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International Journal for Parasitology: Parasites and Wildlife logoLink to International Journal for Parasitology: Parasites and Wildlife
. 2023 Feb 24;20:162–169. doi: 10.1016/j.ijppaw.2023.02.005

A snapshot of climate drivers and temporal variation of Ixodes ovatus abundance from a giant panda living in the wild

Xueyang Fan a,1, Rui Ma a,1, Changjuan Yue a, Jiabin Liu a, Bisong Yue b, Wanjing Yang a, Yunli Li a, Jiang Gu a, James E Ayala a, Daniel E Bunker c, Xia Yan a, Dunwu Qi a, Xiaoyan Su a, Lin Li a, Dongsheng Zhang a, Hongwen Zhang a, Zhisong Yang d,∗∗, Rong Hou a,∗∗∗, Songrui Liu a,∗
PMCID: PMC9986245  PMID: 36890989

Abstract

Ticks and tick-borne diseases have negative impacts on the health of wild animals including endangered and vulnerable species. The giant panda (Ailuropoda melanoleuca), a vulnerable and iconic flagship species, is threatened by tick infestation as well. Not only can ticks cause anemia and immunosuppression in the giant panda, but also bacterial and viral diseases. However, previous studies regarding tick infestation on giant pandas were limited in scope as case reports from sick or dead animals. In this study, an investigation focusing on the tick infestation of a reintroduced giant panda at the Daxiangling Reintroduction Base in Sichuan, China was conducted. Ticks were routinely collected and identified from the ears of the giant panda from March to September in 2021. A linear model was used to test the correlation between tick abundance and climate factors. All ticks were identified as Ixodes ovatus. Tick abundance was significantly different among months. Results from the linear model showed temperature positively correlated to tick abundance, while air pressure had a negative correlation with tick abundance. To the best of our knowledge, this study is the first reported investigation of tick species and abundance on a healthy giant panda living in the natural environment, and provides important information for the conservation of giant pandas and other species sharing the same habitat.

Keywords: Tick, Ixodes ovatus, Ailuropoda melanoleuca, Reintroduction

Abbreviations: 16s rRNA, 16S ribosomal RNA; AIC, Akaike information criterion; ANOVA, Analysis of variance; BLAST, Basic local alignment search tool; CI, Confidence interval; COI, Coxidase subunit I; HSD, Honest significant differences; NCBI, National center for biotechnology Information; VIF, Variance inflation factors

Graphical abstract

Image 1

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Highlights

  • •

    Tick species and abundance from a giant panda living in the wild were systematically investigated for the first time.

  • •

    Climate drivers were correlated with the Ixodes ovatus daily abundance on a giant panda living in the wild.

  • •

    Ixodesovatus abundance on a giant panda varies among months.

1. Introduction

Ticks are blood-sucking ectoparasites of many vertebrate animals including mammals (Rodríguez et al., 2018). Their feeding behavior can cause indirect effects on hosts such as anemia and immunosuppression. The wounds of hosts after tick biting may result in a secondary infection of bacterial pathogens (Alanazi et al., 2019). Ticks are also arthropod vectors of various pathogens such as bacterial pathogens including Anaplasma spp., Borrelia spp., Coxiella spp., Ehrlichia spp., Rickettsia spp. (Mendoza-Roldan et al., 2021; Sugimoto et al., 2017), protozoan parasites including piroplasmids (Alvarado-Rybak et al., 2016), and veterinary viruses including parvoviruses (Yang et al., 2023), which threaten not only domestic and wild animals, but also human health. Within this area of investigation, a number of studies revealed the threats of ticks and tick-borne disease to wild species (Castellaw et al., 2011; Dantas-Torres et al., 2012) including endangered and vulnerable animals (Dantas-Torres et al., 2011; Khatri-Chhetri et al., 2016). The infestation of ticks therefore has been linked to the decline of the wild population of some species such as black rhino (Diceros bicornis) and moose (Alces alces) (Jones et al., 2019; Nijhof et al., 2003). In those studies, most of the mortalities were correlated to tick infestations or tick-borne diseases.

To make matters worse, the range of tick activity seems to be extending as a result of climate change. Ostfeld and Brunner (2015) reviewed the distribution of ticks in Europe and indicated this trend. Other studies also observed the seasonal effect of environmental factors on tick abundance (Alanazi et al., 2019; Hauck et al., 2020; Yu et al., 2011). Therefore, it is necessary to evaluate the impacts of tick infestation on endangered and vulnerable animals, especially in small isolated populations, to prevent large-scale outbreaks.

The giant panda (Ailuropoda melanoleuca) is recognized as a flagship species and one of the most iconic species for nature conservation. Giant pandas are distributed in six mountain ranges: Minshan, Qionglai, Qinling, Liangshan, Daxiangling, and Xiaoxiangling, mainly in southwestern China (Zhu et al., 2011). Although the conservation status of the giant panda has been downgraded from “endangered” to “vulnerable” (Swaisgood et al., 2016), they are still threatened by even more severe habitat loss and fragmentation (Xu et al., 2017; Connor et al., 2022). Small isolated populations caused by the habitat fragmentation are particularly vulnerable to environmental factors, including disease and parasite outbreaks.

