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Research Article
Checklist of the parasites of European eel Anguilla anguilla (Linnaeus, 1758) (Anguillidae) in Poland
expand article infoJoanna Dzido, Leszek Rolbiecki, Joanna N. Izdebska, Rafał Bednarek
‡ Department of Invertebrate Zoology and Parasitology, Faculty of Biology, University of Gdańsk, Wita Stwosza 59, Gdańsk, Poland
Open Access

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.

Keywords

biodiversity, eel, fish, parasite, species distribution

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.

The species were arranged in taxonomic and then alphabetical order. The Protista taxonomy follows Lom and Dyková (1992); for Trematoda, Gibson et al. (2002) and Jones et al. (2005); for Nematoda, Moravec (2013) and Nadler et al. (2005); for Cestoda, Kahlil et al. (1994); for Acanthocephala, Amin (2013); the taxonomy for Myxozoa, Monogenea, Arthropoda, Annelida and Mollusca follows the WORMS database (WoRMS Editorial Board 2020). As some taxa have been subject to revision over the years, valid and verified species names were used in the list. For instance, Szidat (1944) considered Sphaerostomum bramae (Müller, 1776), a trematode from the study of Markowski (1933) as Plagioporus angulatus. Furthermore, Spironucleus mobilis Wierzbicka & Einszporn-Orecka, 1986 is currently a synonym of Spironucleus anguillae (Lom and Dyková 1992), Trichophrya piscium Buetschli, 1889 is Capriniana piscium (Svobodová et al. 2009), Sphaerospora sphaerocapsularae Wierzbicka 1986 is now Ortholinea sphaerocapsularae (Sitjà-Bobadilla and Alvarez-Pellitero 1994), Sphaerospora anguillae Wierzbicka, 1986 is a synonym of S. gilsoni (Wierzbicka 1994), Ascaris labiata Rudolphi, 1809 is Raphidascaris acus, Anguillicola crassus Kuwahara, Niimi & Itagaki, 1974 is currently known as Anguillicoloides crassus (Moravec 2006) and Contracaecum aduncum (Rudolphi, 1802) is Hysterothylacium aduncum. Bielecki et al. (2011) believe that Cystobranchus respirans (Troschel, 1850) is Piscicola respirans. In addition, it is known that "Diplostomum spathaceum" includes more than one species; there are several species of Diplostomum difficult to identify without using molecular methods (Niewiadomska 2003, Georgieva et al. 2013). Likewise, there is a possibility of wrong species identifitaciton in the case of Pomphorhynchus laevis, due to morphological similarity to P. tereticollis which occurs sympatrically (Špakulová et al. 2011, Hohenadler et al. 2018).

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, L – larvae, 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.

Parasite

life

stage

Micro

habitat

P

[%]

Intensity

range

(mean)

Abun

dance

Locality

Material collection year

References

METAMONADA

Family Hexamitidae

Spironucleus anguillae Einszporn-Orecka, 1979

-

1

-

2

-

Szczecin Lagoon

1974

Einszporn-Orecka 1979

-

intestine

1.9 3

(+)-(++)

-

Szczecin Lagoon

1982-83

Wierzbicka and Einszporn-Orecka 1986, Wierzbicka and Orecka-Grabda 1994

-

intestine

4.2

(++)

-

Oder mouth

1982-83

Wierzbicka and Einszporn-Orecka 1986, Wierzbicka and Orecka-Grabda 1994

EUGLENOZOA

Family Trypanosomatidae

Trypanosoma granulosum Laveran & Mesnil, 1909

trypomastigote

blood

24

(0.2-16.0) 4

-

Lake Siecino

1970-73

Orecka-Grabda and Wierzbicka 1996

trypomastigote

blood

68

(2.2-16.2) 4

-

Lake Dąbie

1970-73

Orecka-Grabda and Wierzbicka 1996

-

blood

-

-

-

Szczecin Lagoon, Lake Dąbie

1970-73

Orecka-Grabda 1986

-

5

46.9 3

(+)-(++)

-

Szczecin Lagoon

1982-83

Wierzbicka and Orecka-Grabda 1994

-

5

95.8

(+)-(++)

-

Oder mouth

1982-83

Wierzbicka and Orecka-Grabda 1994

-

-

50-60

-

-

Lake Śniardwy

1989

Własow et al. 1991

-

-

50

-

-

Lake Mamry

1990

Własow et al. 1991

-

blood

100

variable

-

River Rega

2001-02

Rząd et al. 2007

Trypanosoma sp.

-

blood

24

-

-

Lake Ińsko

1993

Rząd and Pilecka-Rapacz 2002

CILIOPHORA

Family Epistylididae

Apiosoma sp.

-

-

6

-

-

Lake Dąbrowa Wielka

1990-91

Własow et al. 1991

Family Ichthyophthiriidae

Ichthyophthirius multifiliis (Fouquet, 1876)

-

gills, skin

-

-

-

River Darłówka

-

Grabda 1971

-

gills

3.1 3

(+)

-

Szczecin Lagoon

1982-83

Wierzbicka and Orecka-Grabda 1994

Family Trichodinidae

Trichodina jadranica Raabe, 1958

-

gills

68.6 3

(+)-(++++)

-

Szczecin Lagoon

1982-83

Wierzbicka and Orecka-Grabda 1994

-

gills

66.7

(+)

-

Oder mouth

1982-83

Wierzbicka and Orecka-Grabda 1994

Trichodina sp.

