Presence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in native amphibians exported from Madagascar

The emerging infectious disease chytridiomycosis is driven by the spread of amphibian chytrid fungus (Batrachochytrium dendrobatidis, Bd), a highly virulent pathogen threatening global amphibian biodiversity. Although pandemic in distribution, previous intensive field surveys have failed to detect Bd in Madagascar, a biodiversity hotspot home to hundreds of endemic amphibian species. Due to the presence of Bd in nearby continental Africa and the ecological crisis that can be expected following establishment in Madagascar, enhanced surveillance is imperative. I sampled 565 amphibians commercially exported from Madagascar for the presence of Bd upon importation to the USA, both to assist early detection efforts and demonstrate the conservation potential of wildlife trade disease surveillance. Bd was detected in three animals via quantitative PCR: a single Heterixalus alboguttatus, Heterixalus betsileo, and Scaphiophryne spinosa. This is the first time Bd has been confirmed in amphibians from Madagascar and presents an urgent call to action. Our early identification of pathogen presence prior to widespread infection provides the necessary tools and encouragement to catalyze a swift, targeted response to isolate and eradicate Bd from Madagascar. If implemented before establishment occurs, an otherwise likely catastrophic decline in amphibian biodiversity may be prevented

Mischaracterizing wildlife trade and its impacts may mislead policy processes

Overexploitation is a key driver of biodiversity loss but the relationship between the use and trade of species and conservation outcomes is not always straightforward. Accurately characterizing wildlife trade and understanding the impact it has on wildlife populations are therefore critical to evaluating the potential threat trade poses to species and informing local to international policy responses. However, a review of recent research that uses wildlife and trade-related databases to investigate these topics highlights three relatively widespread issues: (1) mischaracterization of the threat that trade poses to certain species or groups, (2) misinterpretation of wildlife trade data (and illegal trade data in particular), resulting in the mischaracterization of trade, and (3) misrepresentation of international policy processes and instruments. This is concerning because these studies may unwittingly misinform policymaking to the detriment of conservation, for example by undermining positive outcomes for species and people along wildlife supply chains. Moreover, these issues demonstrate flaws in the peer-review process. As wildlife trade articles published in peer-reviewed journals can be highly influential, we propose ways for authors, journal editors, database managers, and policymakers to identify, understand, and avoid these issues as we all work towards more sustainable futures

Response to comment on 'Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity'

Lambert et al. question our retrospective and holistic epidemiological assessment of the role of chytridiomycosis in amphibian declines. Their alternative assessment is narrow and provides an incomplete evaluation of evidence. Adopting this approach limits understanding of infectious disease impacts and hampers conservation efforts. We reaffirm that our study provides unambiguous evidence that chytridiomycosis has affected at least 501 amphibian species

Using decision analysis to support proactive management of emerging infectious wildlife diseases

Despite calls for improved responses to emerging infectious diseases in wildlife, management is seldom considered until a disease has been detected in affected populations. Reactive approaches may limit the potential for control and increase total response costs. An alternative, proactive management framework can identify immediate actions that reduce future impacts even before a disease is detected, and plan subsequent actions that are conditional on disease emergence. We identify four main obstacles to developing proactive management strategies for the newly discovered salamander pathogen Batrachochytrium salamandrivorans (Bsal). Given that uncertainty is a hallmark of wildlife disease management and that associated decisions are often complicated by multiple competing objectives, we advocate using decision analysis to create and evaluate trade-offs between proactive (pre-emergence) and reactive (post-emergence) management options. Policy makers and natural resource agency personnel can apply principles from decision analysis to improve strategies for countering emerging infectious diseases

An Activity–Rotation Relationship and Kinematic Analysis of Nearby Mid-to-Late-Type M Dwarfs

