Checklist of the parasites of European eel Anguilla anguilla (Linnaeus, 1758) (Anguillidae) in Poland

Abstract The present paper lists all parasite species of the European eel Anguilla anguilla (Linnaeus, 1758), recorded in Poland, in both its saltwater and freshwater habitats. The list has been drawn up, based on data acquired since 1844. The majority of included parasite species are presented with fish infection parameters together with data on their developmental stages and occupied microhabitats, localities and dates of collection of the eels themselves. The database includes 62 parasite taxa (including 50 species, nine identified to the genus level and three to higher taxa), representing at least 47 genera and 39 families. The most frequently-noted parasites of the European eel are the cestode Bothriocephalus claviceps, the nematodes Anguillicoloides crassus, Camallanus lacustris and Raphidascaris acus and the acanthocephalan Acanthocephalus lucii. Four alien species have been noted from this host: A. crassus, the monogeneans Pseudodactylogyrus anguillae and Pseudodactylogyrus bini and the acanthocephalan Paratenuisentis ambiguus. The present list includes both new host records and earlier records not included in previous lists of parasites of eels.


Introduction
The European eel Anguilla anguilla (Linnaeus, 1758) is a species of fish with a wide distribution in European waters and one with both very high environmental and economic value. Therefore, there is a pressing need to understand the real and potential treats for eel populations, including such death hazards as parasitoses and their secondary consequences. Since the end of the 20th Century, eel populations have decreased by over 99% due to various factors, such as increased water pollution, climate change, overfishing and dam construction and the species is at risk of extinction. It is currently subject to protection by various forms of conservation, including the Washington Convention (CITES) and is listed as critically endangered by the IUCN Red List of Threatened Species (Dekker 2003, Stone 2003, Freyhof and Kottelat 2010. One significant factor in this decline was the appearance of the nematode Anguillicoloides crassus: an alien, invasive parasite which inhabits the swim bladders of eels, resulting in sickness and the disturbance of various vital functions that may prevent the eels from reaching their spawning area and reproducing (Moriarty and Dekker 1997, Lefebvre et al. 2002, Dekker 2003, Kirk 2003, Stone 2003, van Ginneken and Maes 2005. Anguillicoloides crassus was probably introduced from Taiwan, where it was associated with its specific host, the Japanese eel; since its introduction, it has spread rapidly throughout the European eel population (Taraschewski et al. 1987, Moravec 1992, Molnár et al. 1993, Münderle et al. 2006.
A comprehensive analysis of the European eel parasite fauna is complicated by its wide geographical distribution and by the poor understanding of the complex biology of the eel. It is therefore often difficult to draw firm conclusions on the infection routes with parasites or participation of the eel in their life cycles. Eel leptocephalus larvae migrate across the Atlantic Ocean to the coasts of Europe; then they metamorphose into glass eel (montée) and move to rivers and lakes, where they mature. Finally, they take part in catadromous migration to the spawning area in the Sargasso Sea (van Ginneken and Maes 2005). Thus, they inhabit different environmental conditions at different stages of ontogenesis; in addition, during the course of their migrations, they may accumulate parasites originating from different areas and further disseminate them. Parasite accumulation is also supported by their longevity and predatory lifestyle, the oldest known specimen in the wild being 85 years old (Dekker et al. 1998). The eel may constitute a significant link in the life cycles of parasites and their distribution in the environment; however, some differences may be attributed to local factors. Therefore, there is a clear need to better understand the parasite fauna of European eels, its species composition, structural changes and infection level, both on the global and regional scales. Constant parasitological monitoring in all distribution areas would provide a clearer picture of the formation of parasite assemblages across the different parts of the distribution of the eel; it would also allow observation of changes in the parasite ranges and hence, any associated threats. However, being rather local in nature, data on the eel parasite fauna are scattered across a range of publications and reports; in addition, collective analyses are often further complicated by variations in sources or language barrier. Thus far, three checklists of eel parasites have been published concerning various species of Anguilla: two of them are from Japan, the second being a revised and updated checklist, while the other concerns the parasites found in A. anguilla in Europe and North Africa (Nagasawa et al. 2007, Jakob et al. 2016, Nagasawa and Hirotaka 2017. Out of necessity, the latter list is restricted to available sources from selected countries. Its aim was to provide an overview of the parasite fauna acting as the reference point to future analyses of trends in changes in biodiversity. However, this work did not provide a full picture of the data from Poland, as it included only seven original studies; in contrast, the present checklist includes 59.
