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1.  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
2.  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
3.  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
4.  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
5.  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
6.  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
7.  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
8.  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
9.  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
10.  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
11.  Emergence of Epizootic Ulcerative Syndrome in Native Fish of the Murray-Darling River System, Australia: Hosts, Distribution and Possible Vectors 
PLoS ONE  2012;7(4):e35568.
Epizootic ulcerative syndrome (EUS) is a fish disease of international significance and reportable to the Office International des Epizootics. In June 2010, bony herring Nematalosa erebi, golden perch Macquaria ambigua, Murray cod Maccullochella peelii and spangled perch Leiopotherapon unicolor with severe ulcers were sampled from the Murray-Darling River System (MDRS) between Bourke and Brewarrina, New South Wales Australia. Histopathology and polymerase chain reaction identified the fungus-like oomycete Aphanomyces invadans, the causative agent of EUS. Apart from one previous record in N. erebi, EUS has been recorded in the wild only from coastal drainages in Australia. This study is the first published account of A. invadans in the wild fish populations of the MDRS, and is the first confirmed record of EUS in M. ambigua, M. peelii and L. unicolor. Ulcerated carp Cyprinus carpio collected at the time of the same epizootic were not found to be infected by EUS, supporting previous accounts of resistance against the disease by this species. The lack of previous clinical evidence, the large number of new hosts (n = 3), the geographic extent (200 km) of this epizootic, the severity of ulceration and apparent high pathogenicity suggest a relatively recent invasion by A. invadans. The epizootic and associated environmental factors are documented and discussed within the context of possible vectors for its entry into the MDRS and recommendations regarding continued surveillance, research and biosecurity are made.
doi:10.1371/journal.pone.0035568
PMCID: PMC3338419  PMID: 22558170
12.  Pathophysiology in Mountain Yellow-Legged Frogs (Rana muscosa) during a Chytridiomycosis Outbreak 
PLoS ONE  2012;7(4):e35374.
The disease chytridiomycosis is responsible for declines and extirpations of amphibians worldwide. Chytridiomycosis is caused by a fungal pathogen (Batrachochytrium dendrobatidis) that infects amphibian skin. Although we have a basic understanding of the pathophysiology from laboratory experiments, many mechanistic details remain unresolved and it is unknown if disease development is similar in wild amphibian populations. To gain a better understanding of chytridiomycosis pathophysiology in wild amphibian populations, we collected blood biochemistry measurements during an outbreak in mountain yellow-legged frogs (Rana muscosa) in the Sierra Nevada Mountains of California. We found that pathogen load is associated with disruptions in fluid and electrolyte balance, yet is not associated with fluctuations acid-base balance. These findings enhance our knowledge of the pathophysiology of this disease and indicate that disease development is consistent across multiple species and in both laboratory and natural conditions. We recommend integrating an understanding of chytridiomycosis pathophysiology with mitigation practices to improve amphibian conservation.
doi:10.1371/journal.pone.0035374
PMCID: PMC3338830  PMID: 22558145
13.  Interbasin Water Transfer, Riverine Connectivity, and Spatial Controls on Fish Biodiversity 
PLoS ONE  2012;7(3):e34170.
Background
Large-scale inter-basin water transfer (IBWT) projects are commonly proposed as solutions to water distribution and supply problems. These problems are likely to intensify under future population growth and climate change scenarios. Scarce data on the distribution of freshwater fishes frequently limits the ability to assess the potential implications of an IBWT project on freshwater fish communities. Because connectivity in habitat networks is expected to be critical to species' biogeography, consideration of changes in the relative isolation of riverine networks may provide a strategy for controlling impacts of IBWTs on freshwater fish communities.
Methods/Principal Findings
Using empirical data on the current patterns of freshwater fish biodiversity for rivers of peninsular India, we show here how the spatial changes alone under an archetypal IBWT project will (1) reduce freshwater fish biodiversity system-wide, (2) alter patterns of local species richness, (3) expand distributions of widespread species throughout peninsular rivers, and (4) decrease community richness by increasing inter-basin similarity (a mechanism for the observed decrease in biodiversity). Given the complexity of the IBWT, many paths to partial or full completion of the project are possible. We evaluate two strategies for step-wise implementation of the 11 canals, based on economic or ecological considerations. We find that for each step in the project, the impacts on freshwater fish communities are sensitive to which canal is added to the network.
