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The mutually antagonistic processes producing adaptations and counter-adaptations in avian brood parasites and their hosts provide a model system for the study of coevolution; this topic has long been an area of focus in ornithology and evolutionary biology. Although there is an extensive body of literature dealing with avian brood parasitism, few empirical studies have considered the effects of the coevolutionary processes associated with brood parasitism on the acoustic characteristics of parent–offspring communication. Under the strong selection pressures associated with brood parasitism, parasitic birds may, for instance, produce deceptive songs. The host may in turn evolve the ability to recognize these sounds as deceptive. At present, the mechanisms underlying the different competitive strategies employed by hosts and parasitic birds remain unclear. Here, we reviewed previous studies that investigated acoustic traits in scenarios of brood parasitism, highlighting possible adaptive functions. Using a meta-analysis, we identified no heterogeneity among studies of begging call adaptations in parasitic nestlings. However, our results may have been affected by the small number of applicable papers available for analysis. Our meta-analysis also suggested that studies of acoustic communication and transmission in adult hosts were highly heterogenous, suggesting that research methods were inconsistent among studies. Finally, we identified knowledge gaps and proposed several lines of future research.


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Coevolution of acoustical communication between obligate avian brood parasites and their hosts

Show Author's information Jiaojiao WangQihong LiCanchao Yang( )
College of Life Sciences, Hainan Normal University, Haikou, 571158, China

Abstract

The mutually antagonistic processes producing adaptations and counter-adaptations in avian brood parasites and their hosts provide a model system for the study of coevolution; this topic has long been an area of focus in ornithology and evolutionary biology. Although there is an extensive body of literature dealing with avian brood parasitism, few empirical studies have considered the effects of the coevolutionary processes associated with brood parasitism on the acoustic characteristics of parent–offspring communication. Under the strong selection pressures associated with brood parasitism, parasitic birds may, for instance, produce deceptive songs. The host may in turn evolve the ability to recognize these sounds as deceptive. At present, the mechanisms underlying the different competitive strategies employed by hosts and parasitic birds remain unclear. Here, we reviewed previous studies that investigated acoustic traits in scenarios of brood parasitism, highlighting possible adaptive functions. Using a meta-analysis, we identified no heterogeneity among studies of begging call adaptations in parasitic nestlings. However, our results may have been affected by the small number of applicable papers available for analysis. Our meta-analysis also suggested that studies of acoustic communication and transmission in adult hosts were highly heterogenous, suggesting that research methods were inconsistent among studies. Finally, we identified knowledge gaps and proposed several lines of future research.

Keywords: Acoustic communication, Brood parasitism, Coevolution, Parasitic adaptations, Anti-parasitic adaptations

References(182)

Abraham MM, Požgayová M, Procházka P, Piálková R, Honza M. Is there a sex-specific difference between parasitic chicks in begging behaviour? J Ethol. 2015; 33: 151–8.https://doi.org/10.1007/s10164-015-0427-7
DOI

Adams DB, Kitchen DM, Bshary R. Model vs. playback experiments: the impact of sensory mode on predator-specific escape responses in saki monkeys. Ethology. 2020; 126: 1–13.

Anderson MG, Hauber ME. A recognition-free mechanism for reliable rejection of brood parasites. Trends Ecol Evol. 2007; 22: 283–6.

Anderson MG, Ross HA, Brunton DH, Hauber ME. Begging call matching between a specialist brood parasite and its host: a comparative approach to detect coevolution. Biol J Linn Soc. 2009; 98: 208–16.

Attard MRG, Medina I, Langmore NE, Sherratt E. Egg shape mimicry in parasitic cuckoos. J Evol Biol. 2017; 30: 2079–84.

Avilés JM, Moskát C, Bán M, Hargitai R, Parejo D. Common cuckoos (Cuculus canorus) do not rely on indicators of parental abilities when searching for host nests: the importance of host defenses. Auk. 2009; 126: 431–8.

Banks AJ, Martin TE. Host activity and the risk of nest parasitism by brown-headed cowbirds. Behav Ecol. 2001; 12: 31–40.

Barash DP. Evolutionary aspects of parental behavior: distraction behavior of the Alpine Accentor. Wilson Bull. 1975; 87: 367–73.

Boncoraglio G, Saino N, Garamszegi LZ. Begging and cowbirds: brood parasites make hosts scream louder. Behav Ecol. 2009; 20: 215–21.

Book DL, Freeberg TM. Titmouse calling and foraging are affected by head and body orientation of cat predator models and possible experience with real cats. Anim Cogn. 2015; 18: 1155–64.

