Final Report: Understanding the Role of Climate Change and Land Use Modifications in Facilitating Pathogen Invasions and Declines Of Ectotherms

EPA Grant Number: R833835
Title: Understanding the Role of Climate Change and Land Use Modifications in Facilitating Pathogen Invasions and Declines Of Ectotherms
Investigators: Rohr, Jason R. , Raffel, Thomas R. , Blaustein, Andrew
Institution: University of South Florida , Oregon State University
EPA Project Officer: Packard, Benjamin H
Project Period: September 1, 2008 through August 31, 2011 (Extended to August 31, 2013)
Project Amount: $599,353
RFA: Ecological Impacts from the Interactions of Climate Change, Land Use Change and Invasive Species: A Joint Research Solicitation - EPA, USDA (2007) RFA Text |  Recipients Lists
Research Category: Global Climate Change , Aquatic Ecosystems , Ecosystems , Climate Change

Objective:

Two of the greatest environmental challenges of our time are climate change and the unprecedented emergence of invasive parasites. Of particular interest are amphibians, the most threatened vertebrate taxon on the globe.  Many of their declines are associated with climate change and possibly the most deadly invasive pathogen on the planet, the amphibian chytrid fungus, Batrachochytrium dendrobatidis. Despite the spread of many parasites being facilitated by climate change and human modification of landscapes, generalities have not materialized for how climate change and landscape alterations influence the invasiveness of parasites.

We propose a general theory for how climate change influences parasite invasions of ectotherms, which we refer to as the “climatic variability hypothesis.” This hypothesis proposes that in areas where global climate change elevates climatic variability, ectothermic hosts will more often have suboptimal immunity, facilitating the establishment and spread of invasive parasites and in turn generating host declines. However, we propose to test this hypothesis against several other plausible alternative hypotheses for parasite invasions and the declines of amphibians and other ectotherms, such as alternative climate hypotheses and the agrochemical spread hypothesis. These alternative hypotheses are described briefly below. We are aware that most of the proposed plausible hypotheses are not mutually exclusive and may be interactive, and we thus will test for their interactions.

  1. Chytrid thermal optimum hypothesis: this hypothesis postulates that increased cloud cover due to warmer oceanic temperatures leads to higher nighttime and lower daytime temperatures, causing these temperatures to converge on the optimum temperature for growth of B. dendrobatidis. This in turn leads to elevated amphibian extinctions due to B. dendrobatidis.
  2. Drought hypothesis: dry conditions kill or limit the distributions of amphibians.
  3. Agrochemical spread hypothesis: proximity to agricultural land and associated agrochemicals, such as pesticides and fertilizers, either will directly kill ectotherms or increase their susceptibility to parasites that will subsequently trigger their demise (a land use change hypothesis).
  4. Epidemic spread hypothesis: spatiotemporal species extinctions are strictly due to the spatial spread of a highly virulent parasite.

The goal of this grant is to use a weight of evidence approach to evaluate the level of support for the hypothesis that climatic variability (associated with global climate change) facilitates parasite invasions in ectothermic hosts and subsequent host declines. The specific objectives are to evaluate whether:

  1. disease-related extinctions of ectothermic species through time are consistent with the climatic variability hypothesis or alternative hypotheses,
  2. declines and extinctions of ectothermic species in space are consistent with the climatic variability hypothesis or alternative hypotheses, and
  3. the results of manipulative experiments are consistent with the climatic variability hypothesis or alternative hypotheses, such as agrochemical-related declines.

Summary/Accomplishments (Outputs/Outcomes):

Our hypotheses for the spread of invasive/emerging pathogens can be classified into two broad categories, those that are climate related and those that are associated with landscape modifications and pollution. Hence, that is how we will organize the summary of our findings. Below we briefly describe only some of the more salient findings from our work. We have 56 papers published or accepted on this grant and several others have been submitted (see publications).

