Next Article in Journal
First Report of Troglotrema acutum Trematoda Parasitizing a European Polecat (Mustela putorius) in Bulgaria
Previous Article in Journal
Effect of Anthelmintic Treatment on the Agreement Between Real-Time Polymerase Chain Reaction (RT-PCR) and Kato–Katz Microscopic Technique in the Diagnosis of Soil-Transmitted Helminth Infections
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Parasitologia
Volume 4
Issue 4
10.3390/parasitologia4040031
parasitologia-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Potential Role of the Eastern Mosquitofish (Gambusia holbrooki) in the Spread of the Harmful Fish Parasite, Asian Tapeworm Schyzocotyle (Bothriocephalus) acheilognathi

by
Daria I. Lebedeva
1,*,
Andrey B. Petrovskiy
2 and
Andrey N. Reshetnikov
2
1
Karelian Research Centre of RAS, 185000 Petrozavodsk, Russia
2
Severtsov Ecology and Evolution Institute, RAS, 119071 Moscow, Russia
*
Author to whom correspondence should be addressed.
Parasitologia 2024, 4(4), 358-368; https://doi.org/10.3390/parasitologia4040031
Submission received: 8 September 2024 / Revised: 23 October 2024 / Accepted: 28 October 2024 / Published: 4 November 2024
Browse Figures
Versions Notes

Abstract

:
Biological control of undesirable organisms and pathogens often involves the introduction of alien species into new regions. However, alien species themselves pose a potential threat to local ecosystems and economies. The Eastern mosquitofish Gambusia holbrooki is recognised as a dangerous invasive species, but despite this, it is still used for biological control of mosquito larvae, a potential vector of malaria plasmodium transmission to humans, on the Black Sea coast of the Caucasus. We focused on the species composition of helminths in this fish species. We detected adult nematodes Pseudocapillaria (Pseudocapillaria) tomentosa and cestodes Schyzocotyle acheilognathi (formely Bothriocephalus acheilognathi). The above nematode was observed for the first time in fish of the genus Gambusia. Importantly, the cestode S. acheilognathi, which we found in G. holbrooki, is the most successful invasive alien parasite species in freshwaters of the planet and is extremely hazardous to natural ecosystems and aquaculture as it can cause mass mortality of young fish. Thus, the current practice of transferring mosquitofish between water bodies on the Black Sea coast of the Caucasus to control mosquito larvae may contribute to the undesirable spread of a harmful quarantine fish parasite.

1. Introduction

Biological control of unwanted (pest) organisms and pathogens involves the introduction of alien species into new regions [1,2]. However, alien species are able to establish sustainable populations, establish trophic and other relationships with native species, and local parasitic systems are often transformed [3,4]. The Eastern mosquitofish, Gambusia holbrooki Girard, 1859 (family Poeciliidae) is native to North America. Since the first half of the 20th century, this species, along with a closely related form, G. affinis (Baird & Girard, 1853), has been widely used to control malaria, as this fish effectively destroys the larvae of blood-sucking mosquitoes, the adults of which are involved in the transmission to humans of the malaria agent (several species of Plasmodium sp.) then cause malaria, a disease damaging to human health. This is the reason for the widespread geographical distribution of mosquitofish. To date, invasive populations of mosquitofish are known to occur on all continents except Antarctica [5,6]
Mosquitofish has been present in the Caucasus since 1925, when Dr. N.P. Rukhadze, head of the Abkhazian Tropical Institute, brought 153 specimens from Italy to the vicinity of Sukhumi. In the following years, the mosquitofish was deliberately introduced into a number of water bodies in the south-western part of the USSR to control malaria [7]. However, this fish species can pose a threat to native hydrobionts in the areas of introduction [8]. For this reason, mosquitofish release has been removed from the World Health Organisation’s list of recommended malaria control measures since 1982 [9]. Despite this, the practice of using mosquitofish to control mosquito larvae continues to be used on the Black Sea coast of the Caucasus. Currently, the Eastern mosquitofish is considered one of the most dangerous invasive species threatening freshwater ecosystems of small water bodies in southern Russia [6]. However, important information on the involvement of this fish species in the circulation of parasites in this geographical area is lacking.
The aim of this work is to determine the helminth composition of the invasive fish species, G. holbrooki, from water bodies of the Black Sea coast of the Caucasus and to assess the possible participation of this fish in the circulation of parasite species that may be potentially harmful for representatives of the native biota.

2. Materials and Methods

2.1. Study Area

The study was conducted in the area of the city of Sochi, Krasnodar Krai, Russia. This area was chosen because the terrestrial and aquatic ecosystems of the Black Sea coast of the Caucasus are unique in many respects, but are undergoing relatively rapid transformation for various reasons, including invasions of alien species [10,11,12,13,14,15]. The invasion of some alien species in this region has had a significant impact on local ecosystems in terms of loss of biodiversity and destruction of local relict species [16]. One of the undesirable invaders in water bodies of the Caucasus is mosquitofish G. holbrooki [6].

