Review Article |
Corresponding author: Shiping Gong ( gsp621@163.com ) Academic editor: Pavel Stoev
© 2015 Liushuai Hua, Shiping Gong, Fumin Wang, Weiye Li, Yan Ge, Xiaonan Li, Fanghui Hou.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Hua L, Gong S, Wang F, Li W, Ge Y, Li X, Hou F (2015) Captive breeding of pangolins: current status, problems and future prospects. ZooKeys 507: 99-114. https://doi.org/10.3897/zookeys.507.6970
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Pangolins are unique placental mammals with eight species existing in the world, which have adapted to a highly specialized diet of ants and termites, and are of significance in the control of forest termite disaster. Besides their ecological value, pangolins are extremely important economic animals with the value as medicine and food. At present, illegal hunting and habitat destruction have drastically decreased the wild population of pangolins, pushing them to the edge of extinction. Captive breeding is an important way to protect these species, but because of pangolin’s specialized behaviors and high dependence on natural ecosystem, there still exist many technical barriers to successful captive breeding programs. In this paper, based on the literatures and our practical experience, we reviewed the status and existing problems in captive breeding of pangolins, including four aspects, the naturalistic habitat, dietary husbandry, reproduction and disease control. Some recommendations are presented for effective captive breeding and protection of pangolins.
Pangolin, captive breeding, dietary husbandry, disease, conservation
Pangolins, also known as scaly anteaters, are eutherians, and unique placental mammals. Despite fulfilling a similar ecological niche as anteaters and armadillos of the order Xenarthra, they are taxonomically distinct. There are eight existing species of pangolins in the world, and all are the class Mammalia, order Pholidota, family Manidae, and genus Manis. Pangolins mainly distribute in Eastern, Southeastern and Southern Asia, as well as most of Africa. Four species of pangolins are native to Africa, including the Cape Pangolin (Manis temmincki), Giant Pangolin (Manis gigantean), Long-tailed or Black-bellied Pangolin (Manis tetradactyla) and Tree or African White-bellied Pangolin (Manis tricuspis). The other four pangolins are native to Asia, including the Chinese Pangolin (Manis pentadactyla), Indian Pangolin (Manis crassicaudata), Malayan Pangolin (Manis javanica) and Palawan Pangolin (Manis culionensis), a new species identified in 2005 (
As predators preying on ants and termites, pangolins have a specialized diet and perform an important ecological role in regulating insect populations. It has been estimated that an adult pangolin can consume more than 70 million insects annually, and has a significant impact on the control of forest termites (
Because of pangolin’s economic values, illegal hunting and illegal trade take place frequently. For example, approximately 24 tons and 14 tons of frozen pangolins were seized in Vietnam and Indonesia in March 2008 and July 2008, respectively (
With the exhaustion of wild populations, captive breeding becomes an important way to protect pangolins from extinction; however, there still exist many technical barriers for the captive breeding programs because of pangolin’s specialized behavior and dependence on natural ecosystems. According to literature, over the past 150 years, more than 100 zoos or organizations have attempted to maintain pangolins. Most captive pangolins died within six months, although some were held for two to three years, a few cases lived for 12–19 years. Zoo records for pangolins in captivity from 1877 to 2001 had been reviewed by Yang (
Institutes (programs) holding pangolins in captivity in the last decade.
