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1.  Augmenting the Post-Transplantation Growth and Survivorship of Juvenile Scleractinian Corals via Nutritional Enhancement 
PLoS ONE  2014;9(6):e98529.
Size-dependant mortality influences the recolonization success of juvenile corals transplanted for reef restoration and assisting juvenile corals attain a refuge size would thus improve post-transplantation survivorship. To explore colony size augmentation strategies, recruits of the scleractinian coral Pocillopora damicornis were fed with live Artemia salina nauplii twice a week for 24 weeks in an ex situ coral nursery. Fed recruits grew significantly faster than unfed ones, with corals in the 3600, 1800, 600 and 0 (control) nauplii/L groups exhibiting volumetric growth rates of 10.65±1.46, 4.69±0.9, 3.64±0.55 and 1.18±0.37 mm3/week, respectively. Corals supplied with the highest density of nauplii increased their ecological volume by more than 74 times their initial size, achieving a mean final volume of 248.38±33.44 mm3. The benefits of feeding were apparent even after transplantation to the reef. The corals in the 3600, 1800, 600 and 0 nauplii/L groups grew to final sizes of 4875±260 mm3, 2036±627 mm3, 1066±70 mm3 and 512±116 mm3, respectively. The fed corals had significantly higher survival rates than the unfed ones after transplantation (63%, 59%, 56% and 38% for the 3600, 1800, 600 and 0 nauplii/L treatments respectively). Additionally, cost-effectiveness analysis revealed that the costs per unit volumetric growth were drastically reduced with increasing feed densities. Corals fed with the highest density of nauplii were the most cost-effective (US$0.02/mm3), and were more than 12 times cheaper than the controls. This study demonstrated that nutrition enhancement can augment coral growth and post-transplantation survival, and is a biologically and economically viable option that can be used to supplement existing coral mariculture procedures and enhance reef restoration outcomes.
doi:10.1371/journal.pone.0098529
PMCID: PMC4045716  PMID: 24896085
2.  Impact of Plant Cover on Fitness and Behavioural Traits of Captive Red-Eyed Tree Frogs (Agalychnis callidryas) 
PLoS ONE  2014;9(4):e95207.
Despite the importance of ex situ conservation programmes as highlighted in the Amphibian Conservation Action Plan, there are few empirical studies that examine the influence of captive conditions on the fitness of amphibians, even for basic components of enclosure design such as cover provision. Maintaining the fitness of captive amphibian populations is essential to the success of ex situ conservation projects. Here we examined the impact of plant cover on measures of fitness and behaviour in captive red-eyed tree frogs (Agalychnis callidryas). We found significant effects of plant provision on body size, growth rates and cutaneous bacterial communities that together demonstrate a compelling fitness benefit from cover provision. We also demonstrate a strong behavioural preference for planted rather than non-planted areas. We also assessed the impact of plant provision on the abiotic environment in the enclosure as a potential driver of these behavioural and fitness effects. Together this data provides valuable information regarding enclosure design for a non-model amphibian species and has implications for amphibian populations maintained in captivity for conservation breeding programmes and research.
doi:10.1371/journal.pone.0095207
PMCID: PMC3989275  PMID: 24740289
3.  Evaluating Group Housing Strategies for the Ex-Situ Conservation of Harlequin Frogs (Atelopus spp.) Using Behavioral and Physiological Indicators 
PLoS ONE  2014;9(2):e90218.
We have established ex situ assurance colonies of two endangered Panamanian harlequin frogs, Atelopus certus and Atelopus glyphus, but observed that males fought with each other when housed as a group. Housing frogs individually eliminated this problem, but created space constraints. To evaluate the potential stress effects from aggressive interactions when grouping frogs, we housed male frogs in replicated groups of one, two, and eight. We measured aggressive behavioral interactions and fecal glucocorticoid metabolite (GC) concentrations as indicators of stress in each tank. In both small and large groups, frogs initially interacted aggressively, but aggressive interactions and fecal GCs declined significantly after the first 2 weeks of being housed together, reaching the lowest levels by week 4. We conclude that aggressive interactions in same-sex groups of captive Atelopus may initially cause stress, but the frogs become habituated within a few weeks and they can safely be housed in same-sex groups for longer periods of time.
doi:10.1371/journal.pone.0090218
PMCID: PMC3934986  PMID: 24587290
4.  Stability of Microbiota Facilitated by Host Immune Regulation: Informing Probiotic Strategies to Manage Amphibian Disease 
PLoS ONE  2014;9(1):e87101.
