Constance M. O'Connor

Physiology, Behavior, and Conservation

Many animal populations are in decline as a result of human activity. Conservation practitioners are attempting to prevent further declines and loss of biodiversity as well as to facilitate recovery of endangered species, and they often rely on interdisciplinary approaches to generate conservation solutions. Two recent interfaces in conservation science involve animal behavior (i.e., conservation behavior) and physiology (i.e., conservation physiology). To date, these interfaces have been considered separate entities, but from both pragmatic and biological perspectives, there is merit in better integrating behavior and physiology to address applied conservation problems and to inform resource management. Although there are some institutional, conceptual, methodological, and communication-oriented challenges to integrating behavior and physiology to inform conservation actions, most of these barriers can be overcome. Through outlining several successful examples that integrate these disciplines, we conclude that physiology and behavior can together generate meaningful data to support animal conservation and management actions. Tangentially, applied conservation and management problems can, in turn, also help advance and reinvigorate the fundamental disciplines of animal physiology and behavior by providing advanced natural experiments that challenge traditional frameworks.

Behavioral and physiological responses of a wild teleost fish to cortisol and androgen manipulation during parental care.

Proximate mediators of reproductive behaviors in vertebrates have a long history of study. In fishes, relatively few studies have focused on hormonal control of parental care, despite a comprehensive background on the general physiology of fishes, and the frequent occurrence of parental care behaviors. Studies on this taxon have repeatedly found that the relationships between androgens and paternal care do not follow the predictions made in the avian and mammalian literature. Glucocorticoids may also have a role in mediating parental behaviors, possibly through their role as regulators of metabolism. As such, we investigated the role of 11-ketotestosterone (11-KT) and cortisol in mediating parental effort of male smallmouth bass (Micropterus dolomieu) by manipulating hormone titers in wild fish. In smallmouth bass, males spawn annually with a single female and defend a single brood for up to 30 days. Treatment of parental fish with cyproterone acetate (CYA; an androgen receptor antagonist) resulted in a decrease in nest defense in response to a simulated brood predator; however, no changes in nest success, nest tending or biochemical indicators of nutritional status were detected. Treatment with exogenous cortisol did not change parental behavior, but did increase the rate of nest failure, possibly owing to the energetic cost of chronically elevated cortisol concentrations. We discuss these findings in the context of resource-driven trade-offs and highlight life history as an important factor controlling parental effort in species with costly parental care behaviors.

Long-term effects of surgically implanted telemetry tags on the nutritional physiology and condition of wild freshwater fish.

Little is known about the long-term consequences of surgically implanted telemetry devices on wild fish, as they are rarely recaptured. We used wild largemouth bass Micropterus salmoides as a model to evaluate the long-term impacts of telemetry devices on fish physiology and nutritional condition in a closed freshwater lake where recapture rates were reasonably high. Between 2003 and 2005, 68 fish were surgically implanted with acoustic telemetry devices. Between 2005 and 2008, 17 of the tagged fish were recaptured after carrying a transmitter for 335 to 1402 d. Incision sites were examined, and individuals were non-lethally sampled for blood and measured prior to release. Plasma samples were analysed, and physiological measures of stress (glucose, Na+, Cl-, K+), tissue damage (aspartate aminotransferase), and nutritional status (Ca++, Mg+, phosphorus, total protein, triglycerides, cholesterol) were compared between fish carrying transmitters and temporally- and size-matched controls. Of the 17 recaptured fish, 3 retained at least 1 of the absorbable monofilament sutures and showed localised signs of inflammation and infection despite an elapsed time of 362 d post surgery. Five individuals showed signs of pressure necrosis at the incision site despite the fact that the transmitters averaged only 1.89% (range: 0.84 to 3.59%) of the body mass. There was no difference in any physiological parameter measured between the 2 groups, or within the telemetered fish, in relation to days since tagging or condition of the incision site. In summary, transmitter implantation was not correlated with any long-term change in any of the physiological parameters investigated. However, there is opportunity for additional research to optimise surgical techniques, guidelines on transmitter mass to body mass ratios, and choice of suture material to enhance the healing and long-term welfare of tagged fish.

