Haiyang Gao’s research while affiliated with Guangdong Academy of Forestry and other places

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Publications (10)


Chinese pangolins facilitate ecological restoration in burned forest sites by burrowing
  • Article

April 2025

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17 Reads

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1 Citation

Global Ecology and Conservation

Song Sun

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Sheng Zhang

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Fei Wu

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[...]

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Chinese Pangolin Changes Local Vertebrate Assemblages and Contributes to Their Interspecific Interactions by Burrowing and Revisitation

January 2025

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24 Reads

Integrative Zoology

The burrow microhabitats created by burrowing mammals, as a hotspot for biodiversity distribution in ecosystems, provide multiple critical resources for many other sympatric species. However, the cascading effects of burrow resources on sympatric animal community assemblages and interspecific interactions are largely unknown. During 2020–2023, we monitored 184 Chinese pangolin ( Manis pentadactyla ) burrows using camera traps to reveal the burrow utilization patterns of commensal species. We totally recorded up to 57 species, with 19 mammal species, 32 bird species, and 1 reptile species recorded in the burrows revisited by Chinese pangolin, with 19 mammal species and 25 bird species in the non‐revisited burrows. Among them, most bird species as peripheral species primarily utilize soil mounds while most mammal species as burrow‐used species utilize burrow tunnels. The structure of animal communities in the burrows revisited by Chinese pangolins is more complex than that in the burrows not revisited. Furthermore, the positive correlation between community species in pangolin‐revisited burrows is also stronger. Our results demonstrate that the presence and repeated visitation by Chinese pangolins could enhance positive interactions (i.e., the emergence of one species promotes the emergence of another) among species that utilize the burrow resources (particularly, burrow‐used species). Our study provides the first evidence that the ecological role of the Chinese pangolin and its associated burrow microhabitats in promoting the coexistence of burrowing commensals and the restoration of Chinese pangolin populations may potentially contribute to the restoration of local biodiversity and ecological processes.


The ROC verification of distribution of suitable Indian pangolin habitat in the current study area.
Response curves of the predictors for the presence of Indian pangolins in the research region. Note: The blue curves (two shades for categorical variables) reflect the mean +/− one standard deviation, whereas the red curves show the mean response of the five replicate MaxEnt runs. The Y-axis displays the predicted habitat suitability value (logistic output), and the X-axis displays the range of the environmental predictors.
The Indian pangolin habitat suitability model’s regularized training gain of the variables tested.
Variables' contribution to determining suitable habitats for Indian pangolins in the study area.
Insights into Population Status and Habitat Patches of Conservation Concern for the Endangered Indian Pangolin (Manis crassicaudata) in Nowshera District, Northwestern Pakistan
  • Article
  • Full-text available

September 2024

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114 Reads

Simple Summary The Indian pangolin, an endangered species found in Pakistan, was studied in the Nowshera district to assess its population and suitable habitat. We used the line transect method and recorded 56 signs of pangolins, including burrows and digging, over a 156 km² area. The estimated population was very low, with only 29 individuals and a density of 0.013 individuals/km². The MaxEnt model, which predicts habitat suitability, showed that 12.01% of the area was highly suitable and 13.61% was moderately suitable for the pangolin. To protect this fragile population and available habitat patches, the results obtained in the current study recommend stronger law enforcement and conservation efforts. Abstract The Indian pangolin (Manis crassicaudata) stands out among the four surviving species of Asian pangolins, being the sole species present in Pakistan and listed as endangered owing to trafficking and illicit commerce. In the present study, we explored the population status of the Indian pangolin and the existing suitable habitats in Nowshera district, Pakistan. We employed the line transect method to confirm the species presence and subsequent population estimation. In a survey effort of 156 km², a total of 56 signs of Indian pangolin were recorded within the research area. Amongst the 56 signs, 46 were burrows (living burrows (53.57%) and feeding burrows (28.57%)). Digging was observed nine (16.07%) times, along with one direct sighting (1.7%). Our results revealed a population estimate of only 29 pangolins in the Nowshera district, with a population density of 0.013 individuals/km². Later, MaxEnt was applied to the species’ presence points, along with climatic and topographical variables. The MaxEnt model accuracy was good (AUC = 0.811). Of the total area studied, 210 km² (12.01%) were highly suitable and 238 km² (13.61%) were moderately suitable habitat for the Indian pangolin. To safeguard the fragile population and habitat of the Indian pangolin, we highly suggest strengthening watch and ward and law enforcement in the study area. By adopting a comprehensive approach that addresses both the direct threats to Indian pangolins and the underlying factors driving their decline, we can effectively protect this endangered species and ensure the preservation of its essential habitats for robust conservation.