Conclusions/Significance
Importantly, ecological impacts can be reduced by associating the sequence in which canals are added to characteristics of the links, except for the case when all 11 canals are implemented simultaneously (at which point the sequence of canal addition is inconsequential). By identifying the fundamental relationship between the geometry of riverine networks and freshwater fish biodiversity, our results will aid in assessing impacts of IBWT projects and balancing ecosystem and societal demands for freshwater, even in cases where biodiversity data are limited.
doi:10.1371/journal.pone.0034170
PMCID: PMC3314595  PMID: 22470533
14.  Weak Prezygotic Isolating Mechanisms in Threatened Caribbean Acropora Corals 
PLoS ONE  2012;7(2):e30486.
The Caribbean corals, Acropora palmata and A. cervicornis, recently have undergone drastic declines primarily as a result of disease. Previous molecular studies have demonstrated that these species form a hybrid (A. prolifera) that varies in abundance throughout the range of the parental distribution. There is variable unidirectional introgression across loci and sites of A. palmata genes flowing into A. cervicornis. Here we examine the efficacy of prezygotic reproductive isolating mechanisms within these corals including spawning times and choice and no-choice fertilization crosses. We show that these species have subtly different mean but overlapping spawning times, suggesting that temporal isolation is likely not an effective barrier to hybridization. We found species-specific differences in gametic incompatibilities. Acropora palmata eggs were relatively resistant to hybridization, especially when conspecific sperm are available to outcompete heterospecific sperm. Acropora cervicornis eggs demonstrated no evidence for gametic incompatibility and no evidence of reduced viability after aging four hours. This asymmetry in compatibility matches previous genetic data on unidirectional introgression.
doi:10.1371/journal.pone.0030486
PMCID: PMC3279358  PMID: 22348010
15.  Tigers Need Cover: Multi-Scale Occupancy Study of the Big Cat in Sumatran Forest and Plantation Landscapes 
PLoS ONE  2012;7(1):e30859.
The critically endangered Sumatran tiger (Panthera tigris sumatrae Pocock, 1929) is generally known as a forest-dependent animal. With large-scale conversion of forests into plantations, however, it is crucial for restoration efforts to understand to what extent tigers use modified habitats. We investigated tiger-habitat relationships at 2 spatial scales: occupancy across the landscape and habitat use within the home range. Across major landcover types in central Sumatra, we conducted systematic detection, non-detection sign surveys in 47, 17×17 km grid cells. Within each cell, we surveyed 40, 1-km transects and recorded tiger detections and habitat variables in 100 m segments totaling 1,857 km surveyed. We found that tigers strongly preferred forest and used plantations of acacia and oilpalm, far less than their availability. Tiger probability of occupancy covaried positively and strongly with altitude, positively with forest area, and negatively with distance-to-forest centroids. At the fine scale, probability of habitat use by tigers across landcover types covaried positively and strongly with understory cover and altitude, and negatively and strongly with human settlement. Within forest areas, tigers strongly preferred sites that are farther from water bodies, higher in altitude, farther from edge, and closer to centroid of large forest block; and strongly preferred sites with thicker understory cover, lower level of disturbance, higher altitude, and steeper slope. These results indicate that to thrive, tigers depend on the existence of large contiguous forest blocks, and that with adjustments in plantation management, tigers could use mosaics of plantations (as additional roaming zones), riparian forests (as corridors) and smaller forest patches (as stepping stones), potentially maintaining a metapopulation structure in fragmented landscapes. This study highlights the importance of a multi-spatial scale analysis and provides crucial information relevant to restoring tigers and other wildlife in forest and plantation landscapes through improvement in habitat extent, quality, and connectivity.
doi:10.1371/journal.pone.0030859
PMCID: PMC3264627  PMID: 22292063
16.  The Contribution of Vegetation and Landscape Configuration for Predicting Environmental Change Impacts on Iberian Birds 
PLoS ONE  2011;6(12):e29373.
Although climate is known to be one of the key factors determining animal species distributions amongst others, projections of global change impacts on their distributions often rely on bioclimatic envelope models. Vegetation structure and landscape configuration are also key determinants of distributions, but they are rarely considered in such assessments. We explore the consequences of using simulated vegetation structure and composition as well as its associated landscape configuration in models projecting global change effects on Iberian bird species distributions. Both present-day and future distributions were modelled for 168 bird species using two ensemble forecasting methods: Random Forests (RF) and Boosted Regression Trees (BRT). For each species, several models were created, differing in the predictor variables used (climate, vegetation, and landscape configuration). Discrimination ability of each model in the present-day was then tested with four commonly used evaluation methods (AUC, TSS, specificity and sensitivity). The different sets of predictor variables yielded similar spatial patterns for well-modelled species, but the future projections diverged for poorly-modelled species. Models using all predictor variables were not significantly better than models fitted with climate variables alone for ca. 50% of the cases. Moreover, models fitted with climate data were always better than models fitted with landscape configuration variables, and vegetation variables were found to correlate with bird species distributions in 26–40% of the cases with BRT, and in 1–18% of the cases with RF. We conclude that improvements from including vegetation and its landscape configuration variables in comparison with climate only variables might not always be as great as expected for future projections of Iberian bird species.