Briskie JV, Naugler CT, Leech SM. Begging intensity of nestling birds varies with sibling relatedness. Proc R Soc Lond B Biol Sci. 1994; 258: 73–8.

Budden AE, Wright J. Falling on deaf ears: the adaptive significance of begging in the absence of a parent. Behav Ecol Sociobiol. 2001; 49: 474–81.

Butchart SHM, Kilner RM, Fuisz T, Davies NB. Differences in the nestling begging calls of hosts and host-races of the common cuckoo, Cuculus canorus. Anim Behav. 2003; 65: 345–54.

Campobello D, Sealy SG. Enemy recognition of Reed Warblers (Acrocephalus scirpaceus): threats and reproductive value act independently in nest defence modulation. Ethology. 2010; 116: 498–508.

Campobello D, Sealy SG. Evolutionary significance of antiparasite, antipredator and learning phenotypes of avian nest defence. Sci Rep. 2018; 8: 10569.

Cantarero A, López-Arrabé J, Palma A, Redondo AJ, Moreno J. Males respond to female begging signals of need: a handicapping experiment in the pied flycatcher, Ficedula hypoleuca. Anim Behav. 2014; 94: 167–73.

Capek M, Petrusková T, Šebelíková Z, Campos Serrano J, Procházka P, Honza M, et al. Great Reed Warbler singing behavior and conspicuous song structures are not nest-location cues for the Common Cuckoo. J Ornithol. 2017; 158: 925–33.

Caro TM. Antipredator defenses in birds and mammals. Chicago: University of Chicago Press; 2005.

Caro SM, West SA, Griffin AS. Sibling conflict and dishonest signaling in birds. Proc Nat Acad Sci. 2016; 113: 13803–8.

Catchpole CK, Slater PJB. Bird song: biological themes and variations. 2nd ed. Cambridge: Cambridge University Press; 2008.https://doi.org/10.1017/CBO9780511754791
DOI
Chappell MA, Bachman GC. Energetic costs of begging behaviour. In: Wright J, Leonard ML, editors. The evolution of begging: competition, cooperation and communication. Dordrecht: Kluwer; 2002.
Clotfelter ED. What cues do Brown-headed Cowbirds use to locate Red-winged Blackbird host nests? Anim Behav. 1998; 55: 1181–9.https://doi.org/10.1006/anbe.1997.0638
DOI

Colombelli-Négrel D, Hauber ME, Kleindorfer S. Prenatal learning in an Australian songbird: habituation and individual discrimination in superb fairy-wren embryos. Proc Biol Sci. 2014; 281: 20141154.

Colombelli-Négrel D, Hauber ME, Robertson J, Sulloway FJ, Hoi H, Griggio M, et al. Embryonic learning of vocal passwords in superb fairy-wrens reveals intruder cuckoo nestlings. Curr Biol. 2012; 22: 2155–60.

Colombelli-Négrel D, Webster MS, Dowling JL, Hauber ME, Kleindorfer S. Vocal imitation of mother's calls by begging Red-backed Fairywren nestlings increases parental provisioning. Auk. 2016; 133: 273–85.

Courtney J. The juvenile food-begging call of some fledgling cuckoos-vocal mimicry or vocal duplication by natural selection. Emu. 1967; 67: 154–7.

Cunningham S, Magrath RD. Functionally referential alarm calls in noisy miners communicate about predator behaviour. Anim Behav. 2017; 129: 171–9.

Dall SR, Giraldeau LA, Olsson O, McNamara JM, Stephens DW. Information and its use by animals in evolutionary ecology. Trends Ecol Evol. 2005; 20: 187–93.

Davies NB. Cuckoos, cowbirds, and other cheats. London: T. & AD Poyser; 2000.

Davies NB. Cuckoo adaptations: trickery and tuning. J Zool. 2011; 284: 1–14.

Davies NB, Brooke MDL. An experimental study of co-evolution between the Cuckoo, Cuculus canorus, and its hosts. I. Host egg discrimination. J Anim Ecol. 1989; 58: 207–24.

Davies NB, Kilner RM, Noble DG. Nestling cuckoos, Cuculus canorus, exploit hosts with begging calls that mimic a brood. Proc R Soc B Biol Sci. 1998; 273: 693–9.

Davies NB, Madden JR, Butchart SH. Learning fine-tunes a specific response of nestlings to the parental alarm calls of their own species. Proc Biol Sci. 2004; 271: 2297–304.

Davies NB, Madden JR, Butchart SHM, Rutila J. A host-race of the cuckoo Cuculus canorus with nestlings attuned to the parental alarm calls of the host species. Proc R Soc B Biol Sci. 2006; 273: 693–9.

