Asian Fish Tapeworm: The Most Successful Invasive ...

Review

Asian Fish Tapeworm: The Most Successful Invasive Parasite in Freshwaters Roman Kuchta,1 Anindo Choudhury,2 and Tomáš Scholz1,* The Asian fish tapeworm (AFT), Schyzocotyle acheilognathi, is a notorious and highly successful invasive parasite reported in a wide spectrum of freshwater fishes, and new reports of its spread continue to emerge. To date, no thorough review of its worldwide distribution and host associations is available. In the present work, we collected information from 651 articles up until 2017, from which we updated the number of the hosts to 312 fish species and 11 non-fish species, which is quite unusual among helminths. The AFT has spread to all but one continent (Antarctica). The highest number of records are from North America, followed by Asia and Europe. A key feature of its invasive success is its broad environmental tolerance. Introduction The AFT is a member of the cestode order Bothriocephalidea. The species was first described as Bothriocephalus acheilognathi from a small cyprinid fish, Acheilognathus rhombeus, in Lake Ogura, Japan [1]. Since its original description, the AFT has had a convoluted taxonomic history. Over the intervening decades, likely conspecific worms, which possess a typical heartor arrow-shaped scolex with narrow and deep attachment grooves called bothria, were described as different species of several genera from numerous host species, specific localities and even continents (see Table S1 in the supplemental information online; for a review of the taxonomic history, see [2,3]). The most commonly used scientific name of the parasite was B. acheilognathi (51% of records), followed by B. gowkongensis (14%). A comprehensive molecular phylogenetic analysis of the order Bothriocephalidea [2] indicated that the AFT should not be assigned to Bothriocephalus and the genus Schyzocotyle was resurrected. Consequently, the currently accepted scientific name of the AFT is Schyzocotyle acheilognathi [2]. In the 1950s and 1960s, the AFT was spread, primarily through imported common carp, Cyprinus carpio, and grass carp, Ctenopharyngodon idella, from the Russian Far East and China to the western part of the former USSR, and to eastern and central Europe. It became a parasite of cultured cyprinid fishes and a species of veterinary importance causing mortalities, mainly in carp fry, or shortening the life span and stunting the growth of adult fishes [3–5]. The AFT is most pathogenic in newly acquired host species, which appears to be the case in Australia, Europe, and North America [5–7]. The spread of the AFT continued in the 1980s and 1990s, partly due to the unregulated translocation of guppies, mosquito fish, and minnows used as bait fishes throughout continents and between them [8,9]. As a result, the parasite has successfully colonised all but one continent (Antarctica), and including islands such as Puerto Rico, Hawaii, and Mauritius [10–12]. The number of fish species reported as hosts of S. acheilognathi has increased considerably over the last few decades. Dove and Fletcher [13] reported 65 fish species of seven orders, but just 3 years later, Salgado-Maldonado and Pineda-Lopez [14] listed 102 fish species of seven Trends in Parasitology, June 2018, Vol. 34, No. 6

Highlights The AFT is a highly successful invasive parasite of freshwater fishes. We have updated the number of reported hosts of the AFT to 312 fish species and 11 non-fish hosts; the dominant hosts are cypriniform fishes, especially common carp and grass carp, and cyprinodontiform fishes. The AFT has spread to almost all continents with the highest number of records from North America, followed by Asia and Europe. The broad environmental tolerance (biotic and abiotic) of the AFT is a key factor in its success. The AFT represents a potential threat mainly for native endemic and ornamental fishes, and reports of its range expansion continue to emerge, especially in North America. Recently designed microsatellites are now available to assess the genetic variability and geographic origin of individual populations of the AFT.

1 Institute of Parasitology, Biology Centre of the Czech Academy of jovice, Czech Sciences, Ceské Bude Republic 2 Division of Natural Sciences, St Norbert College,100 Grant Street, DePere, WI 54115, USA

*Correspondence: [email protected] (T. Scholz).

https://doi.org/10.1016/j.pt.2018.03.001 © 2018 Elsevier Ltd. All rights reserved.

511

orders. Most recently, Scholz et al. [12] reported 200 fish species of ten orders. However, this increase seems to have been caused only partly by the actual increase in the number of fish host species. A more thorough searching of the literature most likely also contributed to this considerable increase of 50% within just 6 years. A number of articles have been published on the AFT, its distribution, pathogenicity, and treatment of cultured fishes, including reviews such as those of Choudhury and Cole [11], Scholz et al. [12], and Pérez-Ponce de León et al. [15]. However, none of these accounts was based on an exhaustive search of published records. Particularly missing were articles written in Russian and their critical evaluation. Therefore, we carried out an updated review of the literature to gather primary data on the actual spectrum of hosts of the AFT, its distribution, and host specificity. Possible ways in which the parasite spread (history of introduction) throughout the world, as well as key characteristics aiding in its successful spread, are briefly discussed. Moreover, a list of host records confirmed by molecular data is provided for the first time. We consider the present work timely and important because threats from the spread of the AFT continue to emerge. For example, a recent study has found that an alarmingly high proportion of bait shops in Michigan have shiners and minnows infected with the AFT [16]. Such continued range expansion is particularly relevant given the threats from climate change and how climate change impacts species distribution. Understanding timelines and host associations of invasion and colonisation more accurately may also help us anticipate the speed and success of future colonisation events.

Data Search The present review is based on a summary of primary data, that is, information compiled from more than 700 articles, as follows: (i) data sources: Web of Science, Scopus and Helminthological Abstracts from 1900 to 2017; (ii) search terms: all known synonyms of S. acheilognathi as well as nomina nuda (see Glossary) (Table S1); (iii) number of articles that contain primary data (general papers were not considered): 651 articles with a total of 1207 host and locality records (Table S2); (iv) excluded records: 37 records of bothriocephalid cestodes from fishes of the genera, Raiamas Jordan, 1919 (Cyprinidae: Danioninae) and Schizothorax Heckel, 1838 (Cyprinidae: Barbinae) because these records may be of another congeneric species, Schyzocotyle nayarensis (Malhotra, 1983) that occurs in eastern India and differs only slightly in scolex morphology, which prevents reliable identification without examination of voucher specimens (not known to exist). The number of articles in which the AFT was mentioned increased sixfold from the 1960s (only 29 articles) to the 1980s (175; the highest number of articles – 28 articles – was published in 1987). After 2000, the number of articles slowly decreased, with 125 additional articles until 2009, and a further 93 articles between 2009 and 2017 (Figure 1). The Index of Host Specificity (HS) follows that of Caira et al. [17]. The names of fishes, their IUCN red list status, status of endemism, and native climate follow those of Froese and Pauly (http://www.fishbase.se/ search.php).