Therefore, the objective of this study was to provide a complete, verified list of parasitic Protista and Metazoa found, thus far, in the European eel in Poland.

Material and methods
The checklist has been drawn up primarily on the basis of published data (55 items) from the area of Poland, including data from the period 1844-2016. It also includes our own unpublished data, marked in the table as "this study", together with examples of data from conference abstracts regarding the occurrence of A. crassus or the presence of new records from Poland.
For the majority of species, additional data have been provided if included in the source publications: infection parameters such as prevalence (P), mean intensity, intensity range and abundance, as well as the developmental stages of the parasites and their microhabitats. The infection parameters were calculated, based on data included in original studies by means of unification, where possible. Information on dates of fish collection, as well as the geographical location (with GPS coordinates in the Suppl. material 1), have been also included.

Results and Discussion
A total of 62 taxa have been recorded from the European eel in Poland, of which 11 are Protista (eight species and three identified at the genus level), including five Ciliophora (one identified at the genus level as Apiosoma) and two Apicomplexa. Of the 51 representatives of Metazoa (42 identified as species, six to genus level, three to higher taxa), six were Myxozoa, nine Trematoda, five Monogenea (one identified at the genus level -Dactylogyrus and one as Monogenea), five Cestoda (one identified as Cestoda gen. sp. Pseudophyllidearum larvae), ten Nematoda, eight Acanthocephala, two Annelida, three Arthropoda, one Mollusca (identified as Unionidae). In addition to the species mentioned in Table 1, further data on the occurrence of Acanthocephalus clavula and Corynosoma semerme in the European eel were given in overview studies on the parasites of the Polish ichthyofauna (Pojmańska et al. 2007, Popiołek 2016); however, this information was not included in the analysed original studies. Checklist of the protozoan and metazoan parasites of Anguilla anguilla from Poland. The parameters have been provided with accuracy of original data; if the parameter was not given in the original work, it was marked with a dash (-). Parasite life stage: A -adults, e -eggs, F -female, Llarvae, M -male, met -metacercariae, pA -preadults, pl -plasmodia. Microhabitat: sb -swim bladder, ub -urinary bladder. Intensity: (+) -single to not numerous, (++) -rather numerous to numerous, (+++) -very numerous, (++++) -mass occurrence. blood, liver, spleen, kidney, skin, necrotic muscles; single to numerous in spleen, single to very numerous in blood, liver, kidney; very numerous in skin; parameter was calculated on the basis of data from publication; parasite number in smear area 20 x 25 mm; blood, kidney, liver, urinary bladder, gills; rare or sporadic; gills, kidney, intestine, urinary bladder, liver, gall bladder, spleen, skin; fins, gills, urinary bladder, kidney, liver, intestine; calculated from less than ten individuals; questionable microhabitat; unspecified, the authors provided a value for several reservoirs; together Szczecin Lagoon, Vistula Lagoon, Goczałkowicki Reservoir, Lake Charzykowskie, Lake Niegocin, Lake Mamry.
For comparison, the list of European eel parasites (data until 2009) from 30 countries in Europe and North Africa specifies 161 parasitic taxa (129 identified to species), of which 146 were metazoans and 15 were Protista (Jakob et al. 2016): Epieimeria anguillae and Eimeria anguillae, which were listed as two distinct species, are now considered to be the same taxon in the genus Eimeria, according to Benajiba et al. (1994). Similarly to the Polish study, digenetic trematodes (39 species) and nematodes (38 species) formed the most species-rich groups.