Tests of Climate Hypotheses

We have been actively examining the role of climate on invasive pathogens of amphibians. In our Proceedings of the National Academy of Sciences paper (Rohr, et al., 2008), we evaluated the level of support for competing hypotheses for the spread of the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd). Positive correlations between global warming and Bd-related declines sparked the chytrid-thermal-optimum hypothesis, which proposes that global warming increased cloud cover in warm years drove the convergence of daytime and nighttime temperatures toward the thermal optimum for Bd growth. In contrast, the spatiotemporal spread hypothesis states that Bd-related declines are caused by the introduction and spread of Bd, independent of climate change. We provided a rigorous test of these hypotheses by evaluating (i) whether cloud cover, temperature convergence, and predicted temperature-dependent Bd growth were significant positive predictors of amphibian extinctions in the amphibian genus Atelopus (a genus that has experienced 67 extinctions since 1980); and (ii) whether spatial structure in the timing of these extinctions could be detected without making assumptions about the location, timing, or number of Bd emergences. We showed that there is spatial structure to the timing of Atelopus spp. extinctions but that the cause of this structure remains equivocal, emphasizing the need for further molecular characterization of Bd. We also showed that the reported positive multi-decade correlation between Atelopus spp. extinctions and mean tropical air temperature in the previous year is indeed robust, but the evidence that it is causal is weak because numerous other variables, including regional banana and beer production, were better predictors of these extinctions. Finally, almost all of our findings were opposite to the predictions of the heralded chytrid-thermal-optimum hypothesis. Hence, this paper served to support spread of the pathogen, but ruled out the most widely accepted hypothesis for Bd-related declines, the chytrid-thermal-optimum hypothesis.

In a paper recently published in Proceedings of the National Academy of Sciences (Rohr and Raffel, 2010), we provide evidence that global El Niño climatic events drive widespread amphibian extinctions via increased regional temperature variability that can reduce amphibian immune defenses. Of 26 climate variables tested, only factors associated with temperature variability, specifically monthly variation in temperature and diurnal temperature range, were positive predictors of the spatiotemporal patterns of chytrid-fungal-related extinctions. Climatic signals were revealed only after controlling for apparent epidemic spread of Bd by temporally detrending the data. This finding suggests that intrinsic, epidemic spread was the primary factor influencing declines and that it concealed the effects of the extrinsic and secondary factor, climate. Patterns consistent with epidemic spread accounted for 59% of the temporal variation in amphibian extinctions, whereas climate accounted for 59% of the remaining variation. Hence, we could account for 83% of the variation in extinctions with these two variables alone. Given that global climate change is increasing El Niño strength and temperature variability, pathogen introductions coupled with climate change are likely driving worldwide enigmatic extinctions of amphibians. Importantly, these results suggest that changes to variability in temperature associated with climate change might be just as significant to disease emergence as changes to mean temperature, highlighting the importance of understanding the role of temperature variability in infectious disease dynamics.

To experimentally test the climate variability hypothesis, we built 90 incubators so that we had proper replication of the temperature treatments. Each incubator contained three adult Cuban tree frogs, Osteopilus septentrionalis, individually housed on soil. One-half of the frogs were acclimated for 4 weeks to 15°C and the other half was acclimated to 25°C. After acclimation, one-half of the frogs at each temperature were switched to the other temperature and the other half remained at their acclimated temperature. Then, one frog in each incubator was exposed to Bd, one was not exposed to Bd, and the remaining frog was removed 1 week after the acclimation period to quantify the effects of the temperature switch (or not) on cellular immunity and skin peptides, both of which are likely important for defense against Bd. Bd also was grown in culture in each incubator. Interestingly, Bd grew best in culture at 25°C, but grew best on the frogs and was most deadly to the frogs at 15°C, emphasizing that temperature-dependent growth in culture likely does not reflect temperature-dependent growth or virulence on amphibians. Furthermore, this pattern likely explains why annual temperature-dependent growth estimates of Bd based on growth in culture is a significant negative, rather than positive, predictor of Atelopus species extinctions. Most importantly, frogs exposed to a switch in temperature had significantly more Bd growth than frogs exposed to a constant temperature, providing empirical support for the climate variability hypothesis. These findings suggest that, in addition to mean temperature, variation in temperature also can mediate pathogen resistance, emphasizing the importance of considering both changes to the mean and variance when evaluating the impacts of climate change on biodiversity. This paper was published in Nature Climate Change in 2013.

Tests of the Agrochemical Spread Hypothesis

We have thoroughly explored chemical contaminants and associated landscape modifications as contributing factors to the emergence of amphibian diseases. We have tested whether the second most commonly used herbicide, atrazine, and the most commonly used synthetic fungicide, chlorothalonil, affect amphibian survival, immunity, and Bd infections. Interestingly, both atrazine and chlorothalonil decimated Bd populations in culture. Hence, some chemicals might serve as viable control measures for this fungus if they appear to be innocuous to amphibians. Bd did elevate tadpole mortality, but we found no interaction between Bd and agrochemical exposure. We are using quantitative PCR to quantify Bd abundance on these tadpoles.

