Chronic stress increases adaptive immune response over six weeks in the house sparrow, Passer domesticus.

The vertebrate stress response enables an organism to shift energy towards activities that promote immediate survival when facing a threat to homeostasis, but it can also have detrimental effects on organismal health. Acute and chronic stressors generally have contrasting effects on immune responses, but the timeline of this transition between acute and chronic stressors and their effects on immune responses remains unclear. In this study, we investigate changes in immune markers in captive house sparrows (Passer domesticus) after exposure to normal laboratory conditions, an acute stressor, and chronic stressors for 42 days. Specifically, we examined changes in baseline and stress-induced corticosterone concentrations, body condition, heterophil/lymphocyte (H:L) ratio, hemolysis-hemagglutination, and wound healing. We found that individuals exposed to a single acute stressor had significantly higher stress-induced corticosterone concentrations 24 h after stressor exposure, however this effect was reversed after 48 h. Chronic stressor exposure resulted in generally stronger adaptive immune responses, demonstrated by higher baseline and stress-induced lysis, higher baseline hemagglutination, and slower wound healing. Within-trait correlations also increased with chronic stressor exposure, suggesting limitations on phenotypic plasticity. Most of the effects of chronic stressor exposure on immune markers strengthened over the 42 days of the experiment and differences between captivity-only and treatment groups were not apparent until approximately 20 days of chronic stressor exposure. These results highlight the importance of stressor duration in understanding the effects of chronic stressor exposure on immune responses.

Avian haemosporidians of breeding birds in the Davis Mountains sky-islands of west Texas, USA.

Avian haemosporidians are protozoan parasites transmitted by insect vectors that infect birds worldwide, negatively impacting avian fitness and survival. However, the majority of haemosporidian diversity remains undescribed. Quantifying this diversity is critical to determining parasite­host relationships and host-switching potentials of parasite lineages as climate change induces both host and vector range shifts. In this study, we conducted a community survey of avian haemosporidians found in breeding birds on the Davis Mountains sky islands in west Texas, USA. We determined parasite abundance and host associations and compared our results to data from nearby regions. A total of 265 birds were screened and infections were detected in 108 birds (40.8%). Most positive infections were identified as Haemoproteus (36.2%), followed by Plasmodium (6.8%) and Leucocytozoon (0.8%). A total of 71 haemosporidian lineages were detected of which 39 were previously undescribed. We found that regional similarity influenced shared lineages, as a higher number of lineages were shared with avian communities in the sky islands of New Mexico compared to south Texas, the Texas Gulf Coast and central Mexico. We found that migratory status of avian host did not influence parasite prevalence, but that host phylogeny is likely an important driver.

Post-natal corticosterone exposure downregulates the HPA axis through adulthood in a common passerine.

The hypothalamic-pituitaryadrenal (HPA) axis is one of the most important physiological mechanisms for mediating life-history trade-offs by reallocating resources to immediate survival from other life-history components during a perturbation. Early-life stressor experience and associated upregulation of glucocorticoids can induce short- and long-term changes to the HPA axis in ways that may optimize survival and/or reproduction for the expected adult environment. Although short-term changes to the HPA axis following perinatal stress are well documented, we know less about the long-term effects of early-life stress especially for non-mammalian wild species. Here, we determined long-term effects of experimental post-natal increases in a circulating glucocorticoid on the HPA axis in a common passerine bird, the house sparrow (Passer domesticus). We manipulated circulating corticosterone in wild, free-living nestlings, transferred fledglings to captivity and assessed corticosterone response to a standardized capture-restraint protocol at the pre-fledging, juvenile, and adult stages. Early-life corticosterone manipulation was associated with depressed baseline and stress-induced concentrations of corticosterone at all stages of life, through adulthood. These results provide rare evidence for the effects of early-life stressor experiences through adulthood, with important implications for understanding developmental programming of an endocrine mediator of life history trade-offs.

Slowing down the metabolic engine: impact of early-life corticosterone exposure on adult metabolism in house sparrows (Passer domesticus).

