John C. Maerz

Projected Loss of a Salamander Diversity Hotspot as a Consequence of Projected Global Climate Change

Background Significant shifts in climate are considered a threat to plants and animals with significant physiological limitations and limited dispersal abilities. The southern Appalachian Mountains are a global hotspot for plethodontid salamander diversity. Plethodontids are lungless ectotherms, so their ecology is strongly governed by temperature and precipitation. Many plethodontid species in southern Appalachia exist in high elevation habitats that may be at or near their thermal maxima, and may also have limited dispersal abilities across warmer valley bottoms. Methodology/Principal Findings We used a maximum-entropy approach (program Maxent) to model the suitable climatic habitat of 41 plethodontid salamander species inhabiting the Appalachian Highlands region (33 individual species and eight species included within two species complexes). We evaluated the relative change in suitable climatic habitat for these species in the Appalachian Highlands from the current climate to the years 2020, 2050, and 2080, using both the HADCM3 and the CGCM3 models, each under low and high CO2 scenarios, and using two-model thresholds levels (relative suitability thresholds for determining suitable/unsuitable range), for a total of 8 scenarios per species. Conclusion/Significance While models differed slightly, every scenario projected significant declines in suitable habitat within the Appalachian Highlands as early as 2020. Species with more southern ranges and with smaller ranges had larger projected habitat loss. Despite significant differences in projected precipitation changes to the region, projections did not differ significantly between global circulation models. CO2 emissions scenario and model threshold had small effects on projected habitat loss by 2020, but did not affect longer-term projections. Results of this study indicate that choice of model threshold and CO2 emissions scenario affect short-term projected shifts in climatic distributions of species; however, these factors and choice of global circulation model have relatively small affects on what is significant projected loss of habitat for many salamander species that currently occupy the Appalachian Highlands.

The influence of invasive earthworms on indigenous fauna in ecosystems previously uninhabited by earthworms

Recent studies on earthworm invasion of North American soils report dramatic changes in soil structure, nutrient dynamics and plant communities in ecosystems historically free of earthworms. However, the direct and indirect impacts of earthworm invasions on animals have been largely ignored. This paper summarizes the current knowledge on the impact of earthworm invasion on other soil fauna, vertebrates as well as invertebrates.Earthworm invasions can have positive effects on the abundance of other soil invertebrates, but such effects are often small, transient, and restricted to habitats with harsh climates or a long history of earthworm co-occurrence with other soil invertebrates. Middens and burrows can increase soil heterogeneity and create microhabitats with a larger pore size, high microbial biomass, and microclimates that are attractive to micro- and mesofauna. Under harsh climatic conditions, the aggregates formed by earthworms may increase the stability of soil microclimates. Positive effects can also be seen when comminution and mucus secretion increase the palatability of unpalatable organic material for microorganisms which are the main food of most micro- and mesofaunal groups. For larger invertebrates or small vertebrates, invasive earthworms may become important prey, with the potential to increase resource availability. In the longer-term, the activity of invading earthworms can have a strong negative impact on indigenous faunal groups across multiple trophic levels. Evidence from field and laboratory studies indicates that the restructuring of soil layers, particularly the loss of organic horizons, physical disturbance to the soil, alteration of understory vegetation, and direct competition for food resources, lead directly and indirectly to significant declines in the abundance of soil micro- and mesofauna. Though studies of invasive earthworm impacts on the abundance of larger invertebrates or vertebrates are generally lacking, recent evidence suggests that reduced abundance of small soil fauna and alteration of soil microclimates may be contributing to declines in vertebrate fauna such as terrestrial salamanders. Preliminary evidence also suggests the potential for earthworm invasions to interact with other factors such as soil pollution, to negatively affect vertebrate populations.

Loss of migratory behaviour increases infection risk for a butterfly host.

Long-distance animal migrations have important consequences for infectious disease dynamics. In some cases, migration lowers pathogen transmission by removing infected individuals during strenuous journeys and allowing animals to periodically escape contaminated habitats. Human activities are now causing some migratory animals to travel shorter distances or form sedentary (non-migratory) populations. We focused on North American monarch butterflies and a specialist protozoan parasite to investigate how the loss of migratory behaviours affects pathogen spread and evolution. Each autumn, monarchs migrate from breeding grounds in the eastern US and Canada to wintering sites in central Mexico. However, some monarchs have become non-migratory and breed year-round on exotic milkweed in the southern US. We used field sampling, citizen science data and experimental inoculations to quantify infection prevalence and parasite virulence among migratory and sedentary populations. Infection prevalence was markedly higher among sedentary monarchs compared with migratory monarchs, indicating that diminished migration increases infection risk. Virulence differed among parasite strains but was similar between migratory and sedentary populations, potentially owing to high gene flow or insufficient time for evolutionary divergence. More broadly, our findings suggest that human activities that alter animal migrations can influence pathogen dynamics, with implications for wildlife conservation and future disease risks.

