Proximity to Pollution Sources and Risk of Amphibian Limb Malformation

Taylor, Brynn; Skelly, David K.; Demarchis, Livia K.; Slade, Martin D.; Galusha, Deron; Rabinowitz, Peter

doi:10.1289/ehp.7585

Cited by 93 publications

(86 citation statements)

References 36 publications

(39 reference statements)

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“…Contaminants have the potential to cause lethal effects in amphibians, such as reduced survival or sub-lethal effects such as immunosuppression, malformations, compromised reproduction and reduction in growth and development (Hecnar, 1995;Taylor et al, 2005;Johnson et al, 2007;Gahl et al, 2011;Groner and Relyea, 2011). For example, the herbicide atrazine has the potential to cause immunosuppression in adult northern leopard frogs (Brodkin et al, 2007) and impair sexual development of male frogs (Hayes et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

Pesticide concentrations in frog tissue and wetland habitats in a landscape dominated by agriculture

Smalling

Reeves

Muths

et al. 2015

Science of The Total Environment

127

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Habitat loss and exposure to pesticides are likely primary factors contributing to amphibian decline in agricultural landscapes. Conservation efforts have attempted to restore wetlands lost through landscape modifications to reduce contaminant loads in surface waters and providing quality habitat to wildlife. The benefits of this increased wetland area, perhaps especially for amphibians, may be negated if habitat quality is insufficient to support persistent populations. We examined the presence of pesticides and nutrients in water and sediment as indicators of habitat quality and assessed the bioaccumulation of pesticides in the tissue of twonative amphibian species Pseudacris maculata (chorus frogs) and Lithobates pipiens (leopard frogs) at six wetlands (3 restored and 3 reference) in Iowa, USA. Restored wetlands are positioned on the landscape to receive subsurface tile drainage water while referencewetlands receive water fromoverland run-off and shallow groundwater sources. Concentrations of the pesticides frequently detected inwater and sediment samples were not different between wetland types. The median concentration of atrazine in surface water was 0.2 μg/ L. Reproductive abnormalities in leopard frogs have been observed in other studies at these concentrations. Nutrient concentrations were higher in the restored wetlands but lower than concentrations thought lethal to frogs. Complex mixtures of pesticides including up to 8 fungicides, some previously unreported in tissue, were detected with concentrations ranging from 0.08 to 1500 μg/kg wet weight. No significant differences in pesticide concentrations were observed between species, although concentrations tended to be higher in leopard frogs compared to chorus frogs, possibly because of differences in life histories. Our results provide information on habitat quality in restored wetlands that will assist state and federal agencies, landowners, and resource managers in identifying and implementing conservation and management actions for these and similar wetlands in agriculturally dominated landscapes. RightsWorks produced by employees of the U.S. Government as part of their official duties are not copyrighted within the U.S. The content of this document is not copyrighted. H I G H L I G H T S• Habitat quality was similar between restored and reference wetlands in Iowa.• Complex mixtures of pesticides are detected in frog tissues (liver and whole body).• The number of fungicides (up to 8) in frog tissues is largest reported to date.• Life history has the potential to impact pesticide bioaccumulation in frogs. Habitat loss and exposure to pesticides are likely primary factors contributing to amphibian decline in agricultural landscapes. Conservation efforts have attempted to restore wetlands lost through landscape modifications to reduce contaminant loads in surface waters and providing quality habitat to wildlife. The benefits of this increased wetland area, perhaps especially for amphibians, may be negated if habitat quality is insufficient t...

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Section: Introductionmentioning

confidence: 99%

Pesticide concentrations in frog tissue and wetland habitats in a landscape dominated by agriculture

Smalling

Reeves

Muths

et al. 2015

Science of The Total Environment

127

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“…Many abnormal amphibians occur in agricultural and non-agricultural areas in the US and Europe where they have been extensively studied (Ouellet et al 1997, Johnson et al 2003, Taylor et al 2005, Piha et al 2006. Abnormalities have also been reported in amphibian species from Asia (Gurushankara et al 2007) and South America.…”

Section: Introductionmentioning

confidence: 99%

“…Some authors have discussed the necessity to assess and categorize different types of abnormalities and their prevalence considering life stage and species affected in order to improve the evaluation of the potential role of different stressors (Ouellet et al 1997, Ankley et al 2004). However, the relationship between the causative agent(s) and the observed abnormalities in the environment is still poorly understood (Kiesecker 2010).Many abnormal amphibians occur in agricultural and non-agricultural areas in the US and Europe where they have been extensively studied (Ouellet et al 1997, Johnson et al 2003, Taylor et al 2005, Piha et al 2006. Abnormalities have also been reported in amphibian species from Asia (Gurushankara et al 2007) and South America.…”

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confidence: 99%

Abnormalities in amphibian populations inhabiting agroecosystems in northeastern Buenos Aires Province, Argentina

Agostini¹,

Kacoliris²,

Demetrio³

et al. 2013

Dis. Aquat. Org.

