Lucinda B. Johnson

Agrochemicals increase trematode infections in a declining amphibian species

Global amphibian declines have often been attributed to disease, but ignorance of the relative importance and mode of action of potential drivers of infection has made it difficult to develop effective remediation. In a field study, here we show that the widely used herbicide, atrazine, was the best predictor (out of more than 240 plausible candidates) of the abundance of larval trematodes (parasitic flatworms) 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.

Joint analysis of stressors and ecosystem services to enhance restoration effectiveness

With increasing pressure placed on natural systems by growing human populations, both scientists and resource managers need a better understanding of the relationships between cumulative stress from human activities and valued ecosystem services. Societies often seek to mitigate threats to these services through large-scale, costly restoration projects, such as the over one billion dollar Great Lakes Restoration Initiative currently underway. To help inform these efforts, we merged high-resolution spatial analyses of environmental stressors with mapping of ecosystem services for all five Great Lakes. Cumulative ecosystem stress is highest in near-shore habitats, but also extends offshore in Lakes Erie, Ontario, and Michigan. Variation in cumulative stress is driven largely by spatial concordance among multiple stressors, indicating the importance of considering all stressors when planning restoration activities. In addition, highly stressed areas reflect numerous different combinations of stressors rather than a single suite of problems, suggesting that a detailed understanding of the stressors needing alleviation could improve restoration planning. We also find that many important areas for fisheries and recreation are subject to high stress, indicating that ecosystem degradation could be threatening key services. Current restoration efforts have targeted high-stress sites almost exclusively, but generally without knowledge of the full range of stressors affecting these locations or differences among sites in service provisioning. Our results demonstrate that joint spatial analysis of stressors and ecosystem services can provide a critical foundation for maximizing social and ecological benefits from restoration investments.

Recent developments in landscape approaches for the study of aquatic ecosystems

Abstract We summarized landscape approaches used in the study of freshwater ecosystems, updated recent literature reviews on interactions between terrestrial and lotic ecosystems, and discussed the influence of J-NABS on developments in the field. We focused primarily on studies of freshwater ecosystems done at or above the catchment scale. Special issues of J-NABS and other journals have advanced our understanding of the effects of spatially distributed characteristics and phenomena on aquatic ecosystems. Topics that have been well covered in J-NABS include use of classification to predict biotic assemblages and impacts of human disturbance (especially urbanization) on stream structure and function. Early work focused on correlative relationships between landscape variables and various biotic components of stream systems, whereas later studies addressed causal linkages between landscape and biota, including landscape effects on hydrology, habitat at various spatial scales, and ecosystem processes. At large spatial scales (i.e., catchments or regions), landscape context and heterogeneity are important predictors of compositional, structural, and functional attributes of streams and lakes. The size of the study region and catchments and the level of disturbance across the region can interfere with our ability to generalize results across studies. Geographical information systems and remote sensing technologies are important tools for understanding and quantifying these relationships, and new sophisticated tools are available for measuring landscape pattern and context. Lotic ecosystems are challenging to study because of the directional flow of water across (and beneath) the landscape. However, new spatial analysis tools can incorporate hydrologic connectivity. Limited data on surface and groundwater connections and lack of available watershed delineations make finding similar connections between lakes and wetlands and their surrounding landscapes challenging.

Analyzing spatial and temporal phenomena using geographical information systems

In ecological studies the recent emphasis on larger study areas over longer time spans has coincided with the development of geographical information systems (GIS). GISs are a set of computer hardware and software for analyzing and displaying spatially referenced features (i.e., points, lines, polygons) with non-geographic attributes (i.e., species, age). In the fields of natural resources management and ecology the GIS has been used most frequently for 1) derivation of area or length measures, 2) spatial intersection functions such as file merging, analysis of spatial coincidence and detection of temporal change, 3) proximity analyses, and 4) derivation of data for input in simulation or growth models or calculation of specific metrics. Several current applications of GISs in ecology and natural resources are reviewed.

