealy SG (2003) Tests of two functions of alarm calls given by yellow warblers during nest defence. Can J Zool 81:1685–1690CrossRefGoogle Scholar
  16. Gill SA, Sealy SG (2004) Functional reference in an alarm signal given during nest defence: seet calls of yellow warblers denote brood-parasitic brown-headed cowbirds. Behav Ecol Sociobiol 56:71–80CrossRefGoogle Scholar
  17. Gluckman T, Mundy NI (2013) Cuckoos in raptors’ clothing: barred plumage illuminates a fundamental principle of Batesian mimicry. Anim Behav 86:1165–1181CrossRefGoogle Scholar
  18. Griesser M (2008) Referential calls signal predator behavior in a group-living bird species. Curr Biol 18:69–73PubMedCrossRefGoogle Scholar
  19. Griesser M (2009) Mobbing calls signal predator category in a kin group-living bird species. Proc R Soc Lond B 276:2887–2892CrossRefGoogle Scholar
  20. Grim T (2005) Host recognition of brood parasites: implications for methodology in studies of enemy recognition. Auk 122:530–543CrossRefGoogle Scholar
  21. Grim T, Samaš P, Moskát C, Kleven O, Honza M, Moksnes A, Røskaft E, Stokke BG (2011) Constraints on host choice: why do parasitic birds rarely exploit some common potential hosts? J Anim Ecol 80:508–518PubMedCrossRefGoogle Scholar
  22. Halsey LG, Curran-Everett D, Vowler SL, Drummond GB (2015) The fickle P value generates irreproducible results. Nat Methods 12:179–185PubMedCrossRefGoogle Scholar
  23. Hollén LI, Manser MB (2007) Motivation before meaning: motivational information encoded in meerkat alarm calls develops earlier than referential information. Am Nat 169:758–767PubMedCrossRefGoogle Scholar
  24. Honza M, Šicha V, Procházka P, Ležalová R (2006) Host nest defense against a color-dimorphic brood parasite: great reed warblers (Acrocephalus arundinaceus) versus common cuckoos (Cuculus canorus). J Ornithol 147:629–637CrossRefGoogle Scholar
  25. Hosoi SA, Rothstein SI (2000) Nest desertion and cowbird parasitism: evidence for evolved responses and evolutionary lag. Anim Behav 59:82–840CrossRefGoogle Scholar
  26. Kachigan SK (1991) Multivariate statistical analysis: a conceptual introduction, 2nd edn. Radius, New YorkGoogle Scholar
  27. Kilner RM, Langmore NE (2011) Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol Rev 86:836–852PubMedCrossRefGoogle Scholar
  28. Kroodsma DE (1989) Suggested experimental designs for song playbacks. Anim Behav 37:600–609CrossRefGoogle Scholar
  29. Krüger O (2007) Cuckoos, cowbirds and hosts: adaptations, trade-offs and constraints. Philos T Roy Soc B 362:1873–1886CrossRefGoogle Scholar
  30. Leavesley AJ, Magrath RD (2005) Communicating about danger: urgency alarm calling in a bird. Anim Behav 70:365–373CrossRefGoogle Scholar
  31. Liang W, Møller AP (2015) Hawk mimicry in cuckoos and anti-parasitic aggressive behavior of barn swallows in Denmark and China. J Avian Biol 46:216–223CrossRefGoogle Scholar
  32. Liang W, Yang C, Wang L, Møller AP (2013) Avoiding parasitism by breeding indoors: cuckoo parasitism of hirundines and rejection of eggs. Behav Ecol Sociobiol 67:913–918CrossRefGoogle Scholar
  33. Lyon BE, Gilbert GS (2013) Rarely parasitized and unparasitized species mob and alarm call to cuckoos: implications for sparrowhawk mimicry by brood parasitic cuckoos. Wilson J Ornithol 125:627–630CrossRefGoogle Scholar
