Dramatic Population Decline Research Articles

Conservation genomics of the critically endangered Chinese pangolin.

The Chinese pangolin (Manis pentadactyla, MP) has been extensively exploited and is now on the brink of extinction, but its population structure, evolutionary history, and adaptive potential are unclear. Here, we analyzed 94 genomes from three subspecies of the Chinese pangolin and identified three distinct genetic clusters (MPA, MPB, and MPC), with MPB further divided into MPB1 and MPB2 subpopulations. The divergence of these populations was driven by past climate change. For MPB2 and MPC, recent human activities have caused dramatic population decline and small population size as well as increased inbreeding, but not decrease in genomic variation and increase in genetic load probably due to strong gene flow; therefore, it is crucial to strengthen in situ habitat management for these two populations. By contrast, although human activities have a milder impact on MPA, it is at high risk of extinction due to long-term contraction and isolation, and genetic rescue is urgently needed. MPB1 exhibited a relatively healthy population status and can potentially serve as a source population. Overall, our findings provide novel insights into the conservation of the Chinese pangolin and biogeography of the mammals of eastern Asia.

Path for recovery: an ecological overview of the Jambato Harlequin Toad (Bufonidae: Atelopus ignescens) in its last known locality, Angamarca Valley, Ecuador.

The Jambato Harlequin toad (Atelopus ignescens), a formerly abundant species in the Andes of Ecuador, faced a dramatic population decline in the 1980s, with its last recorded sighting in 1988. The species was considered Extinct by the IUCN until 2016, when a fortuitous discovery of one Jambato by a local boy reignited hope. In this study, we present findings from an investigation conducted in the Angamarca parish, focusing on distribution, abundance, habitat preferences, ecology, disease susceptibility, and dietary habits of the species. In one year we identified 71 individuals at different stages of development in various habitats, with a significant presence in agricultural mosaic areas and locations near water sources used for crop irrigation, demonstrating the persistence of the species in a complex landscape, with considerable human intervention. The dietary analysis based on fecal samples indicated a diverse prey selection, primarily comprising arthropods such as Acari, Coleoptera, and ants. Amphibian declines have been associated with diseases and climate change; notably, our study confirmed the presence of the pathogen Batrachochytrium dendrobatidis (Bd), but, surprisingly, none of the infected Jambatos displayed visible signs of illness. When analyzing climatic patterns, we found that there are climatic differences between historical localities and Angamarca; the temporal analysis also exposes a generalized warming trend. Finally, in collaboration with the local community, we developed a series of management recommendations for terrestrial and aquatic environments occupied by the Jambato.

Modelling the effectivity of a land sparing strategy to preserve an endangered steppe-land bird population in cereal farmland: Scopes and limits

Agricultural intensification and the disappearance of fallow land have been identified as a major driver of biodiversity loss in European farmland. In particular, the dramatic population decline of the little bustard (Tetrax tetrax), a flagship bird species in western European cereal farmland, has been largely attributed to the loss of this crucial habitat. Demographic modelling showed that low breeding success and reduced female survival were co-responsible for the little bustard population decline in a NE Iberian cereal pseudo-steppe. An equilibrium finite rate of change can be achieved by raising either female adult survival or fecundity. In both cases, the required increases fall within a biological meaningful range, but a combination of both would be more feasible in practice. Setting farmland aside as managed fallow can boost fecundity to the required equilibrium value, but the potential of this management action is seriously reduced as mortality increases. Socio-economically acceptable amounts of spared-land can only be achieved if actions to reduce mortality are undertaken in combination with providing fallow land. Actions to reduce both natural and anthropogenic mortality have so far been neglected by little bustard conservation programs. Both are needed if we seek to guarantee the long-term viability of the species and an acceptable share of conservation effort from stakeholders. Our results show that the holistic adaptive management approach adopted here can be used to evaluate the effectiveness and limitations of conservation decisions and to provide insights for conservation projects.

Changes in the Eurasian Otter (Lutra lutra) Population Including Assessment of Damage in the Last Decade: Is Their Protection Still Necessary?