Davies NB, Welbergen JA. Cuckoo–hawk mimicry? An experimental test. Proc R Soc B Biol Sci. 2008; 275: 1817–22.

Dawkins R, Krebs JR. Arms races between and within species. Proc R Soc B Biol Sci. 1979; 205: 489–511.

Dawson Pell FSE, Potvin DA, Ratnayake CP, Fernández-Juricic E, Magrath RD, Radford AN. Birds orient their heads appropriately in response to functionally referential alarm calls of heterospecifics. Anim Behav. 2018; 140: 109–18.

De Mársico MC, Gantchoff MG, Reboreda JC. Host-parasite coevolution beyond the nestling stage? Mimicry of host fledglings by the specialist screaming cowbird. Proc Biol Sci. 2012; 279: 3401–8.

De Mársico MC, Ursino CA, Scardamaglia RC, Reboreda JC. Coevolutionary arms race between a specialist brood parasite, the Screaming Cowbird, and its host, the Grayish Baywing. J Ornithol. 2019; 160: 1221–33.

Dearborn DC. Brown-headed cowbird nestling vocalizations and risk of nest predation. Auk. 1999; 116: 448–57.

Deng Z, Lloyd H, Xia C, Moller AP, Liang W, Zhang Y. Components of variation in female common cuckoo calls. Behav Processes. 2019; 158: 106–12.

Dowling JL, Colombelli-Négrel D, Webster MS. Kin signatures learned in the egg? Red-backed fairy-wren songs are similar to their mother's in-nest calls and songs. Front Ecol Evol. 2016; 4: 48.

Duckworth JW. Responses of breeding reed warblers Acrocephalus scirpaceus to mounts of sparrowhawk Accipiter nisus, cuckoo Cuculus canorus and jay Garrulus glandarius. Ibis. 1991; 133: 68–74.

Dutour M, Cordonnier M, Léna J-P, Lengagne T. Seasonal variation in mobbing behaviour of passerine birds. J Ornithol. 2019; 160: 509–14.

Fallow PM, Pitcher BJ, Magrath RD. Alarming features: birds use specific acoustic properties to identify heterospecific alarm calls. Proc Biol Sci. 2013; 280: 20122539.

Feeney WE, Troscianko J, Langmore NE, Spottiswoode CN. Evidence for aggressive mimicry in an adult brood parasitic bird, and generalized defences in its host. Proc Biol Sci. 2015; 282: 893–6.

Feeney WE, Welbergen JA, Langmore NE. The frontline of avian brood parasite–host coevolution. Anim Behav. 2012; 84: 3–12.

Fishbein AR, Idsardi WJ, Ball GF, Dooling RJ. Sound sequences in birdsong: how much do birds really care? Philos Trans R Soc Lond B Biol Sci. 2020; 375: 20190044.https://doi.org/10.1098/rstb.2019.0044
DOI

Flower TP, Gribble M, Ridley AR. Deception by flexible alarm mimicry in an African bird. Science. 2014; 344: 513–6.

Garamszegi LZ, Avilés JM. Brood parasitism by brown-headed cowbirds and the expression of sexual characters in their hosts. Oecologia. 2005; 143: 167–77.

Gill SA, Neudorf DL, Sealy SG. Host responses to cowbirds near the nest: cues for recognition. Anim Behav. 1997; 53: 1287–93.

Gloag R, Kacelnik A. Host manipulation via begging call structure in the brood-parasitic shiny cowbird. Anim Behav. 2013; 86: 101–9.

Gluckman T-L, Mundy NI. Cuckoos in raptors' clothing: barred plumage illuminates a fundamental principle of Batesian mimicry. Anim Behav. 2013; 86: 1165–81.

Godard R. Long-term memory of individual neighbours in a migratory songbird. Nature. 1991; 350: 228–9.

Grim T. The evolution of nestling discrimination by hosts of parasitic birds: why is rejection so rare? Evol Ecol Res. 2006; 8: 785–802.
Grim T. Are Blackcaps (Sylvia atricapilla) defending their nests also calling for help from their neighbours? J Ornithol. 2008; 149: 169–80.https://doi.org/10.1007/s10336-007-0257-7
DOI
Grim T, Kleven O, Mikulica O. Nestling discrimination without recognition: a possible defence mechanism for hosts towards cuckoo parasitism? Proc Biol Sci. 2003; 270(Suppl 1): S73–5.https://doi.org/10.1098/rsbl.2003.0017
DOI

Haff TM, Magrath RD. Calling at a cost: elevated nestling calling attracts predators to active nests. Biol Lett. 2011; 7: 493–5.

