Publications by authors named "Ian Mayer"

41 Publications

Swimming exercise enhances brain plasticity in fish.

R Soc Open Sci 2020 Jan 15;7(1):191640. Epub 2020 Jan 15.

Department of Food Safety and Infection Biology, Norwegian University of Life Sciences, Oslo, Norway.

It is well-established that sustained exercise training can enhance brain plasticity and boost cognitive performance in mammals, but this phenomenon has not received much attention in fish. The aim of this study was to determine whether sustained swimming exercise can enhance brain plasticity in juvenile Atlantic salmon. Brain plasticity was assessed by both mapping the whole telencephalon transcriptome and conducting telencephalic region-specific microdissections on target genes. We found that 1772 transcripts were differentially expressed between the exercise and control groups. Gene ontology (GO) analysis identified 195 and 272 GO categories with a significant overrepresentation of up- or downregulated transcripts, respectively. A multitude of these GO categories was associated with neuronal excitability, neuronal signalling, cell proliferation and neurite outgrowth (i.e. cognition-related neuronal markers). Additionally, we found an increase in () after both three and eight weeks of exercise in the equivalent to the hippocampus in fish. Furthermore, the expression of the neural plasticity markers () and () were also increased due to exercise in the equivalent to the lateral septum in fish. In conclusion, this is the first time that swimming exercise has been directly linked to increased telencephalic neurogenesis and neural plasticity in a teleost, and our results pave the way for future studies on exercise-induced neuroplasticity in fish.
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http://dx.doi.org/10.1098/rsos.191640DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7029906PMC
January 2020

Neuroendocrine indicators of allostatic load reveal the impact of environmental acidification in fish.

Comp Biochem Physiol C Toxicol Pharmacol 2020 Mar 30;229:108679. Epub 2019 Nov 30.

Department of Food Safety and Infection Biology, Norwegian University of Life Sciences, 0454 Oslo, Norway.

When mobilized from surrounding soils and binding to gills at moderately low pH, aluminum (Al) cations can adversely affect fish populations. Furthermore, acidification may lead to allostatic overload, a situation in which the costs of coping with chronic stress affects long-term survival and reproductive output and, ultimately, ecosystem health. The brain's serotonergic system plays a key role in neuroendocrine stress responses and allostatic processes. Here, we explored whether sublethal effects of Al in acidified water affects serotonergic neurochemistry and stress coping ability in a unique land-locked salmon population from Lake Bygelandsfjorden, in southern Norway. Fish were exposed to untreated water with pH 6.5 and 74 μg Al l or acidified (pH 5.5) water with different aluminum concentrations ([Al]; 74-148 μg l) for 5-6 days. Afterward, effects on stress coping ability were investigated by analyzing plasma cortisol levels and telencephalic serotonergic neurochemistry before and after a standardized acute stress test. Before the stress test, positive dose-response relationships existed between [Al], serotonergic turnover rate and plasma cortisol. However, in acutely stressed fish, exposure to the highest [Al] resulted in reduced cortisol values compared with those exposed to lower concentrations, while the positive dose-response relationship between Al concentrations and serotonergic turnover rate persisted in baseline conditions. This suggests that fish exposed to the highest Al concentration were unable to mount a proper cortisol response to further acute stress, demonstrating that neuroendocrine indicators of allostatic load can be used to reveal sublethal effects of water acidification-and potentially, the environmental impacts of other factors.
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http://dx.doi.org/10.1016/j.cbpc.2019.108679DOI Listing
March 2020

Effects of environmental enrichment on forebrain neural plasticity and survival success of stocked Atlantic salmon.

J Exp Biol 2019 12 4;222(Pt 23). Epub 2019 Dec 4.

Uni Environment, Uni Research AS, 5008 Bergen, Norway

Fish reared for stocking programmes are severely stimulus deprived compared with their wild conspecifics raised under natural conditions. This leads to reduced behavioural plasticity and low post-release survival of stocked fish. Environmental enrichment can have positive effects on important life skills, such as predator avoidance and foraging behaviour, but the neural mechanisms underpinning these behavioural changes are still largely unknown. In this study, juvenile Atlantic salmon () were reared in an enriched hatchery environment for 7 weeks, after which neurobiological characteristics and post-release survival were compared with those of fish reared under normal hatchery conditions. Using hybridization and qPCR, we quantified the expression of () and the neural activity marker in telencephalic subregions associated with relational memory, emotional learning and stress reactivity. Aside from lower expression of in the Dlv (a region associated with relational memory) of enriched salmon, we observed no other significant effects of enrichment in the studied regions. Exposure to an enriched environment increased post-release survival during a 5 month residence in a natural river by 51%. Thus, we demonstrate that environmental enrichment can improve stocking success of Atlantic salmon parr and that environmental enrichment is associated with changes in expression in the fish's hippocampus-equivalent structure.
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http://dx.doi.org/10.1242/jeb.212258DOI Listing
December 2019

The Role of Reproductive Sciences in the Preservation and Breeding of Commercial and Threatened Teleost Fishes.

Authors:
Ian Mayer

Adv Exp Med Biol 2019 ;1200:187-224

Norwegian University of Life Sciences, Faculty of Veterinary Medicine, Oslo, Norway.

The teleost fishes are the largest and most diverse vertebrate group, accounting for nearly half of all known vertebrate species. Teleost fish exhibit greater species diversity than any other group of vertebrates and this is reflected in the unique variety of different reproductive strategies displayed by fish. Fish have always been an important resource for humans worldwide, especially as food. While wild capture fisheries have historically been the main source of fish, the farming of fish (aquaculture) is increasingly becoming the more dominant source of food fish, and is predicted to account for 60% of total global fish production by 2030.Fishes are increasingly threatened by a wide range of anthropogenic impacts, including loss of habitat, pollution, invasive species and over-exploitation. In addition, climate change, especially the consequences of global warming, can impact fish at all levels of biological organization from the individual to the population level, influencing both physiological and ecological processes in a variety of direct and indirect ways. As such, there is an urgent need to protect and conserve the huge genetic diversity offered by this diverse vertebrate group, not just as a source of genes for contemporary breeding and for protection against the consequences of climate change and disease, but also as part of our national heritage. While the cryopreservation of reproductive cells is a means of achieving these objectives, currently only fish sperm can be successfully frozen. Due to their large size, large yolk compartment, low membrane permeability and high chilling sensitivity, successful and reproducible protocols for the cryopreservation of fish oocytes and embryos still remains elusive. However, significant advances have been made in the cryopreservation of primordial germ cells as an alternative means of conserving both paternal and maternal genomes. Although more research needs to be carried out on how these cells can be optimally applied to emerging reproductive technologies, including transplantation techniques and surrogate broodstock technologies, the successful cryopreservation of fish germ cells, and the establishment of genetic resource banks, offers the possibility of both conserving and restoring threatened species. Further, current and future conservation efforts need to consider the impact of climate change in both in situ conservation and reintroduction efforts.In conclusion, it is anticipated that the successful cryopreservation of fish germplasm will result in a range of economic, ecological and societal benefits. In partnership with emerging assisted reproductive technologies, the successful cryopreservation of fish germplasm will lead to more efficient reproduction in aquaculture, assist selective breeding programmes, and be of crucial importance to future species conservation actions.
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http://dx.doi.org/10.1007/978-3-030-23633-5_7DOI Listing
September 2019

Establishment of specific enzyme-linked immunosorbent assay (ELISA) for measuring Fsh and Lh levels in medaka (), using recombinant gonadotropins.