2.2. Study Sites

Four water bodies inhabited by mosquitofish were studied (Figure 1). Species identification (G. holbrooki) was determined by the number of rays in the fins and the shape of the gonopodium of males [17,18]. Water body 1 (43.4259 N; 39.9729 E) is a pond (4420 m2) fed by a narrow stream descending from the mountains. According to oral communications from local residents, attempts have been made to stock the pond with pike, Gibel carp, and ‘other species of fish’.
Water bodies 2 and 4 (43.5145 N; 39.9314 E and 43.5121 N; 39.9331 E) are small ponds (1750 m2 and 970 m2, respectively). These ponds are located relatively close to each other but are separated by a road and are not connected to each other. Both ponds are used as watering places for livestock (cows, horses).
Water body 3 (43.421622 N; 39.938412 E) is a slow-flowing stream 1–3 metres wide. Downstream (relative to the mosquitofish collection site), this stream flows through the Yuzhnye Kultury Dendrological Park, where it fills a cascade of ponds. These ponds are inhabited by ornamental koi carp Cyprinus rubrofuscus Lacépède, 1803, and domestic waterfowl (ducks, geese). The stream is partly dry and breaks up into separate puddles in autumn. In the lower part of the stream, near the confluence with the Mzymta River, we registered the three-spined stickleback Gasterosteus aculeatus Linnaeus, 1758.

2.3. Sampling

Samples of G. holbrooki were collected in spring (8–13 March) and autumn (14–17 September) 2023 using a dipnet with 0.4 m rim diameter. In spring, 83 individuals of G. holbrooki were examined from three water bodies. In autumn, 115 individuals of this fish species from four water bodies were examined. In spring and autumn, fish were captured at the same points in the studied water bodies. The fish were collected in the coastal zone in thickets of submerged macrophytes. All procedures were performed in compliance with relevant laws of the Russian Federation. The animal study protocol was approved by the Ethics Committee of the Severtsov Institute of Ecology and Evolution, the Russian Academy of Sciences (protocol # 11 from 8 July 2017, prolongations and additions from 14 May 2018, 23 April 2021, and 12 April 2022). Data on the number, size, and sex ratio of the studied fish samples are given in Table 1.
Fish were examined by partial parasitological autopsy according to the method of Bykhovskaya-Pavlovskaya [19]. Organs of fish (fins, gills, eyes, brain, oral and abdominal cavities, heart, spleen, intestine, gall bladder, liver, urinary bladder, kidney, ureteral tubes, and gonads) were examined for metazoan parasites only, but not for Protozoa and Myxozoa. Nematodes were placed in a mixture of lactic acid and glycerin to increase transparency. Cestodes were stained with acetic acid carmine, passed through a series of alcohols of increasing concentration, cleared in dimethyl phthalate and immersed in Canadian balsam [19]. Measurements and morphological identification of parasites were carried out using an Olympus CX-41 and Levenhuk C1400 NG video system (LevenhukToupView 3.5. software) using keys of Moravec, Vismanis et al., and Protasova [20,21,22]. Parasite systematics are given according to World Register of Marine Species [23]. Ecological characteristics of parasite populations, prevalence (%) and intensity of infection (range, only for infected host individuals), were calculated according to Bush et al. [24].

2.4. DNA Extraction, Amplification, and Phylogenetic Analyses

The detected parasite species were investigated with molecular genetic methods. Genomic DNA was isolated from single ethanol-fixed specimens using DNA-Extran kits (Synthol, Moscow). Amplification of a partial nuclear genome region including 18SrRNA, ITS1, 5.8S, and ITS2 in the found nematodes was carried out with primers TW81 (5′-GTTTCCGTAGGTGAACCTGC-3′) and AB28 (5′-ATATGCTTAAGTTCAGCGGGT-3′) according the conditions provided by Joyce et al. [25]. The 18S rRNA V4 region of the cestodes was amplified using the forward primer Ces1 (5′-CCAGCAGCCGCGGTAACTCCA-3′) and reverse primer Ces2 (5′-CCCCCGCCTGTCTCTTTTGAT-3′) according to conditions described by Scholz et al. [26].
We carried out all PCR reactions in 20 μL of reaction mixture containing ready 5× ScreenMix (Evrogen, Moscow, Russia), 1.5 pmol of 5′ and 3′ primers, and 2 μL of DNA. We purified the PCR products Cleanup Standard Extraction Kit (Evrogen, Moscow, Russia) following the manufacturer’s instructions and then sequenced them with ABI PRISM 3100-Avant (Applied Biosystems Inc., Foster City, CA, USA).
Consensus sequences (1971 bp length for the ITS region of nematodes and 427 nt of 18S rRNA of cestodes) were assembled in MEGA10 and deposited in NCBI GenBank under accession numbers PQ164719–PQ164720 for the nematode and PQ163817–PQ163820 for the cestode.
The BasicLocal Alignment Search Tool (BLASTn) was used to search for previously sequenced close representatives of nematodes and cestodes. We further aligned and analysed them in MEGA10 [27] and trimmed them to the shortest lengths. We identified the best-fitting models (K2 + G + I for the ITS region and TN93 + G for 18S) and applied these models to analyse the phylogenetic relationships using maximum likelihood analysis. We used FigTree v 1.4 to visualise the resulting trees [28]. In total, two nematode and four cestode individuals from our samples were used for phylogenetic analysis.

