Age-related variation in the oral microbiome of urban Cooper's hawks (Accipiter cooperii)

Abstract

Background: Bird species worldwide are affected by trichomoniasis caused by the protist Trichomonas gallinae. In avivorous raptors such as Cooper's hawks (Accipiter cooperii), nestlings are more susceptible than fledglings and adults. Previous research suggested a link between oral pH and susceptibility: the oral pH of fledgling and adult hawks is more than seven times more acidic than that of nestlings. We speculated that this age-specific difference in pH would correspond to age-specific differences in the oral microbiota of Cooper's hawks. We examined the oral microbiomes of 31 healthy, wild Cooper's hawks in Tucson, Arizona (USA). Individuals represented three age classes (nestlings, fledglings, and adults). We designed our study with multiple controls, replicated sampling, mock communities, and stringent quality-controls to address challenges that can limit the inferential quality of microbiome data sets.

Results: Richness of bacterial communities in oral cavities of Cooper's hawks differed as a function of age but not as a function of sex, sampling date, or sampling location. Bacterial communities in oral cavities of nestlings differed from those of fledglings and adults, whereas communities in fledglings and adults did not differ from each other. Communities were similar in males and females and did not differ over the sampling season. Prevalence of acid-producing bacteria in fledgling and adults vs. nestlings is consistent with previous reports of age-specific variation in oral pH, but further research is needed to establish a causal link to pH levels or susceptibility to disease. Analyses of mock communities demonstrated high repeatability and showed that operon number and read abundance were highly correlated.

Conclusions: The oral microbiota of wild Cooper's hawks differs between nestlings and older birds. Variation in the oral microbiome is consistent with differences in oral pH between nestlings and older individuals. Overall our study provides a first perspective on bacterial communities associated with oral cavities of a wild raptor.

Keywords: 16S rRNA; Accipitridae; Bacteria; Porphyromonas; Raptors; Trichomonas; pH.

Fig. 1

Bacterial richness in the oral cavity of individual Cooper’s hawks differed as a function of age class. Mean richness was lower in fledglings than in nestlings or adults. Results reflect data from 430 operational taxonomic units (OTU) that passed stringent quality control. Bars represent 95% confidence intervals for nestlings and adults; variation was relatively low among fledglings

Fig. 2

Communities of bacteria in the oral cavity differed as a function of age class in Cooper’s hawks. Non-metric multi-dimensional scaling analyses of the 55 most common operational taxonomic units (OTU) reveal that communities of bacteria in the oral cavity differ between nestlings (open circles) and more mature age classes (fledglings, open squares; adults, filled circles), which in turn did not differ from each other. Results are consistent when evaluated using (a) presence-absence data (Jaccard’s Index) or (b) read number as a proxy for abundance (Simpson’s Index)