Institutes/Programs | Species | Status |
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Taipei Zoo | Chinese pangolin | They improved artificial diet, and had a new-born record in captivity ( |
Research Base for Pangolin Domestication and Breeding from South China Normal University, China | Chinese pangolin, Malayan pangolin | The habitat, diet and management of captive pangolins were improved a lot, and had several new-born records in captivity ( |
Yunnan Wild Animals Park, China | Chinese pangolin | Successfully mated pangolins in captivity, and had a newborn record, but the cub died within three days ( |
Guangdong Provincial Wildlife Rescue Center; South China Institute of Endangered Animals, China | Malayan pangolin | Supplied pangolins with naturalistic habitats, optimized artificial diet, and kept pangolins for more than 500 days (Programs carried out by ourselves). |
Night Safari, Singapore | Malayan pangolin | They can breed and raise the Malayan pangolins in captivity ( |
Conservation International (CI); Forestry Administration (FA), Cambodia | Malayan pangolin | CI together with the FA have recently set up the Pangolin Rehabilitation Center, to provide care and treatment to animals rescued from the wildlife trade ( |
Cuc Phuong National Park, Vietnam; Cat Tien National Park/ Carnivore & Pangolin Conservation Programme (CPCP) | Malayan pangolin | Some pangolins have kept alive over six years, and got two new-born records in captivity; one of the cubs kept alive for nine months (Visited by ourselves in November 2011). |
Cu Chi Wildlife Rescue Station, Vietnam | Malayan pangolin | Some pangolins have kept alive over two years, and got two new-born records in captivity (Visited by ourselves in November 2011). |
Cambodia/Angkor Centre for Conservation of Biodiversity (ACCB) | Malayan pangolin | ACCB is a pangolin program that has been running since 2004. They have the longest living Malayan pangolin ever to be hand-reared in captivity ( |
Indonesian Institute for Sciences (LIPI), Indonesia | Malayan pangolin | LIPI is undertaking research into the rescue and captive-breeding of pangolins in addition to conducting molecular studies ( |
Breeding center for pangolins, Nandan Kanan Zoological Park, India | Indian pangolin | The special program is aimed at documenting the behavioral pattern and reproductive characteristic of the Indian pangolin. They had a newborn record at 2007 ( |
Tikki Hywood Trust; Zimbabwe Parks; Wildlife Management Authority, Zimbabwe | Cape pangolin | They are working with the Cape pangolin for captive breeding and re-introduction purposes ( |
San Diego Zoo, USA | Tree pangolin | One Tree pangolin lives in the San Diego Zoo for visiting ( |
Pangolins occupy a variety of habitats in the wild, ranging from tropical to sub-tropical, from cleared and cultivated areas, savannah grasslands to mixed forest, broadleaf forest, secondary forest, etc. (
Pangolins are divided into two types: terrestrial and arboreal. Most of the pangolins are terrestrial and they dig burrows or live in other animal’s deserted dens for nesting and shelter. The rest of the pangolins are arboreal, living in hollow trees or on tree branches (
Suitable temperature is another key factor for pangolins’ naturalistic habitat, since pangolins have slower metabolism and little body hair to keep warm. When temperatures were 12–15 °C inside the pangolin cage, pangolins may suffer shivering and a runny nose (
Most pangolins are nocturnal creatures, occasionally active during the day, and are generally shy and timid (
In addition to a suitable accommodation, artificial diet is another critical limiting factor for captive pangolins. Pangolins have adapted to a highly specialized diet of ants and termites making it difficult to replace their natural food completely with artificial food.