Monitoring wildlife populations requires trustworthy assessment methods to get reliable data to be able to make reasonable management decisions. The Eurasian Otter (Lutra lutra) experienced a dramatic population decline throughout Central Europe during the twentieth century but is currently recovering in both distribution range and population size. Their numbers are regularly monitored by the relevant authorities, who issue an annual report on the occurrence of Eurasian Otters and the financial damage caused by them. These data for the last decade show that the abundance of Eurasian Otters in 2020 was 72% higher than in 2011 and that financial losses on fish farms has increased by 148% over the same period. In view of these facts, it is appropriate to discuss whether the Eurasian Otter is still an endangered species in Central Europe or whether the time has come for government regulation of their numbers, as has already happened with other initially protected animal, great cormorant (Phalacrocorax carbo).

Time-Varying Effective Population Sizes of Group-Living Small Mammals

The Wright–Fisher model predicts that the ratio of effective population size (Ne) to actual population size (N) is <1.0 due to inbreeding and random drifts under constant population sizes. However, social structure may prevent inbreeding and result in outbreeding through coancestry, causing the Ne/N ratio to exceed 1.0. We integrated three years of data on seasonal population fluctuations and population genetics of group-living Daurian pikas (Ochotona dauurica) to test the prediction of >1.0 Ne/N ratio for social small mammals. We estimated biweekly pika population sizes using capture–recapture data from May 2010 to October 2012. We genotyped all captured pikas in each of the three years with 11 microsatellite markers. We estimated pika effective population sizes for 2010–2011, 2011–2012, and 2010–2012, respectively, using the temporal methods with the program MLNe. Pika populations underwent a 75% decline in the summer of 2010 and exhibited relatively constant seasonal fluctuations from 2011 to 2012. Bayesian clustering with program STRUCTURE identified two distinct genetic clusters for the pikas of 2010 and 2011–2012, respectively. The Ne/N ratios of the pikas were 0.46, 1.13, and 0 54 for 2010–2011, 2011–2012, and 2010–2012, respectively. Our findings partially support our hypothesis with the Ne/N ratio being >1.0 from 2011 to 2012. The dramatic population decline in the summer of 2010 probably disrupted the social structure of pikas, which subsequently increased the rate of genetic diversity losses. Re-establishments of the social structure during 2011 and 2012 probably restored the outbreeding of pikas like in other social mammals.

Was the San Quintín kangaroo rat really rediscovered?

The San Quintín kangaroo rat ( Dipodomys gravipes Huey, 1925) is one of the three kangaroo rats in northwestern Baja California and the largest of them in most body dimensions. After a dramatic population decline in the 1980s, it was declared as potentially extinct in the wild by Mexican law. In 2017, the species was claimed to be rediscovered, but critical data supporting the species recognition were not provided. The question remained: Was the San Quintín kangaroo rat really rediscovered? We analyzed individuals identified by us as D. gravipes to validate our identification. We compared cranial morphometric and mitochondrial data of on-purpose collected specimens with those of historic specimens and with those of sympatric kangaroo rats in Baja California, particularly the Dulzura kangaroo rat ( Dipodomys simulans (Merriam, 1904)). Cranial morphometry and body dimensions of current specimens are indistinguishable from those of historic D. gravipes, while being different from D. simulans in most dimensions. External measurements such as cranial traits adequately distinguish both species. The mitochondrial analysis revealed strong support for the species grouping of sequences of our specimens and DNA sequences of D. gravipes from the GenBank repository. This study comprises a morphometric and molecular confirmation of the presence of the species after >25 years of failures to find it.

Morphological Variation and Its Environmental Correlates in the Taihangshan Swelled-Vented Frog across the Qinling Mountains.

Simple SummaryAmphibians have weak dispersal abilities and are sensitive to environmental changes, resulting in their disproportionately high risk of extinction, with many species’ populations rapidly declining. Therefore, it is critical for amphibian conservation to understand their adaptive potential by exploring how amphibians respond to environmental changes based on morphological variations. Our results showed that morphological traits of Feirana taihangnica significantly differed among ages. Along with the increase in annual mean temperature, snout-vent length showed an anti-hump trend, indicating no support for Bergmann’s rule. Mean ultraviolet-B of the highest and lowest months were positively and negatively correlated with head width, thigh length and tibia width, respectively. The present study can help understand the effects of environmental changes on morphological variations of this mountain frog species and its adaptive potential, providing important implications for species conservation.The Taihangshan swelled-vented frog (Feirana taihangnica), an endemic species to the Qinling Mountains, central China, has experienced a dramatic population decline over the last few decades. The aim of this work was to quantify morphological variation in F. taihangnica across the Qinling Mountains and examine environmental correlates of this variation of morphological traits. We implemented a hierarchical partitioning to estimate the independent contribution of each environmental variable on morphological variations. Temperature seasonality was the greatest contributor in variations of snout-vent length (SVL) and head width, and ultraviolet-B (UV-B) radiation of the lowest month was the most influential on both thigh length and tibia width. Then, we used generalized additive models to analyze the relationship between each environmental factor and morphological trait variations. Along the increasing of annual mean temperature, SVL decreased firstly and then increased, indicating no support for Bergmann’s rule. Furthermore, SVL was negatively correlated with annual precipitation, while positively with temperature seasonality. The mean UV-B of the highest and lowest months was positively and negatively correlated with head width, thigh length and tibia width, respectively. The results of this study help us to understand adaptive potential of this mountain frog species via morphological variations in the light of environmental changes.

