Breeding stages affect egg recognition in azure-winged magpies (Cyanopica cyanus).
Azure-winged magpies
Brood parasitism
Egg rejection
Nesting stage
Recognition mechanism
Journal
Animal cognition
ISSN: 1435-9456
Titre abrégé: Anim Cogn
Pays: Germany
ID NLM: 9814573
Informations de publication
Date de publication:
30 Oct 2024
30 Oct 2024
Historique:
received:
03
05
2024
accepted:
22
10
2024
revised:
11
10
2024
medline:
31
10
2024
pubmed:
30
10
2024
entrez:
30
10
2024
Statut:
epublish
Résumé
Egg rejection often involves a cognitive process of recognizing foreign eggs, which can vary not only between species or among different individuals of the same species, but also within the same individual during different breeding stages, leading to markedly different responses to parasitic eggs. We conducted a comparative study in Wuhan, Hubei, and Fusong, Jilin, China, on the recognition and rejection behavior of azure-winged magpies (Cyanopica cyanus) at different breeding stages (pre-egg-laying, one-host-egg, multi-host-egg and early incubation stages). In the Fusong population, there was a significant difference in the rejection rate of model eggs by azure-winged magpies at different stages of the egg-laying period. During the one-host-egg stage, the rejection rate (63.6%) was significantly lower than that during the pre-egg-laying stage (85.7%) and the multi-host-egg stage (100%). The population of azure-winged magpies in Wuhan exhibited a 100% rejection rate towards model eggs during the pre-egg-laying stage. Furthermore, during the incubation stage, azure-winged magpies were able to accurately recognize and reject foreign eggs even when those were in majority. This indicates that azure-winged magpies employ a template-based recognition mechanism rather than relying on discordance mechanism for recognition after the onset of incubation. This study suggests that while azure-winged magpies can truly recognize their own eggs, different breeding stages still influence their rejection response towards parasitic eggs, especially during the pre-egg-laying and egg laying stages.
Identifiants
pubmed: 39475969
doi: 10.1007/s10071-024-01915-0
pii: 10.1007/s10071-024-01915-0
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
71Subventions
Organisme : National Natural Science Foundation of China
ID : No. 32160242
Organisme : National Natural Science Foundation of China
ID : Nos. 31970427 and 32270526
Informations de copyright
© 2024. The Author(s).
Références
Abolins-Abols M, Hanley D, Moskát C, Grim T, Hauber ME (2019) Anti-parasitic egg rejection by great reed warblers (Acrocephalus arundinaceus) tracks differences along an eggshell color gradient. Behav Process 166:103902
doi: 10.1016/j.beproc.2019.103902
Avilés JM (2004) Egg rejection by Iberian azure-winged magpies Cyanopica cyanus in the absence of brood parasitism. J Avian Biol 35:295–299
doi: 10.1111/j.0908-8857.2004.03327.x
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
doi: 10.1093/beheco/art004
Davies NB (2000) Cuckoos, cowbirds and other cheats. T & A. D. Poyser, London
Davies NB (2011) Cuckoo adaptations: trickery and tuning. J Zool 284:1–14
doi: 10.1111/j.1469-7998.2011.00810.x
Davies NB, deL Brooke M (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
doi: 10.2307/4995
Davies NB, deL Brooke M, Kacelnik A (1996) Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs. Proceedings of the Royal Society London B: Biological Sciences, 263, 925–931
