Direct and indirect impacts of wildfire on faunal communities of Mediterranean temporary ponds

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Riverine barriers to gene flow in a salamander with both aquatic and terrestrial reproduction

The riverine barrier hypothesis (RBH) posits that rivers comprise geographical barriers to gene flow for terrestrial organisms, thus promoting genetic differentiation between populations. Here, we explored the RBH on larviparous and pueriparous populations of the live-bearing fire salamander (Salamandra salamandra). While larviparous fire salamanders exhibit a semi-aquatic life cycle (females deposit pre-metamorphic larvae on water), pueriparous salamanders present a fully terrestrial life cycle (females deliver terrestrial juveniles) and, therefore, a greater independence from water for survival and reproduction. We performed a fine-scale sampling of opposite transects in 11 rivers (six and five for larviparous and pueriparous populations, respectively) to test the hypothesis that rivers are more effective barriers for pueriparous salamanders due to their terrestrial life cycle. We carried out individual- and population-based genetic analyses using 14 microsatellites and a mitochondrial marker to examine the extent to which rivers hinder short- and long-term gene flow. We found that rivers are semi-permeable obstacles for both larviparous and pueriparous salamanders, although they appear to be more effective barriers for the latter when rivers with similar attributes are compared. We also found that river width and possibly the presence of crossing structures may influence the genetic barrier effects of rivers in fire salamanders. This is one of the very few studies in amphibians showing how different reproductive strategies influence the barrier effects imposed by rivers.

     

The influence of habitat provisioning: use of earthworm burrows by the terrestrial salamander, Plethodon cinereus

Studies examining the influence of habitat provisioning by one species on the behavior of other species can provide key insights regarding impacts of ecosystem engineers on the availability of resources to other species. More specifically, an organism’s use of additional habitat provided by ecosystem engineers may affect the interpretation of observational or demographic data. We chose to examine the possible influence of earthworms, as ecosystem engineers, on the behavior of terrestrial salamanders, common forest vertebrates in North America. We conducted two experiments in microcosms to examine whether the earthworm Lumbricus terrestris acted as an ecosystem engineer by providing additional habitat (burrows) for Plethodon cinereus, a common woodland salamander. We also examined whether the behavioral changes of the non-burrowing, fossorial P. cinereus differed across age classes. Adults and juveniles responded similarly, with both adults and juveniles found under cover objects more often when earthworms were absent and using earthworm burrows when available. Our field data supported our experimental data in that greater numbers of earthworms on field plots were associated with a lower proportion of cover objects being occupied by salamanders (i.e., salamanders were likely underground). We found no differences in the response of adults and juveniles to the presence of earthworms. By providing underground habitat for a common terrestrial amphibian, the presence of earthworms may impact demographic studies on salamanders and conclusions drawn from those studies regarding aboveground faunal communities in eastern North America.     

Effects of Timber Harvests and Silvicultural Edges on Terrestrial Salamanders

Balancing timber production and conservation in forest management requires an understanding of how timber harvests affect wildlife species. Terrestrial salamanders are useful indicators of mature forest ecosystem health due to their importance to ecosystem processes and sensitivity to environmental change. However, the effects of timber harvests on salamanders, though often researched, are still not well understood. To further this understanding, we used artificial cover objects to monitor the relative abundance of terrestrial salamanders for two seasons (fall and spring) pre-harvest and five seasons post-harvest in six forest management treatments, and for three seasons post-harvest across the edge gradients of six recent clearcuts. In total, we recorded 19,048 encounters representing nine species of salamanders. We observed declines in mean encounters of eastern red-backed salamanders (Plethodon cinereus) and northern slimy salamanders (P. glutinosus) from pre- to post-harvest in group selection cuts and in clearcuts. However, we found no evidence of salamander declines at shelterwoods and forested sites adjacent to harvests. Edge effects induced by recent clearcuts influenced salamanders for approximately 20 m into the forest, but edge influence varied by slope orientation. Temperature, soil moisture, and canopy cover were all correlated with salamander counts. Our results suggest silvicultural techniques that remove the forest canopy negatively affect salamander relative abundance on the local scale during the years immediately following harvest, and that the depth of edge influence of clearcuts on terrestrial salamanders is relatively shallow (<20 m). Small harvests (<4 ha) and techniques that leave the forest canopy intact may be compatible with maintaining terrestrial salamander populations across a forested landscape. Our results demonstrate the importance of examining species-specific responses and monitoring salamanders across multiple seasons and years. Long-term monitoring will be necessary to understand the full impacts of forest management on terrestrial salamanders.     