We conducted follow-up work on both chlorothalonil and atrazine. To determine the toxicity of chlorothalonil to amphibians, we reared Rana sphenocephala (Southern leopard frog) and Osteopilus septentrionalis (Cuban treefrog) in outdoor mesocosms for 5 weeks in the presence or absence of one and two times the expected environmental concentration (EEC; 164 µg/L) of chlorothalonil. We conducted two static renewal, dose-response experiments on O. septentrionalis, Hyla squirella (squirrel treefrog), H. cinerea (green treefrogs), and R. sphenocephala. In the mesocosm experiment, the EEC was associated with 99.5% and 97.8% mortality of R. sphenocephala and O. septentrionalis, respectively, and two times the EEC killed 100% of each species. In the laboratory experiments, the EEC caused 100% mortality of all species within 24 hours, half the EEC killed 100% of R. sphenocephala, and the lowest concentration tested, 0.0164 µg/L, caused significant tadpole mortality. The dose-response was non-monotonic for each species, with only low and high, but not intermediate, concentrations causing significant mortality. Additionally, chlorothalonil concentration was negatively associated with frog liver health and numbers of immune cells in the liver (up to 16.4 µg/L). Given that chlorothalonil 1) killed nearly every tadpole at the EEC, 2) caused significant mortality between three and four orders of magnitude below the EEC, 3) induced immunosuppression at environmentally common concentrations, and 4) has been regularly detected at levels causing significant mortality in this study in regions where amphibians are going extinct, chlorothalonil exposure has the potential to both directly and indirectly cause amphibian declines. Despite these results being consistent with the agrochemical spread hypothesis for amphibian declines, more direct links will be necessary before a causal relationship is established. This work is published in Environmental Health Perspectives (McMahon, et al., 2011).

To test if agrochemical exposure can have long-term effects on amphibian defenses against pathogens, we exposed Cuban tree frog tadpoles to atrazine (at the EEC) or solvent controls for 1 week either early or late in their development. These two treatments then were crossed with exposure to pathogens either immediately after the atrazine exposure or exposure to pathogens 7 weeks later after the tadpoles metamorphosed. Amphibians from each replicate were exposed to either Bd or not. What we have discovered so far is that 1 week exposure to atrazine increased Bd-induced mortality regardless of whether the Bd exposure occurred immediately after the atrazine exposure or 7 weeks later. Further, there was no evidence of recovery from the atrazine exposure and exposure to atrazine during the second development window seemed to increase mortality risk more so than exposure during the first window. Hence, even though atrazine is deadly to Bd, it seems to be associated with long-term and perhaps permanent reductions in the defenses of amphibians against Bd that increase their risk of mortality. These findings are consistent with the hypothesis that atrazine could compromise amphibian defenses and facilitate pathogen invasions and emergence. This paper was published in Proceedings of the Royal Society of London B.

Consistent with atrazine and other chemicals increasing amphibian disease risk are the results of papers we published in Ecological Applications (Rohr, et al., 2008), Nature (Rohr, et al., 2008), and the Journal of Parasitology (Raffel, et al., 2009) on emerging trematode (parasitic flatworms) infections of amphibians. In our Ecological Applications and Journal of Parasitology papers, we showed that several pesticides were associated with much greater adverse effects on amphibians than snails (first intermediate host) or trematode cercariae (stage that infects tadpoles) or miracidia (stage that infects snails) that likely increase infection risk for amphibians. In our Nature paper, we showed that atrazine was the best predictor (out of more than 240 plausible candidates) of the abundance of larval trematodes 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.