Whole-organism metabolism is an integrative process that determines not only the energy cost of living but also the energy output that is available for behavioral and physiological processes during the life cycle. Developmental challenge is known to affect growth, development of several organs, and several physiological mechanisms (such as HPA responsiveness, oxidative stress or immunity), which may altogether affect adult metabolism. All of these developmental effects are likely to be mediated by glucocorticoids, but the impact of developmental glucocorticoid exposure on adult metabolism has rarely been studied and the results are equivocal. In this study, we examined the impact of developmental exposure to corticosterone (CORT, the main avian glucocorticoid hormone) on resting metabolic rate (RMR, measured in thermoneutrality, 25°C) and thermoregulatory metabolic rate (TMR, measured in cold challenge conditions, 5°C) in the house sparrow. Following experimental administration of CORT at the nestling stage, house sparrows were kept in captivity until adulthood, when their metabolism was measured. We found that post-natal CORT exposure decreased both RMR and TMR in adult sparrows. This CORT-mediated reduction of metabolism was also associated with a reduced overnight body mass loss. Therefore, our results suggest that developmental CORT exposure can orient the phenotype towards an energy-saving strategy, which may be beneficial in a constraining environmental context.

Post-natal glucocorticoid elevation affects GnRH-induced luteinizing hormone concentration in female house sparrows.

Most non-mammalian studies investigating the long-term effects of early-life stressor exposure on endocrine regulation have focused on the hypothalamic-pituitaryadrenal (HPA) axis. However, the hypothalamic-pituitary-gonadal (HPG) axis may more directly affect fitness by regulating reproduction. Changes in HPG axis regulation could allow vertebrates to adaptively mitigate negative effects of early-life stressor exposure. However, only a few studies have examined long-term effects of early-life stressor experience on the HPG axis, and these have found mixed results. Here, we evaluate long-term effects of post-natal corticosterone exposure on the HPG axis in adult female house sparrows (Passer domesticus). We elevated circulating corticosterone non-invasively in wild nestling house sparrows between 8 and 11 days post-hatching, and then brought birds into captivity at fledging. Early in their first breeding season (ages 285-353d post-hatching), females were given a gonadotropin releasing hormone (GnRH) challenge. We found that early-life corticosterone exposure interacted with current condition such that females exposed to elevated post-natal corticosterone had higher baseline and GnRH-induced luteinizing hormone (LH) concentration than control females, but only if they had a high mass. Our results suggest that female house sparrows may mitigate negative impacts of early-life corticosterone exposure by investing in early reproduction, but only when current energetic condition allows.

Post-natal corticosterone exposure affects ornaments in adult male house sparrows (Passer domesticus).

In vertebrates, the ontogeny of several crucial organismal systems is known to occur early in life. Developmental conditions can ultimately have important consequences on adult fitness by affecting individual phenotype. These developmental effects are thought to be primarily mediated by endocrine systems, and especially by glucocorticoids. In this study, we tested how post-natal exposure to corticosterone (the primary avian glucocorticoid) may subsequently affect the expression of ornaments in adult male house sparrows (Passer domesticus). Specifically, we investigated the long-term consequences of this manipulation on the size and color of several visual signals: badge, wing bar, tarsus and beak. Post-natal corticosterone exposure had a strong negative impact on the size, but not the color, of some male ornaments (badge and wing bar surface area). Because wing bar and badge surface area are used as sexual and/or hierarchical signals in house sparrow, we showed that early life stress can affect some aspect of attractiveness and social status in this species with potentially important fitness consequences (e.g. sexual selection and reproductive performance). Future studies need now to explore the costs and benefits of this developmental plasticity for individuals (i.e. fitness).

Early-life maltreatment predicts adult stress response in a long-lived wild bird.