Survey for the pathogenic chytrid fungus Batrachochytrium dendrobatidis in southwestern North Carolina salamander populations

Batrachochytrium dendrobatidis is a fungal pathogen responsible for a potentially fatal disease of amphibians. We conducted a survey for B. dendrobatidis in the Appalachian Mountains of southwestern North Carolina, USA, from 10 June to 23 July 23 2009. Ventral skin swabs were collected from plethodontid salamanders (n=278) and real-time PCR was performed to test for the presence of B. dendrobatidis. We found no evidence of B. dendrobatidis, suggesting that B. dendrobatidis is absent or present in such low levels that it was undetected. If B. dendrobatidis was present at the time of our sampling, this survey supports evidence of low prevalence of B. dendrobatidis in North American headwater stream salamander populations.     

Evaluating the effects of urbanisation on salamander abundances using a before‐after control‐impact design

1. Urbanisation represents a significant threat to semi‐aquatic amphibian populations, especially stream‐dwelling salamanders. Although studies of urbanisation effects on amphibians have been conducted, there is an urgent need to follow populations over longer time periods, account for imperfect detection and determine the response time to urbanisation. Consequently, we used a before‐after control‐impact (BACI) study design to estimate changes in abundances of larval and adult salamanders in streams affected by urbanisation. 2. From 2005 to 2009, we used standard sampling techniques to obtain a count of salamanders in 13 first‐order streams that underwent urbanisation of their catchments after the first year of sampling. Simultaneously, we counted salamanders in 17 streams that experienced no disturbance within stream catchments. Additionally, we measured environmental variables at each stream. 3. We used Royle’s binomial mixture model to estimate annual mean abundances and individual detection probabilities, and Bayesian inference was used to estimate population parameters for each stage and species. 4. Although mean abundance estimates varied among years in control and urbanised streams, we found that urbanisation had a negative effect on larval and adult salamander abundances. Larval salamander abundances at sites 1 year after urbanisation were significantly lower than abundances from control sites. Abundances of adult two‐lined salamanders (Eurycea cirrigera) at urbanised sites were lower than abundances at control sites 2 years post‐urbanisation, and adult dusky salamander (Desmognathus fuscus) abundances at urbanised sites were lower than abundances at control sites 3 years post‐urbanisation. Maximum conductivity, sedimentation level and maximum stream channel width differed between urban and non‐urban streams. 5. Our results suggest that stream‐dwelling salamanders exhibit little resistance to urbanisation. Our study also highlights the use of the BACI design to study how urbanisation affects populations in semi‐aquatic habitats. We emphasise that inferences regarding urbanisation effects on population response may be compromised unless urban populations are compared to populations in control sites, especially for species in which populations fluctuate.     

