Impairment of branchial and coronary blood flow reduces reproductive fitness, but not cardiac performance in paternal smallmouth bass (Micropterus dolomieu).

The capacity to extract oxygen from the water, and the ability of the heart to drive tissue oxygen transport, are fundamental determinants of important life-history performance traits in fish. Cardiac performance is in turn dependent on the heart's own oxygen supply, which in some teleost species is partly delivered via a coronary circulation originating directly from the gills that perfuses the heart, and is crucial for cardiac, metabolic and locomotory capacities. It is currently unknown, however, how a compromised branchial blood flow (e.g., by angling-induced hook damage to the gills), constraining oxygen uptake and coronary blood flow, affects the energetically demanding parental care behaviours and reproductive fitness in fish. Here, we tested the hypothesis that blocking » of the branchial blood flow and abolishing coronary blood flow would negatively affect parental care behaviours, cardiac performance (heart rate metrics, via implanted Star-Oddi heart rate loggers) and reproductive fitness of paternal smallmouth bass (Micropterus dolomieu). Our findings reveal that branchial/coronary ligation compromised reproductive fitness, as reflected by a lower proportion of broods reaching free-swimming fry and a tendency for a higher nest abandonment rate relative to sham operated control fish. While this was associated with a tendency for a reduced aggression in ligated fish, parental care behaviours were largely unaffected by the ligation. Moreover, the ligation did not impair any of the heart rate performance metrics. Our findings highlight that gill damage may compromise reproductive output of smallmouth bass populations during the spawning season. Yet, the mechanism(s) behind this finding remains elusive.

Cortisol modulates metabolism and energy mobilization in wild-caught pumpkinseed (Lepomis gibbosus).

Acute elevation of cortisol via activation of the hypothalamic-pituitary-interrenal (HPI) axis aids the fish in dealing with a stressor. However, chronic elevation of cortisol has detrimental effects and has been studied extensively in lab settings. However, data pertaining to wild teleosts are lacking. Here, we characterized the metabolic consequences of prolonged cortisol elevation (96 h) in wild-caught pumpkinseed (Lepomis gibbosus). Pumpkinseed were implanted with cocoa butter alone (sham) or containing cortisol (25 mg kg-1 body weight), and at 24, 48, 72, and 96 h, tissue samples were collected, whole-body ammonia excretion was determined, and whole-organism metabolism was assessed using intermittent flow respirometry. Cortisol-treated pumpkinseed exhibited the highest plasma cortisol concentration at 24 h post-implantation, with levels decreasing over the subsequent time points although remaining higher than in sham-treated fish. Cortisol-treated fish exhibited higher standard and maximal metabolic rates than sham-treated fish, but the effect of cortisol treatment on aerobic scope was negligible. Indices of energy synthesis/mobilization, including blood glucose concentrations, hepatosomatic index, hepatic glycogen concentrations, and ammonia excretion rates, were higher in cortisol-treated fish compared with controls. Our work suggests that although aerobic scope was not diminished by prolonged elevation of cortisol levels, higher metabolic expenditures may be of detriment to the animal's performance in the longer term.

Exploring relationships between cardiovascular activity and parental care behavior in nesting smallmouth bass: A field study using heart rate biologgers.

Research in a variety of vertebrate taxa has found that cardiac function is a major limiting factor in the ability of animals to cope with physiological challenges, and thus is suggested to play an important role in mediating fitness-related behaviors in the wild. Yet, there remains a paucity of empirical assessments of the relationships between physiological performance and biological fitness in wild animals, partially due to challenges in measuring these metrics remotely. Using male smallmouth bass (Micropterus dolomieu) as a model, we tested for relationships between cardiac performance (measured using heart rate biologgers) and fitness-related behaviors (assessed using videography and snorkeler observations) in the wild during the parental care period. Our results showed that heart rates were not significantly related to any measured parental care behaviors (e.g., nest tending) except for individual aggression level. After accounting for the effect of water temperature on heart rate, we found within-individual heart rate differed between days and also differed between nights. There was, however, evidence of diel variation in heart rate, where heart rate was higher during the day than at night. Although fitness is thought to be dependent on physiological capacity for exercise in wild animals, inter-individual variation in heart rate alone does not appear to relate to parental care behavior in smallmouth bass at the temporal scales examined here (i.e., hours to days). Further studies are required to confirm relationships between physiological performance and parental care behavior to elucidate the apparently complex relationships between physiology, behavior, and fitness in wild animals.

Cortisol does not increase risk of mortality to predation in juvenile bluegill sunfish: A manipulative experimental field study.

