Glenn T. Crossin

Corticosterone Predicts Foraging Behavior and Parental Care in Macaroni Penguins

Corticosterone has received considerable attention as the principal hormonal mediator of allostasis or physiological stress in wild animals. More recently, it has also been implicated in the regulation of parental care in breeding birds, particularly with respect to individual variation in foraging behavior and provisioning effort. There is also evidence that prolactin can work either inversely or additively with corticosterone to achieve this. Here we test the hypothesis that endogenous corticosterone plays a key physiological role in the control of foraging behavior and parental care, using a combination of exogenous corticosterone treatment, time-depth telemetry, and physiological sampling of female macaroni penguins (Eudyptes chrysolophus) during the brood-guard period of chick rearing, while simultaneously monitoring patterns of prolactin secretion. Plasma corticosterone levels were significantly higher in females given exogenous implants relative to those receiving sham implants. Increased corticosterone levels were associated with significantly higher levels of foraging and diving activity and greater mass gain in implanted females. Elevated plasma corticosterone was also associated with an apparent fitness benefit in the form of increased chick mass. Plasma prolactin levels did not correlate with corticosterone levels at any time, nor was prolactin correlated with any measure of foraging behavior or parental care. Our results provide support for the corticosterone-adaptation hypothesis, which predicts that higher corticosterone levels support increased foraging activity and parental effort.

Pollution, habitat loss, fishing, and climate change as critical threats to penguins

Cumulative human impacts across the worlds oceans are considerable. We therefore examined a single model taxonomic group, the penguins (Spheniscidae), to explore how marine species and communities might be at risk of decline or extinction in the southern hemisphere. We sought to determine the most important threats to penguins and to suggest means to mitigate these threats. Our review has relevance to other taxonomic groups in the southern hemisphere and in northern latitudes, where human impacts are greater. Our review was based on an expert assessment and literature review of all 18 penguin species; 49 scientists contributed to the process. For each penguin species, we considered their range and distribution, population trends, and main anthropogenic threats over the past approximately 250 years. These threats were harvesting adults for oil, skin, and feathers and as bait for crab and rock lobster fisheries; harvesting of eggs; terrestrial habitat degradation; marine pollution; fisheries bycatch and resource competition; environmental variability and climate change; and toxic algal poisoning and disease. Habitat loss, pollution, and fishing, all factors humans can readily mitigate, remain the primary threats for penguin species. Their future resilience to further climate change impacts will almost certainly depend on addressing current threats to existing habitat degradation on land and at sea. We suggest protection of breeding habitat, linked to the designation of appropriately scaled marine reserves, including in the High Seas, will be critical for the future conservation of penguins. However, large-scale conservation zones are not always practical or politically feasible and other ecosystem-based management methods that include spatial zoning, bycatch mitigation, and robust harvest control must be developed to maintain marine biodiversity and ensure that ecosystem functioning is maintained across a variety of scales.

Glucocorticoid manipulations in free-living animals: considerations of dose delivery, life-history context and reproductive state

Summary 1. Experimental glucocorticoid (GC) manipulations can be useful for identifying the mechanisms that drive life-history and fitness variation in free-living animals, but predicting the effects of GC treatment can be complicated. Much of the uncertainty stems from the multifaceted role of GCs in organismal metabolism, and their variable influence with respect to life-history stage, ecological context, age, sex and individual variation. 2. Glucocorticoid hormones have been implicated in the regulation of parental care in many vertebrate taxa but in two seemingly contradictory ways, which sets up a potential GC-induced ‘reproductive conflict’. Circulating GCs mediate adaptive physiological and behavioural responses to stressful events, and elevated levels can lead to trade offs between reproductive effort and survival (e.g. the current reproduction vs. survival hypothesis). The majority of studies examining the fitness effects of GC manipulations extend from this hypothesis. However, when animals are not stressed (likely most of the time) baseline GCs act as key metabolic regulators of daily energy balance, homoeostasis, osmoregulation and food acquisition, with pleiotropic effects on locomotor activity or foraging behaviour. Slight increases in circulating baseline levels can then have positive effects on reproductive effort (e.g. the ‘cort’ fitness/adaptation hypotheses), but comparatively few GC manipulation studies have targeted these small, non-stress induced increases. 3. We review studies of GC manipulations and examine the specific hypotheses used to predict the effects of manipulations in wild, breeding vertebrates. We argue that given the dichotomous function of GCs the current ‘reproduction vs. survival’ paradigm is unnecessarily restrictive and predicts only deleterious GC effects on fitness. Therefore, a broader set of hypotheses should be considered when testing the fitness effects of GC manipulations. 4. When framing experimental manipulation studies, we urge researchers to consider three key points: life-history context (e.g. long vs. short lived, semelparous vs. iteroparous, etc.), ecological context and dose delivery.