Persistent phenotypic changes due to early-life stressors are widely acknowledged, but their relevance for wild, free-living animals is poorly understood. We evaluated effects of two natural stressors experienced when young (maltreatment by adults and nutritional stress) on stress physiology in wild Nazca boobies (Sula granti) 6-8 years later, an exceptionally long interval for such studies. Maltreatment as a nestling, but not nutritional stress, was associated years later with depressed baseline corticosterone in females and elevated stress-induced corticosterone concentration [CORT] in males. These results provide rare evidence of long-term hormonal effects of natural early-life stress, which may be adaptive mechanisms for dealing with future stressors.

House sparrows mitigate growth effects of post-natal glucocorticoid exposure at the expense of longevity.

Acute, short-term effects of early-life stress and associated glucocorticoid upregulation on physiology and survival are widely documented across vertebrates. However, the persistence and severity of these effects are largely unknown, especially through the adult stage and for natural systems. Here, we investigate physiological, morphological, and survival effects of post-natal glucocorticoid upregulation across the nestling, juvenile, and adult life stages in house sparrows (Passer domesticus). We manipulate circulating corticosterone concentration in wild, free-living house sparrow nestlings and monitor body size, size-corrected mass, two measures of health (hematocrit and phytohemagglutinin-induced skin swelling), and survival in a captive environment until adulthood. We find that early-life corticosterone exposure depresses nestling size-corrected mass in both sexes, with no strong effect of the treatment on body size or our two measures of health. Birds are able to compensate for negative effects of high early-life corticosterone exposure in the long-term and this effect largely disappears by the juvenile and adult stages. However, treatment has a negative effect on survival through one year of age, suggesting that long-term compensation comes at a price.

No evidence for an effect of traffic noise on the development of the corticosterone stress response in an urban exploiter.

Anthropogenic noise can have important physiological and behavioral effects on wild animals. For example, urban noise could lead to a state of chronic stress and could alter the development of the hypothalamus-pituitary-adrenal (HPA) axis. Supporting this hypothesis, several studies have found that human disturbance is associated with increased circulating corticosterone (CORT) levels. However, it remains unclear whether increased CORT levels are the result of anthropogenic noise or other anthropogenic factors. Here, we experimentally tested the impact of urban noise on the CORT stress response in an urban exploiter (the house sparrow, Passer domesticus) by exposing chicks to a traffic noise ('disturbed chicks') or not ('control chicks'). If noise exposure has a negative impact on developing chicks, we predicted that (1) disturbed chicks will grow slower, will be in poorer condition, and will have a lower fledging probability than controls; (2) disturbed chicks will have higher baseline CORT levels than control; (3) the CORT stress response will be affected by this noise exposure. Contrary to these predictions, we found no effect of our experiment on growth, body condition, and fledging success, suggesting that house sparrow chicks were not negatively affected by this noise exposure. Moreover, we did not find any effect of noise exposure on either baseline CORT levels or the CORT stress response of chicks. This suggests not only that house sparrow chicks did not perceive this noise as stressful, but also that the development of the HPA axis was not affected by such noise exposure. Our study suggests that, contrary to urban avoiders, urban exploiters might be relatively insensitive to urban noise during their development. Further comparative studies are now needed to understand whether such insensitivity to anthropogenic noise is a consistent phenomenon in urban exploiters and whether this is a major requirement of an urban way of life.

Corticosterone stress response shows long-term repeatability and links to personality in free-living Nazca boobies.

The concept of "coping styles", or consistently different responses to stressors, is of broad interest in behavioral ecology and biomedicine. Two critical predictions of this concept are individual consistency of neurophysiological and behavioral responses (relative to population variability) and a negative relationship between aggression/proactivity and hypothalamic-pituitary-adrenal axis reactivity. Recent studies failed to provide strong support for these predictions, especially outside of strictly controlled conditions, and long-term measures to test the first prediction are rare. Here, we demonstrate individual repeatability across 2-3years of maximum circulating corticosterone concentration [CORT] and area under the [CORT] response curve (AUCI) during a standard capture-restraint test in wild, free-living adult Nazca boobies (Sula granti). We also show that the stress response predicts the personality traits aggression and anxiety in these birds (measured in the wild); however, the strength of these results was weak. Maximum [CORT] and AUCI showed higher repeatability between years than baseline [CORT]. After controlling breeding status, sex, mass, date sampled, and their interactions, baseline [CORT] was most closely related to personality traits, followed by AUCI, and then maximum [CORT]. The direction of these relationships depended on whether the testing context was social or non-social. [CORT] parameters had little to no relationship with cross-context plasticity in personality traits. Our results generally affirm two critical predictions of coping styles, but match the emerging trend that these relationships are weak in the wild, and may depend on testing context.