-

-

30

-

-

Lake Niegocin

1989

Własow et al. 1991

-

-

8

-

-

Lake Mamry

1990

Własow et al. 1991

-

-

6

-

-

Lake Dąbrowa Wielka

1990-91

Własow et al. 1991

Trichodinella epizootica (Raabe, 1950)

-

gills

62.9 3

(+)-(+++)

-

Szczecin Lagoon

1982-83

Wierzbicka and Orecka-Grabda 1994

-

gills

41.7

(+)-(+++)

-

Oder mouth

1982-83

Wierzbicka and Orecka-Grabda 1994

-

-

3.3

1-4 (2.5)

-

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

Family Trichophryidae

Capriniana piscium (Bütschli, 1889)

-

gills

4.2

(+++)

-

Oder mouth

1982-83

Wierzbicka and Orecka-Grabda 1994

APICOMPLEXA

Family Eimeriidae

Eimeria anguillae Léger & Hollande, 1922

oocyst

intestine

11.9 3

(+)-(++++)

-

Szczecin Lagoon

1982-83

Wierzbicka and Orecka-Grabda 1994

oocyst

intestine

20.8

(+)-(+++)

-

Oder mouth

1982-83

Wierzbicka and Orecka-Grabda 1994

Family uncertain

Rhabdospora thelohani Laguessé, 1895

-

-

20

-

-

Lake Niegocin

1989

Własow et al. 1991

-

-

50-60

-

-

Lake Śniardwy

1989

Własow et al. 1991

-

-

17

-

-

Lake Mamry

1990

Własow et al. 1991

-

-

49

-

-

Lake Dąbrowa Wielka

1990-91

Własow et al. 1991

MYXOZOA

Family Myxidiidae

Myxidium giardi Cépède, 1906

spores

7

79.9 3

(+)-(+++)

-

Szczecin Lagoon

1982-83

Wierzbicka and Orecka-Grabda 1994

spores

7

100

(+)-(++++)

-

Oder mouth

1982-83

Wierzbicka and Orecka-Grabda 1994

-

gills

20

(+)-(++)

-

Lake Miedwie

1997-99

Sobecka and Piasecki 2002

-

-

21.1

(++)-(+++)

-

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

Zschokkella stettinensis Wierzbicka, 1987

spores

ub

48.65

(+)-(+++)

-

Szczecin Lagoon, Lake Dąbie

1983, 1985

Wierzbicka 1987

-

ub

11.3 3

(+)-(+++)

-

Szczecin Lagoon

1982-83

Wierzbicka and Orecka-Grabda 1994

-

ub

50.0

(+)-(+++)

-

Oder mouth

1982-83

Wierzbicka and Orecka-Grabda 1994

Family Myxobolidae

Henneguya psorospermica Thélohan, 1895

-

-

6

-

-

Lake Dąbrowa Wielka

1990-91

Własow et al. 1991

Myxobolus portucalensis Saraiva & Molnar, 1990

pl, spores

8

16.9

(+)-(++)

-

Szczecin Lagoon

1982-83

Wierzbicka and Orecka-Grabda 1996

pl, spores

8

29.2

(+)-(++)

-

Skolwiński Canal

1982-83

Wierzbicka and Orecka-Grabda 1996

pl, spores

8

38.5

(+)-(++)

-

Lake Dąbie

1985

Wierzbicka and Orecka-Grabda 1996

Family Ortholineidae

Ortholinea sphaerocapsularae (Wierzbicka, 1986)

spores

ub

7.69

(++)

-

Lake Dąbie

1985

Wierzbicka 1986b

Family Sphaerosporidae

Sphaerospora gilsoni (Debaisieux, 1925)

pl, spores

ub

13.2 3

(+)-(+++)

-

Szczecin Lagoon

1982-83

Wierzbicka and Orecka-Grabda 1994

pl, spores

ub

87.5

(+)-(++++)

-

Oder mouth

1982-83

Wierzbicka and Orecka-Grabda 1994

spores

ub

87.5

(+)-(+++)

-

Szczecin Lagoon

1983

Wierzbicka 1986a

PLATYHELMINTHES: TREMATODA

Family Allocreadiidae

Bunodera luciopercae (Müller, 1776)

A

-

1.1

2

0.023

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

Family Azygiidae

Azygia lucii (Müller, 1776)

-

stomach

0.63 3

1 (1)

0.006 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

Family Deropristidae

Deropristis inflata (Molin, 1859)

A

intestine

18.5 3

1-12 (3.8 3)

0.70 3

Baltic Sea (n. Chłapowo), Puck Bay

1930-31

Markowski 1933

-

intestine

17.6 3

2-30 (13)

-

Gulf of Gdańsk

1967-71

Rokicki 1975

-

-

3

1 (1)

0.03 3

Lake Dąbie

1971

Seyda 1973

-

intestine

3.8 3

1-63 (14.83)

0.56 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

A

intestine

1.43

2-4

0.042

Dead Vistula

1982-90

Sulgostowska 1993

A

intestine

12.17

1-600

2.190

Gulf of Gdańsk

1982-90

Sulgostowska 1993

A

intestine

42.15

1-200

16.016

Baltic Sea (n. Władysławowo)

1982-90

Sulgostowska 1993

-

intestine

1.14

2 (2.00)

0.02

Lake Łebsko

2000-06

Morozińska-Gogol 2011

-

-

0.4

1 (1)

0.002 3

Vistula Lagoon

2001-02

Bystydzieńska et al. 2005

-

-

0.7

1 (1)

0.007 3

Puck Bay

2002

Bystydzieńska et al. 2005

A

-

2.2

2-6 (3)

0.09 3

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

Family Diplostomidae

Diplostomum spathaceum s. l. (Rudolphi, 1819)

met

-

10

1 (1)

0.10 3

Oder (n. Stołczyn)

1971

Seyda 1973

met

-

31

1-4 (1.6 3)

