Journal Home > Volume 10 , Issue 1
Background

Brood parasitic birds such as cuckoos (Cuculus spp.) can reduce their host's reproductive success. Such selection pressure on the hosts has driven the evolution of defense behaviors such as egg rejection against cuckoo parasitism. Studies have shown that Cinereous Tits (Parus cinereus) in China have a good ability for recognizing foreign eggs. However,it is unclear whether egg spots play a role in egg recognition. The aims of our study were to investigate the egg recognition ability of two Cinereous Tit populations in China and to explore the role of spots in egg recognition.

Methods

To test the effect of eggshell spots on egg recognition,pure white eggs of the White-rumped Munia (Lonchura striata) and eggs of White-rumped Munia painted with red brown spots were used to simulate experimental parasitism.

Results

Egg experiments showed that Cinereous Tits rejected 51.5% of pure white eggs of the White-rumped Munia,but only 14.3% of spotted eggs of the White-rumped Munia. There was a significant difference in egg recognition and rejection rate between the two egg types.

Conclusions

We conclude that eggshell spots on Cinereous Tit eggs had a signaling function and may be essential to tits for recognizing and rejecting parasitic eggs.


menu
Abstract
Full text
Outline
About this article

Egg recognition in Cinereous Tits (Parus cinereus): eggshell spots matter

Show Author's information Jianping Liu1Canchao Yang1Jiangping Yu2,3Haitao Wang2,4Wei Liang1( )
Ministry of Education Key Laboratory for Ecology of Tropical Islands, College of Life Sciences, Hainan Normal University, Haikou 571158, China
Jilin Engineering Laboratory for Avian Ecology and Conservation Genetics, School of Life Sciences, Northeast Normal University, Changchun 130024, China
Ministry of Education Key Laboratory of Vegetation Ecology, School of Life Sciences, Northeast Normal University, Changchun 130024, China
Jilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, School of Life Sciences, Northeast Normal University, Changchun 130024, China

Abstract

Background

Brood parasitic birds such as cuckoos (Cuculus spp.) can reduce their host's reproductive success. Such selection pressure on the hosts has driven the evolution of defense behaviors such as egg rejection against cuckoo parasitism. Studies have shown that Cinereous Tits (Parus cinereus) in China have a good ability for recognizing foreign eggs. However,it is unclear whether egg spots play a role in egg recognition. The aims of our study were to investigate the egg recognition ability of two Cinereous Tit populations in China and to explore the role of spots in egg recognition.

Methods

To test the effect of eggshell spots on egg recognition,pure white eggs of the White-rumped Munia (Lonchura striata) and eggs of White-rumped Munia painted with red brown spots were used to simulate experimental parasitism.

Results

Egg experiments showed that Cinereous Tits rejected 51.5% of pure white eggs of the White-rumped Munia,but only 14.3% of spotted eggs of the White-rumped Munia. There was a significant difference in egg recognition and rejection rate between the two egg types.

Conclusions

We conclude that eggshell spots on Cinereous Tit eggs had a signaling function and may be essential to tits for recognizing and rejecting parasitic eggs.

Keywords: Egg rejection, Brood parasitism, Egg recognition, Eggshell spots, Parus cinereus

References(80)

Abernathy VE, Troscianko J, Langmore NE. Egg mimicry by the pacific koel: mimicry of one host facilitates exploitation of other hosts with similar egg types. J Avian Biol. 2017;48:1114-24.

Antonov A, Stokke BG, Moksnes A, Røskaft E. Egg rejection in marsh warblers (Acrocephalus palustris) heavily parasitized by common cuckoos (Cuculus canorus). Auk. 2006;123:419-30.

Antonov A, Stokke BG, Fossøy F, Ranke PS, Liang W, Yang C, et al. Are cuckoos maximizing egg mimicry by selecting host individuals with better matching egg phenotypes? PLoS ONE. 2012;7:e31704.

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

Avilés JM, Stokke BG, Moksnes A, Roskaft E, Åsmul M, Møller AP. Rapid increase in cuckoo egg matching in a recently parasitized reed warbler population. J Evol Biol. 2006;19:1901-10.

Brooker MG, Brooker LC. Cuckoo hosts in Australia. Austr Zool Rev. 1989;2:1-67.

Brooke ML, Davies NB. Egg mimicry by cuckoos Cuculus canorus in relation to discrimination by hosts. Nature. 1988;335:630-2.

