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

Redfern, Julia C.; Cooke, Steven J.; Lennox, Robert J.; Nannini, Michael A.; Wahl, David H.; Gilmour, Kathleen M.

doi:10.1016/j.physbeh.2017.08.001

Cited by 23 publications

(17 citation statements)

References 67 publications

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“…In fish, thermal stress is known to trigger an increased plasma cortisol level (Quigley & Hinch 2006;Ryan 1995;Zubair et al 2012). We however did not find any increase in cortisol concentration into the 17°C eggs sampled before fertilization, which is in agreement with observations made by (Sopinka et al 2014) and (Redfern et al 2017). This finding rules out the participation of egg cortisol and indicates that the maternal observed effects are triggered by other mechanisms than the direct deposition of cortisol into the egg.…”

Section: Maternal Effects On Emotional Responsessupporting

confidence: 91%

“…Angular velocity, which represents erratic swimming and is commonly considered as an expression of fish anxiety (Blaser et al 2010;Egan et al 2009), tended to be lower in 17°C fish during the first 5 minutes of the test. In a previous study performed on wild largemouth bass (Micropterus salmoides), mature females were cortisol-injected (Redfern et al 2017). In line with our results related to lower angular velocity, offspring of treated females exhibited less anxiety, as indicated by decreased thigmotaxis behaviour (e.g.…”

Section: Maternal Effects On Emotional Responsessupporting

confidence: 90%

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Maternal temperature exposure triggers emotional and cognitive disorders and dysregulation of neurodevelopment genes in fish

Colson

Cousture

Zanerato-Damasceno

et al. 2018

Preprint

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Fish are sensitive to temperature, but the intergenerational consequences of maternal exposure to high temperature on offspring adaptive behaviour and underlying mechanisms are unknown. Here we show that a thermal maternal stress induces emotional and cognitive disorders in offspring. Thermal stress in mothers triggered the inhibition of fear responses and decreased spatial learning abilities in progeny. Impaired behavioural phenotypes were associated with the dysregulation of several genes known to play major roles in neurodevelopment, including auts2, a key gene for neurodevelopment, more specifically neuronal migration and neurite extension, and critical for the acquisition of neurocognitive function. In addition, our analysis revealed the dysregulation of another neurodevelopment gene (dpysl5) as well as genes associated with human cognitive disorders (arv1,plp2). We observed major differences in maternal mRNA abundance in the eggs following maternal exposure to high temperature indicating that some of the observed intergenerational effects are mediated by maternally-inherited mRNAs accumulated in the egg. Together, our observations shed new light on the intergenerational determinism of fish behaviour and associated underlying mechanisms. They also stress the importance of maternal history on fish adaptive capacities in a context of global climate changes.

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Section: Maternal Effects On Emotional Responsessupporting

confidence: 91%

Section: Maternal Effects On Emotional Responsessupporting

confidence: 90%

Maternal temperature exposure triggers emotional and cognitive disorders and dysregulation of neurodevelopment genes in fish

Colson

Cousture

Zanerato-Damasceno

et al. 2018

Preprint

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“…In rainbow trout (Oncorhynchus mykiss) it was seen that brief stress episodes, or cortisol applied very early in ontogeny, resulted in a reduced cortisol stress response at 5 months of age, suggesting that different stress responses among adults might reflect their experience during ontogeny, as well as heritable traits (Auperin and Geslin, 2008). Even cortisol treatment of females prior to spawning induced an effect on the offspring of wild largemouth bass (Micropterus salmoides), which resulted in attenuated cortisol response to an acute stressor, together with less anxiety, exploratory behaviour, boldness and aggression of juveniles (Redfern et al, 2017). Both these evidences support the hypothesis that non-genetic factors acting early in life will organize or imprint physiological systems in fish (Auperin and Geslin, 2008), in line with our results, which reflected different stress responses according to fish life history.…”

Section: Discussionmentioning

confidence: 99%

Optimizing rearing and welfare in Senegalese sole (Solea senegalesensis) broodstock: Effect of ambient light intensity and handling time on stress response

