Perspectives on environmental heterogeneity and seasonal modulation of stress response in neotropical birds.

Corticosterone (CORT), the main glucocorticoid in birds, regulates physiological and behavioral traits linked to predictable and unpredictable environmental fluctuations (i.e., stressors). Baseline and stress-induced CORT concentrations are known to fluctuate seasonally, linked to life history stages (LHS) such as breeding, molt, and wintering stage. These variations have been relatively well described in North American birds, but poorly addressed in neotropical species. To fill this gap, we explored how baseline and stress-induced CORT variation by LHS was affected by seasonality and environmental heterogeneity (i.e., frequency of unpredictable events such as droughts, flashfloods, etc) within the Neotropics using two approaches. First, we reviewed all currently available data about CORT concentrations for neotropical bird species. Second, we performed an in-depth analysis comparing the CORT responses of the two most common species of the Zonotrichia genus from North and South America (Z. leucophrys and Z. capensis, respectively) and their subspecies to seasonality and environmental heterogeneity. These species have been analyzed with the same methodology, allowing for an in-depth comparison of CORT variations. Despite scant data on neotropical bird species, we observed overlap between molt and breeding, and lower fluctuations of CORT among LHS. These patterns would be considered atypical compared to those described for North temperate species. Further, we found no significant associations between environmental heterogeneity and the stress-responses. In Zonotrichia we observed a positive association between baseline and stress-induced concentrations of CORT and latitude. We also observed differences by LHS. Both baseline and stress-induced CORT concentrations were higher during breeding and lower during molt. In addition, for both species, the overall pattern of seasonal modulation of stress response was heavily influenced by the migration strategy, with long-distance migrants showing significantly higher stress-induced CORT levels. Our results highlight the need for more data collection in the Neotropics. Comparative data would shed further light on the sensitivity of the adrenocortical response to stress under different scenarios of environmental seasonality and unpredictability.

On the relationship between baseline corticosterone levels and annual survival of the thorn-tailed rayadito.

Baseline concentrations of glucocorticoids (i.e., cortisol and/or corticosterone) can moderately increase with the degree of energy demands that an individual faces. This could be a mechanism based on which glucocorticods (GCs) can mediate life history trade-offs, and therefore fitness. The 'cort-fitness hypothesis' predicts a negative relationship between GCs and fitness, meanwhile the 'cort-adaptation hypothesis' predicts the opposite pattern. Field studies on the relation between baseline GCs and survival rate have shown mixed results, supporting both positive and negative effect. These ambiguous results could be partially consequence of the short time frame in that most of the studies are carried on. In this study, we tested the predictions of the 'cort-fitness hypothesis' and 'cort-adaptation hypothesis' by using long-term data (eight-year of capture-mark-recapture) of Thorn-tailed Rayadito (Aphrastura spinicauda) in two populations at different latitudes. We assessed whether survival varied as a function of Cort levels and whether it varied in a linear (positive: 'cort-adaptation hypothesis' or negative: 'cort-fitness hypothesis') or curvilinear way. The two populations in our study had different baseline Cort levels, then we evaluated whether the association between baseline Cort and survival probability varied between them. In the high latitude population (i.e., lower baseline Cort levels), we observed a marginally quadratic relationship that is consistent with the cort-fitness hypothesis. In contrast, in the low altitude population we did not find this relation. Our findings suggests that the association between baseline Cort and survival probability is context-dependent, and highlights the importance of comparing different populations and the use of long-term data.

Social group signatures in hummingbird displays provide evidence of co-occurrence of vocal and visual learning.

Vocal learning, in which animals modify their vocalizations based on social experience, has evolved in several lineages of mammals and birds, including humans. Despite much attention, the question of how this key cognitive trait has evolved remains unanswered. The motor theory for the origin of vocal learning posits that neural centres specialized for vocal learning arose from adjacent areas in the brain devoted to general motor learning. One prediction of this hypothesis is that visual displays that rely on complex motor patterns may also be learned in taxa with vocal learning. While learning of both spoken and gestural languages is well documented in humans, the occurrence of learned visual displays has rarely been examined in non-human animals. We tested for geographical variation consistent with learning of visual displays in long-billed hermits ( Phaethornis longirostris), a lek-mating hummingbird that, like humans, has both learned vocalizations and elaborate visual displays. We found lek-level signatures in both vocal parameters and visual display features, including display element proportions, sequence syntax and fine-scale parameters of elements. This variation was not associated with genetic differentiation between leks. In the absence of genetic differences, geographical variation in vocal signals at small scales is most parsimoniously attributed to learning, suggesting a significant role of social learning in visual display ontogeny. The co-occurrence of learning in vocal and visual displays would be consistent with a parallel evolution of these two signal modalities in this species.