Methodological considerations for detection of terrestrial small‐body salamander eDNA and implications for biodiversity conservation

Environmental DNA (eDNA) can be used as an assessment tool to detect populations of threatened species and provide fine‐scale data required to make management decisions. The objectives of this project were to use quantitative PCR (qPCR) to: (i) detect spiked salamander DNA in soil, (ii) quantify eDNA degradation over time, (iii) determine detectability of salamander eDNA in a terrestrial environment using soil, faeces, and skin swabs, (iv) detect salamander eDNA in a mesocosm experiment. Salamander eDNA was positively detected in 100% of skin swabs and 66% of faecal samples and concentrations did not differ between the two sources. However, eDNA was not detected in soil samples collected from directly underneath wild‐caught living salamanders. Salamander genomic DNA (gDNA) was detected in all qPCR reactions when spiked into soil at 10.0, 5.0, and 1.0 ng/g soil and spike concentration had a significant effect on detected concentrations. Only 33% of samples showed recoverable eDNA when spiked with 0.25 ng/g soil, which was the low end of eDNA detection. To determine the rate of eDNA degradation, gDNA (1 ng/g soil) was spiked into soil and quantified over seven days. Salamander eDNA concentrations decreased across days, but eDNA was still amplifiable at day 7. Salamander eDNA was detected in two of 182 mesocosm soil samples over 12 weeks (n = 52 control samples; n = 65 presence samples; n = 65 eviction samples). The discrepancy in detection success between experiments indicates the potential challenges for this method to be used as a monitoring technique for small‐bodied wild terrestrial salamander populations.     

Diet composition of two larval headwater stream salamanders and spatial distribution of prey

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Conservation genetics of an endemic mountaintop salamander with an extremely limited range

Montane regions can promote allopatric speciation and harbor unique species with small ranges. The southern Appalachians are a biodiversity hotspot for salamanders, and several montane endemics occur in the region. Here, we present the first DNA sequence data for Plethodon sherando, a terrestrial salamander recently discovered in the Blue Ridge Mountains of Virginia. We sequenced two mitochondrial regions (cyt-b and CO1) from salamanders at reference sites near the center of P. sherando’s range and from two contact zones where P. sherando populations are replaced by Plethodon cinereus, the Northern Red-Backed salamander. We then used these sequence data to examine divergence and hybridization between the two taxa. We found P. sherando and P. cinereus morphotypes from contact zones to be reciprocally monophyletic and highly divergent (~17%). P. sherando exhibited very low sequence diversity (π = 0.0010) as compared to P. cinereus from the same locations (π = 0.0096). Salamander morphology in the contact zone was as distinct as morphology at reference sites, and discriminant function analysis based on morphology successfully classified 98% of salamanders to their mitochondrial lineage. Phylogenetic analysis of cyt-b sequences showed P. sherando to be sister to Plethodon serratus (the Southern Red-Backed salamander) rather than P. cinereus or any nearby mountaintop endemics. Our results suggest that P. sherando is a distinct lineage that is not subject to substantial introgression from P. cinereus and that may have a history of geographic isolation. Given its limited range (<80 km²), we believe P. sherando should merit a conservation status similar to that of other mountaintop salamanders in the region.     

Linking the evolution of habitat choice to ecosystem functioning: direct and indirect effects of pond-reproducing fire salamanders on aquatic-terrestrial subsidies

Shifts in life history traits and in the behaviour of species can potentially alter ecosystem functioning. The reproduction of the central European fire salamander (Salamandra salamandra), which usually deposits its larvae in first-order streams, in small pool and pond-like habitats, is an example of a recent local adaptation in this species. Here we aimed to quantify the direct and indirect effects of the predatory larvae on the aquatic food webs in the ponds and on the flux of matter between the ponds and adjacent terrestrial habitats. Our estimates are based on biomass data of the present pond fauna as well as on the analysis of stomach content data, growth rates and population dynamics of the salamander larvae in pond habitats. By their deposition of larvae in early spring, female fire salamanders import between 0.07 and 2.86 g dry mass m^?2 larval biomass into the ponds. Due to high mortality rates in the larval phase and the relatively small size at metamorphosis of the pond-adapted salamanders compared to stream-adapted ones, the biomass export of the metamorphosed salamanders clearly falls below the initial biomass import. Catastrophic events such as high water temperatures and low oxygen levels may even occasionally result in mass mortalities of salamander larvae and thus in a net 100 % import of the salamander biomass into the pond food webs. Indirect effects further accelerate this net import of matter into the aquatic habitat, e.g. the feeding of salamanders on aquatic insect larvae with the emergence of terrestrial adults—thus preventing export—and on terrestrial organisms that fall on the water surface (supporting import). This study demonstrates that the adaptation of salamanders to pond reproduction can alter food web linkages across ecosystem boundaries by enhancing the flux of materials and energy from terrestrial (i.e. forest) to the aquatic (i.e. pond) habitat.     

