A fruit diet rather than invertebrate diet maintains a robust innate immunity in an omnivorous tropical songbird

Abstract

Diet alteration may lead to nutrient limitations even in the absence of food limitation, and this may affect physiological functions, including immunity. Nutrient limitations may also affect the maintenance of body mass and key life‐history events that may affect immune function. Yet, variation in immune function is largely attributed to energetic trade‐offs rather than specific nutrient constraints. To test the effect of diet on life‐history traits, we tested how diet composition affects innate immune function, body mass and moult separately and in combination with each other, and then used path analyses to generate hypotheses about the mechanistic connections between immunity and body mass under different diet compositions. We performed a balanced parallel and crossover design experiment with omnivorous common bulbuls Pycnonotus barbatus in out‐door aviaries in Nigeria. We fed 40 wild‐caught bulbuls ad libitum on fruits or invertebrates for 24 weeks, switching half of each group between treatments after 12 weeks. We assessed innate immune indices (haptoglobin, nitric oxide and ovotransferrin concentrations, and haemagglutination and haemolysis titres), body mass and primary moult, fortnightly. We simplified immune indices into three principal components (PCs), but we explored mechanistic connections between diet, body mass and each immune index separately. Fruit‐fed bulbuls had higher body mass, earlier moult and showed higher values for two of the three immune PCs compared to invertebrate‐fed bulbuls. These effects were reversed when we switched bulbuls between treatments after 12 weeks. Exploring the correlations between immune function, body mass and moult, showed that an increase in immune function was associated with a decrease in body mass and delayed moult in invertebrate‐fed bulbuls, while fruit‐fed bulbuls maintained body mass despite variation in immune function. Path analyses indicated that diet composition was most likely to affect body mass and immune indices directly and independently from each other. Only haptoglobin concentration was indirectly linked to diet composition via body mass. We demonstrated a causal effect of diet composition on innate immune function, body mass and moult: bulbuls were in a better condition when fed on fruits than invertebrates, confirming that innate immunity is nutrient specific. Our results are unique because they show a reversible effect of diet composition on wild adult birds whose immune systems are presumably fully developed and adapted to wild conditions—demonstrating a short‐term consequence of diet alteration on life‐history traits.

Geographic variation in baseline innate immune function does not follow variation in aridity along a tropical environmental gradient

“…www.nature.com/scientificreports www.nature.com/scientificreports/ We did not consider differences in immune indices between sexes because Common Bulbuls are sexually monomorphic. Moreover, in previous studies with Common Bulbuls where we determined sex molecularly, there were no sex related differences for the same immune indices 43,50 . Common Bulbuls are socially monogamous, so we expect a one-to-one sex ratio.…”

“…Variation in innate immune function may therefore not reflect abundance of antigens in the environment 74 , immune function may be more related to actual infection on individuals, and this may depend on habitat use 75 and annual cycle stage. Another factor that may affect immune function is diet 24,50,76 , and Common Bulbuls feed predominantly on fruits and insects despite spatial differences in aridity ( Table 1). All individuals may, therefore, maintain similar levels of innate immune function because their diet was similar across the aridity gradient, even if food was limited for some individuals.…”

“…High immune indices may also reflect absence of food limitation in more productive environments 49 . For example, we know that well fed Common Bulbuls in good body condition maintain high natural antibody and complement activity, but low haptoglobin concentration, whereas poorly fed Bulbuls in poor body condition show the reverse 50 . So, if increasing aridity decreases infection risk, reduced susceptibility to infection should lead lower immune indices with increasing aridity.…”

Local timing of rainfall predicts the timing of moult within a single locality and the progress of moult among localities that vary in the onset of the wet season in a year-round breeding tropical songbird

“…In Common Bulbuls, the onset of moult is strongly dependent on individual condition and it correlates positively with body mass and immune function which both depend on diet (Nwaogu et al 2020). Therefore, the observation that the mean start date of moult (5th May) is a few weeks after the onset of the wet season in Jos, suggests a causal link between environmental productivity and the onset of moult.…”

“…1) close to the river Benue, there was no bulbul moulting two weeks before we visited Tula. Moult may, therefore, be linked to a range of factors that are associated with specific aspects of environmental condition like food, diet and nutrients rather than the occurrence of water or rainfall (Murphy 1996;Nwaogu et al 2020).…”