Synthesis of Maternal Transfer of Mercury in Birds: Implications for Altered Toxicity Risk.

Maternal transfer is a predominant route of methylmercury (MeHg) exposure to offspring. We reviewed and synthesized published and unpublished data on maternal transfer of MeHg in birds. Using paired samples of females' blood (n = 564) and their eggs (n = 1814) from 26 bird species in 6 taxonomic orders, we conducted a meta-analysis to evaluate whether maternal transfer of MeHg to eggs differed among species and caused differential toxicity risk to embryos. Total mercury (THg) concentrations in eggs increased with maternal blood THg concentrations; however, the proportion of THg transferred from females to their eggs differed among bird taxa and with maternal THg exposure. Specifically, a smaller proportion of maternal THg was transferred to eggs with increasing female THg concentrations. Additionally, the proportion of THg that was transferred to eggs at the same maternal blood THg concentration differed among taxonomic orders, with waterfowl (Anseriformes) transferring up to 382% more THg into their eggs than songbirds (Passeriformes). We provide equations to predict THg concentrations in eggs using female blood THg concentrations, and vice versa, which may help translate toxicity benchmarks across tissues and life stages. Our results indicate that toxicity risk of MeHg can vary among bird taxa due to differences in maternal transfer of MeHg to offspring.

A comparison of the teratogenicity of methylmercury and selenomethionine injected into bird eggs.

Methylmercury chloride and seleno-L-methionine were injected separately or in combinations into the fertile eggs of mallards (Anas platyrhynchos), chickens (Gallus gallus), and double-crested cormorants (Phalacrocorax auritus), and the incidence and types of teratogenic effects were recorded. For all three species, selenomethionine alone caused more deformities than did methylmercury alone. When mallard eggs were injected with the lowest dose of selenium (Se) alone (0.1 µg/g), 28 of 44 embryos and hatchlings were deformed, whereas when eggs were injected with the lowest dose of mercury (Hg) alone (0.2 µg/g), only 1 of 56 embryos or hatchlings was deformed. Mallard embryos seemed to be more sensitive to the teratogenic effects of Se than chicken embryos: 0 of 15 chicken embryos or hatchlings from eggs injected with 0.1 µg/g Se exhibited deformities. Sample sizes were small with double-crested cormorant eggs, but they also seemed to be less sensitive to the teratogenic effects of Se than mallard eggs. There were no obvious differences among species regarding Hg-induced deformities. Overall, few interactions were apparent between methylmercury and selenomethionine with respect to the types of deformities observed. However, the deformities spina bifida and craniorachischisis were observed only when Hg and Se were injected in combination. One paradoxical finding was that some doses of methylmercury seemed to counteract the negative effect selenomethionine had on hatching of eggs while at the same time enhancing the negative effect selenomethionine had on creating deformities. When either methylmercury or selenomethionine is injected into avian eggs, deformities start to occur at much lower concentrations than when the Hg or Se is deposited naturally in the egg by the mother.

Hormesis associated with a low dose of methylmercury injected into mallard eggs.

We injected mallard (Anas platyrhynchos) eggs with methylmercury chloride at doses of 0, 0.05, 0.1, 0.2, 0.4, 0.8, 1.6, 3.2, and 6.4 µg mercury/g egg contents on a wet-weight basis. A case of hormesis seemed to occur because hatching success of eggs injected with 0.05 µg/g mercury (the lowest dose) was significantly greater (93.3%) than that of controls (72.6%), whereas hatching success decreased at progressively greater doses of mercury. Our finding of hormesis when a low dose of methylmercury was injected into eggs agrees with a similar observation in a study in which a group of female mallards was fed a low dietary concentration of methylmercury and hatching of their eggs was significantly better than that of controls. If methylmercury has a hormetic effect at low concentrations in avian eggs, these low concentrations may be important in a regulatory sense in that they may represent a no-observed adverse effect level (NOAEL).

Predicting mercury concentrations in mallard eggs from mercury in the diet or blood of adult females and from duckling down feathers.