MethodsX 2019 17;6:1473-1479. Epub 2019 Jun 17.

Department of Basic Sciences and Aquatic Medicine, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, Norway.

The paucity of information on understanding the regulatory mechanisms that are involved in the control of piscine Fsh and Lh synthesis, secretion, and function, prompted the present work. Part of the problem is related to the molecular heterogeneity and the unavailability of Fsh and Lh assays for quantifying gonadotropins, in particular assays regarding the measurement of Fsh, and such assays are available today for only a few teleost species. The present study reports the development and validation of competitive ELISAs for quantitative determination of medaka Fsh and Lh by first producing medaka recombinant (md) gonadotropins mdFshβ, mdLhβ, mdFshβα, and mdLhβα by generating specific antibodies against their respective β subunits, and their use within the development of ELISAs. The advantages of this protocol include: •The reproducibility of the ELISA demonstrated was relatively high, as shown by reasonably low intra- (Fsh 2.7%, Lh 3%) and interassay CVs (Fsh 5.3%, Lh 5.7%).•The high degree of parallelism between serial dilutions of the recombinant and native pituitary-derived Fsh and Lh, may be a sign of similar structures and immunologically similarity.•Two new competitive ELISAs for the quantification of medaka Fsh and Lh were established for the first time.
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http://dx.doi.org/10.1016/j.mex.2019.06.011DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6594921PMC
June 2019

Melatonin receptors in Atlantic salmon stimulate cAMP levels in heterologous cell lines and show season-dependent daily variations in pituitary expression levels.

J Pineal Res 2019 Oct 23;67(3):e12590. Epub 2019 Jun 23.

Department of Basic Sciences and Aquatic Medicine, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, Oslo, Norway.

The hormone melatonin connects environmental cues, such as photoperiod and temperature, with a number of physiological and behavioural processes, including seasonal reproduction, through binding to their cognate receptors. This study reports the structural, functional and physiological characterization of five high-affinity melatonin receptors (Mtnr1aaα, Mtnr1aaβ, Mtnr1ab, Mtnr1al, Mtnr1b) in Atlantic salmon. Phylogenetic analysis clustered salmon melatonin receptors into three monophyletic groups, Mtnr1A, Mtnr1Al and Mtnr1B, but no functional representative of the Mtnr1C group. Contrary to previous studies in vertebrates, pharmacological characterization of four receptors in COS-7, CHO and SH-SY5Y cell lines (Mtnr1Aaα, Mtnr1Aaβ, Mtnr1Ab, Mtnr1B) showed induction of intracellular cAMP levels following 2-iodomelatonin or melatonin exposure. No consistent response was measured after N-acetyl-serotonin or serotonin exposure. Melatonin receptor genes were expressed at all levels of the hypothalamo-pituitary-gonad axis, with three genes (mtnr1aaβ, mtnr1ab and mtnr1b) detected in the pituitary. Pituitary receptors displayed daily fluctuations in mRNA levels during spring, prior to the onset of gonadal maturation, but not in autumn, strongly implying a direct involvement of melatonin in seasonal processes regulated by the pituitary. To the best of our knowledge, this is the first report of cAMP induction mediated via melatonin receptors in a teleost species.
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http://dx.doi.org/10.1111/jpi.12590DOI Listing
October 2019

Data on Western blot and ELISA analysis of medaka () follicle-stimulating hormone (Fsh) and luteinizing hormone (Lh) using recombinant proteins expressed with .

Data Brief 2019 Feb 19;22:1057-1063. Epub 2019 Jan 19.

Department of Basic Sciences and Aquatic Medicine, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, Norway.

The gonadotropins follicle-stimulating hormone (Fsh) and luteinizing hormone (Lh) play essential roles in vertebrate reproduction. This article presents data on molecular weight validation of recombinant medaka () (md) gonadotropins Fshβ (mdFshβ), Lhβ (mdLhβ), Fshβα (mdFshβα), and Lhβα (mdLhβα) generated by as well as data on a validation of produced antibodies against Fshβ and Lhβ by Western blot analysis. Furthermore, the article includes data on Fsh and Lh protein levels in male medaka pituitaries using recombinant mdFshβα and mdLhβα within enzyme-linked immunosorbent assays (ELISAs), in which protein amounts were analyzed related to body weight and age of the fish. This dataset is associated with the research article entitled "Medaka Follicle-stimulating hormone (Fsh) and Luteinizing hormone (Lh): Developmental profiles of pituitary protein and gene expression" (Burow et al., in press).
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http://dx.doi.org/10.1016/j.dib.2019.01.034DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6355963PMC
February 2019

Medaka follicle-stimulating hormone (Fsh) and luteinizing hormone (Lh): Developmental profiles of pituitary protein and gene expression levels.

Gen Comp Endocrinol 2019 02 18;272:93-108. Epub 2018 Dec 18.

Department of Basic Sciences and Aquatic Medicine, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, Norway. Electronic address:

The two gonadotropins follicle-stimulating hormone (Fsh) and luteinizing hormone (Lh) are of particular importance within the hypothalamic-pituitary-gonadal (HPG) axis of vertebrates. In the current study, we demonstrate the production and validation of Japanese medaka (Oryzias latipes) recombinant (md) gonadotropins Fshβ (mdFshβ), Lhβ (mdLhβ), Fshβα (mdFshβα), and Lhβα (mdLhβα) by Pichia pastoris, the generation of specific rabbit antibodies against their respective β subunits, and their use within the development and validation of competitive enzyme-linked immunosorbent assays (ELISAs) for quantification of medaka Fsh and Lh. mdFsh and mdLh were produced as single-chain polypeptides by linking the α subunit with mdFshβ or mdLhβ mature protein coding sequences to produce a "tethered" polypeptide with the β-chain at the N-terminal and the α-chain at the C-terminal. The specificity of the antibodies raised against mdFshβ and mdLhβ was determined by immunofluorescence (IF) for Fshβ and Lhβ on medaka pituitary tissue, while comparison with fluorescence in situ hybridization (FISH) for fshb and lhb mRNA was used for validation. Competitive ELISAs were developed using antibodies against mdFshβ or mdLhβ, and the tethered proteins mdFshβα or mdLhβα for standard curves. The standard curve for the Fsh ELISA ranged from 97.6 pg/ml to 50 ng/ml, and for the Lh ELISA from 12.21 pg/ml to 6.25 ng/ml. The sensitivity of the assays for Fsh and Lh was 44.7 and 70.8 pg/ml, respectively. A profile of pituitary protein levels of medaka Fsh and Lh comparing juveniles with adults showed significant increase of protein amount from juvenile group (body length from 12 mm to 16.5 mm) to adult group (body length from 21 mm to 26.5 mm) for both hormones in male medaka. Comparing these data to a developmental profile of pituitary mRNA expression of medaka fshb and lhb, the mRNA expression of lhb also increased during male maturation and a linear regression analysis revealed a significant increase of lhb expression with increased body length that proposes a linear model. However, fshb mRNA expression did not change significantly during male development and therefore was not correlated with body length. In summary, we have developed and validated homologous ELISA assays for medaka Fsh and Lh based on proteins produced in P. pastoris, assays that will be used to study the functions and regulations of Fsh and Lh in more detail.
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http://dx.doi.org/10.1016/j.ygcen.2018.12.006DOI Listing
February 2019

Sub-lethal UV radiation during early life stages alters the behaviour, heart rate and oxidative stress parameters in zebrafish (Danio rerio).