Microbial communities can augment host immune responses and probiotic therapies are under development to prevent or treat diseases of humans, crops, livestock, and wildlife including an emerging fungal disease of amphibians, chytridiomycosis. However, little is known about the stability of host-associated microbiota, or how the microbiota is structured by innate immune factors including antimicrobial peptides (AMPs) abundant in the skin secretions of many amphibians. Thus, conservation medicine including therapies targeting the skin will benefit from investigations of amphibian microbial ecology that provide a model for vertebrate host-symbiont interactions on mucosal surfaces. Here, we tested whether the cutaneous microbiota of Panamanian rocket frogs, Colostethus panamansis, was resistant to colonization or altered by treatment. Under semi-natural outdoor mesocosm conditions in Panama, we exposed frogs to one of three treatments including: (1) probiotic - the potentially beneficial bacterium Lysinibacillus fusiformis, (2) transplant – skin washes from the chytridiomycosis-resistant glass frog Espadarana prosoblepon, and (3) control – sterile water. Microbial assemblages were analyzed by a culture-independent T-RFLP analysis. We found that skin microbiota of C. panamansis was resistant to colonization and did not differ among treatments, but shifted through time in the mesocosms. We describe regulation of host AMPs that may function to maintain microbial community stability. Colonization resistance was metabolically costly and microbe-treated frogs lost 7–12% of body mass. The discovery of strong colonization resistance of skin microbiota suggests a well-regulated, rather than dynamic, host-symbiont relationship, and suggests that probiotic therapies aiming to enhance host immunity may require an approach that circumvents host mechanisms maintaining equilibrium in microbial communities.
doi:10.1371/journal.pone.0087101
PMCID: PMC3906108  PMID: 24489847
5.  Invasive Crayfish Threaten the Development of Submerged Macrophytes in Lake Restoration 
PLoS ONE  2013;8(10):e78579.
Submerged macrophytes enhance water transparency and aquatic biodiversity in shallow water ecosystems. Therefore, the return of submerged macrophytes is the target of many lake restoration projects. However, at present, north-western European aquatic ecosystems are increasingly invaded by omnivorous exotic crayfish. We hypothesize that invasive crayfish pose a novel constraint on the regeneration of submerged macrophytes in restored lakes and may jeopardize restoration efforts. We experimentally investigated whether the invasive crayfish (Procambarus clarkii Girard) affects submerged macrophyte development in a Dutch peat lake where these crayfish are expanding rapidly. Seemingly favourable abiotic conditions for macrophyte growth existed in two 0.5 ha lake enclosures, which provided shelter and reduced turbidity, and in one lake enclosure iron was added to reduce internal nutrient loading, but macrophytes did not emerge. We transplanted three submerged macrophyte species in a full factorial exclosure experiment, where we separated the effect of crayfish from large vertebrates using different mesh sizes combined with a caging treatment stocked with crayfish only. The three transplanted macrophytes grew rapidly when protected from grazing in both lake enclosures, demonstrating that abiotic conditions for growth were suitable. Crayfish strongly reduced biomass and survival of all three macrophyte species while waterfowl and fish had no additive effects. Gut contents showed that crayfish were mostly carnivorous, but also consumed macrophytes. We show that P. clarkii strongly inhibit macrophyte development once favourable abiotic conditions for macrophyte growth are restored. Therefore, expansion of invasive crayfish poses a novel threat to the restoration of shallow water bodies in north-western Europe. Prevention of introduction and spread of crayfish is urgent, as management of invasive crayfish populations is very difficult.
doi:10.1371/journal.pone.0078579
PMCID: PMC3813481  PMID: 24205271
6.  Simulated Birdwatchers’ Playback Affects the Behavior of Two Tropical Birds 
PLoS ONE  2013;8(10):e77902.
Although recreational birdwatchers may benefit conservation by generating interest in birds, they may also have negative effects. One such potentially negative impact is the widespread use of recorded vocalizations, or “playback,” to attract birds of interest, including range-restricted and threatened species. Although playback has been widely used to test hypotheses about the evolution of behavior, no peer-reviewed study has examined the impacts of playback in a birdwatching context on avian behavior. We studied the effects of simulated birdwatchers’ playback on the vocal behavior of Plain-tailed Wrens Thryothorus euophrys and Rufous Antpittas Grallaria rufula in Ecuador. Study species’ vocal behavior was monitored for an hour after playing either a single bout of five minutes of song or a control treatment of background noise. We also studied the effects of daily five minute playback on five groups of wrens over 20 days. In single bout experiments, antpittas made more vocalizations of all types, except for trills, after playback compared to controls. Wrens sang more duets after playback, but did not produce more contact calls. In repeated playback experiments, wren responses were strong at first, but hardly detectable by day 12. During the study, one study group built a nest, apparently unperturbed, near a playback site. The playback-induced habituation and changes in vocal behavior we observed suggest that scientists should consider birdwatching activity when selecting research sites so that results are not biased by birdwatchers’ playback. Increased vocalizations after playback could be interpreted as a negative effect of playback if birds expend energy, become stressed, or divert time from other activities. In contrast, the habituation we documented suggests that frequent, regular birdwatchers’ playback may have minor effects on wren behavior.
doi:10.1371/journal.pone.0077902
PMCID: PMC3797570  PMID: 24147094
7.  Variation in Thermal Performance of a Widespread Pathogen, the Amphibian Chytrid Fungus Batrachochytrium dendrobatidis 
PLoS ONE  2013;8(9):e73830.
