Zoonotic parasites carried by invasive alien species in China.

BACKGROUND: The invasive alien species may lead to great environmental and economic crisis due to its strong capability of occupying the biological niche of native species and altering the ecosystem of the invaded area. However, its potential to serve as the vectors of some specific zoonotic pathogens, especially parasites, has been neglected. Thus, the damage that it may cause has been hugely underestimated in this aspect, which is actually an important public health problem. This paper aims to discuss the current status of zoonotic parasites carried by invasive alien species in China. MAIN BODY: This review summarizes the reported zoonotic parasites carried by invasive alien species in China based on the Database of Invasive Alien Species in China. We summarize their prevalence, threat to human health, related reported cases, and the roles of invasive alien species in the life cycle of these parasites, and the invasion history of some invasive alien species. Furthermore, we sum up the current state of prevention and control of invasive alien species in China, and discuss about the urgency and several feasible strategies for the prevention and control of these zoonoses under the background of booming international communications and inevitable globalization.
CONCLUSIONS: Information of the zoonotic parasites carried by invasive alien species neither in China or worldwide, especially related case reports, is limited due to a long-time neglection and lack of monitoring. The underestimation of their damage requires more attention to the monitoring and control and compulsory measures should be taken to control the invasive alien species carrying zoonotic parasites.

Multilingual abstracts

Please see Additional file 1 for translations of the abstract into the five official working languages of the United Nations.

Background

Invasive alien species (IAS) are non-native species introduced deliberately or unintentionally outside their natural habitats where they become established, proliferate and spread in ways that cause damage to a wide range of interests [1].

The screening and monitoring of IAS is of urgent requirement due to its potential capability to damage ecology, economy and most alarmingly, public health. Probably because of the absence of its predators and the great adaptability to different environments, IAS invade and occupy the ecological niche of the native and destructs local biodiversity. Giving its catastrophic nature, IAS have already been regarded as the second greatest factor of species extinction and endangerment [2]. Additionally, the economic loss associated with IAS sums up to about 120 billion dollar/year in the United States of America [3]. The economic loss caused by IAS was estimated nearly 19.8 billion CNY in China [4]. However, the risks from IAS to public health have been neglected. The IAS themselves can impair human health directly. For example, a sting of red imported fire ant (Solenopsis invicta) can cause severe anaphylactic reaction to human beings [5]. In addition, as either the vector or reservoir host of parasites, IAS will carry not only the native parasites, but also the non-native ones, which may threaten the public health, and delay the diagnosis and treatment simply due to the unfamiliar of the native doctors to the pathogens.

With a vast territory of approximate 9.6 million square kilometers covering almost all ecosystems in the world, there are always suitable habitats for many non-native species in China. In addition to a long history of the introduction of non-native species, the rapid development of economy, technology and transportation system since Chinese Economic Reform has also greatly increased the risk of biological invasion by non-native species, accompanied with the increasing in population density and trading activities.

In 2017, according to the Database of Invasive Alien Species in China (www.chinaias.cn) published by Center for Management of Invasive Alien Species, Ministry of Agriculture, a total of 270 invasive alien animal species have been recorded, including one myxozoa, 14 moss animals, one annelid, one echinoderm, 17 nematodes, 20 mollusks, 153 arthropods (140 insects), six ascidians, 34 fishes, four amphibians, three reptiles, six birds, 10 mammals.

About two thirds of the invasive alien species were introduced intentionally [6]. Before the concept of biological invasion were widely accepted, the species introduction was mainly focused on socioeconomic benefit. It was not until middle of 1990s when several Chinese scientists’ papers introduced the concept and impact of IAS that the government and the public began to take actions to deal with the problem of IAS. For such a long time, the impact of IAS had been neglected, especially their impact on public health [7]. As vectors of native pathogens, expanding IAS may lead to an increase of infection rate. [8]. What’s worse, the novel non-native pathogens introduced by these IAS may even cause an outbreak in the native populations. More attention to these parasites should be aroused [9]. This paper aims to discuss the current knowledge of zoonotic parasites carried by invasive mollusks, arthropods and vertebrates in China, mainly focusing on the category, clinical aspects and administration and international cooperation to prevent and control the problems.

Invasive alien mollusk harboring zoonotic parasites

Most mollusks IAS capable of carrying parasites and transmitting parasitic disease are freshwater snails and human may be infected by ingesting raw or undercooked snail. The most common species include the Pomacea canaliculata, Achatina fulica Bowditch and Biomphalaria straminea (Dunker).

Pomacea canaliculata

P. canaliculata, which is commonly known as golden apple snail, originated from Argentina, was first introduced into Taiwan in the 1970s and mainland China in 1981 [6] as edible material [10]. With its wide tolerance toward different environments and high reproduction rate, the snail exhibits the capability to establish wild populations rapidly in new habitats [11]. And it has already spread to at least 16 PAM (province/autonomous region/municipality) in China including Taiwan, Guangdong, Guangxi, Fujian, Zhejiang, Jiangsu, Shanghai, Hubei, Jiangxi, Liaoning, Beijing, Anhui, Sichuan, Chongqing, Gansu, Tianjin [12].

