Final Report: Effects of Multiple Stressors on Aquatic Communities in the Prairie Pothole Region

EPA Grant Number: R830879
Title: Effects of Multiple Stressors on Aquatic Communities in the Prairie Pothole Region
Investigators: Schoff, Pat , Olker, Jennifer H. , Guntenspergen, Glenn R. , Johnson, Carter , Johnson, Lucinda
Institution: University of Minnesota - Duluth
EPA Project Officer: Packard, Benjamin H
Project Period: April 7, 2003 through April 6, 2007
Project Amount: $746,433
RFA: Developing Regional-Scale Stressor-Response Models for Use in Environmental Decision-making (2002) RFA Text |  Recipients Lists
Research Category: Ecological Indicators/Assessment/Restoration , Ecosystems

Objective:

The prairie potholes wetlands of the Great Plains comprise some of the most ecologically valuable freshwater resources of the nation, but they are also exceptionally vulnerable to anthropogenic stressors, particularly those associated with agricultural land use practices. They are also considered likely to be severely impacted by climate change. In this study we have quantified relationships among stressors associated with climate, agricultural land use and amphibian communities throughout much of the prairie pothole region.

The specific objectives of this project were to:

  1. Quantify the relationships among factors directly affected by climate change (e.g., hydroperiod), differing land use, and amphibian community structure and composition in the prairie pothole region (PPR) of the U.S.
  2. Quantify the relationships among physical and chemical wetland attributes (e.g., hydroperiod, thermal regime, pH, and DOC), UV-B radiation, and land use (including associated pesticide use) on amphibian organismal and community responses.
  3. Quantify the effects of multiple stressors (shortened hydroperiod, increased UV-B radiation, and atrazine exposure) on the health and organismal responses of Rana pipiens (northern leopard frog).
  4. Use regional climate scenarios and hydrologic models in conjunction with empirical data gathered through field and mesocosm studies to predict potential effects of multiple stressors on prairie pothole wetlands and their associated amphibian communities.

To achieve our objectives we gathered and integrated data from three hierarchical levels: landscape (referred to in the text as Extensive scale studies), wetland (Intensive scale), and mesocosms. At the landscape scale we established relationships among amphibian community structure, composition and land use, and wetland permanence types across the majority of the U.S. portion of the PPR east of Montana. Wetland scale studies focused on examining relationships among individual wetlands (including hydroperiod and other physical and chemical wetland characteristics), land use (including pesticide use), UV-B, amphibian abundance and community structure, and indices of amphibian health. In mesocosm experiments we focused on quantifying the effects of multiple stressors (hydroperiod and pesticide exposure) on amphibian development and health in artificial ponds.

Summaries of major methods development and results of the studies are reported in the form of extended abstracts in the body of the report that follows. In addition, a final summarization of the various results is included. A digest of results from each of the major portions of the project completes this executive summary.

Summary/Accomplishments (Outputs/Outcomes):

