Abstract
Cuckoos (Cuculus spp.) parasitize the nest of many host birds; however, it is not clear why some potential hosts that occupy the same area as cuckoos are rarely or not used as hosts. Potential hosts might adopt a variety of strategies to defend against cuckoo parasitism, such as attacking adult cuckoos to keep them away from the nest, rejecting cuckoo eggs, or recognizing and refusing to feed cuckoo nestlings. We investigated the strategies used by grey-backed thrushes (Turdus hortulorum), a potential host of cuckoos, to prevent cuckoo or conspecific brood parasitism. Our results indicated that the attack rate of grey-backed thrushes on cuckoo dummies was very low (11.4%). Thrushes showed egg polymorphism and exhibited 100% rejection of non-artificial blue model eggs. Thrushes also failed to identify the eggs (8.3% of rejection) of conspecifics. Thus, grey-backed thrushes show a high egg rejection towards nonmimetic eggs, but low towards conspecific eggs. We suggest that egg recognition and rejection in grey-backed thrushes may be a strategy to cope with interspecific brood parasitism rather than conspecific brood parasitism, and have probably evolved due to previous cuckoo parasitism.
Significance statement
The explanations for high egg rejection in thrush (Turdus spp.) hosts were mixed without consistent conclusions. This study showed that grey-backed thrushes (Turdus hortulorum) show a high egg rejection towards nonmimetic eggs, but low towards conspecific eggs, suggesting that egg recognition and rejection in grey-backed thrushes may be a strategy to cope with interspecific brood parasitism rather than conspecific brood parasitism.
Similar content being viewed by others
References
Briskie JV, Sealy SG, Hobson KA (1990) Differential parasitism of least flycatchers and yellow warblers by the brown-headed cowbird. Behav Ecol Sociobiol 27:403–410
Briskie JV, Sealy SG, Hobson KA (1992) Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution 46:334–340
Campobello D, Sealy SG (2010) Enemy recognition of reed warblers (Acrocephalus scirpaceus): threats and reproductive value act independently in nest defence modulation. Ethology 116:498–508
Davies NB (2000) Cuckoos, cowbirds and other cheats. T. & A. D. Poyser, London, London
Davies NB, de M Brooke L (1989) An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts I. Host egg discrimination. J Anim Ecol 58:207–224
Fossøy F, Sorenson MD, Liang W et al (2016) Ancient origin and maternal inheritance of blue cuckoo eggs. Nat Commun 7:10272
Grim T (2005) Host recognition of brood parasites: implications for methodology in studies of enemy recognition. Auk 122:530–543
Grim T, Honza M (2001) Differences in behaviour of closely related thrushes (Turdus philomelos and T. merula) to experimental parasitism by the common cuckoo Cuculus canorus. Biologia 56:549–556
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 80:508–518
Hanley D, Samaš P, Heryan J, Hauber ME, Grim T (2015) Now you see it, now you don't: flushing hosts prior to experimentation can predict their responses to brood parasitism. Sci Rep 5:9060
Hauber ME, Samaš P, Anderson MG, Rutila J, Low J, Cassey P, Grim T (2013) Life-history theory predicts host behavioural responses to experimental brood parasitism. Ethol Ecol Evol 26:349–364
Hauber ME, Tong L, Bán M, Croston R, Grim T, Waterhouse GIN, Shawkey MD, Barron AB, Moskát C, Foster S (2015) The value of artificial stimuli in behavioral research: making the case for egg rejection studies in avian brood parasitism. Ethology 121:521–528
Honza M, Procházka P, Stokke BG, Moksnes A, Røskaft E, Čapek M, Mrlík V (2004) Are blackcaps current winners in the evolutionary struggle against the common cuckoo? J Ethol 22:175–180
Honza M, Kuiper SM, Cherry MI (2005) Behaviour of African turdid hosts towards experimental parasitism with artificial red chestedcuckoo Cuculus solitarius eggs. J Avian Biol 36:517–522
Liang W, Møller AP, Stokke BG et al (2016) Geographic variation in egg ejection rate by great tits across 2 continents. Behav Ecol 27:1405–1412
Mermoz ME, Fernández GJ (1999) Low frequency of shiny cowbird parasitism on scarlet-headed blackbirds: anti-parasite adaptations or nonspecific host life-history traits? J Avian Biol 30:15–22
Moksnes A, Røskaft E (1992) Responses of some rare cuckoo hosts to mimetic cuckoo eggs and to foreign conspecific eggs. Ornis Scand 23:17–23
Moksnes A, Røskaft E (1995) Egg-morphs and host preference in the Common Cuckoo (Cuculus canorus) an analysis of cuckoo and host eggs from European museum collections. J Zool 236:625–648
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 116:64–89
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
Payne RB (2005) The cuckoos. Oxford University Press, New York
Peer BD, Bollinger EK (1997) Explanations for the infrequent cowbird parasitism on common grackles. Condor 99:151–161
Peer BD, Sealy SG (2001) Conspecific brood parasitism and egg rejection in great-tailed grackles. J Avian Biol 31:271–277
Peer BD, Sealy SG (2004) Fate of grackle (Quiscalus spp.) defenses in the absence of brood parasitism: implications for long-term parasite-host coevolution. Auk 121:1172–1186
Petrie M, Møller AP (1991) Laying eggs in others' nests intraspecific brood parasitism in birds. Trends Ecol Evol 6:315–320
Polacikova L, Takasu F, Stokke BG, Moksnes A, Røskaft E, Cassey P, Hauber ME, Grim T (2013) Egg arrangement in avian clutches covaries with the rejection of foreign eggs. Anim Cogn 16:819–828
