Abstract
In this chapter, we consider the ways in which learning is involved in the anti-brood parasitism defences that hosts deploy across the nesting cycle. Brood parasitism varies in space and through time, and hosts have accordingly evolved plastic defences that can be tuned to local conditions. Hosts can achieve their defence plasticity by individual and social learning, as well as by experience-independent mechanisms. While these mechanisms can profoundly affect the coevolutionary dynamics between hosts and their brood parasites, our understanding of how they feature across the host nesting cycle is far from complete. Hosts can actively defend themselves against brood parasitism via a variety of behaviours, including nest defence, egg discrimination and chick discrimination. Such anti-brood parasite defences rely on the host’s ability to recognise and then defend against the parasitic threat, and there is good evidence that both these components of discrimination can be influenced by learning. To date, most research has focused on the function of learning in nest defence, but the learning mechanisms underlying egg discrimination are much better understood; and despite some notable exceptions, the role of learning in chick discrimination remains largely unexplored. An important challenge now is to understand the observed plasticity of anti-brood parasite defences in the context of environmental heterogeneity and specifically in terms of variation in the presence, detection and reliability of parasitism cues.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Bán M, Moskát C, Barta Z, Hauber ME (2013) Simultaneous viewing of own and parasitic eggs is not required for egg rejection by a cuckoo host. Behav Ecol 24:1014–1021
Boyd R, Richerson PJ (1988) An evolutionary model of social learning: the effects of spatial and temporal variation. In: Zentall TR, Galef BG Jr (eds) Social learning. Lawrence Erlbaum Associates, Hillsdale, pp 29–48
Briskie JV, Sealy SG, Hobson KA (1992) Behavioural defences against avian brood parasitism in sympatric and allopatric populations. Evolution 46:334–340
Brooke ML, Davies NB (1988) Egg mimicry by cuckoos Cuculus canorus in relation to discrimination by hosts. Nature 335:630–632
Brooke ML, Davies NB, Noble DG (1998) Rapid decline of host defences in response to reduced cuckoo parasitism: behavioural flexibility of reed warblers in a changing world. Proc R Soc Lond B 265:1277–1282
Campobello D (2008) A comparative approach to the study of avian nest defence: experience and adaptive significance. PhD thesis, University of Manitoba, Canada
Campobello D, Hare JF (2007) Information transfer determined by association of neighbours in European bee-eater, Merops apiaster, colonies. Ethol Ecol Evol 19:237–243
Campobello D, Sealy SG (2009) Avian brood parasitism in a Mediterranean region: hosts and habitat preferences of Common Cuckoos. Bird Study 56(3):389–400
Campobello D, Sealy SG (2010) Enemy recognition of reed warbler, Acrocephalus scirpaceus: threats and reproductive value act independently in nest defence modulation. Ethology 116:498–508
Campobello D, Sealy SG (2011a) Use of social over personal information enhances nest defence against avian brood parasitism. Behav Ecol 22:422–428
Campobello D, Sealy SG (2011b) Nest defence against avian brood parasites is promoted by egg-removal events in a cowbird-host system. Anim Behav 82:885–891
Campobello D, Hare JF, Sarà M (2015) Social phenotype extended to communities: expanded multilevel social selection analysis reveals fitness consequences of interspecific interactions. Evolution 69:916–925
Canestrari D, Marcos JM, Baglione V (2009) Cooperative breeding in carrion crows reduces the rate of brood parasitism by great spotted cuckoos. Anim Behav 77:1337–1344
