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Wildlife Reproductive Effects

Introduction
Summary of Non-Human PCB Effects
 
The Wildlife Studies

Mink eating contaminated fish.


Introduction

PCBs cause a variety of serious reproductive problems in several types of wildlife (mammal, bird, fish, reptile, crustacean, insect) which shows that PCBs are affecting reproductive traits shared by the wide range of creatures. Human beings share a similar reproductive biochemistry; therefore, these wildlife health risks should serve as a warning of potential human effects.


Summary of Effects

This is not a complete list of all such research, only a sample. For additional study results, visit the TOXNET databases.

Marine Mammals

  • females unable to reproduce
  • decreased testosterone
  • impaired reproductive function
  • impaired immune function
  • mass mortality due to infections
  • female mice fed Beluga Whale blubber had altered ovulation structures, which affects reproduction
  • Beluga Whales have low calf production and/or low survival to adulthood
  • Belugas on the St. Lawrence River (downstream from Lake Michigan) had higher levels of PCBs
  • The Beluga fetuses had 10% higher concentrations of organochlorines (including PCBs) compared to the mothers
  • The source of PCBs is likely global distillation from lower latitudes.
  • The failure of the Beluga population to recover may be due to contamination by organochlorine compounds (including PCBs)
  • Belugas had morphological lesions on the thyroid and adrenal glands, (which may affect reproduction)
Polar Bears
  • Four hermaphroditic polar bears were found in Svalbard, Sweden, in 1996.
  • PCB, dioxin and furan levels were similar in polar bear and human breast milk
  • polar bear fat tissues contained about 21 ppm PCBs
  • human fat tissues contained 0.25 to 5.58 ppm PCBs
Mink
  • delayed onset of estrus (breeding condition)
  • reduced whelping rate
  • litter deaths
  • lower weight pups
  • immune system changes
  • weight differences in kidney, liver, brain, spleen, heart, and thyroid gland
  • increased periportal diffuse vacuolar hepatocellular lipidosis
  • long term effects
Rabbits
  • PCBs accumulated selectively in ovarian, oviductal and uterine tissues
  • the mix of PCBs in the blood serum were different from those in the follicular fluid surrounding the ovaries
  • increased preimplantation embryo mortality
Guinea Pigs
  • delayed sexual maturation
  • vaginal opening at older age and for shorter duration (breeding maturity)
  • lower testis weights
  • no testosterone difference
  • growth retardation
  • induced enzymes
  • inhibited progesterone metabolism and changed the hormonal balance
  • different tissues respond differently to PCBs
Turtles
  • sex reversal
  • altered sexual characteristics in male turtles
  • PCBs accumulate selectively in the testes
  • decrease in populations possible due to reproductive effects
Birds
  • depression of sexual characteristics in males
  • delayed egg laying and diminished laying capacity
  • reduced breaking strength in eggs
  • reduced testis weights (3 studies)
  • decreased testes seminiferous epithelium
  • smaller nuclear volume of Leydig cells
  • lower estrodiol in females
  • inhibited hormone binding in a dose-dependent manner (especially in ducks and rabbits)
  • smaller combs and wattles
  • weight loss
  • no change in adrenals
  • reduced testes
  • increased embryo mortality (2 studies)
  • increased abnormalities
Fish
  • sac fry mortality
  • death of zebrafish larvae
  • reduced number of oocytes in females
  • induced liver enzyme activity
  • altered sex ratios
  • severe gonadal abnormalities
  • inconsistent or extremely limited development of eggs (2 studies)
  • testicular abnormalities (3 studies)
  • altered steroids
  • abnormal gills and livers
  • PCBs tend to accumulate in the ovaries, testes, liver and kidneys (2 studies)
Sea Stars, Insects and Crustaceans
  • reduced reproduction
  • egg maturation delayed
  • disturbed development of embryos
  • reduced survival, increased mortality
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The Wildlife Studies

Overall Statement: from Fox GA.  Wildlife as sentinels of human health effects in the Great Lakes--St. Lawrence basin.  Environ Health Perspect. 2001 Dec;109 Suppl 6:853-61.  Canadian Wildlife Service, National Wildlife Research Centre, Hull, Quebec, Canada. glen.fox@ec.gc.ca
 

"There is no existing formal, long-term program for gathering evidence of the incidence and severity of the health effects of toxic substances in wildlife. However, research-based studies of bald eagles, herring gulls, night herons, tree swallows, snapping turtles, mink, and beluga over the past 30 years have revealed a broad spectrum of health effects in the Great Lakes-St. Lawrence basin including thyroid and other endocrine disorders, metabolic diseases, altered immune function, reproductive impairment, developmental toxicity, genotoxicity, and cancer. These effects occurred most often and were most severe in the most contaminated sites (Green Bay, Saginaw Bay, Lake Ontario, the St. Lawrence estuary, and more recently, Lake Erie), some of which are International Joint Commission-designated Areas of Concern (AOCs). In all cases, a strong argument can be made for an environmental etiology, and in many cases for the involvement of persistent organic pollutants, particularly polychlorinated biphenyls, polychlorinated dibenzo-p-dioxins, and polycyclic aromatic hydrocarbons. For some, the association with particular contaminants is consistent with controlled studies, and in some, dose-response relationships were documented. The biologic significance of these health impairments to the affected species is currently unclear, but they resemble those observed with increased incidence in human subpopulations in one or more AOCs. Formalizing health effects monitoring of sentinel wildlife species by the parties to the Canada-USA Great Lakes Water Quality Agreement is required. This would facilitate the optimal use of sentinel wildlife health data in a larger, epidemiologic weight-of-evidence context upon which to base decisions and policies regarding the effects of chemical exposures on human populations."
Marine Mammals

Study #1

  • female mice fed Beluga Whale blubber had altered ovulation structures, which affects reproduction
The toxic potential of naturally relevant mixtures of PCBs and other organohalogens on the reproductive system of C57Bl/6 female mice was assessed. 
 

Beluga Whales on the St. Lawrence Seaway
are endangered by PCBs and other toxins
Mice were fed diets in which lipids were replaced by blubber of beluga whales from a highly contaminated population of the Saint Lawrence River, and a less contaminated population from the Arctic Ocean. Ratios of blubber from both sources were mixed in order to perform a dose-response study. Control mice were fed diets for 90 d in which fat was replaced by corn oil or beef tallow. There were no significant effects of diets on body, liver, spleen or thymus weights. Similarly ovulation occurred in all control and experimental groups. However, Graafian follicles from ovaries of mice fed contaminated diets showed abnormal development of oocytes. Cumulus granulosa cells bind normally to the oocyte prior to ovulation and are essential for sperm penetration and fertilization. These cells were absent in both Graafian follicles and ovulated oocytes in the oviduct of all groups fed contaminated diets. Oviducts of these mice revealed evidence of epithelial degeneration. These results suggest the female mouse reproductive system is sensitive to organohalogens and illustrate the toxic potential of contaminant mixtures as found in the less contaminated Arctic population.  (Ruby et al, 2003)

