REVIEW

The Future of Legislation, Policy, Risk Analysis, and Management of Non-Native Freshwater Fishes in China

Shan Lia, Hui Weib, Lorenzo Vilizzic, Aibin Zhand,e, Julian D. Oldenf, Daniel L. Prestong, Stacey A. Clarkeh,Becky Cudmorei, Gareth D. Daviesj, Xiaoming Wanga, and Gordon H. Coppc,h,k,l

aNatural History Research Center, Shanghai Natural History Museum, Branch of Shanghai Science & Technology Museum, Shanghai,China; bKey Laboratory of Recreational Fisheries (Ministry of Agriculture & Rural Affairs), Pearl River Fisheries Research Institute,Chinese Academy of Fisheries Science, Guangzhou, China; cDepartment of Ecology and Vertebrate Zoology, Faculty of Biology andEnvironmental Protection, University of Lodz, Lodz, Poland; dResearch Center for Eco-Environmental Sciences, Chinese Academy ofSciences, Beijing, China; eUniversity of Chinese Academy of Sciences, College of Resources and Environment, Beijing, China; fSchool ofAquatic and Fishery Sciences, University of Washington, Seattle, Washington, USA; gDepartment of Forest and Wildlife Ecology,University of Wisconsin-Madison, Madison, Wisconsin, USA; hCentre for Environment, Fisheries and Aquaculture Science (Cefas),England, UK; iCentre of Expertise for Aquatic Risk Assessment, Fisheries and Oceans, Ottawa, Canada; jNational Fisheries Services,Environment Agency, Huntingdon, UK; kCentre for Ecology, Environmental and Sustainability, Bournemouth University, Poole, UK;lSchool of the Environment, Trent University, Peterborough, Canada

ABSTRACTPolicies and legislation for the importation and use of non-native (NN) freshwater fisheshave been rapidly evolving in several countries around the world in response to heightenedevidence of their adverse ecological and economic impacts. In China, the already large andgrowing number of NN freshwater fishes being imported from foreign countries or translo-cated within China has necessitated the development of management strategies supportedby policies at both national and regional levels. Despite increasing awareness of the damagecaused by NN fishes, such initiatives in China continue to lag behind those already imple-mented in other countries. This study endeavors to narrow this policy gap by: (i) providinga synoptic overview of the vectors and pathways of NN freshwater fish introductions anddispersal both into and within China; (ii) evaluating existing policies and legislation relativeto those currently implemented in Europe, the USA and Canada; (iii) examining the role ofdecision-support tools for identifying and assessing the risks posed by NN fishes; and (iv)proposing perspectives and possible options for NN fish policies, legislation and manage-ment in China.

KEYWORDSAlien species; biologicalinvasion; Asia; ornamentalfishes; environmental policy;decision-support tools

1. Introduction

The development of effective strategies to prevent theecological and economic impacts of invasive non-native (NN) species is considered fundamental innational-level policies (see Table 1 for a glossary ofinvasion biology terms). The absence of legislation, orthe ineffective implementation of existing legislation,addressing NN species has led to the transport andintroduction of exotic plants and animals around theworld (Gozlan 2008; Gozlan, Britton et al. 2010; Earlyet al. 2016). Non-native freshwater fishes in particularhave been transferred either deliberately or uninten-tionally for various reasons, including aquaculture,ornamental/aquarium use, fisheries enhancement,and biological control (Lin et al. 2015). Not all

introductions result in adverse consequences (Gozlan2008), but species introductions have in some casesresulted in irreversible ecological and socio-economicimpacts (Cucherousset and Olden 2011). The potentialadverse consequences of NN fish introductions high-lighted by Elton (1958) began to receive more globalrecognition in the 1970s (Gozlan 2008), leading to theenactment of legislation in several countries. This wasaccompanied (or followed) by the establishment ofinitial risk identification and assessment protocols(Kohler and Stanley 1984; Kahn et al. 1999), guide-lines or codes of practice (FAO 1995; ICES 1995; USANS Task Force 1996), and national strategies for themanagement and control of NN species (e.g. UKDefra 2008).

CONTACT Shan Li shanlipsu@163.com Natural History Research Center, Shanghai Natural History Museum, Branch of Shanghai Science &Technology Museum, Shanghai, China.� 2020 Taylor & Francis Group, LLC

REVIEWS IN FISHERIES SCIENCE & AQUACULTURE2021, VOL. 29, NO. 2, 149–166https://doi.org/10.1080/23308249.2020.1782830

Effectively implemented legislation can be success-ful in limiting the introduction, spread and impacts ofinvasive species. For instance, the definition andenforcement of regulatory controls in the UK havecontributed to a reduction in the establishment ofnew species (Copp, Bianco et al. 2005, 2007).Legislative controls and accompanying processes havebeen facilitated by the development of risk analysisschemes (e.g. Baker et al., 2008; Essl et al. 2011;D’hondt et al. 2015; Copp, Russell et al. 2016), includ-ing electronic decision-support tools such as the fresh-water Fish Invasiveness Screening Kit (FISK: Copp,Garthwaite et al. 2005) and the Invasive SpeciesEnvironmental Impact Assessment (ISEIA: Branquartet al. 2009). More recently, the Aquatic SpeciesInvasiveness Screening Kit (AS-ISK), which now offersassessors 32 languages with which to carry out theirscreenings (www.cefas.co.uk/nns/tools/), was designedto be a decision-support tool applicable to any aquaticorganism (Copp, Vilizzi et al. 2016) and to be compli-ant with the ‘minimum standards’ for the risk analysisof species under the EU regulation on the manage-ment of invasive alien species (Roy et al., 2018). Theoutcomes of these risk screening protocols areexpected to help improve the management of thescreened species, such as preventing their initial intro-duction and prioritizing strategies and approaches foreradication or control of established NN species (e.g.UK Defra 2008; European Union 2014).

In China, demand from aquaculture and popularityof the pet aquarium hobby involving NN freshwaterfish has been rising rapidly over the past 50 years (Linet al. 2015; Liu et al. 2017). The enactment of NNspecies legislation and policy, however, has been slow

to develop, with only a few risk analysis-related strat-egies implemented to prevent the invasion of NNfreshwater fishes in the country (Wang and Cao 2006;Fang et al. 2011). With ‘Vision and proposed actionsoutlined on jointly building Silk Road Economic Beltand 21st-Century Maritime Silk Road’ issued in 2015,which is of economic incentives to increase trade,international trade is expected to intensify further,heightening risk of new NN fish introductions andtranslocations (Liu et al. 2019). With the goal of help-ing invasive species policy reform in China, the objec-tives of the present study are to: 1) review the historyof NN freshwater fish introductions and dispersalboth into China and within China (i.e. translocatedspecies); 2) assess the current status of legislation andpolicies on NN freshwater fishes in China, with acomparison to Europe, the USA and Canada; 3) evalu-ate the role of decision-support tools for identifyingand assessing the risks posed by NN species; and 4)provide guidance to help improving NN species legis-lation, policy and management in China, with specificregard to NN freshwater fishes. To clarify any ambi-guity throughout this paper in the usage of termsrelated to biological invasion, definitions are given inTable 1.

