Traffic noise exposure alters nestling physiology and telomere attrition through direct, but not maternal, effects in a free-living bird.

Anthropogenic impacts, such as noise pollution from transportation networks, can serve as stressors to some wildlife species. For example, increased exposure to traffic noise has been found to alter baseline and stress-induced corticosterone levels, reduce body condition and reproductive success, and increase telomere attrition in free-living birds. However, it remains unknown if alterations in nestling phenotype are due to direct or indirect effects of noise exposure. For example, indirect (maternal) effects of noise may occur if altered baseline and stress-induced corticosterone in mothers results in differential deposition of yolk steroids or other components in eggs. Noise exposure may also alter nestling corticosterone levels directly, given that nestlings cannot escape the nest during development. Here, we examined maternal versus direct effects of traffic noise exposure on baseline and stress-induced corticosterone levels, and body condition (as measured by size-corrected mass) in nestling tree swallows (Tachycineta bicolor). We used a two-way factorial design and partially cross-fostered eggs between nests exposed to differing levels (i.e. amplitudes) of traffic noise. For nestlings that were not cross-fostered, we also investigated the effects of traffic noise on telomere dynamics. Our results show a positive relationship between nestling baseline and stress-induced corticosterone and nestling noise exposure, but not maternal noise exposure. While we did not find a relationship between noise and body condition in nestlings, nestling baseline corticosterone was negatively associated with body condition. We also found greater telomere attrition for nestlings from nests with greater traffic noise amplitudes. These results suggest that direct, rather than maternal, effects result in potentially long-lasting consequences of noise exposure. Reduced nestling body condition and increased telomere attrition have been shown to reduce post-fledging survival in this species. Given that human transportation networks continue to expand, strategies to mitigate noise exposure on wildlife during critical periods (i.e. breeding) may be needed to maintain local population health in free-living passerines, such as tree swallows.

Effects of experimental chronic traffic noise exposure on adult and nestling corticosterone levels, and nestling body condition in a free-living bird.

Transportation noise affects urbanized, rural, and otherwise unaltered habitats. Given expanding transportation networks, alterations in the acoustic landscapes experienced by animals are likely to be pervasive and persistent (i.e. chronic). It is important to understand if chronic noise exposure alters behavior and physiology in free-living animals, as it may result in long-lasting impacts, such as reduced reproductive success. Here, we experimentally tested the effects of chronic traffic noise on baseline and stress-induced corticosterone (the primary avian glucocorticoid), parental feeding behavior, and fitness proxies in breeding tree swallows (Tachycineta bicolor). Our results show that chronic traffic noise is related to altered corticosterone in both adult female and nestling tree swallows, suggesting that noise may be a stressor in both groups. In adult females, our results suggest that traffic noise is related to a limited ability to respond to subsequent acute stressors (i.e. reduced stress-induced corticosterone levels after handling). Further, our results show no evidence of habituation to noise during the breeding season, as the negative relationship between traffic noise and adult female stress-induced corticosterone became stronger over time. In nestlings, we found a positive relationship between traffic noise exposure and baseline corticosterone. Finally, we found a negative relationship between traffic noise and nestling body condition, despite no detectable effects of noise on nestling provisioning (e.g. parental feeding rate, or insect bolus size/composition). These results highlight the potential long-term consequences of chronic noise exposure, as increased baseline corticosterone and reduced nestling body condition in noise-exposed areas may have negative, population-level consequences.

Testosterone production and social environment vary with breeding stage in a competitive female songbird.

In many vertebrates, males increase circulating testosterone (T) levels in response to seasonal and social changes in competition. Females are also capable of producing and responding to T, but the full extent to which they can elevate T across life history stages remains unclear. Here we investigated T production during various breeding stages in female tree swallows (Tachycineta bicolor), which face intense competition for nesting sites. We performed GnRH and saline injections and compared changes in T levels 30 min before and after injection. We found that GnRH-injected females showed the greatest increases in T during territory establishment and pre-laying stages, whereas saline controls dramatically decreased T production during this time. We also observed elevated rates of conspecific aggression during these early stages of breeding. During incubation and provisioning, however, T levels and T production capabilities declined. Given that high T can disrupt maternal care, an inability to elevate T levels in later breeding stages may be adaptive. Our results highlight the importance of saline controls for contextualizing T production capabilities, and they also suggest that social modulation of T is a potential mechanism by which females may respond to competition, but only during the period of time when competition is most intense. These findings have broad implications for understanding how females can respond to their social environment and how selection may have shaped these hormone-behavior interactions.