Study #2

  • Beluga Whales have low calf production and/or low survival to adulthood
  • Belugas on the St. Lawrence River (downstream from Lake Michigan) had higher levels of PCBs
An epidemiologic study was carried out over a period of 9 years on an isolated population of beluga whales (Delphinapterus leucas) residing in the St. Lawrence estuary (Quebec, Canada). More than 100 individual deaths were aged, and/or autopsied and analyzed for toxic compounds, and the population was surveyed for size and structure. Arctic belugas and other species of whales and seals from the St. Lawrence were used for comparison. Population dynamics: Population size appeared to be stable and modeling showed this stable pattern to result from low calf production and/or low survival to adulthood. Toxicology: St. Lawrence belugas had higher or much higher levels of mercury, lead, PCBs, DDT, Mirex, benzo(a)pyrene metabolites, equivalent levels of dioxins, furans, and PAH metabolites, and much lower levels of cadmium than Arctic belugas. In other St. Lawrence cetaceans, levels of PCBs and DDT were inversely related to body size, as resulting from differences in metabolic [incomplete abstract] (Beland et al, 1993)

Study #3

  • The Beluga fetuses had 10% higher concentrations of organochlorines (including PCBs) compared to the mothers
  • The source of PCBs is likely global distillation from lower latitudes.
Beluga whales bioaccumulate organochlorines from their environment. Blubber samples of Beluga Whales from Alaska's north coast contain organochlorines, including Toxaphene (polychlorinated camphenes) PCBs, DDTs and chlordane. Toxaphene was the organochlorine pesticide found in the highest concentration in all samples with the exception of the 6 year old male where PCBs were highest. The source of these organochlorines is likely global distillation from lower latitudes. Males had higher concentrations than females and the oldest male had higher concentration than the younger male. Females exhibit a decrease in concentrations with age. The fetus had about 10% higher concentrations for all organochlorines compared to the mother. Transplacental transfer of organochlorines and lactation lower the contaminant concentration in females. Older females have lower contaminate concentrations likely due to continual reproductive success. Consumption of older males will expose humans to higher levels of organochlorines.  (Wade et al, 1997)

Study #4

  • The failure of the Beluga population to recover may be due to contamination by organochlorine compounds (including PCBs)
  • Belugas had morphological lesions on the thyroid and adrenal glands, (which may affect reproduction)
A small isolated population of beluga whales (Delphinapterus leucas) that are highly contaminated by pollutants, mostly of industrial origin, resides in the St. Lawrence estuary, Quebec, Canada. Overhunting in the first half of the century was the probable cause for this population to dwindle from several thousand animals to the current estimate of 500. The failure of the population to recover might be due to contamination by organochlorine compounds, which are known to lead to reproductive failure and immunosuppression in domestic and laboratory animals and seals. Functional and morphological changes have been demonstrated in thyroid gland and adrenal cortex in many species exposed to organochlorinated compounds, including seals. Morphological lesions, although different, were also found in belugas. Functional evaluation of thyroid and adrenal glands of contaminated (St. Lawrence) versus much less contaminated (Arctic) belugas is currently under way. Necropsy of St. Lawrence belugas showed numerous severe and disseminated infections with rather mildly pathogenic bacteria, which suggests immunosuppression. Organochlorine compounds and other contaminants found in beluga whales cause immunosuppression in a variety of animal species including seals. Thirty-seven percent of all the tumors reported in cetaceans were observed in St. Lawrence beluga whales. This could be explained by two different mechanisms: high exposure to environmental carcinogens and suppression of immunosurveillance against tumors. Overall, St. Lawrence belugas might well represent the risk associated with long-term exposure to pollutants present in their environment and might be a good model to predict health problems that could emerge in highly exposed human populations over time.  (DeGuise et al, 1995)

Study #5

  • females unable to reproduce
The environmental poisons DDT and PCB (polychlorinated biphenyls) upset the balance in sex hormones. DDT or PCB may have caused the considerable reduction in sexual reproduction capacity which has been observed in ringed seal (Phoca hispida) in the Bay of Bothnia during the last 10 yr. Earlier studies showed that seals in the Baltic Sea (of

which the Bay of Bothnia is the northernmost part) carry very high burdens of DDT and PCB. In this study, pregnant seals had much lower content of these compounds than non-pregnant animals did. Females carrying over 70 mg PCB/kg of extractable fat are apparently unable to reproduce. Only 19% of the gray seals (Halichoerus grypus) in the Baltic proper have less than 70 mg PCB compared with 25% in the Bay of Bothnia. For ringed seal the values range from 39% up to 54% in the northernmost part of the Bay of Bothnia. Because the seal populations have been greatly reduced it is urgent to protect seals as much as possible. (Helle et al, 1976)

Study #6

  • decreased testosterone
The increasing residue levels of PCBs and DDE in the blubber of dalli-type Dall's porpoises were found to have a negative effect on the testosterone levels in blood. Decrease in the levels of testosterone was statistically significnt with increase in DDE concentrations. The results obtained suggest that the present levels of environmental contamination by persistent organochlorines can cause an imbalance of sex hormones and subsequent reproductive abnormalities in wild. The other hormone measured, aldosterone, which has no sexual function, was independent of the effects of both PCBs and DDE. (Subramanian et al, 1987)

Study #7

  • impaired reproduction function
  • impaired immune function
  • mass mortality due to infections
Many wildlife species may be exposed to biologically active concentrations of endocrine-disrupting chemicals. There is strong evidence obtained from laboratory studies showing the potential of several environmental chemicals to cause endocrine disruption at environmentally realistic exposure levels. In wildlife populations, associations have been reported between reproductive and developmental effects and endocrine-disrupting chemicals. In the aquatic environment, effects have been observed in mammals, birds, reptiles, fish, and mollusks from Europe, North America, and other areas. The observed abnormalities vary from subtle changes to permanent alterations, including disturbed sex differentiation with feminized or masculinized sex organs, changed sexual behavior, and altered immune function. For most reported effects in wildlife, however, the evidence for a causal link with endocrine disruption is weak or nonexisting. Crucial in establishing causal evidence for chemical-induced wildlife effects appeared semifield or laboratory studies using the wildlife species of concern. Impaired reproduction and development causally linked to endocrine-disrupting chemicals are well documented in a number of species and have resulted in local or regional population changes. These include: Masculinization (imposex) in female marine snails by tributyltin, a biocide used in antifouling paints, is probably the clearest case of endocrine disruption caused by an environmental chemical. The dogwhelk is particularly sensitive, and imposex has resulted in decline or extinction of local populations worldwide, including coastal areas all over Europe and the open North Sea. DDE-induced egg-shell thinning in birds has caused severe population declines in a number of raptor species in Europe and North America. Endocrine-disrupting chemicals have adversely affected a variety of fish species. In the vicinity of certain sources (e.g., effluents of water treatment plants) and in the most contaminated areas is this exposure causally linked with the effects on reproductive organs that could have implications for fish populations. However, there is also a more widespread occurrence of endocrine disruption in fish in the U.K., where estrogenic effects have been demonstrated in freshwater systems, in estuaries, and in coastal areas. In mammals, the best evidence comes from the-field studies on Baltic gray and ringed seals, and from the Dutch semifield studies on harbor seals, where both reproduction and immune functions have been impaired by PCBs in the food chain. Reproduction effects resulted in population declines, whereas impaired immune function has likely contributed to the mass mortalities due to morbillivirus infections. Distorted sex organ development and function in alligators has been related to a major pesticide spill into a lake in Florida, U.S.A. The observed estrogenic/antiandrogenic effects in this reptile have been causally linked in experimental studies with alligator eggs to the DDT complex. Although most observed effects currently reported concern heavily polluted areas, endocrine disruption is a potential global problem. This is exemplified by the widespread occurrence of imposex in marine snails and the recent findings of high levels of persistent potential endocrine-disrupting chemicals in several marine mammalian species inhabiting oceanic waters. (Vos et al, 2000)

