A Review of the Ecology and Biology of Chinese Pangolin（Manis pentadactyla）

Jingyu YU，Jianjun PENG，Jun ZENG，Xilin YlN，Jing ZHU

College of Life Sciences，Chongqing Normal University，Chongqing 401331，China

A Review of the Ecology and Biology of Chinese Pangolin（Manis pentadactyla）

Jingyu YU，Jianjun PENG*，Jun ZENG，Xilin YlN，Jing ZHU

College of Life Sciences，Chongqing Normal University，Chongqing 401331，China

Chinese pangolin （Manis pentadactyla）has important value in Chinese medicine，economy and ecology.At present，Chinese pangolin is about to go extinct due to over hunting and habitat destruction，which has caused a dramatic decline in the wild population.Breeding Chinese pangolin in captivity is very difficult and has not succeeded yet.This paper is to review the wild population，habitat，foraging，activity rhythm，breeding and physiology of Chinese pangolin.It provides theoretical basis of ecology and biology for the protection and artificial domestication of Chinese pangolin.Meanwhile，given the demands of protection，future research directions are suggested.

Chinese Pangolin（Manis pentadactyla）；Ecology；Biology；Protection

P angolin is one of the smallest groups in existing mammals（Mammalia），which belongs to the family Manidae in Pholidota（monotypic family and order）.It is one of the higher animal groups distributed in both Paleotropic realm and the Oriental realm［1-2］.The existing eight pangolin species in the world are mainly distributed in tropical and subtropical regions ofsoutheastern Asia and southern Africa.It is Chinese pangolin（Manis pentadactyla）that is mainly distributed in China，and a small number of Indian pangolin （M.crassicaudata）and Malaysian pangolin （M.javanica）are sporadically distributed in Yunnan Province in Southwestern China［1-4］.

Chinese pangolin has three subspecies:Taiwan subspecies（Manis pentadactyla pentadactyla），Hainan subspecies（Manis pentadactyla pusilla）and South China subspecies（Manis pentadactyla aurita），mainly distributed in Taiwan and Hainan islands，southern China and so on［5］.Chinese pangolin has been over hunted because of its great value as medicine and meal，and its habitat was also greatly destroyed，which led to a dramatic decline of wild population［6-7］. Chinese pangolin was listed under second class state protection in 1988 in China，and also was included in CITES（appendix II）in 1994［8］.At present，it is considered as a critically endangered species by the IUCN［9］.In order to protect the endangered species，it is necessary to carry out ecological and biological researches on Chinese pangolin.This paper reviewed the wild population，habitat，foraging，activity rhythm，breeding and physiology of Chinese pangolin.It provides theoretical basis of ecology for the habitat restoration，ex situ conservation and domestication of Chinese pangolin.

Research Progress

Wild population

Researcheshavenevermade long-term investigation and monitoring for wild populations of Chinese pangolin，because of the lack of appropriate methods.Cave counting is the only reliable method for measuring the wild population of Chinese pangolin at present［10-11］.Based on the previous record and survey data in the past 50 years，the population dynamic curve was plotted as Fig.1［6，12-14］.The population of Chinese pangolin has greatly decreased by 97%from 1960 to 2015. According to the survey by the State Forestry Administration of China in 1998，the population density of Chinese pangolin was only 0.000 134-0.056 individuals/km2，and such a low density is difficult to maintain a valid wildpopulation，which pushed the species to the edge of extinction.We inferred the ratio of male to female Chinese pangolins was 2:1 from the rescued wild pangolins in ten years from 1995 to 2004 in Taiwan［15-16］.The number of female Chinese pangolins is only one half of the male in the wild，which is perhaps another factors that leads to extinction.

Habitat and cave

Chinese pangolin inhabits shrubs and grasses on hilly mountains.They usually stay in the caves those they burrow for prey for one or two days，or a longer time period for finishing all the ants if they find a large anthill underground［17］.According to previous studies on the winter habitats and caves of wild Chinese pangolins in Dawuling Nature Reserve in Guangdong Province，as well as their different habitats and caves in Fujian Province and other localities，the optimal selection of habitats and caves by wild Chinese pangolin was summarized，as shown in Table 1［18-23］.However，all the researches involved only one subspeciesinGuangdongandFujian Province，the habitats of other subspecies or the same subspecies in different regions may differ.