Based on the biology of the snail and the meteorological database of 670 weather sites distributed all across China during 1951–1980, the researchers worked out a model to predict the potential habitat for the species. The model suggested that about 52.1% regions represented by the above weather sites (about 2 563 000 km2) were vulnerable to the colonization of the P. canaliculate [13]. Considering the future climate change and the inevitable trend of global warming, an area of approximately 378 700 km2 is expected to be occupied by P. canaliculata from the 2020s to the 2030s, in which the distribution could move further northeast, even covering the Huaihe River valley [12]. The P. canaliculata poses a huge threat to the agriculture industry as well. It is reported to be potential pest for 15 important economic agricultural crops in China [14]. Also, P. canaliculata is able to spread rapidly into wetland [15] and other freshwater ecosystems, resulting in severe habitat modification and a decrease of local biodiversity [16].

Apart from its direct destruction to the ecosystem, P. canaliculata is able to impair the human health directly as the intermediate host of several parasites such as Echinostoma revolutum, Angiostrongylus cantonensis and Gonathostoma spinigerum which respectively cause echinostomiasis, angiostrongyliasis and gnathostomiasis [17].

Angiostrongyliasis is the most common cause of eosinophilic meningitis in southeast Asia and the Pacific basin [18] and usually results from consuming the undercooked snail or other mollusk which carry the infectious larvae of A. cantonensis [19]. The first case reported came from Taiwan in 1945 [20], and was first discovered in Guangdong Province (mainland China) in 1984 [21]. From 2000 to 2006, six outbreaks has attracted the public’s attention [22], among which the most serious one occurred in Beijing in 2006 involving 160 infected and 100 hospitalized [23].

Echinostomiasis is caused by orally intaking the metacercaria of the family Echinostomatide via the raw or undercooked infected snails [24]. The number of involved provinces in mainland China had reached eight by 1994, including Heilongjiang, Sichuan, Yunnan, Zhejiang, Fujian, Hubei, Guangdong, Anhui [25]. In some coastal provinces like Fujian and Guangdong where edible snails are easily accessible, the prevalence of the disease even reaches 5.0% [26].

G. spinigerum is another parasite that may be carried by P. canaliculata [27]. Nevertheless, it is unusual to find a patient infected after consumed the snail. Almost all the cases reported in China got infected by the raw or undercooked fish and the incidence is rather low. From 1919, when index case in China came out to 2011, only 73 cases covering 16 PAM were reported, among which Zhejiang, Shanghai, Fujian, Guangdong had higher incidence [28].

Achatina fulica

Another invasive mollusk capable of transmitting parasites is the A. fulica, also known as giant Africa snail. It is firstly discovered in Xiamen, Fujian Province in the plant carried by a Singapore overseas Chinese in 1931 [29]. After settling down in Xiamen, it began to scatter in southern part of mainland China including Guangdong, Hainan, Guangxi. It invaded Hong Kong, Macau in 1932 and Taiwan in 1933 [30]. The snail in Yunnan was introduced in 1979 from Vietnam [31].

Its various trophic preference and high reproductive ability make it pest for many agricultural crops and ornamental plants. The rapid establishment and expansion can jeopardize the biodiversity and impair the local plants and animals [32]. Besides, it is capable to carry many pathogens which harm human health directly such as A. cantonensis [33]. Due to its biological characteristics, A. fulica is even more vulnerable to the infection of A. cantonensis than P. canaliculata. A survey conducted in Jiangmen, Guangdong Province indicate that the infection rate of A. fulica and P. canaliculata by A. cantonensis reached 41.9 and 1.8%, and the degree of infection was 1–928 per snail and 1–29 per snail respectively [34]. But the threaten caused by A. fulica are not as severe as the P. canaliculata because of its terricolous feature [22]. A. fulica can be infected by the A. costaricensis larvae under laboratory condition, so the snail can be the intermediate host of A. costaricensis as well [35]. However, no relevant case has been reported in China yet.

Biomphalaria straminea

B. straminea attracts attention as the intermediate host of Schistosoma mansoni, which may lead to schistosomiasis [36]. The B. straminea, originated from South America, was first discovered in Hong Kong in 1974 and was thought to be introduced abroad. Later in 1981, it appeared in a pond in the Luohu District of Shenzhen City, which was the first report in mainland China [37]. By 2013, the snail had spread in large range of Shenzhen and overspread to the surrounding regions such as Dongguan and Huizhou in Guangdong Province [38]. While no infection of B. straminea by Sc. mansoni in China has been detected, Sc. mansoni infection in the returnees of China from Africa is increasing in recent years [39]. Because Shenzhen and surrounding regions are key area of labor exporting with large population mobility and numerous international communications, some experts presumed that China is now equipped with the objective condition for the prevalence of Sc. mansoni [40]. B. straminea was also found capable of carrying the larvae of A. cantonensis in Brazil, which may cause angiostrongyliasis but there is no such a case reported in China yet [41].