Plasma Testosterone Levels Increase with Expression of Male Ornaments During Mating, but not Incubation, in Japanese Barn Swallows.

Recent experimental studies involving the manipulation of sexual traits have demonstrated that sexual trait expression feeds back to testosterone levels, perhaps via social interactions, reinforcing the linkage between sexual trait expression and testosterone levels during the mating period. However, information on this reinforcement under the natural variation of sexual traits remains limited. Using Japanese barn swallows, Hirundo rustica gutturalis, in which extra-pair paternity is quite rare (< 3%), we studied the relationship between plasma testosterone level and a male sexual trait, throat patch size, during the mating and incubation periods. Given the importance of social interaction, we predicted that this relationship should be intense during the mating period, but not the incubation period, due to reduced social interaction during the latter. We found low plasma testosterone levels during the incubation period compared with those in the mating period, and plasma testosterone levels were significantly positively related to throat patch area during the mating period, but not the incubation period. Similar relationships were found in another sexual trait, the size of white tail spots. During the incubation period, body condition, instead of male sexual trait expression, was negatively related to plasma testosterone level, indicating that an intrinsic link, rather than reinforcement, is important during this period. These relationships are consistent with the hypothesis that social interaction reinforces the relationship between sexual traits and plasma testosterone levels. The current study provides evidence for a highly variable relationship between testosterone and ornamentation across breeding periods in the natural variation of sexual traits.

Agricultural Intensification Is Linked to Constitutive Innate Immune Function in a Wild Bird Population.

Immunity represents an important defense mechanism against pathogens and is intimately linked to fitness. Previous studies have found significant interindividual variation of immune responses in wild populations and have emphasized the importance of ecological factors in explaining this variability. A deterioration of environmental conditions, such as agricultural intensification, can modify resource availability and, as a result, alter immune functions. The aim of this study was to investigate the effect of agricultural intensification on innate immune functions in breeding adult tree swallows (Tachycineta bicolor) over 6 yr. We investigated the relationship between agricultural intensification and bacteria-killing ability (BKA) against a strain of E. coli. We also assessed how the presence and the number of bacteria on the surface of eggshells changed with agricultural intensification. Contrary to our expectations, we found a positive relationship between agricultural intensification and BKA, where individuals had higher BKA in intensive compared to nonintensive farmlands. While this trend was observed through the 6-yr study, we also found a tendency for a reduction of BKA over time. We found no relationships between the presence or number of different types of eggshell bacteria and agricultural intensification or an association between BKA of females and eggshell bacteria of their clutch. Our results suggest that differences in immune function observed between intensive and nonintensive farmlands could reflect genetic differences among individuals and/or trade-offs with other traits expressed among habitats within our study system.

Nestling rearing is antioxidant demanding in female barn swallows (Hirundo rustica).

Reproduction is a demanding activity, since organisms must produce and, in some cases, protect and provision their progeny. Hence, a central tenet of life-history theory predicts that parents have to trade parental care against body maintenance. One physiological cost thought to be particularly important as a modulator of such trade-offs is oxidative stress. However, evidence in favour of the hypothesis of an oxidative cost of reproduction is contradictory. In this study, we manipulated the brood size of wild barn swallows Hirundo rustica soon after hatching of their nestlings to test whether an increase in nestling rearing effort translates into an increased oxidative damage and a decreased antioxidant protection at the end of the nestling rearing period. We found that, while plasma oxidative damage was unaffected by brood size enlargement, females rearing enlarged broods showed a decrease in plasma non-enzymatic antioxidants during the nestling rearing period. This was not the case among females rearing reduced broods and among males assigned to either treatment. Moreover, individuals with higher plasma oxidative damage soon after the brood size manipulation had lower plasma non-enzymatic antioxidants at the end of the nestling rearing period, suggesting that non-enzymatic antioxidants were depleted to buffer the negative effects of high oxidative damage. Our findings point to antioxidant depletion as a potential mechanism mediating the cost of reproduction among female birds.

