Abstract

Historically, investigations of how organismal investments in immunity fluctuate in response to environmental and physiological changes have focused on seasonally breeding organisms that confine reproduction to seasons with relatively unchallenging environmental conditions and abundant resources. The red crossbill, Loxia curvirostra, is a songbird that can breed opportunistically if conifer seeds are abundant, on both short, cold, and long, warm days, providing an ideal system to investigate environmental and reproductive effects on immunity. In this study, we measured inter- and intra-annual variation in complement, natural antibodies, PIT54 and leucocytes in crossbills across four summers (2010–2013) and multiple seasons within 1 year (summer 2011–spring 2012). Overall, we observed substantial changes in crossbill immune investment among summers, with interannual variation driven largely by food resources, while variation across multiple seasons within a single cone year was less pronounced and lacked a dominant predictor of immune investment. However, we found weak evidence that physiological processes (e.g. reproductive condition, moult) or abiotic factors (e.g. temperature, precipitation) affect immune investment. Collectively, this study suggests that a reproductively flexible organism may be able to invest in both reproduction and survival-related processes, potentially by exploiting rich patches with abundant resources. More broadly, these results emphasize the need for more longitudinal studies of trade-offs associated with immune investment.

Highlights

  • Many temperate, terrestrial organisms experience extensive seasonal variation in weather, disease exposure and resource availability across the annual cycle

  • Flight feather moult (Ff), plumage moult intensity and reproductive measures (CP/brood patch (BP)) were all selected by random forest models (RFMs) for further consideration, yet of these, only flight feather moult displayed a marginally significant, positive relationship with complement

  • Given that feathers erupting through the skin can induce dermal inflammation [63] and chemotaxis of blood monocytes that differentiate into macrophages that are integral to the inflammatory response [49], elevated monocytes during peak moult is not surprising

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Summary

Introduction

Terrestrial organisms experience extensive seasonal variation in weather, disease exposure and resource availability across the annual cycle. Investment in immune function promotes survival by minimizing deleterious effects of pathogens and disease [2]. Empirical data suggest that changing environmental conditions (e.g. pathogens, resource availability) strongly influence allocation to immunity [5,6]. If varying environmental conditions most strongly influence immune allocation, investment in immunity would vary significantly both within and between years according to prevailing conditions (sensu Hegemann et al [7]). Organisms may modulate immunity in direct response to an energy trade-off with competing processes such as reproduction, migration, or plumage/pelage moult, resulting in predictable seasonal or inter-annual patterns of immune investment (sensu Hegemann et al [7])

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