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Recognition and rejection of foreign eggs are effective defense of hosts against brood parasitism. However, brood parasitism can impose various selection pressures on different geographic populations of the same host species. In a multiple cuckoo system in China, Azure-winged Magpies (Cyanopica cyanus) are parasitized by both Indian Cuckoos (Cuculus micropterus) and Asian Koels (Eudynamys scolopaceus). In this study, egg recognition ability and recognition mechanism of the Azure-winged Magpie were investigated using a population in Fusong, southeastern Jilin, China. The results showed that 55.6% (20/36) of the Azure-winged Magpies correctly rejected quail (Coturnix japonica) eggs in their nests, while 13.9% (5/36) of the individuals experienced rejection costs by wrongly rejecting their own eggs. Azure-winged Magpies could accurately reject the experimental eggs when the number of such eggs in the nests was the same as that of the magpie eggs. However, Azure-winged Magpies do not recognize and reject conspecific eggs (0/28). The present study indicates that the Azure-winged Magpie has moderate egg recognition ability toward non-mimetic quail eggs and shows a true recognition mechanism with rejecting foreign eggs by accurately recognizing their own eggs. However, they cannot recognize conspecific eggs.


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Egg rejection and egg recognition mechanism in a Chinese Azure-winged Magpie (Cyanopica cyanus) population

Show Author's information Jianping LiuaLongwu WangbWei Liangc( )
College of Biological Sciences and Engineering, North Minzu University, Yinchuan 750021, China
School of Life Sciences, Guizhou Normal University, Guiyang 550001, China
Ministry of Education Key Laboratory for Ecology of Tropical Islands, Key Laboratory of Tropical Animal and Plant Ecology of Hainan Province, College of Life Sciences, Hainan Normal University, Haikou 571158, China

Abstract

Recognition and rejection of foreign eggs are effective defense of hosts against brood parasitism. However, brood parasitism can impose various selection pressures on different geographic populations of the same host species. In a multiple cuckoo system in China, Azure-winged Magpies (Cyanopica cyanus) are parasitized by both Indian Cuckoos (Cuculus micropterus) and Asian Koels (Eudynamys scolopaceus). In this study, egg recognition ability and recognition mechanism of the Azure-winged Magpie were investigated using a population in Fusong, southeastern Jilin, China. The results showed that 55.6% (20/36) of the Azure-winged Magpies correctly rejected quail (Coturnix japonica) eggs in their nests, while 13.9% (5/36) of the individuals experienced rejection costs by wrongly rejecting their own eggs. Azure-winged Magpies could accurately reject the experimental eggs when the number of such eggs in the nests was the same as that of the magpie eggs. However, Azure-winged Magpies do not recognize and reject conspecific eggs (0/28). The present study indicates that the Azure-winged Magpie has moderate egg recognition ability toward non-mimetic quail eggs and shows a true recognition mechanism with rejecting foreign eggs by accurately recognizing their own eggs. However, they cannot recognize conspecific eggs.

Keywords: Cuckoo parasitism, Egg rejection, True recognition, Azure-winged Magpie, Recognition error

References(55)

Alonso, J.A., Muñoz-Pulido, R., Bautista, L.M., Alonso, J.C., 1991. Nest-site selection and nesting success in the azure-winged magpie in Central Spain. Hous. Theor. Soc. 38, 45–51.

Avilés, J.M., Parejo, D., 2012. Intra-clutch variation in egg appearance assessed by human vision does not relate to rejection of parasite eggs in Iberian azure-winged magpies. Chinese Birds 3, 302–311.

Avilés, J.M., 2004. Egg rejection by Iberian azure-winged magpies Cyanopica cyanus in the absence of brood parasitism. J. Avian Biol. 35, 295–299.

Bán, M., Moskát, C., Barta, Z., Hauber, M.E., 2013. Simultaneous viewing of own and parasitic eggs is not required for egg rejection by a cuckoo host. Behav. Ecol. 24, 1014–1021.

Begum, S., Moksnes, A., Røskaft, E., Stokke, B.G., 2012. Responses of potential hosts of Asian cuckoos to experimental parasitism. Ibis 154, 363–371.

Davies, N.B., 2000. Cuckoos, Cowbirds and Other Cheats. T & AD Poyser, London.
Erritzøe, J., Mann, C.F., Brammer, F., Fuller, R.A., 2012. Cuckoos of the World. Christopher Helm, London.

Feeney, W.E., Welbergen, J.A., Langmore, N.E., 2014. Advances in the study of coevolution between avian brood parasites and their hosts. Annu. Rev. Ecol. Evol. Syst. 45, 227–246.

Golüke, S., Dörrenberg, S., Krause, E.T., Caspers, B.A., 2016. Female zebra finches smell their eggs. PLoS One 11, e0155513.

Krüger, O., 2011. Brood parasitism selects for no defence in a cuckoo host. Proc. R. Soc. B 278, 2777–2783.