doi:10.1371/journal.pone.0029373
PMCID: PMC3245269  PMID: 22216263
17.  Population Size Influences Amphibian Detection Probability: Implications for Biodiversity Monitoring Programs 
PLoS ONE  2011;6(12):e28244.
Monitoring is an integral part of species conservation. Monitoring programs must take imperfect detection of species into account in order to be reliable. Theory suggests that detection probability may be determined by population size but this relationship has not yet been assessed empirically. Population size is particularly important because it may induce heterogeneity in detection probability and thereby cause bias in estimates of biodiversity. We used a site occupancy model to analyse data from a volunteer-based amphibian monitoring program to assess how well different variables explain variation in detection probability. An index to population size best explained detection probabilities for four out of six species (to avoid circular reasoning, we used the count of individuals at a previous site visit as an index to current population size). The relationship between the population index and detection probability was positive. Commonly used weather variables best explained detection probabilities for two out of six species. Estimates of site occupancy probabilities differed depending on whether the population index was or was not used to model detection probability. The relationship between the population index and detectability has implications for the design of monitoring and species conservation. Most importantly, because many small populations are likely to be overlooked, monitoring programs should be designed in such a way that small populations are not overlooked. The results also imply that methods cannot be standardized in such a way that detection probabilities are constant. As we have shown here, one can easily account for variation in population size in the analysis of data from long-term monitoring programs by using counts of individuals from surveys at the same site in previous years. Accounting for variation in population size is important because it can affect the results of long-term monitoring programs and ultimately the conservation of imperiled species.
doi:10.1371/journal.pone.0028244
PMCID: PMC3229540  PMID: 22164250
18.  Effects of Smart Position Only (SPOT) Tag Deployment on White Sharks Carcharodon carcharias in South Africa 
PLoS ONE  2011;6(11):e27242.
We present 15 individual cases of sub-adult white sharks that were SPOT tagged in South Africa from 2003–2004 and have been re-sighted as recently as 2011. Our observations suggest SPOT tags can cause permanent cosmetic and structural damage to white shark dorsal fins depending on the duration of tag attachment. SPOT tags that detached within 12–24 months did not cause long term damage to the dorsal fin other than pigmentation scarring. Within 12 months of deployment, tag fouling can occur. After 24 months of deployment permanent damage to the dorsal fin occurred. A shark survived this prolonged attachment and there seems little compromise on the animal's long term survival and resultant body growth. This is the first investigation detailing the long term effects of SPOT deployment on the dorsal fin of white sharks.
doi:10.1371/journal.pone.0027242
PMCID: PMC3215706  PMID: 22110620
19.  Population Status of a Cryptic Top Predator: An Island-Wide Assessment of Tigers in Sumatran Rainforests 
PLoS ONE  2011;6(11):e25931.
Large carnivores living in tropical rainforests are under immense pressure from the rapid conversion of their habitat. In response, millions of dollars are spent on conserving these species. However, the cost-effectiveness of such investments is poorly understood and this is largely because the requisite population estimates are difficult to achieve at appropriate spatial scales for these secretive species. Here, we apply a robust detection/non-detection sampling technique to produce the first reliable population metric (occupancy) for a critically endangered large carnivore; the Sumatran tiger (Panthera tigris sumatrae). From 2007–2009, seven landscapes were surveyed through 13,511 km of transects in 394 grid cells (17×17 km). Tiger sign was detected in 206 cells, producing a naive estimate of 0.52. However, after controlling for an unequal detection probability (where p = 0.13±0.017; ±S.E.), the estimated tiger occupancy was 0.72±0.048. Whilst the Sumatra-wide survey results gives cause for optimism, a significant negative correlation between occupancy and recent deforestation was found. For example, the Northern Riau landscape had an average deforestation rate of 9.8%/yr and by far the lowest occupancy (0.33±0.055). Our results highlight the key tiger areas in need of protection and have led to one area (Leuser-Ulu Masen) being upgraded as a ‘global priority’ for wild tiger conservation. However, Sumatra has one of the highest global deforestation rates and the two largest tiger landscapes identified in this study will become highly fragmented if their respective proposed roads networks are approved. Thus, it is vital that the Indonesian government tackles these threats, e.g. through improved land-use planning, if it is to succeed in meeting its ambitious National Tiger Recovery Plan targets of doubling the number of Sumatran tigers by 2022.