Host Spectrum of S. acheilognathi The AFT has been reported from 312 freshwater fish species of 38 families and 14 orders (Table S2) and the HS of the AFT is 9.899, which is by far the highest value reported for any metazoan parasite [17]. However, the distribution of records in this extremely high number of hosts is highly uneven, with a majority of hosts from Cypriniformes (185 spp., 76%), almost

512

Trends in Parasitology, June 2018, Vol. 34, No. 6

Glossary Invasive species: a species that is not native to a specific location and whose introduction causes or is likely to cause economic or environmental harm or harm to human health. Nomina nuda: names that fail to conform to certain articles in the International Code of Zoological Nomenclature. Species inquirenda: species of doubtful identity requiring further investigation.

175

180 160

133

140

125

120 100

93

88

80 60 40 20 0

29 2

6

to 1949 1950s

1960s

1970s

1980s

1990s

2000s

2010s

Figure 1. The Number of Records of Schyzocotyle acheilognathi, Including Its Synonyms through Time.

exclusively the family Cyprinidae (170 spp., 74%), followed by the Cyprinodontiformes (49 spp., 12%), mostly from the family Poeciliidae (21 spp., 7%), the Perciformes (40 spp., 6%), the Atheriniformes (15 spp., 4%), and the Siluriformes (eight spp., 1%). Fishes of the remaining orders (14 spp.) represent only 1% of the records. Only 42 fish hosts, 14% of all fish species reported as hosts of S. acheilognathi, have been confirmed using molecular data (i.e., sequencing tapeworms from these fish and other hosts) (Table S3). The most frequently reported hosts of S. acheilognathi are Cy. carpio and Ct. idella, comprising as much as one third (34%) of all records in fishes (300 and 111 records, respectively), followed by Hypophthalmichthys molitrix (Cyprinidae) and Gambusia affinis (Poeciliidae), both around 20 records, which represent 4% of all records (Figure 2). All other species have been reported in less than 16 articles. Almost half (146 species) of all reported fish host species have been reported as hosts of the AFT only once (Figure 2). Fishes of 14 families are represented with only a single record (and an additional five families with two records). More than three fourths (78% of records) were from wild fishes, and only 22% were from fishes in aquaculture. In addition to the negative impact of the AFT on cultured fishes, it has become a frequent and sometimes pathogenic parasite of ornamental fishes worldwide, as documented by Evans and Lester [18] in Australia, Piazza et al. [19] and Santos et al. [20] in Brazil, Hernández-Ocampo et al. [21] in Mexico, Chaudhary et al. [22] in India, Košuthová et al. [23] in Slovakia, and Scholz et al. [12] in the Czech Republic. In addition to fishes, the AFT has also been reported from other vertebrates, but these records should be considered with caution because they may represent cases of postcyclic or accidental parasitism (Table S4). They include five species of amphibians (four frogs, one salamander), one ‘reptile’ (a snake), four bird species, and one finding of the eggs in human stool confirmed genetically [24]. These vertebrates likely do not serve as true definitive hosts of the AFT. Volz [25] described Bothriocephalus spiraliceps based on bothriocephalid tapeworms from the sooty falcon, Falco concolor, in Ethiopia, but this cestode was considered a species inquirenda by Tadros (Table S1) [26]. Local spread of the tapeworm, or passive passage of its eggs by aquatic birds, was assumed to take place based on experiments conducted by Prigli [27] and field observations by Borgarenko [28]. Trends in Parasitology, June 2018, Vol. 34, No. 6

513

Records of fish orders 6%

4%

1%

11%

76%

Records of families

Cypriniformes (185 spp.) CyprinodonƟformes (49) 1% Perciformes (40) 3% Atheriniformes (16) 3% 4% Siluriformes (8) Characiformes (6) 7% Acipenseriformes (1) Esociformes (1) 74% Percopsiformes (1) Salmoniformes (1) Beloniformes (1) Mugiliformes (1) Osmeriformes (1) Synbranchiformes (1)

Records of fish species Species

Red list category CR EN 3% 3% VU 6%

154 spp. (1 rec.) 73 spp. (2 rec.)

13%

Cyprinus carpio 25%

12%

23 spp. 6% (3 rec.) 6% 19 spp. 5% (4 rec.)

Ctenopharyngodon idella 9%

13 spp. (5 rec.)

NT 4%

Not evaluated 38%

LC 46%

Cyprinidae (171 spp.) Poeciliidae (21) Atherinopsidae (15) Goodeidae (17) Cichlidae (18) Centrarchidae (4) Gobiidae (5) Siluridae (2) Catostomidae (6) Eleotridae (5) Profundulidae (5) Characidae (4) CyprinodonƟdae (5) Percidae (3) Fundulidae (1) Nemacheilidae (2) Atherinidae (1) Clariidae (1) CobiƟdae (2) Acipenseridae (1) Esocidae (1) Bagridae (2) Ictaluridae (2) Adrianichthyidae (1) Balitoridae (1) Gyrinocheilidae (1) AlesƟdae (1) Mugilidae (1) Retropinnidae (1) Percopsidae (1) Channidae (1) Moronidae (1) Nandidae (1) OdontobuƟdae (1) Salmonidae (1) Claroteidae (1) Synbranchidae (1) Bryconidae (1)

Records Figure 2. Records of Schyzocotyle acheilognathi by Fish Order, Family and IUCN Red List Category of Host Species. *Clockwise: Hypophthalmichthys molitrix 2%; Gambusia affinis 2%; Cyprinella lutrensis 2%; Hypophthalmichthys nobilis 1%; Pimephales promelas 1%; Chirostoma jordani 1%; Xiphophorus helleri 1%; Chirostoma estor 1%; Algansea lacustris 1%; Gila cypha 1%; Gila robusta 1%; Labeobarbus kimberleyensis 1%; Notemigonus crysoleucas 1%; Schizopyge niger 1%; Tinca tinca 1%; Carassius auratus auratus 1%; Rutilus rutilus 1%; 7 spp. (seven records) 4%; 5 spp. (six records) 5%.