Brooker LC, Brooker MG, Brooker AMH. An alternative population/genetics model for the evolution of egg mimesis and egg crypsis in cuckoos. J Theor Biol. 1990;146:123-43.

Bulla M, Šálek M, Gosler AG. Eggshell spotting does not predict male incubation but marks thinner areas of a shorebird's shells. Auk. 2012;129:26-35.

Cassey P, Honza M, Grim T, Hauber ME. The modelling of avian visual perception predicts behavioural rejection responses to foreign egg colours. Biol Lett. 2008;4:515-7.

Caves EM, Stevens M, Iversen ES, Spottiswoode CN. Hosts of avian brood parasites have evolved egg signatures with elevated information content. Proc R Soc Lond B-Biol Sci. 2015;282:772-5.

Cuthill IC, Partridge JC, Bennett AT, Church SC, Hart NS, Hunt S. Ultraviolet vision in birds. Adv Study Behav. 2000;29:159-214.

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. Cuckoo: cheating by nature. London: Bloomsbury; 2015.

Davies NB, Brooke ML. An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. I. Host egg recognition. J Anim Ecol. 1989a;58:207-24.

Davies NB, Brooke ML. An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. II. Host egg markings, chick discrimination and general discussion. J Anim Ecol. 1989b;58:225-36.

de la Colina MA, Pompilio L, Hauber ME, Reboreda JC, Mahler B. Different recognition cues reveal the decision rules used for egg rejection by hosts of a variably mimetic avian brood parasite. Anim Cogn. 2012;15:881-9.

Duval C, Cassey P, Lovell PG, Mikšík I, Reynolds SJ, Spencer KA. Maternal influence on eggshell maculation: implications for cryptic camouflaged eggs. J Ornithol. 2016;157:303-10.

García-Navas V, Sanz JJ, Merino S, Puente MDL, Lobato E, Cerro SD, et al. Experimental evidence for the role of calcium in eggshell pigmentation pattern and breeding performance in blue tits Cyanistes caeruleus. J Ornithol. 2010;152:71-82.

Gloag R, Keller LA, Langmore NE. Cryptic cuckoo eggs hide from competing cuckoos. Proc R Soc Lond B Biol Sci. 2014;281:20141014.

Gorchein A, Lim CK, Cassey P. Extraction and analysis of colourful eggshell pigments using HPLC and HPLC/electrospray ionization tandem mass spectrometry. Biomed Chromatogr. 2009;23:602-6.

Gosler AG, Higham JP, Reynolds SJ. Why are birds' eggs spotted? Ecol Lett. 2005;8:1105-13.

Hanley D, Cassey P, Doucet SM. Parents, predators, parasites, and the evolution of eggshell colour in open nesting birds. Evol Ecol. 2013;27:593-617.

Hanley D, López AV, Fiorini VD, Reboreda JC, Grim T, Hauber ME. Variation in multicomponent recognition cues alters egg rejection decisions: a test of the optimal acceptance threshold hypothesis. Philos Trans R Soc B. 2019;374:20180195.

Hargitai R, Nagy G, Herényi M, Török J. Effects of experimental calcium availability, egg parameters and laying order on great tit Parus major eggshell pigmentation patterns. Ibis. 2013;155:561-70.

Hargitai R, Heréhyi M, Nagy G, Nyiri Z, Eke Z, Török J. Effects of environmental conditions on the egg mass, yolk antioxidant level, eggshell thickness and eggshell spotting patterns of great tits (Parus major). J Ornithol. 2016;157:995-1006.

Hauber ME. The book of eggs: A life-size guide to the eggs of six hundred of the world's bird species. Brighton: Ivy Press; 2014.https://doi.org/10.7208/chicago/9780226057811.001.0001
DOI

Honza M, Šulc M, Jelínek V, Požgayová M, Procházka P. Brood parasites lay eggs matching the appearance of host clutches. Proc Roy Soc B Biol Sci. 2014;281:20132665.

Igic B, Nunez V, Voss HU, Croston R, Aidala Z, López AV, et al. Using 3D printed eggs to examine the egg-rejection behaviour of wild birds. Peer J. 2015;3:e965.

Johnsgard PA. The avian brood parasites: deception at the nest. Oxford: Oxford University Press; 1997.

Kennedy GY, Vevers HG. A survey of avian eggshell pigments. Comp Biochem Physiol B Comp Biochem. 1976;55:117-23.

