Final Report: Early Career: The hazards of Extreme Climatic Events: Predicting Impacts

EPA Grant Number: R835188
Title: Early Career: The hazards of Extreme Climatic Events: Predicting Impacts
Investigators: Rohr, Jason R.
Institution: University of South Florida
EPA Project Officer: Hiscock, Michael
Project Period: June 1, 2012 through May 31, 2016
Project Amount: $374,936
RFA: Extreme Event Impacts on Air Quality and Water Quality with a Changing Global Climate (2011) RFA Text |  Recipients Lists
Research Category: Air Quality and Air Toxics , Global Climate Change , Water and Watersheds , Climate Change , Air , Water

Objective:

Although climatic extremes have regularly been linked to changes in water quality and disease outbreaks, few generalities have materialized for how temperature variability/extremes affect water quality. This project hypothesizes that the faster metabolism and smaller size of parasites than hosts allows them to acclimate more quickly to unpredictable temperature shifts and extremes, providing parasites with an advantage in a more climatically variable environment. The goal of this grant is to more thoroughly test this hypothesis and to develop tools to predict how climatic variability and extremes, which are increasing with global climate change, will affect water quality by altering water-borne disease risk for wildlife and humans. The specific objectives are to:

A.  Characterize climatic extremes and probabilities of extreme events occurring together.
B.  Determine the generality of the hypothesis that extreme events will increase waterborne pathogens by testing for associations between these factors across spatial and temporal scales and host and pathogen types, including zoonotic pathogens that infect humans.
C.  Quantify how extreme climatic events that occur together or with other stressors, such as pollution, affect disease risk.
D.  Develop predictive models to identify locations and times where water quality and disease risk are impacted so that mitigating measures can be appropriately targeted and sustainable systems can be developed.

By identifying how, when, and where climate change will compromise water quality by increasing wildlife and human exposure to pathogens, this project is directly relevant to Goal 4 of the U.S. EPA’s Strategic Plan and to the U.S. EPA’s responsibility to uphold the Safe Drinking Water and Clean Water Acts.

We have made great progress on all four objectives. In unpublished work, we have characterized extreme temperature and moisture events (Objective A). We have also shown that temperature shifts benefited a bacterium, nematode, and fungal parasite of amphibians, and that the fungal pathogen benefited from temperature shifts in two amphibian host species and across two amphibian age classes (juveniles and adults). These results demonstrate that our hypothesis is general across parasite taxa and host species, addressing Objective B. We also have studied how temperature shifts affect chytridiomycosis (a fungal disease of amphibians that is causing worldwide declines) across moisture levels. Interestingly, the temperature shifts only affected disease risk when the soil was considerably moist, which are the conditions that favor fungal growth. This experiment addresses Objective C above, quantifying how extreme climatic event that occur together affect disease risk. Finally, we have developed a series of predictive models to capture how climatic conditions will affect water quality and disease risk, thus tackling Objective D. We developed a global predictive model for the amphibian chytrid fungus that includes climatic conditions, habitat variables, and international trade. We also generated a heuristic model that evaluates how the magnitude and frequency of temperature shifts will affect host parasite interactions. We completed a dynamical SIR (susceptible-infected-recovered) model to evaluate how host and parasite populations will respond to various scales of temperature variability. These and other manuscripts published with the support of EPA funding are described below.

Conclusions:

Climate Change and Declines of Amphibians, the Most Threatened Vertebrate Taxon
We have reviewed the effects of climate change on amphibians, the most threatened vertebrate taxon. Additionally, we developed a global predictive model for the amphibian chytrid fungus that includes climatic conditions, habitat variables, and international trade. We generated a heuristic model that evaluates how the magnitude and frequency of temperature shifts will affect host parasite interactions. We completed a dynamical SIR (susceptible-infected-recovered) model to evaluate how host and parasite populations will respond to various scales of temperature variability. We have also shown that temperature shifts benefited a bacterium, nematode, and fungal parasite of amphibians, and that the fungal pathogen benefited from temperature shifts in two amphibian host species and across two amphibian age classes (juveniles and adults). Additionally, we have studied how temperature shifts affect chytridiomycosis (a fungal disease of amphibians that is causing worldwide declines) across moisture levels. Interestingly, the temperature shifts only affected disease risk when the soil was considerably moist, which are the conditions that favor fungal growth.

Managing Amphibian Declines
Given that amphibians are the most threatened vertebrate taxon on the Earth and their declines are associated with global climate change, we focused a considerable amount of our efforts on understanding and curbing declines. We showed that crayfish are capable of being infected with the amphibian chytrid fungus that is implicated in worldwide amphibian declines. This is an important discovery because it might help to understand why this pathogen can persist after it wipes out most of the amphibians in an area and it suggests that natural resource managers must consider amphibians and alternative hosts of the fungus if they are to successfully control this fungus and curb amphibian declines. We also demonstrated that amphibians can acquire resistance to live and dead fungus overcoming chytrid fungal immunosuppression. This is a very important finding because this is the pre-requisite to implementing a vaccination campaign to rescue amphibians from this deadly fungus. We are now in the process of testing whether we can release dead chytrid to successfully vaccinate wild amphibians.