Feeney WE, Welbergen JA, Langmore NE (2012) The frontline of avian brood parasite-host coevolution. Anim Behav 84:3–12
doi: 10.1016/j.anbehav.2012.04.011
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
doi: 10.1146/annurev-ecolsys-120213-091603
Feng C, Yang C, Liang W (2019) Nest sanitation facilitates egg recognition in the common tailorbird, a plaintive cuckoo host. Zoological Res 40:466–470
doi: 10.24272/j.issn.2095-8137.2019.054
Grim T, Samas P, Hauber ME (2014) The repeatability of avian egg ejection behaviors across different temporal scales, breeding stages, female ages and experiences. Behav Ecol Sociobiol 68:749–759
doi: 10.1007/s00265-014-1688-9
Guigueno MF, Sealy SG (2009) Nest sanitation plays a role in egg burial by yellow warblers. Ethology 115:247–256
doi: 10.1111/j.1439-0310.2008.01597.x
Guigueno MF, Sealy SG (2017) Implications of nest sanitation in the evolution of egg rejection. In: Soler M (ed) Avian brood parasitism: behaviour, ecology, evolution and coevolution. Springer International Publishing AG, Cham, pp 385–399
doi: 10.1007/978-3-319-73138-4_21
Guigueno MF, Sealy SG, Westphal AM (2014) Rejection of parasitic eggs in passerine hosts: size matters more for a non-ejecter. Auk 131:583–594
doi: 10.1642/AUK-14-36.1
Hanley D, Grim T, Igic B, Samaš P, López AV, Shawkey MD, Hauber ME (2017) Egg discrimination along a gradient of natural variation in eggshell coloration. Proceedings of the Royal Society London B: Biological Sciences, 284, 20162592
Hanley D, Rutledge SL, Villa J (2021) The perceptual and cognitive processes that govern egg rejection in hosts of avian brood parasites. Front Ecol Evol 9:702934
doi: 10.3389/fevo.2021.702934
Hauber ME, Sherman PW (2001) Self-referent phenotype matching: theoretical considerations and empirical evidence. Trends Neurosci 24:609–616
pubmed: 11576676
doi: 10.1016/S0166-2236(00)01916-0
Hauber ME, Moskát C, Bán M (2006) Experimental shift in hosts’ acceptance threshold of inaccurate-mimic brood parasite eggs. Biol Lett 2:177–189
pubmed: 17148357
doi: 10.1098/rsbl.2005.0438
Holen ØH, Johnstone RA (2006) Context-dependent discrimination and the evolution of mimicry. Am Nat 167:377–389
pubmed: 16673346
doi: 10.1086/499567
Kilner RM, Langmore NE (2011) Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol Rev 86:836–852
pubmed: 21223481
doi: 10.1111/j.1469-185X.2010.00173.x
Krüger O (2011) Brood parasitism selects for no defence in a cuckoo host. Proc Royal Soc Lond B: Biol Sci 278:2777–2783
Liu C, Ye P, Cai Y, Quan R, Yang C (2021) Persistent fine-tuning of egg rejection based on parasitic timing in a cuckoo host even after relaxation of parasitism pressure. Behav Process 193:104532
doi: 10.1016/j.beproc.2021.104532
Liu J, Wang L, Liang W (2023) Egg rejection and egg recognition mechanism in a Chinese azure-winged magpie (Cyanopica cyanus) population. Avian Res 14:100112
doi: 10.1016/j.avrs.2023.100112
Liu J, Wang X, Liang W (2024) Attractive egg color? Red eggs facilitate egg acceptance in a cavity-nesting host. Curr Zool 70:112–114
pubmed: 38476137
doi: 10.1093/cz/zoad003
Lotem A, Nakamura H, Zahavi A (1995) Constrains on egg discrimination and cuckoo-host co-evolution. Anim Behav 49:1185–1209
doi: 10.1006/anbe.1995.0152
Ma L, Liang W (2021) Egg rejection and egg recognition mechanisms in oriental reed warblers. Avian Res 12:47
doi: 10.1186/s40657-021-00283-4
Ma L, Liu W, Pan P, Hou J, Liang W (2024) Oriental reed warblers retain strong egg recognition abilities during the nestling stage. Ecol Evol, 14, e11063