Field studies show that except for ants and termites, pangolin’s diet also includes ant larvae, bees (pupas), flies, worms, crickets, and some of other insect larvae, and sometimes sand and grass will be swallowed in the intake process. A pangolin of three kilogram can consume up to 300–400 g of termites per feeding (
According to their natural food compositions, a number of artificial diets for captive pangolins had been developed, ingredients including eggs, meat (minced beef, horse meat, fish), milk, milk powders, canned feline diet, orchid leaves, commercial chows, psyllium seeds, carrots, yeasts, multivitamins, and insects etc. (
Some recipes for captive pangolins were summarized in Table
Species | Formulas and remarks |
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Chinese pangolin | Formula 1: Horsemeat (150 g), milk (180 ml), egg yolk (1), cooked cereal (5 g), milk powder (5 g), calcium powder (1 g), vitamin complex (0.2 ml). Feeding after grinding, mixing, heating. Female pangolin gave birth to a cub. The baby was weaned after 89 days. Both of them survived more than six months ( |
Formula 2: Canned feline diet (2 tin), milk powder (2 tablespoons), flaxseed Meal (2 tablespoons), egg yolk (2). Total feeding quantity of two pairs of pangolin a day. Both of the two female have gave birth, one cub each. A male pangolin survived for 212 days, others more than 460 days ( |
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Formula 3: Bee larvae (100 g), egg yolks (10 g), apple lump (65 g), meal worm larvae (45 g), yeast powder (2.7 g), coconut powder (1.4 g), calcium carbonate (0.9 g), added powdered supplement (1.5 g), vitamin supplements (5 ml), soil (5 g). According to previous formulas, after improvements, the Taipei Zoo developed this formula. Except improved the food intake and digestive disorders, they also got a newborn record in captivity. ( |
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Malayan pangolin | Formula1: Egg (hard boiled) (2 tablespoons), multi-vitamin liquid (2 tablespoons), horse meat (120 g), water (350 ml), mealworm (150 g), insectivore pellets (80 g), salmon Oil (1 pump), powdered termite mound (4 tablespoons). mixed into a paste, feeding at night ( |
Indian pangolin | Formula 1: Warm water (1 cup), ant eggs (1/2 cup). There are three pangolins, each had survived for 2, 4, 30 months respectively ( |
Formula 2: Dry dog food (400 g), horsemeat (200 g), biolac (1/2 tin), raw eggs (2), multiple vitamins (5 drops). A female survived for more than one years, has produced a cub, which only survived for three days ( |
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Cape pangolin | Formula1: Minced meat (1/2 pound), maize paste (1/2 pound), raw eggs (2), milk (2 pint), termites (2 pound). Stir the food without termites, and feeding with termites at 11 am and feeding feed at eight pm. The first pair survived for 28 months, and gave birth to one cub. The cub survived for ten months; The other pair survived for 38 months with one cub born. ( |
Giant pangolin | Formula 1: Chopped bovine heart meat (2 cup), cooked cereal milk powder (2 cup). Feeding in the dusk, add raw egg and wheat germ, sometimes. One survived for four years, the other two survived for two years ( |
Tree pangolin | Formula1: Minced beef. Without water, adding vitamin, mixing into wetting powder. A female pangolin lived for two years, gave birth to a cub which lived for seven months ( |
Reproductive disturbance is another technical barrier for captive pangolins. Only a few newborn records were reported in the last decade. This is an understandable situation, because without a successful diet, even survival and growth are problems for captive pangolins, not to mention successful reproduction. Except for poor adaptation to captive environments, poor understanding of pangolin’s reproductive biology is another limiting factor in pangolin’s captive breeding. In the past, the understanding of pangolin reproductive biology has been limited, owing to fragmentary reproductive records, which are primarily from interviewing with hunters, birthing records of rescued individuals in shelters, and a handful of dead fetus anatomy records. So, the reproduction parameters of pangolins are quite inaccurate. At present only few reproductive traits, including pangolin’s time of birth, estrus, gestation period and litter size were reported (
Typically, pangolins are solitary except in mating season. May to July is their preferred mating seasons. Male pangolins often fight each other for females in the mating seasons. The winner will mate with the female pangolin, with the mating period generally lasting three to five days. Female pangolins have two to five estrous cycles during the mating season, and each will last for 11-26 days, until pregnancy (
Generally, regarding the pangolin’s reproduction, little information has been known. This situation greatly limits the application of artificial reproductive technology in pangolin’s artificial propagation, suggesting more work is needed to overcome the pangolin’s reproductive disturbance in captivity.
