Endogenous biomarkers reveal diet partitioning among three sympatric species of swallows

Since the early 1990s, aerial insectivorous birds have shown serious population declines in North America, but it is not clear if factors common to all species within this guild account for these declines. Among sympatric swallows, population trends differ, and this may be due to differences in ecology operating throughout the annual cycle. Although these species all feed on aerial insects, prey taxa can differ tremendously in their “aeroecology” and use by swallows. We examined the potential for dietary differences among three species of swallows, Barn Swallow (Hirundo rustica), Cliff Swallow (Petrochelidon pyrrhonota), and Tree Swallow (Tachycineta bicolor), breeding sympatrically in southern Ontario, Canada. Potential interspecific differences in nestling diet were examined using two endogenous biomarkers, DNA barcoding of nestling feces and stable isotope analysis (δ 2H, δ 13C, δ 15N) of nestling feathers. We found evidence for differences in dietary sources of provisioned young where Barn Swallows provisioned more terrestrial-based prey, Cliff Swallows provisioned an intermediate diet, and Tree Swallows the most aquatic-emergent insect diet. We suggest this information may help to identify potential factors contributing to differential declines of aerial insectivores operating on the breeding grounds, including diet quality.

Nest decoration: birds exploit a fear of feathers to guard their nest from usurpation

Many species of birds incorporate feathers into their nest as structural support and to insulate the eggs or offspring. Here, we investigated the novel idea that birds reduce the risk of nest usurpation by decorating it with feathers to trigger a fear response in their rivals. We let prospecting birds choose between a dyad of nest-boxes in the wild, both containing some nest materials, but where one had a few white feathers and the other had none. All three species of cavity-nesting birds studied, the pied flycatcher Ficedula hypoleuca , the blue tit Cyanistes caeruleus , and the tree swallow Tachycineta bicolor , hesitated to enter boxes with white feathers. A similar avoidance of white feathers was found when the alternative nest-box of a dyad held black feathers. However, the birds readily collected white feathers that we placed in front of their nest-box, showing the fear of such feathers was context-dependent. We suggest that naive prospecting birds may perceive feathers in nests as the result of a predation event, and that owners decorate nests with bright feathers that can be seen from the opening to deter others from entering.

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.

Oxidative damage increases with degree of simulated bacterial infection, but not ectoparasitism, in tree swallow nestlings

ABSTRACT The purpose of mounting an immune response is to destroy pathogens, but this response comes at a physiological cost, including the generation of oxidative damage. However, many studies on the effects of immune challenges employ a single high dose of a simulated infection, meaning that the consequences of more mild immune challenges are poorly understood. We tested whether the degree of immunological challenge in tree swallows (Tachycineta bicolor) affects oxidative physiology and body mass, and whether these metrics correlate with parasitic nest mite load. We injected 14 day old nestlings with 0, 0.01, 0.1 or 1 mg lipopolysaccharide (LPS) per kg body mass, then collected a blood sample 24 h later to quantify multiple physiological metrics, including oxidative damage (i.e. d-ROMs), circulating amounts of triglyceride and glycerol, and levels of the acute phase protein haptoglobin. After birds had fledged, we identified and counted parasitic nest mites (Dermanyssus spp. and Ornithonyssus spp.). We found that only nestlings injected with 1 mg LPS kg−1 body mass, which is a common dosage in ecoimmunological studies, lost more body mass than individuals from other treatment groups. However, every dose of LPS resulted in a commensurate increase in oxidative damage. Parasitic mite abundance had no effect on oxidative damage across treatments. The amount of oxidative damage correlated with haptoglobin levels, suggesting compensatory mechanisms to limit self-damage during an immune response. We conclude that while only the highest-intensity immune challenges resulted in costs related to body mass, even low-intensity immune challenges result in detectable increases in oxidative damage.

Body temperature is a repeatable trait in a free-ranging passerine bird

Body temperature (Tb) affects animal function through its influence on rates of biochemical and biophysical reactions, the molecular structures of proteins and tissues, and ultimately, organismal performance. Despite its importance in driving physiological processes, there are few data on how much variation in Tb exists within populations of organisms, and whether this variation consistently differs among individuals over time (i.e., repeatability of a trait). Here, using thermal radio-frequency identification implants, we quantified the repeatability of Tb, both in the context of a fixed average environment (∼21 °C) and across ambient temperatures (6 – 31 °C), in a free-living population of tree swallows (Tachycineta bicolor, n=16). By experimentally trimming the ventral plumage of a subset of female swallows (n=8), we also asked whether the repeatability of Tb is influenced by the capacity to dissipate body heat. We found that both female and male tree swallow Tb was repeatable at 21 °C (R=0.89 – 92), but female Tb was less repeatable than male Tb across ambient temperature (Rfemale=0.10, Rmale=0.58), which may be due to differences in parental investment. Trimmed birds had on average lower Tb than control birds (by ∼0.5 °C), but the repeatability of female Tb did not differ as a function of heat dissipation capacity. This suggests that trimmed individuals adjusted their Tb to account for the effects of heat loss on Tb. Our study provides evidence a first critical step toward understanding if Tb is responsive to natural selection, and for predicting how animal populations will respond to climatic warming.

