Constance M. O’Connor

Stress and parental care in a wild Teleost fish: insights from exogenous supraphysiological cortisol implants.

Male largemouth bass (Micropterus salmoides) provide sole parental care over a 4–6‐wk period to a single brood, fanning the eggs to keep them oxygenated and free of silt and defending the brood until the offspring develop antipredator tactics. During this period, fish are highly active and have few opportunities for feeding, so this activity is energetically costly. To understand some of the consequences of stress during this challenging period, we injected fish with cortisol suspended in coconut oil to experimentally raise circulating cortisol in parental males for the first week of the parental care period. We compared parental care behavior between cortisol‐treated, sham‐treated (injected only with coconut oil), and control parental males. We further compared physiological parameters associated with metabolism and reproductive function between cortisol‐treated and control males. The cortisol injections resulted in supraphysiological levels of circulating plasma cortisol, giving us insight into potential maximal effects of stress during parental care. At these supraphysiological levels, the cortisol‐treated fish displayed higher concentrations of circulating glucose and cholesterol and lower concentrations of circulating triglycerides when compared with control fish, with no change in plasma concentrations of total protein. Plasma concentrations of androgen were similarly unaffected by cortisol treatment. In the short term (initial 1–2 wk), parental care of eggs and egg‐sac fry was maintained by all groups, with no differences observed in behavior (e.g., tending, vigilance, defense) among the groups. However, the cortisol‐treated fish abandoned their offspring at a higher rate than in the control or sham groups. The fish treated with cortisol also tended to develop external Saprolegnian infections, indicative of compromised immune function. These data demonstrate that exogenous cortisol elevation during parental care results in changes in energy use and a decrease in immune function. Interestingly, the data also suggest resistance to stress during parental care in largemouth bass, with no changes in parental care behavior before abandonment.

Seasonal carryover effects following the administration of cortisol to a wild teleost fish.

Stress can have sublethal effects that are manifested either immediately or at spatial or temporal scales that are removed from the stress event (i.e., carryover effects). We tested whether a short-term elevation of plasma cortisol would result in seasonal carryover effects in wild largemouth bass Micropterus salmoides. Using exogenous hormone implants, we raised circulating cortisol concentrations in a group of wild fish for approximately 5 d in October 2007. We then compared activity (velocity, distance traveled) of cortisol-treated animals with that of sham-treated and control animals throughout the winter using an automated acoustic telemetry array. Immediately following treatment, the cortisol-treated fish showed increased activity relative to controls. However, this difference disappeared following the cessation of the elevation of circulating cortisol. During the winter of 2007 to 2008, the lake experienced a nearly complete winterkill event, providing insight into how a transient stress response can influence the response of wild animals to subsequent challenges. Most fish carrying acoustic transmitters succumbed during this winterkill event, but cortisol-treated fish died earlier than fish in other groups and showed a decrease in activity relative to controls and sham-treated fish before mortality. This study provides preliminary evidence of seasonal carryover effects in wild fish and yields insight into the ecological consequences of stress across broad temporal scales.

The glucocorticoid stress response is attenuated but unrelated to reproductive investment during parental care in a teleost fish

We investigated whether circulating glucocorticoids and androgens are correlated with reproductive investment in smallmouth bass (Micropterus dolomieu), a teleost fish with sole paternal care. Circulating cortisol and androgens prior to and 25 min following a standardized 3 min emersion stressor were quantified for non-reproductive and parental fish across the parental care period. To experimentally investigate the influence of reproductive investment on endocrine parameters, we manipulated brood size (reduced, enlarged, sham-treated, or unmanipulated) 24h prior to sampling parental fish. We predicted that fish guarding offspring would exhibit increased androgens and baseline cortisol levels, and an attenuated cortisol response to the stressor when compared with non-reproductive individuals. We further predicted that these effects would scale with reproductive investment. As predicted, parental care-providing fish exhibited lower post-stress plasma cortisol concentrations than non-reproductive fish. This difference was strongest early during parental care. However, no differences in baseline or post-stress cortisol concentrations were detected among parents guarding offspring with varying brood sizes. There was, however, a trend for parental fish to exhibit an increased cortisol response following brood manipulation, regardless of the direction of change in brood size, a response that likely reflected disturbance. No differences were found in baseline cortisol concentrations. Circulating androgens were found to be highest during early parental care, and no differences were found among parents guarding manipulated broods. Collectively, these findings demonstrate that the endocrine stress response is affected by reproductive status, but the response in this model species does not appear to be scaled according to reproductive investment as predicted by life-history theory.

Stress Indicators in Fish

1. Why Do We Measure Stress? 2. Quantifying Stress 3. Specific Measures of Fish Stress 3.1. Cellular and Molecular Indicators 3.2. Primary and Secondary Physiological Indicators 3.3. Whole-Organism Indicators 4. Considerations for Measuring and Interpreting Stress 4.1. Interspecific Differences 4.2. Intraspecific Differences 4.3. Context-Specific Differences 4.4. Stressor Severity 4.5. Field Versus Laboratory 4.6. Temporal Aspects 5. From Individual Indicators to Ecosystem Health 6. Stress Indicators of the Future 7. Conclusion A fish is chased with a net in an aquarium before being captured, scooped out of the water, and placed in a nearby testing arena. Is it stressed? How can we tell? Are our indicators reliable? Quantification of stress in fish has evolved from the initial development of radioimmunoassays to measure cortisol in plasma to the rapidly expanding suite of genome-based assays. Indicators range from the intracellular to whole-animal level. Expression of heat shock proteins (HSPs) and activity of metabolic enzymes can be paired with straightforward observations of reflexes and survival. Both traditional and emerging indicators have advantages and disadvantages, and their use is tissue- and context-specific. Ecological, biological, and methodological factors must be considered when selecting, measuring, and interpreting stress indicators. Inter- and intraspecific, sex, life stage, and temporal differences in physiological responses to stressors can confound confirmation of a stressed state. Despite numerous types of indicators, our understanding of how absolute levels of indicators relate to stressor severity and recovery to date remains limited. How accurately indicators characterize stress in wild populations naturally exposed to stressors is still an evolving discussion. The integration of research disciplines and involvement of stakeholders and user groups will aid in filling these knowledge gaps, as well as the translation of individual-level indicators to population- and ecosystem-level processes.