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Polar Bears

Study #1

  • Four hermaphroditic polar bears were found in Svalbard, Sweden, in 1996.
During research on polar bears (Ursus maritimus) at Svalbard in April 1996, we captured two yearlings with a normal vaginal opening and a 20 mm penis containing a baculum. The penis was located caudal to the location in a normal male and was concealed within the vaginal opening by a single pair of labia. The urethral opening was situated laterally about 5 mm from the distal end of the penis. Neither of the yearlings showed signs of a Y chromosome, so both bears were regarded as female pseudohermaphrodites. On separate occasions in two bears, we recorded aberrant genitalia morphology with a high degree of chloral hypertrophy in Svalbard, which we also classified as female pseudohermaphroditism. The observed rate of female pseudohermaphroditism in this area was 1.5% (4/269). Pseudohermaphroditism in this polar bear population could result from excessive androgen excretion by the mother caused by a tumor, or it could be a result of endocrine disruption from environmental (incomplete abstract) (Wiig et al, 1998)

Study #2

  • PCB, dioxin and furan levels were similar in polar bear and human breast milk
Polychlorinated dibenzo-p-dioxins (PCDD), dibenzofurans (PCDF) and non-ortho substituted biphenyls (PCB, CB) were determined in 6 polar bear milk samples from Svalbard (Norway). For these compounds, no data for polar bears have been reported before from this region. Most of the PCDD congeners were found at detectable levels. Concentrations expressed as 2,3,7,8-TCDD equivalents (Nordic model) were in the order of 1-3 pg/g-1 fat (0.2-1.6 pg ml-1 milk) is comparable with ringed and harp seal blubber from the same region. On whole milk basis, concentrations were similar to those found in human milk. An estimation of the daily uptake via milk showed that the intake is lower for polar bears compared to humans. As in human milk, relatively high levels of OCDD were found in some polar bear milk samples. The PCDD/PCDF congener pattern in the milk was different to that found in polar bear fat from the Canadian Arctic. Non-ortho substituted PCB levels in polar bear milk were simil (incomplete abstract) (Oehme et al, 1995)

Study #3

  • polar bear fat tissues contained about 21 ppm PCBs
  • human fat tissues contained 0.25 to 5.58 ppm PCBs
Adipose tissues from two common porpoises (Phocaena phocaena), five bearded seals (Erignathus barbatus), five ringed seals (Phoca hispida), five hooded seals (Cystophora cristata), two arctic foxes (Alopex lagopus), one polar bear (Ursus maritimus), and one sheep (Ovis aries) shot on the west coast of Greenland were analyzed by electron capture gas chromatography for polychlorinated hydrocarbons. Studies were also made on adipose tissue from king eider (Somateria spectabilis), common eider (Somateria mollissima), harlequin duck (Histrionicus histrionicus), long tailed duck (Glangula hyemalis), purple sandpiper (Calidris maritima), Brunnich's guillemot (Uria lomvia), cormorant (Phalocrocorax carbo), ptarmigan (Lagopus mutus), and raven (Corvus corax), as well as adipose tissue from six female Greenlanders. Among the birds, raw p,p'-DDE concentrations ranged from 0.8 ppm (eider duck) to 13.9 ppm (raven), while PCB concentrations ranged from 2.0 ppm (eider duck) to 37.1 ppm (raven); the p,p'-DDE and PCB concentrations were significantly correlated. p,p'-DDT and p,p'-DDD were not traced, and lindane was found in trace amounts in 1/3 of the birds. Among the mammals, lindane concentrations ranged from 0.003 ppm (hooded seal) to 0.053 ppm (bearded seal), heptachlor was found in concentrations of 0.001 ppm (ringed seal) to 0.039 ppm (bearded seal), aldrin ranged from 0.028 ppm (hooded seal) to 3.06 ppm (polar bear), heptachloroepoxide was found in concentrations of 0.026 ppm (ringed seal) to 0.49 ppm (polar bear), raw p,p'-DDE ranged from 0.14 ppm (arctic fox) to 1.25 ppm (polar bear), and PCB ranged from 0.9 ppm (ringed seal) to 21.0 ppm (polar bear). In the human samples, PCB ranged from 0.25-5.58 ppm, p,p'-DDE ranged from 0.04-0.52 ppm, and the other compounds were found only in trace amounts. (Clausen et al, 1976)

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Mink Studies

Study #1

  • delayed onset of estrus (breeding condition)
  • reduced whelping rate
  • litter deaths
  • lower weight pups
  • immune system changes
  • weight differences in kidney, liver, brain, spleen, heart, and thyroid gland
  • increased periportal diffuse vacuolar hepatocellular lipidosis
  • long term effects
This study was conducted to determine the multigenerational effects of consumption of PCB-contaminated carp (Cyprinus carpio) from Saginaw Bay (Lake Huron) on mink (Mustela vison) reproduction and health and to examine selected biomarkers as potential indicators of polyhalogenated hydrocarbon toxicity in mink. The mink were fed diets formulated to provide 0 (control), 0.25, 0.5, or 1.0 ppm polychlorinated biphenyls (PCBs) through substitution of Saginaw Bay carp for ocean fish in the diets. To determine whether the effects of PCB exposure were permanent, half of the parental (P1) animals were switched from their respective treatment diets to the control diet after whelping the first of two F1 generations. Effects of in utero and lactational exposure to PCBs on subsequent reproductive performance of the F1 animals were examined by switching half of the first-year F1 offspring (kits) to the control diet at weaning, while the other half was continued on their parental diet (continuous exposure). Continuous exposure to 0.25 ppm, or more, of PCBs delayed the onset of estrus (as determined by vulvar swelling and time of mating) and lessened the whelping rate. Litters whelped by females continually exposed to 0.5 ppm, or more, of PCBs had greater mortality and lesser body weights than controls. Continuous exposure to 1.0 ppm PCBs had a variable effect on serum T4 and T3 concentrations. Compared to the controls, there were significant differences in kidney, liver, brain, spleen, heart, and thyroid gland weights of the mink continually exposed to 1.0 ppm PCBs. There was an increase in the incidence of periportal and diffuse vacuolar hepatocellular lipidosis in the P1 mink with continuous exposure to increasing concentrations of PCBs. Plasma and liver PCB concentrations of the adult and kit mink were, in general, directly related to the dietary concentration of PCBs and the duration and time of exposure. Short-term parental exposure to PCBs had detrimental effects on survival of subsequent generations of mink conceived months after the parents were placed on "clean" feed. The lowest observed adverse effect level (LOAEL) for dietary PCBs in this study was 0.25 ppm. (Restum et al, 1998)