Previous studies on ticks have relied primarily on the investigation of sick or dead giant pandas. To date, 13 tick species were reported from giant pandas including nine Haemaphysalis spp., three Ixodes spp., and one Dermacentor sp. (Wang et al., 2018). In the past, clinical symptoms like anemia, inflammation, and exhaustion were considered the result of tick infestations (Li et al., 2020). Recently, Babesia sp., a blood parasite that is transmitted by ticks, was reported on a giant panda, which caused a series of symptoms (Yue et al., 2020). Because of the rarity of this species, it is difficult to investigate tick infestation pattern directly from wild pandas. Furthermore, it is very rare that healthy wild giant pandas are anesthetized, which makes collecting ticks consistently from pandas in the wild environment very difficult.

Tick infestation may not only affect wild giant pandas but captive individuals and individuals in reintroduction programs as well. Reintroduction of giant pandas is considered an effective strategy to prevent the decline of small natural populations by translocating individuals to their original geographic ranges (Hong et al., 2019; Nadler et al., 2019). The release of captive born giant pandas into these areas exposes these animals to different natural threats, including tick infestation and must be considered in the case of wildlife reintroductions. For endangered and vulnerable species, the number of animals used for reintroductions are often limited for the purpose of better monitoring and protection (Hong et al., 2019; Nadler et al., 2019). According to Hong et al. (2019), there were only 11 giant pandas released between 2005 and 2018, with two individuals at most in each reintroduction. Nevertheless, despite the limited number of reintroduced animals, in depth studies regarding individual giant pandas living in the wild environment are still valuable and illuminating for the conservation of the species (Yang et al., 2018).

All in all, evaluating the potential threats of ticks on giant pandas in the natural environment is vital both for providing better protection for the small isolated wild populations of this species and to provide additional information for the conservation management including reintroductions. To further safeguard giant pandas, it is necessary to understand the relationship of ticks and giant pandas in the natural environment including the species and seasonal population of ticks that may affect this vulnerable species. In this study, a free-living giant panda undergoing reintroduction training was monitored for tick infestation pattern in the wild environment at the Daxiangling Reintroduction Base in Sichuan, China across seasons for the first time.

2. Material and methods

2.1. Experimental site and animal information

This study occurred in an 0.25 km2 prerelease acclamation area that was enclosed within an iron fence in the Daxiangling Reintroduction Base (29°33′55.076″N–29°32′50.474″N, 102°50′13.866″E−102°51′3.189″E, altitude:1998–2500m) within the Daxiangling Natural Reserve in southwestern China. This reserve is a part of the recently established Giant Panda National Park which is the natural habitat of giant pandas (Huang et al., 2020) (Fig. 1). Mixed coniferous and broad-leaved forest dominate the landscape in this site. A weather station close to the site (29°33′43.31″N, 102°51′2.46″E) recorded climate information during this study. Climate factors including temperature (°C), Solar radiation (W/m2), gust speed (m/s), precipitation (mm) and pressure (KPa) were collected hourly from the weather station. The daily average values of climate factors were calculated for further analysis.

Fig. 1.

Fig. 1

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Experimental site was located in Daxiangling Natural Reserve, which is a part of the Giant Panda National Park in China. The orange area indicates the range of the Giant Panda National Park. The blue star is the location of this experimental site. Continents outline maps by Vemaps.com. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

The subject of this study was a captive-born adult female giant panda. As part of the human-assisted soft reintroduction program of the Chengdu Research Base of Giant Panda Breeding (CRBGPB), this giant panda was habituated to allow the CRBGPB reintroduction team to place and routinely check a GPS collar, as well allow body examinations. The giant panda was in good health and not under any veterinary treatment during the sample period. It was allowed to roam freely and forage naturally within the study area.

2.2. Sample collection and identification

The giant panda body was checked on a daily rotation schedule. Ticks were collected and reported by the CRBGPB reintroduction team if access to the panda was possible. To ensure the health and natural behavior of the panda, anesthesia was not used during the experiment. Therefore, all the routine physical examinations of this panda were done while the animal was awake. As a result, only the head, including face, ears, and neck, were accessible for the tick investigation. All the ticks on the head area were collected and were stored on dry ice in the field and then transferred to −20 °C in the lab, and then eventually stored at −80 °C. Tick species and sex identification and population counting were done in lab.

Thirty ticks were selected randomly from 1425 individuals for species identification by both the morphological method (Guo et al., 2016) and by using Coxidase Subunit I (COI) and 16s rRNA with Basic local alignment search tool (BLAST) using The National Center for Biotechnology Information (NCBI) (Altschul et al., 1990). After the reliability of morphological identification was verified, the remaining samples were identified with the morphological method alone.

2.3. Statistical analysis

Due to the fact that the giant panda was free-ranging in the study area and could not always be examined for numerous reasons, such as poor weather conditions, the rolling average value was used to make up for lost sample data that could not be collected. This method has been used in previous research under similar conditions (Dalziel et al., 2021; Freeman et al., 2022; Hauser et al., 2018; Singleton et al., 2019). We used a five-day rolling average value (the average value of previous four days and current date) of both tick abundance and climate data in the analysis.

