Deanna H. Olson

Mapping the Global Emergence of Batrachochytrium dendrobatidis, the Amphibian Chytrid Fungus

The rapid worldwide emergence of the amphibian pathogen Batrachochytrium dendrobatidis (Bd) is having a profound negative impact on biodiversity. However, global research efforts are fragmented and an overarching synthesis of global infection data is lacking. Here, we provide results from a community tool for the compilation of worldwide Bd presence and report on the analyses of data collated over a four-year period. Using this online database, we analysed: 1) spatial and taxonomic patterns of infection, including amphibian families that appear over- and under-infected; 2) relationships between Bd occurrence and declining amphibian species, including associations among Bd occurrence, species richness, and enigmatic population declines; and 3) patterns of environmental correlates with Bd, including climate metrics for all species combined and three families (Hylidae, Bufonidae, Ranidae) separately, at both a global scale and regional (U.S.A.) scale. These associations provide new insights for downscaled hypothesis testing. The pathogen has been detected in 52 of 82 countries in which sampling was reported, and it has been detected in 516 of 1240 (42%) amphibian species. We show that detected Bd infections are related to amphibian biodiversity and locations experiencing rapid enigmatic declines, supporting the hypothesis that greater complexity of amphibian communities increases the likelihood of emergence of infection and transmission of Bd. Using a global model including all sampled species, the odds of Bd detection decreased with increasing temperature range at a site. Further consideration of temperature range, rather than maximum or minimum temperatures, may provide new insights into Bd-host ecology. Whereas caution is necessary when interpreting such a broad global dataset, the use of our pathogen database is helping to inform studies of the epidemiology of Bd, as well as enabling regional, national, and international prioritization of conservation efforts. We provide recommendations for adaptive management to enhance the database utility and relevance.

Host Identity Matters in the Amphibian- Batrachochytrium dendrobatidis System: Fine-Scale Patterns of Variation in Responses to a Multi-Host Pathogen

Species composition within ecological assemblages can drive disease dynamics including pathogen invasion, spread, and persistence. In multi-host pathogen systems, interspecific variation in responses to infection creates important context dependency when predicting the outcome of disease. Here, we examine the responses of three sympatric host species to a single fungal pathogen, Batrachochytrium dendrobatidis, which is associated with worldwide amphibian population declines and extinctions. Using an experimental approach, we show that amphibian species from three different genera display significant differences in patterns of pathgen-induced mortality as well as the magnitude and temporal dynamics of infection load. We exposed amphibians to one of four inoculation dose treatments at both larval and post- metamorphic stages and quantified infection load on day 8 and day 15 post-inoculation. Of the three species examined, only one (the Pacific treefrog; Pseudacris regilla) displayed “dose-dependent” responses; survival was reduced and infection load was elevated as inoculation dose was increased. We observed a reduction in survival but no differences in infection load across pathogen treatments in Cascades frogs (Rana cascadae). Western toads (Anaxyrus boreas) displayed differences in infection load but no differences in survival across pathogen treatments. Within species, responses to the pathogen varied with life history stage, and the most heavily infected species at the larval stage was different from the most heavily infected species at the post-metamorphic stage. Temporal changes in infection load were species and life history stage-specific. We show that variation in susceptibility to this multi-host pathogen is complex when viewed at a fine-scale and may be mediated through intrinsic host traits.

DNA REPAIR AND RESISTANCE TO UV-B RADIATION IN WESTERN SPOTTED FROGS

We assessed DNA repair and resistance to solar radiation in eggs of members of the western spotted frog complex (Rana pretiosa and R. luteiventris), species whose populations are suffering severe range reductions and declines. Specifically, we measured the activity of photoreactivating enzyme (photolyase) in oocytes of spotted frogs. In some species, photoreactivation is the most important mechanism for repair of UV-damaged DNA. Using field experiments, we also compared the hatching success of spotted frog embryos at natural oviposition sites at three elevations, where some embryos were subjected to ambient levels of UV-B radiation and others were shielded from UV-B radiation. Compared with other amphibians, photolyase activities in spotted frogs were relatively high. At all sites, hatching success was unaffected by UV-B. Our data support the interpretation that amphibian embryos with relatively high levels of photolyase are more resistant to UV-B radiation than those with lower levels of photolyase. At the embryonic stage, UV-B radiation does not presently seem to be contributing to the population declines of spotted frogs.