0.50 3

Szczecin Lagoon

1971

Seyda 1973

met

-

6

1 (1)

0.10 3

Lake Dąbie

1971

Seyda 1973

Diplostomum spp.

met

-

9.1

2 3 (2.0 3)

0.2

Lake Dgał Wielki

1979-84

Grabda-Kazubska et al. 1987

met

-

6

-

-

Lake Mamry

1990

Własow et al. 1991

met

-

19

-

-

Lake Dąbrowa Wielka

1990-91

Własow et al. 1991

met

eyes

3.41

1-3 (3.67)

0.13

Lake Łebsko

2000-06

Morozińska-Gogol 2007, Morozińska-Gogol 2011

met

eyes

51.1

1-88 (6.8)

-

Puck Bay

2002

Bystydzieńska et al. 2005

met

-

8.9

1-2 (1.4)

-

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

met eye lens 14.3 9 6 (6.0) 0.85 Rzeka Łeba 2014-15 This study

Tylodelphys clavata (Nordmann, 1832)

met

vitreous humour

3

1 (1)

0.03 3

Szczecin Lagoon

1971

Seyda 1973

met

vitreous humour

3

1 (1)

0.03 3

Lake Dąbie

1971

Seyda 1973

Family Hemiuridae

Brachyphallus crenatus (Rudolphi, 1802)

-

-

5.9 3

9

0.53 3

Gulf of Gdańsk

1967-71

Rokicki 1975

-

-

0.2

1 (1)

0.002 3

Vistula Lagoon

2001-02

Bystydzieńska et al. 2005

Family Opecoelidae

Plagioporus angulatus (Dujardin, 1845)

A

intestine

7.4 3

1-3 (2)

0.15 3

Baltic Sea (n. Chłapowo)

1930-31

Markowski 1933

Family Strigeidae

Ichthyocotylurus platycephalus (Creplin, 1825)

met

stomach 10

0.63 3

3 (3)

0.02 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

met

-

2.2

3 (3)

0.07 3

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

PLATYHELMINTHES: MONOGENEA

Family Dactylogyridea

Dactylogyrus sp.

-

gills

30

(1)

-

Lake Miedwie

1997-99

Sobecka and Piasecki 2002

Family Pseudodactylogyridae

Pseudodactylogyrus anguillae (Yin & Sproston, 1948)

-

gills

-

-

3.46 3

Lake Strażyn

-

Dzika et al. 1995

-

gills

90

(11.6)

10.4

Lake Dębno

1994-95

Dzika 1999

-

gills

11

(1.82-9.25)

0.14-4.78

Rivers Radew, Rega, Wieprza

1999-2003

Sobecka and Pilecka-Rapacz 2003

-

gills

1.13

3 (3.0)

0.03

Lake Łebsko

2000-06

Morozińska-Gogol 2009, Morozińska-Gogol 2011

-

gills

100 9

6-16 (11)

11.0 3

Puck Bay

2002

Bystydzieńska et al. 2005

Pseudodactylogyrus bini Kikuchi, 1929

-

gills

-

-

2.07 3

Lake Strażyn

-

Dzika et al. 1995

-

gills

71

(18.1)

16.2

Lake Dębno

1994-95

Dzika 1999

-

gills

11

(0.73-3.5)

0.12-1.95

River Radew, Rega, Wieprza

1999-2003

Sobecka and Pilecka-Rapacz 2003

Pseudodactylogyrus sp.

-

gills

1.9 3

1 (1)

0.02 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

Monogenea n. det.

-

-

17

-

-

Lake Dąbrowa Wielka

1990-91

Własow et al. 1991

PLATYHELMINTHES: CESTODA

Family Bothriocephalidae

Bothriocephalus claviceps (Goeze, 1782)

A

intestine

22.2 3

2-3 (2.5 3)

0.55 3

Baltic Sea (n. Chłapowo), Puck Bay

1930-31

Markowski 1933

A

-

-

-

-

Lake Gołdapiwo, Lake Mamry

1954-58

Jarecka 1959

A

intestine

8.3 3

1 (1)

0.08 3

Puck Bay

1959

Sołtyńska 1964

-

-

25

1-11 (4.2 3)

1.05 3

Oder (n. Stołczyn)

1971

Seyda 1973

-

-

37

1-14 (4.9 3)

1.84 3

Szczecin Lagoon

1971

Seyda 1973

-

-

23

2-13 (3.7 3)

0.84 3

Lake Dąbie

1971

Seyda 1973

-

-

9.1

3 3 (3 3)

0.27

Lake Dgał Wielki

1979-84

Grabda-Kazubska et al. 1987

-

intestine

35.2 3

1-5 (1.1 3)

0.40 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

-

intestine

29.2

1-3 (1.4 3)

0.42 3

Skolwiński Canal

1982-83

Orecka-Grabda and Wierzbicka 1994

immature, A

intestine

10.00

1-35

0.807

Dead Vistula

1982-90

Sulgostowska 1993

immature, A

intestine

8.36

1-10

0.183

Gulf of Gdańsk

1982-90

Sulgostowska 1993

immature, A

intestine

11.57

1-18

0.371

Baltic Sea (n. Władysławowo)

1982-90

Sulgostowska 1993

-

-

6

-

-

Lake Dąbrowa Wielka

1990-91

Własow et al. 1991

-

intestine

12.5

1-6 (2.27)

0.28

Lake Łebsko

2000-06

Morozińska-Gogol 2011

-

-

0.8

1-2 (1.5)

-

Vistula Lagoon

2001-02

Bystydzieńska et al. 2005

-

-

30.1

1-11 (2.8)

-

Puck Bay

2002

Bystydzieńska et al. 2005

A

intestine

15.2

1-14 (3.4)