Introduced invertebrates are important prey for a generalist predator

Concern over biological invasions has drawn increased attention to the impacts of introduced predators or competitors, but not to the importance of introduced prey. North American forests are rich in introduced invertebrates, including species that represent relatively novel taxonomic or trophic guilds and show biased distributions among forest types. We analysed the diets of red‐backed salamanders, Plethodon cinereus, from three upland and three lowland forests to determine whether introduced prey are important contributors to geographical or temporal variation in salamander food resources. We found several introduced species were volumetrically important salamander prey, and were responsible for resource differences between forest types and much of the seasonal fluctuation in food resources in both forest types. In lowland forests, rain had a stronger effect on salamander predation on non‐native earthworms than native taxa, creating more dynamic resource fluctuations in resource levels than was observed in upland forests where earthworms were absent. With one exception, predation on non‐native species was positively associated with predation on native species, suggesting non‐native prey have added to salamander resources rather than replaced salamander predation on native taxa. We hypothesize that the novel resource gradients created by non‐native prey introductions are contributing to patterns of geographical and temporal phenotypic variation among salamander populations.     

Evaluating reserves for species richness and representation in northern California

The Klamath‐Siskiyou forests of northern California and southern Oregon are recognized as an area of globally outstanding biological distinctiveness. When evaluated at a national or global level, this region is often, necessarily, considered to be uniformly diverse. Due to large variation in biotic and abiotic variables throughout this region, however, it is unlikely that biological diversity is uniformly distributed. Furthermore, land management decisions nearly always occur at spatial scales smaller than this entire region. Therefore, we used field data from a random sampling design to map the distribution of local and regional richness of terrestrial molluscs and salamanders within northern California's portion of the Klamath‐Siskiyou region. We also evaluated the protection afforded by reserves established for varying reasons (e.g. for inspiration and recreation for people vs. species conservation) to hotspots of species richness and species representation of these taxa. No existing reserves were created with these taxa in mind, yet it was assumed that reserves established largely around considerations for the northern spotted owl (Strix occidentalis caurina) would afford adequate protection for many lesser‐known species. Species of terrestrial molluscs and salamanders share two general features: (1) they have extremely low vagility, and (2) they are often associated with moist, cool microclimates. Existing reserves disproportionately included areas of hotspots of species richness for both taxa, when hotspots included the richest c. 25% of the area, whereas non‐reserved lands contained greater than expected areas with lower species richness. However, when a more strict definition of hotspot was used (i.e. the richest c.10% of areas), local hotspots for both taxa were not disproportionately found in reserves. Reserves set aside largely for human aesthetics and recreation and those set aside for biodiversity both contributed to the protection of areas with high (greatest 25%) species richness. Existing biodiversity reserves represented 68% of mollusc species and 73% of salamander species, corresponding to the 99th and 93rd percentiles, respectively, of species representation achieved by simulating a random distribution of the same total area of reservation. Cumulatively, however, reserves set aside for inspiration and biodiversity represented 83% of mollusc species and 91% of salamander species. The existing reserves provide conservation value for terrestrial molluscs and salamanders. This reserve network, however, should not be considered optimal for either taxa.     