Kilner RM. The evolution of egg colour and patterning in birds. Biol Rev. 2006;81:383-406.

Lahti DC, Lahti AR. How precise is egg discrimination in weaverbirds? Anim Behav. 2002;63:1135-42.

Langmore NE, 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, Kilner RM. Are dark cuckoo eggs cryptic in host nests? Anim Behav. 2009;78:461-8.

Lawes MJ, Kirkman S. Egg recognition and interspecific brood parasitism rates in red bishops (Aves: Ploceidae). Anim Behav. 1996;52:553-63.

Liang W, Møller AP, Stokke BG, Yang C, Kovařík P, Wang H, et al. Geographic variation in egg ejection rate by great tits across 2 continents. Behav Ecol. 2016;27:1405-12.

Liu J, Ma L, Zhang Z, Gu D, Wang J, Li J, et al. Maximum frequency of songs reflects body size among male dusky warblers Phylloscopus fuscatus (Passeriformes: Phylloscopidae). Eur Zool J. 2017;84:186-92.

López-De-Hierro MDG, DeNeve L. Pigment limitation and female reproductive characteristics influence eggshell spottiness and ground colour variation in the house sparrow (Passer domesticus). J Ornithol. 2010;151:833-40.

López-De-Hierro MDG, Moreno-Rueda G. Egg-spot pattern rather than egg colour affects conspecific egg rejection in the house sparrow (Passer domesticus). Behav Ecol Sociobiol. 2009;64:317-24.

Luro AB, Igic B, Croston R, López AV, Shawkey MD, Hauber ME. Which egg features predict egg rejection responses in American robins? Replicating Rothstein's (1982) study. Ecol Evol. 2018;8:1673-9.

Marchetti K. Egg rejection in a passerine bird: size does matter. Anim Behav. 2000;59:877-83.

Mason P, Rothstein SI. Coevolution and avian brood parasitism: cowbird eggs show evolutionary response to host discrimination. Evolution. 1986;40:1207-14.

Maurer G, Portugal SJ, Cassey P. An embryo's eye view of avian eggshell pigmentation. J Avian Biol. 2011;42:494-504.

Medina I, Troscianko J, Stevens M, Langmore NE. Brood parasitism is linked to egg pattern diversity within and among species of Australian passerines. Am Nat. 2016;187:351-62.

Meshcheryagina SG, Mashanova A, Bachurin GN, Mitiay IS, Golovatin MG. Host species determines egg size in Oriental cuckoo. J Zool. 2018;306:147-55.

Mikšík I, Holáň V, Deyl Z. Avian eggshell pigments and their variability. Comp Biochem Physiol B Biochem Mol Biol. 1996;113:607-12.

Newton AV. A dictionary of birds. London: A & C Black; 1896.https://doi.org/10.5962/bhl.title.168963
DOI

Päckert M, Martens J, Eck S, Nazarenko AA, Valchuk OP, Petri B, et al. The great tit (Parus major)—a misclassified ring species. Biol J Linn Soc. 2005;86:153-74.

Payne RB. The cuckoos. Oxford: Oxford University Press; 2005.

Poláček M, Griggio M, Mikšík I, Bartíková M, Eckenfellner M, Hoi H. Eggshell coloration and its importance in postmating sexual selection. Ecol Evol. 2017;7:941-9.

Polačiková L, Grim T. Blunt egg pole holds cues for foreign egg discrimination: experimental evidence. J Avian Biol. 2010;41:111-6.

Polačiková L, Honza M, Procházka P, Topercer J, Stokke BG. Colour characteristics of the blunt egg pole: cues for recognition of parasitic eggs as revealed by reflectance spectrophotometry. Anim Behav. 2007;74:419-27.

Polačiková L, Stokke BG, Procházka P, Honza M, Moksnes A, Røskaft E. The role of blunt egg pole characteristics for recognition of eggs in the song thrush (Turdus philomelos). Behaviour. 2010;147:465-78.

Reynolds SJ, Martin GR, Cassey P. Is sexual selection blurring the functional significance of eggshell colouration hypotheses? Anim Behav. 2009;78:209-15.

Rothstein SI. Mechanisms of avian egg-recognition—additional evidence for learned components. Anim Behav. 1978;26:671-6.