The difference of tick abundance, female-to-male sex ratio and climate data among months were tested with ANOVA test by “aov” function in R statistical software (version 4.1.2) (R Core Team, 2013). A Tukey Honest Significant Differences (HSD) was conducted as the post-hoc test done by the “multcom” R package (Hothorn et al., 2008).

A linear regression model was used to explore the correlation between climate factors and the abundance of ticks by the “lm” function of R (R Core Team, 2013). We used “step” function to select the best fitted model by dropping independent factors and selecting the model with the lowest Akaike information criterion (AIC). The significance of climate factors in the final model were tested with a t-test method done by “summary” function in the stats package in R. The correlation between female-to-male sex ratio and climate factors was tested as well. Significance test between female and male ticks was done with Welch t-test in R. All analyses met the assumptions of homoscedasticity and normality and were log-transformed where necessary. The effects of correlations between environmental variables on variance inflation factors (VIF) was evaluated, and only non-correlated variables with VIF lower than five were used in the final linear model.

3. Results

3.1. Tick identification and abundance

A total of 1425 ticks were found and collected from the giant panda's ears between March 5th and September 30th in 2021 while none were found on the other parts of the head. Only adult ticks were found. The research team reported the investigation of ticks for 162 days during the total eight-month experiment (Table 1). Thirty ticks were randomly selected and identified by using both COI and 16s rRNA barcodes and showed that all of the tested ticks are Ixodes ovatus. Morphological traits agreed with the molecular identification. The remaining samples were all then identified as I. ovatus morphologically (Fig. 2). Daily average tick abundance was 6.78 (95% CI: 6.17–7.39) including 1.79 daily males (95% CI: 1.61–1.98) and 4.99 for females (95% CI: 4.53–5.44).

Table 1.

The average daily tick abundance among months in 2021.

Months Days (with tick data collected) Average daily tick abundance Daily tick abundance range with 95% CI
March 21 3.29 1.66–4.91
April 24 6.58 3.95–9.22
May 23 10.87 6.27–15.47
June 26 12.96 6.98–18.95
July 26 11.85 8.06–15.63
August 18 10.39 5.93–14.85
September 24 4.83 3.03–6.63
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Fig. 2.

Fig. 2

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Ixodes. ovatus collected from the giant panda. A: Dorsal of the adult female I. ovatus; B: Ventral of the adult female I. ovatus; C: Dorsal of the adult male I. ovatus; D: Ventral of the adult male I. ovatus.

Daily tick abundance was significantly different among months (F (6, 203) = 26.8, P < 0.01). Tick abundance increased from March to June and reached the highest point in June and July, and then decreased in the following months. June and July together have the highest average value (10.50 ticks per day) that was significantly higher than the average tick abundance in March–April (3.76 ticks per day) and August–September (5.01 ticks per day) (Fig. 3A).

Fig. 3.

Fig. 3

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Boxplot of tick abundance, female-to-male ratio and important climate factors change by months. A: Tick daily abundance; B: Daily female-to-male ratio of ticks; C: Daily temperature; D: Daily air pressure. Variables sharing the same letters among months were not significantly different. The five-day-rolling average values were calculated for all the variables that change by months.

3.2. Tick abundance and climate factors

After evaluating the VIF value and excluding the variables with collinearity, we tested two full regression models: “Tick daily abundance ∼ Temperature + Solar radiation + Gust speed + Precipitation + Pressure”, and “Tick sex ratio ∼ Temperature + Solar radiation + Gust speed + Precipitation + Pressure”.

We found no significant correlation between the sex ratio of ticks and climate factors. A linear model of daily abundance of ticks and climate factor was selected: “Tick daily abundance ∼ Temperature + Pressure”.

Temperature and air pressure were the important climate factors for this model (F (2, 207) = 29.03, P < 0.001). The tick daily abundance was positively correlated with temperature (Coefficient = 0.37, R2 = 0.140, t = 6.22, P < 0.001) but negatively correlated with the air pressure (Coefficient = −5.87, R2 = 0.087, t = − 4.49, P < 0.001) (Fig. 4, Fig. 5, Fig. 6). During this study, the average daily temperature was 10.9 °C (95% CI: 10.28 °C–11.53 °C), while the average daily air pressure was 76.11 KPa (95% CI: 76.09 KPa–76.14 KPa). The daily temperature was significantly different among months. It increased from March to July until reaching the highest point in July and August (average temperature: 15.13 °C; 95% CI: 14.78 °C–15.49 °C), then it decreased in September (Fig. 2C). The air pressure was relatively stable, there were no significant changes from March to August until a decline in September (Fig. 2D).

Fig. 4.

Fig. 4

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The correlation plot of daily tick abundance and the daily temperature with the trending line. The five-day-rolling average values were calculated for tick abundance and temperature.

Fig. 5.

Fig. 5

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The correlation plot of daily tick abundance and the daily air pressure with trending line. The five-day-rolling average values were calculated for tick abundance and the air pressure.