We also conducted a meta-analysis on the effects of atrazine on amphibians and freshwater fish (Rohr and McCoy, 2010 in Environmental Health Perspectives). In this paper, we found little evidence that atrazine consistently caused direct mortality of fish or amphibians, but we found evidence that it can have indirect and sublethal effects. The relationship between atrazine concentration and timing of amphibian metamorphosis was regularly nonmonotonic, indicating that atrazine can both accelerate and delay metamorphosis. Atrazine reduced size at or near metamorphosis in 15 of 17 studies. Atrazine elevated amphibian and fish activity in 12 of 14 studies, reduced antipredator behaviors in 6 of 7 studies, and reduced olfactory abilities for fish but not for amphibians. Atrazine was associated with a reduction in 33 of 43 immune function end points and with an increase in 13 of 16 infection end points. Atrazine altered at least one aspect of gonadal morphology in 8 of 10 studies and consistently affected gonadal function, altering spermatogenesis in 2 of 2 studies and sex hormone concentrations in 6 of 7 studies. Atrazine did not affect vitellogenin in 5 studies and only increased aromatase in 1 of 6 studies. Effects of atrazine on fish and amphibian reproductive success, sex ratios, gene frequencies, populations, and communities remain uncertain. Although there is much left to learn about the effects of atrazine, we identified several consistent effects of atrazine that must be weighed against any of its benefits and the costs and benefits of alternatives to atrazine use. We hope that this meta-analysis clears up the controversy surrounding atrazine and facilitates the EPA’s decision making regarding atrazine use and monitoring. In a follow-up paper, we document bias and errors in the atrazine and amphibian literature associated with conflicts of interest and provide a practical guide for identifying and managing conflicts of interest (Rohr and McCoy, 2010 in Conservation Letters).

General Findings on Anthropogenic Change, Disease, and the Fundamental Biology of Host-Parasite Interactions

We have conducted considerable follow-up work to that which already was described on anthropogenic change and disease. We showed that American toad, Bufo americanus, tadpoles can detect and avoid trematode cercariae, but that atrazine does not affect their olfactory detection of trematode cercariae (Rohr, et al., 2009 in Oecologia). We disentangled the potential drivers of a parasite age-intensity relationship in tadpoles and their relation with climate change (Raffel, et al., 2010 in Oecologia). We quantified the effects of four agrochemicals and their pair-wise mixtures on indicator bacteria that are used to identify disease risk to humans (Staley, et al., 2010 in Environmental Microbiology). We also have written several review papers on anthropogenic change and species interactions, with an emphasis on host and parasites and disease. We summarize our present knowledge of trematodes and their relationship to amphibian declines and deformities in a book chapter (Rohr, et al., 2009). We review our understanding of community responses to contaminants in a paper in Environmental Toxicology and Chemistry (Clements and Rohr, 2009). We review the effects of anthropogenic global change on immune functions and disease resistance (Martin, et al., 2010), in an invited submission to Annals of the New York Academy of Sciences. In papers in Trends in Ecology and Evolution (Raffel, et al., 2009 and Rohr, et al., 2011), we attempt to unify the predator-prey and parasite-host ecology under natural enemy ecology and describe areas where each field can advance the other, and identify the frontiers of climate-change-disease research.

We also have published studies on the fundamental biology of host-parasite interactions. In a paper in International Journal of Parasitology, we provide evidence that the eastern red-spotted newts possess immune memory that influences disease dynamics (Raffel, et al., 2009). In a paper published in Ecology, we elucidate the trait-mediated effects of predation and competition on amphibian trematode infections (Raffel, et al., 2010). In a paper published in Functional Ecology, we describe developmental variation in resistance and tolerance in a multi-host-parasite system (Rohr, et al., 2010). Additionally, in a paper published in Proceedings of the National Academy of Sciences, we showed that crayfish are non-amphibian hosts of Bd and in a paper published in the Proceedings of the Royal Society of London B, we showed that both that fundamental niche (climate and vegetation) and propagule pressure factors (overall trade and introduced hosts) contribute unique variation to the global distribution of Bd.

Conclusions:

We have accomplished the goals and objectives of this grant and believe we have greatly improved our understanding of the impacts of pollution and climate change on biodiversity and have made great advances towards developing a general theory for how global climate change, through changes in climatic variability, facilitates parasite invasions in ectothermic hosts and subsequent host declines.