Rothstein SI. Mechanisms of avian egg recognition: which egg parameters elicit responses by rejecter species? Behav Ecol Sociobiol. 1982;11:229-39.

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

Sanz JJ, García-Navas V. Eggshell pigmentation pattern in relation to breeding performance of blue tits Cyanistes caeruleus. J Anim Ecol. 2009;78:31-41.

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

Soler JJ, Møller AP. A comparative analysis of the evolution of variation in appearance of eggs of European passerines in relation to brood parasitism. Behav Ecol. 1996;7:89-94.

Spottiswoode CN, Stevens M. Visual modeling shows that avian host parents use multiple visual cues in rejecting parasitic eggs. Proc Natl Acad Sci USA. 2010;107:8672-6.

Starling M, Heinsohn R, Cockburn A, Langmore NE. Cryptic gentes revealed in pallid cuckoos Cuculus pallidus using reflectance spectrophotometry. Proc R Soc B Biol Sci. 2006;273:1929-34.

Stoddard MC, Stevens M. Pattern mimicry of host eggs by the common cuckoo, as seen through a bird's eye. Proc R Soc Lond B Biol Sci. 2010;277:1387-93.

Stoddard MC, Stevens M. Avian vision and the evolution of egg color mimicry in the common cuckoo. Evolution. 2011;65:2004-13.

Stoddard MC, Fayet A, Kilner RM, Hinde C. Egg spots patterns do not advertise offspring quality or influence male provisioning in great tits. PLoS ONE. 2012;7:e40211.

Stoddard MC, Kilner RM, Town C. Pattern recognition algorithm reveals how birds evolve individual egg pattern signatures. Nat Commun. 2014;5:4117.

Stokke BG, Moksnes A, Røskaft E. Obligate brood parasites as selective agents for evolution of egg appearance in passerine birds. Evolution. 2002;56:199-205.

Stokke BG, Takasu F, Moksnes A, Røskaft E. The importance of clutch characteristics and learning for anti-parasite adaptations in hosts of avian brood parasites. Evolution. 2007;61:2212-28.

Stokke BG, Røskaft E, Moksnes A, Møller AP, Antonov A, Fossøy F, et al. Disappearance of eggs from nonparasitized nests of brood parasite hosts: the evolutionary equilibrium hypothesis revisited. Biol J Linn Soc. 2016;118:215-25.

Stokke BG, Fossøy F, Røskaft E, Moksnes A. Adaptations of brood parasitic eggs. In: Soler M, editor. Avian brood parasitism: behaviour, ecology, evolution and coevolution. Cham: Springer International Publishing AG; 2017. p. 363-84.https://doi.org/10.1007/978-3-319-73138-4_20
DOI

Šulc M, Procházka P, Capek M, Honza M. Birds use eggshell UV reflectance when recognizing non-mimetic parasitic eggs. Behav Ecol. 2016;27:677-84.

Šulc M, Troscianko J, Štětková G, Hughes AE, Jelínek V, Capek M, Honza M. Mimicry cannot explain rejection type in a host-brood parasite system. Anim Behav. 2019;155:111-8.

Swynnerton CFM. Rejections by birds of eggs unlike their own: with remarks on some of the cuckoo problems. Ibis. 1918;6:127-54.

Takasu F. Co-evolutionary dynamics of egg appearance in avian brood parasitism. Evol Ecol Res. 2003;5:345-62.

Underwood TJ, Sealy SG. Parameters of brown headed cowbird Molothrus ater egg discrimination in warbling vireos Vireo gilvus. J Avian Biol. 2006;37:457-66.

Yang C, Liang W, Cai Y, Shi S, Takasu F, Møller AP, et al. Coevolution in action: disruptive selection on egg colour in an avian brood parasite and its host. PLoS ONE. 2010;5:e10816.

Yang C, Liang W, Møller AP. Egg retrieval versus egg rejection in cuckoo hosts. Philos Trans R Soc B. 2019;374:20180200.

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.

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 25 July 2019
Accepted: 17 September 2019
Published: 04 October 2019
Issue date: January 2019

Copyright

© The Author(s) 2019.

Acknowledgements

Acknowledgements

We thank Saihanba National Forest Park of Hebei and Zuojia Nature Reserve of Jilin for their help and cooperation, and Jianwei Zhang, Xintong Li, Jing Yue and Hailin Lu for assistance with field work. We are also grateful to the two anonymous referees for their constructive comments.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Return