  34. Moksnes A, Røskaft E, Braa AT, Korsnes L, Lampe HM, Pedersen HC (1991) Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour 116:64–89CrossRefGoogle Scholar
  35. Møller AP (1994) Sexual selection and the barn swallow. Oxford University Press, OxfordGoogle Scholar
  36. Møller AP, Jennions MD (2002) How much variance can be explained by ecologists and evolutionary biologists. Oecologia 132:492–500CrossRefGoogle Scholar
  37. Møller AP, Stokke BG, Samia D (2015) Hawk models, hawk mimics and anti-predator behavior of prey. Behav Ecol 26:1039–1044CrossRefGoogle Scholar
  38. Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045CrossRefGoogle Scholar
  39. Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605PubMedCrossRefGoogle Scholar
  40. Pavey CR, Smyth AK (1998) Effects of avian mobbing on roost use and diet of powerful owls, Ninox strenua. Anim Behav 55:313–318PubMedCrossRefGoogle Scholar
  41. Røskaft E, Moksnes A, Stokke BG, Bicík V, Moskát C (2002) Aggression to dummy cuckoos by potential European cuckoo hosts. Behaviour 139:613–628CrossRefGoogle Scholar
  42. Rothstein SI (1990) A model system for coevolution: avian brood parasitism. Annu Rev Ecol Syst 21:481–508CrossRefGoogle Scholar
  43. Scaife M (1976) The response to eye-like shapes by birds. I. The effect of context: a predator and a strange bird. Anim Behav 24:195–199CrossRefGoogle Scholar
  44. Sealy SG (1995) Burial of cowbird eggs by parasitized yellow warblers: an empirical and experimental study. Anim Behav 49:877–889CrossRefGoogle Scholar
  45. Sealy SG, Neudorf DL, Hobson KA, Gill SA (1998) Nest defense by potential hosts of the brown-headed cowbird: methodological approaches, benefits of defense, and coevolution. In: Rothstein SI, Robinson SK (eds) Parasitic birds and their hosts: studies in coevolution. Oxford University Press, New York, pp 194–211Google Scholar
  46. Shields WM (1984a) Barn swallow mobbing: self-defence, collateral kin defence, group defence, or parental care? Anim Behav 32:132–148CrossRefGoogle Scholar
  47. Shields WM (1984b) Factors affecting nest and site fidelity in Adirondack barn swallows (Hirundo rustica). Auk 101:780–789CrossRefGoogle Scholar
  48. Stoddard MC (2012) Mimicry and masquerade from the avian visual perspective. Curr Zool 58:630–648Google Scholar
  49. Strnad M, Němec M, Veselý P, Sýkorová J, Fuchs R (2012) Red-backed shrikes (Laniu scollurio) adjust the mobbing intensity, but not mobbing frequency, by assessing the potential threat to themselves from different predators. Ornis Fennica 89:206–215Google Scholar
  50. Suzuki TN (2012) Referential mobbing calls elicit different predator-searching behaviours in Japanese great tits. Anim Behav 84:53–57CrossRefGoogle Scholar
  51. Suzuki TN (2014) Communication about predator type by a bird using discrete, graded and combinatorial variation in alarm calls. Anim Behav 87:59–65CrossRefGoogle Scholar
  52. Suzuki TN, Ueda K (2013) Mobbing calls of Japanese tits signal predator type: field observations of natural predator encounters. Wilson J Ornithol 125:412–415CrossRefGoogle Scholar
  53. Templeton CN, Greene E, Davis K (2005) Allometry of alarm calls: black-capped chickadees encode information about predator size. Science 308:1934–1938PubMedCrossRefGoogle Scholar
  54. Thorogood R, Davies NB (2013) Hawk mimicry and the evolution of polymorphic cuckoos. Chin Birds 4:39–50CrossRefGoogle Scholar