Measurements of Hg concentrations in avian eggs can be used to predict possible harm to reproduction, but it is not always possible to sample eggs. When eggs cannot be sampled, some substitute tissue, such as female blood, the diet of the breeding female, or down feathers of hatchlings, must be used. When female mallards (Anas platyrhynchos) were fed diets containing methylmercury chloride, the concentration of Hg in a sample of their blood was closely correlated with the concentration of Hg in the egg they laid the day they were bled (r2 = 0.88; p < 0.001). Even when the blood sample was taken more than two weeks after an egg was laid, there was a strong correlation between Hg concentrations in female blood and eggs (r2 = 0.67; p < 0.0002). When we plotted the dietary concentrations of Hg we fed to the egg-laying females against the concentrations of Hg in their eggs, the r2 value was 0.96 (p < 0.0001). When the concentrations of Hg in the down feathers of newly hatched ducklings were plotted against Hg in the whole ducklings, the r2 value was 0.99 (p < 0.0003). Although measuring Hg in eggs may be the most direct way of predicting possible embryotoxicity, our findings demonstrate that measuring Hg in the diet of breeding birds, in the blood of egg-laying females, or in down feathers of hatchlings all can be used to estimate what concentration of Hg may have been in the egg.

Enhanced reproduction in mallards fed a low level of methylmercury: an apparent case of hormesis.

Breeding pairs of mallards (Anas platyrhynchos) were fed a control diet or a diet containing 0.5 microg/g mercury (Hg) in the form of methylmercury chloride. There were no effects of Hg on adult weights and no overt signs of Hg poisoning in adults. The Hg-containing diet had no effect on fertility of eggs, but hatching success of eggs was significantly higher for females fed 0.5 microg/g Hg (71.8%) than for controls (57.5%). Survival of ducklings through 6 d of age was the same (97.8%) for controls and mallards fed 0.5 microg/g mercury. However, the mean number of ducklings produced per female was significantly higher for the pairs fed 0.5 microg/g Hg (21.4) than for controls (16.8). Although mercury in the parents' diet had no effect on mean duckling weights at hatching, ducklings from parents fed 0.5 microg/g Hg weighed significantly more (mean = 87.2 g) at 6 d of age than did control ducklings (81.0 g). The mean concentration of Hg in eggs laid by parents fed 0.5 microg/g mercury was 0.81 microg/g on a wet-weight basis. At this time, one cannot rule out the possibility that low concentrations of Hg in eggs may be beneficial, and this possibility should be considered when setting regulatory thresholds for methylmercury.

Intraperitoneal injections as a possible means of generating varied levels of methylmercury in the eggs of birds in field studies.

The ideal study of the effects of methylmercury on the reproductive success of a species of bird would be one in which eggs contained mercury concentrations ranging from controls to very heavily contaminated, all at the same site. Such a study cannot be realized at a Hg-contaminated area or under laboratory conditions but could be achieved by introducing methylmercury into breeding females and allowing them to deposit Hg in their eggs. Female mallards (Anas platyrhynchos) were intraperitoneally injected with solutions of methylmercury chloride dissolved in corn oil, propylene glycol, dimethyl sulfoxide, mineral oil, Olestra, Crisco, lard, hard paraffin, and a combination of hard and soft paraffin. In some cases, egg laying was delayed, as a result of either the solvent itself (in the case of Olestra, Crisco, and lard) or the highest concentration of methylmercury chloride (500 microg/g) in some of the solvents. Mercury in eggs ranged from a control level (<0.1 microg/g) to approximately 14 microg/g on a wet weight basis, which more than covers the range of concentrations reported in wild bird eggs. Mercury concentrations in a series of eggs from the same female declined mostly as a result of excretion of Hg in prior eggs and not because of the length of time since the injection. Intraperitoneal injections hold promise in field studies in which one would like to study the reproductive effects of a wide range of methylmercury levels in the eggs of a wild bird and under the natural conditions that exist in the field.

Reproduction in mallards exposed to dietary concentrations of methylmercury.