Species-level correlates of susceptibility to the pathogenic amphibian fungus Batrachochytrium dendrobatidis in the United States

Disease is often implicated as a factor in population declines of wildlife and plants. Understanding the characteristics that may predispose a species to infection by a particular pathogen can help direct conservation efforts. Recent declines in amphibian populations world-wide are a major conservation issue and may be caused in part by a fungal pathogen, Batrachochytrium dendrobatidis (Bd). We used Random Forest, a machine learning approach, to identify species-level characteristics that may be related to susceptibility to Bd. Our results suggest that body size at maturity, aspects of egg laying behavior, taxonomic order and family, and reliance on water are good predictors of documented infection for species in the continental United States. These results suggest that, whereas local-scale environmental variables are important to the spread of Bd, species-level characteristics may also influence susceptibility to Bd. The relationships identified in this study suggest future experimental tests, and may target species for conservation efforts.

Heterogeneous Occupancy and Density Estimates of the Pathogenic Fungus Batrachochytrium dendrobatidis in Waters of North America

Biodiversity losses are occurring worldwide due to a combination of stressors. For example, by one estimate, 40% of amphibian species are vulnerable to extinction, and disease is one threat to amphibian populations. The emerging infectious disease chytridiomycosis, caused by the aquatic fungus Batrachochytrium dendrobatidis (Bd), is a contributor to amphibian declines worldwide. Bd research has focused on the dynamics of the pathogen in its amphibian hosts, with little emphasis on investigating the dynamics of free-living Bd. Therefore, we investigated patterns of Bd occupancy and density in amphibian habitats using occupancy models, powerful tools for estimating site occupancy and detection probability. Occupancy models have been used to investigate diseases where the focus was on pathogen occurrence in the host. We applied occupancy models to investigate free-living Bd in North American surface waters to determine Bd seasonality, relationships between Bd site occupancy and habitat attributes, and probability of detection from water samples as a function of the number of samples, sample volume, and water quality. We also report on the temporal patterns of Bd density from a 4-year case study of a Bd-positive wetland. We provide evidence that Bd occurs in the environment year-round. Bd exhibited temporal and spatial heterogeneity in density, but did not exhibit seasonality in occupancy. Bd was detected in all months, typically at less than 100 zoospores L−1. The highest density observed was ∼3 million zoospores L−1. We detected Bd in 47% of sites sampled, but estimated that Bd occupied 61% of sites, highlighting the importance of accounting for imperfect detection. When Bd was present, there was a 95% chance of detecting it with four samples of 600 ml of water or five samples of 60 mL. Our findings provide important baseline information to advance the study of Bd disease ecology, and advance our understanding of amphibian exposure to free-living Bd in aquatic habitats over time.

Downed Wood Microclimates and Their Potential Impact on Plethodontid Salamander Habitat in the Oregon Coast Range

Abstract Downed wood provides important faunal microhabitat in forests for numerous invertebrate taxa, small mammals and amphibians. Habitat suitability of downed wood as refugia is an increasing concern in managed Pacific Northwest forests, where overstory reduction may result in both reduced downed wood recruitment and increased temperatures within logs. We examined temperature profiles in western Oregon to assess differences in thermal regimes of logs and soil relative to summer air temperature extremes and their implications with respect to habitat suitability for plethodontid salamanders. Temperature profiles of small- (0.3–0.45 m) and large- (0.7–1.0 m) diameter logs, as well as ambient soil and air temperatures, were measured in a 60-year-old forest stand at two different positions (0–5 m and 35–40 m from stream edge) in three case studies: 1) along a headwater stream with a narrow riparian buffer (∼6 m) and moderate upslope thinning; 2) along a headwater stream with a wider riparian buffer (∼15 m) and moderate upslope thinning; and 3) along a headwater stream with an unthinned upslope. Streamside and upslope maximum air temperatures measured during July 2006 along all three streams were near or exceeded 30°C, the critical thermal tolerance threshold for western plethodontid salamanders. Streamside and upslope temperatures inside small logs, large logs and soils stayed below critical temperatures. Our results suggest that logs of a wide size range, as well as soils, may provide sufficient protection against thermal extremes in uncut forests and thinned stands with limited overstory.