Fig. 6.

Fig. 6

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Daily average tick abundance, daily average air pressure and daily average temperature with standard deviations by months. All the values are calculated with five-day-rolling average values.

The daily abundance of male ticks (average value: 1.79, 95% CI: 1.61–1.98) was significantly lower than female ticks (average value: 4.99, 95% CI: 4.53–5.44) through months during this study (t = − 12.81, P < 0.001). The female-male sex ratio of ticks in July was significantly higher than March and August, while sex ratio of ticks in August was significantly lower than April and May. However, there was no obvious trend of the sex ratio by months (Fig. 2B).

4. Discussion

Many endangered and vulnerable species are threatened by tick biting and tick-borne diseases (Hart and Hart, 2018). Giant pandas are one of the most iconic and recognizable wild animal species in nature conservation, and understanding the impacts of ticks and tick-borne diseases on these animals, particularly in the small isolated populations, is of utmost importance. However, a limited number of studies have addressed the effects of ticks on giant pandas. Most of the previous studies regarding ticks and giant pandas were limited as forms of case reports of dead or diseased individuals and lack a systematic investigation in a wild environment. In this study, we conducted a survey of tick abundance on one giant panda undergoing reintroduction training over seven tick-active months in 2021.

In this research, we found all the ticks from the ears of the giant panda were I. ovatus. Although there were multiple tick species frequently reported on animals, a number of cases found that animals can be infested by a single tick species. For example, a survey of tick abundance on American black bears (Ursus americanus) found that all 1976 ticks collected from multiple areas of 278 black bears were identified as I. scapularis (Tiffin et al., 2021). An early case reported more than 2000 ticks as Haemaphysalis warburtoni from a two-year old giant panda in a natural reserve in Sichuan, China (Wu and Hu, 1985). Although one meta-analysis study showed that a larger host body size may correlate to a higher diversity of ticks in the neotropics (Esser et al., 2016), that study only included data from the neotropical area and did not consider the tick distribution on host body locations.

A study by Tadesse et al. (2012) investigating tick species diversity on cattle revealed a significant difference across body parts, with only 1.6% of the total tick species found on the ears. Another investigation of tick distribution found that tick species were specifically located on the different body parts of horses (Tirosh-Levy et al., 2018). In that study, only the Rhipicephalus spp. were reported in the ear area of horses. Regarding the life stage of ticks, according to previous studies, adult ticks were usually found from mammals with medium to large body size (Bouchard et al., 2013). For example, 98% and 100% of I. scapularis collected from the ear area and upper spine of black bears were adults (Tiffin et al., 2021). In our study, all the ticks were collected from the ear area of the giant panda and identified as adults. This finding agrees with the parasitical pattern of ticks’ behavior on large mammals in previous studies.

Ixodes ovatus was the only tick species found in this study. This species was previously reported in Southern and Southeast Asia, including China, in which samples were collected within a wide altitudinal range from 1400 m to 4600 m in multiple studies (Hoogstraal et al., 1973). In our study, the giant panda lived in the wild environment from 1998 m to 2500 m, which is the natural altitudinal range for I. ovatus as documented.

Ixodes ovatus were mostly reported parasitizing domestic and wild mammals including the Bovidae family (cattle, buffalo and goat), rodents, cats, dogs, bears and human (Hoogstraal et al., 1973). To the best of our knowledge, only one other case previously reported I. ovatus on giant pandas and was reported from one dead giant panda in 1987 in Ganxu province, China (Ma, 1987). In that case, 103 various ticks were collected in total but only two of them were identified as I. ovatus. However, in that study, the location was in the northwest of China, which is not in the same area to our current research site.

In our research, the average daily abundance of I. ovatus increased over time from March to June, then decreased until September. One previous investigation of the seasonal activity of I. ovatus in a natural environment (Fujimoto, 1996), using mark-recapture methods on ticks, found adult I. ovatus showed high activity from April to mid-July, but decreased significantly in late August. These results showed tick activity peaked in June, which matches the abundance pattern of I. ovatus collected from the giant panda in our study.

Multiple factors may affect the activity of I. ovatus. Previous research that examined I. ovatus activity in an experimental environment found an increasing activity from April to June followed by a sharp decreasing after June (Fujimoto, 1997). In that study, ticks were put into plastic cylinders that were placed outdoors where adults were not exposed to sunlight and rain. Another study about the oviposition and development of I. ovatus showed that 17–25 °C was the optimal range for the egg hatching and development of I. ovatus (Fujimoto, 1989). However, they only tested five temperatures (15, 17, 20, 25, 27 and 30 °C). In our study, the average daily temperature was 10.9 °C (95% CI: 10.28 °C–11.53 °C). Even in the months with highest temperature range (15.13 °C; 95% CI: 14.78 °C–15.49 °C), the temperature was lower than the highest point of the optimal temperature tested in that previous study. Studies about other Ixodid species showed that the temperature positively corresponded to the activity of questing ticks (Li et al., 2012; Schwarz et al., 2009). Therefore, our results showed that the chance for I. ovatus to actually get on giant pandas may be positively correlated to the temperature. Furthermore, the chance for the giant panda to get I. ovatus may be even higher in environments with higher temperatures.