Presence of spraint at bridges as an effective monitoring tool to assess current Eurasian fish otter distribution in Austria

Monitoring carnivore populations requires sensitive and trustworthy assessment methods to make reasonable and effective management decisions. The Eurasian fish otter Lutra lutra experienced a dramatic population decline throughout Europe during the twentieth century but is currently recovering in both distribution range and population size. In Austria, most assessments on otter distribution have applied a modified version of the so-called “British” or “standard” method utilizing point-wise surveys for otter spraints at predefined monitoring bridges. In this study, we synthesize several recent statewide assessments to compile the current otter distribution in Austria and evaluate the efficiency and sensitivity of the “monitoring bridge” approach in comparison to the “standard” method. The otter shows an almost comprehensive distribution throughout eastern and central Austria, while more western areas (Tyrol and Vorarlberg) are only partially inhabited, likely due to a still ongoing westward expansion. Furthermore, the bridge monitoring method utilizing presence/absence information on otter spraints reveals itself to be a time- and cost- effective monitoring tool with a tolerable loss of sensitivity for large-scale otter distribution assessments. Count data of spraints seem to be prone to observer bias or environmental influences like weather or flooding events making them less suitable for quantitative analyses.

Lions in a coexistence landscape: Repurposing a traditional field technique to monitor an elusive carnivore.

Throughout Africa, lions are thought to have experienced dramatic population decline and range contraction. The greatest declines are likely occurring in human‐dominated landscapes where reliably estimating lion populations is particularly challenging. By adapting a method that has thus far only been applied to animals that are habituated to vehicles, we estimate lion density in two community areas in Kenya's South Rift, located more than 100 km from the nearest protected area (PA). More specifically, we conducted an 89‐day survey using unstructured spatial sampling coupled with playbacks, a commonly used field technique, and estimated lion density using spatial capture‐recapture (SCR) models. Our estimated density of 5.9 lions over the age of 1 year per 100 km2 compares favorably with many PAs and suggests that this is a key lion population that could be crucial for connectivity across the wider landscape. We discuss the possible mechanisms supporting this density and demonstrate how rigorous field methods combined with robust analyses can produce reliable population estimates within human‐dominated landscapes.

INITIAL HUMAN COLONIZATION OF THE AMERICAS, REDUX

ABSTRACTThe study of the peopling of the Americas has been transformed in the past decade by astonishing progress in paleogenomic research. Ancient genomes now show that Native American ancestors were formed in Siberia or the Amur region by admixture of ca. 15–30% Ancient North Eurasian genes with those of East Asians. The Anzick infant, buried with Clovis bifaces at 12,900 cal BP, belonged to a group that was ancestral to later Native Central and South Americans. Fishtail points, derived from Clovis, mark the arrival and rapid expansion of Clovis-descended Paleoindians across South America, also evident in the sharp increase of radiocarbon dates, continent-wide, at 13,000–12,500 cal BP. In both North and South America, extinction of most genera of megafauna was virtually simultaneous with Paleoindian expansion. Human hunting must have been involved, perhaps in concert with other indirect impacts. Contrary to the alternative bolide impact theory, there is no evidence of a dramatic human population decline after 12,800 cal BP. Ancient genomes show that divergent lithic traditions after 13,000 cal BP need not be attributed to a separate Pacific Rim migration stream. Several recent finds raise the possibility that pre-Clovis people might have reached the Americas before 20,000 cal BP, but these precursors must have either failed to thrive, or were ultimately replaced by proto-Clovis or Clovis people. Consilient paleogenomic and archaeological data indicate that initial colonization by Paleoindian ancestors of living Native Americans occurred after 14,500 cal BP.