Haff TM, Magrath RD. Learning to listen? Nestling response to heterospecific alarm calls. Anim Behav. 2012; 84: 1401–10.

Haskell D. Experimental evidence that nestling begging behaviour incurs a cost due to nest predation. Proc R Soc Lond B Biol Sci. 1994; 257: 161–4.

Haskell D. Begging behaviour and nest predation. In: Wright J, Leonard ML, editors. The evolution of begging: competition, cooperation and communication. Dordrecht: Kluwer; 2002.

Haskell DG. The effect of predation on begging-call evolution in nestling wood warblers. Anim Behav. 1999; 57: 893–901.

Hauber ME, Dearborn DC. Parentage without parental care: what to look for in genetic studies of obligate brood-parasitic mating systems. Auk. 2003; 120: 1–13.

Hauber ME, Kilner RM. Coevolution, communication, and host chick mimicry in parasitic finches: who mimics whom? Behav Ecol Sociobiol. 2007; 61: 497–503.

Hauber ME, Pearson HE, Reh A, Merges A. Discrimination between host songs by brood parasitic brown-headed cowbirds (Molothrus ater). Anim Cogn. 2002; 5: 129–37.

Hauber ME, Ramsey CK. Honesty in host-parasite communication signals: the case for begging by fledgling brown-headed cowbirds Molothrus ater. J Avian Biol. 2003; 34: 339–44.

Honza M, Taborsky B, Taborsky M, Teuschl Y, Vogl W, Moksnes A, et al. Behaviour of female common cuckoos, Cuculus canorus, in the vicinity of host nests before and during egg laying: a radiotelemetry study. Anim Behav. 2002; 64: 861–8.

Hurd CR. Interspecific attraction to the mobbing calls of blackcapped chickadees (Parus atricapillus). Behav Ecol Sociobiol. 1996; 38: 287–92.

Hurd PL, Enquist M. A strategic taxonomy of biological communication. Anim Behav. 2005; 70: 1155–70.

Jamie GA, de Silva WG. Similarity of the calls of juvenile pied cuckoo Clamator jacobinus and its Sri Lankan host species, yellow-billed babbler Turdoides affinis. Forktail. 2014; 30: 133–4.

Jamie GA, Kilner RM. Begging call mimicry by brood parasite nestlings: adaptation, manipulation and development. In: Soler M, editor. Avian brood parasitism Fascinating life sciences. Cham: Springer; 2017. p. 517–38.
Jelínek V, Karasová T, Weidinger K, Procházka P, Honza M. Do common cuckoo chicks suffer nest predation more than host nestlings? Behav Ecol Sociobiol. 2016; 70: 1975–87.

Jelínek V, Šulc M, Weidinger K, Honza M. Parent-absent begging and the risk of nest predation. J Ornithol. 2019; 160: 127–36.

Kacelnik A, Cotton PA, Stirling L, Wright J. Food allocation among nestling starlings: sibling competition and the scope of parental choice. Proc R Soc Lond B Biol Sci. 1995; 259: 259–63.

Kalb N, Anger F, Randler C. Subtle variations in mobbing calls are predator-specific in great tits (Parus major). Sci Rep-UK. 2019; 9: 6572.

Kalb N, Randler C. Behavioral responses to conspecific mobbing calls are predator-specific in great tits (Parus major). Ecol Evol. 2019; 9: 9207–13.

Katsis AC, Davies MH, Buchanan KL, Kleindorfer S, Hauber ME, Mariette MM. Prenatal exposure to incubation calls affects song learning in the zebra finch. Sci Rep-UK. 2018; 8: 15232.

Khayutin SN. Sensory factors in the behavioral ontogeny of altricial birds. Adv Stud Behav. 1985; 15: 105–52.

Kilner RM, Noble DG, Davies NB. Signals of need in parent–offspring communication and their exploitation by the common cuckoo. Nature. 1999; 397: 667–72.

Kim H, Lee J-W, Yoo J-C. Comparing vocal structures of the parasitic and nonparasitic groups in Cuculinae. Avian Res. 2017; 8: 27.

Kisilevsky BS, Hains SM, Brown CA, Lee CT, Cowperthwaite B, Stutzman SS, et al. Fetal sensitivity to properties of maternal speech and language. Infant Behav Dev. 2009; 32: 59–71.

Kleindorfer S, Evans C, Colombelli-Négrel D. Females that experience threat are better teachers. Biol Lett. 2014; 10: 20140046.

Kleindorfer S, Evans C, Hauber ME, Colombelli-Négrel D. Could prenatal sound discrimination predict vocal complexity later in life? BMC Zoology. 2018; 3: 11–9.

