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The concept of stress in fish

The general physiological response of fish to threatening situations, as with all vertebrates, is referred to as stress . A stress response is initiated almost immediately following the perception of a stressor. Mildly stressful situations can have beneficial or positive effects (eustress), while higher severities induce adaptive responses but also can have maladaptive or negative consequences (distress). The stress response is initiated and controlled by two hormonal systems , those leading to the production of corticosteroids (mainly cortisol) and catecholamines (such as adrenaline and noradrenaline and their precursor dopamine). Together these regulate the secondary stress response factors that alter the distribution of necessary resources such as energy sources and oxygen to vital areas of the body, as well as compromise hydromineral imbalance and the immune system. If fish can resist death due to a stressor, they recover to a similar or somewhat similar homeostatic norm. Long-term consequences of repeated or prolonged exposures to stress are maladaptive by negatively affecting other necessary life functions (growth, development, disease resistance, behavior, and reproduction), in large part because of the energetic cost associated with mounting the stress response (allostatic load). There is considerable variation in how fish respond to a stressor because of genetic differences among different taxa and also within stocks and species. Variations within the stress response are introduced by the environmental history of the fish, present ambient environmental conditions, and the fish's present physiological condition. Currently, fish physiology has progressed to the point where we can easily recognize when fish are stressed, but we cannot always recognize when fish are unstressed because the lack of clinical signs of stress does not always correspond to fish being unstressed. In other words, we need to be aware of the possibility of false negatives regarding clinical signs of stress. In addition, we cannot use clinical data to precisely or accurately infer severity of a stressor.

Fish Physiology

Changes in reproductive biomarkers in an endangered fish species (bonytail chub, Gila elegans) exposed to low levels of organic wastewater compounds in a controlled experiment

In arid regions of the southwestern United States, municipal wastewater treatment plants commonly discharge treated effluent directly into streams that would otherwise be dry most of the year. A better understanding is needed of how effluent-dependent waters (EDWs) differ from more natural aquatic ecosystems and the ecological effect of low levels of environmentally persistent organic wastewater compounds (OWCs) with distance from the pollutant source. In a controlled experiment, we found 26 compounds common to municipal effluent in treatment raceways all at concentrations <1.0 μg/L. Male bonytail chub (Gila elegans) in tanks containing municipal effluent had significantly lower levels of 11-ketotestosterone (p = 0.021) yet higher levels of 17β-estradiol (p = 0.002) and vitellogenin (p = 0.036) compared to control male fish. Female bonytail chub in treatment tanks had significantly lower concentrations of 17β-estradiol than control females (p = 0.001). The normally inverse relationship between primary male and female sex hormones, expected in un-impaired fish, was greatly decreased in treatment (r = 0.00) versus control (r = −0.66) female fish. We found a similar, but not as significant, trend between treatment (r = −0.45) and control (r = −0.82) male fish. Measures of fish condition showed no significant differences between male or female fish housed in effluent or clean water. Inter-sex condition did not occur and testicular and ovarian cells appeared normal for the respective developmental stage and we observed no morphological alteration in fish. The population-level impacts of these findings are uncertain. Studies examining the long-term, generational and behavioral effects to aquatic organisms chronically exposed to low levels of OWC mixtures are needed.

Aquatic Toxicology

An overview of estrogen-associated endocrine disruption in fishes: Evidence of effects on reproductive and immune physiology

Simply and perhaps intuitively defined, endocrine disruption is the abnormal modulation of normal hormonal physiology by exogenous chemicals. In fish, endocrine disruption of the reproductive system has been observed worldwide in numerous species and is known to affect both males and females. Observations of biologically relevant endocrine disruption most commonly occurs near waste water treatment plant outfalls, pulp and paper mills, and areas of high organic loading sometimes associated with agricultural practices. Estrogenic endocrine disrupting chemicals (EEDCs) have received an overwhelmingly disproportionate amount of scientific attention compared to other EDCs in recent years. In male fishes, exposure to EEDCs can lead to the induction of testicular oocytes (intersex), measurable plasma vitellogenin protein, altered sex steroid profiles, abnormal spawning behavior, skewed population sex ratios, and lessened reproductive success. Interestingly, contemporary research purports that EDCs modulate aspects of non-reproductive physiology including immune function. Here we present an overview of endocrine disruption in fishes associated with estrogenic compounds, implications of this phenomenon, and examples of EDC related research findings by our group in the Potomac River Watershed, USA.