Ecotoxicol Environ Saf 2018 Dec 1;166:359-365. Epub 2018 Oct 1.

Centre for Environmental Radioactivity (CERAD CoE), NMBU, 1433 Ås, Norway; Norwegian Radiation Protection Authority, P.O. Box 329 Skøyen, 0213 Oslo, Norway.

Environmental UV radiation in sufficient doses, as a possible consequence of climate change, is potent enough to affect living organisms with different outcomes, depending on the exposure life stage. The aim of this project was to evaluate the potentially toxic effects of exposure to sub-lethal and environmentally relevant doses of UVA (9.4, 18. 7, 37.7 J/cm) and UVB radiation (0.013, 0.025, 0.076 J/cm) on the development and behaviour in early life stages (4.5-5.5 h post fertilization, hpf) of the zebrafish (Danio rerio). The used doses were all below the median lethal dose (LD) and caused no significant difference in survival, deformities, or hatching between exposed and control groups. Compared to controls, there were transient UVA and UVB exposure effects on heart rate, with dose dependent reductions at 50 hpf, and at 60 hpf for UVA only. The UVB exposure caused an increasing trend in reactive oxygen species (ROS) formation at the two highest doses, even though only significant at 120 hpf for the second highest dose. Both UVA and UVB caused an increasing trend in lipid peroxidation (LPO) at the highest doses tested at 72 hpf. Furthermore, UVA exposure led to significant reductions in larval movement following exposure to the two highest doses of UVA, i.e., reduction in the time spent active and the total distance moved compared to control at 100 hpf, while no effect on the swimming speed was observed. The lowest dose of UVA had no effect on behaviour. In contrast, the highest dose of UVB led to a possible increase in the time spent active and a slower average swimming speed although these effects were not significant (p = 0.07). The obtained results show that UV doses below LD levels are able to cause changes in the behaviour and physiological parameters of zebrafish larvae, as well as oxidative stress in the form of ROS formation and LPO. Further testing is necessary to assess how this type of radiation and the effects observed could affect fish population dynamics.
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http://dx.doi.org/10.1016/j.ecoenv.2018.09.082DOI Listing
December 2018

Neurobiology of Wild and Hatchery-Reared Atlantic Salmon: How Nurture Drives Neuroplasticity.

Front Behav Neurosci 2018 11;12:210. Epub 2018 Sep 11.

Uni Environment, Uni Research AS, Bergen, Norway.

Life experiences in the rearing environment shape the neural and behavioral plasticity of animals. In fish stocking practices, the hatchery environment is relatively stimulus-deprived and does not optimally prepare fish for release into the wild. While the behavioral differences between wild and hatchery-reared fish have been examined to some extent, few studies have compared neurobiological characteristics between wild and hatchery-reared individuals. Here, we compare the expression of immediate early gene and neuroplasticity marker brain-derived neurotrophic factor () in telencephalic subregions associated with processing of stimuli in wild and hatchery-reared Atlantic salmon at basal and 30 min post (acute) stress conditions. Using hybridization, we found that the expression level of these markers is highly specific per neuronal region and affected by both the origin of the fish, and exposure to acute stress. Expression of was increased by stress in all brain regions and was more highly expressed in the Dlv (functional equivalent to the mammalian hippocampus) of hatchery-reared compared to wild fish. Expression of was higher overall in hatchery fish, while acute stress upregulated in the Dm (functional equivalent to the mammalian amygdala) of wild, but not hatchery individuals. Our findings demonstrate that the hatchery environment affects neuroplasticity and neural activation in brain regions that are important for learning processes and stress reactivity, providing a neuronal foundation for the behavioral differences observed between wild and hatchery-reared fish.
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http://dx.doi.org/10.3389/fnbeh.2018.00210DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6141658PMC
September 2018

Gamma irradiation during gametogenesis in young adult zebrafish causes persistent genotoxicity and adverse reproductive effects.

Ecotoxicol Environ Saf 2018 Jun 22;154:19-26. Epub 2018 Feb 22.

Centre for Environmental Radioactivity (CERAD CoE), NMBU, 1433 Ås, Norway; Norwegian University of Life Sciences (NMBU), Faculty of Veterinary Medicine and Biosciences, P.O. Box 8146 Dep., 0033 Oslo, Norway.

The biological effects of gamma radiation may exert damage beyond that of the individual through its deleterious effects on reproductive function. Impaired reproductive performance can result in reduced population size over consecutive generations. In a continued effort to investigate reproductive and heritable effects of ionizing radiation, we recently demonstrated adverse effects and genomic instability in progeny of parents exposed to gamma radiation. In the present study, genotoxicity and effects on the reproduction following subchronic exposure during a gametogenesis cycle to Co gamma radiation (27 days, 8.7 and 53 mGy/h, total doses 5.2 and 31 Gy) were investigated in the adult wild-type zebrafish (Danio rerio). A significant reduction in embryo production was observed one month after exposure in the 53 mGy/h exposure group compared to control and 8.7 mGy/h. One year later, embryo production was significantly lower in the 53 mGy/h group compared only to control, with observed sterility, accompanied by a regression of reproductive organs in 100% of the fish 1.5 years after exposure. Histopathological examinations revealed no significant changes in the testis in the 8.7 mGy/h group, while in 62.5% of females exposed to this dose rate the oogenesis was found to be only at the early previtellogenic stage. The DNA damage determined in whole blood, 1.5 years after irradiation, using a high throughput Comet assay, was significantly higher in the exposed groups (1.2 and 3-fold increase in 8.7 and 53 mGy/h females respectively; 3-fold and 2-fold increase in 8.7 and 53 mGy/h males respectively) compared to controls. A significantly higher number of micronuclei (4-5%) was found in erythrocytes of both the 8.7 and 53 mGy/h fish compared to controls. This study shows that gamma radiation at a dose rate of ≥ 8.7 mGy/h during gametogenesis causes adverse reproductive effects and persistent genotoxicity (DNA damage and increased micronuclei) in adult zebrafish.
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http://dx.doi.org/10.1016/j.ecoenv.2018.02.031DOI Listing
June 2018

Hormonal changes over the spawning cycle in the female three-spined stickleback, Gasterosteus aculeatus.