2. Chinese fish culture

In China, fish have for centuries been a symbol ofdiligence, kindness and good fortune. Indeed, the art-istic image of fish has become a visual symbol of trad-itional Chinese culture. The character that represents‘fish’ in Chinese is found in many four-characterwords. This is because the pronunciation of ‘fish’ in

Table 1. Definition of terms used in biological invasions (after Copp, Bianco et al. 2005).Terms Definition

Native, indigenous A taxon that occurs naturally in a geographical area, with dispersal occurring independentof human intervention, whether direct or indirect, intentional, or unintentional.

Non-native, non-indigenous, alien, exotic A taxon that does not occur naturally in a geographical area, and whose dispersal intothe area was facilitated directly or indirectly by humans, whether intentionally orunintentionally.

Transferred A taxon that has been moved across a national border to a country within itsnatural range.

Translocation Introduction of a taxon from one part of a political entity (country) in which it is nativeto another part of the same country in which it is not native.

Establishment The process undergone by a non-native taxon, following introduction, to create a self-sustaining population in the wild, beginning with successful reproduction.

Naturalisation The process undergone by a non-native taxon following its introduction andestablishment that is if it has been present for a sufficient duration of time and hasincorporated itself within the resident community of organisms.

Introduction The deliberate or unintentional transfer and/or release of the taxon, which can be theresult of direct or indirect human intervention. The organism introduced into the wild,not completely isolated from the surrounding environment, is the result of humanactivities in those geographical areas where the taxon is not native. This also appliesto translocations within or between political states/provinces (countries).

Invasion A collection of processes related to the appearance and impacts on communities andecosystems of non-native taxon.

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Chinese (yu: 鱼) is the homophonic word that means‘more’. During the Chinese New Year celebration, thepicture of a boy holding a large carp and a lotus inhis hand is often hung on doors or windows to prayfor good luck (Figure 1A). Live fish are also preparedfor exchanges of gifts, and fish patterns are alsofrequently found in ancient Chinese porcelain(Figure 1B).

Freshwater fish aquaculture in China began in theYin Dynasty about 3100 years ago (Zhong and Power1997). Fan Li (536–448 BC), a famous politician andbusiness theorist, wrote the world’s earliest fish aqua-culture book Scripture of Pisciculture, in which rearingtechniques of common carp Cyprinus carpio were dis-cussed. In this book, Cyprinus carpio, the representa-tive species of the family Cyprinidae, is considered amilestone species for aquaculture (Zhong and Power1997). The most famous species reared are those ofChinese origins: grass carp Ctenopharyngodon idella,silver carp Hypophthalmichthys molitrix, bighead carpHypophthalmichthys nobilis, and black carpMylopharyngodon piceus. Other profitable speciesinclude mud carp Cirrhinus molitorella, crucian carpCarassius carassius, white Amur bream Parabramispekinensis, and Japanese eel Anguilla japonica.

Ornamental fish rearing also has a long history inChina. Goldfish Carassius auratus, one of the world’smost famous ornamental species, originated in China1700 years ago. The ornamental varieties of goldfish aswe know them today were produced from wild(brown) Carassius auratus through long-term naturalmutation, artificial selection and hybridization. Thefirst two characters of the Chinese four-characterword Jin Yu Man Tang (金玉满堂) are pronouncedthe same as ‘goldfish’. And the entire four-characterword represents abundant wealth and many childrenfor the family. In the last 20 years, as the ornamental

fish industry developed quickly, the introduction ofbright-coloured NN fish species, especially of tropicalorigin, have been favored in China.

Besides aquaculture and ornamental fish rearing,‘Life release’ is also important in Chinese fish culture,which may have facilitated NN fish invasion. This is afamous traditional Buddhist practice that endeavors tosave lives that are being destined for slaughter. Life-release events are routinely held across China,especially in the Tibet Autonomous Region (AR), tocelebrate birthdays of the gods or other memorial days.

3. Current status of non-native freshwaterfishes in China

3.1. Numbers, vectors and pathways

China has an extremely diverse native freshwater fishfauna comprising 1,513 species, which represent�10% of the world’s endemism (Closs et al. 2015).This diversity, however, has been severely threatenedby increased human activities (Xiong et al. 2015; Liet al. 2016; Liu et al. 2017), with several fish speciesintroduced from other countries or translocated fromtheir native ranges to river basins elsewhere acrossChina (Gozlan, Britton et al. 2010; Xiong et al. 2015).Of these, 53 species have been found in a recent studyto have established self-sustaining populations (Xionget al. 2015), and some 147 NN fish species were intro-duced after 1950 of which 56 species originated fromoutside the country and 91 were translocated (Liuet al. 2017).

The motivations for NN fish introductions varyaround the world, but in general these include aqua-culture, aquarium use, sport fishing, stock enhance-ment, and biological control (Gozlan 2008; Lin et al.2015). Non-native fish species introductions to China,either intentional or accidental, consist of 347 species

Figure 1. A. Typical Chinese New Year door painting showing a pudgy boy holding a common carp and a lotus in hand. B. Vaseof the Song Dynasty (960–1279 D.C.) with a pattern of the common carp.

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for the aquarium trade, 91 species for aquaculture,and one species for bio-control (Xiong et al. 2015).However, during the 20th century, aquaculture hasbeen the most important driver for NN fish introduc-tions in China due to rapidly-developing markets (Linet al. 2015). Global aquaculture production hasincreased from 32.4 to 80 million tons between 2000and 2016, and over 60% of the world production nowoccurs in China of which over 25% involves NN spe-cies (FAO, 2016; Shelton and Rothbgard 2006).

Non-native fish introductions for aquaculture pur-poses from other countries began in the 1930s, reach-ing their peak in the 1990s due to the worldwidetrade of salmonid, tilapia and carp species (Li and Li2001; Pan et al. 2006; Chen et al. 2011). Nile tilapiaOreochromis niloticus, blue tilapia Oreochromis aureus,the O. aureus � O. niloticus hybrid, rainbow troutOncorhynchus mykiss, mrigal carp Cirrhinus mrigala,brown trout Salmo trutta, roho Labeo rohita andCyprinus carpio were common species introducedbefore 2000 for aquaculture use (Table 2). Theproduction of tilapia exceeds that of other NN fishspecies in aquaculture in China, reaching 1.8 milliontons in 2017 (http://www.fao.org/fi/static-media/MeetingDocuments/TiLV/dec2018/p13.pdf).