Caro TM (2005) Antipredator defences in birds and mammals. University of Chicago Press, Chicago
Chance EP (1940) The truth about the cuckoo. Country Life, London
Colombelli-Negrel D, Hauber ME, Robertson J, Sulloway FJ, Hoi H, Griggio M, Kleindorfer S (2012) Embryonic learning of vocal passwords in superb fairy-wrens reveals intruder cuckoo nestlings. Curr Biol 22:2155–2160
Davies NB (2000) Cuckoos, cowbirds and other cheats. T&AD Poyser, London
Davies NB, Brooke ML (1988) Cuckoos versus reed warblers: adaptations and counteradaptations. Anim Behav 36:262–284
Davies NB, Welbergen JA (2008) Cuckoo–hawk mimicry? An experimental test. Proc R Soc Lond B 275:1817–1822
Davies NB, Welbergen JA (2009) Social transmission of a host defence against cuckoo parasitism. Science 324:1318–1320
Davies NB, Butchart SHM, Burke TA, Chaline N, Stewart IRK (2003) Reed warblers guard against cuckoos and cuckoldry. Anim Behav 65:285–295
De Mársico MC, Gantchoff MG, Reboreda JC (2012) Host–parasite coevolution beyond the nestling stage? Mimicry of host fledglings by the specialist screaming cowbird. Proc R Soc Lond B 279:3401–3408
DeWitt TJ, Scheiner SM (2004) Phenotypic variation from single genotypes: a primer. In: DeWitt TJ, Scheiner SM (eds) Phenotypic plasticity. Oxford University Press, New York, pp 1–9
Doligez B, Pärt T, Danchin E (2004) Prospecting in the collared flycatcher: gathering public information for future breeding habitat selection? Anim Behav 67:457–466
Duckworth JW (1991) Responses of breeding reed warblers, Acrocephalus scirpaceus, to mounts of sparrowhawk, Accipiter nisus, cuckoo, Cuculus canorus, and jay, Garrulus glandarius. Ibis 133:68–74
Dukas R (1998) Cognitive ecology: the evolutionary ecology of information processing and decision making. University of Chicago Press, Chicago
Dukas R (1999) Costs of memory: ideas and predictions. J Theor Biol 197:41–50
Feeney WE, Langmore NE (2013) Social learning of a brood parasite by its host. Biol Lett 9:20130443
Feeney WE, Welbergen JA, Langmore NE (2012) The frontline of avian brood parasite–host coevolution. Anim Behav 84:3–12
Feeney WE, Welbergen JA, Langmore NE (2014) Advances in the study of coevolution between avian brood parasites and their hosts. Annu Rev Ecol Evol Syst 45:227–246
Feeney WE, Troscianko J, Langmore NE, Spottiswoode CN (2015) Evidence for aggressive mimicry in an adult brood parasitic bird, and generalized defences in its host. Proc R Soc Lond B 282:20150795
Forsman JT, Monkkonen M (2001) Responses by breeding birds to heterospecific song and mobbing call playbacks under varying predation risk. Anim Behav 62:1067–1073
Fraga RM (1998) Interactions of the parasitic screaming and shiny cowbirds (Molothrus rufoaxillaris and M. bonariensis) with a shared host, the bay-winged cowbird (M. badius). In: Rothstein SI, Robinson SK (eds) Parasitic birds and their hosts. Oxford University Press, Oxford, pp 173–193
Freeberg TM, Duncan SD, Kast TL, Enstrom DA (1999) Cultural influences on female mate choice: an experimental test in cowbirds, Molothrus ater. Anim Behav 57:421–426
Galef BG Jr, Laland KN (2005) Social learning in animals: empirical studies and theoretical models. Bio Sci 55:489–499
Getty T (1996) The maintenance of phenotypic plasticity as a signal detection problem. Am Nat 148:378–385
Gill SA, Sealy SG (2003) Tests of two functions of alarm calls given by yellow warblers during nest defence. Can J Zool 81:1685–1690
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 56:71–80
Gill SA, Neudorf DL, Sealy SG (1997) Host responses to cowbirds near the nest: cues for recognition. Anim Behav 53:1287–1293
Gill SA, Neudorf DLH, Sealy SG (2008) Do hosts discriminate between sexually dichromatic male and female brown-headed cowbirds? Ethology 114:548–556