Manipulating glucocorticoids in wild animals: basic and applied perspectives

Experimental elevations of glucocorticoids are used to understand how chronic exposure to stressors affects vertebrate performance. A variety of methods exist to exogenously manipulate glucocorticoids. Animal responses to glucocorticoid manipulations are variable within and among species. Incorporating glucocorticoid measures into conservation physiology should involve consideration of factors driving this variation.

Acoustic telemetry and fisheries management

This paper reviews the use of acoustic telemetry as a tool for addressing issues in fisheries management, and serves as the lead to the special Feature Issue of Ecological Applications titled Acoustic Telemetry and Fisheries Management. Specifically, we provide an overview of the ways in which acoustic telemetry can be used to inform issues central to the ecology, conservation, and management of exploited and/or imperiled fish species. Despite great strides in this area in recent years, there are comparatively few examples where data have been applied directly to influence fisheries management and policy. We review the literature on this issue, identify the strengths and weaknesses of work done to date, and highlight knowledge gaps and difficulties in applying empirical fish telemetry studies to fisheries policy and practice. We then highlight the key areas of management and policy addressed, as well as the challenges that needed to be overcome to do this. We conclude with a set of recommendations about how researchers can, in consultation with stock assessment scientists and managers, formulate testable scientific questions to address and design future studies to generate data that can be used in a meaningful way by fisheries management and conservation practitioners. We also urge the involvement of relevant stakeholders (managers, fishers, conservation societies, etc.) early on in the process (i.e., in the co-creation of research projects), so that all priority questions and issues can be addressed effectively.

Postmigratory Body Condition and Ovarian Steroid Production Predict Breeding Decisions by Female Gray-Headed Albatrosses

Carryover effects have been documented in many migratory bird species, but we know little about the physiological mechanisms that mediate those effects. Here we show that the energetic, endocrine, and aerobic characteristics of postmigratory female gray-headed albatrosses (Thalassarche chrysostoma) can affect their decision to breed. All females in this study, whether breeding or not, were secreting ovarian steroids when they arrived at the breeding colony at Bird Island, South Georgia, which suggests that all were responding to seasonal cues. However, deferring, nonbreeding birds were characterized by a steroid profile of high progesterone (P4) and low testosterone (T), whereas breeding birds showed the opposite pattern. Deferring birds also had low body mass, hematocrit, and hemoglobin. These results suggest that postmigratory condition can influence patterns of ovarian steroidogenesis and that the maintenance of high P4 without subsequent conversion to T favors breeding deferral. Whereas breeding females normally convert P4 to T, which is a key deterministic step toward 17β-estradiol synthesis, vitellogenesis, and follicle development, deferring females did not make this conversion and instead maintained high levels of P4, perhaps due to inhibition of the hydroxylase-lyase enzyme complex, thus rendering them infertile for the current season. Results are discussed within the context of the biennial breeding system of this species, and comparisons with other biennially and annually breeding albatrosses are made.

Physiological stress response, reflex impairment and delayed mortality of white sturgeon Acipenser transmontanus exposed to simulated fisheries stressors

Simulated angling stress caused a physiological disturbance and reflex impairment in sub-adult/adult white sturgeon. Ventilation was the first reflex to become compromised, followed by orientation, mouth extension, tail grab and body flex. Reflex impairment indicated a compromised physiological state which correlated with the degree of the stressor (i.e. severity). Higher reflex impairment scores correlated with longer recovery times. Compromised physiological state was significantly higher in summer than winter treated fish. Two mortalities occurred >24 hours after the cessation of the stressor during the summer. Both individuals had all reflexes impaired upon release into the recovery tank, excess stress metabolites (i.e. lactate), and were ‘unrecovered’ following the 30 min. observation period post-release.