Rates of growth and reproduction of the pathogens that cause emerging infectious diseases can be affected by local environmental conditions; these conditions can thus influence the strength and nature of disease outbreaks. An understanding of these relationships is important for understanding disease ecology and developing mitigation strategies. Widespread emergence of the fungal disease chytridiomycosis has had devastating effects on amphibian populations. The causative pathogen, Batrachochytriumdendrobatidis (Bd), is sensitive to temperature, but its thermal tolerances are not well studied. We examined the thermal responses of three Bd isolates collected across a latitudinal gradient in eastern Australia. Temperature affected all aspects of Bd growth and reproduction that we measured, in ways that often differed among Bd isolates. Aspects of growth, reproduction, and their relationships to temperature that differed among isolates included upper thermal maxima for growth (26, 27, or 28°C, depending on the isolate), relationships between zoospore production and temperature, and zoospore activity and temperature. Two isolates decreased zoospore production as temperature increased, whereas the third isolate was less fecund overall, but did not show a strong response to temperature until reaching the upper limit of its thermal tolerance. Our results show differentiation in life-history traits among isolates within Australia, suggesting that the pathogen may exhibit local adaptation. An understanding of how environmental temperatures can limit pathogens by constraining fitness will enhance our ability to assess pathogen dynamics in the field, model pathogen spread, and conduct realistic experiments on host susceptibility and disease transmission.
doi:10.1371/journal.pone.0073830
PMCID: PMC3762749  PMID: 24023908
8.  Sight of a Predator Induces a Corticosterone Stress Response and Generates Fear in an Amphibian 
PLoS ONE  2013;8(8):e73564.
Amphibians, like other animals, generate corticosterone or cortisol glucocorticoid responses to stimuli perceived to be threatening. It is generally assumed that the corticosterone response of animals to capture and handling reflects the corticosterone response to stimuli such as the sight of a predator that are thought to be natural stressors. Fijian ground frogs (Platymantisvitiana) are preyed upon by the introduced cane toads (Rhinellamarina), and we used ground frogs to test the hypothesis that the sight of a predator will induce a corticosterone stress response in an amphibian. Urinary corticosterone metabolite concentrations increased in male ground frogs exposed to the sight of a toad for 1, 3 or 6 h, whereas corticosterone did not change in frogs exposed to another male ground frog, a ball, or when no stimulus was present in the test compartment. The frogs exposed to a toad initially moved towards the stimulus then moved away, whereas frogs exposed to another frog moved towards the test frog and remained closer to the frog than at the start of the test. Tonic immobility (TI) was measured as an index of fearfulness immediately after the test exposure of the frogs to a stimulus. The duration of TI was longer in frogs exposed to a toad than to another frog or to a ball. The results provide novel evidence that the sight of a predator can induce a corticosterone response and lead to increased fearfulness in amphibians. In addition, they show that endemic frogs can recognise an introduced predator as a threat.
doi:10.1371/journal.pone.0073564
PMCID: PMC3757005  PMID: 24009756
9.  Habitat Use by Fishes in Coral Reefs, Seagrass Beds and Mangrove Habitats in the Philippines 
PLoS ONE  2013;8(8):e65735.
Understanding the interconnectivity of organisms among different habitats is a key requirement for generating effective management plans in coastal ecosystems, particularly when determining component habitat structures in marine protected areas. To elucidate the patterns of habitat use by fishes among coral, seagrass, and mangrove habitats, and between natural and transplanted mangroves, visual censuses were conducted semiannually at two sites in the Philippines during September and March 2010–2012. In total, 265 species and 15,930 individuals were recorded. Species richness and abundance of fishes were significantly higher in coral reefs (234 species, 12,306 individuals) than in seagrass (38 species, 1,198 individuals) and mangrove (47 species, 2,426 individuals) habitats. Similarity tests revealed a highly significant difference among the three habitats. Fishes exhibited two different strategies for habitat use, inhabiting either a single (85.6% of recorded species) or several habitats (14.4%). Some fish that utilized multiple habitats, such as Lutjanus monostigma and Parupeneus barberinus, showed possible ontogenetic habitat shifts from mangroves and/or seagrass habitats to coral reefs. Moreover, over 20% of commercial fish species used multiple habitats, highlighting the importance of including different habitat types within marine protected areas to achieve efficient and effective resource management. Neither species richness nor abundance of fishes significantly differed between natural and transplanted mangroves. In addition, 14 fish species were recorded in a 20-year-old transplanted mangrove area, and over 90% of these species used multiple habitats, further demonstrating the key role of transplanted mangroves as a reef fish habitat in this region.
doi:10.1371/journal.pone.0065735
PMCID: PMC3748118  PMID: 23976940
10.  The Relationship between Diver Experience Levels and Perceptions of Attractiveness of Artificial Reefs - Examination of a Potential Management Tool 
PLoS ONE  2013;8(7):e68899.
