Macroparasites and Their Communities of the European Eel Anguilla Anguilla (Linnaeus) in the Czech Republic

Research Article Macroparasites and their communities of the European eel Anguilla anguilla (Linnaeus) in the Czech Republic

František Moravec and Tomáš Scholz

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Abstract: G!!>!?Anguilla anguilla (Linnaeus) in the 67!"H$! "JK-+H'M- 77!7KK!7>!*;& K>!!9;7!!?7Q7 and Oder river basins. Of the 31 species of adult and larval macroparasites including Monogenea (4 species), Trematoda (3), Cestoda (3), Nematoda (11), Acanthocephala (5), Hirudinea (1), Bivalvia (1), Copepoda (1), Branchiura (1) and Acariformes (1), most of them H&+JK!?767G7![ [H;E[J@[[HE'[J@[H'&[JG !7H'MJK\$[!!G!!@ !>7! ecological conditions. The parasite fauna of A. anguilla67!K?G nematode Cucullanus egyptae7@]7@]7^!!;+'9 as a species inquirenda. Keywords: [[?767Q767_67 ?

` > K!7 >!H6'<*&'M+<~ nematode Anguillicoloides crassus (Kuwahara, Niimi et '<**!$'M+'\$"'M-&"!$'M-- $'M*9JK? Q$\$"'M-E'M-*'ME&5$'M-M? of eels Anguilla anguillaH\J'M<+R 'ME'Q$'ME9'MEE'M*''M*<'M*M'MM; there were few helminthological studies on this species ;++'?\!'M*+'M<+x= [KKK@ 'M<*"x'M<<"'M!H'M<-J Hx='M<<"7'MM*x @! 7@ 'MM<'MMMx;++'" ogy and ecology of endohelminths parasitising eels in the ";++'_;++;$@6 \$H 5J[!@ "7$ ;++9 " ;++- x! !7!>@ |;++*J otic species of helminth parasites, the nematode A. crassus 67H!$J and the monogeneans Pseudodactylogyrus anguillae (Yin K7[7 "'M9

!"$&'&*++-5$ D56789;+&<***-9&;=>89;+&<-&'+&<<=?@!!B

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. '+'99''F;+'-+&& Moravec and Scholz: Macroparasites of Anguilla anguilla67

Table 1. List of the localities from where eels, Anguilla anguilla H\JK>!

No. Locality >! Year(s) and month(s) ?\?6?6"H&-J 1 ?76|T$ 13 'MM';++';++- ; x!6|T$ < 'M*<'M*M 3 665$\ ;9 'MM9 4 ~D$"$6$ 9 ;++';++; 5 56 5 'MM9 E "6K!$6 1 'M*- 7 _T6 31 'MM9 < \76$"$ 1 ;+++ 9 G6x '< 'ME&M'ME* 10 KG6G 'E 'M<< 11 \$[!Q$ ;+M 'ME-M;++<M '; 67 13 'M<< 13 _$K6 117 'MM9M'MM*M 14 6G! 3 'M<< 15 \K6 ; 'MMM;++' 'E `6\H\J 1 'ME; 17 _$| 1 'ME; '< 5$ D5 'E 'M<<'M

Within broad investigations on the helminth parasites of munities in different localities. Based on the high number [677 >!77 of the Institute of Parasitology, Czech Academy of Scienc@ the most comprehensive studies on the parasites of this es (previously the Czechoslovak Academy of Sciences), ![G!@ 'M<-5$ D5 !!-+67 H;++';+'&J!! !7? K >! -+ "! K >!@ MATERIALS AND METHODS 77H?'ME' G7!>!@ 'M<-$$'MMEJ7!7@ tions of eels Anguilla anguilla from the territory of the Czech tained remain unpublished, even though they represent im@ 67@ portant information about the species composition of the emy of Sciences (previously the Czechoslovak Academy of Sci@ 677@ JK-+H'M-!7

;+'-E;+&& ;'* '+'99''F;+'-+&& Moravec and Scholz: Macroparasites of Anguilla anguilla67

Fig. 1. K!67!KKH!7 Table 1).