Conference Paper

Effects of aqueous exposure to polychlorinated biphenyls (Aroclor 1254) on physiology and behavior of smolt development of Atlantic salmon

Polychlorinated biphenyls (PCBs) are a widespread aquatic contaminant and are present in both wild and hatchery raised Atlantic salmon, Salmo salar. The possible sub-lethal alterations in smolt physiology and behavior due to PCB exposure of salmon have not been widely examined. In this study, we examined the effects of the PCB mixture Aroclor 1254 on survival and smolt development of Atlantic salmon. In separate experiments, fish were exposed as yolk-sac larvae or as juveniles just prior to the parr-smolt transformation in April to 1 ??g l-1 (PCB-1) or 10 ??g l-1 (PCB-10) aqueous Aroclor 1254 (A1254), or vehicle for 21 days. After exposure, yolk-sac larvae were reared at ambient conditions for 1 year, until the peak of smolting the following May. Juveniles were sampled immediately after exposure. Both groups were assessed for behavioral, osmoregulatory, and endocrine disruption of smolt development at the peak of smolting. PCB-1 and PCB-10 treated yolk-sac larvae exhibited significant increases in the rate of opercular movement after 14 and 21 days of exposure. At the peak of smolting, prior exposure as yolk-sac larvae to PCB-1 did not affect behavior, while PCB-10 dramatically decreased volitional preference for seawater. Neither concentration of A1254 had long-term effects on the osmoregulatory or endocrine parameters measured in animals exposed as yolk-sac larvae. Juvenile fish exposed to PCB-1 or PCB-10 during smolting exhibited a dose-dependent reduction in preference for seawater. Fish treated with the higher dose of A1254 also exhibited a 50% decrease in gill Na+,K+-ATPase activity and a 10% decrease in plasma chloride levels in freshwater. In addition, plasma triiodothyronine was reduced 35-50% and plasma cortisol 58% in response to exposure to either concentration; whereas plasma thyroxine, growth hormone, and insulin-like growth factor I levels were unaffected. These results indicate that the effects of exposure to A1254 may vary according to developmental stage. Exposure to A1254 in the freshwater environment can inhibit preparatory adaptations that occur during smolting, thereby reducing marine survival and sustainability of salmon populations. ?? 2007 Elsevier B.V. All rights reserved.

Aquatic Toxicology

Breeding behavior and reproductive life history of the Neosho Madtom, Noturus placidus (Teleostei: Ictaluridae)

The Neosho madtom, Noturus placidus , is a small catfish listed by the U. S. Fish and Wildlife Service as threatened. Little is known of its breeding biology and behavior because high turbidity and flow during its spawning season prevent direct observation in the field, and captive propagation has met with limited success. We held Neosho madtoms in laboratory aquaria in 1996 and 1998 to study sexual dimorphism during breeding season, courtship and nesting behavior, egg and clutch size, and embryological and larval development. We also attempted to induce spawning. Courtship behaviors were recorded on videotape, including “carousel” and “tail curl” displays in which the fish spun in circles, head to tail, then quivered, with the male's tail wrapped around the female's head. Three clutches were observed, all in nest cavities that had been excavated by the fish under a structure; one clutch (1996) consisted of approximately 60 eggs, with a mean chorion diameter of 3.1 mm, and two (1998) consisted of approximately 30 eggs, with mean diameter of 3.7 mm. In all situations, eggs hatched after eight or nine days, and yolk-sacs were fully depleted seven days later. One spawn (1998) occurred after two days of injection with synthetic hormone. Male parental care of eggs and larvae was observed in 1996. Larvae remained in the nest until yolk-sacs were absorbed, after which they dispersed throughout the tank. Dissection of two females that laid clutches in this study revealed previtellogenic eggs in the lumen of ovaries, with a mean chorion diameter of 0.9 mm. Swollen lips of males, distended abdomen of females, and differences in head shape, premaxillary tooth patch coloring, and genital papillae of breeding males and females were documented during spawning periods.