3. Results

We found two species of helminths in the mosquitofish. Nematodes of the family Capillariidae were found in the fishes of water body 3 in spring. Nematodes were absent in mosquitofish samples from other three studied water bodies. In autumn sampling, plerocercoids of cestodes of the family Bothriocephalidae Blanchard, 1849, were found in fish from water body 1 and were not found in other three water bodies. The total prevalence for both parasite species was 4% and the intensity of infection was 1–2. We did not find any infected fish in water bodies 2 and 4.
Nematodes of the family Capillariidae, namely, Pseudocapillaria (Pseudocapillaria) tomentosa (Dujardin, 1843) Lomakin & Trofimenko, 1982, were found in the intestines of four of 30 fish (13.3%). Only females were infected with nematodes. Each infected fish had 1 nematode specimen (intensity of infection = 1). Nematodes were found in relatively large specimens of mosquitofish, with body lengths ranging from 43 to 48 mm. The morphology of the parasites was consistent with that reported by Vismanis et al. [21] and Moravec [20]. Additionally, molecular genetic analyses performed on partial nuclear genome sequences (Figure 2) showed that these sequences matched those of P. tomentosa from the red shiner fish, Cyprinella lutrensis (Baird & Girard, 1853) from the USA [29] and those of parasites from an unknown host in China (MZ724160; NCBI GenBank: Zou, unpublished). The both our sequences were identical. The P-distances between them and the above-mentioned samples were 0.12% for P. tomentosa from the USA (KU987805) and 0.09% for a sample from China (MZ724160).
In the population of water body 1, four fish (three females and one male) out of 70 examined were infected (prevalence 5.7%) by cestode plerocercoids. Three fish had one plerocercoid each, and one fish had two plerocercoids (intensity of infection 1–2). Parasites revealed in the intestines were relatively small, with body lengths ranging from 20 to 30 mm (Figure 3). The sequences of the investigated plerocercoid individuals were identical. They also were identical to samples from pale chub Zacco platypus (Temminck & Schlegel, 1846) from China [30] as well to samples from Homo sapiens from France [31].
Plerocercoid cestodes had a rounded scolex, 180 μm long and 200 μm wide, with well-expressed and deep botryas. The apical disc was fairly well expressed, had three small protrusions, and was 165 µm long and 30 µm wide. The neck of the scolex was long, approximately 180 µm. The larval stage of development of the parasite made species identification difficult; therefore, in addition to morphological characterisation, molecular genetic analysis was carried out using partial sequences of the 18S rRNA region. The phylogenetic analysis showed that the found cestode larvae belong to Schyzocotyle acheilognathi (Yamaguti, 1934) Brabec, Waeschenbach, Scholz, Littlewood & Kuchta, 2015 (Figure 4).

4. Discussion

The nematode P. tomentosa, which we found in mosquitofish, is a common parasite mainly of cyprinid fishes of the Holarctic region but has also been recorded in some other fish taxa, including cyprinodontoforms [32]. This nematode is usually localised in the rectum and posterior parts of the intestine. The life cycle of P. tomentosa is probably direct, without an intermediate host, but freshwater oligochaetes may play the role of a paratenic host [20]. In the basins of the Black and Azov seas, this parasite was previously recorded in several cyprinid species: the common bream (Abramis brama (Linnaeus, 1758)), the vimba bream Vimba vimba (Linnaeus, 1758), the ziege Pelecus cultratus (Linnaeus, 1758), and the shemaya Alburnus sp. [21,33]. The stream in which we found P. tomentosa in mosquitofish is a tributary of Mzymta River, with diverse fish fauna [34]. From the list of fishes inhabiting Mzymta river basin, the aforementioned nematode species can parasitise at least shemaya and Gibel carp [21,33,35] and probably Barbus tauricus Kessler, 1877, because Moravec et al. [36] mentioned that P. tomentosa was found in the closely related Barbus barbus (Linnaeus, 1758). Passing through the Youzhnye Kultury Dendrological Park, the stream forms a cascade of ponds with large numbers of koi carp, but hitherto we have no evidence that koi can be the host of the nematode P. tomentosa. Mosquitofish may have become infected with the nematode by ingesting free-swimming parasite eggs or by feeding on small oligochaetes of the genera Tubifex and Limnodrilus, which may serve as additional or reservoir hosts for the nematodes [20].
The detection of infestation of mosquitofish by an alien helminth species, the Asian tapeworm, S. acheilognathi (formely known as Bothriocephalus acheilognathi), which is harmful to native ichthyofauna and aquaculture facilities, is very important. This cestode has a two-host life cycle. Fish are the definitive host for this parasite and become infected by ingesting parasitised copepods. The parasite lives in the intestine of the fish. Each segment of the adult worm is capable of producing eggs, which are released with the faeces into the water, where they infect copepods [37]. Common carp (Cyprinus carpio Linnaeus, 1758), grass carp (Ctenophyaryngodon idella (Valenciennes, 1844)), and crucian carp (Carassius carassius (Linnaeus, 1758)) are most commonly infected. However this cestode species has a wide host range and has been found in more than three hundred fish species, mostly cyprinids [38]. This parasite damages fish by attaching to them and blocking intestinal function; this may cause mass mortality of juvenile fish [37,39,40].
The cestode S. acheilognathi originates from the north-eastern regions of China and the Far East of the Russian Federation [21,41]. This parasite has been spread from the regions of its native range to the western part of the former USSR and to the countries of Eastern and Central Europe, mainly together with translocated common carp, C. carpio, and grass carp, C. idella. To date, this cestode has colonised tropical, temperate, and subtropical regions of all continents and is only absent from Antarctica [42,43,44,45,46,47] and has been identified as the most successful invasive parasite in freshwaters [37,38].
The first record of S. acheilognathi in Europe is from western region of the USSR (1958); in the European part of the Russian Federation, this parasite was first reported in 1971–1972; the first record in southern Russia (Pre-Caucasus region) is from 1987 [38]. The cestode S. acheilognathi can infect fishes of the family Poeciliidae (21 spp. or 7% of total list of the known fish hosts of this parasite). This cestode can be detected in both widely distributed invasive poeciliid species: G. affinis and G. holbrooki e.g., [48,49]; G. affinis is the third species (after C. carpio and H. molitrix) in the list of the most frequently reported fish hosts of this parasite [38].
Water body 1, in which we detected S. acheilognathi in mosquitofish in 2023, is an artificially created park pond with a maximum depth of up to 3 metres. According to information from local residents, they had tried to stock the pond with Gibel carp, pike, and ‘other fishes’ on their own. During the collection of material for this study, no fish species other than G. holbrooki were caught but some relatively large fish were splashing in the middle of the pond. It is likely that the parasite was translocated into the pond with fish introduced by local people, but experimental evidence suggests that the parasite may have been introduced into ponds by passive transfer of parasite eggs on waterfowl [50].
The data we obtained for water bodies of the Black Sea coast of the Caucasus indicate that the species composition of helminths of mosquitofish is poor. The same number of parasite species (two) was recorded in a study of the mosquitofish parasite fauna in Spain: parasitic copepod Lernaea sp. and unidentified digeneans [51], while another study covering several river basins on the French–Spanish border identified only one parasite species: pleurocercoid cestodes belonging to the order Pseudophyllidea [52]. In areas much further south of our study area, a significantly higher number of parasites have been recorded in mosquitofish: eight species in Azerbaijan [53] and nine parasite species in Turkey [54]. In general, our data are consistent with the hypothesis that the species diversity of parasites in mosquitofish is comparatively low in more northern latitudes [52].
Importantly, the cestode S. acheilognathi has been found at the larval stage (plerocercoid), making it difficult to accurately identify the species of this parasite. Despite the large amount of data on the wide geographical distribution of S. acheilognathi and its wide range of hosts, experts note that only a small proportion of these records have been confirmed genetically, i.e., genotyping tapeworms from these hosts; it is therefore recommended that species identification be confirmed by sequencing the worms [38]. This is the molecular genetic approach that was implemented in the present study. According to information from the NCBI GenBank, the cestode S. acheilognathi we found is the first record of this species from the European part of Russia that has been reliably confirmed using a molecular genetic method.
Invasive fish species are known to affect syntopic native fish species through parasite transmission [55,56]. In Australia, the introduced mosquitofish G. holbrooki has become a major host for the invasive cestode S. acheilognathi [57]. Relatively high levels of fish infestation (20–40%, up to 65%) and intensity of infection (1–163 individuals per host individual) have been observed in some localities. In Turkey, G. holbrooki is also known as a host for this harmful parasite [49]. Taking into account that the northernmost finding of S. acheilognathi in the European part of Russia is located in the Rybinsk Reservoir (58°22′30″ N), which is significantly north of the northern limit of G. holbrooki distribution in this region [6,38], it can be argued that these two invader species (the fish and its parasite) may be syntopic within the entire potential range of mosquitofish in Russia. It is noteworthy that the parasitofauna of mosquitofish invasive populations has been studied only fragmentarily and is unknown in many areas of the invaded range. Regular monitoring of the parasitofauna of this and other particularly dangerous invasive fish species is therefore necessary for a comprehensive assessment of the impact on native ecosystems.