Responsiveness of Great Lakes Wetland Indicators to Human Disturbances at Multiple Spatial Scales: A Multi-Assemblage Assessment

ABSTRACT Developing indicators of ecosystem condition is a priority in the Great Lakes, but little is known about appropriate spatial scales to characterize disturbance or response for most indicators. We surveyed birds, fish, amphibians, aquatic macroinvertebrates, wetland vegetation, and diatoms at 276 coastal wetland locations throughout the U.S. Great Lakes coastal region during 2002–2004. We assessed the responsiveness of 66 candidate indicators to human disturbance (agriculture, urban development, and point source contaminants) characterized at multiple spatial scales (100, 500, 1,000, and 5,000 m buffers and whole watersheds) using classification and regression tree analysis (CART). Non-stressor covariables (lake, ecosection, watershed, and wetland area) accounted for a greater proportion of variance than disturbance variables. Row-crop agriculture and urban development, especially at larger spatial scales, were about equally influential and were more explanatory than a contaminant stress index (CSI). The CSI was an important predictor for diatom indicators only. Stephanodiscoid diatoms and nest-guarding fish were identified as two of the most promising indicators of row-crop agriculture, while Ambloplites rupestris (fish) and Aeshna (dragonflies) were two of the strongest indicators of urban development. Across all groups of taxa and spatial scales, fish indicators were most responsive to the combined influence of row-crop and urban development. Our results suggest it will be critical to account for the influence of potentially important non-stressor covariables before assessing the strength of indicator responses to disturbance. Moreover, identifying the appropriate scale to characterize disturbance will be necessary for many indicators, especially when urban development is the primary disturbance.

Effects of wetland vs. landscape variables on parasite communities of Rana pipiens: links to anthropogenic factors

The emergence of several diseases affecting amphibian populations worldwide has prompted investigations into determinants of the occurrence and abundance of parasites in frogs. To understand the spatial scales and identify specific environmental factors that determine risks of parasitism in frogs, helminth communities in metamorphic frogs of the northern leopard frog (Rana pipiens) were examined in relation to wetland and landscape factors at local (1 km) and regional (10 km) spatial extents in an agricultural region of Minnesota (USA) using regression analyses, ordination, and variance partitioning techniques. Greater amounts of forested and woody wetland habitats, shorter distances between woody wetlands, and smaller-sized open water patches in surrounding landscapes were the most consistently positive correlates with the abundances, richness, and diversity of helminths found in the frogs. Wetland and local landscape variables were suggested as most important for larval trematode abundances, whereas local and regional landscape variables appeared most important for adult helminths. As previously reported, the sum concentration of atrazine and its metabolite desethylatrazine, was the strongest predictor of larval trematode communities. In this report, we highlight the additional influences of landscape factors. In particular, our data suggest that anthropogenic activities that have resulted in the loss of the availability and connectivity of suitable habitats in the surrounding landscapes of wetlands are associated with declines in helminth richness and abundance, but that alteration of wetland water quality through eutrophication or pesticide contamination may facilitate the transmission of certain parasite taxa when they are present at wetlands. Although additional research is needed to quantify the negative effects of parasitism on frog populations, efforts to reduce inputs of agrochemicals into wetlands to limit larval trematode infections may be warranted, given the current high rates of amphibian declines and extinction events.

Methods for Generating Multi-scale Watershed Delineations for Indicator Development in Great Lake Coastal Ecosystems

ABSTRACT Watersheds represent spatially explicit areas within which terrestrial stressors can be quantified and linked to measures of aquatic ecosystem condition. We delineated thousands of Great Lakes watersheds using previously proven and new watershed delineation techniques. These were used to provide summaries for a variety of anthropogenic stressors within the Great Lakes. All delineation techniques proved useful, but each had applications for which they were most appropriate. A set of watershed delineations and stressor summaries was developed for sampling site identification, providing relatively coarse strata for selecting sites along the U.S. Great Lakes coastline. Subsequent watershed delineations were used for high-resolution site characterization of specific sites and characterizing the full coastal stressor gradient. For these delineations we used three general approaches: 1) segmentation of the shoreline at points midway between adjacent streams and delineation of a watershed for each segment; 2) specific watershed delineations for sampled sites; and 3) a Great Lakes basin-wide, high-resolution approach wherein sub-basins can be agglomerated into larger basins for specific portions of the coast. The third approach is unique in that it provides a nested framework based on hierarchies of catchments with associated stressor data. This hierarchical framework was used to derive additional watershed delineations, and their associated stressor summaries, at four different scales. Providing anthropogenic stressor metrics in such a format that can quickly be summarized for the entire basin at multiple scales, or specifically for particular areas, establishes a strong foundation for quantifying and understanding stressor-response relationships in these coastal environments.

