Innate immune function and antioxidant capacity of nestlings of an African raptor covary with the level of urbanisation around breeding territories

Abstract

Urban areas provide breeding habitats for many species. However, animals raised in urban environments face challenges such as altered food availability and quality, pollution and pathogen assemblages. These challenges can affect physiological processes such as immune function and antioxidant defences which are important for fitness. Here, we explore how levels of urbanisation influence innate immune function, immune response to a mimicked bacterial infection and antioxidant capacity of nestling Black Sparrowhawks Accipiter melanoleucus in South Africa. We also explore the effect of timing of breeding and rainfall on physiology since both can influence the environmental condition under which nestlings are raised. Finally, because urbanisation can influence immune function indirectly, we use path analyses to explore direct and indirect associations between urbanisation, immune function and oxidative stress. We obtained measures of innate immunity (haptoglobin, lysis, agglutination, bactericidal capacity), indices of antioxidant capacity (total non‐enzymatic antioxidant capacity (tAOX) and total glutathione from nestlings from 2015 to 2019. In addition, in 2018 and 2019, we mimicked a bacterial infection by injecting nestlings with lipopolysaccharide and quantified their immune response. Increased urban cover was associated with an increase in lysis and a decrease in tAOX, but not with any of the other physiological parameters. Furthermore, except for agglutination, no physiological parameters were associated with the timing of breeding. Lysis and bactericidal capacity, however, varied consistently with the annual rainfall pattern. Immune response to a mimicked a bacterial infection decreased with urban cover but not with the timing of breeding nor rainfall. Our path analyses suggested indirect associations between urban cover and some immune indices via tAOX but not via the timing of breeding. Our results show that early‐life development in an urban environment is associated with variation in immune and antioxidant functions. The direct association between urbanisation and antioxidant capacity and their impact on immune function is likely an important factor mediating the impact of urbanisation on urban‐dwelling animals. Future studies should explore how these results are linked to fitness and whether the responses are adaptive for urban‐dwelling species.

Urban living can rescue Darwin's finches from the lethal effects of invasive vampire flies

“…(2017) observed overrepresented genes involved in the secretion and receptor‐binding of cytokines in urban great tits ( Parus major ) compared to non‐urban tits. Additionally, urban nestling black sparrowhawks ( Accipiter melanoleucus ) had a stronger innate response to an immune challenge compared to non‐urban nestlings (Nwaogu et al., 2023). These studies provide evidence that urban living could confer an advantage against parasitism.…”

“…Gene expression profiles showed that urban nestlings differentially express innate immune genes associated with pro-inflammatory cytokines, specifically type-1 IFNs, compared to non-urban nestlings. When larval flies chew through the skin of their hosts, effective inflammation by the host (e.g., thickening the skin and restricting blood flow) can prevent ectoparasite feeding (reviewed in Owen et al, 2010) (Nwaogu et al, 2023). These studies provide evidence that urban living could confer an advantage against parasitism.…”

The impact of urbanization on health depends on the health metric, life stage and level of urbanization: a global meta-analysis on avian species

“…It is well documented in the literature that organisms inhabiting urban environments can face negative implications to their health and wellbeing [ 19 , 29 , 73 ]. Our results indicate that there is no significant effect of urbanization on overall avian health.…”

“…In two Australian passerines, coccidian infection increases with increasing urbanization in red-brown finches ( Neochima temporalis ), but not in superb fairy wrens ( Malurus cyaneus ) [ 28 ]. In black sparrowhawks ( Accipiter melanoleucus ), urbanization was negatively associated with some biomarkers of immunity and oxidative stress, while the majority of such markers were not affected [ 29 ]. Similarly, a large comparative analysis on the prevalence of Salmonella and Campylobacter in birds, two avian gastrointestinal bacteria, showed that while Salmonella prevalence was mostly affected by ecological factors including urbanization where prevalence was higher in urban areas, Campylobacter prevalence was largely associated with life-history traits [ 30 ].…”

Urban living can rescue Darwin’s finches from the lethal effects of invasive vampire flies

“…For example, Watson et al, (2017) observed overrepresented genes involved in the secretion and receptor-binding of cytokines in urban great tits ( Parus major ) compared to non-urban tits. Additionally, urban nestling black sparrowhawks ( Accipiter melanoleucus ) had a stronger innate response to an immune challenge compared to non-urban nestlings (Nwaogu et al, 2023). Although these studies were unable to link the heightened innate immune response in urban nestlings to parasite resistance, they provide evidence that urban living could confer an advantage against parasitism.…”