Alien fishes are regarded as one of the major causes of the decline of aquatic fauna and biodiversity. Up to now, more than 500 fish species have been introduced into China from other countries. However, nationwide documentation of the established alien fishes is still lacking and their ecological risk is unclear. We compiled a comprehensive inventory of the colonized alien fish species based on various sources, and then provided a summary of their potential ecological risk. The results indicated that 68 alien fish species (13.44%) have successfully established in the natural waters. These species belong to 12 orders and 29 families. Among them, 56 species (82.35%) were introduced for aquaculture purposes, 11 species (16.18%) were introduced for aquarium and one species (1.47%) was introduced for bio-control. Over 85% of the established fishes were introduced after the 1970s. Geographically, these species are native to 12 regions around the world. Eighteen species and two hybrid species are native to North America which is the most dominant donor. Among these species, 61 can live in freshwater, 41 species can live in brackish and 19 species can live in marine water. Although large number of species, high taxonomic diversity, intensive human activity, diverse geographical origins and high adaptability of non-native species may lead to the increase of invasion risk, previous research about invasive risk just focus on the general impact of aquaculture activities, invasiveness screening using semi-quantitative models and distribution prediction using species distribution models. Further studies will need to be conducted on comprehensive risk assessment, ecological interaction between non-native fish and new environment, on fish species, ecosystem, the impact of human activity and global change on non-native fish colonization.
Fish are the most frequently introduced aquatic animal group and alien fishes are regarded as one of the major causes of the decline of the native aquatic fauna (Vitule et al., 2010). Establishment and spread of non-native (NN) species is one of the key factors leading to a dramatic reconfiguration of modern biodiversity. Species introductions and extirpations have resulted in the change of China’s freshwater fish fauna over the past century. China harbors a relatively high biodiversity with at least 752 endemic fish species (Zhang, 2016). Nevertheless, the established alien fishes have extensive influences on native fish community in the main drainages in China (Zhang, 2016; Liu et al., 2017). A total of 439 freshwater fish species have been introduced to China from other countries (Xiong et al., 2015). Although the extent of negative effects of NN fish are increasing in recent years, ecological risks raised by these NN fishes have been overlooked and most research only focus on freshwater fish (Lin et al., 2015). Additionally, there is limited nationwide documentation for the NN fishes which have established self-sustaining population in China, as well as their eco-economic risk.
Colonization is the occupation of the habitat by a community. It is a dynamic process that begins when habitats are available, or when organisms have the ability to survive and reproduce through a process of adaptation (Gargaud et al., 2011). Biological invasion, in most cases, is a process which comprises several successive stages, including colonization, competetion and spread. Fish introduction process includes transportation, domestication and breeding and NN fish species may be released or escape from captivities in this process. Some individuals may establish self-sustaining populations in natural waters, and then spread in drainages (Closs et al., 2016). There would be a rapid diversification after the NN fish colonization (Moser et al., 2018). Thus, colonization is an intermediate stage which is the key information for taking effective strategies to manage NN fishes. In this respect, NN fish species which have colonized in the natural waters are in the top priority to be assessed their ecological risks.
China has abundant water body types and climate patterns, which provided a highly diverse habitats for aquatic species (Li et al., 2015). However it has being severely affected by aquatic invasive species. But risk assessment for NN fish has been merely conducted. As a result, it is extremely urgent to conduct risk assessment to aquatic NN species, especially for NN fishes through existing risk assessment protocol or newly developed methods (Wan et al., 2017). Risk assessment comprehensively combine a series of factors to analyze the impact, screen the invasiveness, predict the potential distribution, display the invasion scenario, which can help decision makers to develop management measures for invasive species. Therefore, what is the latest comprehensive colonizing pattern of the introduced fish in China? How about their related potential risk?
The purposes of this study were to: (1) compile a comprehensive inventory of the established alien fish species, which were introduced into China from other countries. We investigated and analyzed the number of colonized species, their taxonomic diversity, introduction history and purpose, geographic origin and adaption to local environment. And (2) review the ecological risk of the fish species compiled in this study.
The definition of established alien fish species
Biological colonization is a dynamic process. Species can colonize when habitats or territories are available, or when the organisms were able to survive and reproduce under new environmental conditions through adaptation (Gargaud et al., 2011). It begins with the arrival of the NN individuals and ends when the extinction probability of the population is no longer dependent on the initial population (Ebenhard, 1991). Here, we defined all the established fish species as colonized species no matter they colonized in small extent or large extent. Non-native species refers to species which has been introduced to areas beyond its native range (Kolar et al., 2001; Xiong et al., 2015). This study focused on non-native fish species which established self-sustaining population in natural waters after their introduction into China from other countries. Fishes species which were translocated within China, were not included in this study. Fish species (e.g. Lates calcarifer and Takifugu rubripes) which were recorded to be introduced from other countries, but native to China, are also not included in the study.