Transactions of the Kansas Academy of Science

Baseline glucocorticoids are drivers of body mass gain in a diving seabird

Life-history trade-offs are influenced by variation in individual state, with individuals in better condition often completing life-history stages with greater success. Although resource accrual significantly impacts key life-history decisions such as the timing of reproduction, little is known about the underlying mechanisms driving resource accumulation. Baseline corticosterone (CORT, the primary avian glucocorticoid) mediates daily and seasonal energetics, responds to changes in food availability, and has been linked to foraging behavior, making it a strong potential driver of individual variation in resource accrual and deposition. Working with a captive colony of white-winged scoters ( Melanitta fusca deglandi ), we aimed to causally determine whether variation in baseline CORT drives individual body mass gains mediated through fattening rate (plasma triglycerides corrected for body mass). We implanted individuals with each of three treatment pellets to elevate CORT within a baseline range in a randomized order: control, low dose of CORT, high dose of CORT, then blood sampled and recorded body mass over a two-week period to track changes in baseline CORT, body mass, and fattening rates. The high CORT treatment significantly elevated levels of plasma hormone for a short period of time within the biologically relevant, baseline range for this species, but importantly did not inhibit the function of the HPA (hypothalamic&ndash;pituitary&ndash;adrenal) axis. Furthermore, an elevation in baseline CORT resulted in a consistent increase in body mass throughout the trial period compared to controls. This is some of the first empirical evidence demonstrating that elevations of baseline CORT within a biologically relevant range have a causal, direct, and positive influence on changes in body mass.

Ecology and Evolution

Larval exposure to 4-nonylphenol and 17β-estradiol affects physiological and behavioral development of seawater adaptation in Atlantic salmon smolts

Population declines of anadromous salmonids are attributed to anthropogenic disturbances including dams, commercial and recreational fisheries, and pollutants, such as estrogenic compounds. Nonylphenol (NP), a xenoestrogen, is widespread in the aquatic environment due to its use in agricultural, industrial, and household products. We exposed Atlantic salmon yolk-sac larvae to waterborne 10 or 100 &mu;g L -1 NP (NP-L or NP-H, respectively), 2 &mu;g L -1 17&beta;-estradiol (E 2 ), or vehicle, for 21 days to investigate their effects on smolt physiology and behavior 1 year later. NP-H caused approximately 50% mortality during exposure, 30 days after exposure, and 60 days after exposure. Mortality rates of NP-L and E 2 fish were not affected until 60 days after treatment, when they were 4-fold greater than those of controls. Treatment with NP-L or E 2 as yolk-sac larvae decreased gill sodium-potassium-activated adenosine triphosphatase (Na + ,K + -ATPase) activity and seawater (SW) tolerance during smolt development, 1 year after exposure. Exposure to NP-L and E 2 resulted in a latency to enter SW and reduced preference for SW approximately 2- and 5-fold, respectively. NP-L-exposed fish had 20% lower plasma insulin-like growth factor I (IGF-I) levels and 35% lower plasma triiodothyronine (T 3 ). Plasma growth hormone and thyroxine (T 4 ) were unaffected. Exposure to E 2 did not affect plasma levels of IGF-I, GH, T 3 , or T 4 . Both treatment groups exhibited increased plasma cortisol and decreased osmoregulatory capacity in response to a handling stressor. These results suggest that early exposure to environmentally relevant concentrations of NP, and other estrogenic compounds, can cause direct and delayed mortalities and that this exposure can have long term, &ldquo;organizational&rdquo; effects on life-history events in salmonids.

Environmental Science & Technology

Evidence That GABA Mediates Dopaminergic and Serotonergic Pathways Associated with Locomotor Activity in Juvenile Chinook Salmon (Oncorhynchus tshawytscha)

The authors examined the control of locomotor activity in juvenile salmon (Oncorhynchus tshawytscha) by manipulating 3 neurotransmitter systems-gamma-amino-n-butyric acid (GABA), dopamine, and serotonin-as well as the neuropeptide corticotropin releasing hormone (CRH). Intracerebroventricular (ICV) injections of CRH and the GABAAagonist muscimol stimulated locomotor activity. The effect of muscimol was attenuated by administration of a dopamine receptor antagonist, haloperidol. Conversely, the administration of a dopamine uptake inhibitor (4???,4??? -difluoro-3-alpha-[diphenylmethoxy] tropane hydrochloride [DUI]) potentiated the effect of muscimol. They found no evidence that CRH-induced hyperactivity is mediated by dopaminergic systems following concurrent injections of haloperidol or DUI with CRH. Administration of muscimol either had no effect or attenuated the locomotor response to concurrent injections of CRH and fluoxetine, whereas the GABAA antagonist bicuculline methiodide potentiated the effect of CRH and fluoxetine.

Behavioral Neuroscience