Complex relationships between physiological stress and endoparasite infections in natural populations

Short-term elevation of glucocorticoids (GCs) is one of the major physiological mechanisms by which vertebrates cope with challenging environmental or social factors (stressors). However, when exposure to stressors occurs repeatedly or over a prolonged period of time, animals may experience chronic elevation of GCs, which reduces the immune response efficiency and can lead to higher intensity of parasitic infection. Here, we used invasive grey squirrels Sciurus carolinensis introduced in N. Italy and their two most prevalent gastro-intestinal parasites, the nematode Strongyloides robustus and coccidia of the genus Eimeria, as a model to investigate relationships among macroparasite infection and concentrations of faecal glucocorticoid metabolites (FGMs), an integrated measure of circulating GCs. Our results revealed an association of FGMs with infection by S. robustus, but not with coccidia. Individuals with higher FGMs appear to be responsible for the greatest S. robustus egg shedding within grey squirrel populations, thus possibly acting as super-spreaders. However, FGMs were negatively associated with adult S. robustus, suggesting that the abundance of adults of this nematode species does not induce elevation in FGMs, but is only affected by it through immune-mediated effects on its fecundity. Finally, the relationship between S. robustus (both eggs and adult parasites) and FGMs was not linear, suggesting that only high levels of physiological stress influence parasite infection. Our findings highlight that the direction and magnitude of the stress-infection relationship may depend not only on the specific host-parasite system, but also on the different life stages of the same parasite.