Early Life-History Consequences of Growth- Hormone Transgenesis in Rainbow Trout Reared in Stream Ecosystem Mesocosms

There is persistent commercial interest in the use of growth modified fishes for shortening production cycles and increasing overall food production, but there is concern over the potential impact that transgenic fishes might have if ever released into nature. To explore the ecological consequences of transgenic fish, we performed two experiments in which the early growth and survival of growth-hormone transgenic rainbow trout (Oncorhynchus mykiss) were assessed in naturalized stream mesocosms that either contained predators or were predator-free. We paid special attention to the survival bottleneck that occurs during the early life-history of salmonids, and conducted experiments at two age classes (first-feeding fry and 60 days post-first-feeding) that lie on either side of the bottleneck. In the late summer, the first-feeding transgenic trout could not match the growth potential of their wild-type siblings when reared in a hydrodynamically complex and oligotrophic environment, irrespective of predation pressure. Furthermore, overall survival of transgenic fry was lower than in wild-type (transgenic = 30% without predators, 8% with predators; wild-type = 81% without predators, 31% with predators). In the experiment with 60-day old fry, we explored the effects of the transgene in different genetic backgrounds (wild versus domesticated). We found no difference in overwinter survival but significantly higher growth by transgenic trout, irrespective of genetic background. We conclude that the high mortality of GH-transgenic trout during first-feeding reflects an inability to sustain the basic metabolic requirements necessary for life in complex, stream environments. However, when older, GH-transgenic fish display a competitive advantage over wild-type fry, and show greater growth and equal survival as wild-type. These results demonstrate how developmental age and time of year can influence the response of genotypes to environmental conditions. We therefore urge caution when extrapolating the results of GH-transgenesis risk assessment studies across multiple life-history or developmental stages.

Migratory constraints on yolk precursors limit yolk androgen deposition and underlie a brood reduction strategy in rockhopper penguins.

Hormonally mediated maternal effects link maternal phenotype and environmental conditions to offspring phenotype. The production of lipid-rich maternal yolk precursors may provide a mechanism by which lipophilic steroid hormones can be transported to developing yolks, thus predicting a positive correlation between yolk precursors in mothers and androgen levels in eggs. Using rockhopper penguins (Eudyptes chrysocome), which produce a two-egg clutch characterized by extreme egg-size dimorphism, reversed hatching asynchrony and brood-reduction, we examined correlations between circulating concentrations of the primary yolk-precursor vitellogenin (VTG) and levels of yolk androgens. Previous work in Eudyptes penguins has shown that egg-size dimorphism is the product of migratory constraints on yolk precursor production. We predicted that if yolk precursors are constrained, androgen transport to developing yolks would be similarly constrained. We reveal positive linear relationships between maternal VTG and androgens in small A-eggs but not larger B-eggs, which is consistent with a migratory constraint operating on the A-egg. Results suggest that intra-clutch variation in total yolk androgen levels depends on the production and uptake of yolk precursors. The brood reduction strategy common to Eudyptes might thus be best described as the result of a migratory constraint.

Sources of diel variation in energetic physiology in an Arctic-breeding, diving seaduck

Diel variation in baseline glucocorticoid (GC) secretion influences energetics and foraging behaviors. In temperate breeding, diurnal vertebrates, studies have shown that daily patterns of baseline GC secretion are influenced by environmental photoperiod, with baseline GCs peaking prior to sunrise to stimulate waking and foraging behaviors. Measures of physiological energy acquisition are also expected to peak in response to foraging activity, but their relationship to GC levels have not been well studied. In contrast to temperate breeding species, virtually nothing is known about diel GC and energetic metabolite secretion in Arctic breeding species, which experience almost constant photoperiods in spring and summer. Using a ten-year dataset, we examined the daily, 24-h pattern of baseline corticosterone (CORT) and triglyceride (TRIG) secretion in approximately 800 female pre-breeding Arctic-nesting common eiders (Somateria mollissima). We related these traits to environmental photoperiod and to tidal cycle. In contrast to temperate breeding species, we found that that neither time of day nor tidal trend predicted diel variation in CORT or TRIG secretion in Arctic-breeding eiders. Given the narrow window of opportunity for breeding in polar regions, we suggest that eiders must decouple their daily foraging activity from light and tidal cycles if they are to accrue sufficient energy for successful breeding. As CORT is known to influence foraging behavior, the absence of a distinct diel pattern of CORT secretion may therefore be an adaptation to optimize reproductive investment and likelihood for success in some polar-breeding species.