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McCoy, KA, LJ Bortnick, CM Campbell, HM Hamlin, LJ Guillette Jr., and CM St. Mary. 2008. Agriculture Alters Gonadal Form and Function in Bufo marinus. Environmental Health Perspectives |
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Scientists in Florida report that intersex conditions found in amphibians are associated with agricultural land use. Comparing areas of heavy agricultural use with a series of other locations, including suburbs, they found that the greater the intensity of agriculture, the higher the proportion of abnormal frogs. In the most heavily farmed area, almost 40% of male toads have abnormalities that make them less male and more like females. The results suggest that agricultural chemicals may be responsible. Finding these significantly gender-challenged toads also raises concerns that the cause of the abnormalities may be at least partly to blame for the worldwide amphibian declines. |
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A cane toad, Bufo marinus
Photo by Michael Henderson(c) |
Context: Many synthetic chemicals found in the environment act as estrogen hormones. These contaminants can cause female-like qualities in males exposed to them during development.
Hormones are essential molecules that act as signaling agents to guide almost every important life process, including development, growth, metabolism and reproduction. The major vertebrate animal groups - fish, amphibians, reptiles and mammals - all produce similar sex hormones, including the estrogen estradiol and the androgen testosterone.
Estrogens are a group of hormones best known for their role in guiding female development and producing feminine qualities in animals. In people, these messenger molecules are responsible for creating cell-to-cell signals that guide the growth of the ovaries and other female reproductive organs during development, breast enlargement at puberty and the menstrual cycle during adult life.
Because of the similarities in how sex hormones work in males and females, some chemicals that perform like estrogen can produce female traits in (or feminize) males if exposure occurs during important times of development. In a similar way, the compounds that feminize individuals in one animal group, are likely to feminize those in other groups.
Agricultural areas are often polluted with pesticides, which are used to control weeds, insects and fungus, and their residues. Both can remain in the soil and water after application and can be carried by wind and other weather to places all over the world. Laboratory studies have confirmed that many of these pesticides can feminize animals exposed to them.
Field studies, though, are not so cut and dry. There remains some disagreement by scientists over the role of agricultural contaminants in abnormal gonad development and physical deformities that are found in wild populations of amphibians.
The pesticide atrazine, for example, causes ovarian tissue to grow inside male frogs (Hayes et al. 2006) and causes a number of health problems in people, including reproductive cancers (Fan et al. 2007). Although the European Union banned atrazine in 2003, it is still used in the United States and was the second most frequently detected pesticide in drinking water wells according to the US Environmental Protection Agency.
Another example is the herbicide glyphosate, known commercially as Round Up™. It causes harmful effects in the male genital system of animals and reduces the production of testosterone (Oliveira et al. 2007).
Globally, amphibian populations are declining in size and number. Scientists do not agree on exactly what is causing the widespread disappearances. Not one, but many, stressors may be acting in concert to affect this diverse group of animals that include frogs, toads and salamanders. Some of those identified are parasites, endocrine disrupting chemicals, UV light, habitat loss and climate change |
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What did they do? The authors collected cane toads (Bufo marinus) from five study sites in Florida that differed in the amount of farming activity, from completely suburban (and thus non-agricultural) to completely agricultural. To determine the intensity of agriculture they used image analysis software of Google Earth digital satellite images to calculate the total percentage of agricultural land around each collection site. Based upon that analysis, they assigned each site an 'agricultural intensity" score of 1 to 5: 1 (no agriculture within 11 miles, and suburban), 2 (no agriculture for 5 miles and suburban), 3 (34% agriculture), 4 (51% agriculture) and 5 (97% of the land was used for crop agriculture).
They examined approximately 20 male toads from each of the five sites during a two-year period. The researchers noted various aspects of the toad’s biology that are related to differences between males and females, including coloration, number and thickness of footpads, forearm width, appearance of ovaries or testes and sex hormone concentrations. The toads were scored based on the number and severity of reproductive abnormalities.