Artificial reefs are increasingly used worldwide as a method for managing recreational diving since they have the potential to satisfy both conservation goals and economic interests. In order to help maximize their utility, further information is needed to drive the design of stimulating resources for scuba divers. We used a questionnaire survey to explore divers’ perceptions of artificial reefs in Barbados. In addition, we examined reef resource substitution behaviour among scuba divers. Divers expressed a clear preference for large shipwrecks or sunken vessels that provided a themed diving experience. Motives for diving on artificial reefs were varied, but were dominated by the chance of viewing concentrated marine life, increased photographic opportunities, and the guarantee of a ‘good dive’. Satisfaction with artificial reef diving was high amongst novices and declined with increasing experience. Experienced divers had an overwhelming preference for natural reefs. As a management strategy, our results emphasize the capacity of well designed artificial reefs to contribute towards the management of coral reef diving sites and highlight a number of important areas for future research. Suggested work should validate the present findings in different marine tourism settings and ascertain support of artificial reefs in relationship to level of diver specialization.
doi:10.1371/journal.pone.0068899
PMCID: PMC3720904  PMID: 23894372
11.  The Population Decline and Extinction of Darwin’s Frogs 
PLoS ONE  2013;8(6):e66957.
Darwin’s frogs (Rhinoderma darwinii and R. rufum) are two species of mouth-brooding frogs from Chile and Argentina. Here, we present evidence on the extent of declines, current distribution and conservation status of Rhinoderma spp.; including information on abundance, habitat and threats to extant Darwin’s frog populations. All known archived Rhinoderma specimens were examined in museums in North America, Europe and South America. Extensive surveys were carried out throughout the historical ranges of R. rufum and R. darwinii from 2008 to 2012. Literature review and location data of 2,244 archived specimens were used to develop historical distribution maps for Rhinoderma spp. Based on records of sightings, optimal linear estimation was used to estimate whether R. rufum can be considered extinct. No extant R. rufum was found and our modelling inferred that this species became extinct in 1982 (95% CI, 1980–2000). Rhinoderma darwinii was found in 36 sites. All populations were within native forest and abundance was highest in Chiloé Island, when compared with Coast, Andes and South populations. Estimated population size and density (five populations) averaged 33.2 frogs/population (range, 10.2–56.3) and 14.9 frogs/100 m2 (range, 5.3–74.1), respectively. Our results provide further evidence that R. rufum is extinct and indicate that R. darwinii has declined to a much greater degree than previously recognised. Although this species can still be found across a large part of its historical range, remaining populations are small and severely fragmented. Conservation efforts for R. darwinii should be stepped up and the species re-classified as Endangered.
doi:10.1371/journal.pone.0066957
PMCID: PMC3680453  PMID: 23776705
12.  Preliminary Genetic Analysis Supports Cave Populations as Targets for Conservation in the Endemic Endangered Puerto Rican Boa (Boidae: Epicrates inornatus) 
PLoS ONE  2013;8(5):e63899.
The endemic Puerto Rican boa (Epicrates inornatus) has spent 42 years on the Endangered Species List with little evidence for recovery. One significant impediment to effective conservation planning has been a lack of knowledge of the distribution of genetic variability in the species. It has previously been suggested that boas might best be protected around caves that harbor large populations of bats. Prior study has found Puerto Rican boas at relatively high densities in and around bat caves, which they use both to feed and seek shelter. However, it is unknown whether these behaviorally distinctive populations represent a distinct evolutionary lineage, or (conversely) whether caves harbor representative genetic diversity for the species across the island. We provide the first genetic study of the Puerto Rican boa, and we examine and compare genetic diversity and divergence among two cave populations and two surface populations of boas. We find three haplogroups and an apparent lack of phylogeographic structure across the island. In addition, we find that the two cave populations appear no less diverse than the two surface populations, and harbor multiple mtDNA lineages. We discuss the conservation implications of these findings, including a call for the immediate protection of the remaining cave-associated populations of boas.
doi:10.1371/journal.pone.0063899
PMCID: PMC3655012  PMID: 23691110
13.  Prevalence of Batrachochytrium dendrobatidis in Xenopus Collected in Africa (1871–2000) and in California (2001–2010) 
PLoS ONE  2013;8(5):e63791.
