Status and Analysis of Artificial Breeding and Management of Aquatic Turtles in China

Simple Summary Turtles have been on Earth for 300 million years, but their survival has been challenged as human activity has expanded. The results of a census and statistical analysis of artificially domesticated aquatic turtles in 15 provinces of China showed that 29 species were aquatic turtles native to China and a large number of exotic aquatic turtles are domesticated in China. This paper presents the current situation and problems of aquaculture and conservation of aquatic turtles in major provinces of China, and puts forward some suggestions for the conservation and management of aquatic turtles. Abstract China is a major country in turtle cultivation and has a long history of artificial breeding of turtles. In this study, a census and statistical analysis of artificially domesticated aquatic turtles in 15 provinces of China were conducted. The results showed that 29 species were aquatic turtles native to China, accounting for approximately 9% of the world’s total, and a large number of exotic aquatic turtles are also domesticated in China. The present situation of artificial breeding and protection of aquatic turtles in major provinces of China is shown, and existing problems are also put forward, with suggestions for the protection and management of aquatic turtles.


Introduction
Turtles have been on earth for 300 million years, but with the expansion of human activities, their survival is facing challenges. There are 36 species in six families in China, including five sea turtles and three tortoises, out of approximately 330 species in 14 families worldwide [1][2][3]. Because of the turtle culture in China, artificial breeding of turtles was initiated, and the history of turtle culture can be traced back to prehistoric times. In the Shang Dynasty, the turtle shell was already used as a divination tool. Now China's breeding turtles are mainly used for food, medicine, and ornamental and wild proliferation. The Law of the People's Republic of China on the Protection of Wildlife was implemented in 1989. The current effective version is the fourth revision, passed in 2018, and it aims to protect wild animals, save precious and endangered wild animals, maintain biodiversity and ecological balance, and promote ecological civilization-building laws.
The Regulations on the Implementation of the Protection of Aquatic Wildlife of the People's Republic of China is a law that was issued in 1993. After two revisions in 2011 and 2013, it clearly stipulates that people who domesticate and breed aquatic wildlife under state protection should hold domestication and breeding licenses issued by relevant fishery administrative departments. The Aquatic Wildlife Licensing Measures of the People's Republic of China is a law that was issued in 1996 and that has been amended several times, in 2004, 2010, and 2013, to regulate the issuance and use of the licensing certificates for the utilization of aquatic wildlife; this license is called the Aquatic Wildlife Domestication and Breeding License and Aquatic Wildlife Operation and Utilization License. China is a major country in the domestication and reproduction of turtles and tortoises. Since the implementation of the domestication permit policy in 1996, it is still unknown what the current management and protection status is. Based on survey data, this paper gives a general overview of the protection and management of aquatic turtles in China and proposes solutions to existing problems.

Materials and Methods
From 2019 to 2020, a census was sent to the fishery and fishery administration departments of 15 provinces and municipalities, including Anhui Province, Hubei Province, Guangdong Province, Shanghai City, et al. (Figure 1), to count the licenses for the use of aquatic wild turtles (units might have a breeding license, operating license, or both) and to count factors related to operations and utilization (the number of operating and utilization institutions in each province and municipalities, species types, total number of animals, and contact details). The census forms collected in 15 provinces and municipalities were sorted, and questionable information was checked by telephone consultation to make the data as accurate as possible.
Turtles are classified according to the book Turtles of the World [1].
Using the fishery yearbook [4], the output of edible turtles (Chinese softshell turtle, Pelodiscus sinensis) in China from 2004 to 2021 was calculated.

Turtle Species
According to government statistics, the turtle species that are certified for commercial rearing in China include all 12 families except the Pelomedusidae family (because the Testudinidae family does not belong to the fishery management department, no research has been done on this family), for a total of 88 species. Among the 88 species of turtles, 29 are native species in China, and 59 are exotic species. See Table 1 for details; see Table A1 for species diversity. Table 1.
Number of genera/species of freshwater aquatic turtles in the surveyed provinces/municipalities.

Certificate Status
A total of 28,862 artificial domestication, breeding, and business utilization units in 15 provinces and municipalities were surveyed. Among them, 17,007 units independently held artificial breeding licenses, and 489 units independently held operation and utilization licenses. There were 11,349 units that held two certificates; see Table 2.

Artificial Domestication and Breeding
The number of cultured turtles in the surveyed provinces is shown in Table 3. In addition to the three species of the Testudinidae family, 29 native turtle species were counted, and both the protected turtles and the unprotected Chinese softshell turtle have been artificially domesticated. Inferring from the amount of domesticated individuals, the two large turtles are the most endangered, and Swinhoe's Softshell Turtle Rafetus swinhoei is the least endangered; the most endangered species had just one male in the units surveyed, and the Asian giant softshell turtle Pelochelys cantorii had just adult 13 individuals and nearly 1000 offspring ( Figure 2).  There are a number of sea turtles held in parks for the public to view. The most endangered sea turtle is the leatherback turtle, Dermochelys coriacea, of which only two individuals were counted.
All species of the genus Cuora are protected species, and the number of Cuora zhoui is the lowest, 357, followed by Cuora yunnanensis, Cuora mccordi, Cuora pani, and Cuora aurocapitata with 1340, 4801, 5427, and 5476 individuals, respectively. Some domestication certificates show that there are as few as one domestic Cuora turtle in some units.