Leclaire, S., Bourret, V., Bonadonna, F., 2017. Blue petrels recognize the odor of their egg. J. Exp. Biol. 220, 3022–3025.

Lee, J.W., 2014. Searching for hosts of avian brood parasites breeding in Korea. Korean J. Ornithol. 21, 25–37.

Liang, W., Møller, A.P., Stokke, B.G., Yang, C., Kovařík, P., Wang, H., et al., 2016. Geographic variation in egg ejection rate by great tits across 2 continents. Behav. Ecol. 27, 1405–1412.

Liu, J., Yang, C., Yu, J., Wang, H., Liang, W., 2019. Egg recognition in cinereous tits (Parus cinereus): eggshell spots matter. Avian Res. 10, 37.

Liu, J., Zhang, L., Zhang, L., Yang, C., Yao, C.-T., Lu, X., et al., 2020. Egg recognition abilities of tit species in the Paridae family: do Indomalayan tits exhibit higher recognition than Palearctic tits? Zool. Res. 41, 726–732.

Luro, A.B., Igic, B., Croston, R., López, A.V., Shawkey, M.D., Hauber, M.E., 2018. Which egg features predict egg rejection responses in American robins? Replicating Rothstein's (1982) study. Ecol. Evol. 8, 1673–1679.

Lyon, B., 2007. Mechanism of egg recognition in defenses against conspecific brood parasitism: American coots (Fulica americana) know their own eggs. Behav. Ecol. Sociobiol. 61, 455–463.

Ma, L., Liang, W., 2021. Egg rejection and egg recognition mechanisms in Oriental reed warblers. Avian Res 12, 47.

Madge, S., 2020. Asian azure-winged magpie (Cyanopica cyanus). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A., Juana, E.D. (Eds.), Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona.
DOI
Madge, S., Juana, E.D., 2020. Iberian azure-winged magpie (Cyanopica cooki). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A., Juana, E.D. (Eds.), Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona.
DOI
Manna, T., Moskát, C., Hauber, M.E., 2017. Cognitive decision rules for egg rejection. In: Soler, M. (Ed.), Avian Brood Parasitism: Behaviour, Ecology, Evolution and Coevolution. Springer International Publishing, Cham, pp. 437–448.
DOI

Meshcheryagina, S.G., Golovatin, M.G., Bachurin, G.N., 2016. Experimental study of discrimination behavior in the yellow-browed warbler (Phylloscopus inornatus) brood-parasitized by the oriental cuckoo (Cuculus (saturatus) optatus). Russ. J. Ecol. 47, 104–106.

Moksnes, A., Røskaft, E., Braa, A.T., Korsnes, L., Lampe, H.L., Pedersen, H.C., 1991. Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour 116, 64–89.

Moskát, C., Bán, M., Székely, T., Komdeur, J., Lucassen, R.W., van Boheemen, L.A., et al., 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.

Moskát, C., Hauber, M.E., Avilés, J.M., Bán, M., Hargitai, R., Honza, M., 2009. Increased host tolerance of multiple cuckoo eggs leads to higher fledging success of the brood parasite. Anim. Behav. 77, 1281–1290.

Moskát, C., Zölei, A., Bán, M., Elek, Z., Tong, L., Geltsch, N., et al., 2014. How to spot a stranger's egg? A mimicry-specific discordancy effect in the recognition of parasitic eggs. Ethology 120, 616–626.

Nakamura, H., Kubota, S., Suzuki, R., 1998. Coevolution between the common cuckoo and its major hosts in Japan. In: Rothstein, S.I., Robinson, S.K. (Eds.), Parasitic Birds and Their Hosts: Studies in Coevolution. Oxford University Press, New York, pp. 94–112.

Roncalli, G., Ibáñez-Álamo, J.D., Soler, M., 2017. Size and material of model parasitic eggs affect the rejection response of Western Bonelli's warbler Phylloscopus bonelli. Ibis 159, 113–123.

Rothstein, S.I., 1975. Mechanisms of avian egg-recognition: do birds know their own eggs? Anim. Behav. 23, 268–278.

Ruiz-Raya, F., Soler, M., 2020. Signal detection and optimal acceptance thresholds in avian brood parasite-host systems: Implications for egg rejection. Philos. T. Roy. Soc. B 375, 20190477.

Ruiz-Raya, F., Soler, M., Roncalli, G., Abaurrea, T., Ibáñez-Álamo, J.D., 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, M.E., Honza, M., 2021. A meta-analysis of avian egg traits cueing egg-rejection defenses against brood parasitism. Front. Ecol. Evol. 9, 703208.

Shang, Y., Li, L., Wang, F., Wang, H., 1994. Behavioural ecology of Azure-winged Magpie (Cyanopica cyana) during its breeding period. Chin. J. Appl. Ecol. 5, 263–268.