Our study showed a negative correlation between average tick abundance and daily air pressure (R2 = 0.087, P < 0.001). One previous investigation found that the cases of severe fever with thrombocytopenia syndrome, one tick-borne disease, negatively correlated to the monthly average air pressure (Wang et al., 2022), which indicated the negative effect of air pressure on tick activity.

The results of this study are limited in scope due to the fact that data was collected from only one individual giant panda, therefore, the variation of tick infestation among host giant pandas was not tested. It should be noted though that the reintroductions of medium to large bodied animals are often characterized by small sample sizes and therefore data from these individuals are still useful (Taylor et al., 2017). To increase the reliability of the result in this study and to neutralize the daily data fluctuation caused by chance, a consistent investigation about tick infestation was conducted through six months. The temporal pattern of the abundance of I. ovatus and its correlation to the temperature and air pressure matches the previous studies in both laboratory and field settings. Despite the limitation of the sample size of hosts, this study aimed to provide information by investigating the species, potential effective climate factors, and temporal variation of tick abundance during the reintroduction of giant pandas, providing valuable information for the conservation and management of this vulnerable species (Canessa et al., 2016; Taylor et al., 2017).

Ixodes ovatus is the important disease vector transmitting multiple pathogens including Rickettsia, Ehrlichia, Anaplasma, Borrelia, Babesia and Theileria in the East Asia (Shimada et al., 2003). A high level of Babesia was recently detected from one female giant panda with the associated severe symptoms of fever, anemia, jaundice and hemoglobinuria (Yue et al., 2020). In addition, the Babesia found on the giant panda in that study was genetically close to the Babesia strains found from Ixodes ovatus on Japanese black bears (Ursus thibetanus japonicus) (Ikawa et al., 2011), which may indicate a specification pattern of vectors. Further study about the correlation among hosts, Ixodes ovatus and pathogens is needed to reveal this potential specification.

5. Conclusions

Our study directly investigated for the first time the tick species and pattern of abundance on a giant panda in a wild environment. We found that adult I. ovatus was the only tick species collected from the ear area of the giant panda. The pattern of the abundance of I. ovatus agreed with previous studies of this tick species. Among environmental factors, temperature was positively correlated to tick abundance, while air pressure was negatively correlated to tick abundance. This study revealed the activity of I. ovatus on a giant panda living in the natural environment. Compared to the previous records of ticks on giant pandas, this current study provided new information about tick species and abundance on a living individual, which suggests that the strategy of giant panda conservation should consider tick activity and abundance, especially in regards to reintroduction. In summary, this study provides knowledge for the conservation and reintroduction of giant pandas in Sichuan, China as well as other wild animals that are threatened by tick and tick-borne diseases.

Declaration of competing interest

No potential conflict of interest was reported by authors.

Acknowledgements

This study was supported by Chengdu Research Base of Giant Panda Breeding, China (2021CPB-B16), the National Natural Science Foundation of China (U21A20193) and the National Forestry and Grassland Administration and Sichuan Province Finance Department, China (project title: study on main epidemiological investigation and prevention of giant panda). We also appreciate the reintroduction team of Chengdu Research Base of Giant Panda Breeding, Daxiangling Natural Reserve and Yingjing management and Protection Station of giant panda National Park and staffs from Chengdu Research Base of Giant Panda Breeding for the support on research and administration.

Contributor Information

Zhisong Yang, Email: yangzhisong@126.com.

Rong Hou, Email: 405536517@qq.com.

Songrui Liu, Email: srui_liu@163.com.