5. Conclusions

Our results confirm the involvement of an invasive fish species (G. holbrooki) on the Caucasian Black Sea coast in maintaining populations of S. acheilognathi, a parasite damaging to natural ecosystems and aquaculture, which causes intestinal damage to fish and mortality of juvenile carp and a number of other fish species. Thus, the existing practice of transferring mosquitofish between water bodies on the Black Sea coast of the Caucasus to control mosquito larvae may contribute to the undesirable spread of a harmful quarantine pest.

Author Contributions

Conceptualization, A.N.R. and A.B.P.; methodology, A.N.R., D.I.L. and A.B.P.; software, D.I.L.; validation, D.I.L. and A.N.R.; formal analysis, D.I.L.; investigation, A.N.R. and D.I.L.; resources, A.N.R., A.B.P. and D.I.L.; data curation, D.I.L.; writing—original draft preparation, A.N.R.; writing—review and editing, D.I.L. and A.B.P.; visualization, D.I.L. and A.B.P.; supervision, A.N.R.; project administration, A.N.R.; funding acquisition, A.N.R., A.B.P. and D.I.L. All authors have read and agreed to the published version of the manuscript.

Funding

The work of D.I. Lebedeva (parasitological autopsy, molecular and morphological analyses) was supported by Ministry of Science and Education of Russian Federation, grants number 122032100130-3. The work of A.B. Petrovskiy and A.N. Reshetnikov (invasion ecology and analysis of literature) was supported by Ministry of Science and Education of Russian Federation, grant number 1022040700480-0-1.6.15.

Institutional Review Board Statement

The animal study protocol was approved by the Ethics Committee of the Severtsov Institute of Ecology and Evolution, the Russian Academy of Sciences (protocol no. 11 from 8 July 2017, prolongations and additions from 14 May 2018, 23 April 2021, and 12 April 2022).

Data Availability Statement

Data are provided within the body of the article.

