Carotenoid‐induced maternal effects interact with ectoparasite burden and brood size to shape the trade‐off between growth and immunity in nestling great tits

Abstract

1. Carotenoids are fat-soluble pigments that stimulate the immune system and can act as antioxidants. Carotenoids are thus expected to buffer the effects of environmental stressors on health. As carotenoids are a limited resource, the ability of an individual to use and metabolize carotenoids is assumed to influence its stress-resistance. Accordingly, it has been found that nestlings hatched from eggs with increased carotenoid concentration, show an enhanced ability to use carotenoids and a lower susceptibility of tissues to lipid peroxidation. 2. We tested the prediction that nestling great tits (Parus major), hatched from eggs laid by carotenoid-supplemented mothers, cope better with a transient stressor encountered after hatching. We supplemented half of the breeders with carotenoids during egg production (C+), used the other half as a control (C-), and cross-fostered the eggs between nests after clutch completion. Three days after hatching, we applied a stressor in two-third of the nests either by increasing brood size, or by infesting nests with hen fleas (Ceratophyllus gallinae) during five consecutive days. A third group was kept as a control. We then assessed the responses of C+ and C- nestlings to each stressor by measuring mass gain, body condition, plumage coloration, humoral immune response and fever response to a lipopolysaccharide injection. 3. In control nests, C+ and C- nestlings showed similar body condition but C+ nestlings had a higher increase in body temperature and tended to have a higher wing web swelling in response to lipopolysaccharide injection. Under stress, however, there were no differences in overall condition between C+ and C- nestlings. The two stressors led to different responses: when sibling competition was increased, C- nestlings favoured immune development, whereas C+ nestlings favoured mass gain and body condition, while under parasite exposure C+ and C- nestlings seemed to invest in immune development and body growth similarly. 4. Our results support the hypothesis that carotenoid-induced maternal effects provide developmental benefits under natural conditions without additional stressors. Additionally, we show that the response to sudden environmental changes depends on the environment during the initial phases of development, which thus shape phenotype and individual variation.