Nest predation risk modifies nestlings’ immune function depending on the level of threat

Abstract

Predation risk is thought to modify the physiology of prey mainly through the stress response. However, little is known about its potential effects on the immunity of animals, particularly in young individuals, despite the importance of overcoming wounding and pathogen aggression following a predator attack. We investigated the effect of four progressive levels of nest predation risk on several components of the immune system in common blackbird () nestlings by presenting them with four different calls during 1 h: non-predator calls, predator calls, parental alarm calls and conspecific distress calls to induce a null, moderate, high and extreme level of risk, respectively. Nest predation risk induced an increase in ovotransferrin, immunoglobulin and the number of lymphocytes and eosinophils. Thus, the perception of a potential predator per se could stimulate the mobilization of a nestling's immune function and enable the organism to rapidly respond to the immune stimuli imposed by a predator attack. Interestingly, only high and extreme levels of risk caused immunological changes, suggesting that different immunological parameters are modulated according to the perceived level of threat. We also found a mediator role of parasites (i.e. ) and the current health status of the individual, as only nestlings not parasitized or in good body condition were able to modify their immune system. This study highlights a previously unknown link between predation risk and immunity, emphasizing the complex relationship among different selective pressures (predation, parasitism) in developing organisms and accentuating the importance of studying predation from a physiological point of view.

Immunological changes in nestlings growing under predation risk

“…1), we collected a blood sample (250-300 μl) from the brachial vein of all chicks of that nest. We always collected the blood sample in a day in which the speakers did not play to ensure that we quantify the long-term effect of increased predation rather than the short-term increase in nest predation risk (Roncalli et al 2018). All blood samples were collected between 10 am and 2 pm and kept refrigerated (4°C, maximum 5 h) until centrifugation (13 000 rpm for 10 min).…”

“…We performed several immunological assays to quantify 12 parameters belonging to both the humoral and cellular component of the immune system as well as to innate and acquired immunity (Janeway et al 1997). The objective of this multiple measurements was to capture the complexity of the immune system (Matson et al 2006), since we previously found that not all components of blackbirds' immune system respond similarly to a (punctual) increase of nest predation risk (Roncalli et al 2018).…”

“…A recent study in common blackbird Turdus merula nestlings has shown a more complex immune response to predators as only some of the parameters analyzed (e.g. ovotransferrin, immunoglobulins and part of their white blood cells) changed due to a short-term increased predation risk (Roncalli et al 2018). These alterations are suggested to be used for preparing the organism to cope with the potential deleterious consequences imposed by the imminent predator attack (Roncalli et al 2018).…”

“…ovotransferrin, immunoglobulins and part of their white blood cells) changed due to a short-term increased predation risk (Roncalli et al 2018). These alterations are suggested to be used for preparing the organism to cope with the potential deleterious consequences imposed by the imminent predator attack (Roncalli et al 2018). These changes may therefore be adaptive and not a by-product of corticosterone variations, enabling nestlings to improve their probability of surviving a predator's attack.…”

“…We experimentally increased the risk of perceived nest predation during the whole nestling period in common blackbird nestlings and analyzed 12 immunological variables to obtain a complete overview of the potential changes associated with our long-term experiment. Regarding the first objective and based on the results of a short-term manipulation of nest predation risk in the same blackbird population (Roncalli et al 2018), we predict that chicks exposed to our treatment will activate (at least) part of their immune system to face a potential attack (prediction 1a). However, given that an activation of the immune system seems to be initially induced by a threat, whereas an immunosuppression is a more common response to long-term stressors, when stress hormonal levels are high (Dhabhar 2002, Martin 2009, it could be also predicted a down-regulation of the immune system when facing a long-term increase in predation risk (prediction 1b).…”