After 2000, NN fish introductions for ornamentalpurposes increased rapidly (Xiong et al. 2015).Although the introduction history of aquarium fish inChina is relatively short, some species have alreadyestablished self-sustaining populations and causedadverse ecological and economic impacts due to thelack of proper risk analysis and implementation oflocal regulations (Lin et al. 2015; Xiong et al. 2015).For instance, sailfin catfishes Pterygoplichthys spp.have been introduced around the world as aquariumfish (Nico et al. 2012; Moroni et al. 2015), and theirescape (or release) into natural waters has already ledto serious invasion consequences in North America(Fuller et al. 1999), South Africa (Jones et al. 2013),

and several Asian countries (Ishikawa and Tachihara2014; Bijukumar et al. 2015). The giant pangasiusPangasius sanitwongsei and vermiculated sailfin catfishPterygoplichthys disjunctivus were recently reported tobe ornamental NN species that are likely to pose ahigh risk of being invasive in South Africa due topropagule pressure, i.e. repeated frequency and size oftheir imports and possible release to open waters(Ellender and Weyl 2014). In the 1990s,Pterygoplichthys spp. were introduced to GuangdongProvince where they have since spread rapidly due tothe suitable habitat and climate conditions of theregion (Wei et al. 2017). Pterygoplichthys spp. werefirst recorded in Jianjiang (southwest of Guangdong)in 2001, and then quickly spread northwards toXijiang, Beijiang and the Pearl River Delta by 2010,and eventually further east to Dongjiang andRongjiang to encompass the entire GuangdongProvince by 2015 (Figure 2). The currently developingaquarium trade, climate warming and lack of NN spe-cies management are likely to facilitate the species’expansion further north into other parts of China(Wei et al. 2017).

The only fish species introduced specifically forbio-control purposes has been the western mosquito-fish Gambusia affinis, which represents the earliestrecord of a fish introduction to China from outside itsborders (Xiong et al. 2015). Introduced to Shanghaifrom the Philippines in 1927 for bio-control of mos-quitoes, G. affinis is now widely distributed in theRiver Yangtze and Pearl basins, as well as in othersmall water bodies throughout the southeast of China(Yan et al. 2009). This species has been proven harm-ful to a wide range of native aquatic organismsincluding invertebrates, fishes and amphibians(Pyke 2008).

The source countries of introduced NN fishes inChina encompass all six inhabited continents: Africa(94 species introduced of which 21 have established

Table 2. Summary of non-native fish introductions for aquaculture purposes from 1950 to 2000.Species name Origin Introduced to Year Reference

Cirrhinus mrigala India Guangdong Province 1982 Chen and Ye (1994)Cyprinus carpio Japan/Germany Provinces across China 1980 Chen and Ye (1994)Labeo rohita Thailand Guangdong Province 1978 Chen and Ye (1994)Oncorhynchus mykiss Korea Heilongjiang Province 1959 Li et al. (2007)Oreochromis aureus Africa Southern China 1980 Li et al. (2007)Oreochromis niloticus Egypt Hunan Province 1985 Li et al. (1997)

Egypt Shanghai 1998 Wu et al. (1998)Philippines Shanghai 1994 Wu et al. (1998)Sudan Hubei Province 1978 Zhang et al. (1979)Sudan Hubei Province 1995 Wu et al. (1998)Thailand Guangdong Province 1985 Pan and Liang (1983)USA Beijing 1993 Li and H (1998)

O. aureus�O. niloticus Thailand Southern China 1981 Chen and Ye (1994)Salmo trutta Europe Tibet AR 1976 Lou (2000)

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self-sustaining populations), Asia (19 out of 101),North America (21 out of 52), Central and SouthAmerica (6 of 156), Europe (14 out of 19), andOceania (3 out of 17) (Xiong et al. 2015; Liu et al.2017). Although relatively fewer species have beenintroduced to China from North America andEurope, a larger proportion of fishes from these twocontinents have already established self-sustainingpopulations in China’s open waters (Xiong et al. 2015;Liu et al. 2017).

3.2. Translocations

Fish translocations within China have been recordedless often than introductions even though they arequite common for husbandry and fisheries enhance-ment. The history of fish translocations for food pro-visioning in China can be traced back to the HanDynasty (202 BC–220 AD) of Cyprinus carpio (Maet al. 2003), with an additional 91 fish species translo-cated within China since then. The highest number ofspecies has been translocated to the River Yangtze(n¼ 57), and the lowest to the rivers Haihe (3) andHuaihe (2) (Liu et al. 2017). Amongst these, 61 spe-cies have been translocated for aquaculture (Lin et al.2015) of which ten are already known to have resultedin biological invasions. For example, the four speciesof Chinese carp favored as food in China (see above,Chinese Fish Culture) have been translocated to fishfarms nation-wide (Wang et al. 2009). These specieshave established self-sustaining populations, and someof them have resulted in significant declines ofendemic fish species (Peng et al. 2009), specificallyKunming nase Xenocypris yunnanensis and barblesscarp Cyprinus pellegrini in lakes of Yunnan Province,and in the disappearance of big-head schizothoracinAspiorhynchus laticeps in Xinjiang Province (Liet al. 2016).

Fish eggs, juveniles and adults of endangered spe-cies are released to large natural waters from commer-cial fisheries or ex-situ facilities for conservationpurposes. Such releases have been widely employed toenhance commercial fisheries stocks, becominganother driver of fish translocation in China since2005. In this regard, the total national investment intofisheries enhancement amounted to 7.1 billion RMBin 2010 – a 20% increase from 2009 (Yang et al.2013). Many of these fish translocations were due to alack of proper legislation or enforcement thereof,resulting in considerable adverse impacts on thereceiving waters, such as in the lakes of YunnanProvince (e.g. Kang et al. 2015). Similarly, the num-bers of native species in Lake Dian has dropped from25 species in the 1960s to only four in 2001 – adecline coinciding with the introduction and establish-ment of the four major Chinese carps (Chenet al. 2001).

4. Legislation and policies on non-nativefreshwater fishes

4.1. China

In 2002, motivated by the report of an invasive redpiranha Pygocentrus nattereri in Nanning (GuangxiProvince), alien invasive species (AIS) were officiallyrecognized by the Ministry of EnvironmentalProtection (Ministry of Ecology and Environment,after institutional reform) with a declaration of the16 worst species that have already caused seriousinvasion consequences (No. 2003/11) [note thatChina’s post-2018 institutional reform names will begiven hereafter in brackets]. The list of AIS wasrevised in 2010 and twice in 2017, with the followingfour fish species included: Amazon sailfin catfishPterygoplichthys pardalis, Pygocentrus nattereri,Oreochromis niloticus and Gambusia affinis.Additional information on AIS was provided in the

Figure 2. Distributional range of sailfin catfish Pterygoplichthys spp. in the river drainages of Guangdong Province (China) from2005 to 2015. (Data source from H Wei unpublished data).

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Database of Invasive Alien Species in China (www.chinaias.cn) in 2013, with 34 NN fish species listedas invasive among which 17 have self-sustaining pop-ulations. This database is managed by the Center forManagement of AIS under the Ministry ofAgriculture (Ministry of Agriculture and RuralAffairs) and the Institute of Plant Protection,Chinese Academy of Agricultural Sciences. The data-base contains information on geographic distribution,field collection, biosafety, DNA barcoding, andremote monitoring of AIS. Special authorization isrequired for the use of most modules except thosecontaining the most basic information about species’name, habitat type, and time of introduction.Another database called Invasive Alien Species ofChina (www.iplant.cn) is managed by the Instituteof Botany, The Chinese Academy of Science. A listof invasive species, an update of new invasions, exist-ing legislation and policy, together with literaturereferences are provided in the database. Despite theseefforts, the true number of invasive fish species inChina remains underestimated (Xiong et al. 2015;Liu et al. 2017).