The data were obtained from comprehensive documentary surveys, including peer-reviewed papers, monographs and dissertations on fish resource investigation, combined with internet sources and field investigation. Geographically, drainages and administrative divisions are also used as key words to search and identify the colonized fish species. Data from field investigations and government reports are included. Expert consultation was also used to confirm those uncertain species. Both freshwater fish and marine fish were included in the compiled inventory. The taxonomy, scientific and common name, origin and the purpose of introduction were summarized in the inventory (Appendix; Table 1). The number of species in each taxonomic group was analyzed.
According to our research, 568 species of aquatic animals have been legally or illegally introduced into China, including 506 fish species. There were 68 alien fish species established in the natural waters in China (Appendix; Table 1). In the view of phylogenetic classification and ordinal memberships, these species belonged to 29 families and 12 orders, including 10 speceis in Cichlidae, eight species in Cyprinidae, eight species in Salmonidae, five species in Centrarchidae, four species in Clariidae and four species in Moronidae, which represented 57.35% of the colonized species. Although these species scattered in 12 orders, the top four orders, including Perciformes with 25 species, Siluriformes with 10 species, Cypriniformes with nine species and Salmoniformes with eight species, represented 76.47% of the established alien fishes.
Despite some species have multi-introduction history, current data indicated that fish introductions began at the 1920s and peaked at 1980s (Figure 1). Three quarters (51 species) fishes were imported during the 1970s to 1990s and eight species were introduced after 2000s. 86.76% of the established fish were introduced after the 1970s. All established fish species were introduced for aquaculture, aquarium and bio-control purposes. Among them, 56 species (82.35%) were introduced for aquaculture purposes, 11 species (16.18%) were introduced for aquarium purposes and one species (1.47%) was introduced for the bio-control purposes (Figure 2a).
These species originated widely from 12 regions around the world. Most (54 species, 79.41%) were native to North America, Asia, Europe, Africa and South America (Figure 2b). North America where18 species and two hybrid species origin from, was the pool of established NN fish species in China. According to the characteristics of the colonized fish species in the current research, they can adapt to five types of habitable water milieu (Figure 2c). Twenty-six species are purely freshwater fish. Twenty-three fish species can live in both freshwater and brackish habitats. Twelve fish species can adapt to marine, freshwater and brackish habitats. Six species can adapt themselves to both marine and brackish habitats and one species are purely marine fish. To sum up, sixty-one established species could live in freshwater, forty-one species could live in brackish and nineteen species could live in marine water.
Although 68 NN fish species have established in China, high biodiversity, and intensive human activity and high adaptability of non-native species may increase the ecological risk of these species. Research regarding risk assessment of NN fish had been insufficiently conducted in recent years. A review paper presented four main aquaculture activities or related events of transfers, accidental introductions, artificial hybridization and mass release for ranching of NN species, and provided corresponding risks for each human activity on fish introduction and invasion (Lin et al., 2015). The Oreochromis niloticus and Hypostomus plecostomus were reported to compete with native species and affect algal community and indigenous snails in mangrove due to their relative high genetic diversity and generalist feeding habits (Wang, 2010). Invasive mosquitofish (Gambusia affinis) was reported to compete with native white cloud mountain minnow (Tanichthys albonubes). It suggested that alien fishes had a strong effect on reproductive activity and population growth of indigenous species (Chen, 2010). The invasion of Pterygoplichthys spp. resulted in decrease of economic important taxa in the rivers (Wei et al., 2017).
A large number of alien fish species were found in natural waters in the fish resources investigations (Fan et al., 2016). However, only a few studies had deliberately explored the ecological risk of fish invasion on native ecosystems (Chen et al., 2017). Recent study revealed the differences on functional diversity between native and NN fish species, may result in decrease of species richness and functional diversity in Pearl River (Shuai et al., 2018). The escape of NN cultivated sturgeons may lead to negative impact on native ecosystem in Yangtze River (Gao et al., 2017).
The impacts of fish invasion were merely reported until 2000. A environmental simulation model was used to assess the ecological risk of NN species in 2006 (Hu et al., 2006). Alien invasive species lists were published by Ministry of Ecology and Environment of the People's Republic of China (MEEC) and Chinese Academy of Science in 2003, 2010 and 2014. Pterygoplichthys pardalis, Pygocentrus nattereri and O. niloticus were listed as alien invasive species in 2014 (Luo et al., 2015). A technical guideline of assessment on environmental risk of alien species was also published by MEEC in 2011. In the same year, a quantitative risk assessment system for NN fishes were designed (Dou et al., 2011). This system, consisting of five first-grade indicators, twelve second-grade indicators and forty-four third-grade indicators, as well as weight of each indicator was used to evaluate the ecological risk of O. niloticus in Hainan and Jiangsu province respectively. A risk assessment model was constructed to assess the invasion risk of NN marine species (Wang et al., 2014).