Kondo N, Watanabe S. Contact calls: Information and social function. Jpn Psychol Res. 2009; 51: 197–208.

Langmore NE, Cockburn A, Russell AF, Kilner RM. Flexible cuckoo chick-rejection rules in the superb fairy-wren. Behav Ecol. 2009; 20: 978–84.

Langmore NE, Maurer G, Adcock GJ, Kilner RM. Socially acquired host-specific mimicry and the evolution of host races in Horsfield's bronze-cuckoo Chalcites basalis. Evolution. 2008; 62: 1689–99.

Langmore NE, Spottiswoode CN. Visual trickery in avian brood parasites. In: Hughes DP, Brodeur J, Thomas F, editors. Host manipulation by parasites. Oxford: Oxford University Press; 2012.

Langmore NT, Hunt S, Kilner RM. Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature. 2003; 422: 157–60.

Langmore NE, Stevens M, Maurer G, Heinsohn R, Hall ML, Peters A, et al. Visual mimicry of host nestlings by cuckoos. Proc Biol Sci. 2011; 278: 2455–63.

Lee J-W, Kim H-N, Yoo S, Yoo J-C. Common cuckoo females may escape male sexual harassment by color polymorphism. Sci Rep-UK. 2019; 9: 7515.

Leech SM, Leonard ML. Begging and the risk of predation in nestling birds. Behav Ecol. 1997; 8: 644–6.

Leonard M, Horn A. Dynamics of calling by tree swallow (Tachycineta bicolor) nestmates. Behav Ecol Sociobiol. 2001; 50: 430–5.

Leonard ML, Horn AG. Ambient noise and the design of begging signals. Proc Biol Sci. 2005; 272: 651–6.

Leonard ML, Horn AG, Porter J. Does begging affect growth in nestling tree swallows, Tachycineta bicolor? Behav Ecol Sociobiol. 2003; 54: 573–7.

Li D, Wei H, Zhang Z, Liang W, Stokke BG. Oriental reed warbler (Acrocephalus orientalis) nest defence behaviour towards brood parasites and nest predators. Behaviour. 2015; 152: 1601–21.

Liang W, Møller AP. Hawk mimicry in cuckoos and anti-parasitic aggressive behavior of barn swallows in Denmark and China. J Avian Biol. 2015; 46: 216–23.

Lichtenstein G. Selfish begging by screaming cowbirds, a mimetic brood parasite of the bay-winged cowbird. Anim Behav. 2001; 61: 1151–8.

Lorenzana JC, Sealy SG. Are begging calls of generalist parasitic cowbirds adapted for brood parasitism? UFS (Delta Marsh). Annu Rep. 1996; 31: 85–93.

Louder MIM, Balakrishnan CN, Louder AAN, Driver RJ, London SE, Hauber ME. An acoustic password enhances auditory learning in juvenile brood parasitic cowbirds. Curr Biol. 2019; 29(4045–51): e3.

Lyon BE, Gilbert GS. Rarely parasitized and unparasitized species mob and alarm call to cuckoos: implications for sparrowhawk mimicry by brood parasitic cuckoos. Wilson J Ornithol. 2013; 125: 627–30.

Ma L, Yang C, Liang W. Hawk mimicry does not reduce attacks of cuckoos by highly aggressive hosts. Avian Res. 2018; 9: 35.

Madden JR, Davies NB. A host-race difference in begging calls of nestling cuckoos Cuculus canorus develops through experience and increases host provisioning. Proc Biol Sci. 2006; 273: 2343–51.

Madden JR, Kilner RM, Davies NB. Nestling responses to adult food and alarm calls: 1. Species-specific responses in two cowbird hosts. Anim Behav. 2005a; 70: 619–27.
Madden JR, Kilner RM, Davies NB. Nestling responses to adult food and alarm calls: 2. Cowbirds and red-winged blackbirds reared by eastern phoebe hosts. Anim Behav. 2005b; 70: 629–37.
Marler P. Bird calls: a cornucopia for communication. In: Marler P, Slabbekoorn H, editors. Nature's music. San Diego: Academic Press; 2004.

Marton A, Fülöp A, Ozogány K, Moskát C, Bán M. Host alarm calls attract the unwanted attention of the brood parasitic common cuckoo. Sci Rep-UK. 2019; 9: 1–11.

McLean LG, Griffin JM. Structure, function, and mimicry in begging calls of passerines and cuckoos. Acta Int Ornithol Congress. 1991; 2: 1273–84.