Manna T, Moskát C, Hauber ME (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: 10.1007/978-3-319-73138-4_24
Manna TJ, Hanley D, Honza M, Capek M, Rutila J, Samaš P, Abolins-Abols M, Hauber ME (2020) Fitting different visual models to behavioral patterns of parasitic egg rejection along a natural egg color gradient in a cavity-nesting host species. Vision Res 167:54–59
pubmed: 31958715
doi: 10.1016/j.visres.2019.12.007
Martínez JG, Molina-Morales M, Precioso M, Avilés JM (2020) Age-related brood parasitism and egg rejection in magpie hosts. Am Nat 195:876–885
pubmed: 32364781
doi: 10.1086/708155
McRae SB (1995) Temporal variation in responses to intraspecific brood parasitism in the moorhen. Anim Behav 49:1073–1088
doi: 10.1006/anbe.1995.0136
Moksnes A, Røskaft E, Braa AT, Korsnes L, Lampe HL, Pedersen HC (1991) Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour 116:64–89
doi: 10.1163/156853990X00365
Molina-Morales M, Martínez JG, Martín-Gálvez D, Dawson DA, Burke T, Avilés JM (2014) Cuckoo hosts shift from accepting to rejecting parasitic eggs across their lifetime. Evolution 68:3020–3029
pubmed: 24916150
doi: 10.1111/evo.12471
Moskát C (2005) 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 42:579–586
Moskát C, Hauber ME (2007) Conflict between egg recognition and egg rejection decisions in common cuckoo (Cuculus canorus) hosts. Anim Cogn 10:377–386
pubmed: 17279422
doi: 10.1007/s10071-007-0071-x
Moskát C, Honza M (2002) European cuckoo Cuculus canorus parasitism and host’s rejection behaviour in a heavily parasitized great reed warbler Acrocephalus arundinaceus population. Ibis 144:614–622
doi: 10.1046/j.1474-919X.2002.00085.x
Moskát C, Székely T, Kisbenedek T, Karcza Z, Bártol I (2003) The importance of nest cleaning in egg rejection behaviour of great reed warblers Acrocephalus arandinaceas. J Avian Biol 34:16–19
doi: 10.1034/j.1600-048X.2003.02919.x
Moskát C, Avilés JM, Bán M, Hargitai R, Zölei A (2008) Experimental support for the use of egg uniformity in parasite egg discrimination by cuckoo hosts. Behav Ecol Sociobiol 62:1885–1890
doi: 10.1007/s00265-008-0618-0
Moskát C, Bán M, Székely T, Komdeur J, Lucassen RW, 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
pubmed: 20472785
doi: 10.1242/jeb.040394
Moskát C, Hauber ME, Elek Z, Gommers M, Bán M, Groenewoud F, Versluijs TSL, Hoetz CWA, Komdeur J (2014a) Foreign egg retention by avian hosts in repeated brood parasitism: why do rejecters accept? Behav Ecol Sociobiol 68:403–413
doi: 10.1007/s00265-013-1654-y
Moskát C, Zölei A, Bán M, Elek Z, Tong L, Geltsch N, Hauber ME (2014b) How to spot a stranger’s egg? A mimicry-specific discordancy effect in the recognition of parasitic eggs. Ethology 120:616–626
doi: 10.1111/eth.12234
Reeve HK (1989) The evolution of conspecific acceptance thresholds. Am Nat 133:407–435
doi: 10.1086/284926
Rojas Ripari JM, Ursino CA, Reboreda JC, De Mársico MC (2021) Tricking parents: a review of mechanisms and signals of host manipulation by brood-parasitic young. Front Ecol Evol 9:725792
doi: 10.3389/fevo.2021.725792
Rothstein SI (1974) Mechanisms of avian egg recognition: possible learned and innate factors. Auk 91:796–807
doi: 10.2307/4084731
Rothstein SI (1975) Mechanisms of avian egg-recognition: do birds know their own eggs? Anim Behav 23:269–278
doi: 10.1016/0003-3472(75)90075-5
