Jesse S. Krause

RNA interference of gonadotropin-inhibitory hormone gene induces arousal in songbirds

Gonadotropin-inhibitory hormone (GnIH) was originally identified in quail as a hypothalamic neuropeptide inhibitor of pituitary gonadotropin synthesis and release. However, GnIH neuronal fibers do not only terminate in the median eminence to control anterior pituitary function but also extend widely in the brain, suggesting it has multiple roles in the regulation of behavior. To identify the role of GnIH neurons in the regulation of behavior, we investigated the effect of RNA interference (RNAi) of the GnIH gene on the behavior of white-crowned sparrows, a highly social songbird species. Administration of small interfering RNA against GnIH precursor mRNA into the third ventricle of male and female birds reduced resting time, spontaneous production of complex vocalizations, and stimulated brief agonistic vocalizations. GnIH RNAi further enhanced song production of short duration in male birds when they were challenged by playbacks of novel male songs. These behaviors resembled those of breeding birds during territorial defense. The overall results suggest that GnIH gene silencing induces arousal. In addition, the activities of male and female birds were negatively correlated with GnIH mRNA expression in the paraventricular nucleus. Density of GnIH neuronal fibers in the ventral tegmental area was decreased by GnIH RNAi treatment in female birds, and the number of gonadotropin-releasing hormone neurons that received close appositions of GnIH neuronal fiber terminals was negatively correlated with the activity of male birds. In summary, GnIH may decrease arousal level resulting in the inhibition of specific motivated behavior such as in reproductive contexts.

The relationship of telomere length to baseline corticosterone levels in nestlings of an altricial passerine bird in natural populations

BackgroundEnvironmental stressors increase the secretion of glucocorticoids that in turn can shorten telomeres via oxidative damage. Modification of telomere length, as a result of adversity faced early in life, can modify an individual’s phenotype. Studies in captivity have suggested a relationship between glucocorticoids and telomere length in developing individuals, however less is known about that relationship in natural populations.MethodsIn order to evaluate the effect of early environmental stressors on telomere length in natural populations, we compared baseline corticosterone (CORT) levels and telomere length in nestlings of the same age. We collected blood samples for hormone assay and telomere determination from two geographically distinct populations of the Thorn-tailed Rayadito (Aphrastura spinicauda) that differed in brood size; nestlings body mass and primary productivity. Within each population we used path analysis to evaluate the relationship between brood size, body mass, baseline CORT and telomere length.ResultsWithin each distinct population, path coefficients showed a positive relationship between brood size and baseline CORT and a strong and negative correlation between baseline CORT and telomere length. In general, nestlings that presented higher baseline CORT levels tended to present shorter telomeres. When comparing populations it was the low latitude population that presented higher levels of baseline CORT and shorter telomere length.ConclusionsTaken together our results reveal the importance of the condition experienced early in life in affecting telomere length, and the relevance of integrative studies carried out in natural conditions.

Decreases in Mineralocorticoid but not Glucocorticoid Receptor mRNA Expression During the Short Arctic Breeding Season in Free-Living Gambel's White-Crowned Sparrow (Zonotrichia leucophrys gambelii)

The acute stress response in vertebrates is a highly adaptive suite of physiological and behavioural mechanisms that promote survival in the face of deleterious stimuli from the environment. Facultative changes of physiology and behaviour are mediated through changes in circulating levels of glucocorticoids (corticosterone, cortisol) and their subsequent binding to the high‐affinity mineralocorticoid receptor (MR) or the low‐affinity glucocorticoid receptor (GR). Free‐living male wild Gambels white‐crowned sparrows (Zonotrichia leucophrys gambelii) display annual fluctuations in the stress response with marked attenuation during the transition from the pre‐parental to the parental stage. We investigated whether this rapid reduction in the stress response is mediated through changes in MR and GR mRNA expression in the brain using in situ hybridisation. MR mRNA expression was found to be significantly lower in the hippocampus as the male birds became parental. No changes were observed in GR mRNA expression in the paraventricular nucleus (PVN) or preoptic area (POA) at this time. No significant correlations were found between initial capture levels of corticosterone and GR or MR mRNA expression. No differences were found in basal levels of corticosterone between pre‐parental and parental in birds collected for in situ hybridisation. Stress response data revealed no difference at baseline but reductions in peak levels of corticosterone as birds became parental. These data suggest that changes in MR expression may be important for the regulation of the stress response or behavioural stress sensitivity with respect to promoting parental care and investment.