Riparian swallows as integrators of landscape change in a multiuse river system: implications for aquatic-to-terrestrial transfers of contaminants.

Recent research has highlighted the transfer of contaminants from aquatic to terrestrial ecosystems via predation of aquatic emergent insects by riparian consumers. The influence of adjacent land use and land cover (LULC) on aquatic-to-terrestrial contaminant transfer, however, has received limited attention. From 2010 to 2012, at 11 river reaches in the Scioto River basin (OH, USA), we investigated the relationships between LULC and selenium (Se) and mercury (Hg) concentrations in four species of riparian swallows. Hg concentrations in swallows were significantly higher at rural reaches than at urban reaches (t=-3.58, P<0.001, df=30), whereas Se concentrations were positively associated with adjacent land cover characterized by mature tree cover (R(2)=0.49, P=0.006). To an extent, these relationships appear to be mediated by swallow reliance on aquatic emergent insects. For example, tree swallows (Tachycineta bicolor) at urban reaches exhibited a higher proportion of aquatic prey in their diet, fed at a higher trophic level, and exhibited elevated Se levels. We also found that both Se and Hg concentrations in adult swallows were significantly higher than those observed in nestlings at both urban and rural reaches (Se: t=-2.83, P=0.033, df=3; Hg: t=-3.22, P=0.024, df=3). Collectively, our results indicate that riparian swallows integrate contaminant exposure in linked aquatic-terrestrial systems and that LULC may strongly regulate aquatic contaminant flux to terrestrial consumers.

Testosterone, plumage colouration and extra-pair paternity in male North-American barn swallows.

In most monogamous bird species, circulating testosterone concentration in males is elevated around the social female's fertile period. Variation in elevated testosterone concentrations among males may have a considerable impact on fitness. For example, testosterone implants enhance behaviours important for social and extra-pair mate choice. However, little is known about the relationship between natural male testosterone concentration and sexual selection. To investigate this relationship we measured testosterone concentration and sexual signals (ventral plumage colour and tail length), and determined within and extra-pair fertilization success in male North American barn swallows (Hirundo rustica erythrogaster). Dark rusty coloured males had higher testosterone concentrations than drab males. Extra-pair paternity was common (42% and 31% of young in 2009 and 2010, respectively), but neither within- nor extra-pair fertilization success was related to male testosterone concentration. Dark rusty males were less often cuckolded, but did not have higher extra-pair or total fertilization success than drab males. Tail length did not affect within- or extra-pair fertilization success. Our findings suggest that, in North American barn swallows, male testosterone concentration does not play a significant direct role in female mate choice and sexual selection. Possibly plumage colour co-varies with a male behavioural trait, such as aggressiveness, that reduces the chance of cuckoldry. This could also explain why dark males have higher testosterone concentrations than drab males.

The stress of parenthood? Increased glucocorticoids in birds with experimentally enlarged broods.

Variation in baseline glucocorticoid (cort) levels can be attributed, at least in part, to differences in energetic demands confronting individuals. Elevated baseline cort levels are routinely interpreted as indicating individuals in poor condition, with low relative fitness. However, when greater reproductive effort increases energetic demands, individuals with high cort might paradoxically be those with the highest fitness. Here, we experimentally test the hypothesis that increased reproductive demand causes increases in baseline cort (the Cort-Adaptation hypothesis). We measured maternal baseline cort before and after experimentally enlarging and reducing brood sizes in tree swallows (Tachycineta bicolor). Females with experimentally enlarged broods had greater increases in baseline cort and fledged more offspring than females with reduced broods. Additionally, females with greater increases in baseline cort had higher offspring-provisioning rates than females with lower changes in cort. These findings demonstrate that increased reproductive demand can cause increased baseline cort. As yet, we do not know if these increases in cort cause increased allocation of resources towards reproduction, but the positive relationship between parental behaviour and cort suggests that increased cort does not always interfere with reproductive investment, and might instead facilitate it.

Mercury exposure and survival in free-living tree swallows (Tachycineta bicolor).