Circulating androgens are influenced by parental nest defense in a wild teleost fish

While social interactions influence vertebrate endocrine regulation, the dynamics of regulation in relation to specific behaviors have not been clearly elucidated. In the current study, we investigated whether androgens (testosterone) or glucocorticoids (cortisol) play a functional role in aggressive offspring defense behavior in wild smallmouth bass (Micropterus dolomieu), a teleost fish with sole paternal care. We measured circulating testosterone and cortisol concentrations in plasma samples taken from parental males following a simulated nest intrusion by a common nest predator, the bluegill sunfish (Lepomis macrochirus). To understand whether endocrine regulation changes across the parental care period, we looked both at males guarding fresh eggs and at males guarding hatched embryos. Plasma testosterone levels increased in males subjected to a simulated nest intrusion when compared to sham controls. Testosterone concentrations in males guarding embryos were lower than in males guarding fresh eggs, but circulating testosterone was positively correlated with the level of aggression towards the nest predator at both offspring development stages. However, there was no increase in cortisol levels following a simulated nest intrusion, and no relationship between cortisol and any measured parameter. These results suggest that androgens play an important role in promoting aggressive nest defense behavior in teleost fish.

Reproductive History and Nest Environment Are Correlated with Circulating Androgen and Glucocorticoid Concentrations in a Parental Care–Providing Teleost Fish

Using a long-term study population of wild smallmouth bass Micropterus dolomieu in a connected river-lake system, we investigated whether circulating glucocorticoid (cortisol) and androgen (testosterone) concentrations are influenced by reproductive investment and nesting environment in fish providing nest-guarding paternal care. For all individuals, we collected measures of reproductive history and the value of current parental care. We assessed nest environment and monitored individuals to quantify seasonal reproductive success. Finally, we measured circulating cortisol concentrations following a standardized stressor and circulating testosterone concentrations. Using general linear models, we found that poststress circulating cortisol concentrations were positively related to water temperature and were higher in fish nesting in the river than in the lake. Circulating testosterone concentrations were negatively related to water temperature and were higher in reproductively experienced fish. When considering the factors that influence reproductive success, we found that only parental size was positively related to current nest success. In summary, the results demonstrate that nesting environment is correlated with parental stress responses during parental care, while reproductive history and nesting environment are correlated with circulating androgen concentrations. Collectively, these results offer insight into the roles of both glucocorticoid and androgen steroid hormones during parental care in teleost fish.

Electric Fish Handling Gloves Provide Effective Immobilization and Do Not Impede Reflex Recovery of Adult Largemouth Bass

AbstractElectric fish handling gloves (FHGs) have been developed to immobilize fish during handling, with the potential benefit of reducing the time needed for sedation and recovery of fish relative to chemical anaesthetics. We examined the secondary stress responses (i.e., hematocrit, blood glucose, lactate, and pH) and reflex responses of Largemouth Bass Micropterus salmoides that were immobilized in water using electric FHGs for multiple durations (0, 30, and 120 s) relative to fish that were handled using only bare hands in water. We also evaluated the efficacy of the immobilization by quantifying the number of volitional movements that were observed during handling. Our findings suggested that when FHGs were used, fish tended to remain still (i.e., to show full reflex impairment) during handling relative to controls. Fish that were held with FHGs showed negligible reflex impairment immediately after the electricity was terminated. After a 30-min posttreatment retention period, blood chemistry and ven...

The Preference for Social Affiliation Renders Fish Willing to Accept Lower O2 Levels

Animals are bombarded with information about their environment and must select and interpret the relevant cues to make behavioral adjustments critical to survival. How animals integrate and balance the many signals they receive about their environment is rarely assessed. We investigated how signals from the social and physical environment interact to influence environmental preferences in the endemic Tanganyikan cichlid Neolamprologus pulcher. Specifically, we explored how fish respond to the physiological challenge of declining O2 levels in light of embedded social preferences using a modified shuttle box apparatus to test O2 preferences. In the presence of a conspecific, the average (preferred) partial pressure of oxygen (Po2) and minimum Po2 experienced were significantly lower (14.90±2.13 and 12.35±3.15 kPa, respectively) than in trials without a conspecific (17.18±2.55 and 15.62±3.09 kPa, respectively). Fish with conspecifics also spent more time in the low Po2 zone of the shuttle box and moved between the high and low Po2 zones less frequently. Hence, O2 preferences were modified, and fish willingly remained in an area of continuously declining O2 availability to associate with a conspecific. The O2 preferences of an individual during social trials correlated with its excess postexercise O2 consumption following an exhaustive chase but not with its aerobic scope, routine O2 consumption rate, or body mass. These results suggest that some aspects of respiratory and metabolic physiology (such as the propensity to use anaerobic metabolism) but not others (such as O2 transport capacity) underpin some variation in social behavior under environmental stress.