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Identifying habitat modification by Chinese pangolin in subtropical forests of southern China

July 2024

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46 Reads

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4 Citations

Integrative Zoology

The excavation of Chinese pangolin ( Manis pentadactyla ) is expected to alter habitat heterogeneity and thus affect the functioning and structure of forest ecosystems. In this study, the bioturbation of Chinese pangolin on forest soils in three regions (Heping, Tianjingshan, and Wuqinzhang) across Guangdong province was quantified. Overall, a mean of 2.66 m ³ ·ha ⁻¹ and 83.1 m ² ·ha ⁻¹ of burrows and bare mounds, respectively, was excavated by Chinese pangolin; the disturbed soils had significantly lower water content and P, C, available N concentrations, but higher bulk density, pH, and microbial abundance than those undisturbed soils. The unevenness of habitat heterogeneity improvement was mainly ascribed to the stronger soil disturbance caused in resting burrows by pangolins. Patterns of altering habitat heterogeneity were site‐specific, with high‐intensity soil disturbance occurring most in shrubs, meadows, steep habitats at high elevations, and mountain tops in Heping, while in broad‐leaved, coniferous and mixed coniferous and broad‐leaved forests away from human settlements in Tianjingshan and upper mountains at high elevations far away from roads and human settlements in Wuqinzhang. Road networks are the main interference for the burrow distribution in Heping and Wuqinzhang and should be programmed.


Severe Disturbance of Chinese Pangolins Caused by Free-Ranging Domestic Dogs in Unprotected Areas

July 2024

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76 Reads

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1 Citation

Unprotected areas with endangered species generally face severe human disturbance. Domestic dogs are a special form of human disturbance and are sympatrically distributed with critically endangered Chinese pangolins in remote mountainous regions of Guangdong, China. Conflicts in habitat utilization between domestic dogs and Chinese pangolins have rarely been evaluated, yet these conflicts might result in a decline in population viability in the wild. To address how domestic dogs affect Chinese pangolins (Manis pentadactyla) in spatiotemporal niches, we used camera traps to obtain information on the distribution and activity of Chinese pangolins and GPS collars to track free-ranging domestic dog activity in the Wuqinzhang and Pengzhai forest areas of Guangdong, China. Combined with environmental variables, we used individual and cave locations to predict a potentially suitable habitat for Chinese pangolins with Maxent. We used the minimum convex polygon method (MCP) to obtain the home ranges of the domestic dogs. Then, we calculated the overlap between the potentially suitable habitat for Chinese pangolins and the home ranges of free-ranging domestic dogs. In the temporal niche, we compared the daily activity rhythms between domestic dogs and Chinese pangolins and assessed the influences of domestic dogs on Chinese pangolins through avoidance–attraction ratios (AARs). Our results show that the potentially suitable habitat of the Chinese pangolin comprises only approximately 24% of the Wuqinzhang forest area and 12% of the Pengzhai forest area. The percentages of habitat overlap were approximately 48% and 71% in the Wuqinzhang and Pengzhai forest areas, respectively. There was less overlap in the temporal niche between Chinese pangolins and free-ranging domestic dogs, but their AAR was significant. Our results reveal that the Chinese pangolin is facing severe disturbances from free-ranging domestic dogs in spatial niches in unprotected areas. We suggest that assessments of Chinese pangolins’ survival status should be conducted as soon as possible, especially in unprotected areas. To expand and optimize established nature reserves for the Chinese pangolin, further strengthening of domestic dog management is necessary.




Local chronicles reveal the effect of anthropogenic and climatic impacts on local extinctions of Chinese pangolins (Manis pentadactyla) in mainland China

October 2022

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174 Reads

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9 Citations

Anthropogenic and climatic factors affect the survival of animal species. Chinese pangolin is a critically endangered species, and identifying which variables lead to local extinction events is essential for conservation management. Local chronicles in China serve as long‐term monitoring data, providing a perspective to disentangle the roles of human impacts and climate changes in local extinctions. Therefore, we established generalized additive models to identify factors leading to local extinction with historical data from 1700–2000 AD in mainland China. Then we decreased the time scale and constructed extinction risk models using MaxEnt in a 30‐year transect (1970–2000 AD) to further assess extinction probability of extant Chinese pangolin populations. Lastly, we used principal component analysis to assess variation of related anthropogenic and climatic variables. Our results showed that the extinction probability increased with global warming and human population growth. An extinction risk assessment indicated that the population and distribution range of Chinese pangolins had been persistently shrinking in response to highly intensive human activities (main cause) and climate change. PCA results indicated that variability of climatic variables is greater than anthropogenic variables. Overall, the factors causing local extinctions are intensive human interference and drastic climatic fluctuations which induced by the effect of global warming. Approximately 28.10% of extant Chinese pangolins populations are confronted with a notable extinction risk (0.37 ≤ extinction probability≤0.93), specifically those in Southeast China, including Guangdong, Jiangxi, Zhejiang, Hunan and Fujian Provinces. To rescue this critically endangered species, we suggest strengthening field investigations, identifying the exact distribution range and population density of Chinese pangolins and further optimizing the network of nature reserves to improve conservation coverage on the landscape scale and alleviate human interference. Conservation practices that concentrate on the viability assessment of scattered populations could help to improve restoration strategies of the Chinese pangolin. This study evaluated the effect of anthropogenic and climatic impacts on local extinctions of Chinese pangolins through 300 years of local chronicles and historical environment data in China. Extinction probability increased with population growth (main cause) and climate warming. A quarter of the extant Chinese pangolin population is exposed to notable extinction risk and we need to improve conservation and restoration strategies.