Røskaft E, Moksnes A, Stokke BG, Bicik V, Moskat C (2002) Aggression to dummy cuckoos by potential European cuckoo hosts. Behaviour 139:613–628
Rothstein SI (1975) An experimental and teleonomic investigation of avian brood parasitism. Condor 77:250–271
Rothstein SI, Robinson SK (1998) Parasitic birds and their hosts: studies in coevolution. Oxford University Press, Oxford
Ruiz-Raya F, Soler M, Roncalli G, Abaurrea T, Ibáñez-Álamo JD (2016) Egg rejection in blackbirds Turdus merula: a by-product of conspecific parasitism or successful resistance against interspecific brood parasites? Front Zool 13:16
Samaš P, Hauber ME, Cassey P, Grim T (2014) Host responses to interspecific brood parasitism: a by-product of adaptations to conspecific parasitism? Front Zool 11:34
Sealy SG, Bazin RC (1995) Low frequency of observed cowbird parasitism on eastern kingbirds host rejection, effective nest defense, or parasite avoidance. Behav Ecol 6:140–145
Sealy SG, Neudore 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 194–211
Soler M (2014) No evidence of conspecific brood parasitism provoking egg rejection in thrushes. Front Zool 11:68
Soler M, Ruiz-Raya F, Roncalli G, Ibáñez-Álamo JD (2015) Nest desertion cannot be considered an egg-rejection mechanism in a medium-sized host: an experimental study with the common blackbird Turdus merula. J Avian Biol 46:369–377
Soler M, Ruiz-Raya F, Roncalli G, Ibáñez-Álamo JD (2017) Relationships between egg-recognition and egg-ejection in a grasp-ejector species. PLoS One 12:e0166283
Stoddard MC, Stevens M, Svensson E (2011) Avian vision and the evolution of egg color mimicry in the common cuckoo. Evolution 65:2004–2013
Stokke BG, Rudolfsen G, Moksnes A, Røskaft E (2004) Rejection of conspecific eggs in chaffinches: the effect of age and clutch characteristics. Ethology 110:459–470
Stokke BG, Ratikainen II, Moksnes A, Røskaft E, Schulze-Hagen K, Leech DI, Møller AP, Fossøy F (2018) Characteristics determining host suitability for a generalist parasite. Sci Rep 8:6285
Yang C, Liang W, Cai Y et al (2010) Coevolution in action: disruptive selection on egg colour in an avian brood parasite and its host. PLoS One 5:e10816
Yang C, Stokke BG, Antonov A, Cai Y, Shi S, Moksnes A, Røskaft E, Møller AP, Liang W, Grim T (2013) Host selection in parasitic birds: are open-cup nesting insectivorous passerines always suitable cuckoo hosts? J Avian Biol 44:216–220
Yang C, Liu Y, Zeng L, Liang W (2014a) Egg color variation, but not egg rejection behavior, changes in a cuckoo host breeding in the absence of brood parasitism. Ecol Evol 4:2239–2246
Yang C, Wang L, Cheng SJ, Hsu YC, Stokke BG, Røskaft E, Moksnes A, Liang W, Møller AP (2014b) Deficiency in egg rejection in a host species as a response to the absence of brood parasitism. Behav Ecol 26:406–415
Yang C, Huang Q, Wang L, Jiang A, Stokke BG, Fossøy F, Tunheim OH, Røskaft E, Liang W, Møller AP (2016a) Plaintive cuckoos do not select tailorbird hosts that match the phenotypes of their own eggs. Behav Ecol 27:835–841
Yang C, Li Z, Zhang Y, Wang H, Liang W, Møller AP (2016b) Egg polymorphism and egg discrimination in the daurian redstart Phoenicurus auroreus, a host of the common cuckoo Cuculus canorus. Ornithol Sci 15:127–132
Yang C, Liang W, Møller AP (2017a) Why do hosts with obvious egg polymorphism suffer low parasitism rates under avian brood parasitism? A theoretical consideration. Behav Ecol Sociobiol 71:30
Yang C, Liang W, Møller AP (2017b) Egg color polymorphism in brood parasites and their hosts: adaptation and evolution. In: Soler M (ed) Avian brood parasitism: behaviour, ecology, evolution and coevolution. Springer International Publishing, Cham, pp 345–361
Yang C, Wang L, Liang W, Møller AP (2019) High egg rejection rate in a Chinese population of grey-backed thrush (Turdus hortulorum). Zool Res 40:226–230
Zhou D, Zhou C, Kong X, Deng W (2011) Nest-site selection and nesting success of grey-backed thrushes in northeast China. Wilson J Ornithol 123:492–501
Acknowledgments
We would like to thank Prof. Theo C. M. Bakker, Prof. M. Soler, and two anonymous reviewers for their constructive comments on an early version of this manuscript. We are grateful to Dagang Forestry Farm, Jilin, China, for their support and cooperation. We thank Bing Zhou for his assistance with the fieldwork.
Funding
This work was supported by the National Natural Science Foundation of China (Nos. 31372219 to WD, and 31772453 and 31970427 to WL).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare that they have no competing interests.
Ethics approval
All applicable international, national, and/or institutional guidelines for the use of animals were followed. The experiments comply with the current laws of China, where they were performed. Fieldwork was carried out with permission from Dagang Forestry Farm, Jilin. Experimental procedures were in agreement with the Animal Research Ethics Committee of Hainan Provincial Education Centre for Ecology and Environment, Hainan Normal University (permit no. HNECEE-2012-004).
Additional information
Communicated by M. Soler
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zhang, J., Shi, J., Deng, W. et al. Nest defense and egg recognition in the grey-backed thrush (Turdus hortulorum): defense against interspecific or conspecific brood parasitism?. Behav Ecol Sociobiol 73, 148 (2019). https://doi.org/10.1007/s00265-019-2759-8
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-019-2759-8