2010 Progress 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 Period Covered by this Report: September 1, 2009 through August 31,2010
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 (Bd). 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 will thus 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 Bd. This in turn leads to elevated amphibian extinctions due to Bd.
  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, will either 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

Progress Summary:

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 only briefly describe some of the more salient findings from some of our work. We have published 27 papers thus far on this grant (see below).

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 that 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 sine 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 multidecade 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 the 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 only revealed 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. Half the frogs were acclimated for 4 weeks to 15°C and the other half was acclimated to 25°C. After acclimation, half 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 was also 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 a 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 can also 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 is written and will be

Tests of the Agrochemical Spread Hypothesis

We also 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 followup 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 tree frog) 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), Hyla cinerea (green tree frogs), 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 nonmonotonic 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 in press in Environmental Health Perspectives (McMahon et al., in press).

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 expected environmental concentration) or solvent controls for 1 week either early or late in their development. These two treatments were then 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, trematode cercariae, Aeromonas hydrophila (bacterium), or no pathogen. 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 directly 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 is in progress.

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 (the stage that infects tadpoles) or miricidiae (the 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, Environmental Health Perspectives, 2010). 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 six of seven studies, and reduced olfactory abilities for fish but not for amphibians. Atrazine was associated with a reduction in 33 of 43 immune function endpoints and with an increase in 13 of 16 infection endpoints. Atrazine altered at least one aspect of gonadal morphology in 8 of 10 studies and consistently affected gonadal function, altering spermatogenesis in two of two studies and sex hormone concentrations in six of seven studies. Atrazine did not affect vitellogenin in five studies and only increased aromatase in only one of six 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 EPA’s decision making regarding atrazine use and monitoring. In a followup paper, we documented bias and errors in the atrazine and amphibian literature associated with conflicts of interest and provided a practical guide for identifying and managing conflicts of interest (Rohr and McCoy, Conservation Letters, 2010).

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

We have conducted considerable followup work to that which was already 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., Oecologia, 2009). We disentangled the potential drivers of a parasite age-intensity relationship in tadpoles and their relation with climate change (Raffel et al., Oecologia, 2010). 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). We have also written several review papers on anthropogenic change and species interactions, with an emphasis on host and parasites and disease. We summarized our present knowledge of trematodes and their relationship to amphibian declines and deformities in a book chapter (Rohr et al., 2009). We reviewed our understanding of community responses to contaminants in a paper in Environmental Toxicology and Chemistry (Clements and Rohr, 2009). We reviewed the effects of anthropogenic global change on immune functions and disease resistance (Martin et al., Anals of the New York Academy of Sciences invited submission, 2010). In papers in Trends in Ecology and Evolution (Raffel et al. 2009, Rohr et al. in press), we attempted to unify the predator-prey and parasite-host ecology under natural enemy ecology, described areas where each field can advance the other, and identifed the frontiers of climate change-disease research.

We have also published studies on the fundamental biology of host-parasite interactions. In a paper in International Journal for Parasitology, we provided 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 elucidated the trait-mediated effects of predation and competition on amphibian trematode infections (Raffel et al., 2010). In a paper published at Functional Ecology, we described developmental variation in resistance and tolerance in a multi-host-parasite system (Rohr et al., 2010). We have also published on arthropod parasites of plants.

Future Activities:

We are continuing to explore the effects of contaminants and climate change on the spread of invasive pathogens. We are looking at interactions between contaminants and climate and studying a much broader spectrum of chemicals.


Journal Articles on this Report : 26 Displayed | Download in RIS Format

Other project views: All 145 publications 70 publications in selected types All 69 journal articles
Type Citation Project Document Sources
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 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 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 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 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 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 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 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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  • 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, chemicals, toxics, organics, pathogens, bacteria, acid rain, ecosystem, indicators, regionalization, scaling, terrestrial, aquatic, habitat, integrated assessment, public policy, decision making, biology, ecology, epidemiology, pathology, zoology, modeling, surveys, climate models, northeast, northwest, southeast, pacific northwest, Florida, FL, Oregon, OR, EPA Region 4, EPA Region 10, agriculture

    Relevant Websites:

    http://shell.cas.usf.edu/rohrlab/index.html Exit

    Progress and Final Reports:

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