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Rabbit Studies

Study #1

  • PCBs accumulated selectively in ovarian, oviductal and uterine tissues
  • the mix of PCBs in the blood serum were different from those in the follicular fluid surrounding the ovaries
The female rabbit was used to study (i) accumulation of lipophilic chlorinated hydrocarbons in genital tract tissues and (ii) subsequent morphological and functional effects after long-term low-dose exposure. Polychlorinated biphenyl (PCB), 1,1-di(p-chlorophenyl)-2,2,2-trichloroethane (DDT) and gamma-hexachlorocyclohexane (gamma-HCH) (dosages: 4, 3 and 0.8 mg per kg body weight, respectively) and a combination of these three components (and dosages) were administered to sexually mature rabbits over a period of 12-15 weeks. The animals were killed shortly before and at various times after ovulation. Accumulation of chlorinated hydrocarbons was high in ovarian, oviductal and uterine tissues, in follicular fluid and clearly detectable in uterine secretions. In follicular fluid, the concentration and patterns of congeners and isomers of PCB and DDT were distinctly different from serum. DDT- and gamma-HCH-treated animals showed a significantly reduced ovulation rate (P < 0.002 and 0.05, respectively). (Lindenau et al, 1994)

Study #2

  • increased preimplantation embryo mortality
  • study used PCB commercial mixture Aroclor 1260
Oral application of a commercial PCB mixture (Aroclor 1260) to female rabbits (4 mg/kg BW for 14 weeks) resulted in a significant accumulation of PCB in 6 day old blastocysts and in an increased preimplantation embryo mortality (Seiler, Fischer, Lindenau, Beier, 1993). In present study the direct embryotoxicity of PCB was investigated employing embryo in vitro culture. Three day old rabbit morulae were cultured in BSM II supplemented with 1.5% BSA under 5% O2. They were exposed to 100, 10 or 1 ug Aroclor 1260/mL medium for 24 h. The organochlorines had been dissolved in 1% DMSO before addition to the medium. Controls were cultured in PCB-free DMSO-containing medium. For retrospective analysis of the actual exposure, the PCB concentration of the culture media was determined after culture. 100 ug PCB led to a complete degeneration of the exposed embryos (n = 47 embryos, 3 replicates). Following exposure to 10 ug (n = 53, 3 replicates) only a few morulae developed into blastocysts. The others were either arrested in the morulae stage or were degenerated. Cell proliferation (measured by incorporation of tritiated thymidine) of the non-degenerated embryos was approximately 20% of that of corresponding control embryos. Compared with non-exposed controls, addition of 1 ug PCB/mL (n = 32, 2 replicates) showed either no or only a slight impairment of development. (Lindenau et al, 1993)

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Guinea Pig Studies

Study #1

  • delayed sexual maturation
  • vaginal opening at older age and for shorter duration
  • lower testis weights
  • no testosterone difference
  • growth retardation
  • study used Clophen A50 commercial mix of PCBs
Female and male guinea pigs exposed to polychlorinated biphenyls (PCBs) in utero and via mother's milk showed growth retardation and signs of delayed onset of sexual maturation. In female young exposed to PCBs first vaginal opening occurred at a significantly older age and was of shorter duration compared with control females. The age at the first ovulation did not differ significantly between PCB-exposed females and control females. Male young exposed to PCBs had significantly lower absolute and relative testis weights at 3 months of age compared with control males. No differences in plasma testosterone concentrations were observed. (Lundkvist, 1990)

Study #2

  • induced enzymes
  • inhibited progesterone metabolism and changed the hormonal balance
  • different tissues respond differently to PCBs
  • study used PCB commercial mixture Aroclor 1254
The effects of Aroclor-1254 on the metabolism of progesterone by cytochrome-P-450 in adrenal and testes microsomes were studied. Male guinea-pigs were given four intraperitoneal injections of 80mg/kg Aroclor-1254, and microsomal fractions of liver, adrenal, and testes were prepared after 48 hours. For in-vitro studies, microsomes were treated with 2.7, 6.6 or 13.3 micromoles Aroclor-1254 for 10 and 20 minutes. Hepatic microsomal cytochrome-P-450 increased two times after Aroclor-1254 treatment, while a 30% decrease in adrenal microsomal cytochrome-P-450 content was noted. An overall inhibitory effect of Aroclor-1254 on progesterone metabolism in adrenal microsomes was observed in-vivo, specifically a three fold decrease in the production of 11-deoxycortisol and 11-deoxycorticosterone. Consistent results were demonstrated with the in-vitro studies. No effects of Aroclor-1254 treatment on the metabolism of progesterone in testes microsomes were observed in-vivo or in-vitro. The authors conclude that different steroidogenic tissues respond differently to Aroclor-1254. (Goldman et al, 1990)

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Turtle Studies

Study #1

  • sex reversal
Polychlorinated biphenyls (PCBs) are widespread, low-level environmental pollutants associated with adverse health effects such as immune suppression and teratogenicity. There is increasing evidence that some PCB compounds are capable of disrupting reproductive and endocrine function in fish, birds, and mammals, including humans, particularly during development. Research on the mechanism through which these compounds act to alter reproductive function indicates estrogenic activity, whereby the compounds may be altering sexual differentiation. Here we demonstrate the estrogenic effect of some PCBs by reversing gonadal sex in a reptile species that exhibits temperature-dependent sex determination. [The researchers showed that turtle embryos can be sexually reversed (male to female) by estrogenic PCBs.] (Bergeron et al, 1994)

Study #2

  • altered sexual characteristics in male turtles
Recent research has suggested that contaminants in the environment may influence sex differentiation and reproductive endocrine function in wildlife. Concentrations of organochlorine contaminants (total polychlorinated biphenyls, pesticides) were higher in the blood plasma of snapping turtles from contaminated sites than in those from reference sites. The ratio of the precloacal length to the posterior lobe of the plastron (PPR) is sexually dimorphic in snapping turtles. There were significant reductions in the PPR at three contaminated sites versus two reference sites. The magnitude of the response was such that a significantly higher proportion of PPRs of males from a contaminated site (Cootes Paradise) overlapped with those of females than PPRs of males from a reference site (Lake Sasajewun). Observers can incorrectly identify the sex of turtles at the contaminated site based on secondary sexual characteristics alone. Unlike the changes to the morphology, there were few changes in 17 beta-estradio (abstract incomplete) (de Solla et al, 1998)

