Short-term test for predicting the potential of xenobiotics to impair reproductive success in fish (original) (raw)
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Limitations of extrapolating toxic effects on reproduction to the population level
Ecological Applications, 2014
For the ecological risk assessment of toxic chemicals, standardized tests on individuals are often used as proxies for population-level effects. Here, we address the utility of one commonly used metric, reproductive output, as a proxy for population-level effects. Because reproduction integrates the outcome of many interacting processes (e.g., feeding, growth, allocation of energy to reproduction), the observed toxic effects in a reproduction test could be due to stress on one of many processes. Although this makes reproduction a robust endpoint for detecting stress, it may mask important population-level consequences if the different physiological processes stress affects are associated with different feedback mechanisms at the population level. We therefore evaluated how an observed reduction in reproduction found in a standard reproduction test translates to effects at the population level if it is caused by hypothetical toxicants affecting different physiological processes (physiological modes of action; PMoA). For this we used two consumer-resource models: the Yodzis-Innes (YI) model, which is mathematically tractable, but requires strong assumptions of energetic equivalence among individuals as they progress through ontogeny, and an individual-based implementation of dynamic energy budget theory (DEB-IBM), which relaxes these assumptions at the expense of tractability. We identified two important feedback mechanisms controlling the link between individual-and population-level stress in the YI model. These mechanisms turned out to also be important for interpreting some of the individual-based model results; for two PMoAs, they determined the population response to stress in both models. In contrast, others stress types involved more complex feedbacks, because they asymmetrically stressed the production efficiency of reproduction and somatic growth. The feedbacks associated with different PMoAs drastically altered the link between individual-and population-level effects. For example, hypothetical stressors with different PMoAs that had equal effects on reproduction had effects ranging from a negligible decline in biomass to population extinction. Thus, reproduction tests alone are of little use for extrapolating toxicity to the population level, but we showed that the ecological relevance of standard tests could easily be improved if growth is measured along with reproduction.
Contaminant effects on reproductive success in selected benthic fish
Marine Environmental Research, 1993
Field studies on ovarian development in English sole from urban and nonurban sites in Puget Sound, Washington, USA, demonstrated that animals with elevated levels of fluorescent aromatic compounds (FACs) in bile were less likely to enter vitellogenesis and had lower plasma ...
Environmental Toxicology and Chemistry, 2002
In ecotoxicological testing, there are few studies that report on reproductive output (egg production) of marine or estuarine fish. Cunner (Tautogolabrus adspersus) were studied as a potential model species to evaluate the impact of pollutants with estrogenic activity on reproduction in estuarine fish populations. Cunner inhabit marine and estuarine areas where contaminant discharges are likely. Baseline values for cunner gonadosomatic index (GSI), hepatosomatic index (HSI), and plasma vitellogenin (VTG) were determined in a field reference site (April 1999-December 1999). Male and female GSI indicated that cunner spawning is synchronized. Female HSI and VTG increased prior to GSI. From our laboratory observations, cunner are suitable for conducting experiments with reproductive endpoints indicative of both exposure (vitellogenin levels) and effects (egg production). However, cunner are not sexually dimorphic and stripping ripe fish is the only method to distinguish sex. In preparation for laboratory exposure studies with cunner, we designed a laboratory experimental holding system to accommodate cunner's reproductive behavior, a vertical spawning run to the water surface. Cunner were successfully acclimated from overwintering torpor to spawning condition in the laboratory by gradually changing the environmental conditions of fish held at winter conditions (4ЊC and 9:15-h light:dark photoperiod) to spawning condition (18ЊC and 15:9-h light:dark photoperiod). Our results show that cunner successfully spawned daily in the laboratory. They produced fertile eggs in our experimental system designed to accommodate cunner's vertical spawning runs, demonstrating that male and female reproductive behavior was synchronized in the laboratory. Our observations indicate that cunner would be a useful model species for evaluating reproductive effects of environmental contaminants in laboratory studies.
Endocrine Toxicants and Reproductive Success in Fish
Human and Ecological Risk Assessment: An International Journal, 2001
There is compelling evidence on a global scale for compromised growth and reproduction, altered development, and abnormal behaviour in feral fish that can be correlated or in some cases causally linked with exposure to endocrine disrupting chemicals (EDCs). Attributing cause and effect relationships for EDCs is a specific challenge for studies with feral fish as many factors including food availability, disease, competition and loss of habitat also affect reproduction and development. Even in cases where there are physiological responses of fish exposed to EDCs (e.g., changes in reproductive hormone titres, vitellogenin levels), the utility of these measures in extrapolating to whole animal reproductive or developmental outcomes is often limited. Although fish differ from other vertebrates in certain aspects of their endocrinology, there is little evidence that fish are more sensitive to the effects of EDCs. Therefore, to address why endocrine disruption seems so widespread in fish, it is necessary to consider aspects of fish physiology and their environment that may increase their exposure to EDCs. Dependence on aquatic respiration, strategies for iono-osmotic regulation, and maternal transfer of contaminants to eggs creates additional avenues by which fish are exposed to EDCs. This paper provides an overview of responses observed in feral fish populations that have been attributed to EDCs and illustrates many of the factors that need consideration in evaluating the risks posed by these chemicals.
