Graduation Year

2015

Document Type

Dissertation

Degree

Ph.D.

Degree Name

Doctor of Philosophy (Ph.D.)

Degree Granting Department

Integrative Biology

Major Professor

Jason Rohr, Ph.D.

Committee Member

Earl McCoy, Ph.D.

Committee Member

Marc Lajeunesse, Ph.D.

Committee Member

Thomas Crisman, Ph.D.

Keywords

fertilizer, fungicide, herbicide, insecticide, pesticide, schistosomiasis

Abstract

The global human population is expected to exceed 9 billion individuals by 2050, putting greater strain on the natural resources needed to sustain such a population. To feed this many people, some expect agricultural production will have to double and agrochemical use will have to increase anywhere from two- to five-fold relative to the turn of the century. Although industrial agriculture has provided many benefits to society, it has caused declines in biodiversity, both directly (e.g., through conversion of habitat) and indirectly (e.g., through contamination of adjacent natural habitats). Agricultural activity has also been linked to increased prevalence and intensity of trematode infections in wildlife and humans - directly by increasing available aquatic habitat for the snail intermediate hosts of trematode parasites and indirectly by altering the biological composition of aquatic habitats in ways that increase snail density. While the effects of single agrochemical contaminants on aquatic communities and trematode disease risk have been examined, agrochemical pollution typically occurs as mixtures of multiple chemical types in surface waters and the effects of mixtures on aquatic communities have received less attention. Moreover, given the high number of chemicals approved for agricultural use, the number of potential combinations of agrochemicals renders testing all possible combinations implausible. Thus, there is a critical need to develop better risk assessment tools in the face of this complexity.

I developed and tested a theoretical framework that posits that the net effects of agrochemical mixtures on aquatic communities can be predicted by integrating knowledge of each functional group's 1) sensitivity to the chemicals (direct effects), 2) reproductive rates (recovery rates), 3) interaction strength with other functional groups (indirect effects), and 4) links to ecosystem properties. I conducted a freshwater mesocosm experiment to quantify community- and ecosystem-level responses to pairwise mixtures of four major agrochemical types (fertilizer, herbicide, insecticide, and fungicide) and single chemical treatments. The responses of biodiversity and ecosystem properties to agrochemicals alone and in mixtures were indeed predictable. Moreover, these results show that community ecology theory holds promise for predicting the effects of contaminant mixtures and offer recommendations on which types of agrochemicals to apply together and separately to reduce their impacts on aquatic ecosystems.

I extended this framework to test if the direct effects of pesticides can be predicted by chemical class and/or mode of action. I performed standard toxicity trials on two invertebrate predators of snails (crayfish and giant water bugs) exposed to six insecticides belonging to two chemical classes (organophosphates and pyrethroids) to determine if environmental risk can be generalized to either insecticide class or insecticide exposure. Survival analyses demonstrated that insecticide class accounted for 55.7% and 91.1% of explained variance in crayfish and water bug survival, respectively. Simulated environmental exposures using US EPA software suggested that organophosphate insecticides present relatively low risk (as defined by the US EPA) to both crayfish and water bugs, while pyrethroid insecticides present consistently high risk to crayfish but not to water bugs, where only λ-cyhalothrin produced consistently high-risk exposure scenarios. Thus, risk to non-target organisms is well predicted by pesticide class. Furthermore, identifying insecticides that pose low risk to aquatic macroarthropods might help meet increased demands for food while mitigating against potential negative effects on ecosystem functions.

Because evidence from field data and manipulated experiments demonstrated both top-down and bottom-up effects of agrochemical pollution that increased snail densities and trematode infections in wildlife, I conducted an additional agrochemical mixture experiment with freshwater communities containing the snail hosts of schistosomiasis, which has also been linked to agriculture. As expected, top-down and bottom-up effects of insecticide, herbicide, and fertilizer exposure indirectly increased snail densities, individually and as mixtures. Agrochemical exposure and snail density together accounted for 88% of the variation in the density of infected snails. Thus, agrochemical pollution has great potential to increase human exposure to schistosome parasites, and underscores the importance of identifying low-risk alternative pesticides. A subsequent mesocosm experiment with the same six insecticides used previously in laboratory trials confirmed that insecticide exposure indirectly mediates the densities of snail hosts that can transmit schistosomiasis through the direct effects of insecticides on crayfish mortality. Importantly, crayfish mortality in semi-natural mesocosm trials closely matched mortality from controlled laboratory trials. Thus, standard laboratory toxicity tests can be a useful tool for identifying alternative insecticides that might pose lower environmental risks to important predators that regulate snail densities.

Identifying practices or agrochemicals that minimize this risk is critical to sustainably improving human health in schistosome-endemic regions. The theoretical framework presented here demonstrates the feasibility of predicting the effects of contaminant mixtures and highlights consistent effects of major agrochemical types (e.g. fertilizers, insecticides, etc.) on freshwater aquatic community composition. Furthermore, the strong top-down effects of invertebrate snail predators highlight that managing for high snail predator densities in might be a particularly effective strategy for reducing the burden of schistosomiasis in tropical countries.

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