Global challenges in aging: insights from comparative biology and one health.

The well-being of wildlife populations, ecosystem health, and human health are interlinked, and preserving wildlife is crucial for sustaining healthy ecosystems. Wildlife numbers, and in particular avian populations, have steeply declined over the past century, associated with anthropogenic factors originating from industry, urbanization, changing land use, habitat loss, pollution, emerging diseases, and climate change. All these factors combine to exert increasing stress and impair health for both humans and wildlife, with diminished metabolic, immune, and reproductive function, deteriorating overall health, and reduced longevity. The "toxic aging coin" suggests that these stressors may have dual impacts on aging-they can accelerate the aging process, and older individuals may struggle to cope with pollutants compared to younger ones. These responses are reflected in the health and productivity of individuals, and at a larger scale, the health and ability of populations to withstand disturbances. To understand the potential risk to health over the lifespan, it is important to articulate some of these global challenges and consider both their impacts on aging populations and on the aging process. In this review, we use the toxic aging coin and One Health conceptual frameworks to examine the interconnected health of humans, wildlife, and ecosystems. This exploration aims to develop proactive approaches for optimizing wildlife and human health.

Local weather affects body condition of three North American songbird species on the Texas Coast.

Body condition is a frequently used physiological indicator of avian health and can be affected by an array of environmental variables. Although a number of studies have investigated the specific effects of individual weather variables on body condition in birds, few have analyzed the effects of both temperature and precipitation within the context of an extreme weather event such as hurricanes. In this study, we examined the relationship between breeding-season body condition and daily maximum temperature, daily minimum temperature, and monthly total precipitation for three passerine bird species at the Welder Wildlife Refuge near Rockport, Texas. We also evaluated yearly changes in body condition over a 12-year period for northern cardinals (Cardinalis cardinalis), painted buntings (Passerina ciris), and white-eyed vireos (Vireo griseus), focusing on the extreme precipitation event of Hurricane Harvey, which caused heavy localized flooding. We found that body condition declined with average daily minimum and maximum temperatures, while precipitation had varied, species-specific effects in the three species analyzed. Our results also suggest that northern cardinals experienced a notable reduction in average body condition in the 2 years following Hurricane Harvey. Taken together, we conclude that short-term precipitation and temperature drivers can be important correlates of body condition in songbirds and that severe weather events may reduce body condition in some bird species.

Hormonal effects of maltreatment in Nazca booby nestlings: implications for the "cycle of violence".

Non-breeding Nazca booby adults exhibit an unusual and intense social attraction to non-familial conspecific nestlings. Non-parental Adult Visitors (NAVs) seek out and approach unguarded nestlings during daylight hours and display parental, aggressive, and/or sexual behavior. In a striking parallel to the "cycle of violence" of human biology, degree of victimization as a nestling is strongly correlated with frequency of future maltreatment behavior exhibited as an adult. Here, we investigate candidates for permanent organization of this behavior, including immediate and long-term changes in growth and circulating corticosterone and testosterone due to victimization, by protecting some nestlings with portable exclosures that prevented NAV visits and comparing them to controls. During maltreatment episodes, nestlings experience an approximately five-fold increase in corticosterone concentration, and corticosterone remains elevated approximately 2.8-fold until at least the following morning. Our results are consistent with the possibility that repeated activation of the hypothalamic-pituitary-adrenal axis permanently organizes future adult maltreatment behavior. No effect on growth, acute or chronic changes in testosterone, or chronic corticosterone elevation was detected or appeared to be components of an organizational effect. This unusual behavior presents an opportunity to investigate neural, endocrine, and behavioral organization resulting from early social trauma that may be conserved across vertebrate classes.