Acknowledgments

The authors are grateful to E. Kozhanova for assistance in the field as well as to I. Sukhovskaya and A. Kochneva for the kind help in the keeping and processing the fish studied.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Huffaker, C.B. Theory and Practice of Biological Control; Elsevier: Amsterdam, The Netherlands, 2012; 810p. [Google Scholar]
  2. Heimpel, G.E.; Mills, N.J. Biological Control: Ecology and Applications; Cambridge University Press: Cambridge, UK, 2017; 380p. [Google Scholar]
  3. Lodge, D.M. Biological invasions: Lessons for ecology. Trends Ecol. Evol. 1993, 8, 133–137. [Google Scholar] [CrossRef] [PubMed]
  4. Simberloff, D.; Martin, J.-L.; Genovesi, P.; Maris, V.; Wardle, D.A.; Aronson, J.; Courchamp, F.; Galil, B.; García-Berthou, E.; Pascal, M. Impacts of biological invasions: What’s what and the way forward. Trends Ecol. Evol. 2013, 28, 58–66. [Google Scholar] [CrossRef] [PubMed]
  5. Walton, W.E.; Henke, J.A.; Why, A.M. Gambusia affinis (Baird and Girard) and Gambusia holbrooki Girard (Mosquitofish). In A Handbook of Global Freshwater Invasive Species; Earthscan: London, UK, 2012; pp. 261–273. [Google Scholar]
  6. Reshetnikov, A.N.; Zibrova, M.G.; Dgebuadze, Y.Y. Gambusia holbrooki (Girard, 1859). In The Most Dangerous Invasive Species of Russia (TOP-100); Dgebuadze, Y.Y., Petrosyan, V.G., Khlyap, L.A., Eds.; KMK: Moscow, Russia, 2018; pp. 538–545. [Google Scholar]
  7. Reznik, P.A. About introduction of mosquitofish on Northern Causasus (Voroshilovsk town). Priroda 1938, 5, 97–99. [Google Scholar]
  8. Miura, T.; Takahashi, R.M.; Wilder, W.H. Impact of the mosquitofish (Gambusia affinis) on a rice field ecosystem when used as a mosquito control agent. Mosq. News 1984, 44, 510–517. [Google Scholar]
  9. White, A.; Pyke, G. World War II and the rise of the plague minnow Gambusia holbrooki (Girard, 1859) in Australia. Aust. Zool. 2011, 35, 1024–1032. [Google Scholar] [CrossRef]
  10. Tuniyev, B.S.; Shagarov, L.M.; Arribas, O.J. Podarcis siculus (Reptilia: Sauria: Lacertidae), a new alien species for Russian fauna. Proc. Zool. Inst. Russ. Acad. Sci. 2020, 324, 364–370. [Google Scholar] [CrossRef]
  11. Karabanov, D.P.; Kodukhova, Y.V.; Pashkov, A.N.; Reshetnikov, A.N.; Makhrov, A.A. “Journey to the West”: Three phylogenetic lineages contributed to the invasion of Stone Moroko, Pseudorasbora parva (Actinopterygii: Cyprinidae). Russ. J. Biol. Invasions 2021, 12, 67–78. [Google Scholar] [CrossRef]
  12. Makhrov, A.A.; Artamonova, V.S.; Sun, Y.-H.; Fang, Y.; Pashkov, A.N.; Reshetnikov, A.N. New Records of the Alien Chinese Ricefish (Oryzias sinensis) and Its Dispersal History across Eurasia. Diversity 2023, 15, 317. [Google Scholar] [CrossRef]
  13. Reshetnikov, A.N.; Zibrova, M.G.; Ayaz, D.; Bhattarai, S.; Borodin, O.V.; Borzée, A.; Brejcha, J.; Çiçek, K.; Dimaki, M.; Doronin, I.V.; et al. Rarely naturalized, but widespread and even invasive: The paradox of a popular pet terrapin expansion in Eurasia. NeoBiota 2023, 81, 91–127. [Google Scholar] [CrossRef]
  14. Zabaluev, I.A.; Bieńkowski, A.O.; Orlova-Bienkowskaja, M.J. First record of potential cabbage pest Aulacobaris cuprirostris (Coleoptera, Curculionidae) in Russia. Russ. J. Biol. Invasions 2020, 11, 314–317. [Google Scholar] [CrossRef]
  15. Fedorova, M.V.; Shvez, O.G.; Patraman, I.V.; Medyanik, I.M.; Otstavnova, A.D.; Lenshin, S.V.; Vyshemirskij, O.I. Invasive mosquito species of the Black sea coast of the Caucasus: Current ranges. Med. Parasitol. Parasit. Dis. 2019, 1, 47–55. [Google Scholar]
  16. Krivosheina, M.G.; Khlyap, L.A. Cydalima perspectalis (Walker, 1859). In The Most Dangerous Invasive Species of Russia (TOP-100); Dgebuadze, Y.Y., Petrosyan, V.G., Khlyap, L.A., Eds.; KMK: Moscow, Russia, 2018; pp. 472–477. [Google Scholar]
  17. Cabrera, M.B.; Bogan, S.; Posadas, P.; Somoza, G.M.; Montoya-Burgos, J.I.; Cardoso, Y.P. Risks associated with introduction of poeciliids for control of mosquito larvae: First record of the non-native Gambusia holbrooki in Argentina. J. Fish Biol. 2017, 91, 704–710. [Google Scholar] [CrossRef] [PubMed]
  18. Veenvliet, P. Species identity of Gambusia (Pisces: Poeciliidae) introduced to Slovenia. Nat. Slov. 2007, 9, 43–46. [Google Scholar] [CrossRef]
  19. Bykhovskaya-Pavlovskaya, I.E. Fish Parasites. Study Guide; Nauka: Leningrad, Russia, 1985; 121p. [Google Scholar]
  20. Moravec, F. Parasitic Nematodes of Freshwater Fishes of Europe; Springer: Berlin/Heidelberg, Germany, 1994; 470p. [Google Scholar]
  21. Vismanis, K.O.; Lomakin, V.V.; Roitman, V.A.; Semenova, M.K.; Trofimenko, V.Y. Nemathehelminthes. In Key to the Parasites of Freshwater Fishes of the Fauna of the USSR. Part 2; Bauer, O.N., Ed.; Nauka: Leningrad, Russia, 1987. [Google Scholar]
  22. Protasova, E.N. Botryocephalates-Tapeworm Helminths of Fishes; Fundamentals of Cestodology; Nauka: Leningrad, Russia, 1977; Volume 8, 290p. [Google Scholar]
  23. World Register of Marine Species: WoRMS. Available online: https://www.marinespecies.org (accessed on 1 July 2024).
  24. Bush, A.O.; Lafferty, K.D.; Lotz, J.M.; Shostak, A.W. Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 1997, 83, 575–583. [Google Scholar] [CrossRef]
  25. Joyce, S.A.; Reid, A.P.; Driver, F.; Curran, J. Application of polymerase chain reaction (PCR) methods to the identification of entomopathogenic nematodes. In Proceedings of the Symposium & Workshop, St. Patrick’s College, Maynooth, County Kildare, Ireland; Burnell, A.M., Ehlers, R.-U., Masson, J.P., Eds.; European Commission: Luxembourg, 1994; pp. 178–187. [Google Scholar]