Journal Articles on this Report : 68 Displayed | Download in RIS Format

Other project views: All 145 publications 70 publications in selected types All 69 journal articles
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Journal Article Boone MD, Bishop CA, Boswell LA, Brodman RD, Burger, J, Davidson C, Gochfeld M, Hoverman JT, Neuman-Lee LA, Relyea RA, Rohr JR, Salice C, Semlitsch RD, Sparling D, Weir S. Pesticide regulation amid the influence of industry. Bioscience 2014;64(10):917-922. R833835 (2012)
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  • Journal Article Buck JC, Scholz KI, Rohr JR, Blaustein AR. Trophic dynamics in an aquatic community:interactions among primary producers, grazers, and a pathogenic fungus. Oecologia 2015;178(1):239-248. R833835 (Final)
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  • Journal Article Civitello DJ, Rohr JR. Disentangling the effects of exposure and susceptibility on transmission of the zoonotic parasite Schistosoma mansoni. Journal of Animal Ecology 2014;83(6):1379-1386. R833835 (Final)
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  • Journal Article Clements WH, Rohr JR. Community responses to contaminants: using basic ecological principles to predict ecotoxicological effects. Environmental Toxicology and Chemistry 2009;28(9):1789-1800. R833835 (2009)
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  • Journal Article Halstead NT, McMahon TA, Johnson SA, Raffel TR, Romansic JM, Crumrine PW, Rohr JR. Community ecology theory predicts the effects of agrochemical mixtures on aquatic biodiversity and ecosystem properties. Ecology Letters 2014;17(8):932-941. R833835 (Final)
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  • Journal Article Halstead NT, Civitello DJ, Rohr JR. Comparative toxicities of organophosphate and pyrethroid insecticides to aquatic macroarthropods. Chemosphere 2015;135:265-271. R833835 (Final)
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  • Journal Article Jennings DE, Krupa JJ, Raffel TR, Rohr JR. Evidence for competition between carnivorous plants and spiders. Proceedings of the Royal Society B-Biological Sciences 2010;277(1696):3001-3008. R833835 (Final)
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  • Journal Article Jennings DE, Congelosi AM, Rohr JR. Insecticides reduce survival and the expression of traits associated with carnivory of carnivorous plants. Ecotoxicology 2012;21(2):569-575. R833835 (2012)
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  • Journal Article Johnson PTJ, Rohr JR, Hoverman JT, Kellermanns E, Bowerman J, Lunde KB. Living fast and dying of infection:host life history drives interspecific variation in infection and disease risk. Ecology Letters 2012;15(3):235-242. R833835 (2011)
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  • Journal Article Koprivnikar J, Marcogliese DJ, Rohr JR, Orlofske SA, Raffel TR, Johnson PTJ. Macroparasite infections of amphibians: what can they tell us? Ecohealth 2012;9(3):342-360. R833835 (2012)
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  • Journal Article Lekberg Y, Meadow J, Rohr JR, Redecker D, Zabinski CA. Importance of dispersal and thermal environment for mycorrhizal communities: lessons from Yellowstone National Park. Ecology 2011;92(6):1292-1302. R833835 (2010)
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  • Journal Article Leslie TW, Biddinger DJ, Rohr JR, Fleischer SJ. Conventional and seed-based insect management strategies similarly influence nontarget coleopteran communities in maize. Environmental Entomology 2010;39(6):2045-2055. R833835 (Final)
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  • Journal Article Leslie TW, Biddinger DJ, Rohr JR, Hulting AG, Mortensen DA, Fleischer SJ. Examining shifts in Carabidae assemblages across a forest-agriculture ecotone. Environmental Entomology 2014;43(1):18-28. R833835 (2012)
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  • Journal Article Li Y, Cohen JM, Rohr JR. Review and synthesis of the effects of climate change on amphibians. Integrative Zoology 2013;8(2):145-161. R833835 (2012)
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  • Journal Article Liu X, Rohr JR, Li Y. Climate, vegetation, introduced hosts and trade shape a global wildlife pandemic. Proceedings of the Royal Society of London B 2013;280(1753):20122506. R833835 (2011)
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  • Journal Article Martin LB, Hopkins WA, Mydlarz LD, Rohr JR. The effects of anthropogenic global changes on immune functions and disease resistance. Annals of the New York Academy of Sciences 2010;1195:129-148. R833835 (2009)
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  • Journal Article McMahon TA, Halstead NT, Johnson S, Raffel TR, Romansic JM, Crumrine PW, Boughton RK, Martin LB, Rohr JR. The fungicide chlorothalonil is nonlinearly associated with corticosterone levels, immunity, and mortality in amphibians. Environmental Health Perspectives 2011;119(8):1098-1103. R833835 (2010)