Mercury has become a ubiquitous contaminant in food chains worldwide. A large body of literature detailing bioaccumulation and effects on birds has revealed the potential for mercury to adversely impact avian physiology and reproduction. However, the extent to which these effects impair survival remains poorly understood. The objective of this study was to determine whether mercury exposure was associated with reduced annual survivorship in tree swallows (Tachycineta bicolor) breeding at a site with legacy industrial contamination. From 2005 to 2008, we captured and marked 932 adult swallows. We used Cormack-Jolly-Seber models and an information-theoretic approach to test our hypotheses that adult survival varied by sex, breeding location, and cumulative individual mercury exposure. Blood mercury was significantly elevated on contaminated sites (2005-2007 combined mean ± SE: 2.84 ± 0.09 µg/g; reference: 0.17 ± 0.01 µg/g). Model-averaged estimates of female apparent survival ranged from 0.483 to 0.488 on reference sites and 0.473 to 0.477 on contaminated sites. For males, apparent survival ranged from 0.451 to 0.457 on reference sites and 0.444 to 0.448 on contaminated sites. Thus, we observed approximately a 1% difference in survival between mercury-contaminated and reference sites. Such a small difference is unlikely to impact population viability in this short-lived species; however, some songbirds accumulate mercury to a greater degree than tree swallows and do not possess the migratory behavior that removes swallows to less contaminated areas for the majority of the year. Identifying whether such species are at risk of suffering biologically significant reductions in survival should become a focus of future research.

Body condition is associated with adrenocortical response in the barn swallow (Hirundo rustica L.) during early stages of autumn migration.

Migration is an energy-demanding life-history period and also a significant population-limiting factor of long-distance migratory birds. It is important to understand how corticosterone, the main energy regulating hormone in birds, is associated with behavioural and physiological changes during migration. According to the migration modulation hypothesis (MMH), individual birds may express elevated levels of baseline corticosterone to facilitate fuelling, but down-regulate the adrenocortical response in order to protect skeletal muscles from the catabolic effects of the hormone. We measured the baseline and stress-induced levels of corticosterone in barn swallows (Hirundo rustica L.) during early stages of autumn migration. Here, we show that, while barn swallows clearly responded to the capture and handling stress by increasing the corticosterone level, the strength of this acute response was related to their energetic condition: birds with high body mass responded more rapidly and had lower peak values of corticosterone than lighter birds. Further, the baseline levels of corticosterone correlated negatively with the magnitude of the adrenocortical response. Barn swallows did not show elevated baseline levels of corticosterone in the course of autumn, which suggests that, instead of fuelling, the birds were actively migrating. Our results indicate that MMH also applies to aerial feeders, whose foraging habits differ from model birds of previous studies.

Increased oxidative stress in barn swallows from the Chernobyl region.

The Chernobyl nuclear accident produced the largest unintended release of radionuclides in history, with dramatic consequences for humans and other organisms. Exposure to ionizing radiation is known to reduce circulating and stored levels of specific antioxidants in birds and humans, thus potentially increasing oxidative stress. However, overall effects of radioactive exposure on oxidative status have never been investigated in any free ranging vertebrate. We measured plasma antioxidant capacity and concentration of reactive oxygen metabolites in adult barn swallows (Hirundo rustica) from colonies with variable background radiation levels in the Chernobyl region in Ukraine and Belarus. We predicted that antioxidants would decrease while reactive oxygen metabolites would increase with exposure to increasing levels of radiation at the breeding sites. Consistent with this expectation, radiation level positively predicted plasma concentration of reactive oxygen metabolites, whereas no significant covariation was found with non-enzymatic plasma antioxidant capacity. An index of oxidative stress was also larger in barn swallows exposed to high contamination levels. Thus, radioactive contamination appeared to be responsible for the increased generation of reactive oxygen metabolites and the imbalance between reactive oxygen metabolites and non-enzymatic plasma antioxidant capacity.

Peripheral blood leukocyte counts in welcome swallow nestlings.

It is unclear whether developmental trends in total leukocyte (WBC) and differential lymphocyte (PropL) counts in peripheral blood of altricial birds typically mirror the known ontogenetic increase in immunocompetence. We documented the development of leukocyte and lymphocyte numbers in peripheral blood of wild, altricial Welcome Swallow (Hirundo neoxena) nestlings. Nestlings had a mass-overshoot-recession growth profile. Hatchlings' mean WBC (7.94 x 10(9) cells/l) and PropL (0.65) were respectively 4x and approximately 1.7x the mean adult value. Both variables declined at a steady rate throughout nestling development and were 1.3x the mean adult value at fledging. Hatching WBC values that substantially exceeded those of adults could have reflected the parasite- and pathogen-rich nest environment of this species. The developmental declines in peripheral blood WBC and PropL were not inconsistent with an ontogenetic increase in specific immunocompetence; they are likely to have resulted mainly from an increase in the rate of leukocyte trafficking to vulnerable tissues and organs.

