Overview. The focus of my research is to investigate how multiple stressors can affect biota at different levels of biological organization: cellular, individual, population, and community level. Additionally, I am interested in how these responses can potentially scale up to ecosystem level consequences. Environmental and anthropogenic stressors, such as water pollution, can disrupt homeostasis and negatively affect organisms over time. As effects of multiple stressors can impact and manifest at different levels of biological organization, from the molecular level (i.e., changes in the gene transcription and expression patterns) to effects on entire communities1, measuring a suite of indicators is often necessary to assess ecological integrity in ecotoxicological testing 2, 3(Fig. 1).
To understand effects of multiple stressors in aquatic ecosystems, I use traditional as well as innovative techniques in my research. Stressors include abiotic factors such as temperature and salinity, plus anthropogenic materials such as pesticides, pharmaceuticals, and endocrine disruptors. At the cellular level, I characterize stress via RNA sequencing and molecular biomarkers. At the individual level, I quantify behavioral changes using video tracking software and reproductive responses using chronic exposures. At the population and community level my research addresses how multiple stressors affect predator-prey interactions, bottom-up community effects and community composition.
My long-term research goals are to apply innovative approaches to understand the effects of multiple stressors on aquatic ecosystems for conservation of aquatic ecosystems. My research is highly interdisciplinary and combines approaches used in the fields of molecular toxicology, aquatic toxicology, physiology, ecology, and analytical chemistry with a high emphasis on ecological relevance, complimenting small scale, single-species laboratory tests with more complex outdoor mesocosm and in-situ field assessments.
Organic micropollutants represent one of the greatest challenges in ecotoxicology today as they may have adverse effects on aquatic organisms even at very low concentrations (nanograms per liter). As such, I believe that integrating multiple organizational levels and study systems of different complexity is essential to make predictive and mechanistic generalizations about the role of micropollutants in shaping patterns of species abundance in natural systems. My research foments collaborations across academic disciplines and integrates necessary associated regulatory agencies, local communities and stakeholder groups, with academic institutions.
From Individual to Community Responses. Since organisms in aquatic environments are characteristically exposed to complex mixtures of chemicals, exposure can elicit toxic effects even though the individual contaminants are present at very low concentrations 4, or even below the limit of analytical detection. While much research is focused on the effects of individual chemicals on mortality, understanding effects of contaminant mixtures at the sublethal level remains one of the most pressing needs in the field of ecotoxicology. Not only may multiple sublethal exposures combine in unforeseen ways, but such effects can cause changes in behavior or physiology that lead to altered population and community dynamics.
My doctoral and postdoctoral research focused on assessing effects of binary and tertiary mixtures of insecticides and herbicides. I combined laboratory with mesocosm exposures using invertebrates (see publications listed in CV). Responses at lower levels of biological organization (swimming behavior and growth) detected early signs of toxicological effects on populations, as well as an understanding of respective mechanistic processes5. Responses at higher levels (communities and ecosystems) occurred at broader spatiotemporal scales and provided a direct linkage to ecological effects. This research highlighted that sublethal endpoints are highly sensitive in revealing effects due to micropollutants and could serve as early-warning tools in risk assessment efforts.
Molecular Responses in Conjunction with Field Exposures. I currently utilize RNA sequencing to assess the effects of in-situ exposure of the amphipod Hyalella azteca to various stressors in the San Francisco Estuary (SFE), California. The SFE is a highly altered and invaded ecosystem, which has resulted in the declines of many native species. The differentially expressed gene set determined by RNA sequencing will be used to create genomic “fingerprints” with concurrent chemical “fingerprints” determined by High-resolution chromatographic (LC or GC) quadrupole time-of-flight-mass spectrometry (QTOF-MS) methods. In a next step, identified biomarker genes of significance will be used in qPCR profiling analyses, comparing field responses to responses observed in laboratory exposures, providing specific information on distance-to-source effects on H. azteca. This approach will allow to determine stressor specific responses at each field site, as well as to highlight the presence and fate of chemical stressors in the field.
