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Article

Estimating the Population Size of Masked Palm Civets Using Hair-Snaring in Southwest China

by
Di Wang
1,†,
Dan Zhang
1,†,
Hongliang Bu
1,
John B. Hopkins III
1,2,
Mengyin Xiong
1,
Dajun Wang
1,
Meng Yao
1,3,
Sheng Li
1 and
Rongjiang Wang
1,*
1
School of Life Sciences, Peking University, Beijing 100871, China
2
Center for Wildlife Studies, Camden, ME 04843, USA
3
Institute of Ecology, College of Urban and Environmental Sciences, Peking University, Beijing 100871, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Diversity 2024, 16(7), 421; https://doi.org/10.3390/d16070421
Submission received: 14 June 2024 / Revised: 11 July 2024 / Accepted: 16 July 2024 / Published: 19 July 2024
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Abstract

:
Mesocarnivores are major components of carnivore assemblages, and they play important roles in structuring communities and regulating community dynamics. In Southwest China, many apex predators have been extirpated, and this has potentially resulted in the ecological release of mesocarnivores. Estimating the sizes of mesocarnivore populations is challenging. We used DNA derived from hairs and spatial capture–mark–recapture techniques to estimate the population size of masked palm civets (Paguma larvata) in Laohegou Nature Reserve in the Minshan Mountains of Sichuan Province, China. In the fall of 2014 and the spring of 2015, we collected 144 and 230 hair samples, respectively, at 30 baited stations. We used 16S rRNA fragments, microsatellite genotyping, and sexing to determine that 191 samples were derived from 44 masked palm civet individuals (24 males and 20 females). Using spatially explicit capture–recapture analysis, we estimated that there were 82 ± 13 masked palm civets in the study area, with a density of 1.7 individuals/km2. This is the first study to estimate the population size of masked palm civets in the wild. Our data provide important new information on the density of masked palm civets.

1. Introduction

Carnivores occupy the highest trophic level in many terrestrial ecosystems and play important roles in structuring communities [1]. Although large carnivores, such as tigers (Panthera tigris), lions (P. leo), and wolves (Canis lupus), are charismatic apex predators that receive much public attention, mesocarnivores, which are medium-sized (body weight < 15 kg) mid-trophic level predators, are the main carnivores in most carnivore assemblages [2]. Following the extirpation of apex predators, the abundance of mesocarnivores increases, and this commonly observed phenomenon is known as “mesocarnivore release” [3,4]. Increases in the abundance of mesocarnivores can then increase predation pressure on their prey and interspecific competition within a mesocarnivore guild, both of which have major effects on community structure and function [2,4]. Determining the functional role of mesocarnivores in ecosystems has become a major goal of ecological research, wildlife management, and conservation programs [5,6,7,8]. Estimates of the abundance and density of mesocarnivores across the landscape are essential, not only for understanding fundamental ecological information, but also for understanding interspecific interactions in ecosystems, such as mesocarnivore release [7].
Estimating the abundance of mesocarnivores, however, is often challenging. Traditional capture–mark–recapture techniques typically require researchers to repeatedly capture or observe marked animals [9]. Such tasks are often time-intensive and expensive. During the last two decades, non-invasive capture–mark–recapture methods that rely on either DNA [10] or camera-trap photos [11] have become increasingly used to estimate carnivore population sizes.
Here, we estimated the population size and density of the masked palm civet (Paguma larvata), which is one of the most northerly distributed members of the family Viverridae (Mammalia, Carnivora); this species ranges from tropical Southeast Asia to temperate North China [12,13]. Given that mesocarnivore release has been observed throughout its range, the masked palm civet plays an important role in shaping community structure. The masked palm civet is a ubiquitous member of the mesocarnivore guild in various ecosystems across its vast range. Compared with other species in the mesocarnivore guild, the masked palm civet has a broader diet, which includes various small vertebrates (e.g., small rodents, shrews, birds, and frogs), eggs, invertebrates, and fruits, and the composition of prey in its diet is associated with prey availability [12,14]. As fruit is a major food source for masked palm civets, they are important agents for the dispersal of seeds in forest ecosystems [15]. In addition, our previous studies have shown that the masked palm civet and hog badger (Arctonyx collaris) tend to avoid each other, and Siberian weasels (Mustela sibirica) avoid masked palm civets [16,17]. Accurate estimates of population abundance would be beneficial for further clarifying the ecosystem-level effects of the masked palm civet. However, there is no information regarding the population abundance of the masked palm civet.
Masked palm civets are black and white, and have a simple pattern on their fur, which increases the difficulty of identifying individuals through pelage patterns. In addition, masked palm civets defecate in creeks [18], which precludes the collection of fecal samples for DNA analysis. Recently, hair-snaring has been shown to be a reliable approach for collecting hair from masked palm civets, and this indicates that DNA-based approaches can be used to identify individuals [19]. Hence, we estimated the abundance and density of a population of masked palm civets in Southwest China by integrating non-invasive hair-snaring, DNA analysis, and spatially explicit capture–recapture modeling. The results of our study will aid the development of a feasible approach for estimating the population size and density of the masked palm civet and other elusive mesocarnivore species. The aim of this study was to provide a proof of concept for other researchers in Southwest China interested in studying mesocarnivores and their effects on community dynamics.