0.52

Lake Wdzydze

2004

This study

A

-

18.9

1-3 (1.3)

-

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

Family Proteocephalidae

Proteocephalus macrocephalus (Creplin, 1825)

A

intestine

22.2 3

1-20 (5.0 3)

1.10 3

Baltic Sea (n. Chłapowo), Puck Bay

1930-31

Markowski 1933

plerocercoid

intestine

8.3 3

1 (1)

0.08 3

Puck Bay

1959

Sołtyńska 1964

-

intestine

4.1 3

1-19

-

Gulf of Gdańsk

1967-71

Rokicki 1975

-

-

10

1-3 (2.0 3)

0.20 3

Oder (n. Stołczyn)

1971

Seyda 1973

-

-

22

1-10 (2.9 3)

0.62 3

Szczecin Lagoon

1971

Seyda 1973

-

-

26

1-4 (4.5 3)

1.16 3

Lake Dąbie

1971

Seyda 1973

-

intestine

39.0 3

1-33 (3.3 3)

1.30 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

-

intestine

16.7

1-2 (1.5 3)

1.50 3

Skolwiński Canal

1982-83

Orecka-Grabda and Wierzbicka 1994

immature, A

intestine

15.71

1-5

0.300

Dead Vistula

1982-90

Sulgostowska 1993

immature, A

intestine

10.12

1-25

0.253

Gulf of Gdańsk

1982-90

Sulgostowska 1993

immature, A

intestine

24.79

1-12

0.743

Baltic Sea (n. Władysławowo)

1982-90

Sulgostowska 1993

-

intestine

27.27

1-15 (3.75)

1.02

Lake Łebsko

2000-06

Morozińska-Gogol 2011

-

-

8.4

1-22 (3.8)

-

Vistula Lagoon

2001-02

Bystydzieńska et al. 2005

-

-

23.3

1-42 (4.8)

-

Puck Bay

2002

Bystydzieńska et al. 2005

A

-

31.1

1-5 (2.5)

-

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

A intestine 20.0 9 2 (2.0) 0.40 River Szkarpawa 2014-16 This study

Proteocephalus sp.

juvenile

-

16.7

1-6 (2.2)

-

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

Family Triaenophoridae

Triaenophorus nodulosus (Pallas, 1781)

-

intestine

20.0 3,9

1

0.203

Vistula (n. Warszawa)

1924-25

Dąbrowska 1970

Family n. det.

Cestoda gen. sp. Pseudophyllidarum larvae

L

intestine

8.3 3

1 (1)

0.08 3

Puck Bay

1959

Sołtyńska 1964

NEMATODA

Family Anguillicolidae

Anguillicoloides crassus (Kuwahara, Niimi & Itagaki, 1974)

-

sb

75

-

-

Vistula Lagoon

1988

Grawiński 1994

-

sb

80

-

-

Lakes Przywłoczne, Skąpe, Wielewickie

1989

Grawiński 1994

-

-

68.3

1-25

-

Vistula Lagoon

1988-90

Rolbiecki et al. 1996

-

-

2.7 3

1-2

-

Lake Niegocin

1989

Własow et al. 1991

-

-

70.0 3

5-25

-

Goczałkowicki Reservoir

1989-90

Własow et al. 1991

-

-

2.7 3

2-33

-

Lake Mamry

1990

Własow et al. 1991

-

-

-

-

-

12

-

Własow 1991

L2-L4, pA, A

sb

78.3

1-204600

-

Lake Strażyn

1993

Własow et al. 1991

L2-L4, pA, A

sb

25

1-102

-

reservoir near the village of Gaj

1993

Własow et al. 1991

-

-

100

15-20

-

Vistula Lagoon

1993

Grawiński 1994

L, A

sb

78.7

1-15

-

Lake Ińsko

1993

Orecka et al. 1995

-

sb

88.7

1-15

-

Lake Ińsko

1993

Rząd and Pilecka-Rapacz 2002

juvenile, F

sb

23.4 3

0-36

-

Szczecin Lagoon

1993-94

Garbacik-Wesołowska et al. 1994

juvenile, F

sb

69.0

0-22

-

Lake Łętowskie

1994

Garbacik-Wesołowska et al. 1994

juvenile, F

sb

23.1 3

0-10

-

Pomeranian Bay

1994

Garbacik-Wesołowska et al. 1994

L

sb

70

1-35

-

Szczecin Lagoon

1994-96

Rząd and Pilecka-Rapacz 2001

-

sb

37.5 9

3-8 (5.0)

-

Dead Vistula

1996

Rolbiecki and Rokicki 2005

-

sb

37.5

5-16 (7.3)

-

Lake Druzno

1997

Rolbiecki and Rokicki 2005

e, L4, pA, A

sb, intestine

41.9

(3.0)

-

Gulf of Gdańsk

1997-98

Rolbiecki et al. 2000

-

sb

100

3-44 (8.2)

6.7

Lake Miedwie

1997-99

Sobecka and Piasecki 2002

L3, L4, A

sb

33.3

1-7

-

River Wieprza (near Darłowo)

1999

Pilecka-Rapacz 2001

L3, L4, A

sb

40

1-10

-

River Rega (near Trzebiatów)

1999

Pilecka-Rapacz 2001

-

sb

59.1

1-11 (1.7)

-

River Rega (Lake Rejowice)

1999-2003

Pilecka-Rapacz and Sobecka 2004

-

sb

41.7

1-8 (1.3)

-

River Wieprza (nearDarłowo)

1999, 2001

Pilecka-Rapacz and Sobecka 2004

-

sb

65.6

1-12 (2.1)