Introductions and subsequent impacts of NN fishspecies in China have been driven by commercialinterests and encouraged by government policies insome circumstances. For example, Oreochromis niloti-cus was introduced as an important aquaculture spe-cies and reared in most provinces of China since the1970s (Li and Li 2001). After escaping from fishfarms, this species has spread in rivers of southernChina, resulting in a reduction of the total catch ofother fish. This has led to a loss in income for fisher-men due to the lower market price of this species (Guet al. 2015). Also, Pterygoplichthys pardalis, a popularNN ornamental fish, was accidentally released acrossChina (Li et al. 2007), and it is reported to have estab-lished self-sustaining populations in the rivers ofGuangdong Province (Wei et al. 2017).

Non-native invasive species have received increas-ing attention from scientists and policy-makers sincethe 1990s, with legislation regarding introduction andrearing incorporated into various legislative acts,including the Quarantine Act, the EnvironmentalProtection Act, the Agriculture and WildlifeProtection Act, and the Law on the Entry and Exit

Figure 3. Current national laws and legislation on non-native aquatic species in China (in brackets, names of institutions after the2018 institutional reform).

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Animal and Plant Quarantine (Figure 3). Regulationsfor the Implementation of the latter were issued bythe General Administration of Quality Supervision,Inspection and Quarantine in 1992 and 1997. Theseregulations prohibit the introduction of infectious orparasitic diseases of animals, pathogens, insect pestsand weeds dangerous to plants and other organisms.This legislation requires the inspection and quaran-tine of NN species introduced for scientific purposes.The Marine Environment Protection Law, which wasenacted in 1982, also prohibits the introduction ofNN fish species, sub-species or races without anyscientific assessment. The Fishery Act and theRegulation on Aquaculture Propagules regardingtrans-national and trans-provincial introductions ofaquaculture propagules was enacted in 1986 andamended in 2000 and 2004. In the act, NN intro-ductions are prohibited unless approved by theDepartment of Fishery Administration, with intro-ductions of NN species forbidden except underlicense or consent. Any plans to import NN speciesfor aquaculture must include a risk assessmentreport that considers potential impacts on nativeecosystems and species, the likelihood of the targetNN species hosting pests or diseases, as well asother likely hazards. In addition, NN aquaculturespecies should only be introduced by research insti-tutes and reared in closed facilities for domestica-tion. Although these actions were expected toprevent invasions, risk assessments of NN specieshave rarely been undertaken prior to their introduc-tions. The Act for the Administration of AquaticFingerlings and the Fisheries Law were enacted in2005 to protect the utilization of aquatic resourcesand manage the import and export of aquatic spe-cies and products. Article 20-31 of this Act addressesthe management of NN species imports andexports, requiring:

1. Classification of the aquatic species or productsinto Type I (no introduction), Type II [permitissued by the Ministry of Agriculture (Ministry ofAgriculture and Rural affairs)], and Type III (per-mit issued by the Fishery AdministrationDepartment of the provincial government).

2. Conduct a scientific risk assessment and providereports prior to an introduction.

3. Trial rearing of the species in a closed facility[assigned by the Ministry of Agriculture (Ministryof Agriculture and Rural affairs)].

4. Stipulation on any release of the NN species aftertrials have been completed.

Based on national regulations, each province ormunicipality in China has its own regulations on theintroduction and release of NN propagules and adultsfor aquaculture, and these vary among provinces ormunicipalities in their application (strictly or loosely)depending on local strategies. The regulations of 39%of provinces have stipulations that scientific assess-ments or quarantine should be conducted prior to anyintroduction or release of NN aquaculture species, butno penalties exist for violation of these regulations;whereas, another 32% of provinces have stipulationson the introduction or release of NN aquaculture spe-cies with penalties enacted. Xinjiang Province has thestrictest regulation with penalties of fines or criminalliability. The remaining 29% of provinces have nostipulations on the introduction of NN aquaculturespecies. In this respect, Tibet AR, Yunnan, GuizhouProvince and Chongqing City in southwest Chinapossess high biodiversity levels, and as such they facea greater risk of impacts from biological invasions.Therefore, governments in these regions are requiredto enact more comprehensive laws and regulations(Tian and Shi 2013; Zhang et al. 2014). The freshwateraquaculture industries are well developed inGuangdong and Hubei provinces, where relativelystrict quarantine rules require thorough risk assess-ment prior to the introduction or release of a NN fishspecies for aquaculture. Whereas, provinces withlower freshwater aquaculture production levels, andtherefore lower obligations from a biodiversity per-spective, have no regulations pertaining to the intro-duction of NN freshwater fish species for aquaculture.

Enacted in 2011, the Regulation on Management ofNN species in Hunan Province, issued by the standingcommittee of the People’s Congress of HunanProvince, is the first specific regulation specifically forNN species in China. This regulation has specific stip-ulations on risk assessment, introduction, monitoring,control, eradication and supervision, and it alsoimposes a duty of care (responsibility/liability) on thestakeholders and government bodies responsible forintroducing NN species. Non-native species introduc-tions, as well as species translocations from outside ofHunan Province, are prohibited except under licenseor consent with a proper facility and use of isolatedbreeding trials if necessary. The unified supervisionsystem developed in Hunan Province through theDepartment of Agriculture (Ministry of Agricultureand Rural affairs) includes the establishment of a pro-vincial center for invasive species management tocoordinate and lead the enforcement of this regula-tion. In practice, NN species are categorized based on

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risk assessments and comparisons with the nationalinvasive species list as ‘harmful’, ‘undetermined’ or‘harmless’. Corresponding management strategies canthen be implemented based on the species’ categoriza-tion. Elsewhere, in Yunnan Province, a list of AIS isdue to be listed in June 2020 by the YunnanDepartment of Ecology and Environment, in collabor-ation with Kunming Institute of Botany and KunmingInstitute of Zoology, Chinese Academy of Science.This is the first provincial list of AIS in China, and itwill contain 441 NN invasive species, among which 29are fish species.

A program named ‘Eradication of noxious speciesin ten provinces and 100 counties’, proposed byChina’s Ministry of Agriculture (China’s Ministry ofAgriculture and Rural affairs), has been conducted tocontrol the spread of invasive NN species (Xiao et al.2014). Corresponding management strategies, how-ever, have mostly focused on invasive plants, insectsor pathogens, and only four NN fish species (i.e.Gambusia affinis, spotted gar Lepisosteus oculatus,Pterygoplichthys pardalis and Pygocentrus nattereri),consistent with the Ministry of EnvironmentalProtection (Ministry of Ecology and Environment) ofChina’s list, have been included in the NN species listreleased by Hunan Province.