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.

Contrasting seasonal and aseasonal environments across stages of the annual cycle in the rufous-collared sparrow, Zonotrichia capensis: Differences in endocrine function, proteome and body condition.

The timing and duration of life-history stages (LHSs) within the annual cycle can be affected by local environmental cues which are integrated through endocrine signalling mechanisms and changes in protein function. Most animals express a single LHS within a given period of the year because synchronous expression of LHSs is thought to be too costly energetically. However, in very rare and extremely stable conditions, breeding and moult have been observed to overlap extensively in rufous-collared sparrows (Zonotrichia capensis) living in valleys of the Atacama Desert-one of the most stable and aseasonal environments on Earth. To examine how LHS traits at different levels of organization are affected by environmental variability, we compared the temporal organization and duration of LHSs in populations in the Atacama Desert with those in the semiarid Fray Jorge National Park in the north of Chile-an extremely seasonal climate but with unpredictable droughts and heavy rainy seasons. We studied the effects of environmental variability on morphological variables related to body condition, endocrine traits and proteome. Birds living in the seasonal environment had a strict temporal division of LHSs, while birds living in the aseasonal environment failed to maintain a temporal division of LHSs resulting in direct overlap of breeding and moult. Further, higher circulating glucocorticoids and androgen concentrations were found in birds from seasonal compared to aseasonal populations. Despite these differences, body condition variables and protein expression were not related to the degree of seasonality but rather showed a strong relationship with hormone levels. These results suggest that animals adjust to their environment through changes in behavioural and endocrine traits and may be limited by less labile traits such as morphological variables or expression of specific proteins under certain circumstances. These data on free-living birds shed light on how different levels of life-history organization within an individual are linked to increasing environmental heterogeneity.

How birds cope physiologically and behaviourally with extreme climatic events.

As global climate change progresses, the occurrence of potentially disruptive climatic events such as storms are increasing in frequency, duration and intensity resulting in higher mortality and reduced reproductive success. What constitutes an extreme climatic event? First we point out that extreme climatic events in biological contexts can occur in any environment. Focusing on field and laboratory data on wild birds we propose a mechanistic approach to defining and investigating what extreme climatic events are and how animals cope with them at physiological and behavioural levels. The life cycle of birds is made up of life-history stages such as migration, breeding and moult that evolved to match a range of environmental conditions an individual might expect during the year. When environmental conditions deteriorate and deviate from the expected range then the individual must trigger coping mechanisms (emergency life-history stage) that will disrupt the temporal progression of life-history stages, but enhance survival. Using the framework of allostasis, we argue that an extreme climatic event in biological contexts can be defined as when the cumulative resources available to an individual are exceeded by the sum of its energetic costs-a state called allostatic overload. This allostatic overload triggers the emergency life-history stage that temporarily allows the individual to cease regular activities in an attempt to survive extreme conditions. We propose that glucocorticoid hormones play a major role in orchestrating coping mechanisms and are critical for enduring extreme climatic events.This article is part of the themed issue 'Behavioural, ecological and evolutionary responses to extreme climatic events'.

Does Environmental Heterogeneity Promote Cognitive Abilities?

In the context of global change the possible loss of biodiversity has been identified as a major concern. Biodiversity could be seriously threatened as a direct consequence of changes in availability of food, changing thermal conditions, and loss and fragmentation of habitat. Considering the magnitude of global change, an understanding of the mechanisms involved in coping with a changing environment is urgent. We explore the hypothesis that species and individuals experiencing highly variable environments are more likely to develop a wider range of responses to handle the different and unpredictable conditions imposed by global change. In the case of vertebrates, the responses to the challenges imposed by unpredictable perturbations ultimately are linked to cognitive abilities allowing the solving of problems, and the maximization of energy intake. Our models were hummingbirds, which offer a particularly compelling group in which to examine the functional and mechanistic links between behavioral and energetic strategies in individuals experiencing different degrees of social and environmental heterogeneity.