-

River Radew

2000-01

Pilecka-Rapacz and Sobecka 2004

A, L

sb

68.18

1-27 (5.82)

3.97

Lake Łebsko

2000-06

Morozińska-Gogol 2005, Morozińska-Gogol 2007, Morozińska-Gogol 2009, Morozińska-Gogol 2011

-

sb

66.7

11-24 (17.5)

-

Lake Bukowo

2000-07

Morozińska-Gogol 2009

-

sb

100

5-11 (8.0)

-

Lake Kopań

2000-07

Morozińska-Gogol 2009

-

75

1-58 (10)

-

Vistula Lagoon

2001-02

Bystydzieńska et al. 2005

L4, L5, A

sb

75.9 3

1-11 (3.2)

-

River Rega

2001-02

Rząd et al. 2007

-

-

74.4

1-62 (8.3)

-

Puck Bay

2002

Bystydzieńska et al. 2005

L2-L4, A, e

sb

79.3

1-46 (7.2)

5.7

Lake Wdzydze

2002-05

Rolbiecki 2008

-

sb

100 9

6-18 (12)

-

Lake Raduńskie Dolne, Lake Raduńskie Górne

2004

Rolbiecki and Rokicki 2005

-

sb

58.3

2-12 (6.0)

-

Dead Vistula

2004

Rolbiecki and Rokicki 2005

L3, L4, A, e

sb

67.8

1-37 (4.2)

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

L2, L4, A, e

sb

65.2

1-20 (5.5)

3.6 3

Lake Ostrzyckie

2005-07

Rolbiecki 2011

-

-

-

-

-

Lake Kuc

2006-07

Jeżewski et al. 2007

L2, A, e

sb

50.0

1-12 (3.8)

1.9 3

Lake Żarnowieckie

2006-08

Rolbiecki 2011

L2, A, e

sb

40.0

2-3 (3.0)

1.2 3

Lake Raduńskie Dolne, Lake Raduńskie Górne

2006-08

Rolbiecki 2011

L4, A

sb

28.6 9

4-6 (5.0)

1.4 3

Vistula (near Tczew)

2007

Rolbiecki 2011

L3, A

sb, intestine wall

100 9

3-6

4.5 3

Lake Żarnowieckie

2007

Rolbiecki 2011

pA, A

sb

92.9

1-49 (10.8)

-

Szczecin Lagoon

-

Popielarczyk et al. 2012

pA, A

sb

64.7

1-5 (1.9)

-

Lake Dąbie

-

Popielarczyk et al. 2012

pA, A

sb

64.2

3-62 (18.5)

-

Lake Bukowo

-

Popielarczyk et al. 2012

pA, A

sb

100 9

1-50 (13.6)

-

Lake Łebsko

-

Popielarczyk et al. 2012

pA, A

sb

80.0 9

3-16 (8.0)

-

Lake Gardno

-

Popielarczyk et al. 2012

pA, A

sb

85.7

1-23 (7.2)

-

Lake Resko

-

Popielarczyk et al. 2012

pA, A

sb

76.9

1-55 (11.6)

-

Lake Jamno

-

Popielarczyk et al. 2012

pA

sb

50.0

1-7 (3.2)

-

Oder

-

Popielarczyk et al. 2012

pA, A

sb

71.4

1-6 (3.4)

-

Vistula

-

Popielarczyk et al. 2012

pA

sb

62.5

1-4 (1.7)

-

River Węgorapa

-

Popielarczyk et al. 2012

pA, A

sb

66.7

1-7 (2.6)

-

River Drwęca

-

Popielarczyk et al. 2012

A sb 100 9 7 (7.0) 7.0 River Piaśnica 2014-16 This study
A, L4 sb 40.0 9 6-9 (7.5) 3.0 River Szkarpawa 2014-16 This study
A sb 42.9 9 2-4 (3.0) 1.28 Lake Sarbsko 2016 This study

Family Camallanidae

Camallanus lacustris (Zoega, 1776)

-

intestine

20.0 3,9

1 (1.0)

0.20 3

Vistula (near Warszawa)

1924-25

Dąbrowska 1970

-

intestine

100 3,9

87 (87.0 3)

87.0 3

Lake Wdzydze

1958

Grabda et al. 1961

-

intestine

-

-

-

Lake Gardno, River Nogat (near Tczew), Lake Kalwa

-

Grabda 1971

-

-

15

1-4 (2.7 3)

0.40 3

Oder (near Stołczyn)

1971

Seyda 1973

-

-

3

12 (12)

0.39 3

Lake Dąbie

1971

Seyda 1973

-

-

45.5

(4.2 3)

1.9

Lake Dgał Wielki

1979-84

Grabda-Kazubska et al. 1987

A

intestine

3.1 3

1-7 (3.4 3)

0.11 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

L4, A

intestine

5.00

1-3

0.057

Dead Vistula

1982-90

Sulgostowska 1993

L4, A

intestine

2.93

1-20

0.152

Gulf of Gdańsk

1982-90

Sulgostowska 1993

-

-

7

-

-

Lake Dabrowa Wielka

1990-91

Własow et al. 1991

-

intestine

-

-

-

Lake Ińsko

1993

Rząd and Pilecka-Rapacz 2002

-

intestine

10

1 (1)

-

Lake Miedwie

1997-99

Sobecka and Piasecki 2002

-

intestine

3.41

1-2 (1.67)

0.06

Lake Łebsko

2000-06

Morozińska-Gogol 2011

-

-

3.8

1-7 (2.0)

-

Puck Bay

2002

Bystydzieńska et al. 2005

A

stomach

2.2

2

0.04

Lake Wdzydze

2004

This study

A

-

2.2

2 (2)

