Reject the odd egg: egg recognition mechanisms in parrotbills

Behavioral Ecology The official journal of the ISBE International Society for Behavioral Ecology Behavioral Ecology (2014), 25(6), 1320–1324. doi:10.1093/beheco/aru124 Original Article Reject the odd egg: egg recognition mechanisms in parrotbills Received 4 February 2014; revised 13 May 2014; accepted 10 June 2014; Advance Access publication 28 July 2014. Studies of the behavior of animals when confronted with tasks differing in complexity can improve our understanding of animal cognition and learning mechanisms. Coevolutionary interactions between brood parasites and their hosts provide an ideal opportunity for studying animal cognition because egg recognition and rejection are some of the most important adaptations evolved in hosts to counter brood parasitism. The cognitive mechanisms hosts employ in egg recognition have received substantial interest, with 2 main hypotheses being put forward: 1) true egg recognition based on a knowledge of the hosts’ own egg appearance (template that is innate and/or learned) and 2) discordancy by which individuals simply recognize eggs that are in minority as parasitic. These hypotheses are not necessarily mutually exclusive. We conducted egg experiments in the ashy-throated parrotbill (Paradoxornis alphonsianus), a common cuckoo (Cuculus canorus) host that lays immaculate, polymorphic eggs, and we obtained support for both hypotheses. Parrotbills use the presence of own eggs as a cue for recognizing parasitic eggs, supporting true recognition, but without the presence of own eggs as a template they failed to recognize the parasitic egg. Furthermore, some individuals erroneously rejected their own eggs when in minority, supporting recognition by discordancy. Such a combination of cognitive mechanisms that involves true recognition and discordancy in egg recognition in a single population has as far as we can tell never previously been described. Key words: brood parasitism, cognition, cuckoo, discordancy, egg recognition, online processing. Introduction Decision making depends on a number of related cognitive processes, and studies of animal cognition can improve our understanding of this process (Hauber and Sherman 2001). Avian brood parasites like the common cuckoo (Cuculus canorus, hereafter cuckoo) lay eggs in host nests and thus transfer the cost of parental care to their hosts (Davies and Brooke 1989). Hence, successful parasitism conversely triggers the evolution of antiparasite behavior like rejection of the parasitic egg (Davies and Brooke 1989; Moksnes et al. 1991). Interactions between brood parasites and their hosts provide an ideal opportunity for studying animal cognition because egg rejection is based on cognitive mechanisms related to recognition of the parasitic egg (Rothstein 1974; Hauber and Sherman 2001). Two major hypotheses have been developed to explain cognitive mechanisms responsible for Address correspondence to W. Liang. E-mail: . © The Author 2014. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: egg recognition in brood parasite hosts: 1) true or template-based recognition, in which hosts imprint on their own egg color (innate ability and/or by learning) as a template for rejecting alien eggs and 2) recognition by discordancy, by which hosts reject eggs that are present in minority (no innate template or learning required) (Rensch 1925; Rothstein 1974, 1975; Hauber and Sherman 2001; Bán et al. 2013; Stevens et al. 2013). Most studies so far have obtained support for true or template-based recognition with or without learning, a combination of these, and various duration of the sensitive period for learning (Rothstein 1974, 1975; Moksnes 1992; Lotem et al. 1995; Sealy and Bazin 1995; Lahti and Lahti 2002; Lyon 2007). Recognition by discordancy has received far less support (Rensch 1925; Rothstein 1975; Lyon 2007). Recently, recognition based on true recognition and discordancy has been shown to work in tandem as both effects of recognition and discordancy have been found in the same study (Marchetti 2000; Moskát et al. 2009, 2010; Bán et al. 2013; Stevens et al. 2013). These latter studies have all in common that the host species in question lay maculate eggs. Hence, it was not Canchao Yang,a Anders Pape Møller,b Eivin Røskaft,c Arne Moksnes,c Wei Liang,a and Bård G. Stokkec aMinistry of Education Key Laboratory for Tropical Plant and Animal Ecology, College of Life Sciences, Hainan Normal University, Haikou 571158, China, bLaboratoire Ecologie, Systematique et Evolution, UMR 8079 CNRS-Université Paris-Sud XI-AgroParisTech, Batiment 362, F-91405 Orsay Cedex, France, and cDepartment of Biology, Norwegian University of Science and Technology (NTNU), NO-7491 Trondheim, Norway Yang et al. • Egg recognition mechanisms in parrotbills 1321 minority indicates that some host pairs base their recognition on discordancy rather than true recognition. Such variation in cognitive mechanisms used for egg recognition has also been found in other host species (Moskát et al. 2010; Bán et al. 2013; Stevens et al. 2013). Parrotbill hosts use the presence of own eggs as a cue for recognizing parasitic eggs, supporting true recognition, but without the presence of own eggs as a template, they failed to recognize the parasitic egg. Furthermore, some individuals erroneously rejected their own eggs when in minority, supporting recognition by discordancy. Such a combination of cognitive mechanisms that involves true recognition and discordancy in egg recognition in a single population has never previously been described. Our study, therefore, constitutes an important part of the puzzle resolving cognitive mechanisms used in egg recognition by hosts of brood parasites. What are the consequences of template-based recognition mechanism in parrotbills? Moskát et al. (2009) and Stevens et al. (2013) found that probability of egg acceptance increased with multiple parasitism. Unlike their host–parasite systems, where multiple parasitism is common, more than 1 cuckoo egg has never been found in our parrotbill nests. Hence, the egg recognition mechanisms in parrotbills are well suited to deal with cuckoo parasitism in natural situations. The different results obtained from various study species suggest that no single egg recognition mechanism is universal, but rather that there is variation among species. In parrotbills, we do not know the importance of learning for egg recognition. According to theoretical models, species like parrotbills with a low intraclutch variation in egg appearance should not need a prolonged learning period, but rather imprint on their first egg or just have an internal template without any need for learning at all (Stokke et al. 2007). In parrotbills, both sexes are known to incubate and reject parasitic eggs. Hence, we predicted that the cognitive mechanisms used in egg rejection should b (...truncated)