Traits, not origin, explain impacts of plants on larval amphibians

Managing habitats for the benefit of native fauna is a priority for many government and private agencies. Often, these agencies view nonnative plants as a threat to wildlife habitat, and they seek to control or eradicate nonnative plant populations. However, little is known about how nonnative plant invasions impact native fauna, and it is unclear whether managing these plants actually improves habitat quality for resident animals. Here, we compared the impacts of native and nonnative wetland plants on three species of native larval amphibians; we also examined whether plant traits explain the observed impacts. Specifically, we measured plant litter quality (carbon : nitrogen : phosphorus ratios, and percentages of lignin and soluble phenolics) and biomass, along with a suite of environmental conditions known to affect larval amphibians (hydroperiod, temperature, dissolved oxygen, and pH). Hydroperiod and plant traits, notably soluble phenolics, litter C:N ratio, and litter N:P ratio, impacted the likelihood that animals metamorphosed, the number of animals that metamorphosed, and the length of larval period. As hydroperiod decreased, the likelihood that amphibians achieved metamorphosis and the percentage of tadpoles that successfully metamorphosed also decreased. Increases in soluble phenolics, litter N:P ratio, and litter C:N ratio decreased the likelihood that tadpoles achieved metamorphosis, decreased the percentage of tadpoles metamorphosing, decreased metamorph production (total metamorph biomass), and increased the length of larval period. Interestingly, we found no difference in metamorphosis rates and length of larval period between habitats dominated by native and nonnative plants. Our findings have important implications for habitat management. We suggest that to improve habitats for native fauna, managers should focus on assembling a plant community with desirable traits rather than focusing only on plant origin.

Earthworm effects on the incorporation of litter C and N into soil organic matter in a sugar maple forest

To examine the mechanisms of earthworm effects on forest soil C and N, we double-labeled leaf litter with 13C and 15N, applied it to sugar maple forest plots with and without earthworms, and traced isotopes into soil pools. The experimental design included forest plots with different earthworm community composition (dominated by Lumbricus terrestris or L. rubellus). Soil carbon pools were 37% lower in earthworm-invaded plots largely because of the elimination of the forest floor horizons, and mineral soil C:N was lower in earthworm plots despite the mixing of high C:N organic matter into soil by earthworms. Litter disappearance over the first winter-spring was highest in the L. terrestris (T) plots, but during the warm season, rapid loss of litter was observed in both L. rubellus (R) and T plots. After two years, 22.0% +/- 5.4% of 13C released from litter was recovered in soil with no significant differences among plots. Total recovery of added 13C (decaying litter plus soil) was much higher in no-worm (NW) plots (61-68%) than in R and T plots (20-29%) as much of the litter remained in the former whereas it had disappeared in the latter. Much higher percentage recovery of 15N than 13C was observed, with significantly lower values for T than R and NW plots. Higher overwinter earthworm activity in T plots contributed to lower soil N recovery. In earthworm-invaded plots isotope enrichment was highest in macroaggregates and microaggregates whereas in NW plots silt plus clay fractions were most enriched. The net effect of litter mixing and priming of recalcitrant soil organic matter (SOM), stabilization of SOM in soil aggregates, and alteration of the soil microbial community by earthworm activity results in loss of SOM and lowering of the C:N ratio. We suggest that earthworm stoichiometry plays a fundamental role in regulating C and N dynamics of forest SOM.

Comparison of Hematological Stress Indicators in Recently Captured and Captive Paedomorphic Mole Salamanders, Ambystoma talpoideum

Abstract Measuring stress in animals is an important component of many research studies, and it has traditionally been performed via sampling levels of corticosterone in plasma. A secondary, “hematological” approach used most commonly by researchers of birds, mammals, and other taxa involves evaluating leukocyte profiles from blood smears. Such research has shown that leukocytes have a characteristic response to stress, although in amphibians this phenomenon is not as well studied. In general, stress can induce a rise in the ratio of neutrophils to lymphocytes. We evaluated the hematological response of paedomorphic Mole Salamanders (Ambystoma talpoideum) to captivity stress, specifically focusing on this parameter, but also examining other white blood cell types. Individuals captured in the wild and held in captivity for ten days before sampling had significantly more neutrophils, fewer lymphocytes, and higher ratios of neutrophils to lymphocytes than those captured from the same locations and sampled within one hour. Captive individuals also had significantly higher numbers of eosinophils. These results are consistent with hematological research in birds and other taxa and highlight the utility of this approach for measuring stress in amphibians.

Premigratory autumn foraging forays in the green frog, Rana clamitans

Abstract Observations on post-breeding movements of radio-implanted green frogs (Rana clamitans) revealed that frogs made repetitive forays away from and back to breeding ponds before final migrations to overwintering sites away from the pond. We used a drift fence and radio-transmitters to test the hypothesis that these movements were related to preoverwintering foraging and not overwintering site selection. Movements were oriented directly to habitats away from the pond, the terrestrial habitats had more food than those closer to the pond edge, and frog mass increased during forays away from the pond but declined at the pond. Foray directions were not correlated with migration direction and were considerably shorter than migration distances to overwintering sites. An intense, late season, foraging period is probably necessary for the green frog to rebuild lipid reserves following breeding and to prepare for overwintering.