0.04 3

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

A intestine 25.0 9 7 (7.0) 1.75 Lake Kłodno 2015 This study

Camallanus truncatus (Rudolphi, 1814)

-

-

3

1 (1)

0.033

Szczecin Lagoon

1971

Seyda 1973

L4

-

0.29

1-3

0.005

Gulf of Gdańsk

1982-90

Sulgostowska 1993

A

-

2.2

2-4 (3)

0.073

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

A intestine 10.0 9 4 (4.0) 0.40 Lake Choczewskie 2008-15 This study
A intestine 25.0 9 1 (1.0) 0.25 Lake Kłodno 2015 This study
A intestine 20.0 9 1 (1.0) 0.20 Lake Dargin 2015 This study

Family Cystidicolidae

Cystidicola farionis Fischer, 1798

-

-

0.7

7 (7)

0.05 3

Puck Bay

2002

Bystydzieńska et al. 2005

Spinitectus inermis (Zeder, 1800)

F

intestine

3.7 3

3 (3)

0.11 3

Baltic Sea (near Chłapowo), Puck Bay

1930-31

Markowski 1933

A, L

intestine

3.3

1-5 (3.0 3)

0.10 3

River Wieprza (near Darłowo)

1999, 2001

Pilecka-Rapacz and Sobecka 2004

A, L

intestine

6.1

1-10 (3.4 3)

0.21 3

River Rega (Lake Rejowice)

1999-2003

Pilecka-Rapacz and Sobecka 2004

A, L

intestine

10.9

1-6 (2.3 3)

0.25 3

River Radew

2000-01

Pilecka-Rapacz and Sobecka 2004

Family Daniconematidae

Daniconema anguillae Moravec & Køie, 1987

-

gills

1.9 3

1 (1.0)

0.02 3

Lake Dąbrowa Wielka

1990-91

Własow et al. 1991

F

sb wall

-

1

-

Reservoir near village Gaj

1993

Własow et al. 1991

Family Dioctophymatidae

Eustrongylides excisus Jägerskiöld, 1909

L

intestine wall

3

3

0.09 3

Szczecin Lagoon

1971

Seyda 1973

L

stomach, body cavity

2.5 3

1-3 (2.2 3)

0.06 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

Family Raphidascarididae

Hysterothylacium aduncum (Rudolphi, 1802)

-

intestine

33.3 3,9

1 (1.0)

0.33 3

River Gnilna

-

Grabda 1971

-

-

0.2

1 (1)

0.002 3

Vistula Lagoon

2001-02

Bystydzieńska et al. 2005

-

-

0.7

1 (1)

0.01 3

Puck Bay

2002

Bystydzieńska et al. 2005

A

-

2.2

1-2 (1.5)

0.03 3

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

Raphidascaris acus (Bloch, 1779)

-

intestine

20.0 3,9

1 (1)

0.20 3

Vistula (near Warszawa)

1924-25

Dąbrowska 1970

M

intestine

3.7 3

1 (1)

0.04 3

Baltic Sea (near Chłapowo), Puck Bay

1930-31

Markowski 1933

-

intestine

100 3,9

1 (1.0)

1.00 3

Lake Druzno

1951

Kozicka 1959

-

intestine

-

-

-

River Gnilna, Lake Blanki

-

Grabda 1971

-

-

10

1-2 (1.5 3)

0.15 3

Oder (near Stołczyn)

1971

Seyda 1973

-

-

6

3-4 (3.5 3)

0.22 3

Szczecin Lagoon

1971

Seyda 1973

-

-

13

1-6 (2.5 3)

0.32 3

Lake Dąbie

1971

Seyda 1973

A

-

9.1

1 3 (1 3)

0.09

Lake Dgał Wielki

1979-84

Grabda-Kazubska et al. 1987

A

intestine

2.5 3

1-6 (4.0 3)

0.10 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

-

-

4.2

2 (2)

0.08

Skolwiński Canal

1982-83

Orecka-Grabda and Wierzbicka 1994

L4, A

intestine

24.28

1-26

0.900

Dead Vistula

1982-90

Sulgostowska 1993

L4, A

intestine

19.06

1-68

1.067

Gulf of Gdańsk

1982-90

Sulgostowska 1993

L4, A

intestine

9.09

1-2

0.107

Baltic Sea (near Władysławowo)

1982-90

Sulgostowska 1993

-

intestine

-

-

-

Lake Ińsko

1993

Rząd and Pilecka-Rapacz 2002

L

intestine

0.4 3

1 (1.0)

0.003 3

Rivers Rega (Lake Rejowice), Radew, Wieprza (near Darłowo)

1999-2003

Pilecka-Rapacz and Sobecka 2004

-

intestine

1.14

1 (1.00)

0.01

Lake Łebsko

2000-06

Morozińska-Gogol 2011

-

-

56.1

1-92 (5.6)

-

Vistula Lagoon

2001-02

Bystydzieńska et al. 2005

-

-

4.5

1-12 (5)

-

Puck Bay

2002

Bystydzieńska et al. 2005

A

intestine

2.2

2 (1.0)

0.02

Lake Wdzydze

2004

This study

Family Quimperiidae

Paraquimperia tenerrima (von Linstow, 1878)

L

intestine

0.4

1

0.0033

Rivers Rega (Lake Rejowice), Radew, Wieprza (near Darłowo)

1999-2003

Pilecka-Rapacz and Sobecka 2004

ACANTHOCEPHALA

Family Echinorhynchidae

Acanthocephalus anguillae (Müller, 1780)

-

intestine

20.0 3,9

1 (1)

0.20 3

Vistula (near Warszawa)