Stone Lakes virus (family Togaviridae, genus Alphavirus), a variant of Fort Morgan virus isolated from swallow bugs (Hemiptera: Cimicidae) west of the Continental Divide.

Multiple isolates of an alphaviruses within the western equine encephalomyelitis-serocomplex that were related closely to Ft. Morgan and its variant Buggy Creek virus were made from swallow bugs, Oeciacus vicarius Horvath (Hemiptera: Cimicidae), collected from cliff swallow (Petrochelidon pyrrhonota) nests at the Stone Lakes National Wildlife Refuge, Sacramento County, CA, during the summers of 2005 and 2006. This virus (hereafter Stone Lakes virus, family Togaviridae, genus Alphavirus, STLV) was the first record of this viral group west of the Continental Divide. STLV replicated well in Vero and other vertebrate cell cultures but failed to replicate in C6/36 cells or infect Culex tarsalis Coquillett mosquitoes. STLV failed to produce elevated viremias in adult chickens or house sparrows and was weakly immunogenic. In addition, STLV was not isolated from cliff swallow nestlings nor was antibody detected in adults collected at mist nets. We suggest that STL and related swallow bug viruses may be primarily infections of cimicids that are maintained and amplified either by vertical or nonviremic transmission and that cliff swallows may primarily be important as a bloodmeal source for the bugs rather than as an amplification host for the viruses.

The corticosterone stress response and mercury contamination in free-living tree swallows, Tachycineta bicolor.

We determined mercury concentrations in tree swallows, Tachycineta bicolor, from Massachusetts and Maine with different levels of contamination. Baseline and stress-induced plasma corticosterone concentrations from adults and nestlings (Massachusetts only) were compared with mercury concentrations. In Massachusetts, adult baseline corticosterone was negatively correlated with blood mercury, but showed a nearly-significant positive correlation with feather mercury. There was a negative relationship between baseline corticosterone and blood mercury in nestlings and between baseline corticosterone and egg mercury. There was no relationship between mercury and stress-induced corticosterone in any of the groups, or with baseline corticosterone in Maine sites where mercury levels were lower. The findings suggest blood and egg mercury may be a better indicator of current condition than feather mercury. Further, mercury contamination may not alter stress-induced corticosterone concentrations in tree swallows but appears to have a significant impact on baseline circulating corticosterone.

The relationship between fitness and baseline glucocorticoids in a passerine bird.

Glucocorticoid (cort) hormones are increasingly applied in studies of free-ranging animals, with elevated baseline cort levels generally assumed to indicate individuals or populations in worse condition and with lower fitness (the Cort-Fitness Hypothesis). The relationship between cort and fitness is rarely validated and studies investigating the cort-fitness relationship often find results inconsistent with the Cort-Fitness Hypothesis. The inconsistency of these studies may result in part from variation in the cort-fitness relationship across life history stages. Here we address the following questions in a two-year study in free-ranging tree swallows (Tachycineta bicolor): (1) Do baseline cort levels correlate with fitness within a life history stage? (2) Does the cort-fitness relationship vary across different life history stages? (3) Does the cort-fitness relationship vary across life history stages within an individual? (4) Does reproductive effort influence cort levels, and do cort levels influence reproductive effort? We measured baseline cort and fitness components in female birds of known breeding stages. We find correlations between baseline cort levels and fitness within some life history stages, but the relationship shifts from negative during early breeding to positive during late breeding, even within the same individuals. A positive relationship between baseline cort and fitness components during the nestling period suggests that reproductive investment may elicit higher cort levels that feedback to reallocate more effort to reproduction during critical periods of nestling provisioning. Our findings provide reason to question the Cort-Fitness Hypothesis, and have implications for the application of cort measures in monitoring the condition of populations of conservation concern.

Patterns of variation in leucocyte counts of female tree swallows, Tachycineta bicolor: repeatability over time and relationships with condition and costs of reproduction.