Inferred genetic structure of Chinese pangolin subpopulations of Guangdong Province according to (a)ADMIXTURE analysis when K = 2, (b, c) PCA, and (d) DensiTree showing 100,000 phylogenetic tree topologies inferred from whole mitochondrial genome sequences using BEAST. In (a), codes above and below the plot refer to individual and subpopulation, respectively. *denotes the optimal K value. In (a), (b) and (c), different subpopulations are indicated with different colours. In (d), blue line represents the most well-represented tree topology, followed by the red topology and finally the green. Labels on nodes indicate the posterior probabilities of the Maximum Clade Credibility Tree
Demographic history of the studied Chinese pangolin subpopulations. a PSMC estimate based on the de novo assembly, and population genomic estimates from (b) MSMC2, (c) STAIRWAY PLOT and (d) BSP based on 10 whole mitochondrial genomes across four time periods: the current time, the Mid-Holocene (MH; 7.5–5 ka), the last glacial maximum (LGM; approximately 21 ka) and the last interglacial (LIG; approximately 140–120 ka). The thick dark green line in (d) indicates the average estimated trajectory, while the light green lines indicate the 90% credibility interval. (e) Split time inferred by MSMC2 between the GDA and GDB subpopulations. (f) Reconstruction of past variations in the GDA subpopulation in Ne and split time between GDA and GDB subpopulations inferred by SMC +  + . The detailed information in each dataset used in those analysis is described in Table S5
Species distribution models for the Chinese pangolin. a to (d) are the potential suitable areas in the current and historical (Mid-Holocene [MH], 5–7.5 ka, last glacial maximum [LGM], ~ 21 ka, and the last interglacial [LIG], 120–140 ka) times, respectively. Colours indicate the probability of occurrence as predicted by MAXENT [23]
Shifts in the Chinese pangolin distribution in four time periods. a to (d) represent the total area, elevational, latitudinal, and longitudinal dimensions under climate change (over the four time periods of the LIG, LGM, MH, and Current). *Statistical differences, p < 0.05
Map showing the occurrence points of Chinese pangolins in Guangdong Province, China
Influence of Pleistocene climate fluctuations on the demographic history and distribution of the critically endangered Chinese pangolin (Manis pentadactyla)

September 2022

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223 Reads

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14 Citations

BMC Zoology

Background Pleistocene climate fluctuations have strongly modified species genetic diversity and distributions. The Chinese pangolin (Manis pentadactyla) has been recognized as a critically endangered animal due to heavy poaching and trafficking. However, the effect of Pleistocene climate fluctuations on the genetic diversity and spatial distribution of the Chinese pangolin remains largely unknown. Here, we combined whole genome sequencing data, analysis of complete mitochondrial genomes, and a large amount of occurrence data from field surveys to infer the ancestral demographic history and predict the past spatial dynamics of the Chinese pangolin in Guangdong Province, China. Results Our results indicated that there were two subpopulations, which showed similar trends of population size change in response to past climatic changes. We estimated a peak effective population size (Ne) during the last interglacial (LIG), followed by a marked decrease (~ 0.5 to fivefold change) until the last glacial maximum (LGM) and a rebound to a small peak population size during the Mid-Holocene (MH). The estimated time of the separation event between two subpopulations was approximately 3,000–2,500 years ago (ka). We estimated that the distribution of suitable areas shrank by 14.4% from the LIG to LGM, followed by an expansion of 31.4% from the LGM to MH and has been stable since then. In addition, we identified an elevational shift and suitable area decreased significantly during the LGM, but that the geographic extent of suitable areas in the western region increased from the LIG to present. The eastern region of Guangdong Province had the highest habitat suitability across all the climate scenarios. Conclusions Our results suggested that Pleistocene climate fluctuations played an important role in shaping patterns of genetic diversity and spatial distribution, and that human stressors likely contributed to the recent divergence of two Chinese pangolin subpopulations sampled here. We argue that a key protected area should be established in the eastern region of Guangdong Province. As such, this study provides a more thorough understanding of the impacts of Pleistocene climate fluctuations impacts on a mammalian species in southern China and suggests more robust management and conservation plans for this Critically Endangered species of special interest.