1924-25

Dąbrowska 1970

-

intestine

55.5 3,9

1-7

-

Potok Oliwski

-

Grabda 1971

-

intestine

33.3 3,9

8

2.67 3

River Łupawa

-

Grabda 1971

-

intestine

36.4 3

1-9

-

Vistula (near Tczew)

-

Grabda 1971

-

intestine

40.0 3,9

1

0.40 3

River Nogat (near Malbork)

-

Grabda 1971

-

intestine

-

-

-

Lake Probark

-

Grabda 1971

-

-

35

1-37 (9.1 3)

3.20 3

Oder (near Stołczyn)

1971

Seyda 1973

-

-

29

1-74 (11.1 3)

3.23 3

Lake Dąbie

1971

Seyda 1973

-

intestine

2.5 3

1-2 (1.2 3)

0.03 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

-

intestine

4.2

17 (17)

0.71

Skolwiński Canal

1982-83

Orecka-Grabda and Wierzbicka 1994

A

intestine

4.29

1-9

0.157

Dead Vistula

1982-90

Sulgostowska 1993

A

intestine

1.61

1-23

0.061

Gulf of Gdańsk

1982-90

Sulgostowska 1993

-

intestine

43.4

-

-

Lake Ińsko

1993

Rząd and Pilecka-Rapacz 2002

-

intestine

7.95

1-21 (6.57)

0.52

Lake Łebsko

2000-06

Morozińska-Gogol 2011

-

-

0.6

1-8 (3.3)

-

Vistula Lagoon

2001-02

Bystydzieńska et al. 2005

-

-

1.5

1 (1)

0.01 3

Puck Bay

2002

Bystydzieńska et al. 2005

Acanthocephalus lucii (Müller, 1776)

-

intestine

100 3,9

2 (2.0)

2.00 3

Lake Druzno

1951

Styczyńska 1958

-

intestine

100 3,9

2 (2.0)

2.00 3

Lake Druzno

1951

Kozicka 1959

-

intestine

100 3,9

7 (7.0 3)

7.00 3

Lake Wdzydze

1958

Grabda et al. 1961

-

intestine

-

-

-

Vistula mouth, River Łupawa, River Dadaj, Lake Dąbrowa Wielka

-

Grabda 1971

-

-

15

2-8 (4.0 3)

0.60 3

Oder (near Stołczyn)

1971

Seyda 1973

-

-

3

1 (1)

0.03 3

Szczecin Lagoon

1971

Seyda 1973

-

-

10

1 (1)

0.10 3

Lake Dąbie

1971

Seyda 1973

-

intestine

5.0-16.7

1-7 (2.4 3)

0.25 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

-

intestine

16.7

1-11 (3.8 3)

0.62

Skolwiński Canal

1982-83

Orecka-Grabda and Wierzbicka 1994

A

-

3.57

1-5

0.092

Dead Vistula

1982-90

Sulgostowska 1993

A

-

0.88

1-7

0.024

Gulf of Gdańsk

1982-90

Sulgostowska 1993

-

-

6

-

-

Lake Śniardwy

1989

Własow et al. 1991

-

-

6

-

-

Lake Mamry

1990

Własow et al. 1991

-

-

6

-

-

Lake Dąbrowa Wielka

1990-91

Własow et al. 1991

-

-

0.2

14 (14)

0.03 3

Vistula Lagoon

2001-02

Bystydzieńska et al. 2005

-

intestine

15.91

1-80 (14.14)

2.41

Lake Łebsko

2000-06

Morozińska-Gogol 2011

-

-

0.7

14 (14)

0.11 3

Puck Bay

2002

Bystydzieńska et al. 2005

A

intestine

28.3

1-8 (2.6)

0.74

Lake Wdzydze

2004

This study

A

-

1.1

1

0.01 3

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

Echinorhynchus gadi Zoega in Müller, 1776

A

-

0.73

1-4

0.014

Gulf of Gdańsk

1982-90

Sulgostowska 1993

-

-

0.2

1 (1)

0.002 3

Vistula Lagoon

2001-02

Bystydzieńska et al. 2005

-

-

3

1-10 (3.2)

-

Puck Bay

2002

Bystydzieńska et al. 2005

Echinorhynchus truttae (Schrank, 1788)

-

intestine

33.3 3,9

3 (3.0)

1.00 3

River Łupawa

-

Grabda 1971

-

intestine

11.1 3,9

1 (1.0)

0.11 3

Potok Oliwski

-

Grabda 1971

-

intestine

3.41

2-21 (8.67)

0.30

Lake Łebsko

2000-06

Morozińska-Gogol 2011

Family Neoechinorhynchidae

Neoechinorhynchus rutili (Müller, 1780)

-

intestine

5.9 3

2

0.12 3

Gulf of Gdańsk

1967-71

Rokicki 1975

-

intestine

2.27

1-2 (1.5)

0.03

Lake Łebsko

2000-06

Morozińska-Gogol 2011

Family Polymorphidae

Corynosoma strumosum (Rudolphi, 1802)

cystacanth

-

1.1

1 (1)

0.01 3

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

Family Pomphorhynchidae

Pomphorhynchus laevis (Zoega in Müller, 1776)

A

intestine

14.8 3

1-37 (10.8 3)

1.59 3

Baltic Sea (near Chłapowo), Puck Bay

1930-31

Markowski 1933

-

-

3

1 (1)

0.03 3

Lake Dąbie

1971

Seyda 1973

A

intestine

0.44

1-2

0.005

Gulf of Gdańsk

1982-90

Sulgostowska 1993

A

intestine

1.65

1-3

0.033

Baltic Sea

1982-90

Sulgostowska 1993

-

-

6

1-10 (2.8)