The information concerning the invasive alien mollusks and the parasites carried by them worldwide is listed in Table 1.

Table 1

Zoonotic parasites carried by invasive alien mollusks

Species	Common name	Parasites	Reference
Mytilus galloprovincialis Lamarck	Mediterranean mussel	Cryptosporidium parvum	[111]
		Giardia duodenalis	[112]
		Toxoplasma gondii	[113]
Dreissena polymorpha	Zebra mussel	Acanthamoeba spp.	[114]
		Cryptosporidium spp.	[115]
		G. duodenalis	[116]
Pomacea canaliculata	Golden apple snail	A. cantonensis	[19]
		Echinostoma revolutum	[24]
		Gonathostoma spinigerum	[27]
Achatina fulica Bowditch	Giant African snail	Angiostrongylus costaricensis	[35]
		A. cantonensis	[33]
Biomphalaria straminea Dunker		Schistosoma mansoni	[36]
		A. cantonensis	[117]

Invasive alien arthropods harboring zoonotic parasites

Invasive alien crustaceans harboring zoonotic parasites

Procambarus clarkii, also commonly acknowledged as the red swamp crayfish or red swamp crawfish, is the native species of North America [42]. It was introduced to Japan in 1918, and then brought into Nanjing, China in the 1930s during the Second World War from Japan [43]. Nowadays, it expanded all over China as an important food resource [44] and the sales are becoming increasingly larger [45], but it is not completely safe. In 1952, Paragonimus westermani was first discovered in P. clarkii in Japan [46]. People may get infected through the intake of the undercooked crayfish [47]. The paragonimiasis is a zoonotic disease prevailing in 25 PAM at varied extent and has higher incidence in southwest China including Sichuan, Chongqing and Yunnan [48]. More than 100 counties in Sichuan Province had reported cases through past 50 years and the incidence shows an upward trend because of the changing in the lifestyle and diet [49]. However, there has been no definite report regarding to P. clarkii as the cause of the paragonimiasis in China so far. Patients commonly got infected by consuming the undercooked Potamon spp., or some freshwater snails or through direct contact with the contaminated water. This could be explained by the fact that most edible P. clarkii in China comes from the aquafarm where the safety is guaranteed.

Invasive alien insects harboring zoonotic parasites

Most invasive alien insects in China have a closer relationship with plants instead of animals except Blattella germanica, Periplaneta Americana, Periplaneta australasiae, S. invicta and so on.

Tribolium castaneum

The Tribolium castaneum (Herbst), also known as red floor betel, is recognized as the pest of stored grain. The species distributes worldwide in 6 continents except the Antarctica according to the Bureau of Entomology and Plant Quarantine, United States Department of Agriculture [50]. It was reported that the betel could only be found in 4 provinces in China by the 1960s. The species made its way through the transportation and trading of grain food. In consideration of the tradition of food allocation and transportation around China, researchers assumed the T. castaneum as one of the IAS [51]. Nowadays, this specie has invaded 23 PAM of China, while no evidence found in Shanghai, Shanxi, Shaanxi, Qinghai, Gansu, Xinjiang, Taiwan, Guizhou and Tibet [52].

T. castaneum is experimentally proved as the potential intermediate host for Pseudanoplocephala crawfordi, which may cause psudanoplocephalosis [53]. P. crawfordi inhabits in the small intestines of many mammals including the swine, mouse and human. The patients usually take on some abdominal symptoms [54]. The prevalence of the parasites in the swine of China can reach 15.2–91.6% which makes it a big threat to the livestock industry [55]. Twenty-one cases [56] related to this parasite had been reported in Henan [56], Liaoning [53] and Shaanxi [57] until 2016. Patients can be infected by undertaking insanitary food contaminated by the T. castaneum or eating the T. castaneum carrying the cysticercoids directly.

Cockroaches

Cockroach is one of the most common synanthropic insects in the world, especially in the areas with bad sanitary condition. In China, before 1980s, the dominant species of city cockroaches are P. americana, while the distribution of B. germanica is limited to several cities. Later, the invasive B. germanica replaced P. americana to be the dominant species in city and spread nationwide rapidly [58].

Because cockroaches usually feed on human feces, they may transmit various zoonotic parasites mechanically. An investigation in Taiwan revealed a high infection rate, 25.0% in P. americana and 10.0% in B. germanica, by Entamoeba histolytica or Entamoeba dispar respectively [59]. Besides, cockroaches can induce allergic reaction in some people directly [60].

More zoonotic parasites carried by the invasive alien insects documented worldwide are listed in Table 2.