In my most recently funded research grant, I am developing molecular biomarkers to detect the presence and impacts of chlorantraniliprole (CHL) and imidacloprid (IMI) for Daphnia magna, Chironomus dilutus, Hyalella azteca, and fathead minnow. CHL and IMI are emerging insecticides with novel mode of actions, and unknown sublethal impacts on aquatic invertebrates and fish. CHL is an anthranilic diamide insecticide that causes toxicity by interrupting normal muscle contraction by activating the ryanodine receptor (RyR). Neurotoxicity of the neonicotinoid insecticide IMI is based on a covalent bond to the nicotinic acetylcholine receptor (nAChR), via which continued exposure can lead to cumulative detrimental effects. As such, individuals may be affected at the cell level, which can contribute to alterations in population dynamics, and potentially change community compositions6. Molecular biomarkers will aid in assessing whether environmentally relevant exposures alter the subcellular physiology of aquatic organisms before effects are apparent at higher levels of biological organization, particularly at low insecticide concentrations.
Climate Change and Contaminants. During my postdoctoral research, my interest has expanded to incorporate effects of global climate change (GCC) with contaminants. In the light of GCC, increases in pests and consequential increase in pesticide use is predicted over the next decades. Current predictions also include increases in abiotic stressors such as temperature extremes and changing salinity due to rising sea levels 7. GCC stressors are predicted to interact with contaminants in two ways: causing “toxicant-induced climate susceptibility” where contaminants weaken the organisms’ ability to acclimate to climate change and “climate-induced toxicant sensitives” where changes in temperature and salinity alter organisms’ tolerance to contaminants 8. Temperature changes can also alter the toxicity of pesticides, e.g., pyrethroids are more toxic at the whole organism level at lower temperatures, while causing greater endocrine disruption at higher temperatures. Salinity differences can influence the bioavailability of pesticides potentially resulting in elevated bioconcentration in benthic macroinvertebrates such as H. azteca. In addition, salinity changes can influence sensitivity to contaminant exposure. By applying a salinity x temperature matrix, in combination with the pyrethroid insecticide bifenthrin, I examined mechanistic responses in H. azteca, and contrasted this to effects on survival, development and behavior. The presence of the pyrethroid negatively affected all endpoints, with more severe effects with increasing salinity.
- Geist, J., Integrative freshwater ecology and biodiversity conservation. Ecological Indicators 2011, 11, (6), 1507-1516.
- Adams, S. M.; Crumby, W. D.; Greeley, M. S., Jr.; Ryon, M. G.; Schilling, E. M., Relationships between physiological and fish population responses in a contaminated stream. Environ. Toxicol. Chem. 1992, 11, (11), 1549-1557.
- Karr, J. R., Defining and assessing ecological integrity: Beyond water quality. Environ. Toxicol. Chem. 1993, 12, (9), 1521-1531.
- Kortenkamp, A., Low dose mixture effects of endocrine disrupters: implications for risk assessment and epidemiology. Int. J. Androl. 2008, 31, (2), 233-237.
- Clements, W. H., Integrating effects of contaminants across levels of biological organization: An overview. J. Aquat. Ecosyst. Stress Recovery 2000, 7, (2), 113-116.
- Pörtner, H. O., Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 2002, 132, (4), 739-761.
- Meehl, G. A.; Stocker, T. F.; Collins, W. D.; P. Friedlingstein, A. T. G., J.M. Gregory, A. Kitoh, R. Knutti, J.M. Murphy, A. Noda, S.C.B. Raper, I.G. Watterson, A.J. Weaver and Z.-C. Zhao, Global Climate Projections. In: Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change; Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA., 2007.
- Hooper, M. J.; Ankley, G. T.; Cristol, D. A.; Maryoung, L. A.; Noyes, P. D.; Pinkerton, K. E., Interactions between chemical and climate stressors: a role for mechanistic toxicology in assessing climate change risks. Environmental toxicology and chemistry / SETAC 2013, 32, (1), 32-48.