Survival and Growth of Larval Coastal Giant Salamanders (Dicamptodon tenebrosus) in Streams in the Oregon Coast Range

Abstract Conditions that affect amphibian larval growth and survival can affect population structure through both larval and adult stages of their life history. We conducted a two-year, mark-recapture study of larval, Coastal Giant Salamanders, Dicamptodon tenebrosus, in 14 small streams in the Oregon Coast Range to assess spatial and temporal variation in growth and apparent survival. We modeled larval survival and growth by season and age class and examined these demographic rates in the presence of road crossing culverts. Cormack-Jolly-Seber models indicated that apparent survival was lower for first-year larvae than second/third-year larvae (13%, SE  =  0.03; 28%, SE  =  0.08) and apparent survival varied by time/season. The >5% difference in the effect of age on survival is potentially biologically significant (effect size  =  −0.10; confidence interval  =  −0.05, −0.16). Effects of culverts on larval survival were inconclusive, while no effects on growth were detected.

Differences in sensitivity to the fungal pathogen Batrachochytrium dendrobatidis among amphibian populations

Contributing to the worldwide biodiversity crisis are emerging infectious diseases, which can lead to extirpations and extinctions of hosts. For example, the infectious fungal pathogen Batrachochytrium dendrobatidis (Bd) is associated with worldwide amphibian population declines and extinctions. Sensitivity to Bd varies with species, season, and life stage. However, there is little information on whether sensitivity to Bd differs among populations, which is essential for understanding Bd-infection dynamics and for formulating conservation strategies. We experimentally investigated intraspecific differences in host sensitivity to Bd across 10 populations of wood frogs (Lithobates sylvaticus) raised from eggs to metamorphosis. We exposed the post-metamorphic wood frogs to Bd and monitored survival for 30 days under controlled laboratory conditions. Populations differed in overall survival and mortality rate. Infection load also differed among populations but was not correlated with population differences in risk of mortality. Such population-level variation in sensitivity to Bd may result in reservoir populations that may be a source for the transmission of Bd to other sensitive populations or species. Alternatively, remnant populations that are less sensitive to Bd could serve as sources for recolonization after epidemic events.

Batrachochytrium salamandrivorans: The North American Response and a Call for Action.

Batrachochytrium salamandrivorans (Bsal) is an emerging fungal pathogen that has caused recent die-offs of native salamanders in Europe and is known to be lethal to at least some North American species in laboratory trials [1]. Bsal appears to have originated in Asia, and may have been introduced by humans into wild populations in Europe through commercial trade of amphibians [1]. Since the first outbreaks of Bsal in the Netherlands, it has been the etiologic agent of mortality events in Belgium (wild) and Germany (captivity), and was recently found in imported salamanders in the United Kingdom [1–4]. Substantial concern has been raised about the associated risk of Bsal to native salamanders in North America [5]. Herein, we review what policy actions are occurring in North America and elsewhere, and call for creation of a North American Bsal Strategic Plan.

Options for biodiversity conservation in managed forest landscapes of multiple ownerships in Oregon and Washington, USA

We examine existing and developing approaches to balance biodiversity conservation and timber production with the changing conservation roles of federal and nonfederal forest land ownerships in the US Pacific Northwest. At landscape scales, implementation of the reserve-matrix approach of the federal Northwest Forest Plan in 1994 was followed by proposals of alternative designs to better integrate disturbance regimes or to conserve biodiversity in landscapes of predominantly young forests through active management without reserves. At stand scales, landowners can improve habitat heterogeneity through a host of conventional and alternative silvicultural techniques. There are no state rules that explicitly require biodiversity conservation on nonfederal lands in the region. However, state forest practices rules require retention of structural legacies to enhance habitat complexity and establishment of riparian management areas to conserve aquatic ecosystems. Habitat Conservation Plans (HCPs) under the US Endangered Species Act provide regulatory incentives for nonfederal landowners to protect threatened and endangered species. A state-wide programmatic HCP has recently emerged as a multi-species conservation approach on nonfederal lands. Among voluntary incentives, the Forest Stewardship Council certification comprehensively addresses fundamental elements of biodiversity conservation; however, its tough conservation requirements may limit its coverage to relatively small land areas. Future changes in landscape management strategies on federal lands may occur without coordination with nonfederal landowners because of the differences in regulatory and voluntary incentives between ownerships. This raises concerns when potentially reduced protections on federal lands are proposed, and the capacity of the remaining landscape to compensate has been degraded.