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The occurrence of abnormalities in amphibians has been reported in many populations, and its increase could be related to environmental pollution and habitat degradation. We evaluated the type and prevalence of abnormalities in 5 amphibian populations from agroecosystems with different degrees of agricultural disturbance (cultivated and reference areas). We detected 9 types of abnormalities, of which the most frequent were those occurring in limbs. The observed prevalence of abnormality in assessed populations from cultivated and reference areas was as follows: Rhinella fernandezae (37.1 and 10.2%, respectively), Leptodactylus latrans adults (28.1 and 9.2%) and juveniles (32.9 and 15.3%), and Hypsiboas pulchellus (11.6 and 2.8%). Scinax granulatus populations did not show abnormalities. Pseudis minuta, which was only detected in the reference area, exhibited a prevalence of 13.3%. For R. fernandezae, L. latrans, and H. pulchellus, generalized linear mixed models showed that prevalence of abnormalities was significantly higher (p < 0.05) in cultivated than in reference areas. L. latrans juveniles were more vulnerable to abnormalities than adults (p < 0.05). The presence of abnormalities in some species inhabiting different agroecosystems suggests that environmental stress factors might be responsible for their occurrence. While we detected pesticides (endosulfan, cypermethrin, and chlorpyrifos) and lower dissolved oxygen levels in ponds of the cultivated area, no data are currently available on how other factors, such as injuries from predators and parasite infections, vary by land use. Further research will be necessary to evaluate possible causes of abnormalities detected in the present study mainly in the context of factor interactions.KEY WORDS: Agricultural disturbance · Pesticide · Brachydactyly · Ectrodactyly · Scoliosis · Developmental abnormality · Teratogen Resale or republication not permitted without written consent of the publisherDis Aquat Org 104: [163][164][165][166][167][168][169][170][171] 2013 studied . Experimental and field evidence supports a causal association between the trematode Ribeiroia and limb malformations (Johnson et al. 2003, Johnson & Hartson 2009. Predators, such as leeches, fish, and odonate naiads, can cause the loss of an appendage and/or abnormalities during the regeneration process . Laboratory studies indicate that UV-B radiation and chemical contaminants, including pesticides used in agricultural practices, can cause malformations (Greulich & Pflugmacher 2003, Brunelli et al. 2009, Agostini et al. 2010), but to date field studies have not provided conclusive evidence (Lannoo 2008. Some of these factors are considered the cause of amphibian population decline and extinction reported on a global scale, although the relationship between amphibian malformations and population declines remains unclear (Blaustein et al. 2011). Some authors have discussed the necessity to assess and categorize different types of abnormalities and their prevalence considering life s...

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“…Although the infections with parasites that were related to eutrophication were thought to be the mechanism of malformation (19,20), the causes for frog deformities still remain controversial (21)(22)(23). Some clues point to RAs, including all-trans-RA (atRA), 13-cis-RA (13cRA), and 9-cis-RA (9cRA), or RA mimics (16,17).…”

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confidence: 99%

Cyanobacteria blooms produce teratogenic retinoic acids

Jiang

Wan

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Deformed amphibians have been observed in eutrophic habitats, and some clues point to the retinoic acids (RAs) or RA mimics. However, RAs are generally thought of as vertebrate-specific hormones, and there was no evidence that RAs exist in cyanobacteria or algae blooms. By analyzing RAs and their analogs 4-oxo-RAs in natural cyanobacteria blooms and cultures of cyanobacteria and algae, we showed that cyanobacteria blooms could produce RAs, which were powerful animal teratogens. Intracellular RAs and 4-oxo-RAs with concentrations between 0.4 and 4.2 × 10 2 ng/L were detected in all bloom materials, and extracellular concentrations measured in water from Taihu Lake, China, were as great as 2.0 × 10 ng/L, which might pose a risk to wildlife through chronic exposure. Further examination of 39 cyanobacteria and algae species revealed that 32 species could produce RAs and 4-oxo-RAs (1.6-1.4 × 10 3 ng/g dry weight), and the dominant cyanobacteria species in Taihu Lake, Microcystis flos-aquae and Microcystis aeruginosa, produced high amounts of RAs and 4-oxo-RAs with concentrations of 1.4 × 10 3 and 3.7 × 10 2 ng/g dry weight, respectively. Most genera of cyanobacteria that could produce RAs and 4-oxo-RAs, such as Microcystis, Anabaena, and Aphanizomenon, often occur dominantly in blooms. Production of RAs and 4-oxo-RAs by cyanobacteria was associated with species, origin location, and growth stage. These results represent a conclusive demonstration of endogenous production of RAs in freshwater cyanobacteria blooms. The observation of teratogenic RAs in cyanobacteria is evolutionarily and ecologically significant because RAs are vertebrate-specific hormones, and cyanobacteria form extensive and highly visible blooms in many aquatic ecosystems.eutrophication | phytoplankton | deformities | Asia

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Proximity to Pollution Sources and Risk of Amphibian Limb Malformation

Cited by 93 publications

References 36 publications

Pesticide concentrations in frog tissue and wetland habitats in a landscape dominated by agriculture

Pesticide concentrations in frog tissue and wetland habitats in a landscape dominated by agriculture

Abnormalities in amphibian populations inhabiting agroecosystems in northeastern Buenos Aires Province, Argentina

Cyanobacteria blooms produce teratogenic retinoic acids

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