2. Materials and Methods

2.1. Study Area

This study was conducted in Laohegou Nature Reserve (LNR, 32°30′ N, 104°42′ E), Sichuan Province, China (Figure 1). LNR is a 70 km2 reserve that spans a broad elevational range (1160–3479 m). The vegetation types in LNR change along an elevational gradient and include evergreen forest (<1800 m), deciduous forest (1800–2400 m), conifer–deciduous forest (2400–2800 m), coniferous forest (2800–3200 m), and alpine meadow (>3200 m).
LNR lies in the Minshan Mountains, which is in the transition alpine–valley region between the northeast Hengduan Mountains and east Tibetan Plateau, one of the global biodiversity hotspots (i.e., Mountains of Southwest China) [20]. LNR was established to protect the iconic giant panda (Ailuropoda melanoleuca) and its habitat. Apex predators, including tigers, leopards (P. pardus), wolves, and dholes (Cuon alpinus), were extirpated from the Minshan Mountains in the late 20th century [21,22,23,24], but the omnivorous Asiatic black bear (Ursus thibetanus) still occurs in this region.
Previous studies have revealed that the mesocarnivore guild in LNR is diverse and includes masked palm civets, Asiatic golden cats (Catopuma temminckii), leopard cats (Prionailurus bengalensis), red foxes (Vulpes vulpes), hog badgers, Chinese ferret badgers (Melogale moschata), yellow-throated martens (Martes flavigula), Eurasian otters (Lutra lutra), Siberian weasels, and lack-toothed weasels (M. aistoodonnivalis) [16,24,25]. The masked palm civet is one of the most commonly detected mesocarnivore species in camera-trapping surveys in LNR [16,26,27].

2.2. Hair Sample Collection

We used a ground cubby with six gun brushes to collect hair samples from masked palm civets in the study area [18]. Our sampling grid comprised 30 1.5 × 1.5 km cells (Figure 1), which is the approximate home range of masked palm civets reported in previous studies [28,29,30,31]. We placed a ground cubby within 500 m of the center of each cell, with the exception of one cell due to the rugged terrain, which precluded easy access to the cell center (the cubby of cell #L17 was actually placed in cell #L16, Figure 1). Each station was baited with a chicken wing and carnivore scent lure [19]. Masked palm civets are seldom recorded by remote cameras in LNR from November to the following March because they hibernate during this period [17]. Access to sampling stations is also difficult in July and August due to heavy rain and torrential floods. For these reasons, we conducted our field surveys during two seasons: the fall of 2014 (September–November) and the spring of 2015 (April–June). We conducted one survey approximately every 13 days on average (ranging from 5 to 23 days), and performed a total of 12 surveys: 7 in the fall and 5 in the spring (Table S1). In each survey, we visited as many stations as possible to collect hair samples and replace baits. Hairs from each gun brush were regarded as a sample. We disentangled hairs and inserted each sample into a separate envelope. We then transported samples to our laboratory and stored them at −20 °C.