The purpose of this experiment was to use mallards (Anas platyrhynchos) tested under controlled conditions to determine how much harm to reproduction resulted from various concentrations of mercury in eggs. Breeding pairs of mallards were fed a control diet or diets containing 1, 2, 4, or 8 microg/g mercury, as methylmercury chloride. Mean concentrations of mercury in eggs laid by parents fed 0, 1, 2, 4, or 8 microg/g mercury were 0.0, 1.6, 3.7, 5.9, and 14 microg/g mercury on a wet-weight basis. There were no signs of mercury poisoning in the adults, and fertility and hatching success of eggs were not affected by mercury. Survival of ducklings and the number of ducklings produced per female were reduced by the 4 and 8-microg/g dietary mercury treatments (that resulted in 5.9 and 14 microg/g mercury in their eggs, respectively). Ducklings from parents fed the various mercury diets were just as heavy as controls at hatching, but by 6 days of age ducklings whose parents had been fed 4 or 8 microg/g mercury weighed less than controls. Because we do not know if absorption of mercury from our diets would be the same as absorption from natural foods, the mercury concentrations we report in eggs may be more useful in extrapolating to possible harmful effects in nature than are the dietary levels we fed. We conclude that mallard reproduction does not appear to be particularly sensitive to methylmercury.

A simplified method for correcting contaminant concentrations in eggs for moisture loss.

We developed a simplified and highly accurate method for correcting contaminant concentrations in eggs for the moisture that is lost from an egg during incubation. To make the correction, one injects water into the air cell of the egg until overflowing. The amount of water injected corrects almost perfectly for the amount of water lost during incubation or when an egg is left in the nest and dehydrates and deteriorates over time. To validate the new method we weighed freshly laid chicken (Gallus gallus) eggs and then incubated sets of fertile and dead eggs for either 12 or 19 d. We then injected water into the air cells of these eggs and verified that the weights after water injection were almost identical to the weights of the eggs when they were fresh. The advantages of the new method are its speed, accuracy, and simplicity: It does not require the calculation of a correction factor that has to be applied to each contaminant residue.

Rapid increases in mercury concentrations in the eggs of mallards fed methylmercury.

To determine how quickly breeding birds would have to feed in a mercury-contaminated area before harmful concentrations of mercury, as methylmercury, built up in their eggs, we fed female mallards (Anas platyrhynchos) a control diet or diets containing 0.5, 1, 2, 4, or 8 microg/g mercury (on what was close to a dry weight basis) as methylmercury chloride for 23 d. After 18 d on their respective mercury diets, the eggs of mallards fed 0.5, 1, 2, 4, or 8 microg/g mercury contained 97.8, 86.0, 89.9, 88.9, and 85.9%, respectively, of the peak concentrations reached after 23 d. Depending on the dietary concentration of mercury, no more than approximately a week may be required for harmful concentrations (0.5-0.8 microg/g, wet weight) to be excreted into eggs.

A nonlethal microsampling technique to monitor the effects of mercury on wild bird eggs.

Methylmercury is the predominant chemical form of mercury reported in the eggs of wild birds, and the embryo is the most sensitive life stage to methylmercury toxicity. Protective guidelines have been based mainly on captive-breeding studies with chickens (Gallus gallus), mallards (Anas platyrhynchos), and ring-necked pheasants (Phasianus colchicus) or on field studies where whole eggs were collected and analyzed and the effects of the mercury were measured based on the reproductive success of the remaining eggs. However, both of these methods have limitations. As an alternative, we developed a technique that involves extracting a small sample of albumen from a live egg, sealing the egg, returning the egg to its nest to be naturally incubated by the parents, and then relating the hatching success of this microsampled egg to its mercury concentration. After first developing this technique in the laboratory using chicken and mallard eggs, we selected the laughing gull (Larus atricilla) and black-necked stilt (Himantopus mexicanus) as test subjects in the field. We found that 92% of the microsampled laughing gull eggs met our reproductive endpoint of survival to the beginning of hatching compared to 100% for the paired control eggs within the same nests. Microsampled black-necked stilt eggs exhibited 100% hatching success compared to 93% for the paired control eggs. Our results indicate that microsampling is an effective tool for nonlethally sampling mercury concentrations in eggs and, as such, can be used for monitoring sensitive species, as well as for improving studies that examine the effects of mercury on avian reproduction.

Species differences in the sensitivity of avian embryos to methylmercury.