The hypothalamic-pituitary-interrenal (HPI) or stress axis in teleost fishes produces their primary glucocorticoid, cortisol. Although generally an adaptive response, prolonged HPI axis stimulation can impair organismal performance. Previous work has shown that stressed teleosts have higher mortality to predation than unstressed conspecifics, suggesting a role for HPI axis in modulating predator-prey interactions. Our current study investigated whether elevated cortisol levels altered the predation rate of a wild teleost fish, the bluegill sunfish (Lepomis macrochirus). Wild juvenile bluegill were given intraperitoneal implants of cocoa butter (i.e., sham), or cocoa butter containing cortisol or cortisol and the glucocorticoid receptor antagonist RU486. After 24 hr, fish were tethered along the bottom of the lake and their survival under natural predation was recorded following 24 hr. A subset of fish was used to validate the efficacy of cortisol implants in this setting. No treatment effect on survival was observed, suggesting that elevated cortisol has minimal involvement in mediating predator-prey interactions in this context. However, experimental fish may have demonstrated resiliency to physiological perturbations owing to the relatively acute duration of our experimental series, and negative effects might be manifested over a more chronic period.

Chronic Plasma Cortisol Elevation Does Not Promote Riskier Behavior in a Teleost Fish: A Test of the Behavioral Resiliency Hypothesis.

Stressed fish have been shown to have higher predator-induced mortality than unstressed conspecifics, suggesting a role for the hypothalamic-pituitary-interrenal axis in modifying risk-taking behaviors. Yet, there is also evidence of behavioral resiliency in the face of chronic stressors. Here, we tested the behavioral resiliency hypothesis, which posits that animals can maintain consistent behavioral phenotypes in the face of significant physiological challenges. We determined whether chronic plasma cortisol elevation promotes risk-taking behaviors in a model teleost fish, the pumpkinseed sunfish (Lepomis gibbosus). Experimental fish were implanted with cocoa butter either as a sham or with cortisol. At 48 h post-implantation, the behavior of individual focal fish was tested in an experimental arena comprising of a simulated physical refuge, an open zone containing a constrained conspecific shoal, and a compartment containing either a model of a northern pike (Esox lucius) paired with corresponding pike olfactory cues in lake water or no pike model (control) paired with sham lake water cues only. The fish were assayed individually for their refuge utilization, shoaling tendency, and general activity. Neither cortisol treatment nor predation-risk treatment influenced any of these behaviors. This suggests that sunfish, in the context of our experiment, were behaviorally resilient to the physiological effects of chronic plasma cortisol elevation and in the face of an apparent threat of predation. Our results thus provide support for the behavioral resiliency hypothesis in fish under both physiological and ecological stressors. We posit that behavioral resiliency is an evolutionary adaptation ensuring appropriate responses to environmental conditions.

Elevação Crônica do Cortisol Plasmático não Promove Comportamento Mais Arriscado em um Peixe Teleósteo: Um teste da Hipótese de Resiliência Comportamental (Chronic Plasma Cortisol Elevation Does Not Promote Riskier Behavior in a Teleost Fish: A Test of the Behavioral Resiliency Hypothesis) Foi demonstrado que peixes estressados têm maior mortalidade causada por predadores do que co-específicos não estressados, sugerindo um papel para o eixo hipotálamo­hipófise­interrenal na modificação de comportamentos de risco. No entanto, há também evidências de resiliência comportamental frente a estressores crônicos. Aqui testamos a hipótese de resiliência comportamental, que postula que os animais podem manter fenótipos comportamentais consistentes frente a desafios fisiológicos significativos. Determinamos se a elevação crônica do cortisol plasmático promove comportamentos de risco em um peixe teleósteo modelo, o perca-sol (Lepomis gibbosus). Peixes experimentais foram implantados com manteiga de cacau, tanto como um placebo ou com cortisol. Após 48 h da implantação, o comportamento de peixes individuais foi testado em uma arena experimental composta por um refúgio simulado, uma zona aberta contendo um cardume co-específico e um compartimento contendo um modelo de lúcio-do-norte (Esox lucius) pareado com as pistas olfativas correspondentes de lúcios em água fluvial ou sem modelo (controle) pareado apenas com iscas falsas. Os peixes foram analisados individualmente quanto à utilização de refúgio, tendência de formar cardumes, e atividade geral. Nem o tratamento com cortisol e nem o com risco de predação influenciaram qualquer um desses comportamentos. Isto sugere que os perca-sol, no contexto do nosso experimento, eram comportamentalmente resilientes aos efeitos fisiológicos da elevação crônica do cortisol plasmático e diante de uma aparente ameaça de predação. Nossos resultados fornecem apoio para a hipótese de resiliência comportamental em peixes sob estressores fisiológicos e ecológicos. Nós postulamos que a resiliência comportamental é uma adaptação evolutiva que garante respostas apropriadas às condições ambientais. translated to Portuguese by G. Sobral (gabisobral@gmail.com).