Mclean IG, Waas JR. Do cuckoo chicks mimic the begging calls of their hosts? Anim Behav. 1987; 35: 1896–8.

Møller AP, Stokke BG, Samia DSM. Hawk models, hawk mimics, and antipredator behavior of prey. Behav Ecol. 2015; 26: 1039–44.

Montgomerie RD, Weatherhead PJ. Risk and rewards of nest defence by parent birds. Q Rev Biol. 1988; 63: 167–87.

Moon C, Lagercrantz H, Kuhl PK. Language experienced in utero affects vowel perception after birth: a two-country study. Acta Paediatr. 2013; 102: 156–60.

Morton ES, Farabaugh SM. Infanticide and other adaptations of the nestling striped cuckoo Tapera naevia. Ibis. 1979; 121: 212–3.

Moskát C. Nest defence and egg rejection in great reed warblers over the breeding cycle: are they synchronised with the risk of brood parasitism? Ann Zool Fenn. 2005; 42: 579–86.
Moskát C, Elek Z, Bán M, Geltsch N, Hauber ME. Can common cuckoos discriminate between neighbours and strangers by their calls? Anim Behav. 2017; 126: 253–60.

Mundy PJ. Vocal mimicry of their hosts by nestlings of the great spotted cuckoo and striped crested cuckoo. Ibis. 1973; 115: 602–4.

Neuenschwander S, Brinkhof MW, Kölliker M, Richner H. Brood size, sibling competition, and the cost of begging in great tits (Parus major). Behav Ecol. 2003; 14: 457–62.

Nieder A, Mooney R. The neurobiology of innate, volitional and learned vocalizations in mammals and birds. Philos Trans R Soc Lond B Biol Sci. 2020; 375: 20190054.

Noguera JC, Velando A. Bird embryos perceive vibratory cues of predation risk from clutch mates. Nat Ecol Evol. 2019; 3: 1225–32.

Noh H-J, Gloag R, Langmore NE. True recognition of nestlings by hosts selects for mimetic cuckoo chicks. Proc R Soc B: Biol Sci. 2018; 285: 20180726.

Norman RF, Robertson RJ. Nest-searching behavior in the brown-headed cowbird. Auk. 1975; 92: 610–1.

Pagnucco K, Zanette L, Clinchy M, Leonard ML. Sheep in wolf's clothing: host nestling vocalizations resemble their cowbird competitor's. Proc R Soc B Biol Sci. 2008; 275: 1061–5.

Partan SR. Ten unanswered questions in multimodal communication. Behav Ecol Sociobiol. 2013; 67: 1523–39.

Patterson TL, James LPK. Reproductive value and appropriateness of response to predators by white-crowned sparrows. Behav Ecol Sociobiol. 1980; 7: 227–31.

Payne RB, Payne LL. Begging for parental care from another species: specialization and generalization in brood-parasitic finches. Dordrecht: Springer; 2002.

Platzen D, Magrath RD. Adaptive differences in response to two types of parental alarm call in altricial nestlings. Proc Biol Sci. 2005; 272: 1101–6.

Price K, Harvey H, Ydenberg RON. Begging tactics of nestling yellow-headed blackbirds, Xanthocephalus xanthocephalus, in relation to need. Anim Behav. 1996; 51: 421–35.

Rackham H. Pliny: natural history. Cambridge: Harvard University Press; 1997.

Ranger GA. On three species of honey-guide; the Greater; (Indicator indicator) the Lesser (Indicator minor) and the Scaly-throated (Indicator variegatus). Ostrich. 1955; 26: 70–87.

Redondo T. Exploitation of host mechanisms for parental care by avian brood parasites. Etologia. 1993; 3: 235–97.

Redondo T, Reyna LAD. Vocal mimicry of hosts by great spotted cuckoo Clamator glandarius: further evidence. Ibis. 1988; 130: 540–4.

Rek P. Acoustic location of conspecifics in a nocturnal bird: the corncrake Crex crex. Acta Ethol. 2014; 17: 31–5.

Rivera M, Louder MIM, Kleindorfer S, Wan-chun L, Hauber ME. Avian prenatal auditory stimulation: progress and perspectives. Behav Ecol Sociobiol. 2018; 72: 112.

Rivers JW. Nest mate size, but not short-term need, influences begging behavior of a generalist brood parasite. Behav Ecol. 2007; 18: 222–30.

Rivers JW, Blundell MA, Loughin TM, Peer BD, Rothstein SI. The exaggerated begging behaviour of an obligate avian brood parasite is shared with a nonparasitic close relative. Anim Behav. 2013; 86: 529–36.