We injected doses of methylmercury into the air cells of eggs of 26 species of birds and examined the dose-response curves of embryo survival. For 23 species we had adequate data to calculate the median lethal concentration (LC(50)). Based on the dose-response curves and LC(50)s, we ranked species according to their sensitivity to injected methylmercury. Although the previously published embryotoxic threshold of mercury in game farm mallards (Anas platyrhynchos) has been used as a default value to protect wild species of birds, we found that, relative to other species, mallard embryos are not very sensitive to injected methylmercury; their LC(50 )was 1.79 microg/g mercury on a wet-weight basis. Other species we categorized as also exhibiting relatively low sensitivity to injected methylmercury (their LC(50)s were 1 microg/g mercury or higher) were the hooded merganser (Lophodytes cucullatus), lesser scaup (Aythya affinis), Canada goose (Branta canadensis), double-crested cormorant (Phalacrocorax auritus), and laughing gull (Larus atricilla). Species we categorized as having medium sensitivity (their LC(50)s were greater than 0.25 microg/g mercury but less than 1 microg/g mercury) were the clapper rail (Rallus longirostris), sandhill crane (Grus canadensis), ring-necked pheasant (Phasianus colchicus), chicken (Gallus gallus), common grackle (Quiscalus quiscula), tree swallow (Tachycineta bicolor), herring gull (Larus argentatus), common tern (Sterna hirundo), royal tern (Sterna maxima), Caspian tern (Sterna caspia), great egret (Ardea alba), brown pelican (Pelecanus occidentalis), and anhinga (Anhinga anhinga). Species we categorized as exhibiting high sensitivity (their LC(50)s were less than 0.25 microg/g mercury) were the American kestrel (Falco sparverius), osprey (Pandion haliaetus), white ibis (Eudocimus albus), snowy egret (Egretta thula), and tri-colored heron (Egretta tricolor). For mallards, chickens, and ring-necked pheasants (all species for which we could compare the toxicity of our injected methylmercury with that of published reports where methylmercury was fed to breeding adults and was deposited into the egg by the mother), we found the injected mercury to be more toxic than the same amount of mercury deposited naturally by the mother. The rank order of sensitivity of these same three species to methylmercury was, however, the same whether the methylmercury was injected or maternally deposited in the egg (i.e., the ring-necked pheasant was more sensitive than the chicken, which was more sensitive than the mallard). It is important to note that the dose-response curves and LC(50)s derived from our egg injections are useful for ranking the sensitivities of various species but are not identical to the LC(50)s that would be observed if the mother bird had put the same concentrations of mercury into her eggs; the LC(50)s of maternally deposited methylmercury would be higher.

Further declines in organochlorines in eggs of red-breasted mergansers from Lake Michigan, 1977-1978 versus 1990 versus 2002.

From 1977-1978 to 1990, concentrations of polychlorinated biphenyls (PCBs) and most organochlorine pesticides declined in eggs of red-breasted mergansers (Mergus serrator) nesting on islands in northwestern Lake Michigan. Further declines took place between 1990 and 2002. Between 1977-1978 and 1990 total PCBs decreased 60% (from 21 to 8.5 microg/g, wet weight). An additional decline of 46% took place between 1990 and 2002 (8.5 to 4.6 microg/g). Between 1977-1978 and 1990 p,p (')-DDE decreased 66% (from 6.5 to 2.2 microg/g), and from 1990 to 2002 an additional decline of 36% took place (from 2.2 to 1.4 microg/g). Between 1977-1978 and 1990 dieldrin decreased only 16% (from 0.82 to 0.69 microg/g), but from 1990 to 2002 a 96% decrease occurred (from 0.69 to 0.03 microg/g).

Phosphorus amendment reduces hepatic and renal oxidative stress in mallards ingesting lead-contaminated sediments.

Lead poisoning of waterfowl has been reported for decades in the Coeur d'Alene River Basin (CDARB) in Idaho as a result of the ingestion of lead-contaminated sediments. This study was conducted to determine whether the addition of phosphoric acid to CDARB sediments would reduce the bioavailability and toxicity of lead to the liver and kidney of mallards (Anas platyrhynchos). Mallards received diets containing 12% clean sediment (controls) or 12% sediment from three different CDARB sites containing 4520, 5390, or 6990 microg/g lead (dry weight) with or without phosphoric acid amendment. Liver and kidney lead concentrations were significantly higher in all CDARB treatment groups and ranged from geometric mean values of 18.2 (liver) and 28.7 (kidney) for the first 2 sites to 22.5 (liver) and 45.6 (kidney) microg/g (wet weight) for the third site. With amendments all liver lead concentrations were reduced 36 to 55%, and all kidney lead concentrations were lowered 54 to 73%. Unamended CDARB sediment from the third site resulted in the following hepatic effects: over 1.6-fold elevation of liver glutathione (reduced form; GSH) concentration, higher GSH S-transferase and oxidized glutathione (GSSG) reductase activities, and lower protein-bound thiols (PBSH) concentration. Renal effects included higher kidney GSH concentrations for all CDARB sites, with over 2.1-fold higher for the third site. Resulting kidney GSSG to GSH ratios were lower at two sites. At the third site, gamma-glutamyl transferase (GGT) activity was elevated, and lipid peroxidation as thiobarbituric acid-reactive substances (TBARS) was 1.7-fold greater. Amendment restored all hepatic variables as well as the renal variables TBARS and GGT so they did not differ from controls. Although amendments of phosphorus substantially reduced the bioavailability of lead and some of the adverse effects, lead concentrations in the tissues of mallards fed the amended sediments were still above those considered to be harmful to waterfowl under the present conditions.