Using spectroscopic observations and photometric light curves of 238 nearby M dwarfs from the MEarth exoplanet transit survey, we examine the relationships between magnetic activity (quantified by Hα emission), rotation period, and stellar age. Previous attempts to investigate the relationship between magnetic activity and rotation in these stars were hampered by the limited number of M dwarfs with measured rotation periods (and the fact that v sin i measurements probe only rapid rotation). However, the photometric data from MEarth allows us to probe a wide range of rotation periods for hundreds of M dwarf stars (from shorter than one to longer than 100 days). Over all M spectral types that we probe, we find that the presence of magnetic activity is tied to rotation, including for late-type, fully convective M dwarfs. We also find evidence that the fraction of late-type M dwarfs that are active may be higher at longer rotation periods compared to their early-type counterparts, with several active, late-type, slowly rotating stars present in our sample. Additionally, we find that all M dwarfs with rotation periods shorter than 26 days (early-type; M1–M4) and 86 days (late-type; M5–M8) are magnetically active. This potential mismatch suggests that the physical mechanisms that connect stellar rotation to chromospheric heating may be different in fully convective stars. A kinematic analysis suggests that the magnetically active, rapidly rotating stars are consistent with a kinematically young population, while slow-rotators are less active or inactive and appear to belong to an older, dynamically heated stellar population

Use of micro CHP plants to support the local operation of electric heat pumps

Fig. 1. Global distribution of chytridiomycosis-associated amphibian species declines. Bar plots indicate the number (N) of declined species, grouped by continental area and classified by decline severity. Brazilian species are plotted separately from all other South American species (South America W); Mesoamerica includes Central America, Mexico, and the Caribbean Islands; and Oceania includes Australia and New Zealand. No declines have been reported in Asia. n, total number of declines by region. [Photo credits (clockwise from top left): Anaxyrus boreas, C. Brown, U.S. Geological Survey; Atelopus varius, B.G.; Salamandra salamandra, D. Descouens, Wikimedia Commons; Telmatobius sanborni, I.D.l.R; Cycloramphus boraceiensis, L.F.T.; Cardioglossa melanogaster, M.H.; and Pseudophryne corroboree, C. Doughty

Ecology: Stop Madagascar's toad invasion now

[Extract]Asian common toads (Duttaphrynus melanostictus) have begun to invade Madagascar, threatening the biodiversity of its unique fauna. Time is short, so we are issuing an urgent call to the conservation community and to governments to prevent an ecological disaster.\u

Pathways of amphibian chytrid fungus dispersal: global biosecurity and conservation implications