Local chronicles reveal the effect of anthropogenic and climatic impacts on local extinctions of Chinese pangolins in China

April 2022

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32 Reads

Anthropogenic and climatic factors affect the survival of animal species. Chinese pangolins are a critically endangered species, and identifying which variables lead to local extinction events is essential for conservation management. Local chronicles in China serve as long-term monitoring data, providing a perspective to disentangle the roles of human impacts and climate changes in local extinctions. Through a generalized additive model, extinction risk assessment model and principal component analysis, we combined information from local chronicles over a period of three hundred years (1700-2000) and reconstructed environmental data to determine the causes of local extinctions of the Chinese pangolin in China. Our results showed that the extinction probability increased with population growth and climate warming. An extinction risk assessment indicated that the population and distribution range of Chinese pangolins has been persistently shrinking in response to highly intensive human activities (main cause) and climate warming. Overall, the factors that cause local extinction, intensive human interference and drastic climatic fluctuations induced by global warming, might increase the local extinction rate of Chinese pangolins. Approximately 25% of extant Chinese pangolins are confronted with a notable extinction risk (0.36≤extinction probability≤0.93), specifically those distributed in Southeast China, including Guangdong, Jiangxi, Zhejiang, Hunan, Fujian, Jiangsu and Taiwan Provinces. To rescue this endangered species, we suggest strengthening field investigations, identifying the exact distribution range and population density of Chinese pangolins and further optimizing the network of nature reserves to improve conservation coverage on the territory scale. Conservation practices that concentrate on the viability assessment of scattered populations could lead to the successful restoration of the Chinese pangolin population.

Citations (4)


... The Chinese pangolin (Manis pentadactyla Linnaeus, 1758) is one of the four extant pangolin species in Asia, distributed across South Asia, Southeast Asia, and East Asia, including Hainan Island and Taiwan (Corlett, 2007;Wu et al., 2020). As an ecological engineer, the Chinese pangolin significantly influences habitat heterogeneity, impacting the structure and function of forest ecosystems (Sun et al., 2024a). Over recent decades, its population has declined drastically due to poaching for traditional medicines, dietary supplements, leather products, and decorative items (Challender et al., 2014;Shirley et al., 2023). ...

Reference:

Characteristics, location, and usage patterns of resting burrows in Chinese pangolins: Insights from radio-telemetry tracking
Identifying habitat modification by Chinese pangolin in subtropical forests of southern China
  • Citing Article
  • July 2024

Integrative Zoology

... The algorithms employed include artificial neural networks (ANN), classification tree analysis (CTA), flexible discriminant analysis (FDA), generalized additive models (GAM), generalized boosted models (GBM), generalized linear models (GLM), multivariate adaptive regression splines (MARS), maximum entropy (MAXNET), random forest (RF), and surface range envelope (SRE) ( Table S3). The biomod2 ensemble approach is widely recognized and used (Gao et al., 2024;Marmion et al., 2009;Thuiller, 2003) for mitigating biases and predictive uncertainties inherent in individual models, thus improving the accuracy of species distribution prediction. The modeling process consisted of four steps: generation of pseudo-absence points, model F.-L. Liu et al. ...

Ensemble SDMs reveal the effect of environmental suitability and nature reserves on conserving Chinese pangolins in Guangdong, China
  • Citing Article
  • April 2024

Journal for Nature Conservation

... In recent decades, Chinese pangolin populations have faced dramatic declines due to poaching for use in traditional medicines, dietary supplements, and as decorative items (Challender et al., 2014;Shirley et al., 2023). Furthermore, the populations of Chinese pangolins have been affected by several factors, including human disturbance, climate change, and habitat fragmentation (Gao et al., 2022). Therefore, the International Union for Conservation of Nature (IUCN) has classified the Chinese pangolin as "Critically Endangered" on its Red List of Threatened Species (Challender et al., 2019). ...

Local chronicles reveal the effect of anthropogenic and climatic impacts on local extinctions of Chinese pangolins (Manis pentadactyla) in mainland China

... The Quaternary Period's cycles of global cooling and warming spurred continuous adaptation and evolution in species (Hewitt 2004). The early to mid-Pleistocene transition brought about major changes in the earth's climatic condition which have significantly impact on present-day distributions and demography signatures in pangolins (Hu et al. 2020;Wei et al. 2022;Wang et al. 2022b). In this study, we undertook DNA analysis of confiscated pangolin seizures obtained from the westernmost distribution of the Chinese pangolin from the Indo-Burma region. ...

Influence of Pleistocene climate fluctuations on the demographic history and distribution of the critically endangered Chinese pangolin (Manis pentadactyla)

BMC Zoology