Tim S. Jessop

Stress, reproduction, and adrenocortical modulation in amphibians and reptiles

While the hypothalamo-pituitary-adrenocortical (HPA) response to stress appears to be conserved in vertebrates, the manner in which it is activated and its actions vary. We examine two trends in the stress biology literature that have been addressed in amphibian and reptilian species: (1). variable interactions among stress, corticosterone, and reproduction and (2). adrenocortical modulation. In the first topic we examine context-dependent interactions among stress, corticosterone, and reproduction. An increasing number of studies report positive associations between reproduction and corticosterone that contradict the generalization that stress inhibits reproduction. Moderately elevated levels of stress hormones appear to facilitate reproduction by mobilizing energy stores. In contrast, pronounced activation of the HPA axis and extremely elevated levels of stress hormones appear to inhibit reproduction. Much of these contrasting effects of stress and reproduction can be explained by expanding the Energetics-Hormone Vocalization Model, proposed for anuran calling behavior, to other taxa. In the second topic, a number of amphibians and reptiles modulate their HPA stress response. Adrenocortical modulation can occur at multiple levels and due to a variety of factors. However, we have little information as to the physiological basis for the variability. We suggest that several ecologically based ideas, such as variability in the length of the breeding season and lifetime reproductive opportunities, can be used to explain the utility of adrenocortical modulation in these taxa.

Life history and the ecology of stress: how do glucocorticoid hormones influence life‐history variation in animals?

Summary 1. Glucocorticoids hormones (GCs) are intuitively important for mediation of age-dependent vertebrate life-history transitions through their effects on ontogeny alongside underpinning variation in life-history traits and trade-offs in vertebrates. These concepts largely derive from the ability of GCs to alter energy allocation, physiology and behaviour that influences key life-history traits involving age-specific life-history transitions, reproduction and survival. 2. Studies across vertebrates have shown that the neuroendocrine stress axis plays a role in the developmental processes that lead up to age-specific early life-history transitions. While environmental sensitivity of the stress axis allows for it to modulate the timing of these transitions within species, little is known as to how variation in stress axis function has been adapted to produce interspecific variation in the timing of life-history transitions. 3. Our assessment of the literature confirms that of previous reviews that there is only equivocal evidence for correlative or direct functional relationships between GCs and variation in reproduction and survival. We conclude that the relationships between GCs and life-history traits are complex and general patterns cannot be easily discerned with current research approaches and experimental designs. 4. We identify several future research directions including: (i) integration of proximate and ultimate measures, including longitudinal studies that measure effects of GCs on more than one life-history trait or in multiple environmental contexts, to test explicit hypotheses about how GCs and life-history variation are related and (ii) the measurement of additional factors that modulate the effects of GCs on life-history traits (e.g. GC receptors and binding protein levels) to better infer neurendocrine stress axis actions. 5. Conceptual models of HPA/I axis actions, such as allostatic load and reactive scope, to some extent explicitly predict the role of GCs in a life-history context, but are descriptive in nature. We propose that GC effects on life-history transitions, survival probabilities and fecundity can be modelled in existing quantitative demographic frameworks to improve our understanding of how GC variation influences life-history evolution and GC-mediated effects on population dynamics

Modulation of the adrenocortical stress response in marine turtles (Cheloniidae): evidence for a hormonal tactic maximizing maternal reproductive investment

The relationships between reproductive condition, level of reproductive investment and adrenocortical modulation to capture stress in marine turtles form the basis of this study. When subjected to either capture or ecological stressors, nesting marine turtles have demonstrated adrenocortical responses that are both small in magnitude, and slow in responsiveness. These observations were further investigated to determine whether this minimal stress response was a physiological strategy to maximize reproductive investment in adult green Chelonia mydas and hawksbill Eretmochelys imbricata turtles. Female green and hawksbill turtles exhibited a decrease in adrenocortical responsiveness with progressive reproductive condition. Breeding turtles exhibited most suppression of their adrenocortical response to capture compared to both non-breeding and pre-breeding female counterparts. Nesting green turtles maintained a suppressed adrenocortical response to capture throughout the nesting season despite decreased reproductive investment. In contrast, male green and hawksbill turtles were less able to modulate their corticosterone (B) response to acute capture stress. During breeding, male turtles possessed significantly greater adrenocortical responses to capture than females. These results could indicate that the large reproductive investment necessary for female marine turtle reproduction might underlie the marked decrease in adrenocortical responsiveness. This hormonal mechanism could function as one strategy by which female marine turtles maximize their current reproductive event, even though under certain situations this mechanism could entail costs to female survival.