Figueiredo

Aragão

Pinto

et al. 2020

Applied Animal Behaviour Science

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Broodstock rearing conditions and handling procedures should be optimized in aquaculture species in order to benefit fish welfare and guarantee optimal conditions for spawning. In teleosts, basal cortisol levels display daily rhythms, oscillating along the 24 h of the day. In this sense, handling fish at different moments of the day may lead to different stress responses. The present study aimed at investigating the optimal rearing conditions for Senegalese sole broodstock, considering ambient light intensity and handling time. The optimal light intensity (50, 100 or 200 lx) was investigated by measuring fish cortisol levels and monitoring locomotor activity rhythms under each intensity tested. Results showed a significant increase in cortisol levels of fish exposed to 200 lx, when compared to values obtained under 100 lx, accompanied by changes in locomotor activity rhythms in both tanks under study. These results suggested that 200 lx may be too high as light intensity for this species, whereas 100 lx seems to be more adequate. Also, daily rhythms of stress response were investigated in breeders from different origins (Wild and first generation, G1). Basal cortisol levels and cortisol stress response after an acute stressor (air exposure) were monitored at two distinct moments of the day (Mid-Light and Mid-Dark). Basal levels were higher during the day in the wild group, while G1 fish seemed to have lost the daily fluctuations in basal cortisol plasma levels, as well as their daily rhythms of locomotor activity. Both groups showed lower stress responses during night-time, an indication that this is an adequate period of the day to handle this species. Senegalese sole breeders born in captivity presented more pronounced stress responses when compared to wild fish, reflecting their different life history in terms of stress challenges.

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“…Unpredictable chronic stress (social isolation, crowding, tank changes, thermal variations, and chasing) affect zebrafish males but not females (118), highlighting the double effect of species-specificity and sex-biased covariation in stress studies. The offspring of largemouth bass females ( Micropterus salmoides ) treated with cortisol showed lower responsiveness to stress and exhibit less exploratory behavior and aggression than those of non-treated females (119), adding to the stressotope equation the still imprecisely described mechanism of vertical transmission of stress-related phenotypes.…”

Section: Janian Phenomesmentioning

confidence: 99%

Netting the Stress Responses in Fish

2019

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In the last decade, the concept of animal stress has been stressed thin to accommodate the effects of short-term changes in cell and tissue physiology, major behavioral syndromes in individuals and ecological disturbances in populations. Seyle's definition of stress as “the nonspecific (common) result of any demand upon the body” now encompasses homeostasis in a broader sense, including all the hierarchical levels in a networked biological system. The heterogeneity of stress responses thus varies within individuals, and stressors become multimodal in terms of typology, source and effects, as well as the responses that each individual elicits to cope with the disturbance. In fish, the time course of changes after stress strongly depends on several factors, including the stressful experiences in early life, the vertical transmission of stressful-prone phenotypes, the degree of individual phenotypic plasticity, the robustness and variety of the epigenetic network related to environmentally induced changes, and the intrinsic behavioral responses (individuality/personality) of each individual. The hierarchical heterogeneity of stress responses demands a code that may decrypt and simplify the analysis of both proximate and evolutionary causes of a particular stress phenotype. We propose an analytical framework, the stressotope , defined as an adaptive scenario dominated by common environmental selective pressures that elicit common multilevel acute stress-induced responses and produce a measurable allostatic load in the organism. The stressotope may constitute a blueprint of embedded interactions between stress-related variations in cell states, molecular mediators and systemic networks, a map of circuits that reflect the inherited and acquired stress responses in an ever-changing, microorganismal-loaded medium. Several features of the proposed model are discussed as a starting point to pin down the maximum common stress responses across immune-neuroendocrine relevant physiological levels and scenarios, including the characterization of behavioral responses, in fish.

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

Cited by 23 publications

References 67 publications

Maternal temperature exposure triggers emotional and cognitive disorders and dysregulation of neurodevelopment genes in fish

Maternal temperature exposure triggers emotional and cognitive disorders and dysregulation of neurodevelopment genes in fish

Optimizing rearing and welfare in Senegalese sole (Solea senegalesensis) broodstock: Effect of ambient light intensity and handling time on stress response

Netting the Stress Responses in Fish

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