Gen Comp Endocrinol 2018 02 2;257:97-105. Epub 2017 Aug 2.

Department of Zoology, Stockholm University, Stockholm, Sweden.

Female three-spined sticklebacks are batch spawners laying eggs in a nest built by the male. We sampled female sticklebacks at different time points, when they were ready to spawn and 6, 24, 48 and 72h post-spawning (hps) with a male. Following spawning, almost all females (15 out of 19) had ovulated eggs again at Day 3 post-spawning (72hps). At sampling, plasma, brain and pituitaries were collected, and the ovary and liver were weighed. Testosterone (T) and estradiol (E2) were measured by radioimmunoassay. Moreover, the mRNA levels of follicle-stimulating hormone (fsh-β) and luteinizing hormone (lh-β) in the pituitary, and of the gonadotropin-releasing hormones (GnRHs: gnrh2, gnrh3) and kisspeptin (kiss2) and its G protein-coupled receptor (gpr54) in the brain were measured by real-time qPCR. Ovarian weights peaked in "ready to spawn" females, dropped after spawning, before again progressively increasing from 6 to 72hps. Plasma T levels showed peaks at 24 and 48hps and decreased at 72hps, while E2 levels increased already at 6hps and remained at high levels up to 48hps. There was a strong positive correlation between T and E2 levels over the spawning cycle. Pituitary lh-β mRNA levels showed a peak at 48hps, while fsh-β did not change. The neuropeptides and gpr54 did not show any changes. The changes in T and E2 over the stickleback spawning cycle were largely consistent with those found in other multiple-spawning fishes whereas the marked correlation between T and E2 does not support T having other major roles over the cycle than being a precursor for E2.
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http://dx.doi.org/10.1016/j.ygcen.2017.07.030DOI Listing
February 2018

Dietary l-tryptophan leaves a lasting impression on the brain and the stress response.

Br J Nutr 2017 May 19;117(10):1351-1357. Epub 2017 Jun 19.

10BioMar AS,Nordre gate 11,7011 Trondheim,Norway.

Comparative models suggest that effects of dietary tryptophan (Trp) on brain serotonin (5-hydroxytryptamine; 5-HT) neurochemistry and stress responsiveness are present throughout the vertebrate lineage. Moreover, hypothalamic 5-HT seems to play a central role in control of the neuroendocrine stress axis in all vertebrates. Still, recent fish studies suggest long-term effects of dietary Trp on stress responsiveness, which are independent of hypothalamic 5-HT. Here, we investigated if dietary Trp treatment may result in long-lasting effects on stress responsiveness, including changes in plasma cortisol levels and 5-HT neurochemistry in the telencephalon and hypothalamus of Atlantic salmon. Fish were fed diets containing one, two or three times the Trp content in normal feed for 1 week. Subsequently, fish were reintroduced to control feed and were exposed to acute crowding stress for 1 h, 8 and 21 d post Trp treatment. Generally, acute crowding resulted in lower plasma cortisol levels in fish treated with 3×Trp compared with 1×Trp- and 2×Trp-treated fish. The same general pattern was reflected in telencephalic 5-HTergic turnover, for which 3×Trp-treated fish showed decreased values compared with 2×Trp-treated fish. These long-term effects on post-stress plasma cortisol levels and concomitant 5-HT turnover in the telencephalon lends further support to the fact that the extrahypothalamic control of the neuroendocrine stress response is conserved within the vertebrate lineage. Moreover, they indicate that trophic/structural effects in the brain underlie the effects of dietary Trp treatment on stress reactivity.
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http://dx.doi.org/10.1017/S0007114517001428DOI Listing
May 2017

Effects of temperature on the final stages of sexual maturation in Atlantic salmon (Salmo salar L.).

Fish Physiol Biochem 2016 Jun 21;42(3):895-907. Epub 2015 Dec 21.

Institute of Marine Research (IMR), 5005, Bergen, Norway.

Maturing male and female Atlantic salmon (Salmo salar L.) were held under three temperature regimes for 10 weeks between September and December: warm (constant 14-16 °C), ambient (decreasing from 11 to 5 °C), and cold (decreasing from 7 to 3 °C). Blood samples were analyzed for plasma steroid levels, and the fish were inspected for the presence of expressible milt (total volume and spermatocrit) and ovulation weekly. Samples of eggs were dry-fertilized with milt stripped from three males held at the same temperatures and incubated until the eyed stage. In females, levels of plasma testosterone (T) and 17β-oestradiol (E2) dropped as ovulation approached, concurrent with a rapid increase in levels of plasma 17α,20β-dihydroxy-4-pregnen-3-one (17,20β-P). In males, levels of T and 11-ketotestosterone (11-KT) peaked 2-3 weeks after the first appearance of expressible milt, while levels of 17,20β-P increased steadily and did not exhibit a definite peak. Exposure of females to cold water amplified and advanced the profiles of all three steroids compared with the ambient group, and increased the survival rates to the eyed egg stage. Cold water had no immediate effect on the male steroid profiles, but later, higher levels of 17,20β-P were evident compared with both the ambient controls and the warm water group, while the effects on 11-KT and T were more variable. Exposure to warm water completely inhibited both milt production and ovulation. Moreover, warm water modulated the steroid profiles of the males with lower 11-KT levels compared with ambient controls and lower 17,20β-P level compared with cold-water-treated males. In females, warm water resulted in total inhibition of the peri-ovulatory peak in 17,20β-P and prevented the normal decline of T and E2 levels associated with ovulation. The findings of the present study are highly relevant for broodstock management in aquaculture, as well in understanding the impact of climate change/temperature variability on wild salmon spawning.
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http://dx.doi.org/10.1007/s10695-015-0183-1DOI Listing
June 2016

Increased reactivity and monoamine dysregulation following stress in triploid Atlantic salmon (Salmo salar).

Comp Biochem Physiol A Mol Integr Physiol 2015 Jul 14;185:125-31. Epub 2015 Apr 14.

Faculty of Veterinary Medicine and Biosciences, Norwegian University of Life Sciences, Oslo, Norway.

Artificial triploid salmonids are sterile and therefore commercially bred to prevent genetic interactions between wild and domestic fish strains. The full biological effects of having an extra chromosome set are largely unknown, but triploids are considered to be more sensitive to sub-optimal environmental conditions and to be stressed by the presence of diploid conspecifics. Brain serotonergic and dopaminergic activity are known to regulate the stress response in vertebrates, but monoamine systems in diploid and triploid fish have yet to be compared. Here we study monoamine neurochemistry in the telencephalon and brain stem of juvenile diploid and triploid Atlantic salmon (Salmo salar) in response to stress (unstressed vs stressed individuals) and holding (separate- vs mixed-ploidy) conditions. Both diploids and triploids showed an increase in serotonergic activity following stress, but the increase was significantly greater in the telencephalon of triploids compared to diploids. Furthermore, while telencephalic dopaminergic activity was significantly increased in diploids following stress, there was no response in triploids. Holding conditions had a significant effect on dopaminergic activity in the brain stem of diploids only, with lower values in mixed- compared to separate-ploidy conditions. These results suggest artificially produced triploids experience increased reactivity and monoaminergic dysregulation following stress that may impede their welfare and performance.
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http://dx.doi.org/10.1016/j.cbpa.2015.04.004DOI Listing
July 2015

In vivo endocrine effects of naphthenic acids in fish.