Turtle Production
The total breeding volume of Chinese softshell turtles was 182,610 tons in 2004, 364,878 tons in 2021, and has been stable above 300,000 tons in the past 11 years. (Figure 4).

Data Reliability Analysis
Most localities use reports combined with data to submit census results to describe the overall situation of the census in the province. The specific measures for the approval and management of the two licenses vary greatly from place to place, and the information recorded in the statistical tables varies, such as the approval number of the two licenses, the period of issuance, the validity period, the number of approved species, the number used in breeding, the number of individuals in the business, the purpose of the captive breeding, and the locations of sales. In some provinces, such as Shanghai and Yunnan, there are fewer than 10 units that are licensed for domestication, and there may be problems such as data leakage, so the real situation cannot be displayed. At the same time, there are also differences in the specific management of the annual review and renewal of the two certificates. For this reason, the same method cannot be used for statistical data, and individuals doing research need to consult and understand this situation. Even with a well-managed artificial breeding license, there is inevitably some level of uncertainty in the statistical data, so it can be used only as a management reference. However, the survey data can reflect the current situation of aquatic wildlife protection and management in China to a certain extent and provide a certain data basis for further improving the ledger [5], standardizing the approval of aquatic wildlife management and utilization, and combating illegal fishing and illegal management and utilization.

Conservation Management Status
Since the Wildlife Protection Law of the People's Republic of China was issued and implemented in 1989, a series of laws and regulations on wildlife protection have been issued and revised [6]. These laws and regulations and the establishment of related management systems are aimed at improving the maintenance and management level of aquatic wildlife. With its vast territory, China has a large number of domesticated turtles and tortoises, and more than 28,000 households have obtained certificates, which has played an important role in the dynamic monitoring management, legal traceability and information sharing of aquatic wildlife and their products.
With the continuous deepening of turtle protection legislation, the power of law enforcement in this area has been strengthened. In particular, since the outbreak of COVID-19, national awareness of wildlife protection has increased, and law enforcement authorities have dealt with more cases of wild animal abuse and illegal trade, greatly enhancing the protection of turtles and other wild animals [7].
The national awareness of aquatic wildlife protection has been strengthened. The construction of a large number of science museums and national parks, as well as the development of aquatic animal protection publicity activities and aquatic animal proliferation and release activities, have greatly enhanced the national awareness of wildlife protection.

In Situ and Ex Situ Conservation
Artificial breeding plays an important and positive role in the conservation of endangered turtle populations. Aside from the failure of artificial assisted breeding with 2 R. swinhoei (one female and one male; the female turtle died during artificial induction in 2019) [8], other turtle species have been successfully artificially bred. More successful species, such as Platuysternon megacephalum [9] and Mauremys mutica [10], have played an important role in the growth of turtle populations.
Large-scale artificial breeding of turtles has been in China for nearly 40 years. Turtle breeding has played a huge role in people's livelihood and economic development. The total annual supply of Chinese soft-shelled turtles is now stable at 300,000 tons per year, which has played an important role in the needs of people's livelihood. According to the 2020 report of the Guangdong Turtle Breeding Industry Association, the number of employees involved in the artificial breeding of turtles was 265,600, and the direct economic output value exceeded 100 billion yuan in China's Guangdong Province (unpublished).
Another important role of the artificial breeding of wild populations is to implement reintroduction to promote the recovery of wild populations. However, China is still lacking in the artificial release of endangered turtles and the restoration of wild populations. The main activities are the artificial release of Chelonia mydas [11], and some postrelease effect evaluations have been carried out. M. mutica, P. sinensis, and other species have also been artificially released in the wild many times. However, the monitoring and effect evaluation after the release are insufficient, and the effect of the release on the recovery of the wild population is unknown. In recent years, the protection work of China's firstclass national protected animal P. cantorii has had much influence on the protection of turtles across the country. There are 13 known wild P. cantorii individuals in China, and they were domesticated in six different areas [12]. Four of these individuals have been successfully bred (for seven consecutive years), and nearly 1000 offspring are currently alive. To better protect this national first-class protected animal, the state formulated and passed the "Pelochelys cantorii Conservation Action Plan (2019-2035)" and carried out the first breeding-release program for the species in 2020, with 20 artificially hatched individuals aged 4-5 years [13][14][15]. According to the growth data and the health status of the P. cantorii individuals that were recaptured in 2021 and 2022, the released individuals adapted to their wild environment; therefore, the wild adaptation and protection effect is remarkable, and artificial release in suitable historical habitats can be considered. China has further carried out habitat assessment, restoration, and transformation of the historical habitats of the species, carried out large-scale artificial release, and finally achieved the goal of wild population recovery [16].