4.2. Europe

Legislation and policy in Europe regarding NN fishspecies has changed over time. The earliest introduc-tions involved Cyprinus carpio and Carassius auratusin the 15th and 17th centuries, respectively (reviewedin Copp, Bianco et al. 2005). During the subsequentperiod of the ‘acclimatisation societies’ in the 19th and20th centuries, fish introductions included variousNorth American species for sport fishing and aquacul-ture (e.g. largemouth bass Micropterus salmoides,Oncorhynchus mykiss and brook trout Salvelinus fonti-nalis) and for ornamental purposes (e.g. pumpkinseedLepomis gibbosus, and fathead minnow Pimephalespromelas). From the 1970s, legislation was developedand enacted to regulate and restrict the introductionof NN fishes in recognition of their potential adverseimpacts to the environment (Copp, Bianco et al.2005). Although there is still interest in the introduc-tion and rearing of NN species, relatively comprehen-sive legislation and administrative protocols have beenenacted and implemented for the introduction andmanagement of NN and translocated fishes by differ-ent authorities (Copp, Bianco et al. 2005; Copp,Russell et al. 2016).

Initially, EU legislation focused on the use of NNspecies in aquaculture, but excluded ornamental spe-cies (European Union 2007), making aquaculture oneof the better regulated pathways for potential NN spe-cies introductions (Copp, Russell et al. 2016). Morerecently, a broader view has been taken to include alltypes of importation, including the aquarium trade(European Union 2014). The aquaculture-specific EUlegislation for regulating the use of NN species, i.e.Council Regulation (EC) No 708/2007 (EuropeanUnion 2007), covers all aquatic species, applies to alltypes of aquaculture installations, and aims to reducethe chance of unintentional introductions or diseasetransmission to native species. The 2007 Regulationbuilds upon over-arching nature conservation legisla-tion, such as Council Directive 92/43/EEC on the con-servation of natural habitats and of wild fauna andflora (EC Habitats Directive), and requires assessmentof potential human-generated impacts including aqua-culture within or near protected areas. The 2007Regulation also provides a framework including riskassessment protocols, prevention, and precautionaryprinciples, as well as contingency plans (EuropeanUnion 2007). The 2007 regulation includes a list ofNN aquaculture species (Annex IV) that are exemptedfrom regulation because of their well-established eco-nomic importance. Most of these species receivedlow-to-medium risk rankings using the ENSARS, theEuropean Non-native Species in Aquaculture RiskAssessment Scheme (Copp, Russell et al. 2016), butCyprinus carpio, Carassius auratus and red swampcrayfish Procambarus clarkii were ranked as high riskof being invasive (Copp, Godard et al. 2016).Individual member states of the EU may disregardAnnex IV status for listed species, or apply this statusto species not listed, depending upon a NN species’national status.

Council Regulation EC 708/2007 has been trans-posed into UK law (see ‘4’ here below), adding weightto existing national legislation to control NN speciesused in aquaculture. There is a suite of UK legislation(with parallels to regulations in other countries of theEuropean Economic Community, especially France,Norway, the Republic of Ireland, and Spain):

1. Council Regulation EC 708/2007 employs a‘white list’, which means all species are subjectto regulation except those listed on theRegulation’s exemption list (the so-called ‘AnnexIV’), which includes species that have been inaquaculture use for an extended period. For newspecies to be added to the exemption list, they

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must comply with two criteria: sufficiently longuse in aquaculture (the number of generations isspecified in the legislation) and the species hasnot been found to have an adverse impact onnative species and ecosystems.

2. Under the Aquatic Animal Health (England andWales) Regulations 2009, it is an offense to oper-ate an aquaculture production business (APB)unless the business is authorized. Authorizationto establish an APB requires risk assessmentsand biosecurity plans and detailed record keep-ing of fish movements, mortalities and any otherrequirements detailed in the farm specific plan.Inspection prior to authorization and duringoperation is required.

3. Authorization to import live fish and shellfishincludes biosecurity plans and risk screeningespecially for disease purposes. Fish health certif-icates are required as part of the process, withstricter scrutiny for products imported from out-side the EU.

4. Under the Alien and Locally Absent Species inAquaculture Regulations, 2011, a permit can beissued to anyone wishing to introduce NN spe-cies, or locally absent species, to an aquaculturefacility. The regulations apply to species listed inAnnex IV of Council Regulation EC 708/2007.

5. Specific forms of permit are in place for thekeeping and release of NN freshwater fishes intoinland waters in England & Wales. Previously,this protection was offered under the Import ofLive Fish Act 1980 (ILFA). For inland waters,ILFA was replaced in 2015 by the Keeping andIntroduction of Fish Regulations (KIFR), whichapplies to species from similar (temperate) cli-matic zones and covers angled and temperateornamental NN freshwater fishes. In contrast tothe ‘blacklist’ used under ILFA, the KIFR 2015employs a ‘whitened blacklist’. In other words,all species belonging to taxonomic Orders speci-fied in Part 1 of the Schedule are subject toregulation except those specified in Part 2 ofthe Schedule.

6. The keeping or release of NN freshwater fishspecies into aquaria or ornamental ponds inEngland & Wales requires a license under theProhibition of Keeping or Release of Live FishOrder 2014, made under ILFA. Exceptions tothis are Cyprinus carpio, Carassius auratus,Leuciscus idus and O. mykiss (note that cruciancarp Carassius carassius now falls into thisexception, recent genetic evidence refuting its

previous native status (Jeffries et al. 2017). Thekeeping of sturgeon of the genera Acipenser orHuso and Ctenopharyngodon idella in ornamen-tal retail premises, indoor aquaria or gardenponds is permitted by a general license, issuedunder the Order. A second general license allowsthe keeping of listed species in indoor aquariafor ornamental, scientific research, or conserva-tion purposes.

7. Under the Wildlife and Countryside Act 1981, itis illegal to release or allow to escape any wildanimal that is not ordinarily resident to, and isnot a regular visitor in Great Britain or if it isspecified in Schedule 9 of the Act.

8. Specific licensing [The Prohibition of Keeping ofLive Fish (Crayfish) Order 1996] made underILFA regulates the keeping and release of NNcrayfish species into the inland waters ofEngland & Wales and for aquaculture purposes– this legislation also covers movement of suchspecies (species listed in the legislative Order asbeing subject to regulation under that Order)between sites in the UK.

9. Further protection is offered to England &Wales under a recent statutory instrument, TheInvasive Alien Species (Enforcement andPermitting) Order 2019, which restricts theimport, keeping and release of alien species ofUnion concern unless permitted or licensed.This order will also revoke the aforementioned(paragraph 8) Prohibition of Keeping of LiveFish (Crayfish) Order 1996.

10. Northern Ireland and Scotland also have add-itional regulations including the MolluskanShellfish (control of deposit) Order (NorthernIreland) 1972 and the Fisheries Act (NI) 1966(specific Fish Culture Licenses are also requiredfor aquaculture beyond business registration, andrelease of fish into fresh waters is prohibited unlessgranted exemption), and the Aquaculture andFisheries Act (Scotland) 2013, which applies tofish and shellfish, fresh and marine, and seeks tomanage interactions between farmed and wild spe-cies. Country-specific policies exist for two mainreasons: Scotland has a large, economically-import-ant aquaculture industry that has come underincreasing pressure from environmental NGO’s,and Northern Ireland in general has stricter con-trols on import and movement of species.

All these policies and related permissions haveassociated penalties imposed if regulations are not

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followed properly. Often these penalties involve revok-ing permission, additional financial penalties, andpotentially imprisonment for the most seriousoffenses. In most cases, the aim of the penalties is topunish financially the business (as well as the individ-ual) associated with the breach.