Fish host species of the AFT are more or less evenly spread across tropical, temperate, and subtropical regions (37%, 33%, and 30% of species, respectively). However, no fishes in the Arctic have been reported as a host of the AFT. With respect to the number of records, 56% are from hosts in subtropical, 23% from hosts in tropical, and 21% from hosts in temperate regions. As many as 127 fish host species, that is, 41% of all hosts, can be considered endemic, which is evidence of the extraordinary ability of the AFT to infect fish hosts with restricted distribution areas in regions distant from each other and from the putative original distribution area of this tapeworm.

514


The International Union for Conservation of Nature (IUCN) status could be determined for only 193 (62%) of 312 fish species, because the remaining 119 fish species had not been classified by the IUCN. Thirty-one, that is, 16%, of the classified host species are listed as endangered (CR, EN, VU) or close to being threatened (NT), including ten critically endangered fish hosts (Box 1). Around a half of the classified fish species (46%) are categorised as being of least concern (LC) (Figure 2).

Distribution of S. acheilognathi As an invasive parasite introduced to new regions through human activities, the AFT does not follow the natural borders of zoogeographic regions in its distribution. Most of its records are from North America (35%, that is, 419 records) followed by Asia (30%; 362) and Europe (27%, 324). Africa, Australia, Oceania, and South America are together represented by only 8% of the records (60, 18, 16, and six records, respectively) (Figure 3). Eurasia The original description of the AFT was published in 1934 as B. acheilognathi in Japan [1], and the first record from continental Palaearctic Asia was in 1955, as B. gowkongensis Yeh, 1955, from farmed Ct. idella near Canton in China (Figure 4) [4]. The first record from Europe was from Cy. carpio in Ukraine [29]. Other records soon followed from the former USSR, and later from eastern and central Europe, with subsequent colonisation of almost the whole of Europe, except Scandinavia and the Iberian Peninsula (Figure 4). The first records of AFT from southern Asia were published in the 1960s, as B. gowkongensis from the olive barb Systomus sarana (Hamilton, 1822) in Sri Lanka in 1963 [30]. Later, several species, now considered S. acheilognathi were described from cyprinids from Bangladesh, India, Malaysia, the Philippines, and Thailand. Some records from non-cyprinids such as Nandus nandus (Nandidae), Monopterus albus (Synbranchidae), and Sperata seenghala (Bagridae) (Table S1) [31–33] are questionable and should be verified. The AFT was also reported from Iran as Coelobothrium monodi [34] and, under various names, from surrounding countries such as Afghanistan, Iraq, Turkmenistan, and Uzbekistan [35–38]. These records are from a wide range of cyprinids, but also from sturgeon Pseudoscaphirhynchus kaufmanni in Kazakhstan and Uzbekistan and catfish Silurus glanis [36,38,39].

Box 1. International Union for Conservation of Nature (IUCN) Red List Categories (Numbers in Parentheses Show the Number of AFT Hosts) Critically endangered (CR) – Extremely high risk of extinction in the wild (10*) Endangered (EN) – Very high risk of extinction in the wild (10) Vulnerable (VU) – High risk of extinction in the wild (19) Near threatened (NT) – Likely to become threatened in the near future (13) Least concern (LC) – Lowest risk; does not qualify for a higher risk category (141) *Ten fish species infected with Schyzocotyle acheilognathi: Allotoca diazi, Goodeidae (Mexico), Cyprinodon meeki, Cyprinodontidae (Mexico), Gila elegans, Cyprinidae (USA), Parabotia curtus, Cobitidae (Japan), Notropis moralesi, Cyprinidae (Mexico), Plagopterus argentissimus, Cyprinidae (USA), Poblana alchichica, Atherinopsidae (Mexico), Girardinichthys viviparus, Goodeidae (Mexico), Ilyodon whitei, Goodeidae (Mexico), and Pseudoscaphirhynchus kaufmanni, Acipenseridae (Kazakhstan and Uzbekistan).


515

ConƟnents

North America

Canada & Central America

Australia South America

Mexico

2% Africa 5%

Michoacán 16%

North America 35%

Europe 27%

U.S.A

Asia

1%

2% Germany 3% Slovakia 4% UK 5%

Russia (Europe) 23%

Romania 5% Hungary 5%

Ukraine 21%

Poland Czech 7% BulgariaRep. 7% 8% Serbia France Bosnia and Herzegovina Belarus Italy Macedonia Greece

Hidalgo 8% Durando 6% Guanajuato 5%

Hawaii 4% Texas 4% California 4% Arizona 10%

Asia 30%

Europe

Nevada 3%

Austria CroaƟa Latvia Lithuania Moldova Spain Switzerland

1%

2% 3% Thailand 4% Iran 4%

China 21%

Japan 5% Turkey 15% Russia (Asia) 6% Iraq Tajikistan India 9% 6% 7% Uzbekistan 9% Turkmenistan Kazakhstan Kyrgyzstan Afganistan Korea Sri Lanka Indonesia

Georgia Armenia Philippines Azerbaijan Malaysia Bangladesh Nepal

(See figure legend on the bottom of the next page.)