In recent years, more and more new models were used to assess the ecological risk of NN fishes. The effect of environment factors on O. niloticus larval abundance was evaluated by using high-resolution monitoring time-series data and redundancy analysis. Furthermore, the invasion risk of O. niloticus in a subtropical river was predicted by using a univariate approach (Shuai et al., 2015). The invasion risk of mosquitofish (G. affinis) and Mozambique tilapia (Oreochromis mossambicus) introduced to Lixianjiang basin was evaluated by using Fish Invasiveness Screening Kit (Yang et al., 2012). The global distribution prediction of two invasive fishes (Pseudorasbora parva and Carassius auratus) was conducted by using Maxent (Zhang et al., 2014). A software was developed by using C# and GIS’ secondary developing module-ArcGIS Engine to predict the global potential distribution of P. pardalis (Yao et al., 2019). Aquatic Species Invasiveness Screen Kit was applied to assess the risk of NN fish in Tibet and Middle and Lower reaches of Pearl River and the thresholds which used to determine the invasiveness were calibrated respectively (Li et al., 2017; Wei et al., unpublished data).
China has abundant fish diversity, which harbors 1 513 native freshwater fish and more than 3 100 marine species (Kang et al., 2014; Liu et al., 2017). The present study indicated that 68 alien fish species have colonized in the natural waters of China. In terms of quantity, the colonized alien fish account for more than 4% of the native fish species. 13.44% of NN species have established self-sustaining populations in the natural waters, which is not consistent with the hypothesis of Tens Rule that the probability of a non-native species become established in the introduced range. So ecological interaction between introduced species and environments in introduced ranges should be detected though experimental or empirical models. Moreover, the impacts of established introduced species should be properly understood (Jarić and Cvijanović, 2012). A quantitative meta-analysis indicates that about 50% the NN vertebrates are successful in taking consecutive steps of the invasion process (Jeschke and Pyšek, 2018). Therefore, it is likely that the number of both established and invasive species will be larger than we expected and the number will also change over time.
A total of 1 363 native inland fish species in 47 families and 17 orders were recorded in China by 2014. Among them, 75% species were in Cypriniformes, 11% species were in Siluriformes, 8% species were in Perciformes and 1.5% species were in Salmoniformes (Zhang, 2016). By contrast, the established NN fish species mainly belong to Perciformes, Siluriformes, Cypriniformes and Salmoniformes, which is different from species composition of native fishes. So, the established NN fish would pose great threats to the indigenous fish’s diversity through competition with native species for habitats and food resources, as well as prediction. Further studies should be conducted to clarify taxonomic and functional differences.
Numerous studies had confirmed that aquaculture is one of the main vectors for NN fish introduction (Lin et al., 2015). The present study found that more than 80% of the colonized species were introduced for aquaculture and 75% of the fish were imported in the 1970s to 1990s. Both the number of species and introduction history were consistent with the development of aquaculture in China. It is reported that 111 non-native aquaculture-related fish species were introduced to China (Lin et al., 2015). Thereinto, 50.45% (56 species) introduced aquaculture fish species and 3.17% (11 species) introduced aquarium fish established self-sustaining populations (Xiong et al., 2015). It is estimated that at least 1 500 species of freshwater fish were regularly imported into the USA for the aquarium purpose in the early 1980s (Zanden et al., 2015). Over 1 000 exotic species have been imported as ornamental species in Thailand, which is one of the main sources and pools of ornamental fish importation and exportation in China (Vidthayanon, 2005). Thus, the proportion of the finally colonized alien fish might be much bigger in aquaculture than that in the aquarium. Therefore, although introduction of alien species has great contribution to aquatic production, in turn promoted economic growth, these activities can lead to colonization and spread of NN fish in natural waters. The ornamental fish trade is also an important pathway for fish introduction. The threat from ornamental fish is not negligible, due to its huge species numbers (Chan et al., in press).
Most species have relative short introduction history. They were introduced in the near future, even if the history could date back to 1920s. Eight species which established in natural waters were introduced two decades ago. Aquaculture, aquarium and bio-control are the main vectors for the introductions of these established fish. However, attentions should also be paid to the other sources, such as the game and bait fishes, scientific releasing fishes and transgenic fishes in the future (Closs et al., 2016). Sometimes, the established fish species were even more than the endemic fish species in waters of both plateau lakes and island waters (Liang et al., 2006, Ding et al., 2017). Fifteen new freshwater fish species were discovered in between 2015 and 2018 in China. There is such a possibility that the widely established exotic species would threaten the rare fish before it was discovered.