Management
The usage of species names on the certificate is not standardized. The scientific name is often not used; instead, the species names on certificates have many irregularities: they may be local common names (such as Vietnamese stone turtles), abbreviations (such as for southern turtles), only order or genus names (such as for Turtles, Cuora turtles, sea turtles, and the South American side-necked turtle), or hybrid names (e.g., Mauremys iversoni, Ocadia glyphistoma, Sacalia pseudocellata, Ocadia philippeni) [17]. The species name convention on certificates needs to be standardized by national authorities, and at the same time, the training of local administrative staff should be strengthened.
There are also false numbers of captive individuals. Some rare turtles, such as box turtles, have a certain number of false reports from the statistical data and verification results. For example, one farm's domestication certificate stated that the number of Cuora yunnanensis was 1000, but telephone verification revealed that there were actually only a few dozen individuals. The large number reported by the farmer is the index number for the later introduction and transaction of future Cuora turtles. Therefore, relevant government departments need to strengthen the on-site verification of the approval process to prevent false reports.
The skill level of turtle domestication technicians is uneven. The domestication certificate management agency lacks an effective review method for the technical level of the breeding personnel of the unit applying for the domestication certificate. There are some tasks for which farmers have no trained technical personnel; instead, these farmers use technical personnel from other units to obtain the qualifications for the certificate. The end result will be the death of some turtles belonging to rare species due to low skill levels and poor facilities.
During the investigation, it was also found that a relatively important problem was that there are many very small groups of endangered and rare species. For example, some Cuora turtles were represented by only one individual in some units, and in some breeding farms only mature females (and no suitable males). Due to policy and for other reasons, there is a lack of a communication mechanism between units that possess critically endangered turtles, and this prevents the effective integration of resources for increasing the population of endangered species.
To further improve the level of aquatic wildlife management, on 1 July 2021, the Ministry of Agriculture and Rural Affairs of the People's Republic of China developed an "aquatic wildlife under special state protection information management system", which started to be commissioned throughout the country, and gradually achieved the dynamic regulation of aquatic wildlife and its products, legal traceability, and information sharing. China will further strengthen the protection of aquatic wildlife. Species and habitats should be closely linked, but the management of aquatic species and nature reserves in China belongs to different management departments. The administrative structure of aquatic wildlife management is in the agricultural department; aquatic wildlife and nature reserves belong to the forestry department [18], and terrestrial turtles (Testudinidae) belong to the forestry department. There is a disconnection in management and a lack of coordination of powers and responsibilities, which results in inefficient management, hindrance of wildlife conservation, and ineffective enforcement of laws.
Most of the aquatic animal species that are designated as national key protected wild animals (this designation applies to only the wild populations), as found in the "Convention on International Trade in Endangered Species of Wild Animals" appendix, have been bred in captivity successfully. Some of these species are managed separately (for example, the wild original species are separately marked and managed in accordance with the Wild Animal Protection Law). Individuals that were born in captivity and that belong to more abundant species have substantial differences from wild populations, so they are managed in ways that are conducive to artificial breeding, circulation, and utilization, that reduce the difficulty of management, and that help promote resource protection. At the same time, China should also strengthen the training in and publicity of relevant laws and regulations, promote a positive understanding of the standardized management of aquatic wildlife utilization, and ultimately create a positive atmosphere for aquatic wildlife protection.
In terms of species, the survey data showed that exotic turtles accounted for 67.05%, which was similar to 68.29% in the survey of one of the largest turtle trading markets in South China [19]. Either escape or release of non-native turtles will cause irreversible negative impacts on China [20]. After alien turtles enter the wild, they have few or no natural enemies, and may occupy the ecological niche of native species, affect the production and reproduction of native species, and may also have a devastating impact on predators [21]. Alien species may also carry pathogens that native species are not resistant to, which will seriously affect the balance of native ecosystems [22]. At the same time, alien species may have gene exchange with native species, resulting in gene pollution [23]. Therefore, management measures against species invasion need to be more clear and proposed.
China is a major country in turtle breeding. Although there are certain problems in turtle breeding and protection management, the related work has been advancing in a positive direction. Among them, China's artificial propagation technology for endangered tortoises, two-certificate management, aquatic wildlife information management system and label management can provide reference for tortoise species protection in other countries.
With the decision of the Standing Committee of the National People's Congress in 2020 on comprehensively prohibiting illegal wildlife trade, eliminating the ecologically damaging habit of eating wild animals, and effectively protecting the lives, health, and safety of the people, the people's awareness of wildlife protection has become increasingly strong. The management mechanism for the artificial breeding of turtles will become increasingly effective, and the protection and utilization prospects of aquatic turtles in China will be better. Institutional Review Board Statement: This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals followed the National Institutes of Health Guide for the Care and Use of Laboratory Animals in China.

Informed Consent Statement: Not applicable.
Data Availability Statement: All datasets generated or analyzed during this study are included in the published article.

Conflicts of Interest:
The authors declared that they have no conflict of interest or personal relationships that could have appeared to influence the work reported in this paper.