Dietary fatty acids modulate oxidative stress response to air pollution but not to infection.

Anthropogenic changes to the environment expose wildlife to many pollutants. Among these, tropospheric ozone is of global concern and a highly potent pro-oxidant. In addition, human activities include several other implications for wildlife, e.g., changed food availability and changed distribution of pathogens in cities. These co-occurring habitat changes may interact, thereby modulating the physiological responses and costs related to anthropogenic change. For instance, many food items associated with humans (e.g., food waste and feeders for wild birds) contain relatively more ω6-than ω3-polyunsaturated fatty acids (PUFAs). Metabolites derived from ω6-PUFAs can enhance inflammation and oxidative stress towards a stimulus, whereas the opposite response is linked to ω3-derived metabolites. Hence, we hypothesized that differential intake of ω6-and ω3-PUFAs modulates the oxidative stress state of birds and thereby affects the responses towards pro-oxidants. To test this, we manipulated dietary ω6:ω3 ratios and ozone levels in a full-factorial experiment using captive zebra finches (Taeniopygia guttata). Additionally, we simulated an infection, thereby also triggering the immune system's adaptive pro-oxidant release (i.e., oxidative burst), by injecting lipopolysaccharide. Under normal air conditions, the ω3-diet birds had a lower antioxidant ratio (GSH/GSSG ratio) compared to the ω6-diet birds. When exposed to ozone, however, the diet effect disappeared. Instead, ozone exposure overall reduced the total concentration of the key antioxidant glutathione (tGSH). Moreover, the birds on the ω6-rich diet had an overall higher antioxidant capacity (OXY) compared to birds fed a ω3-rich diet. Interestingly, only the immune challenge increased oxidative damage, suggesting the oxidative burst of the immune system overrides the other pro-oxidative processes, including diet. Taken together, our results show that ozone, dietary PUFAs, and infection all affect the redox-system, but in different ways, suggesting that the underlying responses are decoupled despite that they all increase pro-oxidant exposure or generation. Despite lack of apparent cumulative effect in the independent biomarkers, the combined single effects could together reduce overall cellular functioning and efficiency over time in wild birds exposed to pathogens, ozone, and anthropogenic food sources.

Urban tree composition is associated with breeding success of a passerine bird, but effects vary within and between years.

Birds breeding in urban environments have lower reproductive output compared to rural conspecifics, most likely because of food limitation. However, which characteristics of urban environments may cause this deficiency is not clear. Here, we investigated how tree composition within urban territories of passerine birds is associated with breeding probability and reproductive success. We used 7 years of data of breeding occupancy for blue and great tits (Cyanistes caeruleus; Parus major) and several reproductive traits for great tits, from 400 urban nest boxes located in 5 parks within the city of Malmö, Sweden. We found that tits, overall, were less likely to breed in territories dominated by either non-native trees or beech trees. Great tit chicks reared in territories dominated by non-native trees weighed significantly less, compared to territories with fewer non-native trees. An earlier onset of breeding correlated with increased chick weight in great tits. Increasing number of common oak trees (Quercus robur) was associated with delayed onset of breeding in great tits. Notably, as offspring survival probability generally increased by breeding earlier, in particular in oak-dominated territories, our results suggest that delayed onset of breeding induced by oak trees may be maladaptive and indicate a mismatch to this food source. Our results demonstrate that tree composition may have important consequences on breeding success of urban birds, but some of these effects are not consistent between years, highlighting the need to account for temporal effects to understand determinants of breeding success and inform optimal management in urban green spaces.

Quantifying the influence of urban biotic and abiotic environmental factors on great tit nestling physiology.