2.3. Species Identification

We used an EasyPure Genomic DNA Kit (TransGen, Beijing, China) to extract DNA from five hairs in each sample. In some cases, we had less than five hairs, but used the same five-hair procedure. Species were identified based on the sequence of a fragment of the mitochondrial 16S rRNA gene (ca. 380 bp in length). We used the same primer pair and PCR amplification conditions as described by Xiong et al. [32], and identified species through comparison of the complete mitochondrial genome of the masked palm civet (GenBank accession number KT191130) [33] with those of our samples. Species were determined based on >98% similarity with the top-matched sequence.

2.4. Individual Identification

We genotyped samples identified as masked palm civets at 10 microsatellite loci [34,35,36]. The genotyping protocol was the same as that described in a previous study [36]. To identify unique individuals, microsatellite genotypes were analyzed using GenAlEx v6.5 [37]. We distinguished the sex of each sample by amplifying fragments of the zfx and sry genes using primer pairs designed for masked palm civets [38].

2.5. Population Density Estimation

We used spatially explicit capture–recapture methods to estimate population density. We considered one record of an individual at a station during a survey as one capture and then used the software SPACECAP ver. 1.1.0 [39] to perform spatial Bayesian estimates. Our study area was restricted to the main valley in LNR surrounded by high mountain ridges (>2500 m), and masked palm civets were not recorded at this high altitude in our systematic investigation with remote cameras [17]; thus, these mountain ridges might serve as natural barriers that limit the dispersal of masked palm civets. The study area is a likely closed region given that the entrance of the valley is relatively narrow. We generated a grid of equally spaced points at 100 m intervals using ArcGIS to cover LNR and the adjacent area. Points outside LNR and those with >2500 m elevation were marked as unsuitable habitat for the studied population, and the remaining points represented all potential home range centers of masked palm civets. The other two necessary input files for SPACECAP, an animal capture details file and a trap deployment details file, were generated based on our survey details.
We set model definitions as follows: trap response absent, spatial capture–recapture, half-normal detection, and Bernoulli’s process. We ran 100,000 Markov chain Monte Carlo iterations, with a burn-in period of 20,000 and a thinning rate of 10.

3. Results

We collected 144 and 230 hair samples in the fall of 2014 and the spring of 2015, respectively, mainly from lower-elevation stations. Amplification of 16S rRNA fragments failed in 77 samples. Based on obtained sequences, 191 samples were identified as being from masked palm civets; the others were from Siberian weasels (102 samples), Chinese white-bellied rats (2 samples), giant panda (1 sample), and Pére David’s rock squirrel (Sciurotamias davidianus) (1 sample). The 191 hair samples of masked palm civets were determined to be derived from 44 individuals (24 males and 20 females) using microsatellite genotyping and sexing. The number of masked palm civet individuals recorded in each station ranged from zero to seven (mean: 1.7, and standard deviation: 2.1).
A total of 74 captures of masked palm civets were made during the survey period, and the number of captures differed greatly between seasons (24 and 50 captures in the fall and spring, respectively). Sixteen individuals were captured more than once (two to seven times), and eight were recaptured at the same station where they were captured the first time; the others were captured at up to two adjacent stations (i.e., located in adjacent cells). Among the 24 males, we recaptured 7, 3 of which were captured at one station, and 4 at two adjacent stations. Among the 20 females, we recaptured 9, 5 of which were captured at one station, and 4 at two adjacent stations. Detailed capture information is shown in Table S2.
Posterior estimates of the parameters involved were obtained and are summarized in Table 1 using spatially explicit capture–recapture analysis. We estimated that there were 82 masked palm civets (95% highest posterior density (HPD) level: 57–107) in LNR, with a density of approximately 1.7 individuals per km2 (95% HPD level: 1.1–2.1). We found that the pixel densities of masked palm civets were universally higher at lower elevations, which were divided by the main creek into eastern and western regions (Figure 2A). When estimating the number of males and females separately, the population sizes of both sexes were the same (approximately 44 individuals) (Table S3); however, the density of females was higher than that of males (Figure 2B,C). Substantial differences in estimated population sizes were observed when the dataset was divided into spring and fall sub-datasets (i.e., 25 (95% HPD level: 13–41) in fall and 122 (95% HPD level: 63–200) in spring (Table S3)); the same pattern was observed in density data (Figure 2D,E).

