Jeff E. Houlahan

Quantitative evidence for global amphibian population declines

Although there is growing concern that amphibian populations are declining globally, much of the supporting evidence is either anecdotal or derived from short-term studies at small geographical scales. This raises questions not only about the difficulty of detecting temporal trends in populations which are notoriously variable, but also about the validity of inferring global trends from local or regional studies. Here we use data from 936 populations to assess large-scale temporal and spatial variations in amphibian population trends. On a global scale, our results indicate relatively rapid declines from the late 1950s/early 1960s to the late 1960s, followed by a reduced rate of decline to the present. Amphibian population trends during the 1960s were negative in western Europe (including the United Kingdom) and North America, but only the latter populations showed declines from the 1970s to the late 1990s. These results suggest that while large-scale trends show considerable geographical and temporal variability, amphibian populations are in fact declining—and that this decline has been happening for several decades.

The Rauischholzhausen Agenda for Road Ecology

Despite the documented negative effects of roads on wildlife, ecological research on road effects has had comparatively little influence on road planning decisions. We argue that road research would have a larger impact if researchers carefully considered the relevance of the research questions addressed and the inferential strength of the studies undertaken. At a workshop at the German castle of Rauischholzhausen we identified five particularly relevant questions, which we suggest provide the framework for a research agenda for road ecology: (1) Under what circumstances do roads affect population persistence? (2) What is the relative importance of road effects vs. other effects on population persistence? (3) Under what circumstances can road effects be mitigated? (4) What is the relative importance of the different mechanisms by which roads affect population persistence? (5) Under what circumstances do road networks affect population persistence at the landscape scale? We recommend experimental designs that maximize inferential strength, given existing constraints, and we provide hypothetical examples of such experiments for each of the five research questions. In general, manipulative experiments have higher inferential strength than do nonmanipulative experiments, and full before-after-control-impact designs are preferable to before-after or control-impact designs. Finally, we argue that both scientists and planners must be aware of the limits to inferential strength that exist for a given research question in a given situation. In particular, when the maximum inferential strength of any feasible design is low, decision makers must not demand stronger evidence before incorporating research results into the planning process, even though the level of uncertainty may be high.

Compensatory dynamics are rare in natural ecological communities

In population ecology, there has been a fundamental controversy about the relative importance of competition-driven (density-dependent) population regulation vs. abiotic influences such as temperature and precipitation. The same issue arises at the community level; are population sizes driven primarily by changes in the abundances of cooccurring competitors (i.e., compensatory dynamics), or do most species have a common response to environmental factors? Competitive interactions have had a central place in ecological theory, dating back to Gleason, Volterra, Hutchison and MacArthur, and, more recently, Hubbells influential unified neutral theory of biodiversity and biogeography. If competitive interactions are important in driving year-to-year fluctuations in abundance, then changes in the abundance of one species should generally be accompanied by compensatory changes in the abundances of others. Thus, one necessary consequence of strong compensatory forces is that, on average, species within communities will covary negatively. Here we use measures of community covariance to assess the prevalence of negative covariance in 41 natural communities comprising different taxa at a range of spatial scales. We found that species in natural communities tended to covary positively rather than negatively, the opposite of what would be expected if compensatory dynamics were important. These findings suggest that abiotic factors such as temperature and precipitation are more important than competitive interactions in driving year-to-year fluctuations in species abundance within communities.

THE EFFECTS OF ADJACENT LAND USE ON WETLAND SPECIES RICHNESS AND COMMUNITY COMPOSITION

Wetlands provide important ecosystem functions and values, such as wildlife habitat, water filtration and flood protection. Wetland plant communities play a fundamental role in maintaining these functions but are thought to be increasingly threatened by human modifications of the landscape, such as deforestation and road construction. Here, we examine the quantitative relationships between two dependent variables (plant species richness, community composition) and a set of independent variables describing land use (e.g., forest cover, road density, and building density). As independent variables, we further include wetland characteristics that may be related to landuse practices (e.g., area and nutrient status). Wetland size is the most important predictor of both total plant species richness and the species richness within most functional groups. In addition, landscape properties, such as forest cover, presence of streams and nutrient status of water and sediment are significant predictors of plant species richness. Adjacent land use 250–300 m from the wetland affects plant diversity. Differences in the land-use-diversity relationship among different plant functional groups suggest that adjacent land use affects wetland plant communities in two important ways. First, it alters the abundance and distribution of propagules in adjoining habitats. Second, it alters the number of dispersal routes. Our results suggest that current management practices are inadequate and that regulation of adjacent land use is a critical component of wetland conservation.