Because of their poor adaptability to captive environment and a weak immune system, pangolins are easily to get sick. Gastrointestinal disease, pneumonia, skin disease, parasites, etc. are the most common causes of death for captive pangolins (
It is documented that almost all the wild animals have parasites, such as ticks and mites, especially for the pangolins seized from illegal trade (
Since 2010, in order to protect the seized pangolins, a plan of ex situ conservation with captive-breeding has been carried out by South China Institute of Endangered Animals and Guangdong Provincial Wildlife Rescue Center (Guangzhou, China). From 2010–2013, we had kept 35 seized pangolins (2 Chinese Pangolins, 33 Malayan Pangolins) (Figure
Based on three years of work, we got some practical experiences and lessons: (1) Keep the temperature stable in the pangolin's rooms. The sharp change of temperature has serious effect on pangolins’ health. For a case in 2012, when the cold came suddenly, the temperature dropped from 20 °C to 5 °C in one night, such temperature change caused 6 Malayan Pangolins death within 15 hours. (2) Different species, different sources and different body-sized individuals should be kept in deferent rooms to avoid fighting and to minimize the propagation of disease.
Based on the review of current knowledge and our own experience, we give some recommendations for the future practice of captive pangolins, wishing to improve the successful rate of captive breeding of pangolins.
1) Optimize and quantify the environmental parameters. Naturalistic habitat which could simulate their wild microenvironment is the best choice for captive pangolins. It seems that we have achieved some progress in constructing pangolin’s artificial habitat, for example, moderate temperatures, less disturbance, better concealment, supplying an artificial cave or a mound for digging burrows etc. Nevertheless, the detail parameters of the habitat need to be quantified and further optimized in the future, such as the indoor temperature and humidity, area, animal density, light intensity, litter type and height etc. Moreover, reducing the stress level of pangolins in captivity must be noted, and installing a closed-circuit television in their habitat will be convenient to observe their activities without interference.
2) Analyze pangolin’s digestive system and improve their artificial diets. Appropriate artificial diet is another key factor for captive breeding of pangolins. Although there are lots of diet formulas developed, and some of them seem successful, more work is needed to improve their artificial diet in the future, because even the most successful artificial diet can’t replace natural food completely. Generally, artificial diet must match their digestive system and satisfy their nutritional needs. This requires us to understand the physiology of pangolin’s digestive system comprehensively. There are some anatomical analysis of pangolin’s digestive system recently (
3) Determine the reproductive parameters. Although there are successful breeding records of captive pangolins in the past, they are just individual cases. Improving the reproduction rate is the ultimate aim of the pangolin captive programs, so more reproductive parameters need to be determined in the future. Besides the descriptions for the reproductive traits, such as estrus cycle, gonad activity cycle, mating time, pregnancy period etc. Quantitative analysis of hormone concentrations during the reproductive cycle needs more attentions, including testosterone concentration and male sexual behavior, estrogen concentration and estrus, follicle-stimulating hormone (FSH) concentration and ovulation, etc. These studies could provide reference for artificial regulation of reproductions in practice.
4) Disease control. Prevention is much more efficient than treatment in disease control. Supplying a suitable environment or using preventive actions to reduce the chance of illness will be the preferred choices for captive pangolins. For example, suitable temperature and humidity is essential to prevent pneumonia, and appropriate artificial diet is essential to prevent gastrointestinal diseases. Pesticides such as thiabendazole can be used regularly to get rid of parasites. At the same time, more case studies need to be strengthened to find the prevalence of disease in pangolins, and to provide references for future treatments.
The authors would like to thank Prof. Richou Han, Prof. Jinping Chen, Dr. Nguyen Xuan Dang, and Mr. Yanzhong Deng for their help during the material collection and the investigation in some pangolin rescue centers. Mr. Mike Cline reviewed the text and improved the English of this manuscript. This work was supported financially by the Scientific and Technological Program of Guangdong Province, China (No. 2011B050700004) and the Science Foundation for The Excellent Youth Scholars of Guangdong Entomological Institute, China (No. GDEI-yxqn201103).