McCoy et al. then used these observations to assign each toad to one of three sex categories: normal male, intersex (with both testes and ovarian tissue present) and Bidder's males (males with testes, Bidder's organ problems but no female ovarian tissue). Animals were further classified into six groups based on severity of gonad problems and the intensity of agriculture where they lived. Two comparisons were made. First, the three sex groups were compared across sites. Then, the authors' looked for associations between the severity of abnormalities and the degree of agricultural intensity.
What did they find? The number and severity of gender abnormalities in male cane toads - specifically individuals with both ovarian and testes tissue (intersex) or with abnormal Bidder's organs - was greatest at sites with the most agricultural activity. As agricultural activity increased, the proportion of males with abnormalities increased.
For example, toads were most affected in the agriculture area ranked as 5 (greatest agriculture), were less affected in the areas ranked as 4 (lower % agriculture) and were least affected in the area ranked as 1 (no agriculture/suburban).
The gonads and blood hormone concentrations of suburban dwelling male toads, appeared normal in comparison to the cane toads living in or near the farmland areas.
In the most severe cases, the toads living on farmland were classified as “intersex” because they had as many female characteristics as they did male, including an equal presence of both testes and ovary. Males living at the two sites with the most intense farming were 35% and 40% intersex, respectively. More than half of the males at the 4 intensity site and about 60% at the highest level agricultural site had either abnormal testes or intersex conditions.
Normally, males look different than females. They have a distinct color pattern. Their thicker arms and nuptial pads, which are skin patches located on their thumbs, aid in mating with females.
In this study, male toads living in the agricultural areas were more female-like in all three ways. Male toads from all the agriculture sites had female coloration (feminized) called mottling. The degree of mottling increased with increasing levels of agriculture. Forearm widths were significantly smaller in intersexes living on farmland than males taken from nonagriculture areas. They also had fewer nuptial pads.
Farmland toads had abnormal hormone levels that were most likely caused by the altered reproductive tissues. Males living in agricultural areas had significantly lower testosterone levels than the suburban toads and often had pieces of ovary growing near their testes (intersex). Testosterone levels in these intersex amphibians were the lowest of all the males and resembled that of females living in the suburban environments.
Trends were similar when comparing ratios of estrogen to testosterone. Intersex toads had a higher ratio than nonagriculture males, suggesting a higher level of estrogen and a lower testosterone level. Indeed, intersexed animals had more estrogen than testosterone on average.
The males in the study were clearly feminized as based on evidence from sex hormone levels, gonadal structures, coloration and other reproductive factors. |
What does it mean? This study shows clearly that toads living in agricultural land are more likely to be feminized than those living in other settings.
The results suggest that one or more agricultural chemicals used on the food crops grown in the agricultural study sites may be causing male toad feminization. Since toads and humans have the same sex hormones and similar mechanisms of hormone production, a chemical that feminizes toads may also adversely affect humans.
As an exploratory study, this research shows clearly for this region that something about agriculture is tied to gender problems in cane toads. It was not designed to indicate which chemical or chemicals might be responsible for the gender challenges seen in the male toads. Importantly, some of the pesticides used in the farming areas in this study, such as Round Up™ and atrazine, are already known to significantly alter hormone production and have other negative effects on reproduction (Oliveira et al. 2007; Soso et al. 2007).
The lack of field measurements of contaminants also make it difficult to compare to other studies of endocrine disruption in amphibians. One recent report, examining atrazine, found a similar pattern of association (McDaniel et al. 2008). But at least one (as yet unpublished in the peer-reviewed literature) found the opposite trend. It was conducted in a different geographic area with different patterns of pesticide use.
The authors suggest it is likely that a mixture of farming chemicals is causing the feminization of the male toads, observing that, "altered phenotypes, including hormone concentrations, in this study are a result of multiple exposures to several chemicals at various concentrations over the lifetime of the toads."
Results from laboratory studies that test agricultural chemicals for effects sometimes differ from the results found in field studies, which examine animals in natural environments. Lab studies can control conditions whereas it is impossible to control all exposures and factors influencing the animals in real life situations. However, field studies provide a look at what really happens in a natural environment. This is another reason why this study is important. It takes advantage of variations among sites in agricultural use to simulate a laboratory experiment's use of different doses.