Study #3

  • PCBs accumulate selectively in the testes
  • decrease in populations possible due to reproductive effects
  • study used PCB 105
Despite the fact that PCB congeners exhibit very different biochemical activities, it has been necessary, due to former difficulties in separation and quantitation, to assess toxic hazard to tissues in terms of the concentration of the PCB mixture present. This approach is justifiable provided that a dynamic equilibrium is established among all tissues for each congener. Recent biochemical studies, involving individual congeners indicate that this may not always be the case. Toxic PCB congeners, isostereomers of TCDD, are electron acceptors capable of binding to cytoplasmic protein (Ah receptor) and other cellular macromolecules associated with a particular tissue. Specific Congener analysis of snapping turtle tissues has indicated the possible selective disposition of 2,3,3',4,4'-pentachlorobiphenyl in the testes, a situation which may lead to a surreptitious decrease in the population of that species, considering the longevity and wide distribution of these reptiles. (Olafsson et al, 1987)

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Bird Studies

Study #1

  • decreased testes weight
  • depression of sexual characteristics in males
  • several other health effects
A study was carried out to determine the effects of DDT, endrin, and various polychlorinated biphenyls on cardiovascular physiology and hematology as well as some toxicological symptoms of the domestic fowl at both lethal and sublethal levels. A significant increase in hematocrit values and hemoglobin concentration were observed in female adult Single Comb White Leghorn chickens when DDT (2000 ppm) was incorporated into the diet. In contrast, endrin (16-20 ppm) caused a significant increase in these two parameters. Total erythrocyte concentration showed the same trend as HCT values and hemoglobin concentration. In acute dosage experiments endrin infusion (8 mg/kg body weight) produced marked bradycardia and hypertension. These cardiovascular changes were accompanied by convulsions and salivation, indicating stimulation of parasympathetic and sympathetic nervous systems. No significant differences in packed cell volume, total erythrocyte concentration, and hemoglobin concentration were observed before or after endrin infusion in SCWL females. Toxicologic symptoms observed in cockerels after chronic oral administration (50-200 ppm) of various PCBs included depressed body weight and feed intake; general edema and hydropericardium; increased liver weight and decreased heart, spleen, and testes weight; depression of sexual characteristics; and some mortality. (Iturri, 1974)

Study #2

  • delayed egg laying and diminished laying capacity
  • reduced breaking strength in eggs
  • reduced testis weights
  • decreased testes seminiferous epithelium
  • smaller nuclear volume of Leydig cells
  • increased liver weight
  • lower estrodiol in females
  • study used PCB commercial mixture Clophen A 60
Male and female Japanese quail were fed PCB (polychlorinated biphenyl) (Clophen A 60) in concentrations of 0, 50, 100 and 150 ppm for 3 wk during the maturation period (2nd to 4th wk of life). The effects of PCB on gondal histology, sex hormone concentrations in plasma and gonads and plasma Ca levels were investigated. PCB effects on subsequent reproductive processes were measured by evaluating laying capacity, egg, eggshell and semen analysis. In females, no PCB effects were detected on ovary and oviduct weight, nuclear volume and lipid content of the thecal gland cells and on plasma 17beta-estradiol and Ca content. Liver weights were increased in all PCB-treated groups. PCB caused delayed laying and a diminished laying capacity. Egg and shell weights were not affected by PCB treatment or were higher in PCB groups. The breaking strength of the eggs was reduced after PCB ingestion. In males, PCB treatment resulted in a trend towards reduced testis weights, a significantly decreased amount of the testes' seminiferous epithelium and a smaller nuclear volume of the Leydig cells. The lipid content of the latter was not affected and plasma Ca levels were unchanged. Liver weights in all treatment groups were increased. Plasma concentrations of testosterone (T) and 5 alpha-dihydrotestosterone (DHT) or DHT content in the testes were not affected by PCB. T levels in testes were significantly higher after 50 ppm treatment. PCB showed no effect on the percentage of dead spermatozoa in the ejaculates. In another experiment, which consisted of feeding 0 and 150 ppm Clophen, beginning in the 1st wk of life, plasma sex hormone concentrations were measured during the whole experiment from day 24-42 of life. In females, progesterone levels were not greatly affected by PCB but 17 beta-estradiol appeared to be lower before sexual maturity and was more unstable in the PCB group when egg laying occurred. In males, T concentrations or DHT plasma levels were not significantly altered. (BIESSMANN, 1982)

Study #3

  • inhibited hormone binding in a dose-dependent manner (especially in ducks and rabbits)
  • study used Aroclor 1242
The effects of DDE isomers, Aroclor-1242, and chlordane on progesterone/cytoplasmic binding in the eggshell gland mucosa of birds and the uterine mucosa of rabbits were studied in-vitro. Eggshell gland mucosa cytosol obtained from Indian-Runner-ducks, Swedish-Rouen-ducks, and White-Leghorn-hens and the uterine mucosa of rabbits were incubated with 0 to 110x10(-6) molar (M) p,p'-DDE, o,p'-DDE, aroclor-1242, or chlordane. The effects on binding of tritium labeled progesterone to the cytoplasmic receptor were assessed. In untreated cytosol the extent of progesterone receptor binding was significantly higher in hens and rabbits than in the ducks. The DDE isomers, Aroclor-1242, and chlordane inhibited progesterone cytosolic receptor binding in a dose dependent manner. The largest inhibitory effects occurred in ducks and rabbits. o,p'-DDE was more potent than p,p'-DDE in the hens and ducks. In rabbits, the inhibitory effects of o,p'-DDE and p,p'-DDE were similar except at the 110x10(-6)M dose, where o,p'-DDE had a greater effect. Aroclor-1242 and chlordane inhibited progesterone cytosolic receptor binding to a greater extent in ducks. Shell gland mucosa cytosol from hens was incubated with 1x10(-6) to 5x10(-5)M p,p'-DDE, o,p'-DDE, and the calmodulin inhibitors calmidazolium and trifluoperazine. The effects on progesterone cytoplasmic receptor binding were evaluated. Calmidazolium and trifluoperazine inhibited progesterone cytosolic receptor binding to about the same extent as p,p'-DDE, but to a lesser extent than o,p'-DDE. (Lundholm, 1988)

Study #4

  • smaller combs and wattles
  • high mortality
  • weight loss
  • increased liver weight
  • no change in adrenals
  • reduced testes
  • study used PCB commercial mixture Aroclor 1254
The results of some metabolic studies of PCBs (specifically Arochlor 1254) in White Leghorn cockerels are presented in a letter to the editor. Cockerels given 500 ppm PCBs from 1 day of age in a commercial ration had noticeably smaller combs and wattles. Mortality was high, the birds dying between the third and tenth weeks of feeding. At 250 ppm, mortality appeared only by the 13th week of the trial. Six groups of six birds each were then tested to ascertain the PCB effects on body weight, liver, comb, testes and the adrenals. They were fed at 250 ppm for 6, 9 and 13 weeks. Body weight did not show any appreciable change until the ninth week when it was 3/4 of that of the controls; by week 13, the PCB-fed cockerels weighed less than 2/3 as much as did the controls. Liver weights were slightly higher throughout the experiment than in the controls; in terms of the percentage of total body weight, an appreciable increase was noted towards the 13th week. There was no change in the adrenals. The combs showed the striking change already mentioned. Testicular weights were similar between controls and the test birds at 6 weeks. During the next 3 weeks to the 13th week, a significant difference developed, the testes of the PCB-treated birds weighing only [missing percentage] the amount of those of the controls. The slowing of the comb growth appeared before the similar effect in the testes. Data for the results are tabulated. The present observation makes evident the need for further studies of the effects of PCBs on the hormonal system of birds. (Platonow, 1971)