La Elevación Crónica de Cortisol en el Plasma no Promueve un Comportamiento más Riesgoso en un Pez Teleósteo: Una Prueba de la Hipótesis de Resistencia de Comportamiento (Chronic Plasma Cortisol Elevation Does Not Promote Riskier Behavior in a Teleost Fish: A Test of the Behavioral Resiliency Hypothesis) Se ha demostrado que los peces estresados tienen una mayor mortalidad inducida por depredadores que los conespecíficos no estresados, lo que sugiere un papel para el eje hipotálamo­pituitario­interrenal en la modificación de los compartamientos de riesgo. Sin embargo, también hay evidencia de resistencia del comportamiento frente a los factores estresantes crónicos. Aquí, probamos la hipótesis de resistencia del comportamiento, que postula que los animales pueden mantener fenotipos de comportamiento consistentes ante desafíos fisiológicos significativos. Determinamos si la elevación crónica de cortisol en plasma promueve comportamientos de riesgo en un pez modelo teleósteo, el pez sol de semillas de calabaza (Lepomis gibbosus). Los peces experimentales se implantaron con manteca de cacao como una farsa o con cortisol. A las 48 h posteriores a la implantación, se evaluó el comportamiento de los peces focales individuales en un campo experimental que comprende un refugio físico simulado, una zona abierta que contiene un banco de peces conspecificos constreñidos, y un compartimento que contiene un modelo de lucio norteño (Esox lucius) emparejado con señales olfativas de lucio correspondientes en el agua del lago o sin modelo de lucio (control) emparejado solo con señales de agua del lago simulado. Los peces fueron analizados individualmente por su utilización de refugio, tendencia al cardumen y actividad general. Ninguno de estos comportamientos fuero influidos por el tratamiento con cortisol o el tratamiento de riesgo de depredación. Esto sugiere que los peces sol, en el contexto de nuestro experimento, eran resistentes al comportamiento frente a los efectos fisiológicos de la elevación crónica de cortisol en el plasma y ante una amenaza aparente de depredación. Por lo tanto, nuestros resultados brindan apoyo para la hipótesis de resistencia de comportamiento en peces bajo factores de estrés fisiológicos y ecológicos. Postulamos que la resiliencia conductual es una adaptación evolutiva que garantiza respuestas adecuadas a las condiciones ambientales. translated to Spanish by Y. E. Jimenez (yordano_jimenez@brown.edu).

Cortisol treatment affects locomotor activity and swimming behaviour of male smallmouth bass engaged in paternal care: A field study using acceleration biologgers.

Paternal care, where the male provides sole care for the developing brood, is a common form of reproductive investment among teleost fish and ubiquitous in the Centrarchidae family. Throughout the parental care period, nesting males expend energy in a variety of swimming behaviours, including routine and burst swimming, vigilantly monitoring the nest area and protecting the brood from predators. Parental care is an energetically demanding period, which is presumably made even more difficult if fish are exposed to additional challenges such as those arising from human disturbance, resulting in activation of the hypothalamic-pituitary-interrenal axis (i.e., elevation of cortisol). To study this situation, we examined the effects of experimental manipulation of the stress hormone cortisol on locomotor activity and behaviour of nest guarding male smallmouth bass (Micropterus dolomieu). We exogenously elevated circulating cortisol levels (via intracoelomic implants) and attached tri-axial accelerometers to wild smallmouth bass for three days. During the recovery period (i.e., ≤4h post-release), cortisol-treated fish exhibited significantly reduced locomotor activity and performed significantly less burst and routine swimming relative to control fish, indicating cortisol uptake was rapid, as were the associated behavioural responses. Post-recovery (i.e., >4h post-release), fish with high cortisol exhibited lower locomotor activity and reduced routine swimming relative to controls. Fish were less active and reduced routine and burst swimming at night compared to daylight hours, an effect independent of cortisol treatment. Collectively, our results suggest that cortisol treatment (as a proxy for anthropogenic disturbance and stress) contributed to altered behaviour, and consequently cortisol-treated males decreased parental investment in their brood, which could have potential fitness implications.

Parental Care in a Stressful World: Experimentally Elevated Cortisol and Brood Size Manipulation Influence Nest Success Probability and Nest-Tending Behavior in a Wild Teleost Fish.

Parental care is an advantageous reproductive behavior, as the fitness of the caregiver is increased through improving the chances of its offspring's survival. Parental care occurs in a variety of teleost fishes. The body size of parental fish and the size of their brood can affect nest abandonment decisions, where compared with smaller fish with smaller broods, larger fish with larger broods typically invest more energy into reproductive events because they have less future reproductive potential. Although essential for basal metabolism and body maintenance functions, when glucocorticoid hormones (e.g., cortisol) are chronically elevated, as can occur during stress, fish may experience impairments in behavior and immune function, leading to compromised health and condition. Anthropogenic stressors during parental care can lead to elevated stress, therefore making it necessary to understand how stress influences an already-challenging period. Using smallmouth bass as a model, a gradient of body sizes, and experimentally manipulated brood size (i.e., reducing large broods and supplementing small broods) and cortisol levels (i.e., elevated via slow-release intraperitoneal cocoa butter implants containing cortisol versus controls), we tested the hypothesis that the reproductive success and parental care behaviors (i.e., aggression, nest tending) of nest-guarding male smallmouth bass are influenced by parental body size, brood size, and cortisol level. Overall, there was a relationship between cortisol treatment and nest success in which larger fish exhibited lower success when cortisol levels were elevated. Brood size had a significant effect on fish-tending behavior, independent of cortisol level and body size. Lending partial support to our hypothesis, the results of this study indicate that the reproductive success of guarding male smallmouth bass is influenced by cortisol level and that tending behavior is affected by brood size.