Phenotypic differences among wild passerine nestlings in relation to early-life rearing environment

Subtle changes in stress physiology during critical developmental stages have been linked to long-term fitness; however, the biological processes and phenotypic responses to early-life rearing environments such as anthropogenic land use conditions, have not been fully evaluated in insectivorous birds. We manipulated Tree Swallow, Tachycineta bicolor (Vieillot, 1808), brood sizes at sites with contrasting agricultural land use to assess phenotypic changes in body condition and genetic and physiological biomarkers of stress during the sensitive nestling growth phase. We predicted that nestling swallows raised on cropland-dominated sites, especially those in enlarged broods, would have lower body condition, shorter telomeres, and higher feather corticosterone than nestlings raised in smaller broods at grassland sites. Body condition was highest among nestlings raised in reduced broods but was unrelated to land use. Telomere lengths tended to be shorter in nestlings from enlarged broods and at cropland sites. Corticosterone was not related to any factor. Locally-abundant insect populations associated with wetlands may have dampened the effects and/or parent swallows assumed higher costs of reproduction rather than passing these costs to nestlings. Results suggest that food stress could reduce fledgling survival via telomere shortening; a hypothesis that requires further investigation due to its potential importance to population viability in multiple declining aerial insectivore species.

Interacting effects of cold snaps, rain, and agriculture on the fledging success of a declining aerial insectivore

Climate change predicts the increased frequency, duration, and intensity of inclement weather periods, such as unseasonably low temperatures and prolonged precipitation. Many migratory species have advanced the phenology of important life history stages, and as a result are likely exposed to these periods of inclement spring weather more often, thus risking reduced fitness and population growth. For declining avian species, including aerial insectivores, anthropogenic landscape changes such as agricultural intensification are another driver of population declines. These landscape changes may affect the foraging ability of food provisioning parents, as well as reduce the probability a nestling will survive periods of inclement weather, through for example pesticide exposure impairing thermoregulation and punctual anorexia. Breeding in agro-intensive landscapes may thus exacerbate the negative effects of inclement weather under climate change. We used daily temperatures related to significant reductions of insect prey availability (cold snaps), combined with measures of precipitation, and assessed their impact on Tree Swallow (Tachycineta bicolor) fledging success, a declining aerial insectivore breeding across a gradient of agricultural intensification. Fledging success decreased with the number of cold snap days experienced by a brood, and this relationship was worsened during periods of prolonged precipitation. We further found the overall negative effects of experiencing periods of inclement weather are exacerbated in more agro-intensive landscapes. Our results indicate that two of the primary hypothesized drivers of many avian population declines may interact to further increase the rate of declines in certain landscape contexts.

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.

Negative effects of agricultural intensification on energetic gain rates of a declining aerial insectivore

The historical rise of intensive agricultural practices is hypothesized to be related to declines of grassland and aerial insectivorous birds. Drivers of declines may also influence the overall abundance and spatial distribution of insects within agricultural landscapes. Subsequently, average energetic gain rates of birds breeding within more agro-intensive landscapes may be impacted. Lower energetic gain rates in agro-intensive landscapes may lead to reduced growth rate, body condition or fledging success of nestlings but also to diminished body condition of food provisioning adults. In this study, we assessed if energetic gain of nestlings and food provisioning behavior of adults varied across a gradient of agricultural intensification in a declining aerial insectivore, the Tree swallow (Tachycineta bicolor). We found that hourly gain rate was lower in agro-intensive landscapes, and yet travel distances were longest within less agro-intensive landscapes. Our results highlight that, in order to maximize long term average gain rates, Tree swallows breeding within agro-intensive landscapes must forage with greater intensity, perhaps at a cost to themselves, or else costs will transfer to growing broods. Our work provides further evidence that agricultural intensification on the breeding grounds can contribute to the declines of aerial insectivores in part through a trophic pathway.

Agricultural pesticides and ectoparasites: potential combined effects on the physiology of a declining aerial insectivore

Agricultural pesticides usage has been increasing globally. These compounds have been developed to disrupt pest species physiology, but because their specificity is limited, they can also have adverse effects on non-target organisms. Recent studies have shown that the damaging toxicological effects of pesticides can be amplified in stressful environments. However, few studies have documented these effects in natural settings where organisms are simultaneously exposed to pesticides and to other environmental stressors such as parasites. In this study, we assessed both pesticide and ectoparasite effects on the physiology of a free-ranging bird. We measured physiological markers including haematocrit, bacteria-killing ability (BKA) and leucocyte counts, as well as exposure to haematophagous Protocalliphora larvae, in tree swallow nestlings (Tachycineta bicolor), a declining aerial insectivore, in southern Québec, Canada, for over 3 years. We found that combined exposure to pesticides and Protocalliphora larvae was negatively related to haematocrit, suggesting possible synergistic effects. However, we found no such relationships with BKA and leucocyte counts, highlighting the complexity of physiological responses to multiple stressors in natural settings. Populations of several aerial insectivores are declining, and although sublethal pesticide effects on physiology are suspected, our results suggest that exposure to other factors, such as parasitism, should also be considered to fully assess these effects, especially because pesticides are increasingly present in the environment.