Samaš P, Cassey P, Hauber ME, Grim T (2011) Repeatability of foreign egg rejection: testing the assumptions of co-evolutionary theory. Ethology 117:606–619
doi: 10.1111/j.1439-0310.2011.01917.x
Sealy SG (1995) Burial of cowbird eggs by parasitized yellow warblers: an empirical and experimental study. Anim Behav 49:877–889
doi: 10.1006/anbe.1995.0120
Sealy SG, Underwood TJ (2012) Egg discrimination by hosts and obligate brood parasites: a historical perspective and new synthesis. Chin Birds 3:274–294
doi: 10.5122/cbirds.2012.0042
Servedio MR, Lande R (2003) Coevolution of an avian host and its parasitic cuckoo. Evolution 57:1164–1175
pubmed: 12836832
Soler M (2014) Long-term coevolution between avian brood parasites and their hosts. Biol Rev 89:688–704
pubmed: 24330159
doi: 10.1111/brv.12075
Soler M (2017) Avian brood parasitism: Behaviour, ecology, evolution and coevolution. Springer International Publishing AG, Cham
doi: 10.1007/978-3-319-73138-4
Soler M, Ruiz-Castellano C, Carra LG, Ontanilla J, Martín-Galvez D (2013) Do first-time breeding females imprint on their own eggs? Proceedings of the Royal Society London B: Biological Sciences, 280, 20122518
Soler M, Pérez-Contreras T, Soler JJ (2015) Synchronization of laying by great spotted cuckoos and recognition ability of magpies. J Avian Biol 46:608–615
doi: 10.1111/jav.00627
Son SJ, Kim JS, Lee JW, Nam KB, Yoo JC (2015) Egg recognition and rejection ability of azure-winged magpies (Cyanopica cyanus). Korean J Ornithol 22:37–45
Stouffer PC, Kennedy ED, Power HW (1987) Recognition and removal of intraspecific parasite eggs by starlings. Anim Behav 35:1583–1584
doi: 10.1016/S0003-3472(87)80040-4
Strausberger BM, Rothstein SI (2009) Parasitic cowbirds may defeat host defense by causing rejecters to misimprint on cowbird eggs. Behav Ecol 20:691–699
doi: 10.1093/beheco/arp042
Swynnerton CFM (1918) Rejections by birds of eggs unlike their own: with remarks on some of the cuckoo problems. Ibis 60:127–154
doi: 10.1111/j.1474-919X.1918.tb00774.x
Thorogood R, Davies NB (2013) Reed warbler hosts fine-tune their defenses to track three decades of cuckoo decline. Evolution 67:3545–3555
pubmed: 24299407
doi: 10.1111/evo.12213
Wang L, Yang C, Møller AP, Liang W, Lu X (2015) Multiple mechanisms of egg recognition in a cuckoo host. Behav Ecol Sociobiol 69:1761–1767
doi: 10.1007/s00265-015-1988-8
Yang C, Møller AP, Røskaft E, Moksnes A, Liang W, Stokke BG (2014) Reject the odd egg: egg recognition mechanisms in parrotbills. Behav Ecol 25:1320–1324
doi: 10.1093/beheco/aru124
Yang C, Wang L, Liang W, Møller AP (2015) Nest sanitation behavior in hirundines as a pre-adaptation to egg rejection to counter brood parasitism. Anim Cogn 18:355–360
pubmed: 25231538
doi: 10.1007/s10071-014-0806-4
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 Cogn 25:1299–1306
pubmed: 35320446
doi: 10.1007/s10071-022-01613-9
Yi T, Sun Y-H, Liang W (2020) Egg rejection and egg recognition mechanism of chestnut thrushes (Turdus rubrocanus). Behav Process 178:104158
doi: 10.1016/j.beproc.2020.104158
Zhang J, Møller AP, Yan D, Li J, Deng W (2021) Egg rejection changes with seasonal variation in risk of cuckoo parasitism in daurian redstarts, Phoenicurus auroreus. Anim Behav 175:193–200
doi: 10.1016/j.anbehav.2021.03.007
Zhang J, Santema P, Li J, Feeney WE, Deng W, Kempenaers B (2022) The mere presence of cuckoos in breeding area alters egg-ejection decisions in daurian redstarts. Behav Ecol 33:1153–1160
doi: 10.1093/beheco/arac084