The main issue with legislation on NN species con-cerns which species should be regulated/assessed(Fowler et al. 2007). The effectiveness of the regula-tions is related to the definitions of NN species used,biogeographic factors, and socio-economic and polit-ical issues (Copp, Bianco et al. 2005). Some Europeancountries have compiled a list of NN species that areforbidden for introduction. Other countries do nothave such comprehensive lists, but rather prefer toconduct case-by-case evaluations before an introduc-tion is consented. Countries such as France andSlovakia have prohibited any type of NN fish intro-duction except those for scientific use and aquaculturein constrained water bodies authorized by the PrimeMinister. In recent years, some specific regulationsfor NN species have been enacted by theEuropean Community.

Enacted in 2014, Regulation 1143/2014 created anupdated list of invasive species deemed of EuropeanUnion concern after robust risk assessments and alsoprovided a comprehensive management systemincluding early-warning and surveillance, pathwaysdiagnosis, rapid eradication, and long-term mitigation(Tollington et al. 2017). The present list (https://ec.europa.eu/environment/nature/invasivealien/list/index_en.htm), which was updated 18 Feb. 2020, containsthree freshwater fish species. Two were enacted on 3August 2016: Amur (a.k.a. Chinese) sleeper Percottusglenii, which is an emerging threat to European freshwaters (e.g. Grabowska et al. 2010; Verreycken 2015),and topmouth gudgeon (listed as stone moroko)Pseudorasbora parva, which is considered one of themost widespread and successful invasive NN fresh-water fishes in Europe (Gozlan, Andreou et al., 2010).A third fish species, Lepomis gibbosus, was added tothe list on 15 August 2019.

The Member States have the flexibility to add ordelete species, especially those not currently present inthe country (Tollington et al. 2017). The ScientificForum, representing the members of the scientificcommunity appointed by Member States, is respon-sible for compiling an independent list of species ofconcern. To be placed on the list, a full risk assess-ment of the species is required, which effectively lim-its the effectiveness of the Regulation to stop new NNspecies from entering the EU (Lehtiniemi et al. 2016).

It is, however, a tough task for scientists and stake-holders to reach an agreement on the NN species list(Genovesi et al. 2015; Tollington et al. 2017; Royet al., 2019), in part because NN species risk assess-ment, according to risk analysis principles, considersadverse impacts only and not potential benefits, whichare the remit of decision makers (Tollington et al.2017). Although this innovative regulation plays avital role in the global response to biological inva-sions, all of society should enhance its awareness ofthe threats posed by NN species and adopt responsiblebehaviors to mitigate the impacts (Genovesi et al.2015; Tollington et al. 2017). Translocations of native/NN fishes are less regulated than international intro-ductions, although political boundaries are lessimportant than geographic boundaries in the defin-ition of biological invasions. Some countries alreadyhave legislative instruments in place (e.g. the abovementioned KIFR 2015) to control translocations andintroductions of species of interest, such as Europeanbullhead Cottus gobio, S. trutta and European graylingThymallus thymallus, either to avoid impacts or foreconomic reasons. Most commercially beneficial fishspecies that have caused degradation of local geneticdiversity are still being transferred despite theseimpacts, and this is evident in the Annex IV exemp-tion list of the EU (2007) Regulation.

4.3. USA and Canada

Like the EU, legislation and policies occur at multiplelevels of government in the USA and Canada, andthey change through time depending on the know-ledge of the mechanism of invasions and of specificinvasive species. Most remarkably, the USA andCanada have enacted international agreements onaquatic NN species, including regulations on ballastwater that have been effective at limitingnew invasions.

Invasive species regulation in the USA involves apatchwork of policies and legislation enacted by fed-eral, state, local governments and tribal nations,although only at the federal level can species fromother countries be denied entry into the country. TheDepartment of Agriculture uses the Plant ProtectionAct of 2000 to regulate the domestic importation ofweeds and plant pests, whereas the Department ofHealth and Human Services has statutory authorityunder the Public Health Service Act of 1946 to pro-hibit entry of species that may pose a risk to humanhealth. Importantly, species that are not considered toimpose direct damage to human health or agriculture

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are rarely regulated under these statutes. TheInjurious Wildlife Provision of the Lacey Act of 1900,provides the US Fish and Wildlife Service with juris-diction to prohibit the importation and interstatetransport of wildlife included in a list of prohibitedtaxa which are “deemed to be injurious or potentiallyinjurious to the health and welfare of human beings,to the interest of forestry, agriculture, and horticul-ture, and to the welfare and survival of the wildlife orwildlife resources of the United States” (Code ofFederal Regulations, title 50, part 16). This provisionof the Lacey Act is still employed as the primary toolto prevent the importation and spread of invasive ani-mal species considered harmful to natural ecosystems(Fowler et al. 2007).

Acts and regulations have been enacted with thegoal of preventing NN species from being introducedvia specific vectors or into specific ecosystems of con-cern. The US National Aquatic Invasive Species Actand its amended version, the National InvasiveSpecies Act, were enacted in the 1990s with the goalof managing NN aquatic species entering inlandwaters through ballast water carried by ships. TheUSA and Canada reached comprehensive bi-nationalagreements on the management of ballast water in theGreat Lakes (summary of Great Lakes ballast watermanagement, 2018). The Great Lakes Fish andWildlife Restoration Act was enacted in 2006 to pre-vent the unintentional and intentional introduction ofsea lamprey Petromyzon marinus. The USA and EUlegislative acts are similar in that both aim to regulateNN species that can or have caused adverse economicand ecological effects. Both focus on the prevention ofimportation and on the control or eradication of inva-sive NN species, despite invasive NN species beingdifficult to eradicate once established (Williams andGrosholz 2008). And both pieces of legislationinclude, retrospectively, species that already existwithin their legislative jurisdictions. For example, theUSA’s Asian Carp Prevention and Control Act (PublicLaw No: 111-307) was enacted in 2010 to prohibit theimportation and shipment of Asian carp species,which had already become established and causedadverse impacts in some regions by that time.Similarly, the initial list of NN species listed for con-trol under the EU 2014 Regulation was comprisedalmost entirely of species already present (and insome cases widespread) in the EU.

Aquatic invasive species easily cross political boun-daries, therefore a weak link problem manifests whenregulations of individual jurisdictions increase theregion-wide risk of species introductions (Peters and

Lodge 2009). Regulations can often vastly differ acrossStates and the vectors of species introduction. Forexample, some western states require that all boats beinspected for invasive species as soon as they crossthe state border, whereas many eastern states do notenforce such regulations. The globally invasiveGambusia affinis, for instance, is regulated differentlyacross states in the US. In Wisconsin, the stateDepartment of Natural Resources prohibits the trans-port or introduction of G. affinis into any waterways.In contrast, local vector control agencies are permittedto introduce G. affinis legally into waterways inCalifornia and some other western states. Landownersare also allowed to introduce G. affinis on privateproperty, and this species is widely distributed at nocost to the public by local vector control agenciesin California.