The hormone and reproductive tissue problems identified in the toads most likely begin very early in the toad's life and are permanent. The effects could be strong enough at the agricultural sites to interfere with reproduction and hence affect population numbers. It is plausible, therefore, that they are contributing to amphibian declines, which have become a world-wide problem. According to McCoy et al. "gonadal abnormalities, such as those reported here, are likely to reduce the reproductive success of affected individuals and could explain why two independent studies have documented that amphibian populations exposed to pesticides are declining or have gone extinct (Davidson and Knapp 2007; Sparling et al. 2001)."
The next steps in this work should be to identify which agents are responsible for the observed associations. The findings also indicate it would be valuable to conduct epidemiological studies of people living in the area, looking for adverse effects associated with endocrine disruption. Unfortunately, the types of effects seen in the toads might not be apparent in humans until after puberty, following early developmental exposures. Hence carrying them out will be expensive and long-term.
According to McCoy and colleagues:
"We demonstrate that gonadal form and function in the anuran amphibian B. marinus are altered by agricultural land use in a dose dependent fashion; thus our study shifts the focus of the current literature debate from asking if gonadal abnormalities are associated with agriculture-- to a new line of questions focused on identifying affected species, chemical causes, and developmental, physiological, and ecological implications of exposures."
Resources:
Animal Diversity Web. Bufo marinus. Cane toad.
Barringer, F. 2008. Hermaphrodite frogs found in suburban ponds. New York Times.
Colborn, T, D Dumanoski and JP Myers. Our Stolen Future. Dutton.
Davidson C and RA Knapp. 2007. Multiple stressors and amphibian declines: Dual impacts of pesticides and fish on yellow-legged frogs. Ecological Applications 17(2):587-59.
Fan, WQ, T Yanase, H Morinaga, S Ondo, T Okabe, M Nomura, T Komatsu, KI Morohashi, TB Hayes, R Takayanagi and H Nawata. 2007. Atrazine-induced aromatase expression is SF-1 dependent: Implications for endocrine disruption in wildlife and reproductive cancers in humans. Environmental Health Perspectives 115:720-727.
Floridagardener.com. Florida garden critters: Bufo marinus - Giant Toad, Cane Toad, Marine Toad
Hayes TB, AA Stuart, M Mendoza, A Collins, N Noriega, A Vonk, et al. 2006. Characterization of atrazine-induced gonadal malformations in African clawed frogs (Xenopus laevis) and comparisons with effects of an androgen antagonist (cyproterone acetate) and exogenous Estrogen (17-beta-estradiol): Support for the demasculinization/feminization hypothesis. Environmental Health Perspectives 114(S1):134-141.
McDaniel, TV, PA Martin, J Struger, J Sherry, CH Marvin, ME MCMaster, S Clarence, and G Tetreault. 2008. Potential endocrine disruption of sexual development in free ranging male northern leopard frogs (Rana pipiens) and green frogs (Rana clamitans) from areas of intensive row crop agriculture. Aquatic Toxicology, in press.
Oliveira, AG. LF Telles, RA Hess, GAB Mahecha and CA Oliveira. 2007. Effects of the herbicide Roundup on the epididymal region of drakes Anas platyrhynchus. Reproductive Toxicology 23:182-191.
Soso AB, LJG Barcellos and MJ Ranzani-Paiva. 2007. Chronic exposure to sub-lethal concentration of a glyphosate-based herbicide alters hormone profiles and affects reproduction of female Jundia (Rhamdia quelen). Environmental Toxicology and Pharmacology 23:308-313.
Sparling DW, GM Fellers and LL McConnell. 2001. Pesticides and amphibian population declines in California, USA. Environmental Toxicology and Chemistry 20(7):1591-1595.
US Environmental Protection Agency. Atrazine fact sheet.
US Geologic Survey. Amphibian Research and Monitoring Initiative.
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