Common measures of immune function vary with time of day and sampling protocol in five passerine species

Abstract

Ecological immunology is a rapidly growing field of study that focuses on understanding variation in immune systems across species and how this relates to species ecology and evolution. Newly developed field methods aimed at studying variation in immune function in a field setting have yielded many insights. Nonetheless, there continues to be much debate regarding the interpretation of field measures of immune function. There is substantial evidence to suggest that handling stress could introduce variation into measures of immune function, yet no study has examined the impacts of incremental changes in handling times under 30 min on immune measures. Nor has any study examined variation in immune function with time of day, though other physiological measures, including glucocorticoids known to impact immune function, vary with time of day. Here, I used observational field data to test the hypothesis that innate immune function varies with handling stress. Furthermore, I tested the hypothesis that innate immune function changes over the course of the day. I show that measures of innate immune function vary with (1) handling stress over short time periods typical of sample collection in the field, and (2) the time of day that an individual is sampled. I discuss these findings from an ecological perspective and suggest that the observed variation is not random, but is likely to have important adaptive functions. I end with a summary of the practical implications of these findings for field studies of ecological immunology.

Corticosterone rapidly suppresses innate immune activity in the House Sparrow (Passer domesticus)

“…Overall, our results show stress-induced inhibition of innate immune activity and are consistent with previous findings in other free-living birds Matson et al, 2006;Cyr et al, 2007;Merrill et al, 2012;Zylberberg, 2015;Davies et al, 2016). They also indicate that the inhibition of complement-mediated activity occurs with a shorter latency than the inhibition of natural antibody-mediated activity.…”

“…Many studies on this topic have used free-ranging birds as models because the diversity of habitats used by birds and of life history characteristics among species may help identify broad patterns of stress-induced effects on the immune response (Hasselquist, 2007). Several avian species exhibit stressinduced immunosuppression such as reduced microbicidal (Matson et al, 2006;Merrill et al, 2012) and lysozyme activity (Zylberberg, 2015), decreased natural antibody and complement-mediated activity (Davies et al, 2016), and reduced cutaneous immune activity Cyr et al, 2007). Stress, however, has also been observed to enhance acute phase protein activity in the Galápagos flycatcher (Myiarchus magnirostris; Zylberberg, 2015) and phagocytic activity in clay-colored thrushes (Turdus grayi; Millet et al, 2007).…”

“…Several avian species exhibit stressinduced immunosuppression such as reduced microbicidal (Matson et al, 2006;Merrill et al, 2012) and lysozyme activity (Zylberberg, 2015), decreased natural antibody and complement-mediated activity (Davies et al, 2016), and reduced cutaneous immune activity Cyr et al, 2007). Stress, however, has also been observed to enhance acute phase protein activity in the Galápagos flycatcher (Myiarchus magnirostris; Zylberberg, 2015) and phagocytic activity in clay-colored thrushes (Turdus grayi; Millet et al, 2007). These apparently inconsistent findings may result from most studies using one measure of immunity and/or sampling at one point during the stress response.…”

“…In free-ranging birds, by contrast, it is unclear whether corticosterone (CORT), the primary avian glucocorticoid (Schmidt et al, 2010), plays a role in the regulation of stress-induced effects on immunity and whether plasma CORT can directly alter immune activity (Davies et al, 2016). Most studies on this subject have been correlative and do not, therefore, establish a causal relationship between changes in plasma CORT and immune activity (Lindström et al, 2005;Matson et al, 2006;Cyr et al, 2007;Buehler et al, 2008;Zylberberg, 2015). Furthermore, demonstrating that elevated plasma glucocorticoids are the primary regulators of stressinduced changes in immune activity is complicated by the fact that the environment can also influence the development and the function of the immune system (Hasselquist and Nilsson, 2009).…”

Plasticity of immunity in response to eating

“…hemolysis and hemoagglutination are reduced after a flight lasting ≤4 h in European starlings, Sturnus vulgaris: Nebel et al, 2012). These findings suggest a temporally dynamic innate immune system (sensu Zylberberg, 2015) that responds to food consumption. Fine-scale resolution of the speed with which the peak increase occurs and the time until returning to baseline levels will further elucidate the relative importance that eating-induced immune activation has on the energetic budget for consuming food (SDA).…”