Decreased selectivity during mate choice in a small‐sized population of a long‐lived seabird

As biparental care is crucial for breeding success in Procellariiformes seabirds (i.e. albatrosses and petrels), these species are expected to be choosy during pair formation. However, the choice of partners is limited in small‐sized populations, which might lead to random pairing. In Procellariiformes, the consequences of such limitations for mating strategies have been examined in a single species. Here, we studied mate choice in another Procellariiforme, Bulwer's petrelBulweria bulwerii, in the Azores (ca 70 breeding pairs), where the species has suffered a dramatic population decline. We based our approach on both a 11‐year demographic survey (capture–mark–recapture) and a genetic approach (microsatellites, n = 127 individuals). The genetic data suggest that this small population is not inbred and did not experience a genetic bottleneck. Moreover, pairing occurred randomly with respect to genetic relatedness, we detected no extrapair parentage (n = 35 offspring), and pair fecundity was unrelated to relatedness between partners. From our demographic survey, we detected no assortative mating with respect to body measurements and breeding experience and observed very few divorces, most of which were probably forced. This contrasts with the pattern previously observed in the much larger population from the Selvagens archipelago (assortative mating with respect to bill size and high divorce rate). We suggest that the Bulwer's petrels from the Azores pair with any available partner and retain it as long as possible despite the fact that reproductive performance did not improve with pair common experience, possibly to avoid skipping breeding years in case of divorce. We recommend determining whether decreased choosiness during mate choice also occurs in reduced populations of other Procellariiform species. This might have implications for the conservation of small threatened seabird populations.

Dramatic decline in a titi monkey population after the 2016-2018 sylvatic yellow fever outbreak in Brazil.

Platyrrhini are highly vulnerable to the yellow fever (YF) virus. From 2016 to 2018, the Atlantic Forest of southeast Brazil faced its worst sylvatic YF outbreak in about a century, thought to have killed thousands of primates. It is essential to assess the impact of this epidemic on threatened primate assemblages to design effective conservation strategies. In this study, we assessed the impact of the 2016-2018 YF outbreak on a geographically isolated population of Near Threatened black-fronted titi monkeys (Callicebus nigrifrons) in two Atlantic Forest patches of the Santuário do Caraça, MG, Brazil. Extensive preoutbreak monitoring, conducted between 2008 and 2016, revealed that the home range and group sizes of the population remained stable. In 2016, the population size was estimated at 53-57 individuals in 11-12 groups. We conducted monitoring and playback surveys in 2019 and found that the population had decreased by 68% in one forest patch and completely vanished in the other, resulting in a combined decline of 80%. We discuss this severe loss of a previously stable population and conclude that it was highly likely caused by the YF outbreak. The remaining population is at risk of disappearing completely because of its small size and geographic isolation. A systematic population surveys of C. nigrifrons, along other sensible Platyrrhini species, is needed to re-evaluate their current conservation status.

Beyond Sea Turtles: Fusarium keratoplasticum in Eggshells of Podocnemis unifilis, a Threatened Amazonian Freshwater Turtle.

The endangered yellow-spotted river turtle (Podocnemis unifilis) has experienced a dramatic population decline in the Ecuadorian Amazonia, mainly due to overexploitation of its eggs. To reverse this trend, the Wildlife Conservation Society has developed a head-start program in Yasuní National Park since 2008, but the potential risk that microbes associated with its eggs might represent for hatching success has not been evaluated yet. Members of the Fusarium solani species complex (FSSC) are involved in egg failure in sea turtles under natural and hatchery conditions, but their role in infecting the eggs of P. unifilis is unknown. In this study, we collected eggshells of P. unifilis and obtained 50 fungal and bacterial isolates. Some potentially pathogenic fungi of the genera Fusarium, Penicillium and Rhizopus were identified based on molecular data. Most importantly, the sea turtle pathogenic species F. keratoplasticum not only was present, but it was the most frequently found. Conversely, we have also isolated other microorganisms, such as Pseudomonas or Phoma-like species, producing a wide spectrum of antifungal compounds that may have a protective role against fungal diseases. Our survey provides useful information on potential pathogens found in P. unifilis eggshells, upon which the success of conservation programs may depend.