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  • Journal Article McMahon TA, Halstead NT, Johnson S, Raffel TR, Romansic JM, Crumrine PW, Rohr JR. Fungicide-induced declines of freshwater biodiversity modify ecosystem functions and services. Ecology Letters 2012;15(7):714-722. R833835 (2011)
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  • Journal Article McMahon TA, Brannelly LA, Chatfield MWH, Johnson PTJ, Joseph MB, McKenzie VJ, Richards-Zawacki CL, Venesky MD, Rohr JR. Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in the absence of infection. Proceedings of the National Academy of Sciences of the United States of America 2013;110(1):210-215. R833835 (2012)
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  • Journal Article McMahon TA, Romansic JM, Rohr JR. Nonmonotonic and monotonic effects of pesticides on the pathogenic fungus Batrachochytrium dendrobatidis in culture and on tadpoles. Environmental Science & Technology 2013;47(14):7958-7964. R833835 (2012)
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  • Journal Article McMahon TA, Sears BF, Venesky MD, Bessler SM, Brown JM, Deutsch K, Halstead NT, Lentz G, Tenouri N, Young S, Civitello DJ, Ortega N, Fites JS, Reinert LK, Rollins-Smith LA, Raffel TR, Rohr JR. Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature 2014;511(7508):224-227. R833835 (Final)
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  • Journal Article McMahon TA, Rohr JR. Trypan blue dye is an effective and inexpensive way to determine the viability of Batrachochytrium dendrobatidis zoospores. EcoHealth 2014;11(2):164-167. R833835 (Final)
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  • Journal Article McMahon TA, Rohr JR. Transition of chytrid fungus infection from mouthparts to hind limbs during amphibian metamorphosis. EcoHealth 2015;12(1):188-193. R833835 (Final)
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  • Journal Article Raffel TR, Martin LB, Rohr JR. Parasites as predators:unifying natural enemy ecology. Trends in Ecology and Evolution 2008;23(11):610-618. R833835 (2009)
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  • Journal Article Raffel TR, Sheingold JL, Rohr JR. Lack of pesticide toxicity to Echinostoma trivolvis eggs and miracidia. Journal of Parasitology 2009;95(6):1548-1551. R833835 (2009)
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  • Journal Article Raffel TR, LeGros RP, Love BC, Rohr JR, Hudson PJ. Parasite age-intensity relationships in red-spotted newts:does immune memory influence salamander disease dynamics? International Journal for Parasitology 2009;39(2):231-241. R833835 (2009)
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  • Journal Article Raffel TR, Michel PJ, Sites EW, Rohr JR. What drives chytrid infections in newt populations? Associations with substrate, temperature, and shade. Ecohealth 2010;7(4):526-536. R833835 (2010)
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  • Journal Article Raffel TR, Hoverman JT, Halstead NT, Michel PJ, Rohr JR. Parasitism in a community context:trait-mediated interactions with competition and predation. Ecology 2010;91(7):1900-1907. R833835 (2010)
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  • Journal Article Raffel TR, Lloyd-Smith JO, Sessions SK, Hudson PJ, Rohr JR. Does the early frog catch the worm? Disentangling potential drivers of a parasite age-intensity relationship in tadpoles. Oecologia 2011;165(4):1031-1042. R833835 (2010)
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  • Journal Article Raffel TR, Romansic JM, Halstead NT, McMahon TA, Venesky MD, Rohr JR. Disease and thermal acclimation in a more variable and unpredictable climate. Nature Climate Change 2013;3(2):146-151. R833835 (2011)
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  • Journal Article Raffel TR, Halstead NT, McMahon TA, Davis AK, Rohr JR. Temperature variability and moisture synergistically interact to exacerbate an epizootic disease. Proceedings of the Royal Society of London B 2015;282(1801):20142039 (6 pp.). R833835 (Final)
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  • Journal Article Rohr JR, Raffel TR, Romansic JM, McCallum H, Hudson PJ. Evaluating the links between climate, disease spread, and amphibian declines. Proceedings of the National Academy of Sciences of the United States of America 2008;105(45):17436-17441. R833835 (2009)
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  • Journal Article Rohr JR, Schotthoefer AM, Raffel TR, Carrick HJ, Halstead N, Hoverman JT, Johnson CM, Johnson LB, Lieske C, Piwoni MD, Schoff PK, Beasley VR. Agrochemicals increase trematode infections in a declining amphibian species. Nature 2008;455(7217):1235-1239. R833835 (2009)
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  • Journal Article Rohr JR, Raffel TR, Sessions SK, Hudson PJ. Understanding the net effects of pesticides on amphibian trematode infections. Ecological Applications 2008;18(7):1743-1753. R833835 (2009)