4. Discussion

Although the masked palm civet is classified as Near Threatened in China’s Red List of Threatened Species, few studies have estimated its abundance in the wild. In this study, we used hair sampling and DNA-based individual identification to estimate the population size of the masked palm civet in its natural habitat. We estimated that there are 82 ± 13 individuals in LNR. Our study was the first to estimate the population size of masked palm civets in the wild. This study provides fundamental data that could aid the monitoring of masked palm civets. Additional years of data could provide insights into the population dynamics of masked palm civets in LNR, which is critically important for the development of conservation strategies. This study’s assumption that the entrance of the valley is closed for masked palm civets might be challenged. Further investigations are necessary to obtain supportive evidence.
The overall density of masked palm civets is 1.7 individuals/km2 in LNR, and higher densities of masked palm civets (up to ca. 5 individuals/km2) were observed at a couple of sites (Figure 2A), indicating that these sites might provide favored microhabitats. As more than one individual (up to seven) regularly visited the same station according to the detailed capture information (Table S2), these sites were used by several individuals. Our results are consistent with the known activity patterns of masked palm civets. Masked palm civets may form small groups during the breeding season, and groups with one male and one female, two males and one female, and one male and two females have been observed [40,41]. Studies of the home range of masked palm civets reveal that overlapping home ranges are common [28,29,30,31]. For example, in the Houhe National Nature Reserve (Hubei, China), the average overlap of home ranges of masked palm civets is approximately 16%, and the maximum overlap observed is greater than 60% [31]. As all recaptured masked palm civets were detected at one or adjacent stations, we estimate that the home range of masked palm civets in LNR was roughly equivalent to the size of one grid cell (2.25 km2), which is consistent with results (1.1–5.9 km2) obtained using radio-tracking methods [28,29,30,31].
No differences were observed in the population size and average density of males and females in LNR; however, some differences in the density distribution of males and females were observed (Figure 2B,C). This is consistent with the finding that male and female masked palm civets have similar home ranges in Houhe [31] and in Taohong Village, Jiangxi, China [29].
The estimated population size of masked palm civets differed substantially in the fall and spring in LNR. This might be related to seasonal variation in the activity of masked palm civets. Of the 74 total captures, 24 captures were made in the fall, and 50 captures were made in the spring. Similar results were obtained in an investigation with camera traps in the Qinling Mountains, which indicated that the relative activity indices of masked palm civets were higher in the spring–summer than in the fall–winter [7]. Reduced activity in the fall results in a lower capture possibility. In addition, masked palm civets hibernate or semi-hibernate in winter [42]. This is the reason why all civets captured in the fall were captured at low elevation. Surveys conducted over the entire year are needed to avoid biases associated with single-season surveys.
In addition to masked palm civets, hair-snaring devices also attracted other mesocarnivores in this study, such as Siberian weasels. Improvements in hair-sampling devices are needed to increase their efficacy for detecting other elusive mesocarnivores. For example, a narrower cubby may be more efficient for Siberian weasels, which are smaller than masked palm civets.
In conclusion, we estimated the population size and density of masked palm civets in the wild for the first time. We confirmed that the genetic capture–recapture approach can provide useful data for determining the sizes of wild populations. Furthermore, extending this genetic capture–recapture approach to other elusive mesocarnivores (e.g., Siberian weasels) may obtain information regarding population sizes, which is useful for understanding ecological interactions in the mesocarnivore guild.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d16070421/s1, Table S1: The capture dates of masked palm civets (Paguma larvata)in 30 hair-trap stations during 12 surveys in Laohegou Nature Reserve; Table S2. The capture records of masked palm civets (Paguma larvata) in 30 hair-trap stations during 12 surveys in Laohegou Nature Reserve; Table S3. Posterior density estimates of parameters estimated for masked palm civets (Paguma larvata) in Laohegou Nature Reserve.

