Human recreation decreases antibody titres in bird nestlings: an overlooked transgenerational effect of disturbance

Abstract

Outdoor recreational activities are booming and most animals perceive humans as predators, which trigger behavioural and/or physiological reactions (e.g. heart rate increase, activation of the hypothalamic-pituitary-adrenal (HPA) axis). Physiological stress reactions have been shown to affect the immune system of an animal and therefore may also affect the amount of maternal antibodies a female transmits to her offspring. A few studies revealed that the presence of predators affects the amount of maternal antibodies deposited into eggs of birds. In this study, using Eurasian blue and great tit offspring (Cyanistes caeruleus and Parus major) as model species, we experimentally tested whether human recreation induces changes in the amount of circulating antibodies in young nestlings and whether this effect is modulated by habitat and competition. Moreover, we investigated whether these variations in antibody titres have, in turn, an impact on hatching success and offspring growth. Nestlings of great tit females, which had been disturbed by experimental human recreation during egg-laying, had lower antibody titres compared to control nestlings. Antibody titres of nestling blue tits showed a negative correlation with the presence of great tits, rather than with human disturbance. The hatching success was positively correlated with the average amount of antibodies in great tit nestlings, independent of the treatment. Antibody titres in the first days of life in both species were positively correlated with body mass, but this relationship disappeared at fledging and was independent of the treatment. We suggest that human recreation may have caused a stress-driven activation of the HPA-axis in breeding females, chronically increasing their circulating corticosterone, which is known to have an immunosuppressive function. Therefore lower amounts of antibodies can be transmitted to nestlings or impaired transfer mechanisms lead to lower amounts of immunoglobulins in the eggs. Human disturbance could, therefore, have negative effects on nestling survival at early life-stages, when nestlings are heavily relying on maternal antibodies, and in turn lead to lower breeding success and parents’ fitness. This is a so far overlooked effect of disturbance on early life in birds.