Giraldeau L-A, Valone TJ, Templeton JJ (2002) Potential disadvantages of using socially acquired information. Philos Trans R Soc B 357:1559–1566
Gluckman T-L, Mundy NI (2013) Cuckoos in raptors’ clothing: barred plumage illuminates a fundamental principle of Batesian mimicry. Anim Behav 86:1165–1181
Grim T (2006) The evolution of nestling discrimination by hosts of parasitic birds: why is rejection so rare? Evol Ecol Res 8:785–802
Grim T (2007) Experimental evidence for chick discrimination without recognition in a brood parasite host. Proc R Soc Lond B 274:373–381
Grim T, Kleven O, Mikulica O (2003) Nestling discrimination without recognition: a possible defence mechanism for hosts towards cuckoo parasitism? Proc R Soc Lond B 270:S73–S75
Grim T, Rutila J, Cassey P, Hauber ME (2009) Experimentally constrained virulence is costly for common cuckoo chicks. Ethology 115:14–22
Heyes CM (1994) Social learning in animals: categories and mechanisms. Biol Rev 69:207–231
Hobson KA, Sealy SG (1989) Responses of yellow warblers to the threat of cowbird parasitism. Anim Behav 38:510–519
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 147:629–637
Honza M, Polačikovà L, Prochàzka P (2007) Ultraviolet and green parts of the colour spectrum affect egg rejection in the song thrush (Turdus philomelos). Biol J Linn Soc 92:269–276
Hosoi SA, Rothstein SI (2000) Nest desertion and cowbird parasitism: evidence for evolved responses and evolutionary lag. Anim Behav 59:823–840
Johnston TD (1982) Selective costs and benefits in the evolution of learning. Adv Study Behav 12:65–106
Kleindorfer S, Evans C, Colombelli-Négrel D, Robertson J, Griggio M, Hoi H (2013) Host response to cuckoo song is predicted by the future risk of brood parasitism. Front Zool 10:1–10
Lahti DC, Lahti AR (2002) How precise is egg discrimination in weaverbirds? Anim Behav 63:1135–1142
Laland KN, Richerson PJ, Boyd R (1996) Developing a theory of animal social learning. In: Heyes CM, Galef BG Jr (eds) Social learning in animals: the roots of culture. Academic Press, San Diego, pp 129–154
Langmore NE, Stevens M, Maurer G, Heinsohn R, Hall ML, Peters A, Kilner RM (2001) Visual mimicry of host nestlings by cuckoos. Proc R Soc Lond B 278:2455–2463
Langmore NE, Hunt S, Kilner RM (2003) Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422:157–160
Langmore NE, Cockburn A, Russell AF, Kilner RM (2009) Flexible cuckoo chick-rejection rules in the superb fairy-wren. Behav Ecol 20:978–984
Langmore NE, Feeney WE, Crowe-Riddell J, Luan H, Louwrens KM, Cockburn A (2012) Learned recognition of brood parasitic cuckoos in the superb fairy-wren Malurus cyaneus. Behav Ecol 23:798–805
Lefebvre L, Giraldeau L-A (1996) Is social learning an adaptive specialization? In: Heyes CM, Galef BG Jr (eds) Social learning in animals. Academic Press, San Diego, pp 107–128
Li D, Wei H, Zhang Z, Liang W, Stokke BG (2015) Oriental reed warbler, Acrocephalus orientalis nest defence behaviour towards brood parasites and nest predators. Behaviour 152:1601–1621
Lindholm AK (1999) Brood parasitism by the cuckoo on patchy reed warbler populations in Britain. J Anim Ecol 68:293–309
Lindholm AK, Thomas RJ (2000) Differences between populations of reed warblers in defences against brood parasitism. Behaviour 137:25–42
Lotem A (1993) Learning to recognize nestlings is maladaptive for cuckoo Cuculus canorus hosts. Nature 362:743–745
Lotem A, Nakamura H, Zahavi A (1992) Rejection of cuckoo eggs in relation to host age – a possible evolutionary equilibrium. Behav Ecol 3:128–132
Lotem A, Nakamura H, Zahavi A (1995) Constraints on egg discrimination and cuckoo-host co-evolution. Anim Behav 49:1185–1209