Limited effect of anthropogenic habitat fragmentation on molecular diversity in a rain forest skink, Gnypetoscincus queenslandiae.

To examine the effects of recent habitat fragmentation, we assayed genetic diversity in a rain forest endemic lizard, the prickly forest skink (Gnypetoscincus queenslandiae), from seven forest fragments and five sites in continuous forest on the Atherton tableland of northeastern Queensland, Australia. The rain forest in this region was fragmented by logging and clearing for dairy farms in the early 1900s and most forest fragments studied have been isolated for 50–80 years or nine to 12 skink generations. We genotyped 411 individuals at nine microsatellite DNA loci and found fewer alleles per locus in prickly forest skinks from small rain forest fragments and a lower ratio of allele number to allele size range in forest fragments than in continuous forest, indicative of a decrease in effective population size. In contrast, and as expected for populations with small neighbourhood sizes, neither heterozygosity nor variance in allele size differed between fragments and sites in continuous forests. Considering measures of among population differentiation, there was no increase in FST among fragments and a significant isolation by distance pattern was identified across all 12 sites. However, the relationship between genetic (FST) and geographical distance was significantly stronger for continuous forest sites than for fragments, consistent with disruption of gene flow among the latter. The observed changes in genetic diversity within and among populations are small, but in the direction predicted by the theory of genetic erosion in recently fragmented populations. The results also illustrate the inherent difficulty in detecting genetic consequences of recent habitat fragmentation, even in genetically variable species, and especially when effective population size and dispersal rates are low.

Interactions between Behavior and Plasma Steroids within the Scramble Mating System of the Promiscuous Green Turtle, Chelonia mydas

We measured plasma androgen (combined testosterone and 5alpha-dihydrotestosterone) (A) and corticosterone (B) in the promiscuous green turtle (Chelonia mydas) during courtship in the southern Great Barrier Reef. This study examined if reproductive behaviors and intermale aggression induced behavioral androgen and adrenocortical responses in reproductively active male and female green turtles. Associations between reproductive behavior and plasma steroids were investigated in green turtles across the population and within individuals. Levels across a range of both asocial and social behaviors were compared including (a) free swimming behavior; (b) initial courtship interactions; (c) mounted behavior (male and female turtles involved in copulatory activities); (d) intermale aggression (rival males that physically competed with another male turtle or mounted males recipient to these aggressive interactions); and (e) extensive courtship damage (male turtles that had accumulated excessive courtship damage from rival males). Behavioral androgen responses were detected in male turtles, in that plasma A was observed to increase with both attendant and mounted behavior. Male turtles who had been subjected to intermale aggression or who had accumulated severe courtship damage exhibited significantly lower plasma A than their respective controls. No pronounced adrenocortical response was observed after either intermale aggression or accumulation of extensive courtship damage. Female turtles exhibited a significant increase in plasma B during swimming versus mounted behavior, but no change in plasma A. We discuss our results in terms of how scramble polygamy might influence behavioral androgen interactions differently from more typical combative and territorial forms of male polygamy.

Interactions between ecology, demography, capture stress, and profiles of corticosterone and glucose in a free-living population of Australian freshwater crocodiles

In this study we examined three aspects pertaining to adrenocortical responsiveness in free-ranging Australian freshwater crocodiles (Crocodylus johnstoni). First, we examined the ability of freshwater crocodiles to produce corticosterone in response to a typical capture-stress protocol. A second objective addressed the relationship between capture stress, plasma glucose and corticosterone. Next we examined if variation in basal and capture-stress-induced levels of plasma corticosterone was linked to ecological or demographic factors for individuals in this free-ranging population. Blood samples obtained on three field trips were taken from a cross-sectional sample of the population. Crocodiles were bled once during four time categories at 0, 0.5, 6, and 10h post-capture. Plasma corticosterone increased significantly with time post-capture. Plasma glucose also significantly increased with duration of capture-stress and exhibited a positive and significant relationship with plasma corticosterone. Significant variation in basal or stress induced levels of corticosterone in crocodiles was not associated with any ecological or demographic factors including sex, age class or the year of capture that the crocodiles were sampled from. However, three immature males had basal levels of plasma corticosterone greater than 2 standard deviations above the mean. While crocodiles exhibited a pronounced adrenocortical and hyperglycaemic response to capture stress, limited variation in adrenocortical responsiveness due to ecological and demographic factors was not evident. This feature could arise in part because this population was sampled during a period of environmental benigness.