Risk assessment test for lead bioaccessibility to waterfowl in mine-impacted soils.

Due to variations in soil physicochemical properties, species physiology, and contaminant speciation, Pb toxicity is difficult to evaluate without conducting in vivo dose-response studies. Such tests, however, are expensive and time consuming, making them impractical to use in assessment and management of contaminated environments. One possible alternative is to develop a physiologically based extraction test (PBET) that can be used to measure relative bioaccessibility. We developed and correlated a PBET designed to measure the bioaccessibility of Pb to waterfowl (W-PBET) in mine-impacted soils located in the Coeur d'Alene River Basin, Idaho. The W-PBET was also used to evaluate the impact of P amendments on Pb bioavailability. The W-PBET results were correlated to waterfowl-tissue Pb levels from a mallard duck [Anas platyrhynchos (L.)] feeding study. The W-PBET Pb concentrations were significantly less in the P-amended soils than in the unamended soils. Results from this study show that the W-PBET can be used to assess relative changes in Pb bioaccessibility to waterfowl in these mine-impacted soils, and therefore will be a valuable test to help manage and remediate contaminated soils.

Mercury accumulation and loss in mallard eggs.

Female mallards (Anas platyrhynchos) were fed diets containing 5, 10, or 20 ppm mercury as methylmercury chloride. One egg was collected from each bird before the start of the mercury diets and 15 eggs were collected from each bird while it was being fed mercury. The mercury diets were then replaced by uncontaminated diets, and each female was allowed to lay 29 more eggs. Mercury levels in eggs rose to about 7, 18, and 35 ppm wet-weight in females fed 5, 10, or 20 ppm mercury, respectively. Mercury levels fell to about 0.16, 0.80, and 1.7 ppm in the last egg laid by birds that had earlier been fed 5, 10, or 20 ppm mercury, respectively. Higher concentrations of mercury were found in egg albumen than in yolk, and between 95 and 100% of the mercury in the eggs was in the form of methylmercury.

Comparative embryotoxicity of a pentabrominated diphenyl ether mixture to common terns (Sterna hirundo) and American kestrels (Falco sparverius).

Concentrations of polybrominated diphenyl ethers (PBDEs) in Forster's tern (Sterna forsteri) eggs from San Francisco Bay have been reported to range up to 63µgg(-1) lipid weight. This value exceeds the lowest-observed-adverse-effect level (1.8µgg(-1) egg wet weight; ∼32µg(-1) lipid weight) reported in an embryotoxicity study with American kestrels (Falco sparverius). As a surrogate for Forster's terns, common tern (Sterna hirundo) eggs were treated by air cell injection with corn oil vehicle (control) or a commercial penta-BDE formulation (DE-71) at nominal concentrations of 0.2, 2, and 20µgg(-1) egg. As a positive control, kestrel eggs received vehicle or 20µg DE-71g(-1) egg. In terns, there were no effects of DE-71 on embryonic survival, and pipping or hatching success; however, treated eggs hatched later (0.44d) than controls. Organ weights, organ-to-body weight ratios, and bone lengths did not differ, and histopathological observations were unremarkable. Several measures of hepatic oxidative stress in hatchling terns were not affected by DE-71, although there was some evidence of oxidative DNA damage (8-hydroxy-deoxyguanosine; 8-OH-dG). Although DE-71 did not impair pipping and hatching of kestrels, it did result in a delay in hatch, shorter humerus length, and reduced total thyroid weight. Concentrations of oxidized glutathione, reduced glutathione, thiobarbituric acid reactive substances, and 8-OH-dG in liver were greater in DE-71-treated kestrels compared to controls. Our findings suggest common tern embryos, and perhaps other tern species, are less sensitive to PBDEs than kestrel embryos.