A blurring of life-history lines: Immune function, molt and reproduction in a highly stable environment.

Rufous-collared sparrows (Zonotrichia capensis peruviensis) from valleys in the Atacama Desert of Chile, live in an extremely stable environment, and exhibit overlap in molt and reproduction, with valley-specific differences in the proportion of birds engaged in both. To better understand the mechanistic pathways underlying the timing of life-history transitions, we examined the relationships among baseline and stress-induced levels of corticosterone (CORT), testosterone, and bacteria-killing ability of the blood plasma (BKA), as well as haemosporidian parasite infections and the genetic structure of two groups of sparrows from separate valleys over the course of a year. Birds neither molting nor breeding had the lowest BKA, but there were no differences among the other three categories of molt-reproductive stage. BKA varied over the year, with birds in May/June exhibiting significantly lower levels of BKA than the rest of the year. We also documented differences in the direction of the relationship between CORT and BKA at different times during the year. The direction of these relationships coincides with some trends in molt and reproductive stage, but differs enough to indicate that these birds exhibit individual-level plasticity, or population-level variability, in coordinating hypothalamo-pituitary-adrenal axis activity with life-history stage. We found weak preliminary evidence for genetic differentiation between the two populations, but not enough to indicate genetic isolation. No birds were infected with haemosporidia, which may be indicative of reduced parasite pressure in deserts. The data suggest that these birds may not trade off among different life-history components, but rather are able to invest in multiple life-history components based on their condition.

Epaulet size and current condition in red-winged blackbirds: examining a semistatic signal, testosterone, immune function, and parasites.

Some sexually selected signals are thought to convey information about the current condition and genetic/epigenetic quality of the individual signaling, including the ability to resist parasites. However, it is unclear whether semistatic sexual signals that develop periodically and remain stable over protracted periods, such as avian breeding plumage, can relate to measures of current condition and health. We examined a semistatic signal (wing epaulet size) in male red-winged blackbirds (Agelaius phoeniceus) during the breeding season and looked for relationships between this trait and circulating testosterone (T), hematocrit, bacteria-killing ability (BKA) of the blood, and the infection status, richness, and abundance of four functional categories of parasite. We found that epaulet size was positively related to circulating levels of T and ectoparasite infections. We found no relationships between T and parasite infections. In adult males there was a negative relationship between T and BKA, whereas in yearling males there was no relationship. We found no evidence for a general reduction in immunocompetence in males with larger epaulets but rather an increase in susceptibility to specific types of parasites. Our results suggest that semistatic signals can be linked to measures of current condition, and we postulate that these relationships are modulated via activity levels related to breeding-season activities.

Cognitive ecology in hummingbirds: the role of sexual dimorphism and its anatomical correlates on memory.

In scatter-hoarding species, several behavioral and neuroanatomical adaptations allow them to store and retrieve thousands of food items per year. Nectarivorous animals face a similar scenario having to remember quality, location and replenishment schedules of several nectar sources. In the green-backed firecrown hummingbird (Sephanoides sephanoides), males are territorial and have the ability to accurately keep track of nectar characteristics of their defended food sources. In contrast, females display an opportunistic strategy, performing rapid intrusions into males territories. In response, males behave aggressively during the non-reproductive season. In addition, females have higher energetic demands due to higher thermoregulatory costs and travel times. The natural scenario of this species led us to compared cognitive abilities and hippocampal size between males and females. Males were able to remember nectar location and renewal rates significantly better than females. However, the hippocampal formation was significantly larger in females than males. We discuss these findings in terms of sexually dimorphic use of spatial resources and variable patterns of brain dimorphisms in birds.

Baseline corticosterone and stress response in the Thorn-tailed Rayadito (Aphrastura spinicauda) along a latitudinal gradient.