The heterophil to lymphocyte (HL) ratio in the peripheral blood is increasingly being recognized as a reliable indicator of stress in birds. In this study we examined whether HL ratio, as well as the proportion of heterophils and lymphocytes, varied systematically with sampling time, date, age, climate conditions or with measures of maternal investment in female tree swallows (Tachycineta bicolor) over three breeding seasons. We found that HL ratios showed significant annual variation, which appeared to be driven by annual changes in the proportion of heterophils. HL ratios were higher among those females laying larger clutches, suggesting a potential cost of reproduction. Variation in body condition also appeared to affect stress levels of females, as decreases in body condition were associated with elevated HL ratios. Among females that we sampled over multiple breeding seasons, we were unable to detect significant repeatability for both HL ratios and proportion of heterophils, although proportion of lymphocytes showed low but significant repeatability within individuals. We therefore suggest that caution should be exercised in using these measures for illustrating the inherent quality or health of individuals over time frames beyond the current breeding attempt, or as predictors of future reproductive potential.

Glucocorticoid response to food availability in breeding barn swallows (Hirundo rustica).

Parents feeding altricial nestlings have to trade-off the competing demands of self-maintenance and reproductive investment over their lifetime. Corticosterone, a glucocorticoid hormone released by birds in response to stressors, might play a key role in regulating parental investment when conditions unexpectedly deteriorate. However, birds breeding in unpredictable environmental conditions have been shown not to increase circulating levels of corticosterone as a response to bad weather to avoid nest abandonment when investment in offspring is high or when the probability of re-nesting is low. We investigated whether parent barn swallows Hirundo rustica, a passerine bird whose aerial insect food varies greatly in abundance depending on weather, also belongs to those species or whether it responds with an activation of the hypothalamo-pituitary-adrenal axis to natural variation in insect availability. We correlated plasma corticosterone levels of parents with weather conditions, the availability of aerial insects and parental body condition. Plasma corticosterone concentrations increased when mean daytime temperature declined, and consequently insect availability decreased and body condition of the parents deteriorated. Low temperatures also had a negative effect on body mass of the nestlings and there was a negative relationship between circulating corticosterone of parents and body mass of nestlings. We conclude that corticosterone is probably involved in the regulation of parental investment.

Thyroid function in nestling tree swallows and eastern bluebirds exposed to non-persistent pesticides and p, p'-DDE in apple orchards of southern Ontario, Canada.

This study examined the associated effects of pesticides and persistent residues of p,p'-DDE on thyroid function in 16-day-old tree swallows (Tachycineta bicolor) and 12-day-old eastern bluebirds (Sialia sialis). Apple orchards sprayed with pesticides in current use and reference sites were chosen for study in southern Ontario, Canada, during 2000-2001. We assessed thyroid hormone concentrations (plasma and muscle thyroxine [T4], and triiodothyronine [T3]) and the response to a challenge with thyroid stimulating hormone (TSH) as well as parameters of thyroid histology. Individual nests were exposed to as many as seven individual pesticide applications and up to five pesticide mixtures. Concentrations of p,p'-DDE in eggs from both species were highest in orchard sites, and ranged from 0.05 to 5.44 mg/kg wet weight for tree swallows, and from 0.17 to 95.4 mg/kg for eastern bluebirds. In 2000, tree swallows from sprayed orchards had elevated plasma T4 concentrations, and thyroid glands with collapsed follicles, hypertrophic epithelia, and higher follicular epithelial cells relative to chicks from reference sites. Plasma T4 concentration was positively correlated with the total number of pesticide mixtures applied during egg incubation through chick rearing. In 2001, basal plasma T3 concentration in tree swallow chicks did not differ between orchard and reference sites, though there were differences among orchards; T3 was positively correlated with total number of individual sprays applied during egg incubation through chick rearing. Tree swallows challenged with TSH showed no significant difference in thyroid hormone concentration or follicular epithelial cell height between exposure groups; however, a significantly greater proportion of chicks from reference sites were found to have thyroids with focal or diffuse hypertrophic epithelia relative to orchard chicks. In 2001, bluebirds from sprayed orchards had significantly higher T3 concentrations in response to TSH challenge; this response was positively correlated with the total number of pesticides applied during egg incubation through chick rearing.