  26. Scholz, T.; Hanzelová, V.; Škeříková, A.; Shimazu, T.; Rolbiecki, L. An annotated list of species of the Proteocephalus Weinland, 1858 aggregate sensu de Chambrier et al. (2004) (Cestoda: Proteocephalidea), parasites of fishes in the Palaearctic Region, their phylogenetic relationships and a key to their identification. Syst. Parasitol. 2007, 67, 139–156. [Google Scholar] [CrossRef]
  27. Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef]
  28. Rambaut, A. FigTree v1.4. Molecular Evolution, Phylogenetics and Epidemiology. Available online: https://github.com/rambaut/figtree/releases (accessed on 1 July 2024).
  29. Leis, E.; Easy, R.; Cone, D. Report of the potential fish pathogen Pseudocapillaria (Pseudocapillaria) tomentosa (Dujardin, 1843) (Nematoda) from red Shiner (Cyprinella lutrensis) shipped from Missouri to Wisconsin. Comp. Parasitol. 2016, 83, 275–278. [Google Scholar] [CrossRef]
  30. Brabec, J.; Kuchta, R.; Scholz, T.; Littlewood, D.T.J. Paralogues of nuclear ribosomal genes conceal phylogenetic signals within the invasive Asian fish tapeworm lineage: Evidence from next generation sequencing data. Int. J. Parasitol. 2016, 46, 555–562. [Google Scholar] [CrossRef] [PubMed]
  31. Yera, H.; Kuchta, R.; Brabec, J.; Peyron, F.; Dupouy-Camet, J. First identification of eggs of the Asian fish tapeworm Bothriocephalus acheilognathi (Cestoda: Bothriocephalidea) in human stool. Parasitol. Int. 2013, 62, 268–271. [Google Scholar] [CrossRef]
  32. Mejía-Madrid, H.H.; Domínguez-Domínguez, O.; de León, G.P.-P. Adult endohelminth parasites of Goodeinae (Cyprinodontiformes: Goodeidae) from Mexico with biogeographical considerations. Comp. Parasitol. 2005, 72, 200–211. [Google Scholar] [CrossRef]
  33. Gaevskaya, A.V. Parasites and Diseases of Fishes of Black and Azov Seas V.2; EKOSI-Gidrofizika: Sevastopol, Ukraine, 2013; 354p. [Google Scholar]
  34. Reshetnikov, S.I.; Pashkov, A.N. Ecosystems of Small Rivers of Black Sea Coast of North-West Caucasus; Biotekh-Youg: Krasnodar, Russia, 2009; 152p. [Google Scholar]
  35. Chunchukova, M.; Kuzmanova, D.; Kirin, D. Biodiversity of the helminth communities of Carassius gibelio (Bloch, 1782) from Maritsa river, Bulgaria. Sci. Papers Ser. D Anim. Sci. 2023, 66, 532–537. [Google Scholar]
  36. Moravec, F.; Konečný, R.; Baska, F.; Rydlo, M.; Scholz, T.; Molnár, K.; Schiemer, F. Endohelminth Fauna of Barbel, Barbus Barbus (L.), Under Ecological Conditions of the Danube Basin in Central Europe; Academia: Praha, Czech Republic, 1997; 98p. [Google Scholar]
  37. Choudhury, A.; Cole, R. Bothriocephalus acheilognathi Yamaguti (Asian tapeworm). In A Handbook of Global Freshwater Invasive Species; Francis, R.A., Ed.; Earthscan: London, UK, 2012; pp. 385–400. [Google Scholar]
  38. Kuchta, R.; Choudhury, A.; Scholz, T. Asian fish tapeworm: The most successful invasive parasite in freshwaters. Trends Parasitol. 2018, 34, 511–523. [Google Scholar] [CrossRef] [PubMed]
  39. Salgado-Maldonado, G.; Pineda-López, R.F. The Asian fish tapeworm Bothriocephalus acheilognathi: A potential threat to native freshwater fish species in Mexico. Biol. Invasions 2003, 5, 261–268. [Google Scholar] [CrossRef]
  40. Kline, J.; Archdeacon, T.; Iles, A.C.; Bonar, S.A. Factors influencing distribution of introduced Asian tapeworm and effects on selected southwestern fishes (Yaqui topminnow and Yaqui chub). In Heritage Program, Arizona Game and Fish Department, Phoenix; USGS: Yuma, AZ, USA, 2007; 55p. [Google Scholar]
  41. Andreev, M.E.; Voronova, A.N.; Vainutis, K.S. Features of the parasite fauna of the Luchegorsk reservoir in the autumn period. In Proceedings of the All-Russian Scientific Conference with International Participation, Dedicated to the 300th Anniversary of the Russian Academy of Sciences, 55th Anniversary of the Institute of Water and Ecology Problems, FEB RAS, and 60th Anniversary of Nature Reserves in Priamurye, Khabarovsk, Russia, 3–6 October 2023; IWEP FEB RAS: Khabarovsk, Russia, 2023. [Google Scholar]
  42. Chaudhary, A.; Chiary, H.R.; Sharma, B.; Singh, H.S. First molecular identification of invasive tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda: Bothriocephalidea) in India. Bioinvasions Rec. 2015, 4, 269–276. [Google Scholar] [CrossRef]
  43. Hansen, H.; Alarcon, M. First record of the Asian fish tapeworm Schyzocotyle (Bothriocephalus) acheilognathi (Yamaguti, 1934) in Scandinavia. Bioinvasions Rec. 2019, 9, 437–441. [Google Scholar] [CrossRef]
  44. Bychkova, E.I.; Yakovich, M.M.; Degtyarik, S.M. Alien species of fish helminths of Belarus. Russ. J. Biol. Invasions 2022, 13, 15–21. [Google Scholar] [CrossRef]
  45. Dove, A.D.M.; Fletcher, A.S. The distribution of the introduced tapeworm Bothriocephalus acheilognathi in Australian freshwater fishes. J. Helminthol. 2000, 74, 121–127. [Google Scholar] [CrossRef] [PubMed]
  46. Hovhannisyan, R.L.; Rukhkyan, M.Y.; Harutyunova, L.D.; Magomedova, M.Z.; Magomedova, P.D. The fish helminth fauna of Lake Sevan during a period of water level change. South Russ. Ecol. Dev. 2023, 18, 50–59. [Google Scholar] [CrossRef]
  47. Pofuk, M. Non-Indigenous parasites of fish in inland waters of Croatia. Croat. J. Fish. 2021, 79, 187–204. [Google Scholar] [CrossRef]
  48. Riggs, M.R.; Esch, G.W. The suprapopulation dynamics of Bothriocephalus acheilognathi in a North Carolina reservoir: Abundance, dispersion, and prevalence. J. Parasitol. 1987, 73, 877–892. [Google Scholar] [CrossRef]
  49. Öztürk, T.; Özer, A. Comparative invasive Asian tapeworm Bothriocephalus acheilognathi infections on the Lower Kizilirmak delta fishes. J. Acad. Doc. Fish. Aquac. 2014, 1, 1–7. [Google Scholar]
  50. Prigli, M. The role of aquatic birds in spreading Bothriocephalus gowkongensis Yeh, 1955 (Cestoda). Parasitol. Hung. 1975, 8, 61–62. [Google Scholar]