Study #5

  • increased embryo mortality
  • increased abnormalities
  • lower body weights, bursa weights, and liver weights
  • increased spleen and heart weights
  • study used PCBs 77, 105 and 126
Great Lakes waterbird populations have experienced less-than-expected hatchability of eggs and a greater-than-expected incidence of developmental abnormalities. Such deleterious effects have been attributed to polyhalogenated hydrocarbons such as polychlorinated biphenyls (PCBs). PCBs are of primary concern since they are present in significant quantities in the environment. Specific PCB congeners, 3,3',4,4',5-pentachlorobiphenyl (PCB 126), 3,3',4,4'-tetrachlorobiphenyl (PCB 77), and 2,3,3',4,4'-pentachlorobiphenyl (PCB 105), were injected (singly or in combination) into the yolks of White Leghorn chicken (Gallus domesticus) eggs prior to incubation. Teratogenicity was assessed in dead embryos and in hatchlings. Hatchlings were raised for 3 wk to assess body weight gain and mortality. At the end of the 3-wk period, chicks were subjected to necropsy and the brain, bursa, heart, liver, spleen, and testes were removed and weighed. All 3 congeners caused increased embryo mortality, with approximately 50% mortality occurring at 0.6, 8.8, and 5592 micrograms/kg egg for congeners 126, 77, and 105, respectively. All three congeners also produced significantly more abnormalities than the vehicle. Chicks from PCB-injected eggs had lower body weights at wk 2 and 3 of age. Congener 126 caused lower relative bursa weights, congener 77 caused greater relative spleen weights and lower relative liver weights, and all three congeners caused relative heart weights to be greater when compared to control. (Powell et al, 1996)

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Fish Studies

Study #1

  • sac fry mortality
Early life stages of fish are more sensitive than adults to the lethal effects of polychlorinated dibenzo-p-dioxins (PCDDs), dibenzofurans (PCDFs), and biphenyls (PCBs). Part per trillion concentrations of structurally related PCDD, PCDF, and PCB congeners in lake trout (Salvelinus namaycush) and rainbow trout (Oncorhynchus mykiss) eggs manifest toxicity by sac fry mortality associated with yolk sac edema and hemorrhages. In addition, selected PCDD and PCB congeners are more and less potent, respectively, in producing fish early life stage mortality than would be predicted based on their toxic potency in mammals, underscoring the need to determine fish-specific toxic potencies for individual PCDD, PCDF, and PCB congeners known to occur in fish in the environment. Although environmental levels of PCDDs, PCDFs, and PCBs do not produce overt lethality in adult fish, their combined presence in feral fish eggs may pose an increased risk to early life stage survival and, ultimately, to feral fish populations. (Walker et al, 1992)

Study #2

  • death of zebrafish larvae
  • reduced egg production
  • reduced number of oocytes in females
  • induced liver enzyme activity
Zebrafish (Danio rerio) were orally exposed to a mixture of 20 PCBs in three different dose levels (0.008, 0.08, and 0.4 microg of each congener per gram of freeze-dried chironomids). Generally, the PCBs accumulated in a dose-related manner. After 13 weeks of exposure body, liver, and ovary weights, as well as the liver and ovary somatic index, were significantly lower in exposed groups. In addition, the PCB mixture was an effective inducer of hepatic EROD activity. The reproduction study performed with exposed females and unexposed males after 9 weeks revealed that median survival time for larvae was only 7.7 days in the high-dose group as compared with 14 days in controls. Furthermore, egg production was reduced in all three groups exposed. No differences in hatching frequency or median hatching time were recorded. Histologically, females in both the intermediate and high-dose groups contained a reduced number of mature oocytes. The present study demonstrates that the potency of the mixture of selected PCBs induces hepatic EROD activity and has a clearly negative effect on zebrafish reproduction. (Orn et al, 1998)

Study #3

  • altered sex ratios
  • severe gonadal abnormalities
  • inconsistent or extremely limited development of eggs
  • study used PCB commercial mixture Aroclor 1260
Aqueous exposure of newly hatched rainbow trout (Oncorhynchus mykiss) larvae to Aroclor 1260 resulted in altered sex ratios and severe gonadal abnormalities in juvenile females. The proportion of females decreased from 41.9% in combined controls to 31.6 to 36.1% in groups that accumulated 2.5 mug/g Aroclor 1260 after 3-h immersions, although this decrease was not statistically significant (p = 0.057). A total of 18.2% of the females in the treatment group that accumulated 2.1 mug/g Aroclor 1260 had abnormal gonads as compared to 2.7% in combined controls (p = 0.001). Abnormalities were characterized by inconsistent or extremely limited development of oocytes. Although further work is required to validate these results, this study suggests that environmentally realistic tissue concentrations of Aroclor 1260 may disrupt sexual development in female trout. (Matta et al, 1998)

Study #4

  • testicular abnormalities
  • testes selectively accumulate PCBs
  • study used PCB commercial mixture Aroclor 1254
Cod were fed herring containing Aroclor 1254, a polychlorinated biphenyl (PCB), at diet levels of 0, 1, 5, 10, 25, and 50 microgram/g for a period of 5 1/2 months. Histological examinations of the gonads of surviving male fish revealed various testicular abnormalities in 9 of 17 PCB-fed fish but in none of four experimental control and four stock control fish. The abnormalities were observed in testes that were either at functional maturity or in a stage of rapid spermatogenic proliferation but not in testes that were sexually immature or regressed. The testicular abnormalities included disorganization of lobules and spermatogenic elements, inhibition of spermatogenesis, fibrosis of lobule walls, fatty necrosis, and, in one case, total disintegration of the elements in many lobules. There was a significant uptake of PCB by testicular and liver tissues of fish that were fed the higher levels (greater than 1 microgram/g) of Aroclor 1254. (Sangalang et al, 1981)