Marchetti K (2000) Egg rejection in a passerine bird: size does matter. Anim Behav 59:877–883
Martín-Gálvez D, Soler M, Soler JJ, Martín-Vivald M, Palomino JJ (2005) Food acquisition by common cuckoo chicks in rufous bush robin nests and the advantage of eviction behaviour. Anim Behav 70:1313–1321
Medina I, Langmore NE (2016) Batten down the thatches: front-line defences in an apparently defenceless cuckoo host. Anim Behav 112:195–201
Mery F, Burns JG (2010) Behavioural plasticity: an interaction between evolution and experience. Evol Ecol 24:571–583
Moksnes A, Røskaft E (1989) Adaptations of meadow pipits to parasitism by the common cuckoo. Behav Ecol Sociobiol 24:25–30
Moksnes A, Røskaft E, Korsnes L (1993) Rejection of cuckoo (Cuculus canorus) eggs by meadow pipits (Anthus pratensis). Behav Ecol 4:120–127
Moksnes A, Røskaft E, Hagen LG, Honza M, Mörk C, Olsen PH (2000) Common cuckoo, Cuculus canorus, and host behaviour at reed warbler, Acrocephalus scirpaceus, nests. Ibis 142:247–258
Moskát C, Bán M, Székely T, Komdeur J, Lucassen RWG, van Boheemen LA, Hauber ME (2010) Discordancy or template-based recognition? Dissecting the cognitive basis of the rejection of foreign eggs in hosts of avian brood parasites. J Exp Biol 213:1976–1983
Nakamura H (1990) Brood parasitism by the cuckoo Cuculus canorus in Japan and the start of new parasitism on the azure-winged magpie Cyanopica cyana. Jpn J Ornithol 39:1–18
Neudorf DL, Sealy SG (1992) Reactions of four passerine species to threats of predation and cowbird parasitism: enemy recognition or generalized responses? Behaviour 123:84–105
Nováková N, Veselý P, Fuchs R (2017) Object categorization by wild ranging birds—winter feeder experiments. Behav Process 143:7–12
Patten M, Reinking D, Wolfe D (2011) Hierarchical cues in brood parasite nest selection. J Ornithol 152:521–532
Price TD, Qvarnström A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond B 270:1433–1440
Robert M, Sorci G (1999) Rapid increase of host defence against brood parasites in a recently parasitized area: the case of village weavers in Hispaniola. Proc R Soc Lond B 266:941–946
Røskaft E, Moksnes A, Stokke BG, Bicěk V, Moskàt C (2002) Aggression to dummy cuckoos by potential European cuckoo hosts. Behaviour 139:613–628
Rothstein SI (1975) Mechanisms of avian egg-recognition: do birds know their own eggs? Anim Behav 23:268–278
Sealy SG (1992) Removal of yellow warbler eggs in association with cowbird parasitism. Condor 94:40–54
Shettleworth SJ (2010) Cognition, evolution, and behaviour. Oxford University Press, New York
Shizuka D, Lyon BE (2010) Coots use hatch order to learn to recognize and reject conspecific brood parasitic chicks. Nature 463:223–226
Smith JNM, Arcese P, McLean IG (1984) Age, experience, and enemy recognition by wild song sparrows. Behav Ecol Sociobiol 14:101–106
Soler JJ, Martín-Gálvez D, de Neve L, Soler M (2013) Brood parasitism correlates with the strength of spatial autocorrelation of life history and defensive traits in Magpies. Ecology 94(6):1338–1346
Soler M (2011) Could egg rejection behaviour be transmitted by social learning? Anim Behav 81:e1–e6
Soler M, Martinez J, Soler J, Møller A (1994) Micro-evolutionary change in host response to a brood parasite. Behav Ecol Sociobiol 35:295–301
Soler M, Martín-Vivaldi M, Fernández-Morante J (2012) Conditional response by hosts to parasitic eggs: the extreme caseof the rufous-tailed scrub robin. Anim Behav 84:421–426
Soler M, de Neve L, Roncalli G, Macías-Sánchez E, Ibáñez-Álamo JD, Pérez-Contreras T (2014a) Great spotted cuckoo fledglings are disadvantaged by magpie host parents when reared together with magpie nestlings. Behav Ecol Sociobiol 68:333–342
