Abstract
Parasites may, in multi-parasite systems, block the defenses of their hosts and thus thwart host recognition of parasites by frequency-dependent selection. Nest defenses as frontline may block or promote the subsequent stage of defenses such as egg recognition. We conducted comparative studies of the defensive strategies of a host of the Oriental cuckoo Cuculus optatus, the yellow-bellied prinia Prinia flaviventris, in mainland China with multiple species of cuckoos and in Taiwan with a single cuckoo species. Cuckoo hosts did not exhibit aggression toward cuckoos in the presence of multiple cuckoo species but showed strong aggressive defenses of hosts directed toward cuckoos in Taiwan. Furthermore, the cuckoo host in populations with a single cuckoo species was able to distinguish adults of its brood parasite, the Oriental cuckoo, from adult common cuckoos (Cuculus canorus). This represents the first case in which a cuckoo host has been shown to specifically distinguish Oriental cuckoo, from other Cuculus species. Hosts ejected eggs at a higher rate in a single cuckoo species system than in a multi-species cuckoo system, which supports the strategy facilitation hypothesis. Granularity analysis of variation in egg phenotype based on avian vision modeling supported the egg signature hypothesis in hosts because Taiwanese prinias increased consistency in the appearance of their eggs within individual hosts thus favoring efficient discrimination against cuckoo eggs. This study significantly improves our knowledge of intraspecific variation in antiparasitism behavior of hosts between single- and multi-cuckoo systems.
Similar content being viewed by others
References
Barbosa A, Mäthger LM, Buresch KC, Kelly J, Chubb J, Chiao C-C, Hanlon RT (2008) Cuttlefish camouflage: the effects of substrate contrast and size in evoking uniform mottle or disruptive body patterns. Vis Res 48:1242–1253
Bartol I, Karcza Z, Moskát C, Røskaft E, Kisbenedek T (2002) Responses of great reed warblers Acrocephalus arundinaceus to experimental brood parasitism: the effects of a cuckoo Cuculus canorus dummy and egg mimicry. J Avian Biol 33:420–425
Chiao C-C, Chubb C, Buresch KC, Siemann L, Hanlon RT (2009) The scaling effects of substrate texture on camouflage patterning in cuttlefish. Vis Res 49:1647–1656
Davies NB (2000) Cuckoos, cowbirds and other cheats. Poyser, London
Davies NB (2011) Cuckoo adaptations: trickery and tuning. J Zool 284:1–14
Davies NB, Brooke M d 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
Feeney WE, Welbergen JA, Langmore NE (2012) The frontline of avian brood parasite-host coevolution. Anim Behav 84:3–12
Godfrey D, Lythgoe JN, Rumball DA (1987) Zebra stripes and tiger stripes: the spatial frequency distribution of the pattern compared to that of the background is significant in display and crypsis. Biol J Linn Soc 32:427–433
Kettlewell HBD (1973) The evolution of melanism. Clarendon, Oxford
Kilner RM (2006) The evolution of egg colour and patterning in birds. Biol Rev 81:383–406
La Touche JDD (1931–34) A handbook of the birds of Eastern China. Taylor and Francis, London
Langmore NE, Hunt S, Kilner RM (2003) Escalation of a co-evolutionary arms race through host rejection of brood parasitic young. Nature 422:157–160
Langmore NE, Kilner RM, Butchart SHM, Maurer G, Davies NB, Cockburn A, Macgregor NA, Peters A, Magrath MJL, Dowling DK (2005) The evolution of egg rejection by cuckoo hosts in Australia and Europe. Behav Ecol 16:686–692
Langmore NE, Maurer G, Adcock GJ, Kilner RM (2008) Socially acquired host-specific mimicry and the evolution of host races in Horsfield’s bronze-cuckoo Chalcites basalis. Evolution 62:1689–1699
MacKinnon J, Phillipps K (1999) A field guide to the birds of China. Oxford University Press, Oxford
Moksnes A, Røskaft E (1992) Responses of some rare cuckoo hosts to mimetic model cuckoo eggs and to foreign conspecific eggs. Ornis Scand 23:17–23
Nakamura H, Miyazawa Y, Kashiwagi K (2005) Behavior of radio-tracked common cuckoo females during the breeding season in Japan. Ornithol Sci 4:31–41
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
Planqué R, Britton NF, Franks NR, Peletier MA (2002) The adaptiveness of defence strategies against cuckoo parasitism. Bull Math Biol 64:1045–1068
Røskaft E, Moksnes A, Stokke BG, Bicik V, Moskát C (2002) Aggression to dummy cuckoos by potential European cuckoo hosts. Behaviour 139:613–628
Rothstein SI (1975) Mechanisms of avian egg recognition: do birds known their own eggs? Anim Behav 23:268–278
Rothstein SI, Robinson SK (eds) (1998) Parasitic birds and their hosts: studies on coevolution. Oxford University Press, New York
Sato NJ, Tokue K, Noske RA, Mirami OK, Ueda K (2010) Evicting cuckoo nestlings from the nest: a new anti-parasitism behaviour. Biol Lett 6:67–69
Soler JJ, Soler M, Pérez-Contreras T, Aragón S, Møller AP (1999) Antagonistic antiparasite defenses: nest defense and egg rejection in the magpie host of the great spotted cuckoo. Behav Ecol 10:707–713
Stoddard MC, Stevens M (2010) Pattern mimicry of host eggs by the common cuckoo, as seen through a bird’s eye. Proc R Soc B 277:1387–1393
Swynnerton CFM (1916) On the coloration of the mouths and eggs of birds. II. On the coloration of eggs. Ibis 4:529–606
Takasu F (2003) Co-evolutionary dynamics of egg appearance in avian brood parasitism. Evol Ecol Res 5:345–362
Thorogood R, Davies NB (2012) Cuckoos combat socially transmitted defenses of reed warbler hosts with a plumage polymorphism. Science 337:578–580
Turner JRG, Speed MP (1999) How weird can mimicry get? Evol Ecol 13:807–827
Yang C, Liang W, Cai Y, Shi S, Takasu F, Møller AP, Antonov A, Fossøy F, Moksnes A, Røskaft E, Stokke BG (2010) Coevolution in action: disruptive selection on egg colour in an avian brood parasite and its host. PLoS ONE 5:e10816
Yang C, Liang W, Antonov A, Cai Y, Stokke BG, Fossøy F, Moksnes A, Røskaft E (2012) Diversity of parasitic cuckoos and their hosts in China. Chin Birds 3:9–32
Zhang W (1980) A field guide to the birds of Taiwan. Institute of Environmental Science, Tunghai University, Taiwan
Acknowledgments
C.Y. and L.W. contributed equally to this work. We would like to thank Ian Will from University of California, Berkeley, USA, for his assistance with the fieldwork in Guangxi. This work was supported by the National Natural Science Foundation of China (Nos. 31260514 to CY and 31071938 and 31272328 to WL), Program for New Century Excellent Talents in University (NCET-13-0761 to CY and NCET-10-0111 to WL), Program of International S & T Cooperation (KJHZ2013-12), and Key Project of Chinese Ministry of Education (No. 212136) to CY.
Ethical standards
The studies reported in this paper conform to the laws in the countries in which they were performed.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by: Alexandre Roulin
Rights and permissions
About this article
Cite this article
Yang, C., Wang, L., Cheng, SJ. et al. Nest defenses and egg recognition of yellow-bellied prinia against cuckoo parasitism. Naturwissenschaften 101, 727–734 (2014). https://doi.org/10.1007/s00114-014-1209-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00114-014-1209-8