Rivers JW, Briskie JV, Rothstein SI. Have brood parasitic cowbird nestlings caused the evolution of more intense begging by host nestlings? Anim Behav. 2010; 80: e1-5.

Rivers JW, Loughin TM, Rothstein SI. Brown-headed cowbird nestlings influence nestmate begging, but not parental feeding, in hosts of three distinct sizes. Anim Behav. 2010; 79: 107–16.

Rodríguez-Gironés MA, Zúñiga JM, Redondo T. Feeding experience and relative size modify the begging strategies of nestlings. Behav Ecol. 2002; 13: 782–5.

Rojas Ripari JM, Segura LN, Reboreda JC, De Mársico MC. Non-mimetic shiny cowbird nestlings escape discrimination by baywings in absence of host nest mates. Behav Ecol Sociobiol. 2019; 73: 135–43.

Rojas Ripari JM, Ursino CA, Reboreda JC, De Mársico MC. Innate development of acoustic signals for host parent–offspring recognition in the brood-parasitic Screaming Cowbird Molothrus rufoaxillaris. Ibis. 2018; 161: 717–29.

Rosenthal GG. The use of playbacks in behavioral experiments. US: Elsevier; 2019. p. 529–34.

Rothstein SI. A model system for coevolution: avian brood parasitism. Annu Rev Ecol Syst. 1990; 21: 481–508.

Rubi TL, Stephens DW. Should receivers follow multiple signal components? An economic perspective. Behav Ecol. 2016; 27: 36–44.

Samaš P, Žabková K, Petrusková T, Procházka P, Požgayová M, Honza M. Nestlings of the common cuckoo do not mimic begging calls of two closely related Acrocephalus hosts. Anim Behav. 2020; 161: 89–94.

Slabbekoorn H, Smith TB. Bird song, ecology and speciation. Philos Trans R Soc Lond B Biol Sci. 2002; 357: 493–503.

Smith JM. Parental investment: a prospective analysis. Anim Behav. 1977; 25: 1–9.

Smith HG, Montgomerie R. Nestling American robins compete with siblings by begging. Behav Ecol Sociobiol. 1991; 29: 307–12.

Soler M. Breeding strategy and begging intensity: influences on food delivery by parents and host selection by parasitic cuckoos. In: Wright J, Leonard ML, editors. The evolution of begging: competition, cooperation and communication. Dordrecht: Kluwer Academic; 2002.

Soler M. Long-term coevolution between avian brood parasites and their hosts. Biol Rev. 2014; 89: 688–704.

Soler M. Begging behaviour, food delivery and food acquisition in nests with brood parasitic nestlings. In: Soler M, editor. Avian brood parasitism. Fascinating life sciences. Cham: Springer; 2017. p. 493–515.

Soler M, de Neve L, Macías-Sánchez E, Pérez-Contreras T. Great spotted cuckoos respond earlier to the arrival of feeding foster parents and perform less erroneous begging when hungry than their magpie host nest-mates. J Avian Biol. 2019; 50: e01952.

Soler M, Soler JJ, Martinez JG, Møller AP. Magpie host manipulation by great spotted cuckoos: evidence for an Avian Mafia? Evolution. 1995; 49: 770–5.

Suzuki TN. Parental alarm calls warn nestlings about different predatory threats. Curr Biol. 2011; 21: R15–6.

Suzuki TN. Referential mobbing calls elicit different predator-searching behaviours in Japanese great tits. Anim Behav. 2012; 84: 53–7.

Suzuki TN. Communication about predator type by a bird using discrete, graded and combinatorial variation in alarm calls. Anim Behav. 2014; 87: 59–65.

Thorogood R, Davies NB. Hawk mimicry and the evolution of polymorphic cuckoos. Chin Birds. 2013; 4: 39–50.

Trnka A, Grim T. Color plumage polymorphism and predator mimicry in brood parasites. Front Zool. 2013; 10: 25–34.

Trnka A, Prokop P. The effectiveness of hawk mimicry in protecting cuckoos from aggressive hosts. Anim Behav. 2012; 83: 263–8.

Trnka A, Prokop P, Grim T. Uncovering dangerous cheats: how do avian hosts recognize adult brood parasites? PLoS ONE. 2012; 7: e37445.

Trnka A, Trnka M, Grim T. Do rufous common cuckoo females indeed mimic a predator? An experimental test. Biol J Linn Soc. 2015; 116: 134–43.

Uyehara JC, Narins PM. Nest defense by willow flycatchers to brood-parasitic intruders. Condor. 1995; 97: 361–8.

Villain A. Acoustic communication in female songbirds: functions, flexibility and plasticity in calls. PhD Thesis. Lyon: University of Lyon. 2016.

