Wild Skylarks Seasonally Modulate Energy Budgets but Maintain Energetically Costly Inflammatory Immune Responses throughout the Annual Cycle

Abstract

A central hypothesis of ecological immunology is that immune defences are traded off against competing physiological and behavioural processes. During energetically demanding periods, birds are predicted to switch from expensive inflammatory responses to less costly immune responses. Acute phase responses (APRs) are a particularly costly form of immune defence, and, hence, seasonal modulations in APRs are expected. Yet, hypotheses about APR modulation remain untested in free-living organisms throughout a complete annual cycle. We studied seasonal modulations in the APRs and in the energy budgets of skylarks Alauda arvensis, a partial migrant bird from temperate zones that experiences substantial ecological changes during its annual cycle. We characterized throughout the annual cycle changes in their energy budgets by measuring basal metabolic rate (BMR) and body mass. We quantified APRs by measuring the effects of a lipopolysaccharide injection on metabolic rate, body mass, body temperature, and concentrations of glucose and ketone. Body mass and BMR were lowest during breeding, highest during winter and intermediate during spring migration, moult and autumn migration. Despite this variation in energy budgets, the magnitude of the APR, as measured by all variables, was similar in all annual cycle stages. Thus, while we find evidence that some annual cycle stages are relatively more energetically constrained, we find no support for the hypothesis that during these annual cycle stages birds compromise an immune defence that is itself energetically costly. We suggest that the ability to mount an APR may be so essential to survival in every annual cycle stage that skylarks do not trade off this costly form of defence with other annual cycle demands.

Immune response to an endotoxin challenge involves multiple immune parameters and is consistent among the annual-cycle stages of a free-living temperate zone bird

“…While both indices increased as expected due to the stress associated with captivity, we found no significant seasonal pattern in this captivity-related stress response (ΔH/L ratio χ 2 4,46 =4.04, P=0.40; ΔHsp70 χ 2 4,45 =0.40, P=0.53). Furthermore, there were no differences in the metabolic effects (O 2 consumption and nightly mass loss) of an LPS injection when comparing birds that were held in captivity for a few hours according to the protocol used in this study and birds acclimated to captivity for 55days (Hegemann et al, 2012b). Thus we have no evidence that the immune response we experimentally triggered was masked by any stress responses resulting from the short time in captivity.…”

“…Only baseline defences can be traded off with other demands. This conclusion further highlights the interpretational limitations and the importance of distinguishing between baseline values and induced responses when studying ecological immunology (Adamo, 2004;Hegemann et al, 2012b;Hegemann et al, 2012c).This finding -that responses to an LPS injection were constant throughout the annual cycle -necessitates a short discussion of two methodological points. First, skylarks in our study population are partial migrants: some birds migrate; others winter locally and are accompanied by birds from more northern and eastern breeding populations (Hegemann et al, 2010).…”

“…In contrast, wild skylarks (Alauda arvensis) do not modulate the energetic investment in the acute phase response despite seasonal variation in energetic constraints. They maintain a similar response throughout the annual cycle as measured by metabolic rate, body temperature, body mass loss, ketone and glucose concentrations (Hegemann et al, 2012b). The detailed knowledge of non-induced (baseline) immune function and energetic costs of an immune challenge in skylarks make this species an ideal candidate for studying the response of multiple immune indices during an immune challenge in different annual-cycle stages.…”

“…Even though the captivity period was short, we attempted to avoid a potential seasonal bias by using conditions that reflected current social conditions in the wild. Birds had ad libitum access to water and food (mealworms and seeds) until 16:30h on the experimental-protocol start day (for details, see Hegemann et al, 2012b).We started the experimental protocol by isolating birds in a dark box for 1h without food and water. At 17:30h we injected experimental birds with 2.5mg LPS in 10ml phosphate buffered saline (PBS) per kilogram body mass in their abdominal cavities (Hegemann et al, 2012b).…”

“…Birds had ad libitum access to water and food (mealworms and seeds) until 16:30h on the experimental-protocol start day (for details, see Hegemann et al, 2012b).…”