The stress response is attenuated during inclement weather in parental, but not in pre-parental, Lapland longspurs (Calcarius lapponicus) breeding in the Low Arctic

Birds breeding at high latitudes can be faced with extreme weather events throughout the breeding season. In response to environmental perturbations, vertebrates activate the hypothalamic-pituitary-adrenal (HPA) axis and synthesize corticosterone, which promotes changes in behavior and physiology to help the animal survive. The parental care hypothesis suggests that the HPA axis activity should be downregulated during the parental stage of breeding to prevent nest abandonment. However, it is unknown what happens to HPA axis activity in response to severe weather at the transition from the pre-parental to parental stages of breeding. We sampled baseline corticosterone levels and the time course of corticosterone elevation over 60min of restraint stress and assessed body condition and fat stores in Lapland longspurs (Calcarius lapponicus) breeding in the Low Arctic in the presence and absence of snowstorms. The results showed that during the pre-parental stage, HPA axis activity was up-regulated in response to snowstorms, with corticosterone levels continuing to increase through 60min of restraint. However, once birds were parental, HPA axis activity was unaffected by snowstorms and levels peaked at 10min. Fat levels and body condition did not change in response to snowstorms but fat levels declined in males during the pre-parental stage. These data suggest that the parental care hypothesis can be applied to severe storm events; parental birds restrained the activity of the HPA axis, likely to focus on the reproductive effort that is already underway, while pre-parental birds greatly upregulated HPA axis activity in response to snowstorms to maximize self-preservation.

A mechanistic approach to understanding range shifts in a changing world: What makes a pioneer?

Highlights • Many species are expanding or contracting their geographic distribution.• Range changes are caused by climate change, human disturbance and invasive species.• What are the characteristics of pioneers in new habitat?• Individuals at the leading edge appear to be highly variable.• In range expanding songbirds responses to stress are extremely variable.

The Effects of Acute Restraint Stress on Plasma Levels of Prolactin and Corticosterone across Life-History Stages in a Short-Lived Bird: Gambel’s White-Crowned Sparrow (Zonotrichia leucophrys gambelii)

The general reproductive effort model attempts to predict the resources that will be allocated to a current reproductive bout or to future survival by aborting the current reproductive attempt. Life-history theory predicts that short-lived species should devote more resources toward a reproductive event because brood value is far greater compared with that of long-lived species that have multiple breeding opportunities. Previous bird studies have used patterns of hormone secretion to understand the regulation of parental investment in response to environmental challenges, such as stress. The two key hormones investigated have been prolactin, which promotes parental investment, and corticosterone, which can reduce parental investment. Research on long-lived seabirds showed that prolactin levels decrease in response to a stressor, but the magnitude of the decline was positively correlated with future reproductive potential. However, little is known about the role of prolactin in short-lived species. Here we present prolactin and corticosterone data from a short-lived Arctic breeding, migratory songbird—the white-crowned sparrow, Zonotrichia leucophrys gambelii—at multiple stages of the breeding and nonbreeding seasons following standardized acute restraint stress. These data show that both prolactin and corticosterone are modulated seasonally. Corticosterone levels increased significantly in response to acute restraint stress during the breeding season in both sexes, but prolactin levels did not change in response to acute restraint stress at any stage of the annual cycle. We found no relationship between corticosterone or prolactin at either baseline or peak induced levels during any stage of breeding.

The effect of extreme spring weather on body condition and stress physiology in Lapland longspurs and white-crowned sparrows breeding in the Arctic.

Highlights • The spring of 2013 was extreme with record low temperatures and snow cover.• Arrival of migrant birds in Arctic was significantly delayed in 2013 compared to 3 other years.• Body condition was negatively affected in white-crowned sparrows and Lapland longspurs.• Stress physiology was increased in Lapland longspurs but not white-crowned sparrows.• Extreme events have the capacity to affect phenology, body condition and stress physiology.