516


In Europe, most of the records are from Russia (23%; 74 from a total of 94 records are from its European part) followed by the Ukraine (21%), Czech Republic, Bulgaria, and Poland (8%, 7%, and 7%, respectively) (Figure 3). The northern-most record is from the Rybinsk Reservoir on the Volga River in Russia (58 220 N) (Figure 4). The records from the Palaearctic Asia include those from most of the countries south of 60 N, with the majority of records from China (21%; 75 records), Turkey (15%; 55 records), India, and Uzbekistan (9%), followed by Tadjikistan and Iraq (Figures 3 and 4). Records from southeastern Asia, such as Thailand or Bangladesh, are scarce, as are reports from islands such as the Philippines, Sri Lanka, Sumatra, and Padang in Malaysia (Figure 4; Table S2). Noteworthy is the finding of S. acheilognathi from Schizopyge niger in Kashmir, India, by Ummer Rashid Zargar, which was confirmed genetically (Table S3). However, the closely related species S. nayarensis has also been confirmed in North India [2]. North America The AFT was first found by G.L. Hofmann in 1975 in Notemigonus crysoleucas and Pimephales promelas, and somewhat later in Ct. idella in Arkansas [40]. The AFT was most probably first imported to the USA with Ct. idella in 1963 as shipments of fingerlings from Malaysia and Taiwan to the US Fish and Wildlife Federal Fish Hatcheries in Stuttgart, Arkansas, and Auburn, Alabama, respectively [11,41]. This fish species was imported to be reared and further bred as a biological control agent against aquatic weeds [11]. The occurrence of the AFT in North America is well documented, with most numerous records from Mexico (245) and USA (165), but only nine records from Canada. At a finer geographic scale, most of the North American records (16%) are from the Mexican state of Michoacán, followed by Arizona (USA; 10%), Hidalgo and Durango (both Mexico; 8% and 6% of records, respectively) (Figure 3). The northern-most records are from the Parsnip and McGregor Rivers in British Colombia, Canada (around 55 N) and Lake Winnipeg in Manitoba, Canada (around 52 N) (Figure 4). Other Canadian records are from the Great Lakes area. The parasite has been already reported from 20 US states across the whole country, including Hawaii and Puerto Rico, but no records are available from the Pacific Northwest and the northern Central Plains states of the USA and some regions on the Atlantic coast (Figure 4). Numerous records from Mexico include 24 of 31 states (not including Distrito Federal, i.e., the capital) in both its Nearctic and Neotropical regions, with most reports from southern and central parts of Mexico (see Pérez-Ponce de León et al. [15]) (Figures 3 and 4). Central and South America Only three records of S. acheilognathi are available from Central America (Guatemala, Honduras, and Panama), but the parasite has not been found in other countries of this region, that is, Belize, Costa Rica, El Salvador, and Nicaragua [42–44] (Figure 4). All five records from Brazil concern the occurrence of the AFT in fish species imported for aquaculture, that is, the transfer to native fish hosts does not seem to have happened yet in this hot spot of fish diversity (Piazza et al. [19], Santos et al. [20], and Rego et al. [45]) (Figure 4). The only record from wild fish populations is that of Waicheim et al. [46] in Patagonia, Argentina, but the hosts (feral common carp) are not native fish. Eggs of the AFT have been found in the stool Figure 3. Geographic Distribution of the Records of Schyzocotyle acheilognathi. *Clockwise: Estado de Mexico 4%; Querétaro 3%; Jalisco 2%; Chiapas 2%; Chihuahua 1%; Morelos 1%; Puebla 1%; Mexico City 1%; Oaxaca 1%; Tlaxcala 1%; Yucatán 1%; Guerrero 1%; Coahuila 1%; Nayarit 1%; San Luis Potosí 1%; less than 1% – Campeche; Aguascalientes; Tabasco; Veracruz; Zacatecas. **Clockwise: North Carolina 3%; Utah 3%; Arkansas 3%; Michigan 2%; Nebraska 1%; New Mexico 1%; Colorado 1%; less than 1% – Kansas; Kentucky; Florida; Wisconsin; Indiana; Louisiana; New Hampshire; New York. Canada clockwise: Ontario; British Colombia; Manitoba; Quebéc. Central America clockwise: Panama; Guatemala; Honduras.


517

PalearcƟc

60°N

NearcƟc

Carps infected First record on conƟnent

Figure 4. Geographic Distribution of Schyzocotyle acheilognathi, along with the Year It Was First Recorded in Each Country/Region. Yellow dots represent single records.

of a patient from French Guiana, which has been confirmed genetically, but the aetiology of the infection remains unclear [24]. Africa The AFT was reported from tropical Africa as early as in 1958, that is, the same year the AFT was first reported from Europe, from native barbels in Lake Kivu, the Democratic Republic of the Congo, and described as Bothriocephalus (Clestobothrium) kivuensis. Additional material of S.

518


acheilognathi collected by J.G. Baer in Hydrocynus vittatus (Characiformes) from the same country has recently been confirmed [47]. It is worth mentioning that there are no reliable data on imports of cyprinids, including potential hosts of the AFT, from Asia or other regions, to that part of Africa. Together with Volz’s [25] finding of tapeworms that may be conspecific with the AFT in 1861 in Ethiopia, this early report of tapeworms now considered to be the AFT raises the question about the actual origin of this parasite. Nevertheless, its potential African origin does not explain the occurrence of the AFT in a large area of eastern Asia including Japan in the 1930s–1950s. The AFT is currently known to occur in Algeria, the Democratic Republic of the Congo, Egypt, Ethiopia, Morocco, Nigeria, South Africa, and Zimbabwe, with most of the records from South Africa (Figures 3 and 4). Most records are from native species of the Barbinae and Cyprininae (commonly called ‘barbels’) and introduced Cy. carpio. In contrast, clariid catfishes reported as hosts of the AFT in Nigeria and Zimbabwe are considered as accidental (likely postcyclic) hosts; misidentification cannot be ruled out because no vouchers were deposited to verify these reports [47]. Australia The AFT was introduced also to Australia with common carp imported to Boolarra, Victoria [13]. The first record from a native wild host in Australia was published by Dove et al. [6] from New South Wales. So far, 14 fish hosts (seven native species) have been recorded as hosts of AFT in Australia (Figure 4) [13]. Islands The AFT was also introduced to several continental or oceanic islands, including remote ones. The first case included the original description of the AFT from Honshu, Japan [1]. The parasite was later reported from Sri Lanka [30], New Zealand (later eradicated) [48], the UK [49], Cuba [50], the Philippines [51], Hawaii [10], Puerto Rico [52], Mauritius [53], Indonesia [54], and, recently, in endemic cichlids in Madagascar [55] (Figure 4).