The caves of Chinese pangolin have a simple structure with only one tunnel and one exit.In summer，theycreated burrows with a close distance from the ground （about 24-52 cm deep），because there are more ants in summer，they can easily get enough ants without digging deeper［20-22］.

In winter，Chinese pangolin created burrows over 60 cm deep from ground surface，with a large and commodious nest，which is bedded with soft grasses to keep warm.The temperature inside the winter caves is nearly constant does not change with the temperature outside［23］.Cave is the main residence for Chinese pangolin to live through the winter，so they often choose the place with moderate plant canopy density（about 50%）to make cave，so that they can get enough sunlight and the plants can conceal the entrance to the cave.We thought that Chinese pangolins might hibernate for a short period of time in winter，because （i）the food resources of ants and termites are insufficient in winter；（ii）they are easy to catch pneumonia and other diseases in winter because of significant temperature difference inside and outside the cave［15］；（iii）they can endure nesteia for long time in winter with lower metabolic rate and less energy consumption［24］.

Foraging and diet

Pangolin mainly feeds on termites and ants （accounting for more than 90%in its diet），occasionally feeds on larvae of some insects［25］.But it is difficult to observe the kinds of their food in the wild，because pangolins forage in the evening.The diet of wild pangolins is known only through the analysis of their stomach contents，feces and residual foods in deserted caves. The diet of wild Chinese pangolin has rarely reported.Two or three species of termites and ants were identified in several studies［20，26-27］，six species in the study of Liu and XU［17］，and as many as 12 species were reported in the studies of Wu et al［28-29］.The diet of Chinese pangolin was listed in Table 2.Macrotermes barneyi and Odontotermes formosanus have been repeatedly recorded for many times in the wild diet，which indicates that the two species are the key food to decide the distribution of wild Chinese pangolin.

By studying the diet of Chinese pangolin in captivity through the method of single food choice of living animals，Lu et al.［30］found that Chinese pangolin fed mainly on ant，then a smallquantity ofearthworms and hardly on yellow meal worm.Moreover，they also found that 50%fresh milk+45%ant powder+10%nutrition powder was the optimal artificial feed for Chinese pangolin.

Activity rhythms and behavior

Chinese pangolin is a nocturnal species，so there are some difficulties to observe its activity rhythm.Wireless radio was used to observe one adult Chinese pangolin for 7 d and one subadult for 12 d in 1986［31］.The results showed that they were mostly active at night，with a peak of activity at dusk，and stayed in the cave during the daytime.This is the only one report about daily activity rhythm of Chinese pangolin.Wu et al.［28］put forward an ethogram of foraging behaviors for Chinese pangolin after they went to observe the foraging activities of the wild pangolins in Dawuling Nature Reserve from 1985 to 2003，which mainly comprised walking，searching，digging，eating and pausing.It was recorded that pangolin used nose and snout plugging the tunnel of termites and ants，and ballooned the abdomen to exert itself to blow into hole，which may be used to detect the amount of termites and ants in the nest or the length of the tunnel［22］.

By observing the behaviors of Chinese pangolins in captivity，Wang［32］recorded their behaviors of feeding，sleeping，defecating，urinating，drinking，nesting and digging.Because it was very difficultto observe and record the behaviors of wild pangolins，all the behaviors of domesticated ones can provide reference for the comparative research of the behavior of pangolins in the wild.

Reproduction

The estrus and mating period of Chinese pangolin starts from April or May，lasts to late autumn［33］.During this period，the male crosses over mountain after mountain to look for a mate，and often defecates and urinates on the mountain ridge as well as scratches on the ground for luring the females［34］.The mating behavior in the wild occurs mostly in the evening or before dawn，and copulates outside the hole，the duration is approximate 3-5 min［20-21］.During the copulation，the male and female lie down with lateral position，their limbs clasping，heads swinging and tails twisting together. Several studies have recorded the born of Chinese pangolin［17，35-37］.There is no accurate conclusion to the pregnancy period of Chinese pangolin in the wild，and it is only recorded that the pregnancy period is at least 68 d for M. p.pentadactyla and at least 101 d for M.p.aurita.The cub is usually born in late winter to early spring with one or two cubs at a time［17，37］.M.p.auritamay give birth one or two times within one year［17］.Because only a few of samples have beenrecorded andscholars have different opinions，the reproductive parameters of Chinese pangolin are still controversial at present.