doi:10.1371/journal.pone.0025931
PMCID: PMC3206793  PMID: 22087218
20.  Effects of Elevated Temperature and Carbon Dioxide on the Growth and Survival of Larvae and Juveniles of Three Species of Northwest Atlantic Bivalves 
PLoS ONE  2011;6(10):e26941.
Rising CO2 concentrations and water temperatures this century are likely to have transformative effects on many coastal marine organisms. Here, we compared the responses of two life history stages (larval, juvenile) of three species of calcifying bivalves (Mercenaria mercenaria, Crassostrea virginica, and Argopecten irradians) to temperatures (24 and 28°C) and CO2 concentrations (∼250, 390, and 750 ppm) representative of past, present, and future summer conditions in temperate estuaries. Results demonstrated that increases in temperature and CO2 each significantly depressed survival, development, growth, and lipid synthesis of M. mercenaria and A. irradians larvae and that the effects were additive. Juvenile M. mercenaria and A. irradians were negatively impacted by higher temperatures while C. virginica juveniles were not. C. virginica and A. irradians juveniles were negatively affected by higher CO2 concentrations, while M. mercenaria was not. Larvae were substantially more vulnerable to elevated CO2 than juvenile stages. These findings suggest that current and future increases in temperature and CO2 are likely to have negative consequences for coastal bivalve populations.
doi:10.1371/journal.pone.0026941
PMCID: PMC3204984  PMID: 22066018
21.  Estimating Ancestral Ranges: Testing Methods with a Clade of Neotropical Lizards (Iguania: Liolaemidae) 
PLoS ONE  2011;6(10):e26412.
Establishing the ancestral ranges of distribution of a monophyletic clade, called the ancestral area, is one of the central objectives of historical biogeography. In this study, I used three common methodologies to establish the ancestral area of an important clade of Neotropical lizards, the family Liolaemidae. The methods used were: Fitch optimization, Weighted Ancestral Area Analysis and Dispersal-Vicariance Analysis (DIVA). A main difference from previous studies is that the areas used in the analysis are defined based on actual distributions of the species of Liolaemidae, instead of areas defined arbitrarilyor based on other taxa. The ancestral area of Liolaemidae found by Fitch optimization is Prepuna on Argentina, Central Chile and Coastal Peru. Weighted Ancestral Area Analysis found Central Chile, Coquimbo, Payunia, Austral Patagonia and Coastal Peru. Dispersal-Vicariance analysis found an ancestral area that includes almost all the areas occupied by Liolaemidae, except Atacama, Coquimbo and Austral Patagonia. The results can be resumed on two opposing hypothesis: a restricted ancestral area for the ancestor of Liolaemidae in Central Chile and Patagonia, or a widespread ancestor distributed along the Andes. Some limitations of the methods were identified, for example the excessive importance of plesiomorphic areas in the cladograms.
doi:10.1371/journal.pone.0026412
PMCID: PMC3197642  PMID: 22028873
22.  Short-Term Exposure to Warm Microhabitats Could Explain Amphibian Persistence with Batrachochytrium dendrobatidis 
PLoS ONE  2011;6(10):e26215.
Environmental conditions can alter the outcomes of symbiotic interactions. Many amphibian species have declined due to chytridiomycosis, caused by the pathogenic fungus Batrachochytrium dendrobatidis (Bd), but many others persist despite high Bd infection prevalence. This indicates that Bd's virulence is lower, or it may even be a commensal, in some hosts. In the Australian Wet Tropics, chytridiomycosis extirpated Litoria nannotis from high-elevation rain forests in the early 1990 s. Although the species is recolonizing many sites, no population has fully recovered. Litoria lorica disappeared from all known sites in the early 1990 s and was thought globally extinct, but a new population was discovered in 2008, in an upland dry forest habitat it shares with L. nannotis. All frogs of both species observed during three population censuses were apparently healthy, but most carried Bd. Frogs perch on sun-warmed rocks in dry forest streams, possibly keeping Bd infections below the lethal threshold attained in cooler rain forests. We tested whether short-term elevated temperatures can hamper Bd growth in vitro over one generation (four days). Simulating the temperatures available to frogs on strongly and moderately warmed rocks in dry forests, by incubating cultures at 33°C for one hour daily, reduced Bd growth below that of Bd held at 15°C constantly (representing rain forest habitats). Even small decreases in the exponential growth rate of Bd on hosts may contribute to the survival of frogs in dry forests.
doi:10.1371/journal.pone.0026215
PMCID: PMC3196517  PMID: 22028834
23.  Economic Impacts of Non-Native Forest Insects in the Continental United States 
PLoS ONE  2011;6(9):e24587.