  51. Maceda-Veiga, A.; Cano-Rocabayera, O.; de Sostoa, A.; Cable, J. Low parasite prevalence in the invasive fish Gambusia holbroki in riverine and stagnant waters in north-eastern Spain. Bull. Eur. Assoc. Fish Pathol. 2019, 39, 70–76. [Google Scholar]
  52. Benejam, L.; Alcaraz, C.; Sasal, P.; Simon-Levert, G.; García-Berthou, E. Life history and parasites of the invasive mosquitofish (Gambusia holbrooki) along a latitudinal gradient. Biol. Invasions 2009, 11, 2265–2277. [Google Scholar] [CrossRef]
  53. Suleymanova, A.V. Parasites and main parasitoses of fishes of Absheron fish farm in Azerbaijan. In Biodiversity and Ecology of Parasites of Terrestrial and AQUATIC cenoses. Proceedings of the International Conference Dedicated to the 130th Anniversary of Academician K.I. Skryabin, Moscow, Russia, December 9–11; Movsesyan, S.O., Beer, S.A., Zinovieva, S.V., Pelgunov, A.N., Spiridonov, S.E., Eds.; IPEE RAS: Moscow, Russia, 2008. [Google Scholar]
  54. Özer, A.; Çankaya, E.; Öztürk, T. Assessment of endemic tooth-carp (Aphanius danfordii) and invasive mosquitofish (Gambusia holbrooki) health by means of relative condition factor under the coinfection of different parasite groups and revelation of the effects on their competitive interactions. In Proceedings of the International Conference on Parasitology, Philadelphia, PA, USA, 24–26 August 2015; OMICS International Conferences: Philadelphia, PA, USA, 2015. [Google Scholar]
  55. Sokolov, S.G.; Protasova, E.N.; Reshetnikov, A.N.; Voropaeva, E.L. Interactions of the introduced rotan Perccottus glenii Dybowski, 1877 (Osteichthyes, Odontobutidae) with aboriginal fish species: The parasitological aspect. Biol. Bull. 2012, 39, 829–833. [Google Scholar] [CrossRef]
  56. Gaither, M.R.; Aeby, G.; Vignon, M.; Meguro, Y.-I.; Rigby, M.; Runyon, C.; Toonen, R.J.; Wood, C.L.; Bowen, B.W. An invasive fish and the time-lagged spread of its parasite across the Hawaiian archipelago. PLoS ONE 2013, 8, e56940. [Google Scholar] [CrossRef]
  57. Palermo, C.J.; Morgan, D.L.; Beatty, S.J.; Elliot, A.; Greay, T.L. The Asian fish tapeworm (Schyzocotyle acheilognathi) discovered in Western Australia may pose a threat to the health of endemic native fishes. J. Helminthol. 2021, 95, e60. [Google Scholar] [CrossRef]
Parasitologia 04 00031 g001
Figure 1. Study area at the Black Sea coast of the Caucasus. The studied water bodies are shown by black circles. The numbers of water bodies correspond to numbers in Table 1.
Figure 1. Study area at the Black Sea coast of the Caucasus. The studied water bodies are shown by black circles. The numbers of water bodies correspond to numbers in Table 1.
Parasitologia 04 00031 g001
Parasitologia 04 00031 g002
Figure 2. Maximum likelihood (ML) analyses tree for Nematoda gen. spp. based on the alignment of 18SrRNA, ITS1-5.8S-ITS2 sequences. Only significant values of the nodal supports (≥60) are indicated. The scale bar indicates the expected number of substitutions per site. The newly generated sequences are highlighted by asterisks.
Figure 2. Maximum likelihood (ML) analyses tree for Nematoda gen. spp. based on the alignment of 18SrRNA, ITS1-5.8S-ITS2 sequences. Only significant values of the nodal supports (≥60) are indicated. The scale bar indicates the expected number of substitutions per site. The newly generated sequences are highlighted by asterisks.
Parasitologia 04 00031 g002
Parasitologia 04 00031 g003
Figure 3. Plerocercoid Schyzocotyle acheilognathi from intestine of the fish Gambusia holbrooki. Acetic acid carmine staining.
Figure 3. Plerocercoid Schyzocotyle acheilognathi from intestine of the fish Gambusia holbrooki. Acetic acid carmine staining.
Parasitologia 04 00031 g003
Parasitologia 04 00031 g004
Figure 4. Maximum likelihood (ML) analyses tree for Cestoda gen. spp. based on the alignment of 18SrRNA sequences. Only significant values of the nodal supports (≥50) are indicated. The scale bar indicates the expected number of substitutions per site. The newly generated sequences are highlighted by asterisks.
Figure 4. Maximum likelihood (ML) analyses tree for Cestoda gen. spp. based on the alignment of 18SrRNA sequences. Only significant values of the nodal supports (≥50) are indicated. The scale bar indicates the expected number of substitutions per site. The newly generated sequences are highlighted by asterisks.
Parasitologia 04 00031 g004
Table 1. Characteristics of the studied samples of mosquitofish Gambusia holbrooki from four water bodies of the Black Sea coast of the Caucasus. The numbers of the water bodies correspond to the numbers in Figure 1. The quantities of fish individuals (n), sex ratio (females/males), and fish total length (TL ± standard error, range, mm) are presented.
Table 1. Characteristics of the studied samples of mosquitofish Gambusia holbrooki from four water bodies of the Black Sea coast of the Caucasus. The numbers of the water bodies correspond to the numbers in Figure 1. The quantities of fish individuals (n), sex ratio (females/males), and fish total length (TL ± standard error, range, mm) are presented.
Water Bodyn (Females/Males), ind.TL (Range), mm
SpringAutumnSpringAutumn
124 (20/4)70 (47/23)26 ± 0 (21–31)24 ± 0 (20–30)
229 (23/6)15 (10/5)34 ± 1 (26–46)30 ± 1 (20–35)
330 (22/8)15 (9/6)31 ± 1 (23–48)30 ± 2 (20–45)
4-15 (9/6)-30 ± 1 (25–40)
Total8311521–4820–45
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Lebedeva, D.I.; Petrovskiy, A.B.; Reshetnikov, A.N. Potential Role of the Eastern Mosquitofish (Gambusia holbrooki) in the Spread of the Harmful Fish Parasite, Asian Tapeworm Schyzocotyle (Bothriocephalus) acheilognathi. Parasitologia 2024, 4, 358-368. https://doi.org/10.3390/parasitologia4040031