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  • Journal Article Rohr JR, Swan A, Raffel TR, Hudson PJ. Parasites, info-disruption, and the ecology of fear. Oecologia 2009;159(2):447-454. R833835 (2009)
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  • Journal Article Rohr JR, McCoy KA. A qualitative meta-analysis reveals consistent effects of atrazine on freshwater fish and amphibians. Environmental Health Perspectives 2010;118(1):20-32. R833835 (2009)
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  • Journal Article Rohr JR, McCoy KA. Preserving environmental health and scientific credibility:a practical guide to reducing conflicts of interest. Conservation Letters 2010;3(3):143-150. R833835 (2010)
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  • Journal Article Rohr JR, Raffel TR. Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proceedings of the National Academy of Sciences of the United States of America 2010;107(18):8269-8274. R833835 (2009)
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  • Journal Article Rohr JR, Raffel TR, Hall CA. Developmental variation in resistance and tolerance in a multi-host–parasite system. Functional Ecology 2010;24(5):1110-1121. R833835 (2010)
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  • Journal Article Rohr JR, Ruiz Moreno DH, Thomas MB, Paull SH, Dobson AP, Kilpatrick AM, Pascual M, Raffel TR. Toward a general theory for how climate change will affect infectious disease. Bulletin of the Ecological Society of America 2010;91(4):467-473. R833835 (2010)
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  • Journal Article Rohr JR, Halstead NT, Raffel TR. Modeling the future distribution of the amphibian chytrid fungus:the influence of climate and human-associated factors. Journal of Applied Ecology 2011;48(1):174-176. R833835 (2010)
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  • Journal Article Rohr JR, Sesterhenn TM, Stieha C. Will climate change reduce the effects of a pesticide on amphibians?: partitioning effects on exposure and susceptibility to contaminants. Global Change Biology 2011;17(2):657-666. R833835 (2010)
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  • Journal Article Rohr JR, Dobson AP, Johnson PTJ, Kilpatrick AM, Paull SH, Raffel TR, Ruiz-Moreno D, Thomas MB. Frontiers in climate change–disease research. Trends in Ecology & Evolution 2011;26(6):270-277. R833835 (2010)
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  • Journal Article Rohr JR, Martin LB. Reduce, reuse, recycle scientific reviews. Trends in Ecology & Evolution 2012;27(4):192-193. R833835 (2012)
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  • Journal Article Rohr JR, Martin LB. Type I error is unlikely to hinder review recycling: a reply to Montesinos. Trends in Ecology & Evolution 2012;27(6):312-313. R833835 (2012)
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  • Journal Article Rohr JR, Halstead NT, Raffel TR. The herbicide atrazine, algae, and snail populations. Environmental Toxicology and Chemistry 2012;31(5):973-976. R833835 (2012)
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  • Journal Article Rohr JR, Raffel TR, Blaustein AR, Johnson PTJ, Paull SH, Young S. Using physiology to understand climate-driven changes in disease and their implications for conservation. Conservation Physiology 2013;1(1):cot022 (15 pp.). R833835 (Final)
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  • Journal Article Rohr JR, Palmer BD. Climate change, multiple stressors, and the decline of ectotherms. Conservation Biology 2013;27(4):741-751. R833835 (2011)
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  • Journal Article Rohr JR, Raffel TR, Halstead NT, McMahon TA, Johnson SA, Boughton RK, Martin LB. Early-life exposure to a herbicide has enduring effects on pathogen-induced mortality. Proceedings of the Royal Society of London B:Biological Sciences 2013;280(1772):20131502. Erratum in Proc Biol Sci 2014;281(1783):20140629. R833835 (2012)
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  • Journal Article Rohr JR, Johnson P, Hickey CW, Helm RC, Fritz A, Brasfield S. Implications of global climate change for natural resource damage assessment, restoration, and rehabilitation. Environmental Toxicology and Chemistry 2013;32(1):93-101. R833835 (2012)
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  • Journal Article Rohr JR, Civitello DJ, Crumrine PW, Halstead NT, Miller AD, Schotthoefer AM, Stenoien C, Johnson LB, Beasley VR. Predator diversity, intraguild predation, and indirect effects drive parasite transmission. Proceedings of the National Academy of Sciences of the United States of America 2015;112(10):3008-3013. R833835 (Final)
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  • Journal Article Romansic JM, Johnson PT, Searle CL, Johnson JE, Tunstall TS, Han BA, Rohr JR, Blaustein AR. Individual and combined effects of multiple pathogens on Pacific treefrogs. Oecologia 2011;166(4):1029-1041. R833835 (2010)