Supraphysiological Cortisol Elevation Alters the Response of Wild Bluegill Sunfish to Subsequent Stressors

Wild fish are frequently exposed to multiple stressors, but the influence of previous or ongoing stress on an animals subsequent response is poorly understood. Using wild-caught bluegill sunfish (Lepomis macrochirus) as a model, we used exogenous hormone implants to experimentally raise circulating cortisol in a group of fish for ∼10 days. We also maintained sham-treated and control groups of fish. We subjected all animals to a secondary stressor in the form of either a heat challenge or fasting challenge. We compared survival, body condition, and plasma-borne indicators of physiological status among cortisol-treated, sham-treated, and control groups following the secondary stressor. In order to compare short- and long-term effects of cortisol treatment, we initiated the secondary stressor either 4 or 30 days following initial cortisol treatment. Cortisol-treated fish succumbed to the fasting challenge sooner than sham-treated and control fish at both 4 and 30 days. Interestingly, cortisol-treated fish lost equilibrium sooner than sham-treated and control fish during the heat challenge when conducted at 30 days, but not at 4 days. These results demonstrate that multiple simultaneous stressors have cumulative effects on bluegill sunfish. Furthermore, these results demonstrate that supraphysiological cortisol doses alter the long-term responses of bluegill sunfish to additional challenges, even after apparent recovery. Such cumulative and long-term effects may be an important factor in mediating the response of wild animals to natural and anthropogenic stressors, and should be considered in ecological studies.

A conceptual framework for the emerging discipline of conservation physiology

We present a conceptual framework for conservation physiology intended to facilitate the application of physiological knowledge and concepts to conservation problems. The framework is focused on moving from knowledge to action, (e.g., policy, management interventions), which is essential if this mission-oriented discipline is to contribute meaningfully to evidence-based conservation and management.

Paternal aggression towards a brood predator during parental care in wild smallmouth bass is not correlated with circulating testosterone and cortisol concentrations

Male smallmouth bass (Micropterus dolomieu) provide sole parental care including frequent aggressive actions towards conspecifics and potential brood predators. Failure to defend the brood through continual vigilance results in predation reducing the number of offspring and promoting abandonment by the nesting male. However, little is known about how biochemical and endocrine factors and brood size collectively influence paternal aggression. Behavioral assays were conducted during the egg stage of offspring development by placing a brood predator in a jar on the nest to quantify aggression (number of attacks on the potential brood predator in a minute). To determine the correlates of parental aggression, we temporarily removed fish from their nests and measured circulating levels of testosterone and indicators of the primary (plasma cortisol) and secondary stress response (plasma glucose, Cl(-), Na(+), K(+)) from non-lethal blood samples. While the male was removed from the nest, a snorkeler quantified the size of the brood. Brood size was positively correlated with male aggression. The only biochemical correlate of parental aggression was plasma glucose, which also had a positive relationship with brood size. When the effect of brood size was removed, no biochemical or endocrine factors were predictive of male aggression. Hence, brood value appeared to influence parental aggression independent of biochemical or endocrine status. While several-fold individual differences in aggression towards brood predators were noted, the role of androgens and glucocorticoids in mediating these behaviors is currently not well understood.

Brain nonapeptide levels are related to social status and affiliative behaviour in a cooperatively breeding cichlid fish.

The mammalian nonapeptide hormones, vasopressin and oxytocin, are known to be potent regulators of social behaviour. Teleost fishes possess vasopressin and oxytocin homologues known as arginine vasotocin (AVT) and isotocin (IT), respectively. The role of these homologous nonapeptides in mediating social behaviour in fishes has received far less attention. The extraordinarily large number of teleost fish species and the impressive diversity of their social systems provide us with a rich test bed for investigating the role of nonapeptides in regulating social behaviour. Existing studies, mostly focused on AVT, have revealed relationships between the nonapeptides, and both social behaviour and dominance status in fishes. To date, much of the work on endogenous nonapeptides in fish brains has measured genomic or neuroanatomical proxies of nonapeptide production rather than the levels of these molecules in the brain. In this study, we measure biologically available AVT and IT levels in the brains of Neolamprologus pulcher, a cooperatively breeding cichlid fish, using high performance liquid chromatography with fluorescence detection. We found that brain AVT levels were higher in the subordinate than in dominant animals, and levels of IT correlated negatively with the expression of affiliative behaviour. We contrast these results with previous studies, and we discuss the role the nonapeptide hormones may play in the regulation of social behaviour in this highly social animal.