Table 2

Zoonotic parasites carried by invasive alien insects

Species	Common name	Parasites	Reference
Blatella germanica	German cockroach	Ascariasis lumbricoides, Enterobius vermicularis, Entamoeba histolytica, E. dispar, G. lamblia, hookworm, Hymenolepis nana, Strongyloides stercoralis, Sarcocystis muris, Trichuris trichiura, Taenia spp., T. gondii	[118]
Periplaneta americana	American cockroach	Moniliformis moniliformis, Diplogaster sp.	[119]
		A. lumbricoides, Balantidium coli, Entamoeba coli, E. histolytica, E. vermicularis, hookworm, T. trichiura	[120]
		S. muris, T. gondii	[121]
		Schistosoma haematobium, Sc. mansoni	[122]
Tribolium castaneum Herbst	Red flour beetle	Hymenolepis diminuta	[123]
		Pseudanoplocephala crawfordi	[53]
		Steinernema feltiae	[124, 125]
Cydia pomonella	Codling moth	S. feltiae	[126]

Zoonotic parasites carried by invasive alien vertebrates

Zoonotic parasites carried by invasive alien fishes

Unlike other IAS, most invasive alien fishes were initially introduced intentionally. Some of them escaped into natural water, spread rapidly and became the dominant species in local waters. More than 65 species of fishes have been introduced into China [61]. Most of them were introduced for aquaculture to increase the food supply. Since 1957, when Oreochromis mossambicus was introduced into China from Vietnam firstly, more species of tilapias had been introduced, including O. niloticus, Tilapia zillii. Now O. mossambicus has widely distributed in waters of South China and established wild populations [62]. Some species were introduced as ornamental species, like Hypostomus plecostomus. Some are introduced for biological control. The best-known example is the mosquitofish, Gambusia affinis, which was thought to be effective in controlling mosquitoes. However, it was proven that its effect in controlling mosquitoes did not differ from local species significantly. On the contrary, it invaded local waters by feeding on fry. Initially introduced into China from Philippine as early as 1927, mosquitofish have replaced Oryzias latipes and O. Curvinotus to be local dominant species in waters of southern China [63].

Fishes are important source of zoonotic parasites. Almost all fish-borne parasitic zoonoses have been acquired by consuming raw or undercooked fish product like sushi, sashimi and so on. As is estimated by the World Health Organization (WHO), more than half billion people are exposed to the risk of these diseases [64]. The rapidly proliferating IAS may serve as a dramatically expanding source of zoonotic infection or in another way assist the transmission of these zoonotic parasites to other fishes.

Fish-borne zoonotic trematodes

Fish-borne zoonotic trematodes mainly consist of four families, including Opisthorchiidae, Heterophyidae, Nanophyetidae, and Echinostomatidae [65]. For these trematodes, fishes mainly serve as the second intermediate host [66]. Fish-borne zoonotic heterophyids mainly include Heterophyes (H. heterophyes, H. dispar), Haplorchis (H. taichui, H. pumilio, H. yokogawai, and H. vanissimus), Metagonimus (M. minutus, M. yokogawai and M. takahashii), Centrocestus (C. formosanus), Procerovum (P. varium) [67]. Nine heterophyid trematodes have been reported in China, mainly in Southern China, where the patient infected with heterophyid was usually coinfected with Clonorchis sinensis due to the habit of eating raw fish [68]. Information of heterophyids infection in invasive alien fishes in China was displayed in Table 3. These zoonotic parasites were endemic in these regions correspondingly. In Longhai City and Nanjing County of Fujian Province, the infection rate of the local population is 0.3% (13/3867) [69]. A survey in Guangxi, where people has a habit of consuming raw fish, revealed that the infection rate of H. taichui reached about 24.3% there. Surprisingly, in one investigating site, H. taichui infection accounts for 90.5% of people with trematode infection. The most commonly consumed raw fish were C. carpio and C. auratus [70]. Besides, although experimental human infection of C. formosanus has been reported, natural human infection has never been recorded [71].

Table 3

Infection rate of heterophyids in invasive alien species in different cities in China

Parasites	Species of local invasive alien species host	Location	Infection rate	Reference
Haplorchis pumilio	Cyprinus carpio, Carassius auratus	Longhai City and Nanjing County of Fujian Province	36.3%	[69]
H. taichui	C. auratus	Yangshuo County, Nanning City, Mashan County, Fusui County and Binyang County in Guangxi	61.9%	[68]
	C. carpio		42.9%
	Tilapia nilotica		0
	Cirrhinus molitorella		0
	Gambusia affinis		–
H. pumilio	C. auratus		81.0%
	C. carpio		28.6%
	T. nilotica		0
	C. molitorella		0
Centrocestus formosanus	G. affinis, C. carpio, C. auratus	Guangdong, Fujian, Guangxi, and Taiwan	–	[127]

Among family Opisthorchiidae, three liver flukes, C. sinensis, Opisthorchis felineus, and O. viverrini are the most problematic zoonotic parasites [72]. For the Chinese liver fluke C. sinensis, a survey in 27 endemic PAM in China, revealed a high prevalence of about 2.4%, about 12.5 million people [73]. The selectivity on second intermediate host of C. sinensis is low. Sixty eight species of freshwaters as latent second intermediated host of C. sinensis have been reported in China, including C. auratus, C carpio, O. mossambica and so on [74, 75].