Predator diversity, intraguild predation, and indirect effects drive parasite transmission

Significance Humans are altering biodiversity globally and infectious diseases are on the rise; thus, there is considerable interest in understanding how changes to biodiversity affect disease risk. We show that the diversity of predators that consume parasites was the best negative predictor of infections in frogs, suggesting that predation on parasites can be an important mechanism of disease reduction. Follow-up experiments, field data, and mathematical models revealed that intraguild predators, predators that consume both hosts and parasites, decrease macroparasite infections per host less than predators that only consume parasites, representing a general trait of predators that predicts their ability to reduce disease. Consequently, managing assemblages of non-intraguild and intraguild predators is an underutilized tool to minimize human and wildlife diseases. Humans are altering biodiversity globally and infectious diseases are on the rise; thus, there is interest in understanding how changes to biodiversity affect disease. Here, we explore how predator diversity shapes parasite transmission. In a mesocosm experiment that manipulated predator (larval dragonflies and damselflies) density and diversity, non-intraguild (non-IG) predators that only consume free-living cercariae (parasitic trematodes) reduced metacercarial infections in tadpoles, whereas intraguild (IG) predators that consume both parasites and tadpole hosts did not. This likely occurred because IG predators reduced tadpole densities and anticercarial behaviors, increasing per capita exposure rates of the surviving tadpoles (i.e., via density- and trait-mediated effects) despite the consumption of parasites. A mathematical model demonstrated that non-IG predators reduce macroparasite infections, but IG predation weakens this “dilution effect” and can even amplify parasite burdens. Consistent with the experiment and model, a wetland survey revealed that the diversity of IG predators was unrelated to metacercarial burdens in amphibians, but the diversity of non-IG predators was negatively correlated with infections. These results are strikingly similar to generalities that have emerged from the predator diversity–pest biocontrol literature, suggesting that there may be general mechanisms for pest control and that biocontrol research might inform disease management and vice versa. In summary, we identified a general trait of predators—where they fall on an IG predation continuum—that predicts their ability to reduce infections and possibly pests in general. Consequently, managing assemblages of predators represents an underused tool for the management of human and wildlife diseases and pest populations.

Use of GIS and remotely sensed data for a priori identification of reference areas for Great Lakes coastal ecosystems

Identification of reference conditions for ecological assessments of coastal ecosystems poses a challenging problem in highly modified landscapes. A method is described for characterizing disturbance in coastal ecosystems using remotely sensed land classification and other publicly available GIS data. Within ecoregions bordering the US Great Lakes coast, aquatic habitats bordering the shoreline were classified into five ecological types: high‐energy shoreline, embayments, open‐coast, river‐influenced and protected wetlands. Degree of anthropogenic disturbance in contributing areas to these ecosystems was assessed using a watershed approach for wetland types or a moving window approach for high‐energy shorelines. Anthropogenic stress variables included proportions of agricultural or residential land use, information on population and road density, and distance from the nearest point source. Polygons (wetlands) or pixels (high‐energy shoreline) were categorized as ‘reference’ if the magnitude of the most severe stressor, based on its cumulative frequency distribution within that ecoregion, placed it within the lowest 20th percentile. For shorelines, adjacent ‘reference’ pixels were agglomerated into polygons and a final ranking of polygons containing at least 2 km of shoreline was used to identify candidate reference areas. A subset of these sites is currently being sampled for fish, macroinvertebrates and physical habitat attributes. This a priori approach to reference area identification will allow managers to identify biological correlates of reference conditions, providing a benchmark for bioassessment and restoration efforts in coastal regions.

PREVALENCE OF SKELETAL AND EYE MALFORMATIONS IN FROGS FROM NORTH-CENTRAL UNITED STATES: ESTIMATIONS BASED ON COLLECTIONS FROM RANDOMLY SELECTED SITES

Skeletal malformation rates for several frog species were determined in a set of randomly selected wetlands in the north-central USA over three consecutive years. In 1998, 62 sites yielded 389 metamorphic frogs, nine (2.3%) of which had skeletal or eye malformations. A subset of the original sites was surveyed in the following 2 yr. In 1999, 1,085 metamorphic frogs were collected from 36 sites and 17 (1.6%) had skeletal or eye malformations, while in 2000, examination of 1,131 metamorphs yielded 16 (1.4%) with skeletal or eye malformations. Hindlimb malformations predominated in all three years, but other abnormalities, involving forelimb, eye, and pelvis were also found. Northern leopard frogs (Rana pipiens) constituted the majority of collected metamorphs as well as most of the malformed specimens. However, malformations were also noted in mink frogs (R. septentrionalis), wood frogs (R. sylvatica), and gray tree frogs (Hyla spp.). The malformed specimens were found in clustered sites in all three years but the cluster locations were not the same in any year. The malformation rates reported here are higher than the 0.3% rate determined for metamorphic frogs collected from similar sites in Minnesota in the 1960s, and thus, appear to represent an elevation of an earlier baseline malformation rate.