Chemosphere 2013 Nov 12;93(10):2356-64. Epub 2013 Sep 12.

Department of Biology, University of Bergen, Bergen, Norway. Electronic address:

Oil pollution from various sources, including exploration, production and transportation, is a growing global concern. The highest toxicity of hydrocarbon pollutants is associated with the water-soluble phase compounds, including naphthenic acids, a known component found in all hydrocarbon deposits. Recently, naphthenic acids (NAs) have shown estrogenic and anti-androgenic effects in vitro. For this reason we investigated the potential effects of two commercial mixtures of naphthenic acids on fish in vivo, using the three-spined stickleback (Gasterosteus aculeatus) as a model species. Anti-androgenic and estrogenic properties of tested compounds were evaluated using the androgenized female stickleback screen (AFSS) and a variant of the 21-d fish screen (TG230) respectively. One-dimensional gas chromatography-mass spectrometry (GC-MS) showed that the complex commercial NAs mixtures were dominated by acyclic carboxylic acids. In one experiment (freshwater) we found a clear effect of NA exposure on spiggin levels; this was contrary to our hypothesis since NAs enhanced the androgenic potency of DHT (when co-administered) without inducing spiggin when tested in the absence of DHT. Exposure to NAs did not have a statistically significant effect on vitellogenin (Vtg) production in male stickleback, although the Vtg responses were increasing with increasing exposure concentrations. This study shows that in contrast to previous in vitro data, NAs did not exhibit either estrogenic or anti-androgenic properties in vivo, at the concentrations tested. On the contrary, at least in freshwater, NAs appear to have an overall androgenic effect that is not mediated via the androgen receptor involved in spiggin synthesis. Possible reasons for this discrepancy between in vitro and in vivo results as well as between our studies are discussed.
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http://dx.doi.org/10.1016/j.chemosphere.2013.08.033DOI Listing
November 2013

Effects of polar oil related hydrocarbons on steroidogenesis in vitro in H295R cells.

Chemosphere 2013 Jun 2;92(1):106-15. Epub 2013 Apr 2.

Department of Biology, University of Bergen, P.O. Box 7803, N-5020 Bergen, Norway.

Oil pollution from various sources, including exploration, production and transportation, is a growing global concern. Of particular concern is the environmental impact of produced water (PW), the main waste discharge from oil and gas platforms. In this study, we have investigated the potential of polar hydrocarbon pollutants to disrupt or modulate steroidogenesis in vitro, using a human adrenocortical carcinoma cell line, the H295R assay. Effects of two of the major groups of compounds found in the polar fraction of crude oil and PW; alkylphenols (C(2)- and C(3)-AP) and naphthenic acids (NAs), as well as the polar fraction of PW as a whole has been assessed. Endpoints include hormone (cortisol, estradiol, progesterone, testosterone) production at the functional level and key genes for steroidogenesis (17β-HSD1, 17β-HSD4, 3β-HSD2, ACTHR, CYP11A1, CYP11B1, CYP11B2, CYP17, CYP19, CYP21, DAX1, EPHX, HMGR, SF1, STAR) and metabolism (CYP1A) at the molecular level. All compounds induced the production of both estradiol and progesterone in exposed H295R cells, while the C(3)-AP and NAs decreased the production of testosterone. Exposure to C(2)-AP caused an up-regulation of DAX1 and EPHX, while exposure to NAs caused an up-regulation of ACTHR. All compounds caused an up-regulation of CYP1A1. The results indicated that these hydrocarbon pollutants, including PW, have the potential to disrupt the vitally important process of steroidogenesis.
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http://dx.doi.org/10.1016/j.chemosphere.2013.02.046DOI Listing
June 2013

Changes in regional brain monoaminergic activity and temporary down-regulation in stress response from dietary supplementation with l-tryptophan in Atlantic cod (Gadus morhua).

Br J Nutr 2013 Jun 2;109(12):2166-74. Epub 2012 Nov 2.

Department of Basic Sciences and Aquatic Medicine, Norwegian School of Veterinary Science, P.O. Box 8146 Dep, 0033 Oslo, Norway.

The brain monoamines serotonin (5-hydroxytryptamine; 5-HT) and dopamine (DA) both play an integrative role in behavioural and neuroendocrine responses to challenges, and comparative models suggest common mechanisms for dietary modulation of transmission by these signal substances in vertebrates. Previous studies in teleosts demonstrate that 7 d of dietary administration with L-tryptophan (Trp), the direct precursor of 5-HT, suppresses the endocrine stress response. The present study investigated how long the suppressive effects of a Trp-enriched feed regimen, at doses corresponding to two, three or four times the Trp levels in commercial feed, last in juvenile Atlantic cod (Gadus morhua) when the fish are reintroduced to a diet with standard amino acid composition. We also wanted to determine whether Trp supplementation induced changes in brain monoaminergic neurochemistry in those forebrain structures innervated by DA and 5-HTergic neurons, by measuring regional activity of DA and 5-HT in the lateral pallial regions (Dl) of the telencephalon and nucleus lateralis tuberis (NLT) of the hypothalamus. Dietary Trp resulted in a dose-dependent suppression in plasma cortisol among fish exposed to confinement stress on the first day following experimental diet; however, such an effect was not observed at 2 or 6 d after Trp treatment. Feeding the fish with moderate Trp doses also evoked a general increase in DA and 5-HT-ergic activity, suggesting that these neural circuits within the NLT and Dl may be indirectly involved in regulating the acute stress response.
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http://dx.doi.org/10.1017/S0007114512004345DOI Listing
June 2013

Omission of expected reward agitates Atlantic salmon (Salmo salar).

Anim Cogn 2012 Sep 24;15(5):903-11. Epub 2012 May 24.

Norwegian University of Life Sciences, 1432, Ås, Norway.