Interactions between methylmercury and selenomethionine injected into mallard eggs.

Methylmercury chloride and seleno-L-methionine were injected separately or in combinations into mallard eggs (Anas platyrhynchos), and embryo mortality and teratogenic effects (deformities) were modeled using a logistic regression model. Methylmercury was injected at doses that resulted in concentrations of 0, 0.2, 0.4, 0.8, and 1.6 µg/g Hg in the egg on a wet weight basis and selenomethionine at doses that resulted in concentrations of 0, 0.1, 0.2, 0.4, and 0.6 µg/g Se in the egg, also on a wet weight basis. When selenomethionine and methylmercury were injected separately, hatching probability decreased in both cases. However, when methylmercury was injected at 1.6 µg/g in combination with selenomethionine at 0.2 µg/g, the presence of the methylmercury resulted in less embryo mortality than had been seen with 0.2 µg/g Se by itself, but it increased the number of deformed embryos and hatchlings. Selenomethionine appeared to be more embryotoxic than equivalent doses of methylmercury when injected into eggs, and both injected methylmercury and selenomethionine were more toxic to mallard embryos than when deposited naturally in the egg by the mother. The underlying mechanisms behind the interactions between methylmercury and selenomethionine and why methylmercury appeared to improve hatching probability of Se-dosed eggs yet increased deformities when the two compounds were combined are unclear. These findings warrant further studies to understand these mechanisms in both laboratory and field settings.

Toxicity of methylmercury injected into eggs when dissolved in water versus corn oil.

In a previous study, the embryotoxicity of methylmercury dissolved in corn oil was compared among 26 species of birds. Corn oil is not soluble in the water-based matrix that constitutes the albumen of an egg. To determine whether the use of corn oil limited the usefulness of this earlier study, a comparison was made of the embryotoxicity of methylmercury dissolved in corn oil versus water. Mallard (Anas platyrhynchos) and chicken (Gallus gallus) eggs were injected with methylmercury chloride dissolved in corn oil or water to achieve concentrations of 0, 0.2, 0.4, 0.8, and 1.6 µg/g mercury in the egg on a wet weight basis. Hatching success at each dose of mercury was compared between the two solvents. For mallards, 16.4% of the eggs injected with 1.6 µg/g mercury dissolved in water hatched, which was statistically lower than the 37.6% hatch rate of eggs injected with 1.6 µg/g mercury dissolved in corn oil, but no differences in hatching success were observed between corn oil and water at any of the other doses. With chicken eggs, no significant differences occurred in percentage hatch of eggs between corn oil and water at any of the mercury doses. Methylmercury dissolved in corn oil seems to have a toxicity to avian embryos similar to that of does methylmercury dissolved in water. Consequently, the results from the earlier study that described the toxicity of methylmercury dissolved in corn oil to avian embryos were probably not compromised by the use of corn oil as a solvent.

Teratogenic effects of injected methylmercury on avian embryos.

Controlled laboratory studies with game farm mallards (Anas platyrhynchos) and chickens (Gallus gallus) have demonstrated that methylmercury can cause teratogenic effects in birds, but studies with wild species of birds are lacking. To address this need, doses of methylmercury chloride were injected into the eggs of 25 species of birds, and the dead embryos and hatched chicks were examined for external deformities. When data for controls were summed across all 25 species tested and across all types of deformities, 24 individuals out of a total of 1,533 (a rate of 1.57%) exhibited at least one deformity. In contrast, when data for all of the mercury treatments and all 25 species were summed, 188 deformed individuals out of a total of 2,292 (8.20%) were found. Some deformities, such as lordosis and scoliosis (twisting of the spine), misshapen heads, shortening or twisting of the neck, and deformities of the wings, were seldom observed in controls but occurred in much greater frequency in Hg-treated individuals. Only 0.59% of individual control dead embryos and hatchlings exhibited multiple deformities versus 3.18% for Hg-dosed dead embryos and hatchlings. Methylmercury seems to have a widespread teratogenic potential across many species of birds.