Aquatic Toxicology, 2010
Animal alternatives research has historically focused on human safety assessments and has only recently been extended to environmental testing. This is particularly for those assays that involve the use of fish. A number of alternatives are being pursued by the scientific community including the fish embryo toxicity (FET) test, a proposed replacement alternative to the acute fish test. Discussion of the FET methodology and its application in environmental assessments on a global level was needed. With this emerging issue in mind, the ILSI Health and Environmental Sciences Institute (HESI) and the European Centre for Ecotoxicology and Toxicology of Chemicals (ECETOC) held an International Workshop on the Application of the Fish Embryo Test as an Animal Alternative Method in Hazard and Risk Assessment and Scientific Research in March, 2008. The workshop included approximately 40 scientists and regulators representing government, industry, academia, and non-governmental organizations from North America, Europe, and Asia. The goal was to review the state of the science regarding the investigation of fish embryonic tests, pain and distress in fish, emerging approaches utilizing fish embryos, and the use of fish embryo toxicity test data in various types of environmental assessments (e.g., hazard, risk, effluent, and classification and labeling of chemicals). Some specific key outcomes included agreement that risk assessors need fish data for decision-making, that extending the FET to include eluethereombryos was desirable, that relevant endpoints are being used, and that additional endpoints could facilitate additional uses beyond acute toxicity testing. The FET was, however, not yet considered validated sensu OECD. An important action step will be to provide guidance on how all fish tests can be used to assess chemical hazard and to harmonize the diverse terminology used in test guidelines adopted over the past decades. Use of the FET in context of effluent assessments was considered and it is not known if fish embryos are sufficiently sensitive for consideration as a surrogate to the sub-chronic 7-day larval fish growth and survival test used in the United States, for example. Addressing these needs by via workshops, research, and additional data reviews were identified for future action by scientists and regulators.
Environmental Toxicology and Chemistry, 2003
The synthetic estrogen 17␣-ethynylestradiol (EE2) is a commonly used oral contraceptive that has been increasingly detected in sewage effluents. This study determined whether EE2 exposure adversely affected reproduction in sexually maturing male rainbow trout (Oncorhynchus mykiss). We exposed male trout to graded water concentrations of EE2 (10, 100, and 1,000 ng/ L) for 62 d leading up to the time of spawning. Semen and blood plasma samples were removed from each fish. Semen was used to fertilize groups of eggs from one nonexposed female. As a measure of fertility, eggs were incubated for 28 d after fertilization to determine the proportion that attained the eyed stage of embryonic development. Additional endpoints also measured included sperm motility, spermatocrit, gonadosomatic and hepatosomatic indices, testis histology, and circulating plasma levels of the sex steroids 17␣, 20-dihydroxyprogesterone (17,20-DHP) and 11-ketotestosterone (11-KT). Exposure to 1,000 ng/L of EE2 caused complete mortality of the treatment group by day 57. Exposure to lower EE2 water concentrations (10 and 100 ng/L) caused an increase in sperm density, while a significant reduction in testis mass was observed only in the 100-ng/L exposure group. Most significantly, semen harvested from fish exposed to 10 and 100 ng/L EE2 caused an approximately 50% reduction in the number of eggs attaining the eyed stage of embryonic development. Plasma levels of 17,20-DHP in exposed fish were roughly twice the level of the controls, while levels of 11-KT were significantly reduced in fish exposed to 100 ng/L EE2. These results suggest that sexually maturing male rainbow trout are susceptible to detrimental reproductive effects of short-term exposures to environmentally relevant levels of EE2.
Pollutants as Developmental Toxicants in Aquatic Organisms
Environmental Health Perspectives, 1987
Pollutants, by disrupting metabolic processes, can interfere with development, and, at critical periods of development, can act as teratogens. Such interference with normal development can be used as a bioassay. Some screening tests are based on this phenomenon.