Soler M, Pérez-Contreras T, Ibáñez-Álamo JD, Roncalli G, Macías-Sánchez E, de Neve L (2014b) Great spotted cuckoo fledglings often receive feedings from other magpie adults than their foster parents: which magpies accept to feed foreign cuckoo fledglings? PLoS One 9:e107412
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Stephens DW (1991) Change, regularity, and value in the evolution of animal learning. Behav Ecol 2:77–89
Stokke BG, Hafstad I, Rudolfsen G, Moksnes A, Møller AP, Røskaft E, Soler M (2008) Predictors of resistance to brood parasitism within and among reed warbler populations. Behav Ecol 19:612–620
Tewksbury JJ, Martin TE, Hejl SJ, Kuehn MJ, Jenkins JW (2002) Parental care of a cowbird host: caught between the costs of egg-removal and nest predation. Proc R Soc Lond B 269:423–429
Thorogood R, Davies NB (2012) Cuckoos combat socially transmitted defences of reed warbler hosts with a plumage polymorphism. Science 337:578–580
Thorogood R, Davies NB (2016) Combining personal with social information facilitates host defences and explains why cuckoos should be secretive. Sci Rep 6:19872
Tokue K, Ueda K (2010) Mangrove gerygones Gerygone laevigasert eject little bronze-cuckoo Chalcites minutillus hatchlings from parasitized nests. Ibis 152:835–839
Tollrian R, Harvell CD (1999) The ecology and evolution of inducible defences. Princeton University Press, Princeton, NJ
Trnka A, Prokop P (2012) The effectiveness of hawk mimicry in protecting cuckoos from aggressive hosts. Anim Behav 83:263–268
Trnka A, Požgayová M, Samaš P, Honza M (2013) Repeatability of host female and male aggression towards a brood parasite. Ethology 119:907–917
Uyehara JC, Narins PM (1995) Nest defence by willow flycatchers to brood-parasitic intruders. Condor 97:361–368
Welbergen JA, Davies NB (2008) Reed warblers discriminate cuckoos from sparrowhawks with graded alarm signals that attract mates and neighbours. Anim Behav 76:811–822
Welbergen JA, Davies NB (2009) Strategic variation in mobbing as a front line of defence against brood parasitism. Curr Biol 19:235–240
Welbergen JA, Davies NB (2011) A parasite in wolf's clothing: hawk mimicry reduces mobbing of cuckoos by hosts. Behav Ecol 22:574–579
Welbergen JA, Davies NB (2012) Direct and indirect assessment of parasitism risk by a cuckoo host. Behav Ecol 23:783–789
Welbergen J, Komdeur J, Kats R, Berg M (2001) Egg discrimination in the Australian reed warbler (Acrocephalus australis): rejection response toward model and conspecific eggs depending on timing and mode of artificial parasitism. Behav Ecol 12:8–15
Wyllie I (1981) The cuckoo. Batsford, London
Yang C, Wang L, Cheng S-J, Hsu Y-C, Liang W, Møller A (2014) Nest defenses and egg recognition of yellow-bellied prinia against cuckoo parasitism. Naturwissenschaften 101:727–734
Zentall TR, Wasserman EA, Urcuioli PJ (2014) Associative concept learning in animals. J Exp Anal Behav 101(1):130–151
Zölei A, Hauber ME, Geltsch N, Moskát C (2012) Asymmetrical signal content of egg shape as predictor of egg rejection by great reed warblers, hosts of the common cuckoo. Behaviour 149:391–406
Acknowledgements
Constructive comments from Manuel Soler and William E. Feeney greatly improved the early drafts of this chapter.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2017 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Campobello, D., Sealy, S.G., Welbergen, J.A. (2017). Anti-brood Parasite Defences: The Role of Individual and Social Learning. In: Soler, M. (eds) Avian Brood Parasitism. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-319-73138-4_23
Download citation
DOI: https://doi.org/10.1007/978-3-319-73138-4_23
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-73137-7
Online ISBN: 978-3-319-73138-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)