Fish-borne zoonotic cestodes

Fish-borne zoonotic cestodes are mainly composed of Diphyllobothrium (D. latum and D. dendriticum) [76]. A total of 16 cases of D. latum infection through consuming raw fish have been reported in China, but no detailed information about the species of fish was documented [77]. D. latum infection has been recorded in Oncorhynchus mykiss, Salvelinus forntinalis, Stizostedion vitreum, Perca flavescens worldwide as listed in Table 3.

Fish-borne zoonotic nematodes

Fish-borne zoonotic nematodes consist of parasites of family Gnathostomatidae (Gnathostoma spp.), family Anisakidae (Anisakis), family Capillariidae (Capillaria philippinensis), family Dioctophymatidae (Eustrongylides spp.). Among them, the most common species infecting humans are Gnathostoma spp., Anisakis spp. and Pseudoterranova spp. [78]. More than 50 cases of gnathostomiasis have been reported in 16 PAM of China. Most common infection way of Gnathostoma spp. is also consumption of raw freshwater fishes, including C. carpio, and C. auratus [79].

Among these fish-borne zoonotic parasitic infection cases, most of them were wild-caught fishes, while only a few were farm-raised fishes, which have been neglected for a long time. In a research conducted in Guangdong Province, where almost half of the tilapia in China is produced, zoonotic parasites of family Heterophyidae and Echinostomatidae were detected in the cultured tilapias [80].

The zoonotic parasites carried by more invasive alien fishes of China have been listed in Table 4, which is documented worldwide. Although associated information in China is limited, this table provides an insight into the potential risks of consuming these fishes in China, especially under the circumstance that infection rate in some populations, in fact is high but ignored as illustrated above, which may be attributed to the fact that most infections only cause light symptoms like diarrhea or other gastrointestinal disorders. Since most invasive alien fishes were introduced for aquaculture, more attentions should be paid to zoonotic parasites carried by these fishes.

Table 4

Zoonotic parasites carried by invasive alien fishes

Invasive alien species	Common name	Parasites	Reference
Oncorhynchus mykiss	Rainbow trout	Diphyllobothrium dendriticum	[76]
		D. latum	[128, 129]
		Cryptosporidium sp.	[130]
Salvelinus forntinalis	Brook trout	D. dendriticum, D. latum	[131]
Piaractus mesopotamicus Holmberg		Eustrongylides sp.	[78]
Gambusia affinis	Mosquitofish	Centrocestus formosanus	[127, 132]
		Haplorchis taichui	[127]
		H. yokogawai	[67]
		H. pumilio	[127, 133]
Stizostedion vitreum	Walleye	D. latum	[129]
Perca flavescens	Yellow Perch	D. latum	[129, 134]
Lucioperca lucioperca	Pike-perch	Eustrongylides sp.	[135]
		Anisakis simplex	[136]
Cichlasoma managuense, Parachromis managuensis		Gnathostoma sp.	[137]
Oreochromis niloticus	Nile tilapia	H. pumilio, H. taichui, Procerovum varium, Metagonimus spp., C. sinensis	[80]
		Gnathostoma sp.	[138]
		Cryptosporidium spp., Prohemistomum spp.	[139]
		C. formosanus	[140]
Oreochromis nilotica	Red tilapia	C. philippinensis	[141]
		H. yokogawai	[67]
Tilapia zillii		Capillaria sp., Diphyllobothrium sp., H. nana, Trichostrongylus sp.	[142]
Oreochromis sp.		Cryptosporidium sp.	[130]
Oreochromis mossambicus	Black tilapia	C. sinensis	[75, 143]
		Gnathostoma sp.	[138]
Clarias spp.		H. pumilio	[144]
(Clarias lazera Cuvier & Valenciennes Clarias macrocephalus Günther Clarias batrachus L.)		H. taichui (for C. batrachus), H. yokogawai (for C. batrachus)	[145]
		Gnathostoma spinigerum	[146, 147]
Pangasius sp.		H. pumilio	[144]
		C. formosanus	[148]
Siluris glanis	European catfish	Eustrongylides sp.	[135]
Ictalurus punctatus	Channel catfish	Eustrongylides sp.	[149]
Channa striata	Snakehead fish	H. pumilio, H. taichui, O. viverrini, Procerovum sp.	[150]
		G. spinigerum	[147]
Channa micropeltes		Gnathostoma sp.	[151]
Lates calcarifer	Asian seabass	Cryptosporidium sp.	[130]
Cirrhina mrigala/Labeo rohita	Mrigal/Rohu	C. formosanus, C. sinensis, H. pumilio, H. taichui, H. yokogawai, P. varium	[145, 152]
Cyprinus carpio var. specularis.	Mirror carp	C. sinensis	[75, 153]
Cyprinus carpio var. Mirror splittered		C. formosanus, H. pumilio, H. yokogawai	[145]
		O. viverrini	[154]
		H. taichui	[127]
Carassius auratus Cuvieri Temminck & Schlegel	Japanese crucian carp	C. sinensis, Centrocestus armatus, Metagonimus takahashii, Metagonimus spp.	[127]
		Haplorchis spp.	[155]
		Metorchis orientalis	[65]
		O. felineus	[72]
		O. viverrini	[156]
		H. yokogawai	[67]
Chalcalburnus chalcoides		Anisakis sp.	[157]

Zoonotic parasites carried by invasive alien amphibians

Invasive alien amphibians consist of Rana catesbeiana, R. heckscheri, R. grylio, R. tigrine, Trachemys scripta elegans and Mauremys mutica.