International trade of the invasive South African clawed frog (Xenopus laevis), a subclinical carrier of the fungal pathogen Batrachochytrium dendrobatis (Bd) has been proposed as a major means of introduction of Bd into naïve, susceptible amphibian populations. The historical presence of Bd in the indigenous African population of Xenopus is well documented. However, there are no reports documenting the presence of Bd in wild Xenopus populations in the US, particularly in California where introduced populations are well-established after intentional or accidental release. In this report, a survey was conducted on 178 archived specimens of 6 species of Xenopus collected in Africa from 1871–2000 and on 23 archived specimens (all wild-caught Xenopus laevis) collected in California, USA between 2001 and 2010. The overall prevalence rate of Bd in the tested Xenopus was 2.8%. The earliest positive specimen was X. borealis collected in Kenya in 1934. The overall prevalence of Bd in the X. laevis collected in California was 13% with 2 positive specimens from 2001 and one positive specimen from 2003. The positive Xenopus (3/23) collected in California were collected in 2001 (2/3) and 2003 (1/3). These data document the presence of Bd-infected wild Xenopus laevis in California. The findings reported here support the prevailing hypothesis that Bd was present as a stable, endemic infection in Xenopus populations in Africa prior to their worldwide distribution likely via international live-amphibian trade.
doi:10.1371/journal.pone.0063791
PMCID: PMC3655066  PMID: 23691097
14.  Re-Isolating Batrachochytrium dendrobatidis from an Amphibian Host Increases Pathogenicity in a Subsequent Exposure 
PLoS ONE  2013;8(5):e61260.
Controlled exposure experiments can be very informative, however, they are based on the assumption that pathogens maintained on artificial media under long-term storage retain the infective and pathogenic properties of the reproducing pathogen as it occurs in a host. We observed that JEL284, an in vitro cultured and maintained isolate of Batrachochytrium dendrobatidis (Bd), was becoming less infectious with successive uses. We hypothesized that passing an isolate propagated on artificial media through an amphibian host would make the isolate more infectious and pathogenic in subsequent exposures. To test our hypothesis, we used two discreet steps, a reisolation step (step 1) and a comparative exposure step (step 2). In step 1, we exposed eastern spadefoot toads, Scaphiopus holbrooki, to JEL284 and JEL197, another isolate that had been maintained in vitro for over six years. We then re-isolated JEL284 only from a successful infection and named this new isolate JEL284FMBa. JEL197 did not infect any amphibians and, thus, did not proceed to step 2. In step 2, we compared infectivity and pathogenicity (mortality and survival time) of JEL284 and JEL284FMBa by exposing 54 naïve S. holbrooki to three treatments (JEL284, JEL284FMBa, and negative control) with 18 individuals per group. We found that JEL284FMBa caused higher mortality and decreased survival time in infected individuals when compared to JEL284 and negative controls. Thus, our data show that pathogenicity of Bd can decrease when cultured successively in media only and can be partially restored by passage through an amphibian host. Therefore, we have demonstrated that pathogenicity shifts can occur rapidly in this pathogen. Given the potential for shifts in pathogenicity demonstrated here, we suspect Bd to have similar potential in natural populations. We suggest that, when possible, the use of freshly isolated or cryopreserved Bd would improve the quality of controlled exposure experiments using this pathogen.
doi:10.1371/journal.pone.0061260
PMCID: PMC3646005  PMID: 23671564
15.  Predicting Environmental Suitability for a Rare and Threatened Species (Lao Newt, Laotriton laoensis) Using Validated Species Distribution Models 
PLoS ONE  2013;8(3):e59853.
The Lao newt (Laotriton laoensis) is a recently described species currently known only from northern Laos. Little is known about the species, but it is threatened as a result of overharvesting. We integrated field survey results with climate and altitude data to predict the geographic distribution of this species using the niche modeling program Maxent, and we validated these predictions by using interviews with local residents to confirm model predictions of presence and absence. The results of the validated Maxent models were then used to characterize the environmental conditions of areas predicted suitable for L. laoensis. Finally, we overlaid the resulting model with a map of current national protected areas in Laos to determine whether or not any land predicted to be suitable for this species is coincident with a national protected area. We found that both area under the curve (AUC) values and interview data provided strong support for the predictive power of these models, and we suggest that interview data could be used more widely in species distribution niche modeling. Our results further indicated that this species is mostly likely geographically restricted to high altitude regions (i.e., over 1,000 m elevation) in northern Laos and that only a minute fraction of suitable habitat is currently protected. This work thus emphasizes that increased protection efforts, including listing this species as endangered and the establishment of protected areas in the region predicted to be suitable for L. laoensis, are urgently needed.
doi:10.1371/journal.pone.0059853
PMCID: PMC3612071  PMID: 23555808
16.  Population Recovery following Decline in an Endangered Stream-Breeding Frog (Mixophyes fleayi) from Subtropical Australia 
PLoS ONE  2013;8(3):e58559.