Climate Change, Biodiversity Losses, and Diseases in General
Humans are altering the distribution of species by changing the climate and disrupting biotic interactions and dispersal. A fundamental hypothesis in spatial ecology suggests that these effects are scale-dependent; biotic interactions should shape distributions at local scales while climate should dominate at regional scales. If so, common single-scale analyses might misestimate the impacts of anthropogenic modifications on biodiversity and the environment. However, large-scale datasets necessary to test these hypotheses have not been available until recently. Using a metaanalysis of 202 effect sizes on 61 parasite species, we first provided broad evidence that host diversity inhibits parasite abundance, a hypothesis referred to as the dilution effect. Importantly, observational studies overwhelmingly documented dilution effects, and there was also significant evidence for dilution effects of zoonotic parasites of humans. Thus, dilution effects occur commonly in nature, and they may modulate human disease risk. Consequently, anthropogenic declines in biodiversity could increase human and wildlife diseases. Second, we conducted a cross-continental, cross-scale (almost five orders of magnitude) analysis of the influence of biotic (i.e., dilution effect) and abiotic processes and human population density on the distribution of three emerging pathogens: the amphibian chytrid fungus implicated in worldwide amphibian declines, West Nile virus, and the bacterium that causes Lyme disease (Borrelia burgdorferi), which are responsible for ongoing human health crises. In all three systems, we showed that the biotic factor, in particular host diversity, was only a significant predictor of pathogen distributions at local scales (~102-103 km2), whereas climate and human population density were always only significant at relatively larger, regional scales (usually >104 km2). No single scale could detect the importance of all three categories of processes. These results highlight that common, single-scale analyses can misrepresent the true impact of anthropogenic modifications on biodiversity and the environment.

Chemical Contaminant-related Research
This grant also provided new discoveries and syntheses in ecotoxicology that are relevant to EPA. We synthesized the effects of pesticides on microbial persistence in aquatic ecosystems and showed specifically that agrochemicals indirectly increased survival of E. coli O157:H7 and indicator bacteria by reducing ecosystem services. In a similar line of work, we revealed that early-life exposure to an herbicide has enduring increases on pathogen-induced mortality driven by reduced tolerance of infections. We discovered that a common neonicotinoid insecticide travels through a soil food chain, disrupting biocontrol of non-target pests and decreasing soybean yields. A commonly used fungicide was shown to cause widespread declines in freshwater biodiversity, reducing ecosystem functions and services. Finally, we demonstrated that we could predict the effects of agrochemical mixtures on aquatic biodiversity and ecosystem properties using community ecology theory.