Estimating the ‘critical’ distance at which adjacent land-use degrades wetland water and sediment quality

Conversion of forested lands to agriculture or urban/residential areas has been associated with declines in stream and lake water quality. Less attention has been paid to the effects of adjacent land-uses on wetland sediment and water quality and, perhaps more importantly, the spatial scales at which these effects occur. Here we address these issues by examining variation in water and sediment nutrient levels in 73 southeastern Ontario, Canada, wetlands. We modeled the relationship between water and sediment nutrient concentrations and various measures of adjacent land-use such as forest cover and road density, measured over increasing distances from the wetland edge. We found that water nitrogen and phosphorous levels were negatively correlated with forest cover at 2250 meters from the wetland edge, while sediment phosphorous levels were negatively correlated with wetland size and forest cover at 4000 meters and positively correlated with the proportion of land within 4000 meters that is itself wetland. These results suggest that the effects of adjacent land-use on wetland sediment and water quality can extend over comparatively large distances. As such, effective wetland conservation will not be achieved merely through the creation of narrow buffer zones between wetlands and more intensive land-uses. Rather, sustaining high wetland water quality will require maintaining a heterogeneous regional landscape containing relatively large areas of natural forest and wetlands.

Pollution and parasitism in aquatic animals: a meta-analysis of effect size

Numerous studies have indicated that aquatic pollution affects parasite populations and communities. However, the responses of individual taxa and functional groups to specific contaminants, and their effect sizes, have yet to be assessed quantitatively. We began by summarizing general trends in the literature, and found that reports of significant changes in parasitism were most commonly observed in response to eutrophication and metal contamination. Among parasite taxa, significant changes were most commonly reported for acanthocephalans, digeneans and microparasites. We then conducted a quantitative meta-analysis of the effects of pollution on parasitism in aquatic animals. We calculated signed standardized effect sizes (as Cohens d) for all published studies that provided the necessary descriptive statistics, and compared them among major contaminant types (pesticides, hydrocarbons, polychlorinated biphenyls, pulp mill effluent, metals, sewage, eutrophication, and acidification) and parasite taxa (Acanthocephala, Cestoda, Digenea, Monogenea, Nematoda and microparasites). Effect sizes were not significantly different from zero for many parasite/contaminant interactions, and tended to be highly variable within individual taxa. However, consistently strong, significant negative effects were noted in Digenea and Monogenea, especially in response to metal pollution. Significant effect sizes were typically negative, indicating that pollutants have negative effects on parasite populations. Contaminants also had a slightly negative effect on community richness. When parasites were grouped into heteroxenous (with >1 obligatory host in life cycle) vs. monoxenous (1 obligatory host in life cycle) taxa, the latter were more susceptible to a wide range of pollutants. Similarly, directly exposed (external parasites and the free-living transmission stages of internal parasites) and freshwater taxa were more susceptible to a wider range of pollutants than indirectly exposed (internal parasites) and marine taxa. This meta-analysis represented a first attempt to consider the size of the effect of pollution on parasites, and highlighted the potential of susceptible parasite taxa, communities, and functional groups for use in the biological assessment of pollution. For instance, our results indicate that freshwater monogeneans and digeneans are good candidates as potential biological indicators of pollution in aquatic ecosystems.

Setting an optimal α that minimizes errors in null hypothesis significance tests.

Null hypothesis significance testing has been under attack in recent years, partly owing to the arbitrary nature of setting α (the decision-making threshold and probability of Type I error) at a constant value, usually 0.05. If the goal of null hypothesis testing is to present conclusions in which we have the highest possible confidence, then the only logical decision-making threshold is the value that minimizes the probability (or occasionally, cost) of making errors. Setting α to minimize the combination of Type I and Type II error at a critical effect size can easily be accomplished for traditional statistical tests by calculating the α associated with the minimum average of α and β at the critical effect size. This technique also has the flexibility to incorporate prior probabilities of null and alternate hypotheses and/or relative costs of Type I and Type II errors, if known. Using an optimal α results in stronger scientific inferences because it estimates and minimizes both Type I errors and relevant Type II errors for a test. It also results in greater transparency concerning assumptions about relevant effect size(s) and the relative costs of Type I and II errors. By contrast, the use of α = 0.05 results in arbitrary decisions about what effect sizes will likely be considered significant, if real, and results in arbitrary amounts of Type II error for meaningful potential effect sizes. We cannot identify a rationale for continuing to arbitrarily use α = 0.05 for null hypothesis significance tests in any field, when it is possible to determine an optimal α.