Spread of the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) poses the greatest emerging threat to global amphibian biodiversity. Bd's low host species specificity allows the disease it causes — chytridiomycosis — to affect many of the 7,000 species of amphibians and drive population declines and extinctions worldwide. Although discovered nearly 20 years ago, the origin of Bd and catalyst of the seemingly recent global disease event remain obscure. Today, this international epizootic continues to advance virtually uncontrolled. Modes of global Bd dispersal are not well understood, hampering the development and implementation of targeted biosecurity efforts to reduce spread. Bd is an aquatic pathogen most often associated with amphibian species that live in or near permanent bodies of water. It can neither survive desiccation nor extended exposure to elevated temperatures, but few environmental barriers appear to impede the spread of Bd. It has crossed oceans, infected terrestrial direct-developing amphibians that do not live in water, and been introduced to every continent (except Antarctica). Although low densities of Bd have been found in the environment outside of a host, amphibians consistently carry the highest pathogen loads and appear to be the primary host organisms that vector Bd. The international trade in live amphibians transports millions of animals annually. Most previous research has focused on this anthropogenic activity as the primary pathway of global Bd dispersal. This is a sensible assumption—the highly visible movement of Bd hosts together with the lack of disease control suggests that Bd-positive animals are commonly transported in these shipments. Unfortunately, all previous surveillance efforts that aimed to demonstrate this phenomenon were performed in animal markets in Bd-positive countries where contamination from domestic Bd could not be excluded as a potential source of infection. Upon close examination of global Bd distribution patterns, I found that regions of Bd presence do not exclusively overlap those of notable amphibian trade, raising questions as to the sources and pathways involved in pathogen dispersal. For instance, despite the absence of commercial amphibian importation to the islands of Dominica and Montserrat, chytridiomycosis drove the near-extinction of the Mountain Chicken frog (Leptodactylus fallax). Likewise, chytridiomycosis emerged in remote wilderness areas in Central America and Australia, again with no clear link to amphibian trade activity. Thus, despite the similar absence of commercial amphibian importation in Madagascar, it seems unlikely that this alone prevents the introduction of Bd. Meanwhile despite intensive field and market surveillance in Hong Kong — a global amphibian trade hub — Bd has neither been detected nor have amphibian declines been observed. Therefore, I hypothesized that additional pathways of Bd dispersal exist in the absence of commercial amphibian trade that can also transport this pathogen global distances. The aims of this study were to characterize the likelihood and consequence of multiple pathways of amphibian pathogen dispersal, help identify Bd mitigation targets likely to reduce the greatest amount of international disease spread, and suggest potential mitigation activities. I investigated the presence of five potential Bd dispersal pathways that might concurrently contribute towards contemporary global pathogen spread. Because Bd is present both in areas heavily affected by human activity and remote wilderness areas, I explored avenues of dispersal that involved anthropogenic-assisted spread, spread by wildlife, and spread by environmental phenomena. The five pathways I evaluated include: 1. Commercial amphibian trade, 2. Amphibian hitchhikers (unintentional amphibian trade), 3. Atmospheric transport events, 4. Amphibian locomotion, and 5. Fomites. Through my series of studies, I examined high-risk environments where each pathway was most likely to be detected if an active avenue of Bd spread existed. My results demonstrate that global Bd dispersal does involve multiple simultaneous pathways, with all five pathways having been successfully observed, with each varying in frequency and quantity of pathogen spread. At a field site in Cusuco National Park in Honduras, I discovered evidence for both atmospheric and terrestrial dispersal of Bd, previously undocumented for this aquatic pathogen. Bd was detected in rainwater in 5% of the storm events sampled and was present at a low density (1 Bd zoospore/L). Because Bd viability cannot be confirmed from the qPCR test results alone, it remains uncertain whether Bd-positive rainwater is infectious to amphibians. Even in the absence of infection, aerial dispersal can produce Bdpositive field samples and may occasionally be responsible for enigmatic isolated records of Bd detection. Another way that Bd spreads in the absence of human assistance, and in higher densities, is through amphibian locomotion. Although infected animals spread Bd to one another in captive laboratory setting, the likelihood of this pathway was not previously measured in the wild in the natural environment. Because some frogs develop high infection loads as they undergo metamorphosis from tadpole to froglet, I studied whether seasonal mass emergences from aquatic to terrestrial habitats commonly transports Bd across habitat boundaries. In a sample of 52 recently emerged frogs, I detected the presence of Bd on 76.1% (35/46) of terrestrial vegetation surfaces where a Bd-positive frog had been resting. As previously mentioned, the viability of Bd cannot be discerned from qPCR results alone, but the cool