Compensating for a stressful pregnancy? Glucocorticoid treatment during gravidity reduces metabolic rate in female fence lizards post-parturition.

Reproduction is a critical part of an animal's life history, but one which incurs significant costs to survival and future reproductive potential. These physiological consequences are likely to be influenced by context - for example, if an individual is subject to environmental stressors, physiological and behavioral changes associated with reproduction may be altered. Glucocorticoids, hormones produced as part of the physiological response to stressors, may alter how reproduction affects female physiology and behavior, and therefore the outcomes of reproductive trade-offs. Glucocorticoids prioritize immediate survival over reproduction, for example through changes in immune function, metabolic rate, and foraging, which may reduce energy expenditure or increase energy gain. However, we previously found that female eastern fence lizards (Sceloporus undulatus) experiencing elevated glucocorticoid levels during gestation were nevertheless able to maintain reproductive output and body condition. Here we investigate compensatory mechanisms by which eastern fence lizard females may maintain reproduction under experimental increases in a glucocorticoid, corticosterone (CORT). We found that, although CORT-treated females had similar immune function and behavior, they had reduced metabolic rates 3-5 days post-parturition compared to control females. Given that CORT-treated females spent a similar time basking and had equal food intake compared to control females, we suggest that the reduced metabolic rate is a mechanism by which CORT-treated females maintain their energy balance and reduce the energetic costs of gestation during periods of stress. This study suggests that physiological responses to reproduction may be context-dependent and could act to minimize costs of reproduction in situations where CORT is elevated (such as during periods of environmental stress).

Stress as a facilitator? Territorial male impala have higher glucocorticoid levels than bachelors.

Territoriality is a common behavioural adaptation, widespread among ungulates. Here, we tested the hypothesis that territorial individuals have higher glucocorticoid concentrations than non-territorial bachelors, in wild impala (Aepyceros melampus) in the Serengeti ecosystem. We also investigated how the relationship between territoriality and glucocorticoid levels is influenced by environmental context, specifically, food quality, population density (i.e., territory defence intensity), and herd size (i.e., mate defence effort). We collected 139 faecal samples over 4 years and analysed these for faecal glucocorticoid metabolites (FGMs). We used Normalised Difference Vegetation Index (NDVI) as a proxy for food quality, and population density was based on aerial surveys. Territorial males had, on average, higher FGM concentrations than bachelors. Increased food quality did not affect FGM levels in territorial males, but decreased FGM levels in bachelors by 78%. Greater population density increased FGM levels by 47%, but this effect was not different between territorial and bachelor males. Herd size did not affect FGM levels in territorial males. While elevated GC levels are often suggested to be repercussions of being territorial, our findings support the hypothesis that elevated GC levels may be beneficial and act as a facilitator of a male's reproductive potential. The elevated GC levels may increase the ability of territorial males to maintain a territory by increasing energy mobilisation and metabolic rate, ultimately increasing their reproductive fitness. Appreciating that long-term increases in GC levels are not simply costly but may have an adaptive, potentially facilitating role in an animal's life history is key to understanding HPA-axis reactivity and its potential in eco-physiological studies.

Survival and reproductive costs of repeated acute glucocorticoid elevations in a captive, wild animal.

Organisms are continuously encountering both predictable and unpredictable ecological stressors within their environment. The activation of the hypothalamic-pituitaryadrenal (stress) axis is a fundamental process allowing animals to cope with and respond to such encounters. A main consequence of HPA axis activation is the release of glucocorticoid hormones. Although short-term glucocorticoid elevations lead to changes in physiological and behavioral processes that are often adaptive, our understanding of fitness consequences of repeated acute elevations in glucocorticoid hormones over a longer time period is largely lacking. This is of particular current importance as animals are facing a significant increase in exposure to stressors including those associated with human-induced rapid environmental change. Here, we test fitness-relevant consequences of repeated exposure to glucocorticoids in the absence of natural challenges, by treating wild-caught gravid female eastern fence lizards (Sceloporus undulatus) with a daily transdermal dose of a glucocorticoid hormone until laying. This treatment causes an increase in plasma glucocorticoids that mimics the natural response lizards have when they encounter a stressor in the wild, without confounding effects associated with the encounter itself. This treatment reduced females' reproductive success (hatching success) and survival. Further, glucocorticoid-induced reductions in reproductive success were greater when females had experienced higher temperatures the previous winter. This demonstrates the potential significant consequences of repeated exposure to acute elevations in glucocorticoid hormones. Additionally, the costs of repeated glucocorticoid elevation may be further exaggerated by an individual's previous experience, such as the potential compounding effects of winter warming increasing animals' vulnerability to increased glucocorticoid levels during spring breeding.

Determining the adaptive potential of maternal stress.

Ecological and medical researchers are investing great effort to determine the role of Maternally-Derived Stress (MDS) as an inducer of phenotypic plasticity in offspring. Many researchers have interpreted phenotypic responses as unavoidable negative outcomes (e.g., small birth weight, high anxiety); however, a biased underestimate of the adaptive potential of MDS-induced effects is possible if they are not viewed within an ecologically relevant or a life-history optimization framework. We review the ecological and environmental drivers of MDS, how MDS signals are transferred to offspring, and what responses MDS induces. Results from four free-living vertebrate systems reveals that although MDS induces seemingly negative investment trade-offs in offspring, these phenotypic adjustments can be adaptive if they better match the offspring to future environments; however, responses can prove maladaptive if they unreliably predict (i.e., are mismatched to) future environments. Furthermore, MDS-induced adjustments that may prove maladaptive for individual offspring can still prove adaptive to mothers by reducing current reproductive investment, and benefitting lifetime reproductive success. We suggest that to properly determine the adaptive potential of MDS, researchers must take a broader integrated life-history perspective, appreciate both the immediate and longer term environmental context, and examine lifetime offspring and maternal fitness.