References

  1. Alanazi A.D., Al-Mohammed H.I., Alyousif M.S., Said A.E., Salim B., Abdel-Shafy S., Shaapan R.M. Species diversity and seasonal distribution of hard ticks (Acari: Ixodidae) infesting mammalian hosts in various districts of Riyadh Province, Saudi Arabia. J. Med. Entomol. Suppl. 2019;56:1027–1032. doi: 10.1093/jme/tjz036. [DOI] [PubMed] [Google Scholar]
  2. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  3. Alvarado-Rybak M., Solano-Gallego L., Millán J. A review of piroplasmid infections in wild carnivores worldwide: importance for domestic animal health and wildlife conservation. Parasites Vectors. 2016;9:1–19. doi: 10.1186/s13071-016-1808-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bouchard C., Leighton P., Beauchamp G., Nguon S., Trudel L., Milord F., Lindsay L., Bélanger D., Ogden N. Harvested white-tailed deer as sentinel hosts for early establishing Ixodes scapularis populations and risk from vector-borne zoonoses in southeastern Canada. J. Med. Entomol. 2013;50:384–393. doi: 10.1603/ME12093. [DOI] [PubMed] [Google Scholar]
  5. Canessa S., Guillera-Arroita G., Lahoz-Monfort J.J., Southwell D.M., Armstrong D.P., Chadès I., Lacy R.C., Converse S.J. Adaptive management for improving species conservation across the captive-wild spectrum. Biol. Conserv. 2016;199:123–131. doi: 10.1016/j.biocon.2016.04.026. [DOI] [Google Scholar]
  6. Castellaw A.H., Chenney E.F., Varela-Stokes A.S. Tick-borne disease agents in various wildlife from Mississippi. Vector Borne Zoonotic Dis. 2011;11:439–442. doi: 10.1089/vbz.2009.0221. [DOI] [PubMed] [Google Scholar]
  7. Connor T., Qiao M., Scribner K., Zhang J., Hull V., Bai W., Shortridge A., Li R., Zhang H., Liu J. Complex effects of habitat amount and fragmentation on functional connectivity and inbreeding in a giant panda population. Biol. Conserv. 2022;36 doi: 10.1111/cobi.13828. [DOI] [Google Scholar]
  8. Dalziel B.D., Novak M., Watson J.R., Ellner S.P. Collective behaviour can stabilize ecosystems. Nat. Ecol. Evol. 2021;5:1435–1440. doi: 10.1038/s41559-021-01645-3. [DOI] [PubMed] [Google Scholar]
  9. Dantas-Torres F., Chomel B.B., Otranto D. Ticks and tick-borne diseases: a One Health perspective. Trends Parasitol. 2012;28:437–446. doi: 10.1016/j.pt.2012.07.003. [DOI] [PubMed] [Google Scholar]
  10. Dantas-Torres F., Testini G., DiGeronimo P.M., Lorusso V., Mallia E., Otranto D. Ticks infesting the endangered Italian hare (Lepus corsicanus) and their habitat in an ecological park in southern Italy. Exp. Appl. Acarol. 2011;53:95–102. doi: 10.1007/s10493-010-9387-3. [DOI] [PubMed] [Google Scholar]
  11. Esser H.J., Foley J.E., Bongers F., Herre E.A., Miller M.J., Prins H.H., Jansen P.A. Host body size and the diversity of tick assemblages on Neotropical vertebrates. Int. J. Parasitol. Parasites Wildl. 2016;5:295–304. doi: 10.1016/j.ijppaw.2016.10.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Freeman G., Matthews E., Stehr E., Acevedo-Gutiérrez A. Individual variability in foraging success of a marine predator informs predator management. Sci. Rep. 2022;12:1–11. doi: 10.1038/s41598-022-15200-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fujimoto K. Ecological studies on ixodid ticks: 6. The effects of temperature on the oviposition, development and survival of Ixodes ovatus Neumann (Acarina: Ixodidae) Med. Entomol. Zool. 1989;40:187–193. doi: 10.7601/mez.40.187. [DOI] [Google Scholar]
  14. Fujimoto K. Effect of repeated removal in a survey of the seasonal activity of Ixodes ovatus adults (Acari: Ixodidae) by the flagging method. Med. Entomol. Zool. 1996;47:375–377. doi: 10.7601/mez.47.375. [DOI] [Google Scholar]
  15. Fujimoto K. Disappearance of Ixodes ovatus adults (Acari: Ixodidae) in autumn clarified by analysis of field and experimental studies. Med. Entomol. Zool. 1997;48:275–278. doi: 10.7601/mez.48.275. [DOI] [Google Scholar]
  16. Guo Y., Sun Y., Xu R. The genus Ixodes (Acari: Ixodidae) in China with three new record species. Acta Parasitol. 2016;61:729–742. doi: 10.1515/ap-2016-0102. [DOI] [PubMed] [Google Scholar]
  17. Hart B.L., Hart L.A. How mammals stay healthy in nature: the evolution of behaviours to avoid parasites and pathogens. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2018;373 doi: 10.1098/rstb.2017.0205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hauck D., Springer A., Chitimia-Dobler L., Strube C. Two-year monitoring of tick abundance and influencing factors in an urban area (city of Hanover, Germany) Parasites Vectors. 2020;11 doi: 10.1016/j.ttbdis.2020.101464. [DOI] [PubMed] [Google Scholar]