Phylogeography and Population Biology of the AFT Surprisingly, no rigorous analysis on the geographic origin of the AFT has been carried out. Recently, Brabec et al. [56] developed a set of 15 polymorphic microsatellite markers that may help in future studies on the phylogeography and population biology of the AFT. Microsatellite loci were selected from partial Illumina shotgun genome sequences of three parasite specimens and their universality tested on a set of 12 geographically distant populations of the parasite, representing its global diversity. These newly developed markers may help to overcome the limited utility of the nuclear rRNA sequences, including widely used internal transcribed spacers [56].

Factors in Successful Colonisation On a global scale, the AFT is probably the most successful invasive metazoan parasite [57] and thus it is worth discussing possible factors that may have facilitated this success. Based on the conclusions of Bauer and Hoffman [58] and Bauer [59], Kennedy [8] analysed the introduction of helminth parasites from an ecological perspective and discussed the attributes of a good colonist. Whereas some of the factors appear to explain the colonisation success of the AFT, others do not, as is obvious (Box 2). The success of S. acheilognathi as an invasive species is also worth discussing in the context of key characteristics that have been proposed to more broadly determine the success of alien


519

Box 2. Factors in Successful Colonisation (i) Complexity of life cycles. The colonisation ability of a parasite is considered to be inversely proportional to the complexity of its life cycle; parasites with direct life cycles such as monogeneans are thus likely to be more successful as invasive species. This generalisation is contradicted by S. acheilognathi, a tapeworm with a complex, indirect, developmental cycle that includes copepods as intermediate hosts (but see ii, below). (ii) Low host specificity. A parasite capable of utilising a broad spectrum of hosts, at the level of both definitive and intermediate hosts, is likely to be more successful as an invasive species than one that is narrowly host specific at one or more stages of its life cycle. As noted earlier, a long list of definitive hosts spanning a wide phylogenetic spectrum of freshwater fishes and a broad range of suitable copepod intermediate hosts allow the AFT to utilise multiple hosts as links in its trophic transmission, in a variety of biomes across the globe [63,72–74]. This supports Kennedy’s proposition that generalist parasites and those ‘using cosmopolitan invertebrates, such as some species of copepod, would also make more successful colonists’ [8]. (iii) Similarity of abiotic and biotic conditions between the original and new localities. Considering the fact that AFT has colonised regions and ecosystems with substantially different physicochemical characteristics, this factor does not readily explain its colonisation success. The AFT is considered a thermophilic species with an optimum temperature range of 25–30 C for reproduction [75], but the tapeworm is also found in the Amur River and has successfully colonised Lake Winnipeg in Manitoba, Canada. Therefore, it is also able to thrive in colder temperate zones where the transmission window is narrower and open only for a short period during summer [8]. The eggs of the AFT can develop over a broad range of water temperatures but development is notably slow below 12 C, and the parasite is largely absent in extreme cold climatic zones, that is, north of 60 C (see Figure 3 in main text). (iv) Composition and richness of parasite communities in recipient hosts. The nature of parasite communities in recipient hosts may also play a role in the success of colonisation, with species-poor and isolationist parasite communities, as well as vacant niches in recipient hosts, representing favourable circumstances for successful invaders. A common recipient host group for invasive AFT are the cyprinodontoids, a fish group notably lacking their own typical adult tapeworm fauna in their gastrointestinal tract. This general absence of adult native tapeworms is also true for most cichlids and atherinids. It is thus possible that AFT is exploiting an available open niche in these fishes. However, it is also possible that the AFT is primarily adapting to the physiological conditions of the gut of these fishes.

invasive species in freshwater ecosystems [57,60,61], which include (i) synanthropic associations, (ii) efficient resource use and wide environmental/physiological tolerance, (iii) life history strategy, reproductive style, capacity and timing, (iv) phenotypic plasticity or rapid genetic differentiation or both, and (v) membership of a certain taxonomic group. (i) Based on the literature, it is plausible to assume that the AFT got its start as an invasive species by anthropogenic activities (translocation and stocking) related to the aquaculture of carps in Eurasia, the oldest and culturally most valued freshwater fishes associated with human civilisation there. Such activities were also repeated and sustained, thereby providing the tapeworm opportunities for multiple colonisation events. These aquaculture practices were followed by other human activities such as translocating grass carp to control aquatic vegetation in the USA and elsewhere, and movement of baitfish [9,11,12]. Thus, the deliberate translocation of the AFT’s hosts – and thereby its own inadvertent dispersal into distant ecosystems and habitats – was primarily anthropogenic, and later enhanced by the natural dispersal of their introduced fish hosts in the wild. (ii) The idea that species that are able to efficiently exploit crucial resources for growth and metabolism will also be successful invasive species [57,62] appears to be intuitive because of the competitive edge this may provide invasive species in new habitats. The AFT develops quickly in both the copepod and fish hosts at temperatures between 25 C and 28 C but can also develop, albeit more slowly, at much lower temperatures [11,12]. The AFT also develops in a wide range of cyclopoid copepods [63] and thrives in the intestine of hosts as disparate as cyprinids and cyprinodontoids. Without detailed information on the nutritional physiology of the

520


AFT and the gut physiology of their disparate hosts, it is difficult to determine if these life-history traits suggest efficient use of key nutritional resources. However, these attributes do suggest broad environmental and physiological tolerance, a key feature of several highly successful aquatic invasive species [64,65]. (iii) Many successful invasive species are r-strategists with high fecundity [59]; the AFT is no exception [11,12]. In the case of the AFT, this strategy allows for the introduction of thousands of eggs – that also have a wide temperature tolerance – as ‘propagules’ in the invasion process. The eggs of the AFT develop in a temperature-dependent manner over a period of days to weeks, which can allow changes in water flow due to flooding and spring run-off to disperse the eggs over a wide area before they hatch. The hatched larvae of the AFT are short-lived (2–6 days depending on temperature) but can also be dispersed by water currents. (iv) While a considerable body of information suggests that many invasive species, especially ‘weed’ species, may owe their success to their ‘general purpose genotype’ [57,66], these factors are difficult to apply to the AFT because our estimates of genetic diversity of the AFT populations worldwide are still incomplete [67–70]. (v) The success of the AFT as an invasive species is in fact unusual and unexpected, because most cestode species do not cross wide divides in host phylogeny and are rather specific in a small subset of closely related hosts [71]. The AFT is exceptional in its ability to infect and mature in host lineages as distantly related as cyprinids (its original host family), cyprinodontoids, and cichlids. To our knowledge, no other tapeworm species (and probably no other helminth parasite) has such a widely divergent spectrum of definitive hosts. Therefore, the AFT is without precedent in its taxonomic group.