Twenty six parasite species, included in the present list, are also present in Jakob et al. (2016). However, that list does not include many parasite species and localities from Poland and does not reflect the actual distribution of the parasites. For example, Poland was not given as the area of occurrence for 23 parasite species ( Jakob et al. (2016). In addition, a number of groups and species, included in the present list, were absent from Jakob et al. (2016). For instance, the group of protists from Poland has now been expanded to include Capriniana piscium and Ortholinea sphaerocapsularae and a representative of Apiosoma without species identification. Rhabdospora thelohani is also mentioned; however, considerable controversy exists as to whether this species is indeed a representative of apicomplexan parasites or a host "rodlet cell" (Davies and Ball 1993). In addition, amongst the Metazoa, the new list has been enriched with the addition of Henneguya psorospermica, Cystidicola farionis and an unidentified Dactylogyrus species for Poland, as well as unidentified cestodes found by Sołtyńska (1964). The present list includes a number of new localities for eel parasites, previously unpublished (marked in Table 1 as "this study") In comparison, only nine species of parasites were recorded for European eels in Japan, as well as seven taxa identified at genus level and an unidentified Monogenea. However, these eels also included parasites, thus far unknown from the European A. anguilla (Cryptobia spp., Ichthyobodo spp., Gyrodactylus anguillae, Lernaea cyprinacea) (Nagasawa et al. 2007, Nagasawa andHirotaka 2017). This confirms the possibility that regional differences may exist, not only with regard to the level of infection, but also in the composition and species diversity of the parasite fauna.
Within the parasitofauna of eel, the greatest repeatability between different distribution areas is exhibited by the parasites specific to the genus Anguilla (e.g. the nematode A. crassus, the cestodes Bothriocephalus claviceps and Proteocephalus macrocephalus or the trematode Deropristis inflata), but also certain widely-distributed species with large ranges of hosts, such as the trematode Diplostomum spathaceum s. l., the leech Piscicola geometra or the copepod Ergasilus sieboldi. It is in this area that the number of records of alien and invasive parasites increases for the European eel; for example, A. crassus, which was introduced to Europe in 1982 and recorded in Poland in 1988(Koops and Hartmann 1989, Własow 1991, Bystydzieńska et al. 2005 or Pseudodactylogyrus anguilla and P. bini, recorded in Poland in 1995 by Dzika et al. (1995). It is also important to note the presence of a new, potentially invasive species, the acanthocephalan Paratenuisentis ambiguus, originally a parasite of Anguilla rostrata (Lesueur, 1817), which was first recorded in a European eel from Europe in 1980 and later in Poland by Morozińska-Gogol (2008).
The dispersal of parasites, their increased prevalence and level of infection are linked not only to the life history of eels and their migrations. Parasite infection in local eel populations can also transmitted through stocking material. For instance, protozoan Trichodina fultoni (100% infection) was found in rearing glass eel imported to Poland from France in 1971 (Markiewicz and Migała 1980). In addition, the monogenean P. anguillae and the nematode A. crassus were found in eels originating from the stocking material for the Vistula Lagoon in 2006 . What is more, of the eels originating from farming facilities located in the Warmian-Masurian Voivodeship (northeast Poland) and studied in the period 2010-2014, 77.2% were found to have Pseudodactylogyrus spp.; Trichodina spp. and I. multifiliis were typical parasites at the early rearing stage (Terech-Majewska et al. 2016).
With their resources already being considerably depleted and the growing number threats to eel populations, there has been a growing interest in their parasitic fauna; this growth has been accompanied by a greater need to carry out regular monitoring of parasitological threats, especially actual or potentially pathogenic species, including alien and invasive species. However, such data have to be constantly supplemented and verified with new records of parasites in different parts of distribution of this host. As such research would be complicated by the degree of data scatter, the best solution would be to create a webbased database, supplemented and coordinated by scientific centres from different countries.