Journal Articles on this Report : 56 Displayed | Download in RIS Format

Other project views: All 56 publications 56 publications in selected types All 56 journal articles
Type Citation Project Document Sources
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. R835188 (2013)
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  • Journal Article Boone MD, Rohr JR. The trouble with risk assessment lies at the foundation. BioScience 2015;65(3):227-228. R835188 (2014)
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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. R835188 (2014)
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  • Journal Article Buck JC, Rohr JR, Blaustein AR. Effects of nutrient supplementation on host-pathogen dynamics of the amphibian chytrid fungus: a community approach. Freshwater Biology 2016;61(1):110-120. R835188 (2014)
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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. R835188 (2013)
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  • Journal Article Civitello DJ, Cohen J, Fatima H, Halstead NT, Liriano J, McMahon TA, Ortega CN, Sauer EL, Sehgal T, Young S, Rohr JR. Biodiversity inhibits parasites:broad evidence for the dilution effect. Proceedings of the National Academy of Sciences of the United States of America 2015;112(28):8667-8671. R835188 (2014)
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  • Journal Article Civitello DJ, Cohen J, Fatima H, Halstead NT, McMahon T.A, Ortega CN, Sauer E, Rohr JR. Reply to Salkeld et al.: diversity-disease patterns are robust to study design, selection criteria, and publication bias. Proceedings of the National Academy of the United States of America 2015;112(46):E6262. R835188 (Final)
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  • Journal Article Cohen JM, Civitello DJ, Brace AJ, Feichtinger EM, Ortega CN, Richardson JC, Sauer EL, Liu X, Rohr JR. Spatial scale modulates the strength of ecological processes driving disease distributions. Proceedings of the National Academy of Sciences of the United States of America 2016;113(24):E3359-E3364. R835188 (Final)
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  • Journal Article Cohen JM, Venesky MD, Sauer EL, Civitello DJ, McMahon TA, Roznik EA, Rohr JR. The thermal mismatch hypothesis explains host susceptibility to an emerging infectious disease. Ecology Letters 2017;20(2):184-193. R835188 (Final)
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  • Journal Article De Laender F, Rohr JR, Ashauer R, Baird DJ, Berger U, Eisenhauer N, Grimm V, Hommen U, Maltby L, Meliàn CJ, Pomati F, Roessink I, Radchuk V, Van den Brink PJ. Reintroducing environmental change drivers in biodiversity–ecosystem functioning research. Trends in Ecology & Evolution 2016;31(12):905-915. R835188 (Final)
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  • Journal Article Douglas MR, Rohr JR, Tooker JF. Neonicotinoid insecticide travels through a soil food chain, disrupting biological control of non-target pests and decreasing soya bean yield Journal of Applied Ecology 2015;52(1):250-260. R835188 (2014)
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  • Journal Article Ehrsam M, Knutie SA, Rohr JR. The herbicide atrazine induces hyperactivity and compromises tadpole detection of predator chemical cues. Environmental Toxicology and Chemistry 2016;35(9):2239-2244. R835188 (Final)
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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. R835188 (2013)
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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. R835188 (2014)
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  • Journal Article Jayawardena UA, Rohr JR, Navaratne AN, Amerasinghe PH, Rajakaruna RS. Combined effects of pesticides and trematode infections on the hourglass tree frog Polypedates cruciger. EcoHealth 2016;13(1):111-122. R835188 (Final)
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  • Journal Article Jennings DE, Edwards GB, Rohr JR. Associations among ground-surface spiders (Araneae) and other arthropods in mesic flatwoods. Florida Entomologist 2012;95(2):290-296. R835188 (2012)
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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. R835188 (2012)
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  • Journal Article Jennings DE, Krupa JJ, Rohr JR. Foraging modality and plasticity in foraging traits determine the strength of competitive interactions among carnivorous plants, spiders and toads. Journal of Animal Ecology 2016;85(4):973-981. R835188 (Final)
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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. R835188 (2012)
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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. R835188 (2012)
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  • Journal Article Landis WG, Rohr JR, Moe SJ, Balbus JM, Clements W, Fritz A, Helm R, Hickey C, Hooper M, Stahl RG, Stauber J. Global climate change and contaminants, a call to arms not yet heard? Integrated Environmental Assessment and Management 2014;10(4):483-484. R835188 (2013)
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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. R835188 (2013)
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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. R835188 (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. R835188 (2012)
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  • Journal Article Madliger CL, Cooke SJ, Crespi EJ, Funk JL, Hultine KR, Hunt KE, Rohr JR, Sinclair BJ, Suski CD, Willis CK, Love OP. Success stories and emerging themes in conservation physiology. Conservation Physiology 2016;4 (1):cov057. R835188 (Final)
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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. R835188 (2012)
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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. R835188 (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. R835188 (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. R835188 (2013)
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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. R835188 (2013)
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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. R835188 (2014)
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  • Journal Article Ortega CN, Price W, Campbell T, Rohr JR. Acquired and introduced macroparasites of the invasive Cuban treefrog, Osteopilus septentrionalis. International Journal for Parasitology:Parasites and Wildlife 2015;4(3):379-384. R835188 (Final)
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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. R835188 (2012)
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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.). R835188 (2014)
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  • Journal Article Rohr JR, Martin LB. Reduce, reuse, recycle scientific reviews. Trends in Ecology & Evolution 2012;27(4):192-193. R835188 (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. R835188 (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. R835188 (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.). R835188 (2013)
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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. R835188 (2012)
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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 B: Biological Sciences 2013;280(1772):20131502. R835188 (2013)
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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. R835188 (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. R835188 (2014)
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  • Journal Article Rohr JR, Farag AM, Cadotte MW, Clements WH, Smith JR, Ulrich CP, Woods R. Transforming ecosystems:when, where, and how to restore contaminated sites. Integrated Environmental Assessment and Management September 2016;12(2):273-283. R835188 (2014)
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  • Journal Article Sauer EL, Sperry JH, Rohr JR. An efficient and inexpensive method for measuring long-term thermoregulatory behavior. Journal of Thermal Biology 2016;60:231-236. R835188 (Final)
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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. R835188 (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. R835188 (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.). R835188 (2012)
    R835188 (2013)
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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. R835188 (2014)
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    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. R835188 (2012)
    R835188 (2013)
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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. R835188 (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. R835188 (2013)
    R835188 (2014)
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  • Journal Article Staley ZR, Harwood VJ, Rohr JR. A synthesis of the effects of pesticides on microbial persistence in aquatic ecosystems. Critical Reviews in Toxicology 2015;45(10):813-836. R835188 (2014)
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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. R835188 (2012)
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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.). R835188 (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. R835188 (2012)
    R835188 (2013)
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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. R835188 (2013)
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  • Supplemental Keywords:

    Aeromonas hydrophila, amphibians, amphibian chytrid fungus, Batrachochytrium dendrobatidis, climate change, conservation, E. coli 0157:H7, Salmonella enterica

    Progress and Final Reports:

    Original Abstract
    2012 Progress Report
    2013 Progress Report
    2014 Progress Report