Consequences of climate-induced vegetation changes exceed those of human disturbance for wild impala in the Serengeti ecosystem.

In East Africa, climate change is predicted to reduce vegetation quality, and pervasive human disturbance has already resulted in significant declines in biodiversity. We studied the combined effects of reduced forage quality and human disturbance on faecal glucocorticoid metabolite (FGM) concentrations. We predicted that decreasing nutritional quality and increasing human disturbance would have an additive positive effect on FGM levels in wild impala (Aepyceros melampus). Employing a space-for-time approach, we used normalized difference vegetation index (NDVI) as a measure of forage quality, combined with spatially explicit proxies of human disturbance across areas of different protection management strategies in the Serengeti ecosystem. We collected 639 faecal samples, spread over 4 years, including both wet and dry seasons. Impala FGM levels increased significantly with declining NDVI and, to a lesser extent, with increasing proxies for human disturbance. However, we found no interaction between the two, such that impala had elevated FGM levels with low NDVI and low FGM levels with high NDVI regardless of human disturbance levels. This implies that impala will have high FGM levels if forage quality is poor, even with significant protection and reduced human disturbance. Understanding how animals respond to and cope with changes in forage quality and human land use across different protected areas is important for conservationists and managers to better protect species at risk and predict population viability.

Sex-dependent effects of maternal stress: Stressed moms invest less in sons than daughters.

Multigenerational effects can have important and sex-dependent effects on offspring. Sex allocation theory predicts that females should differentially invest in sons and daughters depending on sex-specific fitness returns and costs of investment. Maternal stress-relevant (glucocorticoid) hormones may be one mechanism driving this effect. We investigated how maternal stress hormones differentially affected sons and daughters by manipulating levels of the glucocorticoid, corticosterone (CORT), in gravid female eastern fence lizards (Sceloporus undulatus) and quantifying reproductive investment and sex ratio of resulting clutches, and the mass, snout-vent length, and body condition of sons versus daughters at hatching. We found no effect of maternal CORT-treatment on the number or size of eggs laid or on the sex ratio of resulting offspring, but sons of CORT-treated mothers were shorter, lighter, and of poorer body condition at hatching than were sons of control mothers. We found no difference in size or condition of daughters with maternal treatment. Our results suggest that maternal stress, mediated by elevations in maternal CORT concentrations, can have sex-specific effects on offspring manifesting as lower investment in sons.

Cardiovascular effects of angiotensin II in the rostral ventrolateral medulla: the push-pull hypothesis.

Neurons within the rostral ventrolateral medulla (RVLM) play a pivotal role in the tonic and phasic control of blood pressure. This region also contains a high density of angiotensin II type 1 (AT1) receptors. There is evidence that tonic activation of AT1 receptors in the RVLM contributes to an increased sympathetic vasomotor activity in some models of hypertension. At the same time, under certain conditions, activation of AT1 receptors in the RVLM can cause sympathoinhibition. In this review we argue that the effect of endogenous angiotensin II in the RVLM on sympathetic vasomotor activity depends upon the balance between tonic excitatory and inhibitory effects on sympathetic premotor neurons mediated by AT1 receptors within this region, and that this balance may be altered in different physiological or pathophysiological conditions.

Long-term regulation of arterial blood pressure by hypothalamic nuclei: some critical questions.

1. The long-term level of arterial pressure is dependent on the relationship between arterial pressure and the urinary output of salt and water, which, in turn, is affected by a number of factors, including renal sympathetic nerve activity (RSNA). In the present brief review, we consider the mechanisms within the brain that can influence RSNA, focusing particularly on hypothalamic mechanisms. 2. The paraventricular nucleus (PVN) in the hypothalamus has major direct and indirect connections with the sympathetic outflow and there is now considerable evidence that tonic activation of the PVN sympathetic pathway contributes to the sustained increased level of RSNA that occurs in conditions such as heart failure and neurogenic hypertension. The tonic activity of PVN sympathetic neurons, in turn, depends upon the balance of excitatory and inhibitory inputs. A number of neurotransmitters and neuromodulators are involved in these tonic excitatory and inhibitory effects, including glutamate, GABA, angiotensin II and nitric oxide. 3. The dorsomedial hypothalamic nucleus (DMH) also exerts a powerful influence over sympathetic activity, including RSNA, via synapses with sympathetic nuclei in the medulla and, possibly, also other brainstem regions. The DMH sympathetic pathway is an important component of the phasic sympathoexcitatory responses associated with acute stress, but there is no evidence that it is an important component of the central pathways that produce long-term changes in arterial pressure. Nevertheless, it is possible that repeated episodic activation of this pathway could lead to vascular hypertrophy and, thus, sustained changes in vascular resistance and arterial pressure. 4. Recent studies have reactivated the old debate concerning the possible role of the baroreceptor reflex in the long-term regulation of sympathetic activity. Therefore, central resetting of the baroreceptor-sympathetic reflex may be an important component of the mechanisms causing sustained changes in RSNA. However, little is known about the cellular mechanisms that could cause such resetting.