R. catesbeiana, bullfrog, was first introduced into China in 1959. Along with the expansion of the farming of bullfrog, some escaped into wild environments and established wild populations, but most wild populations are still small, which makes it hard to capture bullfrog in wild.

Frogs are the second intermediate host of Spirometra mansoni. A reported infection rate of Sp. masoni in bullfrog in Japan and USA were 43.0 and 1.7% respectively [81, 82]. However, in the investigation in Zhejiang Province and Guangzhou City, Guangdong Province, although infection rate is high in the wild frogs, like R. tigrina rugulosa and R. limnocharis, no Sp. mansoni infection was found in the farm-raised bullfrogs [83-85]. It may be associated with the absence of first intermediate host, cyclops or definitive host cat or dogs in the farming process. But high infection rate in wild frogs still alarms us that the wild bullfrog populations should never be neglected even though they are rarely captured. In addition, Gnathostoma nipponicum has also been detected in bullfrog in Japan [86].

Zoonotic parasites carried by invasive alien birds

No information about the zoonotic parasites carried by invasive alien birds is available in China, but there are a few reports about these parasites worldwide, which are listed in Table 5.

Table 5

Zoonotic parasites carried by invasive alien birds

Species	Common name	Parasites	Reference
Psittacula krameri	Ring-necked parrot	Cryptosporidium meleagridisin	[158]
Branta canadensis	Canadian goose	Cryptosporidium parvum	[159, 160]
		Toxoplasma gondii	[161]
		C. hominis	[162]
		Giardia sp.
		Trichobilharzia spp.	[163]

Zoonotic parasites carried by invasive alien mammals

Invasive alien mammals consist of Macaca fascicularis and nine species of rodents, including 6 species of rats. Rats are the most common rodents in the communities and thus play a significant role in human health as a vector of many zoonotic pathogens, especially in the areas with high temperature and poor sanitation.

Invasion history of Rattus norvegicus, R. rattus and Mus musculus can’t be traced because their invasion was far before the foundation of the People’s Republic of China, PRC and the beginning of nationwide monitoring of rodents. Thus, with such a long history and great adaptability to all kinds of environments, they have spread all over China. A survey in Zhejiang Province showed that dominant species of rodents are M. musculus and R. norvegicus indoor and outdoor respectively [87]. And M. musculus and R. norvegicus ranked 2nd and 3rd in number of indoor rodents in Shanghai, respectively [88]. They might be imported through ocean shipping [89]. And modern transportation may accelerate their invasion. Before the railway opened to traffic in Xinjiang Uygur Autonomous Region, there is no record of R. norvegicus. Since 1975 when R. norvegicus was first captured in a train in Xinjiang, R. norvegicus have dramatically expanded in local rodent population and became the dominant species in 1989 [90]. Another species of invasive alien rodent, Ondatra zibethicus, spread into China from Union of Soviet Socialist Republics through the rivers at northwestern and northeastern border [91]. Besides, Myocastor coypus was initially introduced and farmed as fur animal. But as the fur quality dropped in the farmed M. coypus in southern China, they were abandoned and became wild [92].

Heterophyids

H. nana and H. diminuta are the common zoonotic intestinal parasites of wild rats. Xinjiang is a high incidence area of H. nana infection, where some regions can reach even 9.2%. In these areas, H. nana infection rate is relatively high in R. norvegicus and M. musculus [93]. In addition, an average infection rate of 0.02 and 0.01% for H. diminuta and H. nana, respectively was reported in an investigation in Yunnan Province, while it was 0.1 and 0.2% in Henan Province [94, 95].

Angiostrongylus cantonensis

A. cantonensis was first identified in the lung of R. rattus and R. norvegicus in Guangzhou in 1933. It’s thought that R. rattus and R. norvegicus are the most common definitive host of A. cantonensis, which is indispensable for the establishment of its foci [96]. The presence of this parasite in rats indicates that this region is endemic. R. norvegicus, R. tanezumi had been reported to harbor this parasite in China [97].

Babesia microti

There are many natural foci of Babesia microti in China and several sporadic cases of human infection have been reported in 8 PAM [98]. A case of human babesiosis was reported in Zhejiang Province in 2012, and the local investigation found B. microti infection in two R. tanezumi and one R. norvegicus [99].

Echinococcus multilocularis

Echinococcus multilocularis is endemic in northwest China, mainly Xinjiang, Ningxia, Gansu, Sichuan and Qinghai, where there are still many semi-nomads. Over 1000 cases of alveolar echinococcosis caused by E. multilocularis had been reported in China from 1956 to 2005 [100]. In Xinjiang, E. multilocularis was detected in R. norvegicus and M. musculus [100, 101]. However, the infection rate of E. multilocularis might have been underestimated a lot, as about 200 cases were reported just in the First affiliated hospital of Xinjiang Medical University [102]. The low infection rate reported may be attributed to the underdevelopment of those regions and limit of their technology of diagnosis.