  19. Hauser G., Rais O., Morán Cadenas F., Gonseth Y., Bouzelboudjen M., Gern L. Influence of climatic factors on Ixodes ricinus nymph abundance and phenology over a long-term monthly observation in Switzerland (2000–2014) Parasites Vectors. 2018;11:1–12. doi: 10.1186/s13071-018-2876-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hong M., Wei W., Zhou H., Tang J., Han H., Zhang Z. Creative conservation in China: releasing captive giant pandas into the wild. Environ. Sci. Pollut. Res. 2019;26:31548–31549. doi: 10.1007/s11356-019-06384-4. [DOI] [PubMed] [Google Scholar]
  21. Hoogstraal H., Clifford C.M., Saito Y., Keirans J.E. Ixodes (Partipalpiger) ovatus Neumann, subgen. nov.: identity, hosts, ecology, and distribution (Ixodoidea: Ixodidae) J. Med. Entomol. 1973;10:157–164. doi: 10.1093/jmedent/10.2.157. [DOI] [PubMed] [Google Scholar]
  22. Hothorn T., Bretz F., Westfall P. Simultaneous inference in general parametric models. Biom. J. 2008;50:346–363. doi: 10.1002/bimj.200810425. [DOI] [PubMed] [Google Scholar]
  23. Huang Q., Fei Y., Yang H., Gu X., Songer M. Giant Panda National Park, a step towards streamlining protected areas and cohesive conservation management in China. Glob. Ecol. Conserv. 2020;22 doi: 10.1016/j.gecco.2020.e00947. [DOI] [Google Scholar]
  24. Ikawa K., Aoki M., Ichikawa M., Itagaki T. The first detection of Babesia species DNA from Japanese black bears (Ursus thibetanus japonicus) in Japan. Parasitol. Int. 2011;60:220–222. doi: 10.1016/j.parint.2011.02.005. [DOI] [PubMed] [Google Scholar]
  25. Jones H., Pekins P., Kantar L., Sidor I., Ellingwood D., Lichtenwalner A., O'Neal M. Mortality assessment of moose (Alces alces) calves during successive years of winter tick (Dermacentor albipictus) epizootics in New Hampshire and Maine (USA) Can. J. Zool. 2019;97:22–30. doi: 10.1139/cjz-2018-0140. [DOI] [Google Scholar]
  26. Khatri-Chhetri R., Wang H.-C., Chen C.-C., Shih H.-C., Liao H.-C., Sun C.-M., Khatri-Chhetri N., Wu H.-Y., Pei K.J.-C. Surveillance of ticks and associated pathogens in free-ranging Formosan pangolins (Manis pentadactyla pentadactyla) Ticks Tick Borne Dis. 2016;7:1238–1244. doi: 10.1016/j.ttbdis.2016.07.007. [DOI] [PubMed] [Google Scholar]
  27. Li J., Karim M.R., Li J., Zhang L., Zhang L. Review on parasites of wild and captive giant pandas (Ailuropoda melanoleuca): diversity, disease and conservation impact. Int. J. Parasitol. Parasites Wildl. 2020;13:38–45. doi: 10.1016/j.ijppaw.2020.07.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Li S., Heyman P., Cochez C., Simons L., Vanwambeke S.O. A multi-level analysis of the relationship between environmental factors and questing Ixodes ricinus dynamics in Belgium. Parasites Vectors. 2012;5:1–11. doi: 10.1186/1756-3305-5-149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Ma G. Record of giant panda roundworm and ticks collected in Wenxian of Gansu Province. Sichuan. J. Zool. 1987;6:34. (In Chinese) [Google Scholar]
  30. Mendoza-Roldan J.A., Mendoza-Roldan M.A., Otranto D. Reptile vector-borne diseases of zoonotic concern. Int. J. Parasitol. Parasites Wildl. 2021;15:132–142. doi: 10.1016/j.ijppaw.2021.04.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nadler T., Van Tuan B., Huy H.Q. Unexpected incidents during reintroduction of Hatinh langurs (Trachypithecus hatinhensis) Vietnam. J. Primatol. 2019;3:27–40. doi: 10.1007/s11356-019-06384-4. [DOI] [Google Scholar]
  32. Nijhof A.M., Penzhorn B.L., Lynen G., Mollel J.O., Morkel P., Bekker C.P., Jongejan F. Babesia bicornis sp. nov. and Theileria bicornis sp. nov.: tick-borne parasites associated with mortality in the black rhinoceros (Diceros bicornis) J. Clin. Microbiol. 2003;41:2249–2254. doi: 10.1016/j.ijppaw.2021.04.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Ostfeld R.S., Brunner J.L. Climate change and Ixodes tick-borne diseases of humans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2015;370 doi: 10.1098/rstb.2014.0051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Rodríguez Y., Rojas M., Gershwin M.E., Anaya J.-M. Tick-borne diseases and autoimmunity: a comprehensive review. J. Autoimmun. 2018;88:21–42. doi: 10.1016/j.jaut.2017.11.007. [DOI] [PubMed] [Google Scholar]
  35. Schwarz A., Maier W.A., Kistemann T., Kampen H. Analysis of the distribution of the tick Ixodes ricinus L.(Acari: Ixodidae) in a nature reserve of western Germany using Geographic Information Systems. Int. J. Hyg Environ. Health. 2009;212:87–96. doi: 10.1016/j.ijheh.2007.12.001. [DOI] [PubMed] [Google Scholar]
  36. Shimada Y., Inokuma H., Beppu T., Okuda M., Onishi T. Survey of ixodid tick species on domestic cats in Japan. Vet. Parasitol. 2003;111:231–239. doi: 10.1016/S0304-4017(02)00352-7. [DOI] [PubMed] [Google Scholar]
