The role of parasitism in the energy management of a free-ranging bird

Abstract

Parasites often prompt sub-lethal costs to their hosts by eliciting immune responses. These costs can be hard to quantify but are crucial to our understanding of the host's ecology. Energy is a fundamental currency to quantify these costs, as energetic trade-offs often exist between key fitness-related processes. Daily energy expenditure (DEE) comprises of resting metabolic rate (RMR) and energy available for activity, which are linked via the energy management strategy of an organism. Parasitism may play a role in the balance between self-maintenance and activity, as immune costs can be expressed in elevated RMR. Therefore, understanding energy use in the presence of parasitism enables mechanistic elucidation of potential parasite costs. Using a gradient of natural parasite load and proxies for RMR and DEE in a wild population of breeding European shags (Phalacrocorax aristotelis), we tested the effect of parasitism on maintenance costs as well as the relationship between proxies for RMR and DEE. We found a positive relationship between parasite load and our RMR proxy in females but not males, and no relationship between proxies for RMR and DEE. This provides evidence for increased maintenance costs in individuals with higher parasite loads and suggests the use of an allocation energy management strategy, whereby an increase to RMR creates restrictions on energy allocation to other activities. This is likely to have fitness consequences as energy allocated to immunity is traded off against reproduction. Our findings demonstrate that understanding energy management strategies alongside fitness drivers is central to understanding the mechanisms by which these drivers influence individual fitness.

Keywords: Accelerometry; Daily energy expenditure; Immune costs; Resting metabolic rate; Thyroid hormones; Trade-off.

Fig. 1.

Graphical representation of energy budgets and possible energy management strategies. (A) Daily energy expenditure (DEE) is the sum of resting metabolic rate (RMR) and activity metabolism. (B) Three theorized energy management strategies in graphical form adapted from Mathot and Dingemanse (2015) and Careau and Garland (2012) showing the relationship between RMR and DEE and activity metabolism under the three scenarios. The dashed 1-to-1 line is presented to aid interpretation of the slope of the lines. It represents a theoretical situation under which animals are completely inactive and thus DEE is equal to RMR.

Fig. 2.

Relationship between parasite load and plasma total 3,3′-triiodo-L-thyronine (T3) concentration (a proxy for RMR) in female European shags. Data points represent individual T3 concentrations, the predicted lines from the best-supported model (solid lines) and their 95% confidence intervals (dashed). (A) The relationship between parasite load and T3 concentration when year and brood age are accounted. (B) The interaction between parasite load and brood age in relation to T3 concentration, the explanatory terms in the best-supported model. Solid lines represent predicted lines from the best-supported model under different brood age scenarios −1 s.d. of the mean brood age (light blue), mean brood age (mid-blue) and +1 s.d. of the mean (dark blue).

Fig. 3.

Significant relationship between adult age and plasma total T3 concentration (a proxy for RMR) in male European shags. Data points represent individual T3 concentrations, solid lines the predicted lines from the best-supported model and dashed lines their 95% confidence intervals.

Fig. 4.

Relationship between plasma total T3 concentration (a proxy for RMR) and estimated DEE in terms of rate of oxygen consumption in European shags. Dots represent individual T3 concentrations. The predicted lines from the best-supported model (solid lines) and their 95% confidence intervals (dashed) are presented for males (blue) and females (orange). V̇_O2, rate of oxygen consumption.