Metabolic turnover rates of carbon and nitrogen stable isotopes in captive juvenile snakes

Metabolic turnover rates (m) of delta(15)N and delta(13)C were assessed in different tissues of newly hatched captive-raised corn snakes (Elaphe guttata guttata) fed maintenance diets consisting of earthworms (Eisenia foetida) that varied substantially in delta(15)N (by 644 per thousand) and delta(13)C (by 5.0 per thousand). Three treatments were used during this 144 day experiment that consisted of the same diet throughout (control), shifting from a depleted to an enriched stable isotope signature diet (uptake), and shifting from an enriched to depleted stable isotope signature diet (elimination). Values of delta(13)C in the liver, blood, and muscle of the control snakes reached equilibrium with and were, respectively, 1.73, 2.25 and 2.29 greater than in their diet, this increase is called an isotopic discrimination factor (Deltadelta(13)C = delta(13)C(snake) - delta(13)C(food)). Values of delta(15)N in snake tissues did not achieve equilibrium with the diets in any of the exposures and thus Delta(15)N could not be estimated. Values of metabolic turnover rates (m) for delta(13)C and delta(15)N were greater in liver than in muscle and blood, which were similar, and relative results remained the same if the fraction of (15)N and (13)C were modeled. Although caution is warranted because equilibrium values of stable isotopes in the snakes were not achieved, values of m were greater for delta(13)C than delta(15)N, resulting in shorter times to dietary equilibrium for delta(13)C upon a diet shift, and for both stable isotopes in all tissues, greater during an elimination than in an uptake shift in diet stable isotope signature. Multiple explanations for the observed differences between uptake and elimination shifts raise new questions about the relationship between animal and diet stable isotope concentrations. Based on this study, interpretation of feeding ecology using stable isotopes is highly dependent on the kind of stable isotope, tissue, direction of diet switch (uptake versus elimination), and the growth rate of the animal.

The unseen invaders: introduced earthworms as drivers of change in plant communities in North American forests (a meta-analysis).

Abstract Globally, biological invasions can have strong impacts on biodiversity as well as ecosystem functioning. While less conspicuous than introduced aboveground organisms, introduced belowground organisms may have similarly strong effects. Here, we synthesize for the first time the impacts of introduced earthworms on plant diversity and community composition in North American forests. We conducted a meta‐analysis using a total of 645 observations to quantify mean effect sizes of associations between introduced earthworm communities and plant diversity, cover of plant functional groups, and cover of native and non‐native plants. We found that plant diversity significantly declined with increasing richness of introduced earthworm ecological groups. While plant species richness or evenness did not change with earthworm invasion, our results indicate clear changes in plant community composition: cover of graminoids and non‐native plant species significantly increased, and cover of native plant species (of all functional groups) tended to decrease, with increasing earthworm biomass. Overall, these findings support the hypothesis that introduced earthworms facilitate particular plant species adapted to the abiotic conditions of earthworm‐invaded forests. Further, our study provides evidence that introduced earthworms are associated with declines in plant diversity in North American forests. Changing plant functional composition in these forests may have long‐lasting effects on ecosystem functioning.

Effects of chytridiomycosis on circulating white blood cell distributions of bullfrog larvae (Rana catesbeiana)

Bullfrogs (Rana catesbeiana) are widely believed to be nonclinical carriers of Batrachochytrium dendrobatidis (Bd), the fungal pathogen that invades keratinized tissues of amphibians and causes the disease, chytridiomycosis. Although most research on this disease focuses on adults, larval anurans are also susceptible to infections in their keratinized mouthparts, and this allows for visual diagnosis of the disease via the degree of mouthpart depigmentation. When an unplanned outbreak of chytridiomycosis occurred in a set of captive bullfrog tadpoles in our lab, we conducted the current investigation into its effects on the nonspecific immune system (i.e., the leukocyte populations) of the tadpoles. We compared leukocyte counts from blood smears of 27 tadpoles that had contracted the disease (evidenced by severe mouthpart depigmentation and confirmed by histology) to those of 21 tadpoles that had little depigmentation (i.e., with little evidence of the disease). Tadpoles with severe depigmentation had significantly more neutrophils and less eosinophils than those with little depigmentation, while numbers of lymphocytes, basophils, and monocytes were not statistically different. That there was any effect at all on circulating leukocyte numbers is surprising since leukocytes are usually not seen migrating to sites of infection in tissue sections of amphibians infected with Bd, and since most research points to this disease having little outward effect on bullfrogs. Since monocyte numbers were unchanged, the leukocyte alterations were likely not due to a simple inflammation response. It is possible that Bd infections elicit increases in glucocorticoid hormones, which can cause increased numbers of circulating neutrophils and lower numbers of eosinophils, although this is often accompanied by a reduction in lymphocyte numbers, which we did not see. Further research is warranted to clarify if this effect is limited to this species.