Study #5

  • altered steroids
  • abnormal testes
  • abnormal gills and livers
  • study used PCB commercial mixture Aroclor 1254
The effects of diet levels of 1, 5, 10, 25 and 50 micrograms Aroclor 1254/g on the Atlantic cod Gadus morhua were determined after a feeding period of 5 1/2 months. Altered steroid biosynthetic patterns in vitro were observed in the testes and head kidneys (adrenal homologue) of the fish that were fed various levels of PCB in vivo. Histological examination of tissues revealed abnormalities in the testes, gills, and livers of the PCB-fed fish. Various testicular abnormalities including slight-to-marked derangement of lobules, hyperplasia of lobule walls and disintegration and/or fatty necrosis of spermatogenic elements were observed in the testes of PCB-fed fish. Hyperplasia of the epithelial layer of the secondary lamellae was observed in the gills of fish on the 5 to 50 micrograms Aroclor 1254/g diet. Fatty degeneration was observed in the livers of all PCB-fed fish. The PCB content of testes, livers and head kidneys were directly proportional to the level of Aroclor 1254 in the diet. It is apparent (incomplete abstract) (Freeman et al, 1982)

Study #6

  • PCBs tend to accumulate in the ovaries, testes, liver and kidneys
The contamination of Baltic herring and pike from six different areas of the Turku archipelago (the southwestern coast of Finland) with DDT, DDE, TDE, and PCB was studied. Herring muscle contained an average of 0. 38 ppm total DDT and 0. 31 ppm PCB on a fresh tissue basis; however, the values obtained for individual fish specimens showed large variations, depending primarily on differences in the fat content of the individual. The range of DDT and PCB concentrations in the herring from the Turku archipelago was similar to that found in herring from the Gulf of Bothnia. Pike muscle contained an average of 0. 04 ppm total DDT and 0. 05 ppm PCBs on a fresh weight basis. There were local differences in the residue concentrations of the samples. The chlorinated hydrocarbons tended to accumulate in the liver and ovaries of the pike and to a lesser degree in the testes and kidneys. Total DDT and PCB concentrations in the ovaries reached 100 ppm and 190 ppm, respectively. (Linko et al, 1974) 

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Sea Stars, Insects and Crustaceans

Study #1

  • reduced reproduction
  • mortality
  • study used PCB commercial mixtures Aroclor 1221, 1232, 1242, 1248, 1254, 1260, 1262 and 1268
Continuous-flow and static bioassys were conducted at 28 degrees C, with survival and reproduction as measures of relative toxicity of 8 polychlorinated biphenyls (PCBs), Aroclor 1221 (A-1221), A-1232, A-1242, A-1248, A-1254, A-1260, A-1262 and A-1268. Three PCB-mixture bioassays were also conducted. Aroclor 1248 was the most toxic to Daphnia magna of the 8 Aroclors tested in static tests; the 3-wk LC50 was 25 mu g/1. Aroclor 1254 was the most toxic PCB to Daphnia under continuous-flow conditions with a 3-wk LC50 of 1.3 mu g/1. Ninety-six-h LC50 values for A-1242, and A-1246 on Gammarus pseudolimnaeus in continuous-flow tests were 73 and 20 mu g/1. Survival after 60 days was 52% at 8.7 mu/1 1242 and 53% at 5.1 mu g/1 A-1248. Reproduction and survival of young were good at 2.8 mu g/1 A-1242 and 2.2 mu g/1 A-1248. The midge Tanytarsus dissimilis, in continuous-flow tests, did not emerge in abundance above 5.1 mu g/1 A-1248 or 3.5 mu g/1 A-1254. The 3-wk LC50 for Aroclor 1254 was 0.65 mu g/1 for larvae and 0.45 mu g/1 for pupae. Tissue residues in Gammarus pseudolimnaeus ranged from 4.9 mu g/g A-1254 in control animals to 552 mu g/g A-1248 in scuds held for 60 days in water containing 5.1 mu g/1 A-1248. (NEBEKER et al, 1974)

Study #2

  • egg maturation delayed
  • disturbed development of embryos
  • reduced survival
  • study used PCB commercial mixture Clophen A50
In semifield experiments sea stars, Asterias rubens, were exposed to 25 micrograms Cd/liter or fed with mussels containing 0.6 microgram/g wet wt PCBs (Clophen A50). After 5 months of exposure, Cd concentrations in testes and ovaries were respectively 17 and 50 times higher than those in unexposed sea stars. PCB concentrations were respectively 7 and 9 times higher. With spermatozoa obtained from Cd- or PCB-exposed sea stars, normal fertilization could be achieved. However, maturation of oocytes from Cd-exposed animals was delayed and early development of embryos from Cd- or PCB-exposed animals was disturbed. Due to aberrations during the early development only 24 and 30% of the embryos obtained from Cd- or PCB-exposed sea stars, respectively, had developed to normal bipinnaria larvae after 1 week. (den Besten et al, 1989)

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References

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Bergeron JM, Crews D, McLachlan JA PCBs as environmental estrogens: turtle sex determination as a biomarker of environmental contamination. Environ Health Perspect 1994 Sep;102(9):780-1 Author Address: Department of Zoology, Institute of Reproductive Biology, University of Texas at Austin 78712, USA.

BIESSMANN A. Effects of polychlorinated biphenyls on gonads, sex hormone balance and reproduction processes of Japanese quail Coturnix coturnix japonica after ingestion during sexual maturation. ENVIRON POLLUT SER A ECOL BIOL; 27 (1). 1982. 15-30. Author Address: Swedish Univ. Agric. Sci., Dep. Pharmacol., Fac. Vet. Med., BMC, Box 573, S-75123 Uppsala, Sweden. 

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De Guise S, Martineau D, Beland P, Fournier M.  Possible mechanisms of action of environmental contaminants on St. Lawrence beluga whales (Delphinapterus leucas).  Environ Health Perspect. 1995 May;103 Suppl 4:73-7.  TOXEN, Universite du Quebec a Montreal, Canada.

den Besten PJ, Herwig HJ, Zandee DI, Voogt PA. Effects of cadmium and PCBs on reproduction of the sea star Asterias rubens: aberrations in the early development. Ecotoxicol Environ Saf; VOL 18, ISS 2, 1989, P173-80 Author Address: Research Group of Aquatic Toxicology, University of Utrecht, The Netherlands. 

de Solla SR, Bishop CA, Van der Kraak G, Brooks RJ. Impact of organochlorine contamination on levels of sex hormones and external morphology of common snapping turtles (Chelydra serpentina serpentina) in Ontario, Canada. Environ Health Perspect; VOL 106, ISS 5, 1998, P253-60 Author Address: Department of Zoology, University of Guelph, Ontario, Canada. 

Freeman HC, Sangalang G, Flemming B The sublethal effects of a polychlorinated biphenyl (Aroclor 1254) diet on the Atlantic cod (Gadus morhua). Sci Total Environ; VOL 24, ISS 1, 1982, P1-11 

Goldman D, Yawetz A The Interference of Aroclor 1254 with Progesterone Metabolism in Guinea Pig Adrenal and Testes Microsomes. Journal of Biochemical Toxicology, Vol. 5, No. 2, pages 99-107, 30 references, 1990 

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Iturri SJ. The effects of various chlorinated hydrocarbons on the cardiovascular physiology and hematology of the domestic fowl. Diss. Abstr. Int. 35(3): 1371B; 1974. Copies of the thesis are available from University Microfilms, Order no. 74-19,823

Lindenau A, Fischer B. Embryotoxicity of polychlorinated biphenyls (PCB). J Reprod Fertil Abstr Ser 1993 Dec;99(12):8  Author Address: Department of Anatomy and Reproductive Biology, RWTH Aachen, Germany.