Methods Development and Project Results

  1. We developed a novel stratified random sampling design incorporating GIS and field verification components that enabled us to select study wetlands across the prairie pothole region (PPR) landscape very efficiently and objectively, while obtaining the desired proportion of wetlands in each ecoregion and approximate equal treatment sizes (land cover and hydrology). The selected wetlands represented a variety of exposures to local- (90 m buffer) and landscape-scale (up to 3200 m buffer) stressors, gradients of crop and grassland cover types, water depths, seasonal and event-driven hydrological movements, and anthropogenic stressors, such as the herbicide, atrazine.
  2. Our research indicates that Rana pipiens (northern leopard frogs) select breeding sites based on both local- and landscape-scale conditions. Rana pipiens are more likely to breed in wetlands that are surrounded by grassland (within 90 m), maintain average water levels greater than 30 cm and temperatures below 28°C, and that are embedded in a landscape with adequate wetlands within traveling distance for an individual. However, breeding was virtually absent if the distance between wetlands was greater than 1500 m. Understanding these breeding requirements will help guide conservation planning for maintaining stable amphibian populations in environments faced with climate change and development pressures.
  3. Atrazine appears to be a ubiquitous contaminant in PPR wetlands, but very few wetlands contained concentrations high enough to elicit concern under conventional toxicological standards. The US EPA’s Interim Reregistration Eligibility Decision (2003) documents state that atrazine presents “…the potential for community-level and population-level risk to aquatic ecosystems at prolonged concentration … from 10 to 20 ppb.” Of 149 unique wetland sites that were sampled at least once during the current study, only one (33.8 ppb) equaled or exceeded this atrazine concentration, and only three exceeded 1.0 ppb atrazine. However, atrazine at or above 0.1 ppb, which has been reported to cause endocrine disruption in male R. pipiens and Xenopus, was found during at least one survey in the majority of PPR wetlands in both 2004 and 2005.
  4. We collected R. pipiens metamorphs from wetlands located in crop and grassland landscapes that contained a wide range of atrazine concentrations. The sex ratio was virtually 1:1 and 97% of all gonads had normal morphology; however, testicular oocytes were observed in 56% of male metamorphs. The incidence of testicular oocytes ranged from one per pair of gonads to 1856 per pair, with a mean of 76 per affected individual. Neither the prevalence nor the numbers of testicular oocytes per gonad were correlated with wetland atrazine, which has been hypothesized to cause this phenomenon.
  5. Rana pipiens embryos and larvae growing in mesocosm habitats were exposed to atrazine at 0.1, 20, and 200 ppb, and each of these groups were subjected to two hydrologic regimes in which water was withdrawn throughout the developmental period at “normal” and “accelerated” rates. No significant differences were detected in survival, weight at metamorphosis, or developmental time to completion of metamorphosis among the treatments. The only treatment effect was seen in the proportion of larvae completing metamorphosis, which was significantly lowered in the 200 ppb atrazine treatments.
  6. A stratified random site selection process combined with consistent collection and assessment procedures give us confidence that the 2.5% malformation prevalence found in these studies represents a reasonable estimate of occurrence in the Midwest. In addition, malformed specimens were found in over 75% of all sites in which 50 or more metamorphs were collected. These figures are comparable to those reported in studies in other regions for wetlands where the trematode parasite Ribeiroia sp. was not a factor (Johnson et al., 2001). Thus, when compared to the 0.3% prevalence found in archived specimens by Hoppe (2001), it appears that idiopathic malformation prevalence in Midwest anurans may have increased eight-fold in the last several decades.
  7. Ultraviolet radiation (UVR) was rapidly attenuated through the wetland water column; 99% of UV-B attenuated within the top 75 cm in prairie pothole wetlands. However amphibian larvae, which commonly occupy the upper 10 cm of the water column, could be exposed to damaging UVR. The Z65% levels (depth that 65% irradiance reaches), which induced malformations in R. pipiens laboratory studies (Ankley et al. 2002), ranged from 0.9 to 8.2 cm in the prairie pothole wetlands. Attenuation was not driven solely by DOC content, and models of true color, chlorophyll-a, and direct attenuation value were significant, but weak predictors of extinction coefficient of PPR wetlands.
  8. Our studies suggest that R. pipiens prefers to breed in seasonal, as opposed to semi-permanent wetlands, and that successful breeding is influenced by the abundance and density of wetlands, as well as by the presence of row crops or grassland in the immediate proximity. Natural history data indicates that the species needs 80 - 120 days to complete development. Modeling of prairie pothole region seasonal wetlands using WETLANDSCAPE indicates that a 3°C atmospheric temperature increase may be accompanied by a 28% to 47% reduction in the number of years in which wetland hydroperiods equal or exceed 90 days after spring inundation. Areas with higher evaporative demand during the summer (to the north and west in the PPR) will likely have even more dramatic declines in the number of wetlands attaining the minimum hydroperiod needed for R. pipiens metamorphosis.

Semi-permanent wetland hydroperiods were not as markedly affected by a uniform 3°C increase in air temperature, with only a 2% reduction in years with hydroperiods of 90 days or more. Earlier model results suggested that increasing atmospheric temperatures would result in semi-permanent wetlands drying more often and that semi-permanent wetlands located in the south and east of the PPR would come to resemble seasonal wetlands, which breeding R. pipiens prefer. However, semi-permanent wetland density is low in this area, which is dominated by row crop agriculture. According to our logistic model, these characteristics are not optimal for northern leopard frog breeding. Thus amphibian metapopulation survival will depend on both the landscape context in which the remaining wetlands are embedded (e.g., inter-wetland distance and surrounding land use), and on local conditions within the wetland.

Effects of Multiple Stressors on Aquatic Communities in the Prairie Pothole Region

Project Design Summary

Introduction
The prairie potholes of the Great Plains comprise some of the most ecologically valuable freshwater resources of the nation (Hubbard 1988, van der Valk 1989). The diversity of wetland hydrologic regimes and the abundance of macroinvertebrates and plant life in these wetlands provide critical habitat for breeding waterfowl, stopover areas for millions of migrating birds, and habitat for amphibian species. Because of their high productivity and importance for flood storage and habitat, these wetlands represent a critical aquatic resource that should be managed on a regional basis to ensure the persistence of the ecological services they support.

Increasing temperatures and/or reduced precipitation in the Prairie Pothole Region (PPR) can be expected to change the hydrologic regime of PPR wetlands, eliminating some and modifying functions in others. In addition, existing stressors associated with agriculture (e.g., draining and impoundment), may make the PPR wetlands especially susceptible to the effects of climate change. Finally, pesticides could interact with climate change effects in as yet unknown ways, resulting in negative consequences for wetland biota.