-

Puck Bay

2002

Bystydzieńska et al. 2005

-

intestine

3.41

1-2 (1.3)

0.05

Lake Łebsko

2000-06

Morozińska-Gogol 2011

Family Tenuisentidae

Paratenuisentis ambiguus Van Cleave, 1923

A

intestine

6.82

1-163 (28.17)

1.92

Lake Łebsko

2000-06

Morozińska-Gogol (2008), Morozińska-Gogol (2011), Morozińska-Gogol (2009)

MOLLUSCA: BIVALVIA

Family Unionidae

glochidium

-

9.1

1 3 (1 3)

0.09

Lake Dgał Wielki

1979-84

Grabda-Kazubska et al. 1987

glochidium

-

1.14

21 (21)

0.24

Lake Łebsko

2000-06

Morozińska-Gogol 2011

glochidium gills 33.3 9 6 (6.0) 2.0 River Słupia 2015-16 This study

ANNELIDA: CLITELLATA

Family Piscicolidae

Piscicola geometra (Linnaeus, 1761)

-

-

1.1

1

0.01 3

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

Piscicola respirans Troschel, 1850

-

-

-

-

-

River Dunajec with tributaries

-

Sitowski 1937

ARTHROPODA: BRANCHIURA

Family Argulidae

Argulus foliaceus (Linnaeus, 1758)

-

gills

1.9 3

1 (1)

0.02 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

ARTHROPODA: COPEPODA

Family Ergasilidae

Ergasilus gibbus Nordmann, 1832

-

gills

-

-

-

Vistula Lagoon

-

Zaddach 1844

A

gills

28.5

-

-

Vistula Lagoon

1908

Wegener 1909

-

-

16.6

(1.4)

0.23 3

Lake Dąbie

1955

Kozikowska 1957

-

gills

38.3

1-51 (8.5)

3.21 3

Vistula Lagoon

1959

Grabda 1962

-

-

-

-

-

Puck Bay

1959

Grabda 1962

-

gills

27.6

up to 4 (2.3)

-

Puck Bay

1959

Kozikowska 1965

-

gills

75.0 3,9

up to 75

-

Vistula (near Świbno)

1961-63

Grabda 1972

-

-

-

-

-

Vistula mouth

-

Grabda 1967

-

gills

1.9 3

1-4 (3.0 3)

0.06 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

Ergasilus sieboldi von Nordmann, 1832

-

gills

38.3

1-12 (3.2)

1.25 3

Vistula Lagoon

1959

Grabda 1962

-

-

-

-

-

Lake Dąbrowa Wielka

-

Grabda 1962

-

-

45.5

(4.4 3)

2.0

Lake Dgał Wielki

1979-84

Grabda-Kazubska et al. 1987

-

gills

52.2 3

1-16 (3.4 3)

1.79 3

Szczecin Lagoon

1982-83

Orecka-Grabda and Wierzbicka 1994

-

gills

33.3

1-4 (2.2 3)

0.75

Skolwiński Canal

1982-83

Orecka-Grabda and Wierzbicka 1994

-

-

6

-

-

Lake Śniardwy

1989

Własow et al. 1991

-

gills

10.23

1-23 (7.67)

0.78

Lake Łebsko

2000-06

Morozińska-Gogol 2007, Morozińska-Gogol 2011

-

-

9

1-4 (2.3)

0.20 3

Vistula Lagoon

2005

Rolbiecki and Rokicki 2006

A

gills

100 3,9

(3.0 3)

1.50 3

Lake Żarnowieckie

2007

Rolbiecki 2011

A gills 10.0 9 3 (3.0) 0.30 Lake Choczewskie 2008-15 This study
A gills 20.0 9 7 (7.0) 1.40 River Parsęta 2014-16 This study
A gills 20.0 9 5 (5.0) 1.00 Lake Jasień 2015 This study
A gills 28.6 9 2-3 (2.5) 0.71 Lake Sarbsko 2016 This study

Ergasilus sp.

-

gills

10

(2)

-

Lake Miedwie

1997-99

Sobecka and Piasecki 2002

1 blood, liver, spleen, kidney, skin, necrotic muscles;

2 single to numerous in spleen, single to very numerous in blood, liver, kidney; very numerous in skin;

3 parameter was calculated on the basis of data from publication;

4 parasite number in smear area 20 x 25 mm;

5 blood, kidney, liver, urinary bladder, gills;

6 rare or sporadic;

7 gills, kidney, intestine, urinary bladder, liver, gall bladder, spleen, skin;

8 fins, gills, urinary bladder, kidney, liver, intestine;

9 calculated from less than ten individuals;

10 questionable microhabitat;

11 unspecified, the authors provided a value for several reservoirs;

12 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 (Trypanosoma granulosum, Apiosoma sp., Ichthyophthirius multifiliis, Trichodina jadranica, Trichodinella epizootica, Capriniana piscium, Rhabdospora thelohani, Henneguya psorospermica, Myxobolus portucalensis, Myxidium giardi, Zschokkella stettinensis, Ortholinea sphaerocapsularae, Bunodera luciopercae, Dactylogyrus sp., Triaenophorus nodulosus, Cystidicola farionis, Spinitectus inermis, Hysterothylacium aduncum, Paraquimperia tenerrima, Corynosoma strumosum, Echinorhynchus gadi, Echinorhynchus truttae and Paratenuisentis ambiguus) in 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 and Hirotaka 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 (Rolbiecki et al. 2008). 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 web-based database, supplemented and coordinated by scientific centres from different countries.

References

Supplementary material

Suppl. material 1: GPS coordinates of collection sites 
Authors:  Joanna Dzido, Leszek Rolbiecki, Joanna N. Izdebska, Rafał Bednarek
Data type:  Table