Lindenau A, Fischer B, Seiler P, Beier HM. Effects of persistent chlorinated hydrocarbons on reproductive tissues in female rabbits. Hum Reprod; VOL 9, ISS 5, 1994, P772-80 Author Address: Department of Anatomy and Reproductive Biology, Medical Faculty, RWTH University of Aachen, Germany. 

Linko RR, Kaitaranta J, Rantamaki P, Eronen L. Occurrence of DDT and PCB compounds in Baltic herring and pike from the Turku archipelago. Environ. Pollut.7(3): 193-207; 1974(REF:23) 

Lundholm CE. The Effects of DDE, PCB and Chlordane on the Binding of Progesterone to Its Cytoplasmic Receptor in the Eggshell Gland Mucosa of Birds and the Endometrium of Mammalian Uterus. Comparative Biochemistry and Physiology, C: Comparative Pharmacology and Toxicology, Vol.89C, No. 2, pages 361-368, 32 references, 1988

Lundkvist U Clinical and reproductive effects of Clophen A50 (PCB) administered during gestation on pregnant guinea pigs and their offspring. Toxicology 1990 Apr 30;61(3):249-57 Author Address: Department of Zoophysiology, Uppsala University, Sweden.

MATTA MB, CAIRNCROSS C, KOCAN RM. Possible effects of polychlorinated biphenyls on sex determination in rainbow trout. ENVIRONMENTAL TOXICOLOGY AND CHEMISTRY; 17 (1). 1998. 26-29. Author Address: National Oceanic Atmospheric Administration, Coastal Resources CoordinationBranch, Bin C15700, Seattle, WA 98115, USA. 

NEBEKER AV, PUGLISI FA. Effect of polychlorinated biphenyls (PCB's) on survival and reproduction of Daphnia, Gammarus, and Tanytarsus. TRANS AM FISH SOC; 103 (4). 1974 722-728 

OEHME M, BISETH A, SCHLABACH M, WIIG O. Concentrations of polychlorinated dibenzo-p-dioxins, dibenzofurans and non-ortho substituted biphenyls in polar bear milk from Svalbard (Norway). ENVIRONMENTAL POLLUTION; 90 (3). 1995. 401-407. Author Address: Norwegian Inst. Air Research, PO Box 100, N-2007 Kjeller, Norway.

OLAFSSON PG, BRYAN AM, STONE W. PCB congener-specific analysis: A critical evaluation of toxic levels in biota. CHEMOSPHERE; 16 (10-12). 1987. 2585-2594. Author Address: Xenobiotics Corp., 762 3rd St., Albany, N.Y. 12206.

Orn S, Andersson PL, Forlin L, Tysklind M, Norrgren L The impact on reproduction of an orally administered mixture of selected PCBs in zebrafish (Danio rerio). Arch Environ Contam Toxicol 1998 Jul;35(1):52-7 Author Address: Faculty of Veterinary Medicine, Department of Pathology, Swedish University of Agricultural Sciences, S-750 07 Uppsala, Sweden.

Platonow NS JR, Funnell HS JR. Anti-androgenic-like effect of polychlorinated biphenyls in cockerels. Vet. Record; 88(4): 109-10 1971; (REF:7)

Powell DC, Aulerich RJ, Stromborg KL, Bursian SJ Effects of 3,3',4,4'-tetrachlorobiphenyl, 2,3,3',4,4'-pentachlorobiphenyl, and 3,3',4,4',5-pentachlorobiphenyl on the developing chicken embryo when injected prior to incubation. J Toxicol Environ Health 1996 Oct 25;49(3):319-38 Author Address: Department of Animal Science, Michigan State University, East Lansing 48824, USA.

Restum JC, Bursian SJ, Giesy JP, Render JA, Helferich WG, Shipp EB, Verbrugge DA, Aulerich RJ Multigenerational study of the effects of consumption of PCB-contaminated carp from Saginaw Bay, Lake Huron, on mink. 1. Effects on mink reproduction, kit growth and survival, and selected biological parameters. J Toxicol Environ Health 1998 Jul 10;54(5):343-75Author Address: Department of Animal Science, Michigan State University, East Lansing 48824, USA.

Ruby S, Mendoza LT, Fournier M, Brousseau P, Degas V. Reproductive system impairment of mice fed diets containing beluga whale blubber from the St Lawrence estuary and arctic populations.  J Toxicol Environ Health A. 2003 Jun 13;66(11):1073-85. Department of Biology, Concordia University, Montreal, Quebec, Canada. sruby@alcor.concordia.ca
Sangalang GB, Freeman HC, Crowell R. Testicular abnormalities in cod (Gadus morhua) fed Aroclor 1254. Arch Environ Contam Toxicol; VOL 10, ISS 5, 1981, P617-26 

SUBRAMANIAN A, TANABE S, TATSUKAWA R, SAITO S, MIYAZAKI N. Reduction in the testosterone levels by PCBs and DDE in Dall's porpoises of northwestern North Pacific. MAR POLLUT BULL; 18 (12). 1987. 643-646. Author Address: Dep. Environ. Conservation, Ehime Univ., Matsuyama 790, Jpn. 

Vos JG, Dybing E, Greim HA, Ladefoged O, Lambré C, Tarazona JV, Brandt I, Vethaak AD. Health effects of endocrine-disrupting chemicals on wildlife, with special reference to the European situation. Crit Rev Toxicol; VOL 30, ISS 1, 2000, P71-133 (REF: 280) Author Address: National Institute of Public Health and the Environment, Bilthoven, The Netherlands.

WADE TL, CHAMBERS L, GARDINALI PR, SERICANO JL, JACKSON TJ, TARPLEY RJ, SUYDAM R. Toxaphene, PCB, DDT, and chlordane analyses of Beluga Whale blubber.  CHEMOSPHERE; 34 (5-7). 1997. 1351-1357.  Author Address: Geochem. and Environ. Res. Group, Tex. A and M Univ., 833 Graham Road, College Station, TX 77845, USA. 

Walker MK, Peterson RE. Toxicity of polychlorinated dibenzo-p-dioxins, dibenzofurans, and biphenyls during early development in fish. Chemically-Induced Alterations in Sexual and Functional Development: the Wildlife/Human Connection (Advances in Modern Environmental Toxicology; v.21) 1992;:195-202. Author Address: Environmental Toxicology Center, University of Wisconsin, Madison, WI.

WIIG O, DEROCHER AE, CRONIN MM, SKAARE JU. Female pseudohermaphrodite polar bears at Svalbard. JOURNAL OF WILDLIFE DISEASES; 34 (4). 1998. 792-796. Author Address: Zool. Mus., Univ. Oslo, Sars gt. 1, N-0562 Oslo, Norway. 

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