Capillaria hepatica

C. hepatica is a rare zoonotic parasite with only three cases of human infection reported in China [103]. So far, only one case of C. hepatica infection in human has been reported in Fujian Province. However, a local investigation revealed a high infection rate, 10.8 and 7.7% respectively in R. norvegicus and M. musculus [104].

C. sinensis

O. zibethicus, R. norvegicus and M. musculus can serve as the reservoir host of C. sinensis in China [105].

As being estimated, rodents are vectors of at least 60 zoonotic diseases [106]. While researches on the zoonotic parasites carried by these alien invasive rodents are limited in China, many globally reported parasites are not detected, which are listed in Table 6.

Table 6

Zoonotic parasites carried by invasive alien mammals

Invasive alien species	Common name	Parasites	Reference
Rattus norvegicus	Wild brown rats	Angiostrongylus cantonensis	[19, 106, 164–167]
		Echinococcus multilocularis	[168]
		Capillaria hepatica, Hymenolepis diminuta, Taenia taeiaeformis	[169]
		Schistosoma mansoni, Moniliformis moniliformis	[170]
		H. nana, Giardia sp., Cryptosporidium sp., Entamoeba sp.	[171]
		C. parvum	[172]
		Entrobius spp., Trichuiris spp.	[173]
		Leishmania major	[174]
		L. infantum	[175]
		Toxoplasma gondii	[161]
		Trichinella spiralis, T. britovi, T. pseudospiralis	[176]
		Toxocara canis	[177]
		Gongylonema pulchrum	[178]
		Syphacia muris	[179]
		Sarcocystis orientalis	[180]
		Paragonimus westermani, Plagiorchis potamonides, Echinostoma ilocanum, Raillietina madagascariensis	[181]
		S. japonicum	[182]
Rattus rattus	House rat/Roof rat	Rictularia sp., H. diminuta, M. moniliformis	[168]
		C. parvum	[183]
		Fasciola hepatica	[184]
		Taenia taeniaeformis	[185]
		Leishmania donovani donovani, L. donovani infantum	[186]
		A. cantonensis	[166]
		G. pulchrum	[178]
		T. britovi	[176]
		T. gondii	[187]
		Sc. mansoni	[188]
		Sarcocystis sp.	[180]
		Babesia microti	[98]
		T. spiralis, Entamoeba coli, Dientamoeba fragilis	[189]
Mus musculus	House mouse	Enterocytozoon bieneusi	[190]
		C. hepaticum	[191]
		C. parvum	[183]
		H. nana	[192]
		H. diminuta, S. muris, T. taeniaeformis	[193]
		Leishmania major	[194]
		A.s cantonensis	[195]
		H. taichui	[196]
		T. gondii	[197]
		T. canis	[198]
		E. multilocularis	[199]
Rattus tanezumi Temminck	Asian house rats	A. cantonensis, Hymenolepis spp., T. taeniaeformis	[200]
		Syphacia muris, H. diminuta	[201]
		T. gondii	[202]
		C. hepaticum	[203]
		B. microti	[98]
		Artyfechinostomum malayanum, Echinostoma ilocanum, E. lindoense, H. nana, M. moniliformis, P. westermani, Plagiorchis muris, P. philippinensis, P. potamonides, Raillietina madagascariensis, S. japonicum, T. taeniaeformis	[181]
Rattus exulans	Pacific rats	S. japonicum	[182]
		H. diminuta, H. nana, M. moniliformis, Raillietina spp.	[204]
		A. cantonensis	[19]
		T. gondii	[205]
Ondatra zibethicus	Musk rat	E. multilocularis	[206]
		Taenia martis, T. taeniaeformis	[207]
		C. hepatica	[208]
		C. parvum	[183]
Myocastor coypus	Nutria	C. parvum	[183]
		T. gondii	[209]
		E. multilocularis	[206]
		F. hepatica	[210]
		Strongyloides myopotami	[211]
		C. hepatica	[212]
Sciurus vularis exalbidus	Red squirrek	T. gondii	[213]
		C. hepaticum	[203]
		C. parvum	[166]
Callosciurus erythraeus	Red-bellied squirrel	Hymenolepis sp.	[214]
		E. bieneusi	[164]
		A. cantonensis	[215]
Macaca fascicularis		C. parvum	[216]
		Plasmodium knowlesi	[200, 217]
		E. histolytica	[218]
		Endolimax nana, Oesophagostomum	[219]
		Sarcocystis sp.	[220]
		Strongyloides fulleborni	[221]
		H. nana, Strongyloides spp.	[222]
		Armillifer agkistrodontis	[223]
		G. duodenalis	[224]
		T. trichiura	[225]
		E. multilocularis	[226]

Prevention and control

The invasion of alien species becomes much more common with predictable developing international communications and inevitable globalization [107]. Considering the great damage it may cause [108], the Chinese government has focused on the administration, international cooperation, fundamental researches and public awareness to cope with the problems [109]. The Ministry of Agriculture (MOA) has established the institution for administration of invasive alien species and a center for management of invasive alien species. MOA also organized to draw up the Measures for Management of IAS, rectified the Contingency Plans for Emergency of Alien Species Invasion, perfect the database of IAS in China and complete the prevention and control system. The Chinese government has put up some relevant legislation including Law of the RPC on the Entry and Exit Animal and Plant Quarantine against the IAS in 1996 [110], and the science funding regarding associated programs are booming as well [109].