Aquatic Toxicology, 2007
A short-term reproductive bioassay with the mummichog (Fundulus heteroclitus) was developed to link changes in endocrine status to reproductive potential subsequent to endocrine disrupting substance (EDS) exposure. Sexually mature mummichog were separated by sex and exposed to the synthetic estrogen 17␣-ethynylestradiol (EE 2 ) at nominal concentrations of 0-100 ng/L for 21 days using a static daily renewal protocol. Half of the fish were sampled on Day 21. At 100 ng/L, male fish had induction of vitellogenin (VTG), increased gonadosomatic index (GSI), decreased testosterone production and decreased circulating 11-ketotestosterone (11-KT). Female fish had decreased circulating estradiol (E 2 ) and testosterone (T) at 100 ng/L. There were some impacts at lower concentrations of EE 2 in both sexes, though the results were not consistent. On Day 21, the remaining male and female fish were combined at each treatment and exposed for an additional 7 days during which spawning and fertilization success were also assessed. Males exposed to 100 ng/L EE 2 exhibited VTG induction, increased GSI, and decreased T production on Day 28. Female fish had increased E 2 and T production at 1 and/or 10 ng/L and circulating E 2 levels remained depressed above 10 ng/L. Female fish exposed to 100 ng/L spawned fewer eggs; fertilization was also impaired. In a parallel exposure, measured EE 2 water concentrations were approximately 10-20% of nominal for the 100 ng/L EE 2 treatment over a 24-h static exposure; levels in the other treatments were below detectable levels. Fish exposed to nominal concentrations of EE 2 below environmentally relevant levels (i.e., <10 ng/L) showed minimal effects while both the endocrine system and reproductive potential were affected at 100 ng/L EE 2 (nominal).
Aquatic Toxicology, 2011
Produced water (PW), a by-product of the oil-production process, contains large amount of alkylphenols (APs) and other harmful oil compounds. In the last 20 years, there have been increasing concerns regarding the environmental impact of large increases in the amounts of PW released into the North Sea. We have previously shown that low levels of APs can induce disruption of the endocrine and reproductive systems of Atlantic cod (Gadus morhua). The aims of this follow-up study were to: (i) identify the lowest observable effect concentration of APs; (ii) study the effects of exposure to real PW, obtained from a North Sea oil-production platform; and (iii) study the biological mechanism of endocrine disruption in female cod. Fish were fed with feed paste containing several concentrations of four different APs (4tert-butylphenol, 4-n-pentylphenol, 4-n-hexylphenol and 4-n-heptylphenol) or real PW for 20 weeks throughout the normal period of vitellogenesis in Atlantic cod from October to January. Male and female cod, exposed to AP and PW, were compared to unexposed fish and to fish fed paste containing 17oestradiol (E 2 ). Approximately 60% of the females and 96% of the males in the unexposed groups were mature at the end of the experiment. Our results show that exposure to APs and E 2 have different effects depending on the developmental stage of the fish. We observed that juvenile females are advanced into puberty and maturation, while gonad development was delayed in both maturing females and males. The AP-exposed groups contained increased numbers of mature females, and significant differences between the untreated group and the AP-treated groups were seen down to a dose of 4 g AP/kg body weight. In the high-dose AP and the E 2 exposed groups, all females matured and no juveniles were seen. These results suggest that AP-exposure can affect the timing of the onset of puberty in fish even at extremely low concentrations. Importantly, similar effects were not seen in the fish that were exposed to real PW.
Marine Environmental Research, 2008
We exposed sexually maturing male rainbow trout (Oncorhynchus mykiss) to BDE-47 (a polybrominated diphenyl ether) and female rainbow trout to trenbolone (an anabolic steroid). Male trout were orally exposed for 17 days to 55 μg/kg/day BDE-47 and female trout continuously exposed for 60-77 days to a measured trenbolone water concentration of 35 ng/L. After the exposure, eggs and semen were collected and in vitro fertilization trials performed using a sperm:egg ratio of 300,000:1. In the BDE-47 study, eggs from control females were fertilized with semen from exposed males, while in the trenbolone study, eggs from exposed females were fertilized with semen from control males. All treatments were evaluated at two-three early developmental time-points representing first cleavage (0.5 day), embryonic keel (9 days), and eyed stages (19 days), respectively. The results indicated that BDE-47 exposure did not alter fertility as embryonic survival was similar between control and exposed groups. Trenbolone exposure also did not alter embryo survival. However, in the embryos fertilized with eggs from trenbolone exposed females, a noticeable delay in developmental progress was observed. On day 19 when eye development is normally complete, the majority of the embryos either lacked eyes or displayed underdeveloped eyes, in contrast to control embryos. This finding suggests steroidal androgen exposure in sexually maturing female rainbow trout can impact developmental timing of F1 offspring.