Q6!?'M-!!9; H\'*-!G!K This is a parasite of Esox lucius Linnaeus and some !*M';+!7!!@ [!G. lucii was found on K!= $\$[!H H!JKK!>! 'M<-JH'M<;'F*'J= The parasites obtained were treated by usual helminthologi@ this represents an accidental infection. cal methods and these materials are mostly deposited in the Helminthological Collection of the Institute of Parasitology, Gyrodactylus sp. ! " 5$ Numerous live and dead specimens of this parasite were D5 HFFKKKFFFJ " [_T6 7>! >!_7'MM9K@ group. ;E[H

Composition of the fauna of macroparasites of Pseudodactylogyrus anguillae H"'M9Gyrodactylus sp., Crepidostomum met- !"6TH@ oecus (Braun, 1900), Diplostomum spathaceum H6 'MM--9[*F'&'M';!

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Table 2. Occurrence of macroparasites in Anguilla anguilla (Lin@ in the following Bohemian localities, where the propor@ J!!767H@ tions of both species in samples were similar: Mácha Lake ditional records from other countries are given in parentheses). [!H!'E'MM9= Parasite ?76 Q7 _6 recorded in previous years) (prevalence of both species Basin 6 Basin <<['9F'EMM&&+--J=_$K __]?? H"!7'MM9*FM&M;-*_7'MM9 Gyrodactylus lucii 8 <+[';F'-'M;M+E9"!7'MM-<*[;+F;& Gyrodactylus sp. 8 'M&E<&*'MME&E[-F'9'M;< ''~'MME Pseudodactylogyrus anguillae 88 &E[9F'''M;9''_7'MMEE*['+F'-MM<* Pseudodactylogyrus bini 8 H8J &'J=\6G7H'MM9;+[;F'+ G6?G_Q ;MM& 9<J= _ 6 D H 'MM- Azygia lucii 8 '++[';F';;M'-<EMJ= $6"T7 Crepidostomum metoecus 8 H"!7'MM9EF*&ME'&+J=_T6 Diplostomum spathaceum larv. 88 H_7'MM9&;['+F&';M';-J (Metagonimus yokogawai larv.) H8J Q767P. anguillae alone was re@ ?"G_Q $K Bothriocephalus claviceps 888H"!7'MM99+[9F'+&ME-;'J Proteocephalus macrocephalus 88 However, the presence of these parasites in other locali@ Triaenophorus nodulosus5 8 H8J 7>7K ?G_Q monogenean infections of eels in some localities. Anguillicoloides crassus 88 Both P. anguillae and P. bini are pathogenic gill para@ Camallanus lacustris 8 Camallanus truncatus 8 ~Anguilla japonica Temminck et Cucullanus truttae 8 "?!KK Daniconema anguillae 8 H8J ?'M*+R?$ (Hedruris androphora) H8J ?A. anguillaH$$ Paraquimperia tenerrima 88 'MMEJG[7 Raphidascaris acus 8 H8J Salmonema ephemeridarum 8 !$6?H Spinitectus inermis 8 "65$ D5 Eustrongylides mergorum larv. 8 6M7J_7'M!'M**H'M<-J! !!>!'MM9K@ |6`Q? els of infection with P. anguillae and P. bini. The situation Piscicola geometra 8 \ \ ?7[7? Glochidium gen. sp. larv. 88 K]H'M**J6 _?_Q Ergasilus gibbus (?) 8 H8J Trematoda Ergasilus sieboldti 88 6|`6 Azygia lucii H'**EJ Argulus foliaceus 8 This trematode was found in the stomach of eels in two 6_6?" 7?767\$ [!Q$H'M*''F''="!@ Hydrozetes sp. 8 7'M*'*['F'9'='M<;'F-'=~'M<;<[ HJ M ! @ 'F';&='MM9'&[;F'E'J=_$K [!Ergasilus gibbus !'<&;H6 '<*&;++'J D H"!7 'MM- &[ 'F&< 9). Azygia lucii was previously reported from eels in the !7H'M<-J -J=$KH~'MM-&+[EF;+'ME G[A. lucii is the northern &J=56H_7'MM99F- pike, Esox lucius K ? 'MM -J Pseudodactylogyrus bini alone was found in as a subsidiary host. It may be supposed that A. anguilla 6 6 5$ \ H"!@ 7KK[! 7 'MM9 M+[ MF'+ <-M'9-' -&EJ |K 7 small pike and perch. The occurrence of A. lucii in eels P. anguillae and P. bini@ seems to be in correlation with the feeding period of the