The evolutionary background for cognition and awareness is currently under ardent scrutiny. Poikilothermic vertebrates such as teleost fishes are capable of classical conditioning and have long-term memories, but it remains unknown to what degree such capabilities are associated with affective states. Here, we investigate whether the concept of frustration may apply to Atlantic salmon. In mammals, this paradigm comprises the omission of an expected reward (OER), which elicits behavioural and physiological coping responses (e.g. aggression and stress reactions). Six groups with 200 fish in each were conditioned to associate a flashing light (CS) with feeding. Conditioning over 22 days led to a change from aversion to attraction to the CS. Subsequently, 3 groups served as control, and 3 groups were subjected to an OER paradigm for 9 days, in which the expected food reward was delayed for 30 min during two out of three daily meals. Compared to controls, OER groups displayed higher levels of aggression and more heterogeneous growth rates, indicating a more pronounced social hierarchy. Cortisol levels did, however, not differ between treatments and both groups responded similarly to acute stress. These results indicate that teleost fishes, like mammals, respond aggressively to OER. The capacity to respond behaviourally to frustrating conditions thus likely reflects an adaptive response to environmental unpredictability, which has been conserved throughout vertebrate evolution.
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http://dx.doi.org/10.1007/s10071-012-0517-7DOI Listing
September 2012

The effect of triploidy and vaccination on neutrophils and B-cells in the peripheral blood and head kidney of 0+ and 1+ Atlantic salmon (Salmo salar L.) post-smolts.

Fish Shellfish Immunol 2012 Jul 17;33(1):60-6. Epub 2012 Apr 17.

Department of Production Animal Clinical Sciences, Norwegian School of Veterinary Science, PO Box 8146 Dep, 0033 Oslo, Norway.

Sterile triploid fish are being used in aquaculture to prevent early unwanted sexual maturation and the genetic interaction between wild and cultured fish; however, triploid fish are typically considered to be more susceptible to disease than diploid counterparts. Proportions of leucocytes from the head kidney and peripheral blood were identified using monoclonal antibodies and flow cytometry in triploid and diploid, vaccinated and unvaccinated, out-of-season (0+) and 1+ Atlantic salmon (Salmo salar L.) three weeks post seawater transfer. Triploid 1+ fish were significantly (P<0.05) heavier than diploid fish at the time of sampling, whereas triploid 0+ had a significantly lower condition factor than diploids. Ploidy had a significant effect on the proportion of B-cells in the blood of both 0+ and 1+ fish, and the head kidney of 1+ fish, with triploids having lower proportions of B-cells to diploids in both smolt groups. In addition, a significant ploidy×vaccination interaction effect was observed in the response of neutrophils in the blood (vaccinated diploids had a higher mean proportion than diploid unvaccinated) and B-cells in the head kidney (in vaccinated fish, triploids had a lower mean proportion than diploids) in 0+ smolts. Vaccination was found to significantly increase the proportion of B-cells in the head kidney of 1+ smolts in both ploidy. Size (fish weight) was positively correlated with neutrophil proportions in 1+ fish. Our findings are discussed in relation to the physiological differences related to ploidy. The results suggest that ploidy as well as smelting regime influences the immune system of Atlantic salmon post-smolts.
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http://dx.doi.org/10.1016/j.fsi.2012.04.001DOI Listing
July 2012

Multidimensionality of behavioural phenotypes in Atlantic cod, Gadus morhua.

Physiol Behav 2012 Jun 16;106(4):462-70. Epub 2012 Mar 16.

Department of Biology, University of Bergen, Norway.

Much of the inter-individual variation observed in animal behaviour is now attributed to the existence of behavioural phenotypes or animal personalities. Such phenotypes may be fundamental to fisheries and aquaculture, yet there have been few detailed studies of this phenomenon in exploited marine animals. We investigated the behavioural and neuroendocrine responses of Atlantic cod (Gadus morhua L.), to situations reflecting critical ecological challenges: predator attacks and territorial challenges. Both hatchery-reared and wild fish were tested and behavioural profiles were compared with baseline conditions. We then used an objective, multivariate approach, rather than assigning individuals along one-dimensional behavioural axes, to examine whether distinct behavioural phenotypes were present. Our results indicate that two distinct behavioural phenotypes were evident in fish from each background. In hatchery-reared fish, phenotypes displayed divergent locomotor activity, sheltering, brain monoamine concentrations and responses to competitive challenges. In wild fish, phenotypes were distinguished primarily by locomotor activity, sheltering and responsiveness to predator stimuli. Hatcheries presumably represent a more stressful social environment, and social behaviour and neuroendocrine responses were important in discerning behavioural phenotypes in hatchery fish, whereas antipredator responses were important in discerning phenotypes in wild fish that have previously encountered predators. In both fish types, behavioural and physiological traits that classified individuals into phenotypes were not the same as those that were correlated across situations. These results highlight the multidimensionality of animal personalities, and that the processes that regulate one suite of behavioural traits may be very different to the processes that regulate other behaviours.
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http://dx.doi.org/10.1016/j.physbeh.2012.03.010DOI Listing
June 2012

The culturable intestinal microbiota of triploid and diploid juvenile Atlantic salmon (Salmo salar) - a comparison of composition and drug resistance.

BMC Vet Res 2011 Nov 17;7:71. Epub 2011 Nov 17.

Department of Food Safety and Infection Biology, Norwegian School of Veterinary Science, Oslo, Norway.

Background: With the increased use of ploidy manipulation in aquaculture and fisheries management this investigation aimed to determine whether triploidy influences culturable intestinal microbiota composition and bacterial drug resistance in Atlantic salmon (Salmo salar). The results could provide answers to some of the physiological differences observed between triploid and diploid fish, especially in terms of fish health.

Results: No ploidy effect was observed in the bacterial species isolated, however, triploids were found to contain a significant increase in total gut microbiota levels, with increases in Pseudomonas spp., Pectobacterium carotovorum, Psychrobacter spp., Bacillus spp., and Vibrio spp., (12, 42, 9, 10, and 11% more bacteria in triploids than diploids, respectively), whereas a decrease in Carnobacterium spp., within triploids compared to diploids was close to significant (8% more bacteria in diploids). With the exception of gentamicin, where no bacterial resistance was observed, bacterial isolates originating from triploid hosts displayed increased resistance to antibacterials, three of which were significant (tetracycline, trimethoprim, and sulphonamide).

Conclusion: Results indicate that triploidy influences both the community and drug resistance of culturable intestinal microbiota in juvenile salmon. These results demonstrate differences that are likely to contribute to the health of triploid fish and have important ramifications on the use of antibacterial drugs within aquaculture.
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http://dx.doi.org/10.1186/1746-6148-7-71DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3239839PMC
November 2011

Detection of the anti-androgenic effect of endocrine disrupting environmental contaminants using in vivo and in vitro assays in the three-spined stickleback.

Aquat Toxicol 2009 May 21;92(4):228-39. Epub 2009 Feb 21.

University of Bergen, Institute of Biology, HIB, Thormohlensgt. 55, 5020 Bergen, Norway.