Differential Effects of an Intense Wildfire on Survival of Sympatric Snakes

Abstract: We analyzed 16 years of mark-recapture data to investigate whether a wildfire influenced survival of an arboreal ambush-forager (broad-headed snake [Hoplocephalus bungaroides]) and a terrestrial active forager (small-eyed snake Cryptophis nigrescens). We predicted that wildfire would cause direct mortality and reduce subsequent survival of both snake species. Contrary to this prediction, wildfire did not affect abundance of broad-headed snakes, but abundance of small-eyed snakes decreased by 48% after the wildfire. Estimated annual survival of small-eyed snakes was 37% lower after fire (s=0.47, SE=0.07) than before fire (s=0.74, SE=0.05). Prescribed burning may be a suitable tool for creating open habitat mosaics for the endangered broad-headed snake.     

Experimental studies on direct and indirect interactions in a three trophic-level stream system

Summary We used a complete block design to experimentally study direct and indirect interactions in a three trophic-level freshwater system consisting of a top predator, the green sunfish, Lepomis cyanellus, an intermediate predator, small-mouthed salamander larvae, Ambystoma barbouri, and prey, hatchling isopods, Lirceus fontinalis. This system occurs naturally in small stream pools in central Kentucky; experiments were done in laboratory pools. Salamander larvae ate isopods and thus had a direct, negative effect on isopod survival. Accordingly, isopods responded to the presence of salamander larvae by increasing their tendency to bury themselves in the sand substrate. Fish ate salamanders and thus had a direct, negative effect on salamander survival. Salamanders responded to fish presence by increasing their time spent under plexiglass plates that simulate refuge rocks. The overall effect of fish on isopods depended on the presence of salamanders. In the absence of salamanders, fish predation on isopods had a direct, negative effect on isopod survival; isopods thus responded to the presence of fish by burying themselves in the sand. With salamanders present, fish had a positive overall effect on isopod survival; i.e., direct, negative effects of fish on isopods were outweighed by indirect, positive effects. Indirect positive effects of fish on isopods came through a reduction in salamander predation rates on isopods in the presence of fish. The mechanism involved both a decrease in the number of salamanders (a trophic-linkage indirect effect; cf. Miller and Kerfoot 1987) and a reduction in the feeding rate of individual salamanders on isopods (a behavioral indirect effect). The decrease in individual salamander feeding rates on isopods was due to reductions in both salamander activity and in spatial overlap between salamanders and isopods in the presence of fish. The latter effect reflected the fact that salamanders and isopods used different refuges from fish; salamanders went under refuge plates, whereas isopods primarily buried themselves in sand. Estimates of the relative importance of various direct and indirect effects of sunfish on isopods suggested that positive, behavioral indirect effects were of roughly the same magnitude as direct, negative effects, both of which were more important than were trophic-linkage indirect effects. Contrary to expectations, the presence of isopods did not affect the refuge use or survival of salamanders in the presence of fish.     

Estimating Survival for Elusive Juvenile Pond-Breeding Salamanders

Juvenile vital rates have important effects on population dynamics for many species, but this demographic is often difficult to locate and track. As such, we frequently lack reliable estimates of juvenile survival, which are necessary for accurately assessing population stability and potential management approaches to conserve biodiversity. We estimated survival rates for elusive juveniles of 3 species, the ringed salamander (Ambystoma annulatum), spotted salamander (A. maculatum), and small-mouthed salamander (A. texanum), using 2 approaches. First, we conducted an 11-month (2016–2017) mark-recapture study within semi-natural enclosures and used Bayesian Cormack-Jolly-Seber models to estimate survival and recapture probabilities. Second, we inferred the expected annual juvenile survival rate given published vital rates for pre-metamorphic and adult ambystomatids assuming stable population growth. For all 3 species, juvenile survival probabilities were constant across recapture occasions, whereas recapture probability estimates were time-dependent. Further, survival and recapture probabilities among study species were similar. Post-study sampling revealed that the initial study period median estimate of annual survival probability (0.39) underestimated the number of salamanders known alive at 11 months. We therefore appended approximately 1 year of opportunistic data, which produced a median annual survival probability of 0.50, encompassing salamanders that we knew to have been alive. Calculation from literature values suggested a mean annual terrestrial juvenile ambystomatid survival probability of 0.49. Similar results among our approaches indicated that juvenile survival estimates for the study species were robust and likely comparable to rates in nature. These estimates can now be confidently applied to research, monitoring, and management efforts for the study species and ecologically similar taxa. Our findings indicated that similarly robust vital rate estimates for subsets of ecologically and phylogenetically similar species can provide reasonable surrogate demographic information that can be used to reveal key factors influencing population viability for data-deficient species. © 2020 The Wildlife Society.     