China is one of the largest countries in the world, spanning from 4° 15' N to 53° 31' N in latitude and from73° 40' E to 135° 50' E in longitude. The territory extends approximately 5 500 km from north to south and 5 200 km from west to east (Kang et al., 2014). The primary watersheds and ecological regions are very rich in climatic diversity. That may be one of the reasons why these many fishes can widely adapt to the environment of China. It is worth noting that North America, as the dominant origin of the established exotic fish species, has relatively high climatic similarity with China. For these reasons, climatic similarity would be an important factor which driving the colonization of NN fish. This theory has been widely used in predicting the potential geographic distribution of NN species in China (Valeriano et al., 2015; Wang et al., 2018). Besides, the number of established fish species were more than the endemic fish species in plateau lakes or island waters which harbors a large number of rare and endemic species (Liang et al., 2006, Ding et al., 2017).
More species in marine ecosystems are considered to be resistant to fish invasion with strong effects of resource availability. Decreasing native diversity will increase the survival and final percent cover of invaders (Stachowicz et al., 2002). The colonized marine fish species were much less than freshwater fish in this research. Except for the possible screening bias from criteria and information integrity, this pattern was consistent with the introduction efforts and the native fish biodiversity. Even though, the present study also found that the established species have very high adaptability to salinity in waters. Approximately 90% (89.71%) of the colonized fish can live in freshwater, 60% (60.29%) of them can live in brackish and 30% (27.94%) of them can live in marine water. Compared with freshwater fish, the previous invasion research on marine fish and estuarine fish is seriously inadequate in China. These results implied that fish invasion should also be taken into consideration in estuarine and coastal water bodies. NN fish which can tolerant a wide range of salinity may facilitate their colonization in estuarine water bodies (Jud et al., 2015). The width of ecological amplitude would affect the adaptability and distribution of the species.
The introduced alien fishes is a double-edged sword, which can significantly improve aquatic food supplying and may cause severe adverse impacts on local eco-economic systems (Xiong et al., 2015). Once they established self-sustaining populations, these species may lead to negative impacts including hybridization, competition for food and habitat, predation and ecosystem alterations. The rainbow trout (Oncorhynchus mykiss) which escaped from capacities, had established and spread in the upstream of Yellow River. Coregonus peled, Oreochromis sp. and Clarias gariepinus had also established wild populations and had become dominant populations in several reservoirs in Yellow River Basin. The native Yellow River carp (Cyprinus carpio) hybridized with the introduced mirror carp (Cyprinus carpio var. specularis) and the hybrid offspring widely spread in the Yellow River Basin (Li et al., 2008).
Above all, risk screening could be conducted to provide information for preventing high-risk species introduction and eradicating invasive species (Copp, 2013). Systematic assessment tools could be used to identify highly invasive NN fishes in conservation of fishery resources (Li et al., 2017). Niche modelling (i.e. environmental niche modeling or species distribution modeling) have been widely used in ecology and biogeography. It was widely used to forecast the potential distribution of invasive species in predicting species distribution. Environment, specific interaction and dispersal ability were the main parameters which could affect the accuracy of the models (Elith and Leathwick, 2009). Further research could be conducted on comprehensive risk assessment, ecological interaction between NN fish and new environment, the impact of human activity and global change on NN fish colonization. For example, the intraspecific variation in niche space was positively correlated with species richness. So niche processes could be a useful predictor for the management of the established fish species (Faulks et al., 2015; Li et al., 2015), while combination of the introduction efforts and environmental niche models could be an effective way to predict the invasion risk (Cynthia and David, 2002; Herborg et al., 2007). The fish assemblage and phenotypic plasticity of critical traits (e.g. life history traits) are also key factors affecting the relationship between colonization and invasion (Szuwalski et al., 2017; Moser et al., 2018). Additionally, new methods, such as eDNA and response metrics, could be conducted in early warning or rapid response activities (Kemp et al., 2018).
We thank Dr. Chunlong Liu for supplying some useful references. We also appreciate the anonymous referees for their insightful questions, comments and suggestions.
This research was supported by the National Natural Science Foundation of China (31600446), National Key R&D Program of China (2018YFD0900901), the Natural Science Foundation of Guangdong Province (2016A0303 13145), the Central Public-interest Scientific Institution Basal Research Fund CAFS (2019G H09) and Agricultural Biological Resources Protection and Utilization Project (2130108).
Supplementary material for this article can be accessed on the publisher’s website.