Concluding Remarks and Future Perspectives The present review provides the most detailed summary of the spectrum of the hosts of the AFT and its current geographic distribution available so far, following a critical evaluation of published records. As a result, we can update the number of hosts of the AFT to 312 fish hosts, as well as 11 non-fish hosts, an increase of as much as 50%. However, only a small proportion of these records were confirmed genetically, that is, by genotyping tapeworms from these hosts. It is thus recommended that species identification be confirmed by sequencing worms found in other hosts, especially in hosts other than cypriniforms and cyprinidontiforms. The idea of the AFT’s origins in Asia is somewhat challenged by its occurrence in tropical Africa before human introduction of cyprinids from Asia. Finally, the AFT remains singular among helminths for both its phenomenal range and the blend of biological and life history characteristics that make it such a successful invasive species.

Outstanding Questions What specific physiological attributes make the AFT such a successful invasive parasite? Is the thermal preference and/or tolerance of individual populations of the AFT related to that of their original (source) geographic populations? What is the actual geographic area of origin of the AFT? What is the extent of the genetic variability of individual populations from different hosts and geographic regions? How does the genetic diversity of geographic populations of the AFT relate to invasion potential and the invasion process? What is the actual impact of the AFT on cultured ornamental fishes and native endemic fish hosts? How will climate change potentially impact the further spread of the AFT? What is the most effective way to monitor areas and fish populations that are at ‘high risk’ for AFT invasions?

Future research should be focussed on the following questions/problems (see Outstanding Questions): (i) the geographic origin of the AFT based on phylogeographic study of numerous populations from distant localities and zoogeographic regions; (ii) assessment of the genetic variability of individual populations using suitable markers, for example, recently designed microsatellites; (iii) the relationship between genetic diversity and invasion potential of individual geographically distant populations of the AFT; (iv) a critical assessment of the pathogenic impact of the AFT on cultured ornamental fishes and wild endemic fish hosts; (v) testing thermal preference and/or tolerance of individual populations of the AFT in relation to climate change; (vi) experimental studies on the life cycle of the AFT, with a focus on the suitability of different species of copepods as intermediate hosts; and (vii) monitoring of areas and fish populations that are at ‘high risk’ for AFT invasions. Trends in Parasitology, June 2018, Vol. 34, No. 6

521

Acknowledgments The authors are much indebted to four anonymous reviewers and the Editor for numerous valuable comments and suggestions that made it possible to considerably improve this article. The following persons kindly provided specimens: Gerardo Pérez-Ponce de León (Mexico), Takashi Shimazu (Japan), Andrea Vetešníková Šimková (Czech Republic), Misako Urabe (Japan), Ummer Rashid Zargar (India); thanks are also due to Jan Brabec (Czech Republic) who provided unpublished sequences of the AFT. This review was financially supported by the Czech Science Foundation (project No. 15-14198S) and the Institute of Parasitology, BC CAS (project No. 60077344). AC would like to acknowledge support from Faculty Development grants from St Norbert College.

Supplemental Information Supplemental information associated with this article can be found, in the online version, at https://doi.org/10.1016/j.pt. 2018.03.001.

References 1. Yamaguti, S. (1934) Studies on the helminth fauna of Japan. Part 4. Cestodes of fishes. Jpn. J. Zool. 6, 1–112

18. Evans, B.B. and Lester, R.J.G. (2001) Parasites of ornamental fish imported into Australia. Bull. Eur. Assoc. Fish Pathol. 21, 51–55

2. Brabec, J. et al. (2015) Molecular phylogeny of the Bothriocephalidea (Cestoda): molecular data challenge morphological classification. Int. J. Parasitol. 45, 761–771

19. Piazza, R.S. et al. (2006) Parasitic diseases of freshwater ornamental fishes commercialized in Florianópolis, Santa Catarina, Brazil. Bol. Inst. Pesca 32, 51–57

3. Bauer, O.N. et al. (1973) Disease of Pond Fish, Izdatelstvo Kolos

20. Santos, M.A. et al. (2017) Parasitic fauna and histopathology of farmed freshwater ornamental fish in Brazil. Aquaculture 470, 103–109

4. Yeh, L.S. (1955) On a new tapeworm Bothriocephalus gowkongensis n. sp. (Cestoda: Bothriocephalidae) from fresh-water fish in China. Acta Zool. Sin. 7, 69–73 5. Williams, H. and Jones, A. (2002) Parasitic Worms of Fish, Francis & Taylor

21. Hernandez-Ocampo, D. et al. (2012) Parasitic helminth infection in tropical freshwater fishes of commercial fish farms, in Morelos State, Mexico. Int. J. Anim. Vet. Adv. 4, 338–343

6. Dove, A.D.M. et al. (1997) The Asian fish tapeworm, Bothriocephalus acheilognathi, in Australian freshwater fishes. Mar. Freshw. Res. 48, 181–183

22. Chaudhary, A. et al. (2015) First molecular identification of invasive tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda: Bothriocephalidea) in India. BioInvas. Rec. 4, 269–276

7. Hoffman, G.L. (1999) Parasites of North American Freshwater Fishes, University of California Press

23. Košuthová, L. et al. (2015) The pathogenic Asian fish tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda) in the Red discus (Symphysodon discus). Helminthologia 52, 287–292