Amphibians have undergone dramatic declines and extinctions worldwide. Prominent among these have been the stream-breeding frogs in the rainforests of eastern Australia. The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) has been postulated as the primary cause of these declines. We conducted a capture-mark-recapture study over a 7-year period on the endangered Fleay’s barred frog (Mixophyes fleayi) at two independent streams (30 km apart) in order to assess the stability of these populations. This species had undergone a severe decline across its narrow geographic range. Mark-recapture modelling showed that the number of individuals increased 3–10 fold along stream transects over this period. Frog detection probabilities were frequently above 50% but declined as the populations increased. Adult survival was important to overall population persistence in light of low recruitment events, suggesting that longevity may be a key factor in this recovery. One male and female were present in the capture record for >6 years. This study provides an unambiguous example of population recovery in the presence of Bd.
doi:10.1371/journal.pone.0058559
PMCID: PMC3596276  PMID: 23516509
17.  Prior Infection Does Not Improve Survival against the Amphibian Disease Chytridiomycosis 
PLoS ONE  2013;8(2):e56747.
Many amphibians have declined globally due to introduction of the pathogenic fungus Batrachochytrium dendrobatidis (Bd). Hundreds of species, many in well-protected habitats, remain as small populations at risk of extinction. Currently the only proven conservation strategy is to maintain species in captivity to be reintroduced at a later date. However, methods to abate the disease in the wild are urgently needed so that reintroduced and wild animals can survive in the presence of Bd. Vaccination has been widely suggested as a potential strategy to improve survival. We used captive-bred offspring of critically endangered booroolong frogs (Litoria booroolongensis) to test if vaccination in the form of prior infection improves survival following re exposure. We infected frogs with a local Bd isolate, cleared infection after 30 days (d) using itraconazole just prior to the onset of clinical signs, and then re-exposed animals to Bd at 110 d. We found prior exposure had no effect on survival or infection intensities, clearly showing that real infections do not stimulate a protective adaptive immune response in this species. This result supports recent studies suggesting Bd may evade or suppress host immune functions. Our results suggest vaccination is unlikely to be useful in mitigating chytridiomycosis. However, survival of some individuals from all experimental groups indicates existence of protective innate immunity. Understanding and promoting this innate resistance holds potential for enabling species recovery.
doi:10.1371/journal.pone.0056747
PMCID: PMC3579874  PMID: 23451076
18.  Host Identity Matters in the Amphibian-Batrachochytrium dendrobatidis System: Fine-Scale Patterns of Variation in Responses to a Multi-Host Pathogen 
PLoS ONE  2013;8(1):e54490.
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.
doi:10.1371/journal.pone.0054490
PMCID: PMC3554766  PMID: 23382904
19.  Assessing Patterns of Human-Wildlife Conflicts and Compensation around a Central Indian Protected Area 
PLoS ONE  2012;7(12):e50433.
Mitigating crop and livestock loss to wildlife and improving compensation distribution are important for conservation efforts in landscapes where people and wildlife co-occur outside protected areas. The lack of rigorously collected spatial data poses a challenge to management efforts to minimize loss and mitigate conflicts. We surveyed 735 households from 347 villages in a 5154 km2 area surrounding Kanha Tiger Reserve in India. We modeled self-reported household crop and livestock loss as a function of agricultural, demographic and environmental factors, and mitigation measures. We also modeled self-reported compensation received by households as a function of demographic factors, conflict type, reporting to authorities, and wildlife species involved. Seventy-three percent of households reported crop loss and 33% livestock loss in the previous year, but less than 8% reported human injury or death. Crop loss was associated with greater number of cropping months per year and proximity to the park. Livestock loss was associated with grazing animals inside the park and proximity to the park. Among mitigation measures only use of protective physical structures were associated with reduced livestock loss. Compensation distribution was more likely for tiger related incidents, and households reporting loss and located in the buffer. Average estimated probability of crop loss was 0.93 and livestock loss was 0.60 for surveyed households. Estimated crop and livestock loss and compensation distribution were higher for households located inside the buffer. Our approach modeled conflict data to aid managers in identifying potential conflict hotspots, influential factors, and spatially maps risk probability of crop and livestock loss. This approach could help focus allocation of conservation efforts and funds directed at conflict prevention and mitigation where high densities of people and wildlife co-occur.
doi:10.1371/journal.pone.0050433
PMCID: PMC3515612  PMID: 23227173
20.  Disease Risk in Temperate Amphibian Populations Is Higher at Closed-Canopy Sites 
PLoS ONE  2012;7(10):e48205.
