Immune system activation interacts with territory-holding potential and increases predation of the damselfly Calopteryx splendens by birds

Abstract

Activation of the immune system in insects has been shown to be costly in the laboratory setting, but experimental studies in the field are lacking. The costs of immunity in the wild may be different to those in the laboratory because animals in the wild are simultaneously subjected to a suite of selective agents. We have measured the costs of immune system activation in a wild population of the territorial damselfly Calopteryx splendens. Immune-challenged males were found to be less likely to be territorial and had lower overall survival rates than control or sham-manipulated males. Because territorial males have a higher mating success than nonterritorial males, this result suggests that immune-challenged males are also likely to suffer reduced mating success. However, the activation of the immune system as such did not increase predation risk; this occurred due to a combination of the former with a reduced territory-holding potential. As such, immune-challenged males not holding a territory were most susceptible to predation by birds. The size of the wing spots, a known sexually selected male trait, predicted territorial behaviour in control and sham-manipulated males, but not in immune-challenged males. Our data show that immune system activation can have several costs acting in unison and that ubiquitous ecological interactions, such as predation, may affect trade-offs between immunity and other life history traits.

Evolutionary Ecology of Odonata: A Complex Life Cycle Perspective

“…Tests of a direct causal link between these costs and fitness effects are lacking, however, partly because most studies did not manipulate parasite load (but see, e.g., 14). Reduced energetic content may have direct negative effects on life span through starvation and, together with the mechanical costs, cause a reduced ability to escape from predators such as birds (77). Effects on lifetime mating success may be explained indirectly by the shortened life span (2, 24) but also by the increased need to allocate time to foraging (14) and by the lowered ability to pay the energetic costs of searching for females and fighting (18, 36).…”

Support for the Immunocompetence Handicap Hypothesis in the Wild: Hormonal Manipulation Decreases Survival in Sick Damselflies

“…The recapture rates (detectability) we found give support to the idea that Met increased territorial activity in a long term: Met‐treated males were easier to detect during the daily surveys, presumably because they became more territorial and therefore more faithful to their defended sites (Munguía‐Steyer et al 2010). The reduced effect of bacterial treatment on recapture probabilities seems unexpected according to previous findings in other calopterygids, in which immune response activation has been associated with enhanced dispersal (Suhonen et al 2010) and reduced territorial behavior (Rantala et al 2010), which would lead to lower recapture rates in infected animals. Unfortunately, our capture–recapture approach does not allow determining precise causes for the observed recapture rates.…”

Immune deployment increases larval vulnerability to predators and inhibits adult life‐history traits in a dragonfly

“…Because we were interested in estimating just those costs of mounting an immune response, we did not include an unmanipulated control, which often differs from sham treatments in many ways beyond closing the wound caused by the sham treatment (e.g. stress response, Sadd et al ., ; Rantala et al ., ). Although we cannot rule out the possibility of causing an incidental infection during the sham and challenge procedures, we punctured the cuticle of all individuals in the study, and any effects of the immune‐challenge treatments therefore act in addition to any such incidental infection.…”

“…Additionally, predator‐induced behavioural or developmental modifications (Benard, ; Relyea, ) may also deplete resources that would otherwise be available for the trade‐offs between immune deployment and important adult traits. Yet, despite the widespread importance of the lethal and nonlethal effects of predation risk on juvenile life stages (Lima, ; Abrams, ; Moore et al ., ), few studies have experimentally assessed how predation shapes the costs of immune deployment generally (Rantala et al ., ; Otti et al ., ; Janssens & Stoks, ), and no studies have considered how it affects the costs of immune deployment both within and across life stages under ecologically relevant conditions.…”