Canada lacks a national consensus on NN speciesregulations and therefore few protocols and agree-ments have been enacted, with little active enforce-ment to control invasive NN species (Smith et al.2014). Regarding NN freshwater fish species, there isno federal legislation to manage the NN fish trade inthe USA and Canada, though there are some provi-sions in place to restrict the dispersal of potentiallyharmful NN species across provincial/state borders(Thomas et al. 2009). These provisions focus mainlyon the management of aquaculture and baitfish, butwith little concern for the live fish market and pet fishtrade in both countries (Thomas et al. 2009). In gen-eral, although there are some bi-national agreementsfor the management of water bodies stretching overthe Canada-US border to address invasive species (e.g.International Joint Commission, the Great LakesFishery Commission), the USA and Canada have nospecific joint regulations to regulate NN species(Copp, Bianco et al. 2005).

5. Guidelines for the use of decision-supporttools in China

With intensifying economic development and human-induced activities, biological invasions are threateningChina’s biodiversity at an unparalleled magnitude (Liuet al. 2003, 2017; Lin et al. 2015). As part of theConvention on Biological Diversity, China has estab-lished an ambitious plan to control biological inva-sions in the next decades [China National BiodiversityConservation Strategy and Action Plan (2011–2030)],including an objective to “improve capacity of earlywarning, emergency response and monitoring of inva-sive alien species” (Action 23, p. 19–20). Achievement

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of this goal necessitates the development of riskassessments that identify NN species likely to establishand have an impact (Leung et al. 2012).

Decision-support tools have been developed spor-adically by academic groups in China starting in theearly 2000s. In large part, these efforts were adaptedfrom existing decision-support tools, hence someassessment questions were not appropriate for thecases under the current conditions in China. A riskassessment scheme has been developed for aquaticNN species in China based on qualitative assessmentquestionnaires on species’ traits, which includedfecundity, competition, and survival ability (Hu et al.2006). This scheme, however, did not follow the scien-tific framework of invasion (i.e. including transport,establishment, spread and impact) and, more import-antly, did not provide any example of assessment. Inthis respect, more sophisticated assessments based onspecies’ ecological traits associated with specific stagesof invasion have been shown to be beneficial (Howethet al. 2016). For example, seven marine NN specieswere assessed with a risk system based on five pri-mary and 20 secondary indices (Ma et al. 2009);Oreochromis niloticus was assessed using a semi-quantitative assessment system (Dou et al. 2011); anddiscriminant analysis based on 23 biological traitsidentified 15 of 27 assessed species as posing a higherrisk of establishment in the Yarlung Zangbo River(Sui et al. 2016). Although these applications havebeen made regionally on a few species, guidance forthe assessment questions was not provided, calibra-tions were not well performed for the assessmenttools, and the risk identification result was biaseddepending on expert opinion.

A first application of the AS-ISK (Copp, Vilizziet al. 2016) for NN freshwater fishes with regard tothe middle reach of the Yarlung Zangbo River(Tibetan Plateau) in China (Li et al. 2017) found thisdecision-support tool to be a reliable means for identi-fying potential invasive fish species. The AS-ISKcould, therefore, provide a useful tool with which toassist in the future development of NN species legisla-tion and management in China. Overall, this conten-tion is supported by the fact that, relative to otherexisting decision-support tools, AS-ISK (similar to itspredecessor, FISK) has been applied extensivelyworld-wide to a very large number of risk assessmentareas (Vilizzi et al., 2019). The majority of the currentapplications have been to freshwater fishes(Glamuzina et al. 2017; Tarkan, Sari et al. 2017;Tarkan, Vilizzi et al. 2017; Baduy et al. 2019; Doddet al. 2019; Interesova et al. 2020; ZieRba et al. 2020)

but applications to marine species are appearing(Clarke et al. 2020; Killi et al. 2020; Uyan et al. 2020).Of particular note, the AS-ISK is a multi-lingual toolthat offers assessors 32 languages, including simplifiedChinese, with which to carry out and report on theirrisk screening outcomes (i.e. ‘low’, ‘medium’, ‘highrisk’), thus facilitating communication with local andnational environmental managers, stakeholders anddecision-makers in the country’s official language.

Although decision-support tools have been devel-oped by scientists, their integration into national orregional laws and regulations is limited, and they arenot recognized in national-level, round-table discus-sions regarding NN risk strategies in China. Mostlaws and regulations stipulate that scientific assess-ments are required before the introduction of NN spe-cies, but with no risk analysis scheme in place toidentify and evaluate the potential risk of using NNspecies in aquaculture or the aquarium trade.Although an updated list of NN species has been pro-vided by China’s national and regional governments,legislative and/or policy attention appears to havefocused on regulating and eradicating NN speciesalready causing adverse impacts rather than support-ing actions to prevent introductions and transloca-tions. Overall, decisions by governments in China aremore reliant on a case-by-case evaluation than on asystematic protocol for introductions of NN species.

6. Guidelines for improved legislation andpolicy in China

The potential risks and impacts posed by NN fishintroductions and translocations have recently gainedgovernment recognition in China, where this chal-lenge will continue to increase due to the growingnational and international commercial trade of NNfishes. Considering the current status of NN speciesintroductions and fish translocations in China as wellas the legislation status mentioned above, attentionand clarification of the following issues isrecommended.

6.1. Recommendation 1

Establishment of an independent national authority toact as a NN species advisory board and secretariat inChina to advise the ministries and government on theuse of terms to define the invasiveness of NN species,their risk assessment, and management.

Assessments and legislation cannot be effectivewithout consolidated perceptions on the concepts of

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NN, translocated, and invasive species. In China, bio-geographic and ecological considerations could bespecified more in legislation. Species in the updatedList of Alien Invasive Species in China announced byChina’s Ministry of Environmental Protection(Ministry of Ecology and Environment) and theChinese Academy of Science are all introduced fromabroad, and the list does not account for the possibil-ity of translocations. Any intermediate status of anintroduced species before it becomes invasive is farfrom being defined in China, and terms such as‘naturalised’, ‘established’ and ‘acclimatised’ have beenrarely used in the laws, acts or regulations on NNfishes, which may suggest a lack of supervision andresearch on NN species before their introduction toChina. These terms should be therefore clearly definedbefore effective management measures for invasionscan be implemented.

Such an independent authority is urgently neededto coordinate different interests among differentauthorities on the introduction and management ofNN species. This group should have the ability to setup guidelines on risk assessments and should be cen-tralized, hence unlike the currently scattered author-izations in different agencies. Overall, it is a difficultdecision for the government to determine which spe-cies should be regulated whilst considering the differ-ent views of stakeholders, since NN species bring bothinvasive risks and economic benefits, particularly inthe aquaculture and aquarium industries. Executivepower will be diminished if the agency in charge ofthe regulation of NN species is also responsible forenhancing aquaculture production or the aquariumtrade. For example, the Center for Management ofInvasive Alien Species is affiliated with China’sMinistry of Agriculture and Rural Affairs, which isalso responsible for production enhancement. Theexisting laws and regulations are vague and withoutpractical protocols due to greater priority given toeconomic concerns, and some species with high riskof invasiveness are still being introduced (Martin et al.2010; Zengeya et al. 2013). A scoring system could beused to classify the NN species in China according totheir degree of benefits and negative impacts, with theresult of the NN species being categorized as inconse-quential, destructive, beneficial or conflict-generating(Zengeya et al. 2017). Corresponding managementactions can be done considering the protection of eco-systems as well as the needs of different stakeholders.For example, just like Salmo trutta and Oncorhynchusmykiss in South Africa, Oreochromis niloticus (awidely-cultured NN freshwater species in China)

could possibly be identified as a conflicting speciesbecause of the risk perception and socio-economicbenefits derived from the tilapia industry (Cui 2008).Further consensus should be reached among stake-holders to propose better management strategies forsuch conflicting species.