Habitat loss and chytridiomycosis (a disease caused by the chytrid fungus Batrachochytrium dendrobatidis - Bd) are major drivers of amphibian declines worldwide. Habitat loss regulates host-pathogen interactions by altering biotic and abiotic factors directly linked to both host and pathogen fitness. Therefore, studies investigating the links between natural vegetation and chytridiomycosis require integrative approaches to control for the multitude of possible interactions of biological and environmental variables in spatial epidemiology. In this study, we quantified Bd infection dynamics across a gradient of natural vegetation and microclimates, looking for causal associations between vegetation cover, multiple microclimatic variables, and pathogen prevalence and infection intensity. To minimize the effects of host diversity in our analyses, we sampled amphibian populations in the Adirondack Mountains of New York State, a region with relatively high single-host dominance. We sampled permanent ponds for anurans, focusing on populations of the habitat generalist frog Lithobates clamitans, and recorded various biotic and abiotic factors that potentially affect host-pathogen interactions: natural vegetation, canopy density, water temperature, and host population and community attributes. We screened for important explanatory variables of Bd infections and used path analyses to statistically test for the strength of cascading effects linking vegetation cover, microclimate, and Bd parameters. We found that canopy density, natural vegetation, and daily average water temperature were the best predictors of Bd. High canopy density resulted in lower water temperature, which in turn predicted higher Bd prevalence and infection intensity. Our results confirm that microclimatic shifts arising from changes in natural vegetation play an important role in Bd spatial epidemiology, with areas of closed canopy favoring Bd. Given increasing rates of anthropogenic habitat modification and the resulting declines in temperate and tropical frogs, understanding how vegetation cover and disease interact is critical for predicting Bd spread and developing appropriate management tools for wild populations.
doi:10.1371/journal.pone.0048205
PMCID: PMC3485156  PMID: 23118953
21.  Surviving Chytridiomycosis: Differential Anti-Batrachochytrium dendrobatidis Activity in Bacterial Isolates from Three Lowland Species of Atelopus 
PLoS ONE  2012;7(9):e44832.
In the Neotropics, almost every species of the stream-dwelling harlequin toads (genus Atelopus) have experienced catastrophic declines. The persistence of lowland species of Atelopus could be explained by the lower growth rate of Batrachochytrium dendrobatidis (Bd) at temperatures above 25°C. We tested the complementary hypothesis that the toads' skin bacterial microbiota acts as a protective barrier against the pathogen, perhaps delaying or impeding the symptomatic phase of chytridiomycosis. We isolated 148 cultivable bacterial strains from three lowland Atelopus species and quantified the anti-Bd activity through antagonism assays. Twenty-six percent (38 strains representing 12 species) of the bacteria inhibited Bd growth and just two of them were shared among the toad species sampled in different localities. Interestingly, the strongest anti-Bd activity was measured in bacteria isolated from A. elegans, the only species that tested positive for the pathogen. The cutaneous bacterial microbiota is thus likely a fitness-enhancing trait that may (adaptation) or not (exaptation) have appeared because of natural selection mediated by chytridiomycosis. Our findings reveal bacterial strains for development of local probiotic treatments against chytridiomycosis and also shed light on the mechanisms behind the frog-bacteria-pathogen interaction.
doi:10.1371/journal.pone.0044832
PMCID: PMC3438167  PMID: 22970314
22.  Long-Term Field Data and Climate-Habitat Models Show That Orangutan Persistence Depends on Effective Forest Management and Greenhouse Gas Mitigation 
PLoS ONE  2012;7(9):e43846.
Background
Southeast Asian deforestation rates are among the world’s highest and threaten to drive many forest-dependent species to extinction. Climate change is expected to interact with deforestation to amplify this risk. Here we examine whether regional incentives for sustainable forest management will be effective in improving threatened mammal conservation, in isolation and when combined with global climate change mitigation.
Methodology/Principal Findings
Using a long time-series of orangutan nest counts for Sabah (2000–10), Malaysian Borneo, we evaluated the effect of sustainable forest management and climate change scenarios, and their interaction, on orangutan spatial abundance patterns. By linking dynamic land-cover and downscaled global climate model projections, we determine the relative influence of these factors on orangutan spatial abundance and use the resulting statistical models to identify habitat crucial for their long-term conservation. We show that land-cover change the degradation of primary forest had the greatest influence on orangutan population size. Anticipated climate change was predicted to cause reductions in abundance in currently occupied populations due to decreased habitat suitability, but also to promote population growth in western Sabah by increasing the suitability of presently unoccupied regions.