AMA Style

Lebedeva DI, Petrovskiy AB, Reshetnikov AN. Potential Role of the Eastern Mosquitofish (Gambusia holbrooki) in the Spread of the Harmful Fish Parasite, Asian Tapeworm Schyzocotyle (Bothriocephalus) acheilognathi. Parasitologia. 2024; 4(4):358-368. https://doi.org/10.3390/parasitologia4040031

Chicago/Turabian Style

Lebedeva, Daria I., Andrey B. Petrovskiy, and Andrey N. Reshetnikov. 2024. "Potential Role of the Eastern Mosquitofish (Gambusia holbrooki) in the Spread of the Harmful Fish Parasite, Asian Tapeworm Schyzocotyle (Bothriocephalus) acheilognathi" Parasitologia 4, no. 4: 358-368. https://doi.org/10.3390/parasitologia4040031

APA Style

Lebedeva, D. I., Petrovskiy, A. B., & Reshetnikov, A. N. (2024). Potential Role of the Eastern Mosquitofish (Gambusia holbrooki) in the Spread of the Harmful Fish Parasite, Asian Tapeworm Schyzocotyle (Bothriocephalus) acheilognathi. Parasitologia, 4(4), 358-368. https://doi.org/10.3390/parasitologia4040031

Article Metrics

Back to TopTop