Author Contributions

Conceptualization, J.B.H.III, D.W. (Dajun Wang) and R.W.; methodology, H.B. and J.B.H.III; formal analysis, D.W. (Di Wang), D.Z., M.Y. and S.L.; investigation, D.Z., H.B. and M.X.; writing—original draft preparation, D.W. (Di Wang) and D.Z.; writing—review and editing, M.Y., J.B.H.III, S.L. and R.W.; visualization, D.W. (Di Wang); funding acquisition, D.W. (Dajun Wang) and S.L. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the Sichuan Nature Conservancy Foundation and The Nature Conservacy-China Program, grant number: SNCF/PU092013.

Data Availability Statement

The data supporting the results of this study can be found in the supplementary files, or requested from the corresponding author.

Acknowledgments

We thank Chunping Luo, Chunping Liang, Yong Zheng, Xianghui Chen, and Zhenzhong Xiang for their assistance with fieldwork at Laohegou Nature Reserve, Yifan Zhang for assistance in making maps, and Jeff Stetz for his comments on the manuscript. We thank Thomas S. Jung and another anonymous reviewer for their helpful comments regarding this manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Locations of hair-snare stations at Laohegou Nature Reserve, Sichuan Province, China.
Figure 1. Locations of hair-snare stations at Laohegou Nature Reserve, Sichuan Province, China.
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Figure 2. Density distributions of masked palm civets (Paguma larvata) in Laohegou Nature Reserve based on all data (A), male data (B), female data (C), autumn data (D), and spring data (E).
Figure 2. Density distributions of masked palm civets (Paguma larvata) in Laohegou Nature Reserve based on all data (A), male data (B), female data (C), autumn data (D), and spring data (E).
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Table 1. Posterior density estimates of parameters estimated for masked palm civets (Paguma larvata) in Laohegou Nature Reserve.
Table 1. Posterior density estimates of parameters estimated for masked palm civets (Paguma larvata) in Laohegou Nature Reserve.
ParameterPosterior MeanPosterior SD95% Lower
HPD Level		95% Upper
HPD Level
σ574.458.0464.7687.5
λ00.1190.0300.0640.178
ψ0.0800.0150.0510.109
Nsuper (individuals)821357107
D (individuals/km2)1.6500.2661.1442.147
The following parameters were defined in SPACECAP [39]: σ, the range parameter of masked palm civets; λ0, the intercept of the expected encounter frequency; ψ, the fraction of the maximum allowable number; Nsuper, the population size for the state space; and D, the density measured per km2.
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Wang, D.; Zhang, D.; Bu, H.; Hopkins, J.B., III; Xiong, M.; Wang, D.; Yao, M.; Li, S.; Wang, R. Estimating the Population Size of Masked Palm Civets Using Hair-Snaring in Southwest China. Diversity 2024, 16, 421. https://doi.org/10.3390/d16070421

AMA Style

Wang D, Zhang D, Bu H, Hopkins JB III, Xiong M, Wang D, Yao M, Li S, Wang R. Estimating the Population Size of Masked Palm Civets Using Hair-Snaring in Southwest China. Diversity. 2024; 16(7):421. https://doi.org/10.3390/d16070421

Chicago/Turabian Style

Wang, Di, Dan Zhang, Hongliang Bu, John B. Hopkins, III, Mengyin Xiong, Dajun Wang, Meng Yao, Sheng Li, and Rongjiang Wang. 2024. "Estimating the Population Size of Masked Palm Civets Using Hair-Snaring in Southwest China" Diversity 16, no. 7: 421. https://doi.org/10.3390/d16070421

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