Conclusions/Significance
We find strong quantitative support for the Sabah government’s proposal to implement sustainable forest management in all its forest reserves during the current decade; failure to do so could result in a 40 to 80 per cent regional decline in orangutan abundance by 2100. The Sabah orangutan is just one (albeit iconic) example of a forest-dependent species that stands to benefit from sustainable forest management, which promotes conservation of existing forests.
doi:10.1371/journal.pone.0043846
PMCID: PMC3436794  PMID: 22970145
23.  Rediscovery of Leptoxis compacta (Anthony, 1854) (Gastropoda: Cerithioidea: Pleuroceridae) 
PLoS ONE  2012;7(8):e42499.
The Mobile River Basin is a hotspot of molluscan endemism, but anthropogenic activities have caused at least 47 molluscan extinctions, 37 of which were gastropods, in the last century. Nine of these suspected extinctions were in the freshwater gastropod genus Leptoxis (Cerithioidea: Pleuroceridae). Leptoxis compacta, a Cahaba River endemic, has not been collected for >70 years and was formally declared extinct in 2000. Such gastropod extinctions underscore the imperilment of freshwater resources and the current biodiversity crisis in the Mobile River Basin. During a May 2011 gastropod survey of the Cahaba River in central Alabama, USA, L. compacta was rediscovered. The identification of snails collected was confirmed through conchological comparisons to the L. compacta lectotype, museum records, and radulae morphology of historically collected L. compacta. Through observations of L. compacta in captivity, we document for the first time that the species lays eggs in short, single lines. Leptoxis compacta is restricted to a single location in the Cahaba River, and is highly susceptible to a single catastrophic extinction event. As such, the species deserves immediate conservation attention. Artificial propagation and reintroduction of L. compacta into its native range may be a viable recovery strategy to prevent extinction from a single perturbation event.
doi:10.1371/journal.pone.0042499
PMCID: PMC3414462  PMID: 22905139
24.  Monitoring an Alien Invasion: DNA Barcoding and the Identification of Lionfish and Their Prey on Coral Reefs of the Mexican Caribbean 
PLoS ONE  2012;7(6):e36636.
Background
In the Mexican Caribbean, the exotic lionfish Pterois volitans has become a species of great concern because of their predatory habits and rapid expansion onto the Mesoamerican coral reef, the second largest continuous reef system in the world. This is the first report of DNA identification of stomach contents of lionfish using the barcode of life reference database (BOLD).
Methodology/Principal Findings
We confirm with barcoding that only Pterois volitans is apparently present in the Mexican Caribbean. We analyzed the stomach contents of 157 specimens of P. volitans from various locations in the region. Based on DNA matches in the Barcode of Life Database (BOLD) and GenBank, we identified fishes from five orders, 14 families, 22 genera and 34 species in the stomach contents. The families with the most species represented were Gobiidae and Apogonidae. Some prey taxa are commercially important species. Seven species were new records for the Mexican Caribbean: Apogon mosavi, Coryphopterus venezuelae, C. thrix, C. tortugae, Lythrypnus minimus, Starksia langi and S. ocellata. DNA matches, as well as the presence of intact lionfish in the stomach contents, indicate some degree of cannibalism, a behavior confirmed in this species by the first time. We obtained 45 distinct crustacean prey sequences, from which only 20 taxa could be identified from the BOLD and GenBank databases. The matches were primarily to Decapoda but only a single taxon could be identified to the species level, Euphausia americana.
Conclusions/Significance
This technique proved to be an efficient and useful method, especially since prey species could be identified from partially-digested remains. The primary limitation is the lack of comprehensive coverage of potential prey species in the region in the BOLD and GenBank databases, especially among invertebrates.
doi:10.1371/journal.pone.0036636
PMCID: PMC3365883  PMID: 22675470
25.  Chronic Exposure of Corals to Fine Sediments: Lethal and Sub-Lethal Impacts 
PLoS ONE  2012;7(5):e37795.
Understanding the sedimentation and turbidity thresholds for corals is critical in assessing the potential impacts of dredging projects in tropical marine systems. In this study, we exposed two species of coral sampled from offshore locations to six levels of total suspended solids (TSS) for 16 weeks in the laboratory, including a 4 week recovery period. Dose-response relationships were developed to quantify the lethal and sub-lethal thresholds of sedimentation and turbidity for the corals. The sediment treatments affected the horizontal foliaceous species (Montipora aequituberculata) more than the upright branching species (Acropora millepora). The lowest sediment treatments that caused full colony mortality were 30 mg l−1 TSS (25 mg cm−2 day−1) for M. aequituberculata and 100 mg l−1 TSS (83 mg cm−2 day−1) for A. millepora after 12 weeks. Coral mortality generally took longer than 4 weeks and was closely related to sediment accumulation on the surface of the corals. While measurements of damage to photosystem II in the symbionts and reductions in lipid content and growth indicated sub-lethal responses in surviving corals, the most reliable predictor of coral mortality in this experiment was long-term sediment accumulation on coral tissue.
doi:10.1371/journal.pone.0037795
PMCID: PMC3360596  PMID: 22662225

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