There is a long history of avian studies investigating the impacts of urbanization. While differences in several life-history traits have been documented, either between urban and rural populations or across generalized urbanization gradients, a detailed understanding of which specific environmental variables cause these phenotypic differences is still lacking. Here, we quantified several local environmental variables coupled to urbanization (air pollution, tree composition, ambient temperature, and artificial light at night [ALAN]) within territories of breeding great tits (Parus major). We linked the environmental variables to physiological measures of the nestlings (circulating fatty acid composition [FA], antioxidant capacity and an oxidative damage marker [malondialdehyde; MDA]), to garner a mechanistic understanding of the impact of urbanization. We found that the antioxidant capacity of nestlings decreased with higher numbers of oak trees and levels of PM2.5 (airborne particulate matter with a diameter < 2.5 µm). Furthermore, the ratio of ω6:ω3 polyunsaturated FAs, important for immune function, was positively correlated with PM2.5 concentration, while being negatively associated with ambient temperature and number of non-native trees in the territory. Body mass and wing length both increased with the number of local oak trees. We also show, through a principal component analysis, that while the environmental variables fall into an urbanization gradient, this gradient is insufficient to explain the observed physiological responses. Therefore, accounting for individual environmental variables in parallel, and thus allowing for interactions between these, is crucial to fully understand the urban ecosystem.

Contrasting effects of tree origin and urbanization on invertebrate abundance and tree phenology.

The ongoing wide-scale introduction of nonnative plants across the world may negatively influence native invertebrate fauna, due to a lack of coevolved traits related to the novel plants, e.g., unique phytochemicals or shifted phenology. Nonnative plants, specifically trees, are common in urban environments, areas that already pose novel habitats to plants and wildlife through a wide array of anthropogenic factors. For example, impervious surfaces contribute to increased ambient temperatures, the so-called urban heat island effect (UHI), which can affect local plant phenology. Yet, few studies have simultaneously studied the effects of urbanization and tree species origin on urban invertebrate communities. We measured the city-level UHI and phenology of nine native and seven nonnative tree species in five city-center parks in southern Sweden, as well as four common native species in a rural control forest. We quantified the abundance of invertebrates on a subset of native and nonnative tree species through shake sampling, sticky traps, and frass collection. In the urban environment, nonnative trees hosted significantly fewer invertebrates compared to native trees. Furthermore, the nonnative trees had a delayed phenology compared to native species, while the peak of caterpillars associated with the subset of trees surveyed for this measure was significantly earlier compared to that of the native species studied. The effect of tree species origin on urban invertebrate abundance was of a greater magnitude (effect size) than the effect of urbanization on invertebrate abundance in native tree hosts. Hence, the results indicate that the impact of nonnative vegetation may be a stronger driver of invertebrate declines in urban areas than other factors. As the effect of species origin on tree phenology was at a level comparable to the urban effect, increasing prevalence of nonnative vegetation can potentially obscure effects of urbanization on phenology in large-scale studies, as well as induce mismatches to invertebrate populations. Since parks harbor a large proportion of urban biodiversity, native trees play a crucial role in such habitats and should not be considered replaceable by nonnative species in terms of conservation value.

Migrant blackbirds, Turdus merula, have higher plasma levels of polyunsaturated fatty acids compared to residents, but not enhanced fatty acid unsaturation index.

Birds have been observed to have dietary preferences for unsaturated fatty acids during migration. Polyunsaturated fatty acids (PUFAs) may increase the exercise performance of migrant birds; however, PUFAs are also peroxidation prone and might therefore incur increased costs in terms of enhanced oxidative damage in migratory individuals. To shed light on this potential constraint, we analyzed plasma fatty acid (FA) composition and estimated the unsaturation index as a proxy for susceptibility to lipid peroxidation of migrants and residents of the partially migratory common blackbird (Turdus merula) at a stopover site during autumn migration. As predicted, migrant birds had higher relative and absolute levels of PUFAs compared to resident birds. This included the strictly dietary ω-3 PUFA α-linolenic acid, suggesting a dietary and/or storage preference for these FAs in migrants. Interestingly, the FA unsaturation index did not differ between migrants and residents. These findings suggest a mechanism where birds alter their levels of metabolic substrate without simultaneously increasing the susceptibility of the substrate to lipid peroxidation. In summary, our results are in line with the hypothesis that increased exercise performance during migration might be constrained by oxidative stress, which is manifested in changes in the composition of key FAs to retain the unsaturation index constant despite the increased levels of peroxidizable PUFAs.