Differential effects of elevated nest temperature and parasitism on the gut microbiota of wild avian hosts

Background Changes in wild animal gut microbiotas may influence host health and fitness. While many studies have shown correlations between gut microbiota structure and external factors, few studies demonstrate causal links between environmental variables and microbiota shifts. Here, we use a fully factorial experiment to test the effects of elevated ambient temperature and natural nest parasitism by nest flies (Protocalliphora sialia) on the gut microbiotas of two species of wild birds, the eastern bluebird (Sialia sialis) and the tree swallow (Tachycineta bicolor). Results We find that bacterial communities from the nestlings of each host species show idiosyncratic responses to both heat and parasitism, with gut microbiotas of eastern bluebirds more disrupted by heat and parasitism than those of tree swallows. Thus, we find that eastern bluebirds are unable to maintain stable associations with their gut bacteria in the face of both elevated temperature and parasitism. In contrast, tree swallow gut microbiotas are not significantly impacted by either heat or nest parasitism. Conclusions Our results suggest that excess heat (e.g., as a result of climate change) may destabilize natural host-parasite-microbiota systems, with the potential to affect host fitness and survival in the Anthropocene.

Differential Effects of Elevated Nest Temperature and Parasitism on the Gut Microbiota of Wild Avian Hosts

Background: Changes in wild animal gut microbiotas may influence host health and fitness. While many studies have shown correlations between gut microbiota structure and external factors, few studies demonstrate causal links between environmental variables and microbiota shifts. Here, we use a fully factorial experiment to test the effects of elevated ambient temperature and natural nest parasitism by nest flies (Protocalliphora sialia) on the microbiotas of two species of wild birds, the eastern bluebird (Sialia sialis) and the tree swallow (Tachycineta bicolor).Results: We find that bacterial communities from the nestlings of each host species show differential response to both heat and parasitism, with gut microbiotas of eastern bluebirds more disrupted by heat and parasitism than those of tree swallows. Thus, we find that eastern bluebirds are unable to maintain stable associations with their gut bacteria in the face of both elevated temperature and parasitism. In contrast, tree swallow gut microbiotas are not significantly impacted by either heat or nest parasitism.Conclusions: Our results suggest that excess heat (e.g., as a result of climate change) may destabilize natural host-parasite-microbiota systems, with the potential to affect host fitness and survival in the anthropocene.

Elevated nest temperature has opposing effects on host species infested with parasitic nest flies

Hosts have developed or evolved defense strategies, including tolerance and resistance, to reduce damage caused by parasites. Environmental factors, such as elevated temperature, can influence the effectiveness of these different host defenses but also can directly affect parasite fitness. Therefore, the net effect of elevated temperature on host-parasite relationships are determined by its direct effects on the host and the parasite. Furthermore, because host species can defend themselves differently against their parasites, the net effect of temperature might differ across each hosts interaction with the same parasite. Few studies have determined the net effects of temperature on both host defenses and parasites in a multi-host system. To address this gap, we experimentally manipulated temperature and parasite presence in the nests of two host species who defend themselves differently to the same parasitic nest fly (Protocalliphora sialia). Specifically, we conducted a factorial experiment by increasing temperature (or not) and removing all parasitic nest flies (or not) in the nests of tolerant eastern bluebirds (Sialia sialis) and resistant tree swallows (Tachycineta bicolor). We then quantified parasite load in nests and measured nestling body size metrics, blood loss, and survival. If temperature predominately affected parasite fitness, then elevated temperature would cause similar directional effects on parasite abundance across species. If temperature has different effects on hosts, then parasite abundance would differ in response to elevated temperature across host species. In contrast to previous years, we found that bluebird nests had half as many parasites as compared to swallow nests. Elevated temperature affected parasite abundance differently in each host species. Swallows from heated nests had fewer parasites compared to non-heated nests, suggesting that they were more resistant to the parasites. Interestingly, swallows from heated nests were also more tolerant to the effects of parasites than controls. In contrast, bluebirds from heated nests had more parasites and lower body mass compared to controls, suggesting that they lost tolerance, and resistance, to the parasites. Our results suggest that a changing climate could have complex net effects on host-parasite interactions, including on host defenses, with implications for host health and parasite survival.

Eastern Bluebirds (Sialia sialis) use color patterning, but not the colors themselves, as a cue to eject interspecific parasitic eggs

Brood parasitism results in substantial costs to hosts, yet not all species eject foreign eggs. Because the costs of mistakenly ejecting one’s own eggs are high, selection may favor ejection behavior only if it is unlikely a host will incorrectly eject her own eggs. Eastern Bluebirds (Sialia sialis) are currently subject to relatively low levels of interspecific brood parasitism but still sometimes eject parasitic eggs. Therefore, we tested which visual cues they use to eject foreign eggs with the prediction that only the most dissimilar eggs would be ejected, reducing the likelihood of a female making a mistake. House Sparrows (Passer domesticus), which occasionally parasitize bluebirds, lay eggs that have an off-white ground color with brown speckling. Therefore, to test which colors or patterns allow for discrimination of parasitic eggs, we generated 3-dimensional (3D)-printed model House Sparrow eggs and painted them entirely off-white, entirely brown, half off-white and half brown, or off-white with brown speckling. We then sequentially placed these 4 different model eggs in the nests of Eastern Bluebirds, with each nest receiving all treatments over the course of 4 days. After watching females enter and leave the nest box just one time after placement of the model egg, we found that speckled eggs were ejected half the time (7 of 14 nests), while no other treatment was ejected more than 3 times. Thus, Eastern Bluebird females eject eggs based primarily on color patterning (i.e. a speckled pattern) rather than coloration per se, and that they can do so quickly, as the average female had removed the model egg within 6 min of entering the nest. Because Eastern Bluebirds do not lay speckled eggs, but some brood parasites do (e.g., House Sparrows, Brown-headed Cowbirds [Molothrus ater]), selection may specifically favor ejection of eggs with a speckled pattern, not just eggs that have within-egg color contrasts.

Expanding our view of Bartonella and its hosts: Bartonella in nest ectoparasites and their migratory avian hosts

Background Bartonella is a genus of Gram-negative facultative intracellular Alphaproteobacteria of public health importance. Although they are known to mainly infect mammalian hosts with some blood-feeding arthropods having been confirmed as vectors, there is some evidence of Bartonella association with non-mammalian hosts including birds. Methods Here we used high-throughput sequencing of 16S rRNA and Sanger sequencing of the citrate synthase (gltA) genes to test for the presence of Bartonellaceae in the blood of three migratory cavity nesting bird species, purple martins (Progne subis), tree swallows (Tachycineta bicolor) and eastern bluebirds (Sialia sialis) and their most prevalent and abundant nest ectoparasites, Dermanyssus prognephilus (mite), Ceratophyllus idius (flea) and Protocalliphora sialia (bird blow fly larva). We constructed maximum likelihood phylogenetic trees to verify the placement of the resulting sequences in the Bartonellaceae. Results We found evidence of Bartonella in all three bird species and all three arthropod species tested. We report multiple instances of identical Bartonella sequences in both birds and parasites, leading to the likely hypothesis that these ectoparasites are potential vectors of Bartonella. Our phylogenetic analysis suggests that ‘avian Bartonella’ may form its own sub-clade within the genus Bartonella. Conclusions To the best of our knowledge, we provide the first confirmation of overlapping Bartonella strains among bird hosts and various species of nest-associated ectoparasites from the same system, suggesting a possible Bartonella host–vector relationship between these arthropods and a non-mammalian host. Our study adds to the growing appreciation of the Bartonellaceae as a phylogenetically diverse group with a wide range of hosts.