  55. Trnka A, Grim T (2013) Color plumage polymorphism and predator mimicry in brood parasites. Front Zool 10:25PubMedPubMedCentralCrossRefGoogle Scholar
  56. Trnka A, Prokop P (2012) The effectiveness of hawk mimicry in protecting cuckoos from aggressive hosts. Anim Behav 83:263–268CrossRefGoogle Scholar
  57. Trnka A, Prokop P, Grim T (2012) Uncovering dangerous cheats: how do avian hosts recognize adult brood parasites? PLoS ONE 7, e37445PubMedPubMedCentralCrossRefGoogle Scholar
  58. Trnka A, Trnka M, Grim T (2015) Do rufous common cuckoo females indeed mimic a predator? An experimental test. Biol J Linn Soc 116:134–143CrossRefGoogle Scholar
  59. Watve M, Thakar J, Kale A, Puntambekar S, Shaikh I, Vaze K, Jog M, Paranjape S (2002) Bee-eaters (Merops orientalis) respond to what a predator can see. Anim Cogn 5:253–259PubMedCrossRefGoogle Scholar
  60. Welbergen JA, Davies NB (2008) Reed warblers discriminate cuckoos from sparrowhawks with graded alarm signals that attract males and neighbours. Anim Behav 76:811–822CrossRefGoogle Scholar
  61. Welbergen JA, Davies NB (2011) A parasite in wolf’s clothing: hawk mimicry reduces mobbing of cuckoos by hosts. Behav Ecol 22:574–579CrossRefGoogle Scholar
  62. Wheatcroft DJ, Price TD (2008) Reciprocal cooperation in avian mobbing: playing nice pays. Trends Ecol Evol 23:416–419PubMedCrossRefGoogle Scholar
  63. Wheatcroft D, Price TD (2015) Rates of signal evolution are associated with the nature of interspecific communication. Behav Ecol 26:83–90CrossRefGoogle Scholar
  64. Wilson DR, Mennill DJ (2011) Duty cycle, not signal structure, explains conspecific and heterospecific responses to the calls of black-capped chickadees (Poecile atricapillus). Behav Ecol 22:784–790CrossRefGoogle Scholar
  65. Wyllie L (1981) The cuckoo. Batsford, LondonGoogle Scholar
  66. Yang C, Chen M, Wang L, Liang W, Møller AP (2015a) Nest sanitation elicits egg discrimination in cuckoo hosts. Anim Cogn 18:1373–1377PubMedCrossRefGoogle Scholar
  67. Yang C, Liang W, Antonov A, Cai Y, Stokke BG, Fossøy F, Moksnes A, Røskaft E (2012) Diversity of parasitic cuckoos and their hosts in China. Chin Birds 3:9–32CrossRefGoogle Scholar
  68. Yang C, Wang L, Cheng S-J, Hsu Y-C, Liang W, Møller AP (2014) Nest defenses and egg recognition of yellow-bellied prinia against cuckoo parasitism. Naturwissenschaften 101:727–734PubMedCrossRefGoogle Scholar
  69. Yang C, Wang L, Liang W, Møller AP (2015b) Nest sanitation behavior as a pre-adaptation of egg rejection to counter parasitism in hirundines. Anim Cogn 18:355–360PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Jiangping Yu
    • 1
  • Longwu Wang
    • 2
    • 3
  • Xiaoying Xing
    • 4
  • Canchao Yang
    • 2
  • Jianhua Ma
    • 5
  • Anders Pape Møller
    • 6
  • Haitao Wang
    • 1
  • Wei Liang
    • 2
  1. 1.School of Life Sciences, Jilin Provincial Key Laboratory of Animal Resource Conservation and UtilizationNortheast Normal UniversityChangchunChina
  2. 2.Ministry of Education Key Laboratory for Tropical Animal and Plant Ecology, College of Life SciencesHainan Normal UniversityHaikouChina
  3. 3.School of Life SciencesGuizhou Normal UniversityGuiyangChina
  4. 4.College of Wildlife ResourceNortheast Forestry UniversityHarbinChina
  5. 5.Zhalong National Nature ReserveQiqiharChina
  6. 6.Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079Université Paris-SudOrsay CedexFrance

Personalised recommendations