Reliable estimates of the impacts and costs of biological invasions are critical to developing credible management, trade and regulatory policies. Worldwide, forests and urban trees provide important ecosystem services as well as economic and social benefits, but are threatened by non-native insects. More than 450 non-native forest insects are established in the United States but estimates of broad-scale economic impacts associated with these species are largely unavailable. We developed a novel modeling approach that maximizes the use of available data, accounts for multiple sources of uncertainty, and provides cost estimates for three major feeding guilds of non-native forest insects. For each guild, we calculated the economic damages for five cost categories and we estimated the probability of future introductions of damaging pests. We found that costs are largely borne by homeowners and municipal governments. Wood- and phloem-boring insects are anticipated to cause the largest economic impacts by annually inducing nearly $1.7 billion in local government expenditures and approximately $830 million in lost residential property values. Given observations of new species, there is a 32% chance that another highly destructive borer species will invade the U.S. in the next 10 years. Our damage estimates provide a crucial but previously missing component of cost-benefit analyses to evaluate policies and management options intended to reduce species introductions. The modeling approach we developed is highly flexible and could be similarly employed to estimate damages in other countries or natural resource sectors.
doi:10.1371/journal.pone.0024587
PMCID: PMC3170362  PMID: 21931766
24.  Climate Change Hastens the Conservation Urgency of an Endangered Ungulate 
PLoS ONE  2011;6(8):e22873.
Global climate change appears to be one of the main threats to biodiversity in the near future and is already affecting the distribution of many species. Currently threatened species are a special concern while the extent to which they are sensitive to climate change remains uncertain. Przewalski's gazelle (Procapra przewalskii) is classified as endangered and a conservation focus on the Qinghai-Tibetan Plateau. Using measures of species range shift, we explored how the distribution of Przewalski's gazelle may be impacted by projected climate change based on a maximum entropy approach. We also evaluated the uncertainty in the projections of the risks arising from climate change. Modeling predicted the Przewalski's gazelle would be sensitive to future climate change. As the time horizon increased, the strength of effects from climate change increased. Even assuming unlimited dispersal capacity of gazelles, a moderate decrease to complete loss of range was projected by 2080 under different thresholds for transforming the probability prediction to presence/absence data. Current localities of gazelles will undergo a decrease in their occurrence probability. Projections of the impacts of climate change were significantly affected by thresholds and general circulation models. This study suggests climate change clearly poses a severe threat and increases the extinction risk to Przewalski's gazelle. Our findings 1) confirm that endangered endemic species is highly vulnerable to climate change and 2) highlight the fact that forecasting impacts of climate change needs an assessment of the uncertainty. It is extremely important that conservation strategies consider the predicted geographical shifts and be planned with full knowledge of the reliability of projected impacts of climate change.
doi:10.1371/journal.pone.0022873
PMCID: PMC3149626  PMID: 21826214
25.  The World's Rediscovered Species: Back from the Brink? 
PLoS ONE  2011;6(7):e22531.
Each year, numerous species thought to have disappeared are rediscovered. Yet, do these rediscoveries represent the return of viable populations or the delayed extinction of doomed species? We document the number, distribution and conservation status of rediscovered amphibian, bird, and mammal species globally. Over the past 122 years, at least 351 species have been rediscovered, most occurring in the tropics. These species, on average, were missing for 61 years before being rediscovered (range of 3–331 years). The number of rediscoveries per year increased over time and the majority of these rediscoveries represent first documentations since their original description. Most rediscovered species have restricted ranges and small populations, and 92% of amphibians, 86% of birds, and 86% of mammals are highly threatened, independent of how long they were missing or when they were rediscovered. Under the current trends of widespread habitat loss, particularly in the tropics, most rediscovered species remain on the brink of extinction.
doi:10.1371/journal.pone.0022531
PMCID: PMC3144889  PMID: 21818334

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