Amphibians and agricultural chemicals: Review of the risks in a complex environment

Declining amphibian populations have been reported in the past twenty years from locations all over the world. These events have been attributed variously — often without much evidence — to habitat loss, climate change and disease. Now a case study of the northern leopard frog, Rana pipiens, in wetlands across Minnesota points to the use of agrochemicals — combined with parasitic infestation — as a contributor to population decline. The study sought factors associated with the abundance of larval trematodes in the frogs. An abundance of these parasites can be debilitating, causing limb malformation, kidney damage and death. Of more than 240 plausible predictors of trematode infection — ranging from the presence of various plant and animal species to agrochemicals and habitat geography — two stood out: the herbicide atrazine and the fertilizer, phosphate. Atrazine and phosphate are principal agrochemicals for corn and sorghum production, and together they accounted for 74% of the variation in trematode abundance. Global amphibian declines have often been attributed to disease1,2, but ignorance of the relative importance and mode of action of potential drivers of infection has made it difficult to develop effective remediation. In a field study, here we show that the widely used herbicide, atrazine, was the best predictor (out of more than 240 plausible candidates) of the abundance of larval trematodes (parasitic flatworms) in the declining northern leopard frog Rana pipiens. The effects of atrazine were consistent across trematode taxa. The combination of atrazine and phosphate—principal agrochemicals in global corn and sorghum production—accounted for 74% of the variation in the abundance of these often debilitating larval trematodes (atrazine alone accounted for 51%). Analysis of field data supported a causal mechanism whereby both agrochemicals increase exposure and susceptibility to larval trematodes by augmenting snail intermediate hosts and suppressing amphibian immunity. A mesocosm experiment demonstrated that, relative to control tanks, atrazine tanks had immunosuppressed tadpoles, had significantly more attached algae and snails, and had tadpoles with elevated trematode loads, further supporting a causal relationship between atrazine and elevated trematode infections in amphibians. These results raise concerns about the role of atrazine and phosphate in amphibian declines, and illustrate the value of quantifying the relative importance of several possible drivers of disease risk while determining the mechanisms by which they facilitate disease emergence.

Agrochemicals increase trematode infections in a declining amphibian species

https://digitalcommons.usf.edu/cgi/viewcontent.cgi?article=1370&context=bin_facpub

Demasculinization and feminization of male gonads by atrazine: Consistent effects across vertebrate classes

ObjectiveThe biological effects of the herbicide atrazine on freshwater vertebrates are highly controversial. In an effort to resolve the controversy, we conducted a qualitative meta-analysis on th...

A qualitative meta-analysis reveals consistent effects of atrazine on freshwater fish and amphibians.

Environmental change has negatively affected most biological systems on our planet and is becoming of increasing concern for the well-being and survival of many species. At an organism level, effects encompass not only endocrine disruptions, sex-ratio changes and decreased reproductive parameters, but also include teratogenic and genotoxic effects, immunosuppression and other immune-system impairments that can lead directly to disease or increase the risk of acquiring disease. Living organisms will strive to maintain health by recognizing and resolving abnormal situations, such as the presence of invading microorganisms or harmful peptides, abnormal cell replication and deleterious mutations. However, fast-paced environmental changes may pose additional pressure on immunocompetence and health maintenance, which may seriously impact population viability and persistence. Here, we outline the importance of a functional immune system for survival and examine the effects that exposure to a rapidly changing environment might exert on immunocompetence. We then address the various levels at which anthropogenic environmental change might affect wildlife health and identify potential deficits in reproductive parameters that might arise owing to new immune challenges in the context of a rapidly changing environment. Throughout the paper, a series of examples and case studies are used to illustrate the impact of environmental change on wildlife health.

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Effects of environmental change on wildlife health

Atrazine, the most widely used herbicide in the United States, has been shown in several studies to be an endocrine disruptor in adult frogs. Results from this study indicate that atrazine also functions as an immune disruptor in frogs. Exposure to atrazine (21 ppb for 8 d) affects the innate immune response of adult Rana pipiens in similar ways to acid exposure (pH 5.5), as we have previously shown. Atrazine exposure suppressed the thioglycollate-stimulated recruitment of white blood cells to the peritoneal cavity to background (Ringer exposed) levels and also decreased the phagocytic activity of these cells. Unlike acid exposure, atrazine exposure did not cause mortality. Our results, from a dose-response study, indicate that atrazine acts as an immune disruptor at the same effective doses that it disrupts the endocrine system. Keywords—Atrazine Immune disruption Frog Rana pipiens

Atrazine is an immune disruptor in adult northern leopard frogs (Rana pipiens)

Acidic environments are physiological stressors for amphibians. The objective of the present study was to document the effect of an acidic environment on innate immune system function under controlled experimental conditions in Rana pipiens. We developed an in vivo assay, by injecting a suspension of 1-μm fluorescent beads in fluid thioglycollate, to induce peritonitis. The number of peritoneal exudate leukocytes and their phagocytic activity did not increase with thioglycollate injection when frogs were exposed to pH 5.5 compared to when frogs were exposed to pH 7.0. An environment of pH 5.5 disrupted the inflammatory response of frogs compared to an environment of pH 7.0; at pH 5.5, more nonphagocytic leukocytes and fewer highly phagocytic leukocytes were found compared to those in frogs exposed to pH 7.0. Frogs stimulated by thioglycollate injection and exposed to pH 5.5 had a 50% increase in cells that did not exhibit phagocytosis and a 4- to 10-fold reduction in the number of highly phagocytic cells. This is evidence that acid exposure functions as an immune disruptor in adult R. pipiens under laboratory conditions.

https://science.widener.edu/~vatnick/etc_2006.pdf

Muthuramanan Rameswaran

Papers

Atrazine is an immune disruptor in adult northern leopard frogs (Rana pipiens)

Acid exposure is an immune disruptor in adult Rana pipiens.