Interplay between age class, sex and stress response in green turtles (Chelonia mydas)

We investigated plasma hormone profiles of corticosterone in green turtles (Chelonia mydas) in response to a capture stress protocol. Further, we examined whether age class and sex were covariates associated with variation in both basal corticosterone levels and the adrenocortical stress response of non-breeding green turtles. Green turtles responded to the capture stress protocol by significantly increasing plasma levels of corticosterone over an eight-hour period. Further, there was a significant effect of age class on the capacity for green turtles to produce corticosterone in response to a capture stressor, with juvenile green turtles having higher basal levels of corticosterone and producing significantly more corticosterone in response to capture stress than non-breeding adult turtles. In contrast there was no significant sex difference in the corticosterone stress response of green turtles irrespective of age class. In summary, green turtles exhibited an adrenocortical response to a capture stress protocol. This response was significantly associated with different age classes, perhaps suggesting that the response is increased in juvenile turtles to offset the reduced probability of survival consistent with this more vulnerable age class.

A Method for Capturing Dugongs (Dugong dugon) in Open Water

We developed a method to rapidly and safely live capture wild dugongs based on the “rodeo method” employed to catch marine turtles. This method entails close pursuit of a dugong by boat until it is fatigued. The dugong is then caught around the peduncle region by a catcher leaping off the boat, and the dugong is restrained at the water surface by several people while data are collected. Our sampling protocol involves a short restraint time, typically < 5 min. No ropes or nets were attached to the dugong to avoid the risk of entanglement and subsequent drowning. This method is suitable for shallow, open-water captures when weather and water conditions are fair, and may be adapted for deeper waters.

Demographic and Phenotypic Effects of Human Mediated Trophic Subsidy on a Large Australian Lizard (Varanus varius): Meal Ticket or Last Supper?

Humans are increasingly subsidizing and altering natural food webs via changes to nutrient cycling and productivity. Where human trophic subsidies are concentrated and persistent within natural environments, their consumption could have complex consequences for wild animals through altering habitat preferences, phenotypes and fitness attributes that influence population dynamics. Human trophic subsidies conceptually create both costs and benefits for animals that receive increased calorific and altered nutritional inputs. Here, we evaluated the effects of a common terrestrial human trophic subsidies, human food refuse, on population and phenotypic (comprising morphological and physiological health indices) parameters of a large predatory lizard (∼2 m length), the lace monitor (Varanus varius), in southern Australia by comparison with individuals not receiving human trophic subsidies. At human trophic subsidies sites, lizards were significantly more abundant and their sex ratio highly male biased compared to control sites in natural forest. Human trophic subsidies recipient lizards were significantly longer, heavier and in much greater body condition. Blood parasites were significantly lower in human trophic subsidies lizards. Collectively, our results imply that human trophic subsidized sites were especially attractive to adult male lace monitors and had large phenotypic effects. However, we cannot rule out that the male-biased aggregations of large monitors at human trophic subsidized sites could lead to reductions in reproductive fitness, through mate competition and offspring survival, and through greater exposure of eggs and juveniles to predation. These possibilities could have negative population consequences. Aggregations of these large predators may also have flow on effects to surrounding food web dynamics through elevated predation levels. Given that flux of energy and nutrients into food webs is central to the regulation of populations and their communities, we advocate further studies of human trophic subsidies be undertaken to evaluate the potentially large ecological implications of this significant human environmental alteration.

Nocturnal Activity in the Green Sea Turtle Alters Daily Profiles of Melatonin and Corticosterone

In nature, green turtles (Chelonia mydas) can exhibit nocturnal activity in addition to their typically diurnal activity cycle. We examined whether nocturnal activity in captive and free-living green turtles altered daily plasma profiles of melatonin (MEL) and corticosterone (CORT). In captivity, diurnally active green turtles expressed distinct diel cycles in MEL and CORT; a nocturnal rise was observed in MEL and a diurnal rise was observed in CORT. However, when induced to perform both low- and high-intensity nocturnal activity, captive green turtles exhibited a significant decrease in MEL, compared to inactive controls. In contrast, plasma CORT increased significantly with nocturnal activity, and further, the relative increase in CORT was correlated with the intensity of the nocturnal behavior. In free-living green turtles that performed nocturnal activity including: nesting, mate searching, and feeding/swimming behaviors, plasma profiles in MEL and CORT exhibited relatively little, or no, daily fluctuation. Our findings demonstrate that nocturnal activity in green turtles is often associated with MEL and CORT profiles that resemble those measured during the day. We speculate that these conspicuous changes in MEL and CORT during nocturnal activity could either support or promote behaviors that enable acquisition of transient resources important to the survival and reproductive success of green turtles.