air temperature, closed canopy, and high humidity of this cloud forest provides favourable conditions for protection from desiccation and extended Bd persistence. Furthermore, the average Bd zoospore equivalent loads that I detected on affected leaf surfaces (average = 40.48 and range was 0.12–1,040.45) compared to those measured in adjacent Bd-positive river water samples (average was 0.23 and range was 0.03–0.57) show that exposure to affected foliage may pose a greater threat of Bd transmission to terrestrial amphibians than would a comparable period of exposure to nearby river water. I performed several studies to measure and evaluate the presence of Bd in amphibians commercially imported into the United States. Overall, I detected a moderately high prevalence of Bd in amphibians sampled immediately upon importation in the USA, validating prior studies on trade being a major route of spread. Bd was detected in 11.7% of 265 exotic pet trade amphibians from Hong Kong, 58.8% of 102 food trade bullfrogs from the Dominican Republic, 0/35 food trade bullfrogs sampled from Taiwan, and 0.5% of 565 exotic pet trade amphibians from Madagascar. In addition, this trade activity also caused the spread of Bd-contaminated shipping materials; e.g. 59.0% (62/105) of cardboard boxes carrying bullfrogs from the Dominican Republic and 5/8 bags of water carrying amphibians from Hong Kong tested positive for Bd. Despite previous lack of detection, my surveillance data confirmed the presence of Bd in material exported from Madagascar and Hong Kong, and for the first time suggested the pathogen might already have been introduced to those countries' wild amphibian populations. In response, I designed and performed targeted rapid response investigations to determine whether Bd was present and identify potential introduction pathways. In 2013, I detected Bd in Hong Kong in Asian bullfrogs (Hoplobatrachus chinensis) sampled upon importation (8/26), in African clawed frogs (Xenopus laevis) at domestic pet stores (3/60) and in native free-ranging amphibians (2/268). In Hong Kong, I observed trade behaviors that are accompanied by a high risk of pathogen spillover - most notably the release of non-native animals into local amphibian habitats. In contrast, I did not detect the presence of Bd in 508 amphibians and 68 water filter samples tested in Madagascar, although this does not preclude its presence in very limited distributions and/or very low prevalence. I inspected the wildlife trade facility from where my previous Bd-positive frogs originated and did not observe any obvious opportunities for non- Malagasy Bd contamination –animals from other countries do not enter the facility. Despite the absence of commercial amphibian importation, I identified an incursion of Asian toads likely introduced as hitchhikers inside ocean shipping containers. It remains unknown whether these toads have recently introduced foreign pathogens to Madagascar, but this invasion clearly demonstrates how the absence of intentional amphibian trade does not entirely reduce risk of exposure to Bd. Data produced by both rapid response field studies suggests that a virulent strain of Bd (e.g. Bd-GPL) is not yet established in either Hong Kong or Madagascar, despite evidence of Bd introduction pathways, presence of suitable climatic refugia, and an abundance of susceptible host species. Therefore, I believe it remains plausible to prevent Bd-associated declines within these countries if appropriately targeted biosecurity measures are implemented. Applying all information developed and collated to characterize the five potential Bd dispersal pathways, I then performed a risk matrix analysis to compare the amount of risk associated with each in order to better assist management decision-making. Each pathway was assigned a numerical score reflecting the combined likelihood of Bd spread and the severity of the outcome. These values represent the estimated relative contributions of each pathway to the global emergence of Bd. The international trade in live amphibians creates the most consistent and predictable opportunities for long-distance spread of viable and potentially infectious Bd and was ranked the highest risk pathway. My data shows that in the absence of this activity, Bd appears unlikely to frequently cross geographic and biotic boundaries to its survival, and that the emergence of this pandemic is likely due to human-assisted trade. I conclude that biosecurity regulations to reduce the amount of Bd dispersed by the international wildlife trade is the most imperative action to slow the current global spread of Bd and to reduce the likelihood of additional disease emergences. Although methods to control the trade-driven spread of Bd were recommended by the World Organisation of Animal Health nearly five years ago, few countries have formally adopted these practices or require any actions specifically to reduce Bd introduction. My study confirms that the trade in live amphibians is an engine of global pathogen pollution unrivalled by other identified pathways of Bd dispersal and reinforces the need for disease management actions at least to the level commonly offered to livestock. Moving forward, proactive disease surveillance and biosecurity measures must target the international wildlife trade if we are to protect global biodiversity from novel emerging infectious diseases of wildlife

One of two crates of amphibians sampled for <i>Batrachochytrium dendrobatidis</i> upon arrival from Madagascar.

<p>Amphibians were shipped sealed in wooden crates, insulated with 1/4″ Styrofoam, and packed in plastic containers filled with damp sphagnum moss and leaves.</p