Joseph R. Milanovich

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.

Revisiting Burton and Likens (1975): Nutrient Standing Stock and Biomass of a Terrestrial Salamander in the Midwestern United States

Animals found in high densities can have significant influence in nutrient cycles of ecosystems. For example, frogs have been known to influence nutrient cycles in tropical forests. However, research understanding the influence of vertebrates in nutrient cycles of North American forest is limited. It has been found that the biomass of terrestrial salamanders (family Plethodontidae) is higher than that of birds, small mammals, and deer in a New Hampshire forest, and recent studies have found prior estimates of terrestrial salamander densities are likely lower than current estimates using sampling and analysis frameworks to account for imperfect detection. A re-evaluation of the impact plethodontid salamanders could have on forest nutrient cycles is therefore justified. We quantified the degree to which a completely terrestrial, lungless salamander (Plethodon albagula; Western Slimy Salamander) constitutes a standing stock of limiting nutrients in a Missouri, USA forest ecosystem. We utilized values of whole-body nutrient composition of carbon (C), nitrogen (N), phosphorus (P), calcium (Ca), and magnesium (Mg) of P. albagula and spatially explicit density estimates to approximate the contribution of P. albagula to forest nutrient cycles. We found that estimates of the standing crop nutrients varied spatially across the landscape and were dictated by density of P. albagula. Standing crop estimates were lower than measures for leaf litter, but often were greater than those previously reported for plethodontid salamanders, birds, and in some cases small mammals and deer in North American forests.

An investigation of factors influencing erythrocyte morphology of red-backed salamanders (Plethodon cinereus).

Amphibians have long been known to display wide variation in erythrocyte morphology across species, but within species there has been little attention given to individual variation in red blood cell morphology. We captured 49 red-backed salamanders ( Plethodon cinereus ) from central Pennsylvania, USA and used image analysis procedures to measure erythrocyte morphology (size and shape) on blood smears made from all individuals. We then statistically examined whether variation in snout-vent-length, sex, tail loss, or capture location influenced these cell variables. Only snout-vent-length affected erythrocyte size and shape, with increasing body sizes associated with increasing cell areas and increasingly rounder cells. Further, erythrocyte shape was also associated with a measure of body condition that was corrected for body size, such that individuals with high body condition scores had rounder cells. Given the oxygen-carrying role of erythrocytes in all vertebrates, we suspect this discovery is related to size-related changes in oxygen demand, since total oxygen consumption increases with body size in an allometric manner. While our results warrant further investigation to understand the mechanism, the association we found between cell roundness and both body size and condition nevertheless indicates this parameter could be used to assess the health state of plethodontid salamanders in future research, provided non-destructive sampling is employed. Our results also underscore the value of hematological investigations in the study of animal biology.

Influence of catchment land cover on stoichiometry and stable isotope compositions of basal resources and macroinvertebrate consumers in headwater streams

Anthropogenic land use affects aquatic landscapes. For example, landscape-level conversion to urban or agricultural land can heavily influence nutrient cycles in headwater streams via increased nutrient loading and altered hydrologic patterns. Recent studies in headwater streams have found that the stoichiometry and stable isotope compositions of basal resources and consumers can vary as a result of landscape-level change. To this end, we examined the stoichiometry and stable isotope compositions (δ13C and δ15N) of headwater stream flora and fauna in 16 streams located within forested, agricultural, urban, and mixed (urban, forested, and agricultural) catchments. Our results suggest basal resource stoichiometry varied across streams, with leaf litter being the most variable basal resource. Macroinvertebrate consumers maintained stoichiometric homeostasis across stream groups, but consumer stoichiometry differed across families. Values of δ13C did not vary across stream groups for basal resources; however, consumer δ13C did. Although δ15N did not differ among basal resources across stream groups, macroinvertebrate consumer δ15N differed because of the interaction between stream group and family. Our results show catchment land cover did not predictably alter the stoichiometry or stable isotope compositions of basal resources or consumers in headwater streams. The quality of basal resources in headwater streams could differ across catchments with varying land cover, but it is evident that differences in stoichiometry of basal resources did not lead to differences in stoichiometry of consumers in our study. Given the variability of stable isotope compositions, additional effort should be made to improve our understanding of the landscape factors that might influence isotopic data.