8. Kennedy, C.R. (1994) The ecology of introductions. In Parasitic Diseases of Fish (Pike, A.W. and Lewis, J.W., eds), pp. 189–208, Samara Publishing 9. Scholz, T. (1999) Parasites in cultured and feral fish. Vet. Parasitol. 84, 317–335 10. Font, W.F. and Tate, D.C. (1994) Helminth parasites of native Hawaiian freshwater fishes: an example of extreme ecological isolation. J. Parasitol. 80, 682–688 11. Choudhury, A. and Cole, R.A. (2011) The Asian fish tapeworm Bothriocephalus acheilognathi. In A Handbook of Global Freshwater Invasive Species (Francis, R.A., ed.), pp. 389–404, Earthscan 12. Scholz, T. et al. (2012) Bothriocephalus acheilognathi . In Fish Parasites: Pathobiology and Protection, pp. 282–297, CAB International 13. Dove, A.D.M. and Fletcher, A.S. (2000) The distribution of the introduced tapeworm Bothriocephalus acheilognathi in Australian freshwater fishes. J. Helminthol. 74, 121–127 14. Salgado-Maldonado, G. and Pineda-Lopéz, R.F. (2003) The Asian fish tapeworm Bothriocephalus acheilognathi: A potential threat to native freshwater fish species in Mexico. Biol. Inv. 5, 261–268 15. Pérez-Ponce de León, G. et al. (2017) Update on the distribution of the co-invasive Schyzocotyle acheilognathi (= Bothriocephalus acheilognathi), the Asian fish tapeworm, in freshwater fishes of Mexico. J. Helminthol. Published online May 22, 2017. http://dx. doi.org/10.1017/S0022149X1700043 16. Boonthai, T. et al. (2017) The Asian fish tapeworm Schyzocotyle acheilognathi is widespread in baitfish retail stores in Michigan, USA. Parasites Vectors 10, 618 17. Caira, J.N. et al. (2003) On a new index of host specificity. In Taxonomy, Ecology and Evolution of Metazoan Parasites (Combes, C. and Jourdane, J., eds), pp. 161–201, Presses Universitaires de Perpignan

522


24. Yera, H. et al. (2013) First identification of eggs of the Asian fish tapeworm Bothriocephalus acheilognathi (Cestoda: Bothriocephalidea) in human stool. Parasitol. Int. 62, 268–271 25. Volz, W. (1900) Beitrag zur Kenntnis einiger Vogelcestoden. Arch. Naturgeschichte 66, 115–174 26. Tadros, G. (1966) On the classification of the family Bothriocephalidae Blanchard, 1849 (Cestode). J. Vet. Sci. U. A. R. 3, 39–43 27. Prigli, M. (1975) The role of aquatic birds in spreading Bothriocephalus gowkongensis Yeh, 1955 (Cestoda). Parasitol. Hung. 8, 61–62 28. Borgarenko, L.F. (1981) Cestodes of the order Pseudophyllidea in birds in Tadzhikistan. lzv. Akad. Nauk Tadzhikskoi SSR Otdelenie Biol. Nauk 1981, 99–100 29. Malevitskaia, M.A. (1958) The introduction of a parasite with a complex life cycle, Bothriocephalus gowkongensis Yen, 1955, during acclimatization of fish from the Amur River. Dok. Akad. Nauk SSSR Biol. Sci. Sect. 123, 961–964 30. Fernando, C.H. and Furtado, J.I. (1963) A study of some helminth parasites of freshwater fishes in Ceylon. Z. Parasitenk. 23, 141– 163 31. Chandra, K.J. and Golder, M.I. (1987) Effects of helminth parasites on a freshwater fish Nandus nandus. Environ. Ecol. 5, 333– 336 32. Wongsawad, C. et al. (2004) Helminths of vertebrates in Mae Sa Stream, Chiang Mai, Thailand. Southeast Asian J. Trop. Med. Public Health 35 (Suppl. 1), 140–146 33. Deshmukh, V. et al. (2016) Bio-systematic studies on cestode genus Ptychobothrium Loennber 1889 (Cestoda: Ptychobothriidae, Luhe, 1902) from freshwater fish Mystus seenghala (Sykes 1839) with description of a new species. J. Exp. Zool. India 19, 127–130 34. Dollfus, R.P. (1970) D'un cestode ptychobothrien parasite de cyprinide en Iran. Mission C.N.R.S. (Theodore Monod), février 1969. Bull. Mus. Natl. Hist. Nat. Paris 41, 1517–1521

35. Babaev, B. (1965) Distribution of Bothriocephalus gowkongensis Yeh, 1955 (Cestodea, Pseudophyllidea) in the water of the KaraKum Canal. Zool. Zh. 44, 1407–1408

56. Brabec, J. et al. (2018) Development of polymorphic microsatellites for the invasive Asian fish tapeworm Schyzocotyle acheilognathi. Parasitol. Int. 67, 341–343

36. Osmanov, S.O. (1971) Parasites of Fish in Uzbekistan. Izdatelstvo FAN

57. Francis, R.A. (2012) A Handbook of Global Freshwater Invasive Species, Taylor & Francis

37. Ali, N.M. et al. (1987) Parasitic fauna of some freshwater fishes from Tigris river, Baghdad, Iraq. III. Cestoda. J. Biol. Sci. Res. 18, 25–33

58. Bauer, O.N. and Hoffman, G.L. (1976) Helminth range extension by translocation of fish. In Wildlife Diseases (Page, L., ed.), pp. 163–172, Plenum Publishing

38. Moravec, F. and Amin, A. (1978) Some helminth parasites, excluding Monogenea, from fishes of Afganistan. Acta Sci. Nat. Brno 12, 1–45

59. Bauer, O.N. (1991) Spread of parasites and diseases of aquatic organisms by acclimatization: a short review. J. Fish Biol. 39, 679–686

39. Dzhalilov, U.D. (1972) On the distribution of Bothriocephalus gowkongensis Yeh, 1955 in drainage system of the Tadzhik SSR. Iz. Akad. Nauk Tadzhikskoi SSR Otdelenie Biol. Nauk 1972, 67–70

60. Gherardi, F. (2007) Biological invasions in inland waters: an overview. In Biological Invaders in Inland Waters: Profiles, Distribution, and Threats (Gherardi, F., ed.), pp. 3–25, Springer

40. Hoffman, G.L. (1980) Asian tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934, in North America. Fisch Umwelt 8 (Special), 69–75

61. Moyle, P.B. and Marchetti, M.P. (2006) Predicting invasion success: Freshwater fishes in California as a model. Bioscience 56, 515–524

41. Fuller, P.L. et al. (1999) Nonindigenous Fishes Introduced into the Inland Waters of the US. Am. Fish. Soc.

62. Pyšek, P. and Richardson, D.M. (2007) Traits associated with invasiveness in alien plants: where do we stand? In Biological Invasions (Nentwig, W., ed.), pp. 97–125, Springer