From Conquest to Centralization: Domestic Conflict and the Transition to Direct Rule

Why do governments centralize control over regions? We present a theory of the transition from indirect to direct rule, focusing on the strategic interaction between a ruler and local potentates who provide civil order in exchange for a share of tax revenue. When the threat of rebellion from below falls and elites become less crucial intermediaries, the ruler is able to centralize power, replacing local potentates with direct agents of the state and investing in a fiscal bureaucracy for future state development. We assess the theory using subnational data from sixteenth- and seventeenth-century Mexico around the time of a dramatic demographic collapse, which undermined the threat of domestic conflict. Using a difference-in-differences approach and an instrumental variables empirical strategy based on the climate shocks associated with a virulent series of epidemics, we show that state centralization occurred faster in areas experiencing a more dramatic decline in population.

Combining the responses of habitat suitability and connectivity to climate change for an East Asian endemic frog

BackgroundUnderstanding the impacts of past and contemporary climate change on biodiversity is critical for effective conservation. Amphibians have weak dispersal abilities, putting them at risk of habitat fragmentation and loss. Both climate change and anthropogenic disturbances exacerbate these risks, increasing the likelihood of additional amphibian extinctions in the near future. The giant spiny frog (Quasipaa spinosa), an endemic species to East Asia, has faced a dramatic population decline over the last few decades. Using the giant spiny frog as an indicator to explore how past and future climate changes affect landscape connectivity, we characterized the shifts in the suitable habitat and habitat connectivity of the frog.ResultsWe found a clear northward shift and a reduction in the extent of suitable habitat during the Last Glacial Maximum for giant spiny frogs; since that time, there has been an expansion of the available habitat. Our modelling showed that “overwarm” climatic conditions would most likely cause a decrease in the available habitat and an increase in the magnitude of population fragmentation in the future. We found that the habitat connectivity of the studied frogs will decrease by 50–75% under future climate change. Our results strengthen the notion that the mountains in southern China and the Sino-Vietnamese transboundary regions can act as critical refugia and priority areas of conservation planning going forward.ConclusionsGiven that amphibians are highly sensitive to environmental changes, our findings highlight that the responses of habitat suitability and connectivity to climate change can be critical considerations in future conservation measures for species with weak dispersal abilities and should not be neglected, as they all too often are.

Changes in the expression of antimicrobial peptide genes in honey bees (Apis mellifera) under the influence of various pathogens.

Honey bees play an invaluable role in the ecosystem as plant pollinators. The dramatic decline in honey bee population has prompted a search for its underlying causes and effective remedy methods. Insects produce antimicrobial peptides (AMPs) which play an important role in the induced humoral immune response. The presence of apidaecin, abaecin, hymenoptaecin and defensin has been confirmed in honey bees. The expression of genes encoding these proteins is activated via two signalling pathways: toll pathway for apidaecins and defensins, and Imd pathway for abaecin and hymenoptaecin. Bee pathogens and parasites affect the expression of AMP genes, thus stimulating or inhibiting immune responses. The main causative agents of the global decline in bee populations include Varroa destructor, deformed wing virus (DWV), neonicotinoids, and microsporidian parasites of the genus Nosema. Researchers are divided over the influence of these pathogens and insecticides on the expression of AMP genes in insects. There is evidence to suggest that the age of honey bee plays an important role, and that peptides should be identified solely in the context of specific age groups. There is also a general scarcity of research into the long-term effects of immunosuppressive factors. The influence of various pathogens on the immune system of bees should be investigated to better understand their mutual relationships and to develop effective bee protection methods.

Range-Wide Population Assessment of the Endangered Yellow-Naped Amazon (Amazona auropalliata)

Yellow-naped amazons, Amazona auropalliata, have experienced a dramatic population decline due to persistent habitat loss and poaching. In 2017, BirdLife International changed the species’ status from threatened to endangered and estimated that between 10,000 and 50,000 individuals remained in the wild. An accurate estimate of the number of remaining wild individuals is critical to implementing effective conservation plans. Wright et al. conducted roost count surveys in Costa Rica and Nicaragua during 2016 and published their data in 2019; however, no population data exists for the rest of the range. We conducted roost counts at 28 sites across Mexico, Guatemala, and the Bay Islands in Roatan during 2018 and 2019. We counted 679 birds and combined our data with the published Wright et al. (2019) data for a total of 2361 wild yellow-naped amazons observed across the species’ range. There were fewer roosts detected in the northern region of the range than in the southern region. We found that roosts were most likely to occur in built-up rural and pasture habitat, with 71% found within 100 m of human habitation. Our results illustrate the need for immediate conservation action to mitigate decline, such as enforced legal action against poaching, nest guarding, and increased community education efforts.

