Effects of maternal cortisol treatment on offspring size, responses to stress, and anxiety-related behavior in wild largemouth bass (Micropterus salmoides).

Cortisol, the main glucocorticoid stress hormone in teleost fish, is of interest as a mediator of maternal stress on offspring characteristics because it plays an organizational role during early development. The present study tested the hypothesis that maternal exposure to cortisol treatment prior to spawn affects offspring phenotype using wild largemouth bass (Micropterus salmoides). Baseline and stress-induced cortisol concentrations, body size (i.e. length and mass), and behavior (i.e. anxiety, exploration, boldness, and aggression) were assessed at different offspring life-stages and compared between offspring of control and cortisol-treated females. Cortisol administration did not affect spawning success or timing, nor were whole-body cortisol concentrations different between embryos from cortisol-treated and control females. However, maternal cortisol treatment had significant effects on offspring stress responsiveness, mass, and behavior. Compared to offspring of control females, offspring of cortisol-treated females exhibited larger mass right after hatch, and young-of-the-year mounted an attenuated cortisol response to an acute stressor, and exhibited less thigmotaxic anxiety, exploratory behavior, boldness and aggression. Thus, offspring phenotype was affected by elevated maternal cortisol levels despite the absence of a significant increase in embryo cortisol concentrations, suggesting that a mechanism other than the direct deposition of cortisol into eggs mediates effects on offspring. The results of the present raise questions about the mechanisms through which maternal stress influences offspring behavior and physiology, as well as the impacts of such phenotypic changes on offspring fitness.

Manipulating glucocorticoids in wild animals: basic and applied perspectives.

One of the most comprehensively studied responses to stressors in vertebrates is the endogenous production and regulation of glucocorticoids (GCs). Extensive laboratory research using experimental elevation of GCs in model species is instrumental in learning about stressor-induced physiological and behavioural mechanisms; however, such studies fail to inform our understanding of ecological and evolutionary processes in the wild. We reviewed emerging research that has used GC manipulations in wild vertebrates to assess GC-mediated effects on survival, physiology, behaviour, reproduction and offspring quality. Within and across taxa, exogenous manipulation of GCs increased, decreased or had no effect on traits examined in the reviewed studies. The notable diversity in responses to GC manipulation could be associated with variation in experimental methods, inherent differences among species, morphs, sexes and age classes, and the ecological conditions in which responses were measured. In their current form, results from experimental studies may be applied to animal conservation on a case-by-case basis in contexts such as threshold-based management. We discuss ways to integrate mechanistic explanations for changes in animal abundance in altered environments with functional applications that inform conservation practitioners of which species and traits may be most responsive to environmental change or human disturbance. Experimental GC manipulation holds promise for determining mechanisms underlying fitness impairment and population declines. Future work in this area should examine multiple life-history traits, with consideration of individual variation and, most importantly, validation of GC manipulations within naturally occurring and physiologically relevant ranges.

Variation in anti-parasite behaviour and infection among larval amphibian species.

Along with immune defences, many animals exhibit effective anti-parasite behaviours such as parasite avoidance and removal that influence their susceptibility to infection. Host ecology and life history influence investment into comparatively fixed defences such as innate immunity but may affect the strength of anti-parasite behaviours as well. We investigated activity levels in five different species of larval amphibian with varying life histories and ecology in control, novel food stimulus, and trematode parasite (Echinoparyphium sp.) threat conditions. There was a significant interaction of species and treatment given that American toad (Bufo americanus), wood frog (Lithobates sylvaticus), and bullfrog (Lithobates catesbeianus) tadpoles generally increased their activity when parasite infectious stages were present while grey tree frogs (Hyla versicolor) and northern leopard frogs (Lithobates pipiens) did not, even though activity was negatively related to infection. In addition, there was considerable variation among species in their susceptibility to parasitism, with infection prevalence ranging from 17% in bullfrog tadpoles to 70% in wood frogs. However, amphibian life history (larval and adult traits) was not related to parasitism or level of anti-parasite behaviour at the species level. Consequently, we suggest that future investigations include more species with a range of life history traits and also consider host ecology, particularly if conspicuous anti-parasite behaviours are more likely in amphibian species that experience a relatively low risk of predation.

Agricultural effects on amphibian parasitism: importance of general habitat perturbations and parasite life cycles.

Agricultural activity can alter host-parasite interactions through associated contaminants and habitat perturbations. It is critical to determine whether agricultural effects are widespread or limited to specific types of agriculture. We examined influences of soybean agriculture on trematode parasitism of larval amphibians (grey tree frogs; Hyla versicolor) to assess the potential effects of a commonly applied pesticide (glyphosate) and landscape factors relative to previous field studies focusing on the herbicide atrazine. Overall, trematode parasite infection did not differ between soybean-adjacent and nonagricultural ponds (87.7% and 72.6% mean infection, respectively). However, host-generalist echinostome species were more common in tadpoles from soybean-associated ponds (86.3% mean infection versus 36.2% in nonagricultural ponds) as well as sites with large or short average distances to forest cover and roads, respectively. In contrast, the occurrence of a host-specialist (Alaria sp.) group was greater in nonagricultural ponds (50.3% mean infection versus 9.8% in soybean-associated ponds) and increased with shorter distances to the closest forest patch and smaller average forest distance. Because glyphosate was not detected at any site and landscape influences were parasite-specific, we suggest that agriculture may have broad effects on wildlife diseases through habitat alterations that affect pathogen transmission via host habitat suitability. Notably, nonagricultural ponds had a lower mean distance to the nearest forest patch and lower mean forest distance compared with soybean-adjacent ponds. As a result, we emphasize the need for wider investigations of habitat perturbations generally associated with agriculture for host-pathogen interactions, and consequently, wildlife conservation and management strategies.

Infectious personalities: behavioural syndromes and disease risk in larval amphibians.

Behavioural consistency or predictability through time and/or different contexts ('syndromes' or 'personality types') is likely to have substantial influence on animal life histories and fitness. Consequently, there is much interest in the forces driving and maintaining various syndromes. Individual host behaviours have been associated with susceptibility to parasitism, yet the role of pre-existing personality types in acquiring infections has not been investigated experimentally. Using a larval amphibian-trematode parasite model system, we report that tadpoles generally showed consistency in their activity level in response to both novel food and parasite exposure. Not only were individual activity level and exploration in the novel food context correlated with each other and with anti-parasite behaviour, all three were significant predictors of host parasite load. This is the first empirical demonstration that host behaviours in other contexts are related to behaviours mitigating infection risk and, ultimately, host parasite load. We suggest that this system illustrates how reliably high levels of activity and exploratory behaviour in different contexts might maximize both energy acquisition and resistance to trematode parasites. Such benefits could drive selection for the behavioural syndrome seen here owing to the life histories and ecological circumstances typical of wood frog (Lithobates sylvaticus) larvae.