We have previously developed a novel in vitro assay that utilises cultures of primed female stickleback kidney cells for the screening of potential androgenic and anti-androgenic environmental contaminants. Stickleback kidney cells are natural targets for steroid hormones and are able to produce a protein, spiggin, in response to androgenic stimulation. We undertook a combined in vivo/in vitro study where we used the magnitude of spiggin production as an endpoint to test the anti-androgenic properties of the pharmaceutical androgen antagonist flutamide and three environmental contaminants: the organophosphate insecticide fenitrothion, the urea-based herbicide linuron and the fungicide vinclozolin. In vitro, kidney cells were exposed to a range of concentrations [from 10(-14) M (2.5 pg/L) up to 10(-6) M (280 microg/L)] of the test compounds alone for determining agonist activities, or together with 10(-8) M (3 microg/L) dihydrotestosterone (DHT) for determining antagonist activities. An in vivo flow-through aquarium-based study was carried out in parallel. Female sticklebacks were exposed to a range of concentrations of the same chemicals alone or in combination with DHT (5 microg/L) for 21 days. All of the compounds significantly inhibited DHT-induced spiggin production in a concentration-dependent manner in both the in vitro (FN > or = FL > or = LN > VZ) and in vivo (FN > FL > or = VZ > LN) assays. Fenitrothion and flutamide inhibited spiggin production in vitro at a concentration as low as 10(-12) M (P < 0.05), while linuron and vinclozolin inhibited DHT-induced spiggin production at concentrations of 10(-10) M (P < 0.05) and 10(-6) M (P < 0.001) respectively. Similarly, fenitrothion and flutamide were the most potent chemicals in vivo and significantly reduced DHT-induced spiggin production at a concentration of 10 microg/L and 25 microg/L respectively (P < 0.01). Both linuron and vinclozolin induced a significant decrease in DHT-induced spiggin production at a concentration of 100 microg/L when tested in vivo. In addition, kidney cell primary culture was used to test the (anti-)androgenic effects of the major environmental contaminants: oestradiol (E2), nonylphenol (NP) and bisphenol A (BPA) for the first time in teleosts. We observed that these compounds were able to significantly inhibit spiggin production at high doses (E2: 270 microg/L; NP: 2.2 microg/L; BPA: 2.3 microg/L). When tested in the absence of DHT, none of the compounds showed a significant agonistic activity in either in vivo or in vitro assays. Overall, our data further demonstrate that kidney cell primary culture is a reliable and a sensitive screening tool for the detection of (anti-)androgenic compounds. In addition, our study represents the first attempt to develop a combined in vivo/in vitro screening strategy for assessing the effects of (anti-)androgenic endocrine disrupters.
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http://dx.doi.org/10.1016/j.aquatox.2009.02.006DOI Listing
May 2009

Female crucian carp, Carassius carassius, lose predator avoidance behavior when getting ready to mate.

J Chem Ecol 2008 Nov 21;34(11):1487-91. Epub 2008 Oct 21.

Department of Molecular Biosciences, Faculty of Mathematics and Natural Sciences, University of Oslo, P.O. Box. 1041, Blindern, 0316 Oslo, Norway.

In predator-prey interactions, the prey often have to compromise fitness-related behaviors such as feeding, courting, and territorial defense in order to avoid predators. In these trade-off situations, some behaviors have priority over others. These priorities are not rigid, and may be context-dependent; for instance, many animals show increased risk-taking during courtship behavior by paying less attention to potential predators. We investigated whether the fright reaction, a stereotypical avoidance response to olfactory cues from injured conspecifics, may be affected by reproductive status in a teleost fish, the crucian carp. We demonstrate that among individuals not responding to alarm substances with a fright reaction, the majority were ovulated or spermiated. In females, mean plasma concentrations of 17beta-estradiol and testosterone, gonadal steroids known to decrease during the later stages of sexual maturation, were lower in the individuals not responding with a fright reaction compared to those responding. In males, there were no differences between responsive and non-responsive individuals in mean plasma levels of androgens (testosterone and 11-ketotestosterone) involved in spermatogenesis and male sexual behavior. As the fright reaction in crucian carp consists of behavior incompatible with spawning behavior, we hypothesize that this short-term suppression of the alarm response has evolved so that spawning can occur uninterrupted.
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http://dx.doi.org/10.1007/s10886-008-9553-9DOI Listing
November 2008

The combined effects of temperature and GnRHa treatment on the final stages of sexual maturation in Atlantic salmon (Salmo salar L.) females.

Fish Physiol Biochem 2008 Sep 12;34(3):289-98. Epub 2007 Oct 12.

Institute of Marine Research, 5005, Bergen, Norway.

Atlantic salmon (Salmo salar L.) females (2 SW), maturing for the first time, were reared under one of three temperature regimes (high: 14.3 +/- 0.5 degrees C; natural: 10.6 +/- 1.0 degrees C; and cold: 6.9 +/- 1.0 degrees C) in combination with one of two experimental treatments; an injection of GnRH analogue (GnRHa) contained in biodegradable microspheres, or a sham injection (microspheres only). The six experimental groups were then reared under simulated natural photoperiod for 4 weeks. Blood samples were drawn for analysis of plasma steroid levels and the fish were inspected for ovulation weekly. Batches of stripped eggs were incubated in triplicate incubators in raceways until the eyed stage. Treatment with GnRHa resulted in a substantial advancement and synchronization of ovulation at all temperatures, while exposure to cold water also appeared to advance ovulation slightly. While 75% (warm and cold) to 90% (natural) of GnRHa fish ovulated during the 4-week trial, only 30% of sham-treated females exposed to cold water, and none of the sham-treated fish held at higher temperatures, ovulated during this period. Survival rates of embryos to the eyed-stage were significantly higher for broodstock exposed to cold water. Plasma levels of testosterone (T), 17beta-oestradiol (E2), and 17alpha,20beta-dihydroxy-4-pregnen-3-one (17,20betaP) were all significantly affected by treatment with GnRHa and, to a lesser extent, temperature. The efficiency of GnRHa in counteracting the negative effects of high temperature on ovulation and the associated changes in circulating sex steroids suggest that temperature inhibition operates at least in part at the brain or pituitary.
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http://dx.doi.org/10.1007/s10695-007-9187-9DOI Listing
September 2008

Molecular biomarkers of endocrine disruption in small model fish.

Mol Cell Endocrinol 2008 Oct 21;293(1-2):57-70. Epub 2008 Jun 21.

A wide range of environmental contaminants can interfere with hormonal regulation in vertebrates. These endocrine disrupting chemicals (EDCs) are of high relevance for human and wildlife health, since endocrine signalling controls many essential physiological processes which impact on the individual's health, such as growth and development, stress response, and ultimately reproduction and population development. Small fish represent a cost-effective model for testing potential EDCs allowing the possibility to integrate from molecular to phenotypic and functional effects. We have comprehensively reviewed exposure-effect data from four different small model fish: zebrafish, medaka, fathead minnow, and the three-spined stickleback. The majority of available data refer to EDCs interfering with reproductive hormones. However, we have also included interactions with other hormone systems, particularly the thyroid hormones. We demonstrate that the available data clearly indicates the predictive potential of molecular biomarkers, supporting the development and regulatory application of simple molecular-based screening assays using small model fish for EDC testing.
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http://dx.doi.org/10.1016/j.mce.2008.06.008DOI Listing
October 2008

Hormonal regulation of female nuptial coloration in a fish.

Horm Behav 2008 Sep 10;54(4):549-56. Epub 2008 Jun 10.

Department of Marine Ecology, Göteborg University, 566 Kristineberg, SE-450 34 Fiskebäckskil, Sweden.