Table 1 Optimal selection of habitats and caves by wild Chinese pangolin

Physiology

Chinese pangolin is a burrowing mammal，so there are some difficul-ties to study its physiological metabolism in the wild.According to previous reports，we can clearly know that the metabolic rate of Chinese pangolin is very low［15，24］.It was reported that pangolin was suffocated to dead after being dipped in water for an hour［21］.This indicated that except for aquatic mammals，pangolin has the highest anaerobic tolerance among terrestrial mammals.The mechanism of breathing and hypoxia tolerance of Chinese pangolin can be studied in future work through comparative anatomy and physiology research.

Table 2 Diet of Chinese pangolin

Molecular biology and genetics

Pangolin had been classified under the order Xenarthra before，subsequently was classified to the order Pholidota.Dou et al.［39］analyzed the phylogenesis of Chinese pangolin by comparing the complete sequences of mitochondrial genome of Chinese pangolin （NC_016008）with that of 30 mammal species which were downloaded from GenBank.The results showed that Chinese pangolin was the sister branch of carnivore，which provided strong molecular evidence for classifying pangolin to an independent order.

The existing reports showed that Chinese pangolin had higher genetic diversity［40-41］.The reason may be that Chinese pangolin has a wide geographical distribution，and mountains and seas in the wide area caused geographical isolation.Chinese pangolin comprises three subspecies.Because less research has been done in its molecular genetics，whether it should be divided into more subspecies or species is still unclear.

Conclusion and Prospects

The research in ecology of Chinese pangolin is still at the preliminary stage.Due to the existing simple methods and few samples，the ecology of Chinese pangolin cannot be systemically and deeply studied to solve the problems in its conservation. Therefore，in the future more attention should be paid to following aspects:

Long-term monitoring of population dynamics

Various environmental factors influencing Chinese pangolin in the wild change continuously，so it is necessary to monitor the population dynamics of pangolin.Population number，sex-ratio，age structure，genetic diversity and so on are the key factors influencing population fecundity，and also are the key reference data to determine its protection grade.We should develop some more accurate methods for population investigation，which can be used to give a detailed census to the standing crop and sex-ratio of Chinese pangolin.Meanwhile，we should use advanced technology to research the genetic diversity of Chinese pangolin.

Evolution of diet

In the long-term co-evolution with pangolin，ants formed a series of defense mechanisms，such as:strengthening their attack power and making deeper and more covert caves.Meanwhile，pangolin also developed corresponding adaptation，such as:changing the species of ants and termites to eat and enhancing their ability to dig caves.The presentglobalclimate change will influence the survival of pangolins in the wild，and acclimatization of diet is also a big problem for artificial domestication of pangolin.Swart et al.［42］also discussed the maximum feeding benefit of M.temminckii and defense mechanisms of ants.Relevant research should be carried out by referring to previous studies.

Study on habitat

Rapid development of road，railway and tourism in China results in serious habitat fragmentation.Selection of optimal habitat has important significance to establish the nature reserves and off-site conservation for Chinese pangolin.

Study on breeding ecology

Previous reports on breeding parameters of Chinese pangolin are deficient without enough evidence. Breeding parameters are key factors influencing the population dynamics of Chinese pangolin，but the information of parental care and pregnancy is still uncertain.

Study on community ecology

There are many animals in the nature feeding on ants.However，how do pangolins co-exist with these animals at the same trophic level？And what are the ecological niche and function of Chinese pangolin in the community？Perhaps we can study their alternative ecological niche，such as swapping pangolin and armadillos can complement the corresponding function in the ecosystem.The community ecology of Chinese pangolin has not been reported yet，which is closely related to the living conditions of pangolin and evolution of ecosystems.

Study on domestication

At present，much attention has been paid to the reproduction of pangolin，but it is very difficult to breed and reproduce pangolin in captivity.So，it is necessary to carry out studies on artificial breeding and conservation biology for this species and establishvalid population of domesticated pangolins，and thus save this species from extinction and to achieve ecological restoration goals.

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Responsible editor：Qingqing YlN

Responsible proofreader：Xiaoyan WU

Supported by National Natural Science Foundation of China （31470570）；Chongqing Natural Science Foundation （cstc2014jcyjA80013）；Science Foundation of Chongqing Education Commission （kj1400534）；Chongqing Creative Program for Graduate Students（CYS15155）.

*Corresponding author.E-mail:jjpeng74@163.com

Received:September 28，2015 Accepted:November 12，2015