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  • Journal Article Schotthoefer AM, Rohr JR, Cole RA, Koehler AV, Johnson CM, Johnson LB, Beasley VR. Effects of wetland vs. landscape variables on parasite communities of Rana pipiens:links to anthropogenic factors. Ecological Applications 2011;21(4):1257-1271. R833835 (2010)
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  • Journal Article Sears BF, Rohr JR, Allen JE, Martin LB. The economy of inflammation:when is less more? Trends in Parasitology 2011;27(9):382-387. R833835 (2011)
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  • Journal Article Sears BF, Schlunk AD, Rohr JR. Do parasitic trematode cercariae demonstrate a preference for susceptible host species? PLoS ONE 2012;7(12):e51012. R833835 (2012)
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  • Journal Article Sears BF, Rohr JR. Loss of trematode parthenitae in Planorbella trivolvis (Mollusca: Gastropoda). Journal of Parasitology 2013;99(4):738-739. R833835 (2012)
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  • Journal Article Sears BF, Snyder PW, Rohr JR. Infection deflection: hosts control parasite location with behaviour to improve tolerance. Proceedings of the Royal Society B: Biological Sciences 2013;280(1762):20130759 (5 pp.). R833835 (Final)
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  • Journal Article Sears BF, Snyder PW, Rohr JR. Host life history and host-parasite syntopy predict behavioural resistance and tolerance of parasites. Journal of Animal Ecology 2015;84(3):625-636. R833835 (2011)
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  • Journal Article Sears B, Snyder P, Rohr J. No effects of two anesthetic agents on circulating leukocyte counts or resistance to trematode infections in larval amphibians. Journal of Herpetology 2013;47(3):498-501. R833835 (2012)
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  • Journal Article Staley ZR, Rohr JR, Harwood VJ. The effect of agrochemicals on indicator bacteria densities in outdoor mesocosms. Environmental Microbiology 2010;12(12):3150-3158. R833835 (2010)
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  • Journal Article Staley ZR, Rohr JR, Harwood VJ. Test of direct and indirect effects of agrochemicals on the survival of fecal indicator bacteria. Applied and Environmental Microbiology 2011;77(24):8765-8774. R833835 (2011)
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  • Journal Article Staley ZR, Senkbeil JK, Rohr JR, Harwood VJ. Lack of direct effects of agrochemicals on zoonotic pathogens and fecal indicator bacteria. Applied and Environmental Microbiology 2012;78(22):8146-8150. R833835 (2012)
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  • Journal Article Staley ZR, Rohr JR, Senkbeil JK, Harwood VJ. Agrochemicals indirectly increase survival of E. coli O157:H7 and indicator bacteria by reducing ecosystem services. Ecological Applications 2014;24(8):1945-1953. R833835 (Final)
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  • Journal Article Tooker JF, Rohr JR, Abrahamson WG, De Moraes CM. Gall insects can avoid and alter indirect plant defenses. New Phytologist 2008;178(3):657-671. R833835 (2010)
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  • Journal Article Venesky MD, Mendelson III JR, Sears BF, Stiling P, Rohr JR. Selecting for tolerance against pathogens and herbivores to enhance success of reintroduction and translocation. Conservation Biology 2012;26(4):586-592. R833835 (2011)
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  • Journal Article Venesky MD, Hanlon SM, Lynch K, Parris MJ, Rohr JR. Optimal digestion theory does not predict the effect of pathogens on intestinal plasticity. Biology Letters 2013;9(2):20130038 (4 pp.). R833835 (2012)
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  • Journal Article Venesky MD, Raffel TR, McMahon TA, Rohr JR. Confronting inconsistencies in the amphibian-chytridiomycosis system:implications for disease management. Biological Reviews 2014;89(2):477-483. R833835 (2012)
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  • Journal Article Venesky MD, Liu X, Sauer EL, Rohr JR. Linking manipulative experiments to field data to test the dilution effect. Journal of Animal Ecology 2014;83(3):557-565. R833835 (2012)
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  • Supplemental Keywords:

    water, watersheds, acid deposition, global climate, exposure, risk, risk assessment, effects, health effects, ecological effects, vulnerability, sensitive populations, dose-response, animal, organism, population, stressor, susceptibility, climate change, pathogens, biodiversity

    Relevant Websites:

    Rohr Laboratory of Ecology and Public Health | University of South Florida Exit

    Progress and Final Reports:

    Original Abstract
  • 2009 Progress Report
  • 2010 Progress Report
  • 2011 Progress Report
  • 2012 Progress Report