Realistic Fasting Does Not Affect Stable Isotope Levels of a Metabolically Efficient Salamander

Abstract Stable isotopes are commonly used to examine various aspects of animal ecology. The use of stable isotopes generally proceeds under the implicit assumption that resource use is the only factor driving variation in stable isotope levels; however, a wealth of studies demonstrate that a range of common ecological factors can affect the behavior of stable isotopes in animal tissues and potentially confound inferences. For example, studies of some invertebrates and endothermic vertebrates show that animals fasted for ecologically realistic time periods have higher nitrogen (δ15N) or lower carbon (δ13C). We examined whether realistic fasting would influence the stable isotope composition of one of the most metabolically efficient ectothermic vertebrates, the Eastern Red-backed Salamander, Plethodon cinereus. We fasted salamanders for 7, 14, 21, 28, or 35-day intervals and examined whether δ15N or δ13C levels of tissues changed between fasted and fed animals. We investigated whether body condition (body mass to length and C:N [an index of lipid levels]) declined in fasted animals and whether there was a relationship between C:N and δ15N or δ13C. Body mass to length index and C:N, δ13C, and δ15N of tail and liver tissues did not differ between fasted and fed animals between 7 and 35 days. Because of their extreme metabolic efficiency, vertebrate ectotherms such as lungless salamanders (Plethodontidae) may not show the effects of fasting on stable isotopes observed in endothermic vertebrates and some invertebrates. This difference should lead to simpler interpretation of stable isotope results from field studies of these animals.

Effective Use of Trails for Assessing Terrestrial Salamander Abundance and Detection: A Case Study at Great Smoky Mountains National Park

ABSTRACT: The conservation and management of wildlife species is contingent on estimating distribution and abundance. Sampling of wildlife requires repeated visits to accurately determine species occurrence and to quantify abundance across temporal and spatial scales. The use of trails to sample wildlife populations is increasing and offers opportunities to potentially sample more frequently, with increased ease of access, and less disturbance to habitats, which can be important in sensitive natural areas. We examined capture data of terrestrial salamanders within Great Smoky Mountains National Park to determine if detection and abundance estimates from trail and non-trail transects were significantly different. Across two, 3-week periods during June and July 2012, we sampled 195 transects (70 along trails and 125 within non-trail habitat) on multiple occasions. We found that most microhabitat variables associated with salamander detection and abundance did not differ between trail and non-trail transects. Further, our models indicate detection and abundance of terrestrial salamanders were not significantly different on trail and non-trail transects. These results suggest trails can be used to accurately estimate abundance of terrestrial salamanders and may reduce the need to sample for plethodontid salamanders in sensitive habitat.

A global database of nitrogen and phosphorus excretion rates of aquatic animals

Animals can be important in modulating ecosystem-level nutrient cycling, although their importance varies greatly among species and ecosystems. Nutrient cycling rates of individual animals represent valuable data for testing the predictions of important frameworks such as the Metabolic Theory of Ecology (MTE) and ecological stoichiometry (ES). They also represent an important set of functional traits that may reflect both environmental and phylogenetic influences. Over the past two decades, studies of animal-mediated nutrient cycling have increased dramatically, especially in aquatic ecosystems. Here we present a global compilation of aquatic animal nutrient excretion rates. The dataset includes 10,534 observations from freshwater and marine animals of N and/or P excretion rates. These observations represent 491 species, including most aquatic phyla. Coverage varies greatly among phyla and other taxonomic levels. The dataset includes information on animal body size, ambient temperature, taxonomic affiliations, and animal body N:P. This data set was used to test predictions of MTE and ES, as described in Vanni and McIntyre (2016; Ecology DOI: 10.1002/ecy.1582).