Varying Responses of Northeastern North American Amphibians to the Chytrid Pathogen Batrachochytrium dendrobatidis

Chytridiomycosis, caused by Batrachochytrium dendrobatidis (Bd), is widespread among amphibians in northeastern North America. It is unknown, however, whether Bd has the potential to cause extensive amphibian mortalities in northeastern North America as have occurred elsewhere. In the laboratory, we exposed seven common northeastern North American amphibian species to Bd to assess the likelihood of population-level effects from the disease. We exposed larval wood frogs (Lithobates sylvaticus) and postmetamorphic frogs of six other species to two different strains of Bd, a northeastern strain (JEL404) and a strain that caused die-offs of amphibians in Panama (JEL423), under ideal in vitro growth conditions for Bd. Exposed American toads (Anaxyrus americanus) all died; thus, this species may be the most likely to die from Bd-caused disease in the wild. Both Bd strains were associated with mortalities of wood frogs, although half the metamorphs survived. The Bd strain from Panama killed metamorphic green frogs (L. clamitans), whereas the northeastern strain did not, which means novel strains of Bd may lead to death even when local strains may not. No mortality was observed in four species (bullfrogs [L. catesbeianus], northern leopard frogs [L. pipiens], spring peepers [Pseudacris crucifer], and blue-spotted salamanders [Ambystoma laterale]) and in some individuals of green frogs and wood frogs that we exposed. This finding suggests these six species may be Bd vectors. Our results show that systematic exposures of amphibian species to Bd in the laboratory may be a good first step in the identification of species susceptible to Bd-caused declines and in directing regional conservation efforts aimed at susceptible species.

Effects of chytrid fungus and a glyphosate-based herbicide on survival and growth of wood frogs (Lithobates sylvaticus)

Anthropogenic-derived stressors in the environment, such as contaminants, are increasingly considered important cofactors that may decrease the immune response of amphibians to pathogens. Few studies, however, have integrated amphibian disease and contaminants to test this multiple-stressor hypothesis for amphibian declines. We examined whether exposure to sublethal concentrations of a glyphosate-based herbicide and two strains of the pathogenic chytrid fungus, Batrachochrytrium dendrobatidis (Bd) could: (1) sublethally affect wood frogs (Lithobates sylvaticus) by altering the time to and size at metamorphosis, and (2) directly affect survivability of wood frogs after metamorphosis. Neither Bd strain nor herbicide exposure alone significantly altered growth or time to metamorphosis. The two Bd strains did not differ in their pathogenicity, and both caused mortality in post-metamorphic wood frogs. There was no evidence of an interaction between treatments, indicating a lack of herbicide-induced susceptibility to Bd. However, the trends in our data suggest that exposure of wood frogs to a high concentration of glyphosate-based herbicide may reduce Bd-caused mortality compared to animals exposed to Bd alone. These results exemplify the complexities inherent when populations are coping with multiple stressors. In this case, the perceived stressor, glyphosate-based herbicide, appeared to affect the pathogen more than the hosts immune system, relieving the host from disease-caused effects. This suggests caution when invoking multiple stressors as a cause for increased disease susceptibility and indicates that the effects of multiple stressors on disease outcome depend on the interrelationships of stressors to both the pathogen and the host.

Laboratory and field exposure of two species of juvenile amphibians to a glyphosate-based herbicide and Batrachochytrium dendrobatidis

Herbicides are commonly used in agriculture and silviculture to reduce interspecific competition among plants and thereby enhance crop growth, quality, and volume. Internationally, formulations of glyphosate-based herbicides are the most widely used herbicides in both these sectors. A large amount of work has focused on the effects of these herbicides on amphibians. Several laboratory and mesocosm studies have demonstrated that various formulations of glyphosate herbicides can be acutely toxic to larval and juvenile amphibians at concentrations at the upper end of environmental realism. However, to date there has been little work done investigating such effects in natural systems, limited work on juvenile amphibians, and only a few studies have investigated interactions with other stressors. We conducted a 16 day field experiment in which juveniles of two amphibian species (Lithobates clamitans and Lithobates pipiens) were exposed to the herbicide Roundup WeatherMax™ at four application rates (0, 2.16, 4.32 and 8.64 kg a.e./ha) to investigate effects on survival, liver somatic index (LSI), body condition, and incidence of disease caused by Batrachochytrium dendrobatidis (Bd). In a separate 16 day laboratory experiment, we exposed juvenile L. clamitans to both the herbicide and Bd. Results of our studies showed that this particular herbicide formulation had no effect on juvenile survival, LSI, body condition, or disease incidence, nor was there an interaction between exposure to herbicide and exposure to the disease in tests which closely mimic real world exposure scenarios. These experiments suggest that Roundup WeatherMax as typically used in agriculture is unlikely to cause significant deleterious effects on juvenile amphibians under real world exposure conditions.