Hydroperiod may be the best indicator of climate change impacts on wetlands, given its controlling effect on vegetation composition, habitat, and other ecosystem services. Larval amphibians are extremely sensitive to changes in hydroperiod, which may directly affect the diversity and abundance of metamorphosing juveniles. Furthermore, the interactions of stressors associated with climate change (e.g., hydroperiod) have been implicated in global amphibian declines. Because amphibians may integrate effects of climate change and pesticide exposure on wetlands, they are considered excellent indicators of the potential effects of these stressors on aquatic ecosystems.

Objectives
The overall objective of this project was to quantify the relationships among factors directly affected by climate change (e.g., hydroperiod), differing land use, and amphibian community structure and composition in the prairie pothole region (PPR) of the U.S. Specific objectives were to:

  1. Quantify the relationships among factors directly affected by climate change (e.g., hydroperiod), differing land use, and amphibian community structure and composition in the prairie pothole region (PPR) of the U.S.
  2. Quantify the relationships among physical and chemical wetland attributes (e.g., hydroperiod, thermal regime, pH, and DOC), UV-B radiation, and land use (including associated pesticide use) on amphibian organismal and community responses.
  3. Quantify the effects of multiple stressors (shortened hydroperiod, increased UV-B radiation, and atrazine exposure) on the health and organismal responses of Rana pipiens.
  4. Use regional climate scenarios and hydrologic models in conjunction with empirical data gathered through field and mesocosm studies to predict potential effects of multiple stressors on prairie pothole wetlands and their associated amphibian communities.

Experimental Design and Site Selection
To quantify the effects of multiple stressors on amphibians we conducted investigations at three spatial scales: landscape (Extensive study), wetland (Intensive study), and mesocosm study. Extensive studies sites were distributed across the U.S. portion of the Prairie Pothole Region (PPR; Figure 1); Intensive study sites were concentrated in a three county region in east-central South Dakota.

Figure 1. US Prairie Pothole Region.

All sites were stratified based on hydrologic regime (seasonal v. semi-permanent) and land use (grassland v. cropland). Semi-permanent wetlands are relatively deep, discharge wetlands with surface water persisting through the ice-free season in most years. Seasonal wetlands are shallower, and were normally inundated from spring to mid- or late summer. Hydrologic regimes were determined using the USGS Wetland BASINS data for wetlands with seasonal or semi-permanent hydrologic regimes. Isolated wetlands between 0.5 hectares and 5.0 hectares were selected. Land cover was summarized in 90 meter buffers surrounding these selected wetlands to classify wetlands as "cropland" or "grass"; basins with 70 percent or greater row-crop coverage in the 90 m buffer were classified as "cropland" and basins with 70 percent or greater pasture/hay or grassland were classified as "grass."

Intensive sites were selected across stressors gradient from the crop-rich southern PPR to the grassland-dominated northern PPR. We used National Land Cover Data (NLCD) classes for site selection; sites that met land cover, size, and hydrology criteria were randomly selected for field verification and sampling. A total of 35 sites were included in the Intensive study.

For the Extensive portion of the study we selected 114 wetland study sites based on a random design that incorporated ecoregion, land use and wetland hydrologic regime as stratification levels. GAP land cover data was used for Extensive site selection. Sites were distributed across the 5 ecoregions found in the PPR, with the number of sites weighted by the ecoregion’s proportional area in the PPR.

Acknowledgments and disclaimers

This research has been supported by a grant from the U.S. Environmental Protection Agency’s Science to Achieve Results (STAR) program. Award number RD-83087901.

Although the research described in this report has been funded wholly or in part by the U.S. Environmental Protection Agency’s STAR program through grant (number), it has not been subjected to any EPA review and therefore does not necessarily reflect the views of the Agency, and no official endorsement should be inferred.

Journal Articles:

No journal articles submitted with this report: View all 13 publications for this project

Supplemental Keywords:

RFA, Scientific Discipline, Toxics, Air, ECOSYSTEMS, Ecosystem Protection/Environmental Exposure & Risk, RESEARCH, Ecosystem/Assessment/Indicators, climate change, pesticides, Air Pollution Effects, Monitoring/Modeling, Ecological Effects - Environmental Exposure & Risk, Monitoring, Regional/Scaling, Environmental Monitoring, Agroecosystems, Ecological Risk Assessment, Atmosphere, anthropogenic stresses, ecological effects, anthropogenic stress, ecological exposure, biomarkers, ecosystem assessment, stressors, UV effects, thermal stratification, climatic influence, praire pothole region, amphibians, coral bleaching, coastal zone, natural stressors, modeling, multiple stressors, prairie pothole region, biomonitoring, regional scale impacts, ecosystem indicators, amphibian models, agriculture, aquatic ecosystems, environmental stressors, water quality, atrazine, hydrologic modeling, Global Climate Change, land use

Progress and Final Reports:

Original Abstract
  • 2003 Progress Report
  • 2004 Progress Report
  • 2005