Additionally, such an independent authority wouldprovide recommendations that focus on the full inva-sion process, namely: (i) prevention of biological inva-sions by a process of risk identification (including NNspecies and vectors) and assessment before the intro-duction of NN species; (ii) eradication of the invasivespecies after its introduction at the early stage; and(iii) control of the distribution of NN species within acertain range to minimize any adverse effects. Thiscould apply to species that have already establishedbut cannot be eradicated (e.g. to reduce translocationrisk) or for control within aquaculture/research facilities.

The main vectors of introduction of NN speciesinto China are currently aquaculture and the aquar-ium trade. Once successfully established in the coun-try, translocations of a NN species also occur forthese reasons as well as for freshwater fisheriesenhancement. Therefore, it would be prudent to focuson regulations and management of these vectors.Different provinces in China have different interpreta-tions and levels of implementation of national laws,and the methods are not consistent when risk assess-ments are undertaken. This suggests that a generalunderstanding of the impacts of NN species isrequired at the provincial and lower government level,both by relevant businesses (especially larger-scaleimporters) and the public. In addition, the nativeranges of fishes in China need to be clarified to pre-vent invasions by translocated species.

6.2. Recommendation 2

Enforcement of regulatory control and monitoring pro-grammes is needed at different levels of political units

Risk assessment, eradication and control of NNspecies will not be effective without proper enforce-ment of the enacted laws and regulations. Suchenforcement is weak in China, especially at provincialor lower levels. A constraint in the development oflegislation and policies for translocated species is theneed for a nationally-applicable list of AIS, and this isbecause species translocated within China are notincluded. To address this, provincial and local govern-ments could add species to, or exempt species on, thenational list in a manner similar to Europe’s Council

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Regulation (EC) No 708/2007 (European Union2007), which allows Member States to adapt theRegulation’s list of exempted species (Annex IV)according to national circumstances (see Section 4.2).The Bureau of Fisheries under China’s Ministry ofAgriculture and Rural Affairs is the only enforcementagency for NN fish in China, but it is also limited bythe political boundaries that separate a single riverinto different sections. Also, responsibility is vaguedue to staff shortages in the Bureau of Fisheries.Fortunately, in recent years, the River Chief Systemwas established to promote the construction of‘ecological civilisation’ in China. This is an institu-tional innovation for river and lake management andprotection responsible for the protection of waterresources, control of water pollution, improvement ofwater environments, and treatment of polluted water.The list of enforcement actions within provincial orcounty-level directives needs therefore to include ameans of mitigating NNS impacts.

Long-term monitoring and control programmesmay also be needed, regardless of any success in inva-sive species eradication and control. For example, theSea Lamprey Control Program administrated by theGreat Lakes Fishery Commission was established tomonitor and control the population of invasive P.marinus. Although eradication of this species in theGreat Lakes’ tributaries was successfully conducted inthe past, the targets were still set in a five-year perioddepending on the annual mortality rate of lake troutSalvelinus namaycush, and annual reports were alsoprovided on the control efforts (Sullivan and Mullett2018). Invasive status has been effectively monitoredunder such protocols and management strategies.

6.3. Recommendation 3

Establishment of panels of experts that report to theNN species secretariat is needed, focusing on: (i) thedevelopment of a generic NN species risk analysisscheme; (ii) early risk detection and rapid response;(iii) risk communication and public engagement (i.e.citizen science); and (iv) infectious agents hosted andtransmitted by NN species.

Although awareness and general understanding ofthe impacts of NN species has already been raised inChina, legislation, policy, risk analysis and manage-ment of NN fishes are still to be improved. Therefore,international experience is being sought to avoidnegative ecological and economic losses and to pro-pose future strategies with which to manage NN spe-cies in China. To achieve the above objectives, a clear

definition of terms is needed as part of a program ofstudy of freshwater fishes to determine the geograph-ical ranges of native species and the current distribu-tions of NN species. This would enable some clarityin the production of defined native and NN specieslists (at national and biogeographic scales) andenhance our understanding of which species are inva-sive. Also, there is need for a comprehensive review ofthe existing legislation in China with regard to aqua-culture and relevant to the management of NN spe-cies, with specific attention to the two key pathwayvectors (i.e. aquaculture and aquarium trade) in orderto reduce the risks and impacts of NN species fornative species and ecosystems.

7. Conclusions

The positive and negative consequences of NN speciesare difficult to identify and sometimes impossible toquantify, both generally (Mack et al. 2002) and specif-ically for fishes (Vilizzi et al., 2019). Therefore, cat-egorization of a species as ‘non-invasive’ or ‘invasive’is the initial and important stage when developingmanagement strategies. Scientific assessments andcontinuous surveys are therefore necessary to manageNN species successfully. National awareness of NNfish management has been rising in China, and thenational framework of management of NN species isin the process of being established. In this respect,Chapter IV, Article 26 of the Fisheries Law of thePRC in 2019 states that necessary protective effortsshall be taken to prevent escape of aquatic NN speciesand hybrid species used in aquaculture thus avoidingecological risks. This means that the government hasbegun to enhance the management of NN fish byamending the legislation, use appropriate strategies toguide the fishery-related industries, and also avoidfish invasion. NN fish already account for a large pro-portion of aquaculture activities in China and raisesconcerns that most rearing facilities may need moremodification work to prevent NN fish from escaping.Therefore, the enforcement of the legislation shouldbe enhanced, and this could include the establishmentof a thorough risk analysis mechanism, includingnecessary mitigation measures and continuous moni-toring before the introduction of NN fishes, both dur-ing the early stage of invasion and following theirestablishment.

With the Silk Road developing, international tradewill be more prosperous than ever, and NN species,including fishes, will be transferred more and morefrequently. As a result, China is facing greater

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challenges in the management of NN fishes. Since the18th national congress of the Communist Party ofChina, the top-level design and institutional construc-tion of ‘ecological civilisation’ have accelerated, andonly through joint management with profits of mem-ber countries and regions, can rational and effectiveNN management strategies be implemented.

Acknowledgements

The final manuscript benefited greatly from the commentsof two anonymous reviewers.

Funding

This work was supported by Shanghai Natural ScienceFoundation (19ZR1434200). The participation of HW wassupported by Central Public-interest Scientific InstitutionBasal Research Fund, CAFS (Grant No. 2018GH11), andthat of GHC and SC by Cefas’ Science Excellence andrelated funds.

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