Detritus Quality and Locality Determines Survival and Mass, but Not Export, of Wood Frogs at Metamorphosis

Single-site experiments have demonstrated detritus quality in wetlands can have strongly negative, neutral, and even positive influences on wildlife. However, an examination of the influence of detritus quality across several regions is lacking and can provide information on whether impacts from variation in detritus quality are consistent across species with wide ranges. To address this gap in regional studies we examined effects of emergent and allochthonous detritus of different nutrient qualities on amphibians and assessed a mechanism that may contribute to potential impacts. We used aquatic mesocosms to raise wood frogs (Rana sylvatica) from two regions of the United States with whole plants from purple loosestrife (Lythrum salicaria), leaf litter from native hardwood trees, and a mixture of both. We examined several metrics of amphibian fitness and life history, including survival, number of days to metamorphosis, and size at metamorphosis. Further, we quantified whether the effects of detritus type could translate to variation in anuran biomass or standing stock of nitrogen or phosphorus export. Our results show detritus with high nutrient quality (purple loosestrife) negatively influenced survival of wood frogs, but increased size of metamorphic individuals in two different regions of the United States. Despite the decrease in survival, the increase in size of post-metamorphic anurans raised with high quality detritus resulted in anuran biomass and standing stock of N and P export being similar across treatments at both locations. These results further demonstrate the role of plant quality in shaping wetland ecosystem dynamics, and represent the first demonstration that effects are consistent within species across ecoregional boundaries.

Stoichiometry of a semi-aquatic plethodontid salamander: intraspecific variation due to location, size and diet.

Ecological stoichiometry provides a framework to investigate an organisms relationship to nutrient cycles. An organisms stoichiometry is thought to constrain its contribution to nutrient cycles (recycling or storage), and to limit its growth and reproduction. Factors that influence the stoichiometry of a consumer are largely unstudied, but what is known is that consumer stoichiometry is influenced by the elemental requirements of the consumer (e.g. for growth, reproduction and cell maintenance) and the availability of elements. We examined whole-body stoichiometry of larval southern two-lined salamanders (Eurycea cirrigera) and described the influence of location, body size, stoichiometry of diet items, and environmental nutrient supply on whole-body stoichiometry. Mean composition of phosphorous was 2.6%, nitrogen was 11.3%, and carbon was 39.6%, which are similar for other aquatic vertebrate taxa. The most significant predictor of whole-body stoichiometry was the site where the samples were collected, which was significant for each nutrient and nutrient ratio. Body size and stoichiometry of diet items were also predictors of Eurycea cirrigera stoichiometry. Our study suggests that spatial differences in environmental nutrient supply have a stronger influence on consumer whole-body stoichiometry among similar-sized larvae compared to life history traits, such as body size or diet.

Diet of Western Slimy Salamander, Plethodon albagula (Caudata: Plethodontidae), from Two Mountain Ranges in Arkansas

Abstract We identified stomach contents of 80 Plethodon albagula (Western Slimy Salamander) from two mountain ranges in Arkansas (Ozark and Ouachita) to examine if regional differences in diet occur. Museum specimens from 1985 to 2005 were used from locations throughout each mountain range. Although a wide variety of prey were found in stomachs, Hymenoptera: Formicidae and Coleoptera: Carabidae were found to be the most important food items in the diet of P. albagula. Ants and beetles constituted 85% abundance of their total diet (79.6% Ozark and 90.1% Ouachita) and 52.2% of their total biomass (42.6% Ozark and 64.1% Ouachita). Seventy-eight and 87% of individuals examined from the Ozark and Ouachita Mountains, respectively, consumed ants (65% total, 83% for animals with food items in their stomachs), whereas 55% in the Ozarks and 58% in the Ouachitas consumed at least one family of beetle. Occurrence and biomass of prey items that did not include ants and beetles showed P. albagula to be a euryphagic predator, with 9.7% of diet being comprised of other prey types (27.3% biomass). Furthermore, importance values indicate ants were the most important prey item for P. albagula in both the Ozark and Ouachita samples, with carabid beetles (Ozark) and all beetles (Ouachita) being second most important. Jaccard Index indicated Ozark and Ouachita specimens shared 80% similarity in diet. Our data suggest P. albagula in Arkansas have high dependence upon ants and beetles, yet appears to be an opportunistic and euryphagic predator.