Behavioural trait covaries with immune responsiveness in a wild passerine Elin Sild, Tuul Sepp, Peeter Hõrak ⇑ Department of Zoology, Institute of Ecology and Earth Sciences, The Centre of Excellence FIBIR, Tartu University, Vanemuise 46, 51014 Tartu, Estonia article info Article history: Received 11 February 2011 Received in revised form 31 March 2011 Accepted 31 March 2011 Available online 5 April 2011 Keywords: Brucella abortus Carduelis chloris Captivity Chemiluminescence response Coping styles Immunoecology Locomotory behaviour Passerine abstract Immune system is highly integrated with the nervous and endocrine systems, which is thought to result in covariation between behavioural syndromes and stress- and immune-associated diseases. Very little is known about the associations between behaviour and immune traits in wild animals. Here we describe such an association in passerine birds, the greenfinches (Carduelis chloris). When wild-caught greenfinch- es are brought into captivity, some individuals damage their tail feathers against cage walls due to excited behaviour, while others retain their feathers in intact condition. We show that damage to tail feathers was associated with flapping flight movements and the frequency of such flapping bouts was individually consistent over 57 days. Birds with intact tails, i.e., relatively ‘calm’ individuals mounted stronger antibody response to a novel Brucella abortus antigen and their circulating phagocytes were capable of producing stronger oxidative burst in response to stimulation with bacterial lipopolysaccha- ride in vitro. As the behavioural trait was assessed 13–25 days before measuring immune responsiveness, our results demonstrate that individuals’ coping styles with captivity predicted how these individuals would respond to forthcoming immune challenges. This is a novel evidence about covariation between immune responsiveness and a behavioural trait in a wild-caught animal. Ó 2011 Elsevier Inc. All rights reserved. 1. Introduction Animals, including humans, differ systematically in their responses to conspecifics and to their environment and these re- sponses often covary with susceptibility to stress- and immune- related diseases such as cardiovascular disorders, gastric ulceration and various infectious and inflammatory conditions (Friedman, 2008; Koolhaas et al., 1999; Segerstrom, 2000). The correlations be- tween neuroendocrine and behavioural traits have been found in diverse taxa including mammals, birds, fish and reptiles (Groothuis and Carere, 2005; Koolhaas et al., 1999; Réale et al., 2010b). The ultimate explanation for this covariation is that temporally and/or spatially fluctuating selection pressures favour different stress- coping styles (Bergmüller and Taborsky, 2010; Dingemanse et al., 2004) and immune traits (e.g., Lazzaro and Little, 2009) under different circumstances. At proximate level, such covariation is based on bidirectional communication between the brain and the autonomic, cardiovascular, and immune systems via neural and endocrine mechanisms underpinning cognition, experience, and behaviour (reviewed by Koolhaas et al., 1999; Korte et al., 2005; Coppens et al., 2010; McEwen and Gianaros, 2010). However, despite these conceptual advances, the general understanding about the interactions between neuroendocrine– immune systems and behaviour is far from complete (e.g., Réale et al., 2010a), specifically as regards wild animals (Koolhaas et al., 2010). With this respect, looking at avian personalities seems especially promising, as individually consistent variation in behav- ioural syndromes and stress-coping styles among variety of taxa has been firmly established (Cockrem, 2007; Groothuis and Carere, 2005). Furthermore, there exist solid theoretical frameworks, e.g., the one based on the pleiotropy of the melanocortin system that predicts how variation in behavioural traits should relate to pig- mentation, corticosterone responses and immunity (Ducrest et al., 2008). A number of studies in wild barn owls (Tyto alba) provide evidence for the substantial links between different components of this system, e.g., between behaviour, stress- responsiveness and colouration (Almasi et al., 2008), colouration and immune function (Gasparini et al., 2009; Piault et al., 2009) and colouration and stress hormones (Roulin et al., 2008 for similar evidence in fishes see Kittilsen et al., 2009). There is no reason to expect, however, that the melanocortin system forms a single nexus between behaviour and immunity, because glucocorticoid hormones are also known to affect both domains directly (e.g., Korte et al., 2005), along with other neurochemical signalling pathways (Coppens et al., 2010). Despite the well-established links between behavioural traits and corticosterone responses (e.g., Cockrem, 2007), there are no studies on wild bird species associating behavioural traits and im- mune function directly. Here we describe such an association in wild-caught captive greenfinches (Carduelis chloris). We take an 0889-1591/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.bbi.2011.03.020 ⇑ Corresponding author. Fax: +372 7375830. E-mail address: horak@ut.ee (P. Hõrak). Brain, Behavior, and Immunity 25 (2011) 1349–1354 Contents lists available at ScienceDirect Brain, Behavior, and Immunity journal homepage: www.elsevier.com/locate/ybrbi