Physiological color change in camouflage and mating is widespread among fishes, but little is known about the regulation of such temporal changes in nuptial coloration and particularly concerning female coloration. To better understand regulation of nuptial coloration we investigated physiological color change in female two-spotted gobies (Gobiusculus flavescens). Females of this species develop an orange belly that acts as an ornament. The orange color is caused by the color of the gonads combined with the chromathophore based pigmentation and transparency of the skin. Often during courtship and female-female competition, a rapid increase in orange coloration, in combination with lighter sides and back that increases skin and body transparency, gives the belly an intense 'glowing' appearance. To understand how this increased orange coloration can be regulated we analysed chromatic and transparency effects of neurohumoral agents on abdominal skin biopsies in vitro. We found prolactin and alpha-melanocyte stimulating hormone (MSH) to increase orange coloration of the skin. By contrast, melatonin and noradrenaline increased skin transparency, but had a negative effect on orange coloration. However, mixtures of melatonin and MSH, or melatonin and prolactin, increased both orange coloration and transparency. This effect mimics the chromatic 'glow' effect that commonly takes place during courtship and intra sexual aggression. Notably, not only epidermal chromatophores but also internal chromatophores lining the peritoneum responded to hormone treatments. There were no chromatic effects of the sex steroids 17beta-estradiol, testosterone or 11-ketotestosterone. We hypothesize that similar modulation of nuptial coloration by multiple hormones may be widespread in nature.
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http://dx.doi.org/10.1016/j.yhbeh.2008.05.018DOI Listing
September 2008

Intercalibration exercise using a stickleback endocrine disrupter screening assay.

Environ Toxicol Chem 2008 Feb;27(2):404-12

Centre for Environment, Fisheries, and Aquaculture Science, Burnham Laboratory, Burnham-on-Crouch, Essex, UK.

The Organisation for Economic Cooperation and Development (OECD) is currently validating a short-term fish screening protocol for endocrine disrupters (estrogens, androgens, and their antagonists and aromatase inhibitors), using three core species: fathead minnow, Japanese medaka, and zebrafish. The main endpoints proposed for the first phase of validation of the screen are vitellogenin (VTG) concentration, gross morphology (secondary sexual characteristics and gonado-somatic index), and gonadal histopathology. A similar protocol is concurrently being developed in the United Kingdom using the three-spined stickleback, with identical endpoints to those for the core species and, in addition, a unique androgen-specific endpoint in the form of spiggin (glue protein) induction. To assess the suitability of this species for inclusion in the OECD protocol alongside the core species, an intercalibration was conducted using 17beta-estradiol (a natural estrogen) and trenbolone (a synthetic androgen), thus mimicking a previous intercalibration with the core species. All three participating laboratories detected statistically significant increases in VTG in males after 14 d exposure to nominal concentrations of 100 ng/L 17beta-estradiol and statistically significant increases in spiggin in females after 14 d exposure to nominal concentrations of 5,000 ng/L trenbolone. The stickleback screen is reliable, possessing both relevant and reproducible endpoints for the detection of potent estrogens and androgens. Further work is underway to assess the relevance and suitability of the screen for weakly acting estrogens, anti-androgens, and aromatase inhibitors.
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http://dx.doi.org/10.1897/07-228R.1DOI Listing
February 2008

An experimental test of the immunocompetence handicap hypothesis in a teleost fish: 11-ketotestosterone suppresses innate immunity in three-spined sticklebacks.

Am Nat 2007 Oct 1;170(4):509-19. Epub 2007 Aug 1.

Department of Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, August Thienemann Strasse 2, D-24306 Plon, Germany.

The immunocompetence handicap hypothesis (ICHH) provides a functional explanation for how sexual ornaments can provide honest signals of male quality. A key aspect of this hypothesis is that testosterone (T) has a bimodal effect: a higher T level enhances the expression of ornaments (increasing mating success and, ultimately, fitness); however, at the same time, it suppresses immune function. Tests of the latter assumption, which have focused mainly on aspects of adaptive immunity in birds, led to equivocal results. We performed a hormone-implant experiment in male three-spined sticklebacks (Gasterosteus aculeatus) to test the key assumptions of the ICHH in a fish, where the dominant circulating androgen is 11-ketotestosterone (11kT) rather than T. Males were implanted with 11-ketoandrostenedione, which is a natural precursor of 11kT. Each individual's circulating 11kT level, ornamentation, and immunocompetence were measured 2 weeks later. In addition, we quantified oxidative tissue damage because the ICHH has been hypothesized to work via oxidative stress. We found that the males' 11kT levels correlated positively with ornamentation but negatively with immunocompetence, in particular, measures of innate immunity. Moreover, there was a trend for fish with high 11kT levels to suffer more from oxidative stress. Thus, our data provide support for the ICHH.
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http://dx.doi.org/10.1086/521316DOI Listing
October 2007

Development of a stickleback kidney cell culture assay for the screening of androgenic and anti-androgenic endocrine disrupters.

Aquat Toxicol 2006 Aug 14;79(2):158-66. Epub 2006 Jul 14.

Department of Biology, University of Bergen, Institute of Biology, HIB, Thormohlensgt. 55, 5020 Bergen, Norway.

Issues raised by the presence in the environment of chemicals able to mimic or antagonize the action of androgenic hormones are of growing concern. Here we report the development of a novel in vitro test for the screening of (anti-)androgenic chemicals, based on primary cultures of stickleback kidney cells that produce a protein, the spiggin, in response to androgenic stimulation. Cell spiggin content was measured by ELISA. Comparison between cell cultures from quiescent males, photoperiodically stimulated males, control females and dihydrotestosterone (DHT)-primed females led to the selection of cell cultures from DHT-primed females for the development of a standardized protocol. 48h of treatment with androgens proved to be sufficient to induce concentration-dependent increase in spiggin cell content with a high sensitivity. DHT induced a significant spiggin increase at 10(-12)M, while testosterone (T) and the teleost specific androgen 11-ketotestosterone (11-KT) had a significant effect at 10(-10)M. Maximal responses were obtained with 10(-8)M DHT and 10(-6)M T and 11-KT. This indicates a higher sensitivity to DHT than to T and 11-KT, in agreement with previous data on stickleback kidney androgen receptor affinity. No effect was observed with other steroids or thyroid hormone, indicating the androgen specificity of the test. The anabolic steroid 17beta-Trenbolone (TB) was able to stimulate spiggin synthesis in a concentration-dependent manner with a significant effect at a concentration as low as 10(-10)M, and a maximal effect at 10(-6)M. The synthetic human androgen receptor antagonist, flutamide had no effect alone, but concentration-dependently inhibited the stimulatory effect of 10(-8)M 11-KT with a complete inhibition at 10(-6)M flutamide. This cell culture system provides an innovative tool for the rapid and sensitive screening of androgenic and anti-androgenic properties of environmental contaminants.
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http://dx.doi.org/10.1016/j.aquatox.2006.06.005DOI Listing
August 2006