Corticosteroid receptor gene expression is related to sex and social behaviour in a social fish

Circulating corticosteroids have been related to social status in a variety of species. However, our understanding of corticosteroid receptor expression and its relationship with sociality is still in its infancy. Knowledge of variation in receptor expression is critical to understand the physiological relevance of differences in circulating corticosteroid concentrations. In this study, we examined corticosteroid receptor gene expression in relation to dominance rank, sex, and social behaviour in the highly social cichlid fish, Neolamprologus pulcher. We examined the relative gene expression of the three known teleost corticosteroid receptors: glucocorticoid receptor 1 (GR1), glucocorticoid receptor 2 (GR2), and the mineralocorticoid receptor (MR) in liver and brain tissue of dominant and subordinate N. pulcher males and females. Phylogenetic analysis revealed the N. pulcher gene originally described as GR2, clustered with other teleost GR1 genes, while the originally-described N. pulcher GR1 gene clustered with the GR2 genes of other teleosts. Therefore we propose a change in the original nomenclature of the N. pulcher GRs: GR1 (formerly GR2) and GR2 (formerly GR1) and adopt this new nomenclature throughout this manuscript. Liver MR transcript levels were higher in males than females, and positively related to submissive behaviour. Liver GR2 (formerly GR1) transcript levels were also higher in males than females. Collectively, the results demonstrate sex differences in corticosteroid receptor abundance, and suggest tissue- and receptor-specific roles for corticosteroid receptors in mediating aspects of social behaviour.

Is there convergence in the molecular pathways underlying the repeated evolution of sociality in African cichlids

Despite wide variation in the complexity of social interactions across taxa, the basic behavioral components of sociality appear to be modulated by conserved hormone pathways. Specifically, the nonapeptide hormones oxytocin and vasopressin and their receptors have been implicated in regulating diverse social behaviors across vertebrates. Here, we took advantage of the repeated evolution of cooperative breeding in African cichlids to investigate whether there are consistent brain gene expression patterns of isotocin and arginine vasotocin (teleost homologues of oxytocin and vasopressin), as well as their receptors, between four closely related pairs of social (cooperative) and non-social (non-cooperative) species. We first found that the coding sequences for the five genes studied were highly conserved across the eight species. This is the first study to examine the expression of both isotocin receptors, and so we performed a phylogenetic analysis that suggests that these two isotocin receptors are paralogues that arose during the teleost genome duplication. When we then examined brain gene expression patterns relative to social system, we found that there were whole-brain gene expression differences between the social and non-social species in many of the species pairs. However, these relationships varied in both the direction and magnitude among the four species pairs. In conclusion, our results suggest high sequence conservation and species-specific gene expression patterns relative to social behavior for these candidate hormone pathways in the cichlid fishes.

Reproductive sharing in relation to group and colony-level attributes in a cooperative breeding fish

The degree to which group members share reproduction is dictated by both within-group (e.g. group size and composition) and between-group (e.g. density and position of neighbours) characteristics. While many studies have investigated reproductive patterns within social groups, few have simultaneously explored how within-group and between-group social structure influence these patterns. Here, we investigated how group size and composition, along with territory density and location within the colony, influenced parentage in 36 wild groups of a colonial, cooperatively breeding fish Neolamprologus pulcher. Dominant males sired 76% of offspring in their group, whereas dominant females mothered 82% of offspring in their group. Subordinate reproduction was frequent, occurring in 47% of sampled groups. Subordinate males gained more paternity in groups located in high-density areas and in groups with many subordinate males. Dominant males and females in large groups and in groups with many reproductively mature subordinates had higher rates of parentage loss, but only at the colony edge. Our study provides, to our knowledge, the first comprehensive quantification of reproductive sharing among groups of wild N. pulcher, a model species for the study of cooperation and social behaviour. Further, we demonstrate that the frequency of extra-pair parentage differs across small social and spatial scales.