42. Pinacho-Pinacho, C.D. et al. (2015) Checklist of the helminth parasites of the genus Profundulus Hubbs, 1924 (Cyprinodontiformes, Profundulidae), an endemic family of freshwater fishes in Middle-America. Zookeys 523, 1–30

63. Marcogliese, D.J. and Esch, G.W. (1989) Experimental and natural infection of planktonic and benthic copepods by the Asian tapeworm, Bothriocephalus acheilognathi. Proc. Helminthol. Soc. Wash. 56, 151–155

43. Choudhury, A. et al. (2013) The invasive Asian fish tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934, in the Chagres River/Panama Canal drainage, Panama. BioInvas. Rec. 2, 99– 104

64. Dittel, A.I. and Epifanio, C.E. (2009) Invasion biology of the Chinese mitten crab Eriochier sinensis: A brief review. J. Exp. Mar. Biol. Ecol. 374, 79–92

44. Salgado-Maldonado, G. et al. (2015) First record of the invasive Asian fish tapeworm Bothriocephalus acheilognathi in Honduras, Central America. Parasite 22, 5 45. Rego, A.A. et al. (1999) Cestodes in South American freshwater teleost fishes: keys to genera and brief description of species. Rev. Brasil Zool. 16, 299–367 46. Waicheim, A. et al. (2014) Macroparasites of the invasive fish, Cyprinus carpio, in Patagonia, Argentina. Comp. Parasitol. 81, 270–275 47. Kuchta, R. et al. (2012) Bothriocephalidean tapeworms (Cestoda) of freshwater fish in Africa, including erection of Kirstenella n gen. and description of Tetracampos martinae n. sp. Zootaxa 3309, 1– 35 48. Edwards, D.J. and Hine, P.M. (1974) Introduction, preliminary handling, and diseases of grass carp in New Zealand. N. Z. J. Mar. Freshw. Res. 8, 441–454 49. Andrews, C. et al. (1981) The occurrence of Bothriocephalus acheilognathi Yamaguti, 1934 (B. gowkongensis) (Cestoda: Pseudophyllidea) in the British Isles. J. Fish Dis. 4, 89–93 50. Vinjoy, M. et al. (1988) Bothriocephalus acheilognathi Yamaguti 1934 (Cestoda: Bothriocephalidae) in the herbivorous carp Ctenopharyngodon idella. Systematic position anatomy and epizootiology. Rev. Cubana Cien Vet. 19, 261–266 51. Lumanlan, S.C. et al. (1992) Freshwater fishes imported into the Philippines: their parasite faunas and role in the international spread of parasitic diseases. In Diseases in Asian Aquaculture I. Fish Health Section (Shariff, M., ed.), pp. 323–335, Asian Fisheries Society 52. Bunkley-Williams, L. and Williams, E.H. (1994) Parasites of Puerto Rican Freshwater Sport Fishes, Puerto Rico Department of Natural and Environmental Resources, San Juan, Puerto Rico, and Department of Marine Sciences, University of Puerto Rico 53. Paperna, I. (1996) Parasites, Infections and Diseases of Fishes in Africa – An Update, CIFA Technical Paper No. 31, FAO 54. Muchlisin, Z.A. et al. (2015) First report on Asian fish tapeworm (Bothriocephalus acheilognathi) infection of indigenous mahseer (Tor tambra) from Nagan Raya district, Aceh province, Indonesia. Bulgarian J. Vet. Med. 18, 361–366 55. Scholz, T. et al. (2018) The first record of the invasive Asian fish tapeworm (Schyzocotyle acheilognathi) from an endemic cichlid fish in Madagascar. Helminthologia 55, 84–87

65. D’Amore, A. (2012) Rana [Lithobates] catesbeiana Shaw (American bullfrog). In A Handbook of Global Freshwater Invasive Species (Francis, R.A., ed.), pp. 321–330, Abingdon Earthscan 66. Richardson, D. and Pyšek, P. (2006) Plant invasions: Merging the concepts of species invasiveness and community invisibility. Progr. Phys. Geogr. 30, 409–443 67. Luo, H.Y. et al. (2002) Molecular variation of Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda: Pseudophyllidea) in different fish host species based on ITS rDNA sequences. Syst. Parasitol. 52, 159–166 68. Luo, H.Y. et al. (2004) Characterization of development-related genes for the cestode Bothriocephalus acheilognathi. Parasitol. Res. 94, 265–274 69. Li, W.X. et al. (2017) The complete mitochondrial DNA of three monozoic tapeworms in the Caryophyllidea: a mitogenomic perspective on the phylogeny of eucestodes. Parasit. Vectors 10, 314 70. Brabec, J. et al. (2016) Paralogues of nuclear ribosomal genes conceal phylogenetic signals within the invasive Asian fish tapeworm lineage: evidence from next generation sequencing data. Int. J. Parasitol. 46, 555–562 71. Caira, J.N. and Jensen, K. (2017) Planetary Biodiversity Inventory (2008-2017): Tapeworms from the Vertebrate Bowels of the Earth, University of Kansas, Natural History Museum Special Publication No. 25 72. Pár, O. (1978) Intermediate hosts of Bothriocephalus gowkonany district (Czechoslovakia). Bul. gensis in fishponds of the Vodn any 14, 1–28 VÚRH Vodn 73. Urazbaev, A. and Allaniyazova, T. (1977) Biology and life-cycle of Bothriocephalus gowkongensis Yeh, 1955 (Cestoda: Pseudophyllidea) in the Amu-Dar'ya river area. In Diseases of Fish and their Control on Kazakhstan and the Central Asian Republics, pp. 147–150, Akad. Nauk. Kaz. SSR 74. Nedeva, I.L. et al. (1984) Planktonic intermediate hosts of Bothriocephalus acheilognathi Yamaguti (Cestoda) at some fish farms in the Sofia region. Khidrobiologiya 22, 51–58 75. Liao, H.-H. and Shih, L.-C. (1956) Contribution to the biology and control of Bothriocephalus gowkongensis Yeh, a tapeworm parasitic in young grass carp (Ctenopharyngodon idellus C. a. V.). Acta Hytrobiol. Sin. 2, 129–185


523