Nestling growth rates in relation to food abundance and weather in the Arctic

ABSTRACT Raising nestlings to fledging is energetically demanding for songbirds, requiring parents to balance several major tradeoffs. Nestling growth rates are highly susceptible to variation in environmental conditions and parental investment, and highly variable environments with short breeding seasons such as the Arctic magnify these tradeoffs. Arctic-nesting passerines provide a good model system in which to explore variation within and between species in growth rates with regard to environmental conditions and the timing of clutch initiation. Here we investigated interannual and interspecies variation in nestling mass gain for 2 species of Arctic-breeding passerine, Gambels White-crowned Sparrow (Zonotrichia leucophrys gambelii) and Lapland Longspur (Calcarius lapponicus), across 2 years. The nestling period of 2014 was both colder (with lower minimum and maximum temperatures) and wetter (with 73% more rainfall) than 2013. Arthropod biomass was also reduced in shrub tundra in 2014 compared to 2013. Both species showed reductions in rate of daily mass gain of nestlings in 2014 compared to 2013, but we observed no significant difference between species. Furthermore, we found that in 2014 early nesting birds had higher rates of nestling growth than those initiating clutches later in the season. These findings suggest that overall environmental conditions were more challenging for raising nestlings in 2014 compared to 2013 and that these differences were manifested in a reduced rate of nestling mass gain in both species. Furthermore, both species showed a negative correlation between precipitation and growth rates, whereas only Lapland Longspur showed a positive correlation between growth rates and temperature.

Annual Hematocrit Profiles in Two Subspecies of White-Crowned Sparrow: A Migrant and a Resident Comparison

Hematocrit is an easily measured parameter that can be used to assess changes in oxygen carrying capacity necessitated by fluctuations in metabolic demands. Most hematocrit studies draw conclusions from changes in hematocrit that occur over a small sampling interval without an understanding of the variation that exists across the annual cycle. White-crowned sparrows provide an excellent model system due to the existence of a resident subspecies (Zonotrichia leucophrys nuttalli) that serves as a natural control for a migrant subspecies (Zonotrichia leucophrys gambelii). Comparing these two subspecies allows for the investigation of adaptive physiological changes at each life-history stage (i.e., migration, breeding, molt, etc.) in response to changing metabolic demands. Of particular interest, this subspecies comparison, by both calendar month and life-history stage, allows for the separation of adaptive increases in hematocrit due to migration from the natural seasonal variation in hematocrit. Hematocrit levels for males and females ranged throughout the year between 42%–47% and 40%–47% in the resident and between 45%–58% and 45%–56% in the migrant. In both subspecies, hematocrit levels were elevated during the breeding season compared to the nonbreeding season, and levels were reduced in females during egg laying. When grouped by life-history stage, hematocrit levels were always higher in the migrant compared to the resident. During the months in which migration occurred, hematocrit levels were 10%–12% higher in the migrant compared to the resident subspecies. These data suggest differential regulation of hematocrit between the two subspecies that may be attributed to phenotypic plasticity or genetic differences.

Changes in plasma concentrations of progesterone, dehydroepiandrosterone and corticosterone in response to acute stress of capture, handling and restraint in two subspecies of white-crowned sparrows.

The aim of this study was to determine circulating patterns of the three major adrenal steroids in blood in response to stress during acute restraint handling in two subspecies of white-crowned sparrow. Gambels white-crowned sparrows (Zonotrichia leucophrys gambelii) are long distance migrants that breed at high latitudes and Nuttalls white-crowned sparrows (Zonotrichia leucophrys nuttalli) are residents of coastal California. Column partition chromatography was developed to separate progesterone, dehydroepiandrosterone (DHEA), and corticosterone from a small plasma sample. Each of these steroids has the capability to modulate the stress response through various mechanisms. For example, progesterone is bound to corticosterone binding globulin (CBG) with a higher affinity than corticosterone. If plasma levels of progesterone rise during acute stress, then this could displace corticosterone from CBG and increase the amount of biologically active, free, corticosterone in blood. Dehydroepiandrosterone (DHEA) has been implicated to have many anti-stress properties with the potential to mitigate some of the actions of corticosterone. Results indicate that progesterone levels in both subspecies are elevated in response to acute stress handling. DHEA levels declined in Gambels but did not change in Nuttalls. Thus DHEA does not follow the same secretory pattern as in mammals. Corticosterone levels were elevated in response to acute stress handling in both subspecies. This study provides new insight into an integrated stress response among three steroids.