Effects of diet macronutrient content on avian feeding behavior, physiology, and gut microbiota.
Diet macronutrient content did not affect feeding behavior, with birds consuming similar amounts of food regardless of diet treatment. Surprisingly, we did not find an effect of diet on complement activity or baseline or stress-induced corticosterone concentrations. Contrary to our results, several studies have found a relationship between diet and various metrics of the complement pathway. In fish, alternative complement activity (ACH50) is higher when fish were fed diets with 8% or higher lipid levels when compared with fish fed a lipid-free control diet (Lin and Shiau 2003). Similarly, in mice, a high-fat diet induces complement activation and proinflammatory cytokine production (Doerner et al. 2016). Previous work investigating the effects of dietary macronutrients on stress physiology found that kittiwake chicks fed a low-lipid diet had higher baseline and stress-induced concentrations of corticosterone (Kitaysky et al. 2001). Conversely, but similar to our results, corticosterone concentrations were unaffected by dietary supplementation with anthropogenic items like bread in captive white ibis (Cummings et al. 2020). It is possible that more dramatic shifts in macronutrient ratios between diet treatments or having longer time frames on the diets is required to detect large effects on host immune and endocrine physiology.
While we did not find a direct effect of diet treatment on complement activity or corticosterone concentrations, the gut microbiome is capable of both influencing and responding to these physiological endpoints (Williams et al. 2020), which can occur independently of changes in diet, or possibly be indirectly influenced by diet through another metric that was not measured in the present study. For example, higher glucocorticoid levels are associated with lower bacterial diversity in squirrels (Petrullo et al. 2022) and gulls (Noguera et al. 2018). Complement activity has also been linked to changes in gut microbiota. Depletion of gut commensal bacterial inhibits complement activation in mice (Yoshiya et al. 2011), and in tilapia fish complement C3 is positively correlated with the Shannon’s and Simpson’s index of gut microbiota (Zhu et al. 2020). In our study, complement activity was positively correlated with observed richness and Shannon diversity on day 0, but this relationship was disrupted on day 8. Baseline corticosterone concentrations did not significantly affect microbial richness or diversity, while stress-induced concentrations were generally associated with higher Shannon diversity. However, the positive association between stress-induced corticosterone and Shannon diversity was not apparent in birds on a protein diet prior to treatment (day 0) or birds fed a high fat diet post-treatment (day 8). For both complement and stress-induced corticosterone, birds in the high fat diet treatment shifted from having a positive association between physiology and gut microbiota alpha diversity metrics at day 0 to a negative association between metrics following 8 days on a high fat diet. This suggests that diet macronutrient ratios can influence the relationship between gut microbial communities and physiology and that the fat content of diet might be important in altering these relationships.
While the diet treatments in experiment 1 (diet manipulation) did not have major effects on overall gut microbiota composition, we found that protein content can shift the abundance of particular taxa. While community-level changes in gut microbiota can have important implications for host health, smaller changes in specific taxa can also affect host physiological processes (Hooper et al. 2012, Round and Mazmanian 2009). Specifically, we found that birds fed a high protein diet for 8 days had lower proportions of the phylum Campylobacterota. Previous work in mice found that individuals fed a high fat diet have a higher relative abundance of the genus Campylobacter (a member of the Phylum Campylobacterota), and Campylobacter abundance was positively correlated with serum lipid levels (Mu et al. 2020). The association between a high fat diet and members of Campylobacterota might explain why we observed a decrease in the abundance of Campylobacterota in birds on the high protein diet but not birds fed the high fat diet or diet with equal ratios of fat and protein.