Soler, J.J., Pérez-Contreras, T., de Neve, L., Macías-Sánchez, E., Møller, A.P., Soler, M., 2014. Recognizing odd smells and ejection of brood parasitic eggs. An experimental test in magpies of a novel defensive trait against brood parasitism. J. Evol. Biol. 27, 1265–1270.

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

Soler, M., Pérez-Contreras, T., Soler, J.J., 2015. Synchronization of laying by great spotted cuckoos and recognition ability of magpies. J. Avian Biol. 46, 608–615.

Son, S.J., Kim, J.S., Lee, J.W., Nam, K.B., Yoo, J.C., 2015. Egg recognition and rejection ability of azure-winged magpies (Cyanopica cyanus). Korean J. Ornithol. 22, 37–45.

Son, S.J., Kim, J.S., Lee, J.W., Nam, K.B., Yoo, J.C., 2022. Rejection of conspecific eggs associated with the appearance of eggs, in the azure-winged magpie Cyanopica cyanus in Korea. Ornithol. Sci. 21, 45–52.

Stevens, M., Troscianko, J., Spottiswoode, C.N., 2013. Repeated targeting of the same hosts by a brood parasite compromises host egg rejection. Nat. Commun. 4, 2475.

Swynnerton, C.F.M., 1918. Rejections by birds of eggs unlike their own: with remarks on some of the cuckoo problems. Ibis 60, 127–154.

Takasu, F., Kawasaki, K., Nakamura, H., Cohen, J.E., Shigesada, N., 1993. Modeling the population dynamics of a cuckoo-host association and the evolution of host defenses. Am. Nat. 142, 819–839.

Tosi-Germán, R.A., Tassino, B., Reboreda, J.C., 2020. Female and male rufous horneros eject shiny cowbird eggs using a mental template of the size of their own eggs. Behav. Process. 178, 104152.

Valencia, J., de la Cruz, C., González, B., 2003. Flexible helping behaviour in the azure-winged magpie. Ethology 109, 545–558.

Valencia, J., de la Cruz, C., Carranza, J., Solís, E., 2005. No brood parasitism by the great spotted cuckoo Clamator glandarius on the azure-winged magpie Cyanopica cyanus. Hous. Theor. Soc. 52, 204–209.

Wang, L., Yang, C., Hsu, Y.-C., Antonov, A., Moksnes, A., Røskaft, E., et al., 2013. Increase of clutch size triggers clutch destruction behaviour in common moorhens (Gallinula chloropus) during the incubation period. Behaviour 150, 215–223.

Yang, C., Liang, W., Antonov, A.T., Cai, Y., Stokke, B.G., Fossøy, F., et al., 2012. Diversity of parasitic cuckoos and their hosts in China. Chinese Birds 3, 9–32.

Yang, C., Møller, A.P., Røskaft, E., Moksnes, A., Liang, W., Stokke, B.G., 2014. Reject the odd egg: Egg recognition mechanisms in parrotbills. Behav. Ecol. 25, 1320–1324.

Yang, C., Chen, X., Wang, L., Liang, W., 2022. Defensive adaptations to cuckoo parasitism in the black-browed reed warbler (Acrocephalus bistrigiceps): recognition and mechanism. Anim. Cognit. 25, 1299–1306.

Yang, C., Huang, J., Liang, W., Møller, A.P., 2021. Absence of anti-parasitic defenses in an Asian population of the magpie, a regular host of the great spotted cuckoo in Europe. Curr. Zool. 67, 345–347.

Yang, C., Wang, L., Cheng, S.-J., Hsu, Y.-C., Stokke, B.G., Røskaft, E., et al., 2015. Deficiency in egg rejection in a host species as a response to the absence of brood parasitism. Behav. Ecol. 26, 406–415.

Yang, C., Wang, L., Liang, W., Møller, A.P., 2019. High egg rejection rate in a Chinese population of grey-backed thrush (Turdus hortulorum). Zool. Res. 40, 226–230.

Ye, P., Cai, Y., Bi, J., Yao, X., Li, G., Yang, C., 2022a. Parasite egg recognition based on multicomponent cues by green-backed tits (Parus monticolus). Avian Biol. Res. 15, 53–57.

Ye, P., Cai, Y., Wu, N., Yao, X., Li, G., Liang, W., et al., 2022b. Egg rejection based on egg size recognition as a specific strategy against parasitic cuckoos. Curr. Zool. 69, 156–164.

Yi, T., Sun, Y.-H., Liang, W., 2020. Egg rejection and egg recognition mechanism of chestnut thrushes (Turdus rubrocanus). Behav. Process. 178, 104158.

Zheng, G., 2021. A Checklist on the Classification and Distribution of the Birds of the World, second ed. Science Press, Beijing.

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Received: 09 January 2023
Revised: 28 May 2023
Accepted: 30 May 2023
Published: 09 June 2023
Issue date: September 2023

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© 2023 The Authors.

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We are grateful to two anonymous reviewers' constructive comments which help improve this manuscript.

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This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

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