Glucocorticoids are essential for life and their secretion is regulated by the hypothalamic-pituitary-adrenal axis (HPA). The HPA axis is often divided into two components: baseline glucocorticoids levels and stress response glucocorticoids levels, which are affected by changes in ambient temperature and productivity among others factors. An approximation to evaluate how a species copes with these changes is to evaluate differences of this hormone amongst populations of the same species that inhabit places ideally presenting all the possible combinations of temperature and productivity. We aimed to evaluate whether environmental temperature or productivity, represent challenges in terms of stress in the Thorn-tailed Rayadito (Aphrastura spinicauda). We examined circulating baseline levels of CORT and stress responses from three populations, covering the whole geographic distribution of the species across large gradients in weather conditions. If low temperature influences baseline CORT levels, we expect higher levels of this hormone in the southernmost population (higher latitude). However, if productivity is the factor that influences baseline CORT levels, we expect the contrary pattern, that is, lower values of this hormone in the southernmost population (more productive environment). We observed that baseline CORT levels presented lower values in the southernmost population, supporting the environmental productivity hypothesis. Secondly, we tested the hypothesis that individuals breeding at higher latitudes should have a lower stress response than individuals breeding at lower latitudes. Contrary to our expectations, we found that stress response did not vary among populations in any of the three years. We concluded that low environmental temperatures did not represent a stress situation for the Thorn-tailed Rayadito if food abundance was sufficient to support energetic demands.

The impact of exposure to a novel female on symptoms of infection and on the reproductive axis.

BACKGROUND/AIM: Sickness behaviors are the behavioral alterations animals exhibit during the course of an infection, often accompanied by reduced reproductive activity. Adopting sickness behaviors may aid in overcoming the infection, by diverting energy from routine activities towards enhancement of the immune system. Nonetheless, sickness behaviors are plastic, being influenced by specific environmental and social circumstances. Here, we tested whether the presentation of a novel female to males suffering from a simulated infection could impact the behavioral effects of sickness, the reproductive axis, or both. METHODS: Male zebra finches were housed in isolation and injected intramuscularly with lipopolysaccharide or saline. Behaviors were recorded before (3 h before injection) and after (3.5 h after injection) addition of a novel female to the cage for 30 min. Four hours after injection, we collected the brain and testis for the analysis of important reproductive axis modulators, gonadotropin-releasing hormone, and gonadotropin-inhibitory hormone, and to quantify gene expression of a proinflammatory cytokine involved in the regulation of sickness behaviors [interleukin (IL)-1ß]. Testosterone was quantified in the plasma. RESULTS: The presence of a novel female diminished sickness behaviors and induced alterations in the reproductive axis within 30 min, with no associated changes in brain gene expression of IL-1ß. Social environment itself altered brain gene expression of IL-1ß. CONCLUSIONS: Male zebra finches prioritize the opportunity to mate versus investment in recovery from an infection, as determined by reduced expression of sickness behaviors when a potential mate was present. The behavioral effects of IL-1ß appear to be context dependent in this species.

Breaking down seasonality: androgen modulation and stress response in a highly stable environment.

Previous studies show that most birds inhabiting temperate regions have well defined life history stages, and they modulate the production of testosterone (T) and corticosterone (CORT) in response to changes in seasonality. In this study we aimed to examine baseline and stress-induced levels of CORT and circulating T in relation with life history stages in the rufous-collared sparrow, Zonotrichia capensis. We carried out this study for a year in a population inhabiting riparian habitats in the Atacama Desert in Chile, one of the most climatically stable and driest places in the world. This environment shows minimal yearly change in average temperature and precipitation is virtually zero. We found individuals breeding, molting and overlapping breeding and molt year round, although most individuals were molting during March and in breeding condition during October. T levels were not related to individual breeding condition, and at population level they were not significantly different across sampling months. Baseline levels of CORT did not vary across the year. Stress-induced levels of CORT were suppressed during March when most of the birds were molting. This phenomenon was also observed in birds not molting during this period suggesting a mechanism other than molt in determining the stress-response suppression. Our results strongly suggest that in this study site, long-term extremely stable conditions could have relaxed the selective pressures over the timing of life history stages which was evidenced by the breeding and molt schedules, its overlap and endocrine profiles.

Strengthened insectivory in a temperate fragmented forest.

Habitat fragmentation modifies ecological patterns and processes through changes in species richness and abundance. In the coastal Maulino forest, central Chile, both species richness and abundance of insectivorous birds increases in forest fragments compared to continuous forest. Through a field experiment, we examined larvae predation in fragmented forests. Higher richness and abundance of birds foraging at forest fragments translated into more insect larvae preyed upon in forest fragments than in continuous forest. The assessed level of insectivory in forest fragments agrees with lower herbivory levels in forest fragments. This pattern strongly suggests the strengthening of food interactions web in forest fragments of coastal Maulino forest.