Secondhand homes: The multilayered influence of woodpeckers as ecosystem engineers.

Ecosystem engineers alter, and can be influenced in turn by, the ecosystems they live in. Woodpeckers choose foraging and nesting sites based, in part, on food availability. Once abandoned, these cavities, particularly within areas of high forage, may be crucial to secondary cavity-nesting birds otherwise limited by cavities formed through decay. Our study examined factors that influence the nesting success of primary cavity nesters and the subsequent impact on secondary cavity-nesting birds. Using 5 years of point count data, we monitored the outcomes of cavity-nesting birds in South Texas. We used logistic-exposure models to predict daily survival rates based on cavity metrics and used woodpecker foraging trends and insect surveys to determine if nesting where woodpeckers actively forage benefits secondary cavity-nesting birds. Both woodpeckers and secondary cavity nesters shared predictors of daily survival; nests were more successful in cavities with small openings in minimally decayed trees. All secondary cavity nesters had higher probabilities of success when nesting in an abandoned woodpecker cavity, opposed to ones formed by decay. Woodpeckers tended to forage in areas with higher-than-average levels of the insect orders Coleoptera, Hymenoptera, and Orthoptera, and secondary cavity nesters had higher rates of success when nesting in these areas. Our results suggest abandoned woodpecker cavities may be constructed in a way that directly benefit secondary cavity nesters. Additionally, we suggest an interplay between these ecosystem engineers, food availability, and secondary cavity nesters: Woodpeckers engineer superior nesting cavities in areas where food is more abundant, and the resultant cavities in areas of high forage may benefit local secondary cavity nesters. Our findings indicate that there is still much to be explored in the role of ecosystem engineers, and how they influence local communities on multiple trophic levels.

Delayed effect of early-life corticosterone treatment on adult anti-predator behavior in a common passerine.

Acute, short-term effects of early-life stress and associated glucocorticoid upregulation on behavior are widely documented across vertebrates. However, the persistence and severity of these effects are largely unknown, especially through the adult stage and in wild species. Here, we investigate long-term effects of experimental post-natal increases in a circulating glucocorticoid on antipredator behavior in wild house sparrows (Passer domesticus) tested in captivity. We manipulate circulating corticosterone concentration in wild, free-living nestlings, transfer fledglings to captivity, and test juveniles and adults for two measures of antipredator behavior: evasiveness during a direct human encounter, and propensity to escape from a risky environment. We find no effect of early-life stress hormone manipulation on escape behavior, but a delayed effect on evasive behavior: evasive behavior was depressed in adults but not juveniles, and influenced by current body condition. These results highlight the importance of state-behavior interactions and life stage in assessing long-term effects of early-life stress, and provide rare evidence for delayed effects of early-life stress to adults of a wild avian species.

Yawning, acute stressors, and arousal reduction in Nazca booby adults and nestlings.

Yawning is a familiar and phylogenetically widespread phenomenon, but no consensus exists regarding its functional significance. We tested the hypothesis that yawning communicates to others a transition from a state of physiological and/or psychological arousal (for example, due to action of a stressor) to a more relaxed state. This arousal reduction hypothesis predicts little yawning during arousal and more yawning (above baseline) during and after down-regulation of arousal. Experimental capture-restraint tests with wild adult Nazca boobies (Sula granti), a seabird, increased yawning frequency after release from restraint, but yawning was almost absent during tests. Natural maltreatment by non-parental adults also increased yawning by nestlings, but only after the maltreatment ended and the adult left. CORT (corticosterone) was a logical a priori element of the stress response affecting the stressor-yawning relationship under the arousal reduction hypothesis, and cannot be excluded as such for adults in capture-restraint tests but is apparently unimportant for nestlings being maltreated by adults. The arousal reduction hypothesis unites formerly disparate results on yawning: its socially contagious nature in some taxa, its clear pharmacological connection to the stress response, and its temporal linkage to transitions in arousal between consciousness and sleep.