Creosote growth rate and reproduction increase in postfire environments

Human activities are changing patterns of ecological disturbance globally. In North American deserts, wildfire is increasing in size and frequency due to fuel characteristics of invasive annual grasses. Fire reduces the abundance and cover of native vegetation in desert ecosystems. In this study, we sought to characterize stem growth and reproductive output of a dominant native shrub in the Mojave Desert, creosote bush (Larrea tridentata (DC.) Coville) following wildfires that occurred in 2005. We sampled 55 shrubs along burned and unburned transects 12 years after the fires (2017) and quantified age, stem diameter, stem number, radial and vertical growth rates, and fruit production for each shrub. The shrubs on the burn transects were most likely postfire resprouts based on stem age while stems from unburn transects dated from before the fire. Stem and vertical growth rates for shrubs on burned transects were 2.6 and 1.7 times higher than that observed for shrubs on unburned transects. Fruit production of shrubs along burned transects was 4.7‐fold more than shrubs along paired unburned transects. Growth rates and fruit production of shrubs in burned areas did not differ with increasing distance from the burn perimeter. Positive growth and reproduction responses of creosote following wildfires could be critical for soil stabilization and re‐establishment of native plant communities in this desert system. Additional research is needed to assess if repeat fires that are characteristic of invasive grass‐fire cycles may limit these benefits.     

Evolution mediates the effects of apex predation on aquatic food webs

Ecological and evolutionary mechanisms are increasingly thought to shape local community dynamics. Here, I evaluate if the local adaptation of a meso-predator to an apex predator alters local food webs. The marbled salamander (Ambystoma opacum) is an apex predator that consumes both the spotted salamander (Ambystoma maculatum) and shared zooplankton prey. Common garden experiments reveal that spotted salamander populations which co-occur with marbled salamanders forage more intensely than those that face other predator species. These foraging differences, in turn, alter the diversity, abundance and composition of zooplankton communities in common garden experiments and natural ponds. Locally adapted spotted salamanders exacerbate prey biomass declines associated with apex predation, but dampen the top-down effects of apex predation on prey diversity. Countergradient selection on foraging explains why locally adapted spotted salamanders exacerbate prey biomass declines. The two salamander species prefer different prey species, which explains why adapted spotted salamanders buffer changes in prey composition owing to apex predation. Results suggest that local adaptation can strongly mediate effects from apex predation on local food webs. Community ecologists might often need to consider the evolutionary history of populations to understand local diversity patterns, food web dynamics, resource gradients and their responses to disturbance.     

High Occupancy of Stream Salamanders Despite High Ranavirus Prevalence in a Southern Appalachians Watershed

The interactive effects of environmental stressors and emerging infectious disease pose potential threats to stream salamander communities and their headwater stream ecosystems. To begin assessing these threats, we conducted occupancy surveys and pathogen screening of stream salamanders (Family Plethodontidae) in a protected southern Appalachians watershed in Georgia and North Carolina, USA. Of the 101 salamanders screened for both chytrid fungus (Batrachochytrium dendrobatidis) and Ranavirus, only two exhibited low-level chytrid infections. Prevalence of Ranavirus was much higher (30.4% among five species of Desmognathus). Despite the ubiquity of ranaviral infections, we found high probabilities of site occupancy (≥0.60) for all stream salamander species.