  37. Singleton D.A., McGarry J., Torres J.R., Killick D., Jewell C., Smyth S., Brant B., Sánchez-Vizcaíno F., Dawson S., Pinchbeck G.L. Small animal disease surveillance 2019: pruritus, pharmacosurveillance, skin tumours and flea infestations. Vet. Rec. 2019;185:470. doi: 10.1136/vr.l6074. [DOI] [PubMed] [Google Scholar]
  38. Sugimoto C., Thekisoe O., Mtshali K., Nakao R. Occurrence of Coxiella burnetii, Ehrlichia canis, Rickettsia species and Anaplasma phagocytophilum-like bacterium in ticks collected from dogs and cats in South Africa. J. S. Afr. Vet. Assoc. 2017;88:1–6. doi: 10.4102/jsava.v88i0.1390. https://hdl.handle.net/10520/EJC-9bec07993 [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Swaisgood R., Wang D., Wei F. A iluropoda melanoleuca (errata version published in 2017) The IUCN Red List of Threatened Species. 2016 doi: 10.2305/IUCN.UK.2016-2.RLTS.T712A45033386.en. 2016: e.T712A121745669. [DOI] [Google Scholar]
  40. Tadesse F., Abadfaji G., Girma S., Kumsa B., Jibat T. Identification of tick species and their preferred site on cattle's body in and around Mizan Teferi, Southwestern Ethiopia. J. Vet. Med. Anim. Health. 2012;4:1–5. doi: 10.5897/JVMAH11.039. [DOI] [Google Scholar]
  41. Taylor G., Canessa S., Clarke R.H., Ingwersen D., Armstrong D.P., Seddon P.J., Ewen J.G. Is reintroduction biology an effective applied science? Trends Ecol. Evol. 2017;32:873–880. doi: 10.1016/j.tree.2017.08.002. [DOI] [PubMed] [Google Scholar]
  42. Team R.C. 2013. R: A Language and Environment for Statistical Computing.https://www.R-project.org [Google Scholar]
  43. Tiffin H.S., Skvarla M.J., Machtinger E.T. Tick abundance and life-stage segregation on the American black bear (Ursus americanus) Int. J. Parasitol. Parasites Wildl. 2021;16:208–216. doi: 10.1016/j.ijppaw.2021.10.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Tirosh-Levy S., Gottlieb Y., Apanaskevich D.A., Mumcuoglu K.Y., Steinman A. Species distribution and seasonal dynamics of equine tick infestation in two Mediterranean climate niches in Israel. Parasites Vectors. 2018;11:1–10. doi: 10.1016/j.ijppaw.2021.10.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Wang T., Xie Y., Zheng Y., Wang C., Li D., Koehler A.V., Gasser R.B. Parasites of the giant panda: a risk factor in the conservation of a species. Adv. Parasitol. 2018;99:1–33. doi: 10.1016/bs.apar.2017.12.003. bs.apar.2017.12.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wang Z., Yang S., Luo L., Guo X., Deng B., Zhao Z., Rui J., Yu S., Zhao B., Wang Y. Epidemiological characteristics of severe fever with thrombocytopenia syndrome and its relationship with meteorological factors in Liaoning Province, China. Parasites Vectors. 2022;15:1–12. doi: 10.1186/s13071-022-05395-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Wu J., Hu H. Giant panda-the new host of Haemaphysalis warburtoni. Anim. Husb. Vet. Med. 1985;8:10. (In Chinese) [Google Scholar]
  48. Xu W., Viña A., Kong L., Pimm S.L., Zhang J., Yang W., Xiao Y., Zhang L., Chen X., Liu J. Reassessing the conservation status of the giant panda using remote sensing. Nat. Ecol. Evol. 2017;1:1635–1638. doi: 10.1038/s41559-017-0317-1. [DOI] [PubMed] [Google Scholar]
  49. Yang Z., Gu X., Nie Y., Huang F., Huang Y., Dai Q., Hu Y., Yang Y., Zhou X., Zhang H. Reintroduction of the giant panda into the wild: a good start suggests a bright future. Biol. Conserv. 2018;217:181–186. doi: 10.1016/j.biocon.2017.08.012. [DOI] [Google Scholar]
  50. Yang Z., Wang H., Yang S., Wang X., Shen Q., Ji L., Zeng J., Zhang W., Gong H., Shan T. Virome diversity of ticks feeding on domestic mammals in China. Virol. Sin. 2023 doi: 10.1016/j.virs.2023.02.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Yu Z., Zheng H., Yang X., Chen Z., Wang D., Hao M., Yang Y., Liu J. Seasonal abundance and activity of the tick Dermacentor silvarum in northern China. Med. Vet. Entomol. 2011;25:25–31. doi: 10.1111/j.1365-2915.2010.00916.x. [DOI] [PubMed] [Google Scholar]
  52. Yue C., Deng Z., Qi D., Li Y., Bi W., Ma R., Yang G., Luo X., Hou R., Liu S. First detection and molecular identification of Babesia sp. from the giant panda, Ailuropoda melanoleuca, in China. Parasites Vectors. 2020;13:1–8. doi: 10.1186/s13071-020-04412-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Zhu L., Zhang S., Gu X., Wei F. Significant genetic boundaries and spatial dynamics of giant pandas occupying fragmented habitat across southwest China. Mol. Ecol. 2011;20:1122–1132. doi: 10.1111/j.1365-294X.2011.04999.x. [DOI] [PubMed] [Google Scholar]

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