Bone biomarkers in koalas: validation of assays and preliminary analyses.

Traumatic injury, including bone fracture, is, to date, one of the leading causes of koala mortality in the South East Queensland region of Australia. Further, the specialist diet of koalas, which is restricted to certain Eucalyptus spp., may impact their normal bone physiology. Considering the dramatic koala population decline and high incidence of trauma, a greater understanding of koala bone physiology may support conservation. We retrieved from GenBank the protein sequences of parathyroid hormone (PTH), osteocalcin (OCN), and tissue-nonspecific alkaline phosphatase (TNALP) in human, dog, cattle, horse, koala, and gray short-tailed opossum. After homology was determined, plasma samples from 13 koalas were analyzed with human PTH, OCN, and bone-specific ALP (BALP) assay kits. Although koala PTH exhibited relatively low sequence homology with placental mammals, high sequence homology between humans and koalas was observed for both OCN and TNALP, and successful cross-reactivity was achieved using human enzyme immunoassay kits for detection of OCN and BALP biomarkers in koala plasma. However, we identified no correlation between OCN and BALP concentrations of healthy and trauma-affected koalas (p = 0.66 and p = 0.79, respectively). Further analysis of OCN and BALP in healthy and diseased koalas will allow a better understanding of bone physiology in this unique marsupial.

De novo assembly and microsatellite marker development of the transcriptome of the endangered Brachymystax lenok tsinlingensis

Brachymystax lenok tsinlingensis is an endemic freshwater fish in Northeast Asia, but experienced a dramatic population decline due to over-exploitation, deteriorated habitats and global climate change. It has been listed as a threatened or endangered species in South Korea and China, respectively. However, the conservation and restoration work in wild B. lenok tsinlingensis populations require large amount of genetic and molecular data to support effective management of genetic resources, while the corresponding information is very limited. This study was conducted to generate transcriptome assembly and annotation, as well as to develop novel microsatellite markers for B. lenok tsinlingensis. We collected gill and liver tissues and performed transcriptome sequencing. Then the first transcriptome for B. lenok tsinlingensis was de novo assembled and annotated. Microsatellite markers were searched in the assembled transcripts and characterized within ninety individuals collected from three natural sites. A total of 110,712 protein-coding transcripts were assembled, of which 82,861 transcripts were successfully annotated. This assembly displayed a high level of completeness with retrieving 94% of the single-copy orthologs conserved across vertebrate species. Furthermore, 75,891 microsatellite loci were identified from this transcriptome assembly and 20 polymorphic markers were randomly selected for characterization. The microsatellite markers and the first transcriptome assembly would provide valuable resources for investigating genetic diversity and phylogeographic structure of wild populations and molecular mechanisms responding to stressful environments (e.g. increased water temperature) to guide future conservation studies and breeding programs.

Use of historical data to assess the impact of climate change and anthropogenic disturbance on the black-billed capercaillie (Tetrao urogalloides) in northeast China

Species distribution models have been widely used to assess changes in species distribution under climate change. However, these models often neglect anthropogenic drivers of range shifts or contractions, and general circulation models may introduce uncertainties. Therefore, quantifying the impacts of both climate change and anthropogenic disturbance on species distribution remains a challenge. Long-term historical data may overcome the uncertainties introduced by variability in global climate models and thus provide ecologists with comprehensive information on the long-term effects of anthropogenic disturbance. The black-billed capercaillie (Tetrao urogalloides) has undergone a dramatic population decline since the late 20th century and is endangered in China. We used ensemble forecasting to assess the impact of climate change and anthropogenic disturbance on the distribution of this species in northeast China from the 1970s to the 2000s. Our results suggested a decline in the predicted distribution area from 339,638 km2 in the 1970s to 219,083 km2 in the 2000s, representing a total reduction of 35.50%. We estimated that the range contraction caused by climate change equated to 22,038 km2, while that due to anthropogenic disturbance to 98,517 km2 over this time period. Therefore, the observed range contraction for this species is primarily attributable to anthropogenic disturbance.