Voipio P. The hepaticus variety and the juvenile types of the cuckoo. Ornis Fenn. 1953; 30: 97–117.

Walton B, Kershenbaum A. Heterospecific recognition of referential alarm calls in two species of lemur. Bioacoustics. 2019; 28: 592–603.

Wang J, Ma L, Liang W, Yang C. Responses of cuckoo hosts to alarm signals of different nest intruders in non-nesting areas. Zool Res. 2020; 41: 345–50.

Wang J, Yang C. Specific responses of cuckoo hosts to different alarm signals according to breeding stage: a test of the offspring value hypothesis. Curr Zool. 2020. https://doi.org/10.1093/cz/zoaa021

Welbergen JA, Davies NB. Reed warblers discriminate cuckoos from sparrowhawks with graded alarm signals that attract mates and neighbours. Anim Behav. 2008; 76: 811–22.

Welbergen JA, Davies NB. Strategic variation in mobbing as a front line of defense against brood parasitism. Curr Biol. 2009; 19: 235–40.

Welbergen JA, Davies NB. A parasite in wolf's clothing: hawk mimicry reduces mobbing of cuckoos by hosts. Behav Ecol. 2011; 22: 574–9.

Whittingham MJ, Butler SJ, Quinn JL, Cresswell W. The effect of limited visibility on vigilance behaviour and speed of predator detection: implications for the conservation of granivorous passerines. Oikos. 2004; 106: 377–85.

Wojas LE, Podkowa PW, Osiejuk TS. A nocturnal rail with a simple territorial call eavesdrops on interactions between rivals. PLoS ONE. 2018; 13: e0197368.

Yang C, Huang J, Liang W, Møller AP. Absence of anti-parasitic defenses in an Asian population of the magpie, a regular host of the great spotted cuckoo in Europe. Curr Zool. 2020. https://doi.org/10.1093/cz/zoaa018
Yang C, Liang W, Moller AP. Similar immediate costs of raising cuckoo and host chicks can hardly explain low levels of antiparasite defence in hosts. A comment on: Samas et al. (2018). Proc Biol Sci. 2019; 286: 20182430.
Yang C, Si X, Liang W, Møller AP. Spatial variation in egg polymorphism among cuckoo hosts across four continents. Curr Zool. 2020. https://doi.org/10.1093/cz/zoaa011

Yang C, Wang L, Cheng SJ, Hsu YC, Liang W, Moller AP. Nest defenses and egg recognition of yellow-bellied prinia against cuckoo parasitism. Naturwissenschaften. 2014; 101: 727–34.

Yasukawa K, Sollenberger J, Lindsey-Robbins J, DeBruyn E. Calling in the face of danger: do nestling Red-winged Blackbirds (Agelaius phoeniceus) suppress begging in response to predator playbacks? Auk. 2020; 137: ukz071.

Yoo S, Kim HN, Lee JW, Yoo JC. Seasonal and diurnal patterns of population vocal activity in avian brood parasites. Ibis. 2020; 162: 1001–11.

York JE, Davies NB. Female cuckoo calls misdirect host defences towards the wrong enemy. Nat Ecol Evol. 2017; 1: 1520–5.

Yu J, Lu H, Sun W, Liang W, Wang H, Møller AP. Heterospecific alarm-call recognition in two warbler hosts of common cuckoos. Anim Cogn. 2019; 22: 1149–57.

Yu J, Lv W, Xu H, Bibi N, Yu Y, Jiang Y, et al. Function of note strings in Japanese Tit alarm calls to the Common Cuckoo: a playback experiment. Avian Res. 2017; 8: 22.

Yu J, Sun W, Liang W, Wang H, Møller AP. Differently sized cuckoos pose different threats to hosts. Curr Zool. 2019; 22: 1149–57.

Yu J, Wang L, Xing X, Yang C, Ma J, Møller AP, et al. Barn swallows (Hirundo rustica) differentiate between common cuckoo and sparrowhawk in China: alarm calls convey information on threat. Behav Ecol Sociobiol. 2016; 70: 171–8.

Yu J, Xing X, Jiang Y, Liang W, Wang H, Møller AP, et al. Alarm call-based discrimination between common cuckoo and Eurasian sparrowhawk in a Chinese population of great tits. Ethology. 2017; 123: 542–50.

Publication history
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Publication history

Received: 02 June 2020
Accepted: 23 October 2020
Published: 03 November 2020
Issue date: January 2020

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© The Author(s) 2020.

Acknowledgements

We thank the anonymous reviewers for helpful suggestions that improved our manuscript.

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