However, the Chinese government should also issue more regulations to complete the legislation system toward the IAS and the current regulations should be enforced strictly. Surveillance and prevention system should be improved, and some cross-industry obligatory institutions should be established to integrate related work to fulfill the administration. The propagation of science knowledge should also be intensified to raise public awareness of the IAS.

For those species introduced deliberately as food material, the China Food and Drug Administration (CFDA) is supposed to take rigid strategy to restrict the introduction and make rigorous standard to ensure the safety and harmlessness of the species. For those IAS which entered China coincidentally, related institutions at the national border should intensify the surveillance and monitor system to prevent the invasion of unwanted species. For some IAS which have the potential to cause or has already caused enormous economic, environmental or public health problems, some eradication steps are supposed to be considered to prevent further loss.

Conclusions

It can be predicted that the IAS issue may become a progressively important problem globally with the development of society and booming international communication. The government should raise awareness of the possible destructions the IAS may cause and take some measures in advance to prevent possible loss.

Apart from IAS’s direct damage to the ecology and economy, its capability as the vector to transmit parasitic disease should arouse public awareness. In China, as mentioned above, many species may play an important role in the transmission of some specific diseases, but the relative researches are rather scarce which suggests insufficient emphasis regarding such an issue. The risk of the parasites carried by the IAS is vastly underestimated. With various climates and multiple landforms, China is suitable for numerous IAS and parasites to settle down. However, few associated reports or researches can be found in China, as most case reports of zoonotic parasites carried by invasive alien species in China were listed in Table 7. More efforts about associated problems should be paid in both researching and administration. For those species which has already caused some zoonotic diseases, compulsory measures to control the species should be conducted to ensure the safety of public and some eradication methods ought to be considered for some more dangerous disease. For those species capable of transmitting parasites with no specific case reported yet, the screening surveys and control measures should be strictly fulfilled periodically to guarantee the safety of those species.

Table 7

Reported distribution and case reports of zoonotic parasites carried by invasive alien species in China

Parasites	Location of report	Reported local invasive alien host	Infection rate in investigated population	Number of Case reports	Reference
Angiostrongylus cantonensis	Yunnan, Guangxi, Hainan, Guangdong, Fujian, Zhejiang, Jiangsu, Beijing, Tianjin, Liaoning, Heilongjiang.	Rattus rattus, R. norvegicus, Pomacea canaliculate, Achatina fulica	–	334	[34, 96]
Paragonimus westermani	Hunan, Liaoning, Jilin, Heilongjiang, Sichuan, Yunnan, Shanxi, Zhejiang, Henan, Hubei, Hebei, Shaanxi, Gansu, Anhui, Guizhou, Guangdong, Hainan, Jiangxi, Fujian	Procambarus clarkii	1.71%	–	[47, 48]
Haplorchis taichui	Guangxi	Cyprinus carpio, C. auratus	24.3–90.5% (in people with a habit of consuming raw fish)	–	[70]
Clonorchis sinensis	Guangdong, Guangxi, Heilongjiang, Jilin, Liaoning, Hunan, Chongqing, Jiangsu, Anhui, Fujian, Hainan, Tianjin, Sichuan, Henan, Shandong, Hubei, Guizhou, Xinjiang, Hebei, Jiangxi, Shanghai, Shanxi, Beijing, Yunnan, Shanxi, Gansu, Zhejiang	C. auratus, C carpio, O. mossambica	2.4% (about 12.5 million people)	–	[73–75]
Diphyllobothrium latum	Taiwan, Heilongjiang, Jilin	Oncorhynchus mykiss, Salvelinus forntinalis, Stizostedion vitreum, Perca flavescens	–	16	[77]
Gnathostoma spp.	Zhejiang, Jiangsu, Anhui, Hunan, Hubei, Shandong, Henan, Jiangxi, Guangdong, Hainan, Taiwan, Fujian, Shanghai, Jilin, Heilongjiang, Xinjiang	C. carpio, C. auratus	–	More than 50	[79]
Babesia microti	Chongqing, Yunnan, Inner Mongolia, Taiwan, Zhejiang, Shandong, Shanxi, Xinjiang	R. tanezumi, R. norvegicus	–	27	[98]
Echinococcus multilocularis	northwest China, mainly Xinjiang, Ningxia, Gansu, Sichuan and Qinghai	R. norvegicus, M. musculus	–	Over 1000	[100–102]
Capillaria hepatica	–	R. norvegicus, M. musculus	–	3	[103, 104]

- Not applicable

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