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[K ferent families (rarely also frogs) serve as the second in@ !H\'M<;JA. lucii was not re@ !H5$'M*9;++'"$ corded. In addition to A. anguilla, Linnae@ ;++EJ H;++'J ! us and Sander lucioperca (Linnaeus) were also recorded D. spathaceumK!-+[@ as subsidiary hosts of A. lucii\$[ cies (mainly cyprinids) in the former Czechoslovakia, but !H'M<-J not from A. anguilla[ _ H'M*EJ ! these parasites in eels represent a new host record. A. lucii are various species of freshwater snails of the fami@ Taxonomic note:G>!Diplosto- 7\! mum!'<&;[ ! [ ! Crepidostomum metoecus (Braun, 1900) >! The only locality where this trematode was found in the studies that combined molecular and morphological data K ~D$" $ 6$ have revealed cryptic diversity in the Diplostomum species H;++''FE'J7?767 !>H];+'&@ G![C. metoecus are salmonids, ;+'9"$;+'9JG!K ?!7KSalmo trutta fario Lin@ be that metacercariae from eels reported under the name H;++9J!@ D. spathaceum actually belong to more than one species [ ! ! Esox lucius of Diplostomum. H?J Lota lota (Linnaeus) (Lotidae) or - viatilisHJK7@ Cestoda tion of adult trematodes while feeding on small salmonids H;++9JG[C. metoecus in A. an- Bothriocephalus claviceps H]'*<;J guilla suggests a similar way of transmission, i.e. that the This cestode was recorded from eels in the following lo@ !7KK!@@ calities belonging to all three main river drainage systems: fected trout. In the same locality, C. metoecus was recorded ?767x!$~T\|@ !9+[S. trutta fario>!H;++&JG H 'ME9 'F' &;J= \ [!C. metoecus are bivalves (Pis- 6 G7 H 'ME9 'F; -= 'M<+ ;F; idiumJ=!Gammarus pulex H\J 'M&;='M<''F''=7'M<*;F; ! HEphemera Linnaeus, Cloeon 'M;;J=\$[!Q$H7@ Leach, Siphlonurus ?JK@ 'ME*'F'E='M*E;FM'M&;='M*E !?H;++9J 'F;;='M*E'F'<="!7'M*E;F-'=_@ 7'M*E;F9'M'EM=Q!7'M*E;F- 7 G [ !@ 'MM-'+[;F;+'MM-="6T ate host is the freshwater snail Lymnaea (Radix) peregra H'MM-<['F'&'J=\76$"$ ovata HQJ= ! [ 7 @ H~;+++'F''-J

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Q7 6 7 Q!$" T the maturation cycles of B. claviceps75! 5!H!7'M-<'F;'J=6$6 local ecological factors, may be very different in other lo@ !H~'M<*'F''J=x5$6 =!7@ x6H"!7'MM9'<[;F'';M-9J=$ er months or nearly throughout the year in different locali@ KH"!7'MM9&+[&F'+'J= H\$"'M-&x4'M*+77'M<; DK_6$ 'M<-J T6H'MM-'E[9F;-'M9;J _ 6 7 x7$ K Proteocephalus macrocephalus H'<;-J 6x7$H~'MME-F<'M';&J This species was recorded from the following localities Bothriocephalus claviceps was previously reported 7?7Q76! ! ?7 Q7 6@ ?7 6 7 \ 6 \! 7677!$H'M+'J6 \H'ME9'F;'='M<+'F;'=7 H'M+! K J ! H 'M[&F'E-M'+<J=GT7NH_7 \$ [ ! 7 <+[JG [ 'MM9-F*'MME9-J=_T6H_@ B. clavicepsx7$[ 7'MM9'E[-F&''M;'J=\!@ !_67 \H_7'MM9*+[*F'+'M9''&J= 67 $ K H~ 'MM- E-[ '&F;+ 'M'; G!7[ 9J= " 6 T H 'MM- ;&[ eels and A. anguilla has so far been recorded as the only &F'& ;M'+ -J= _ 6 D H [[67 'MM--<[*F';;M-9J=\$[! H;++'=JBothriocephalus claviceps Q$HQ!7;++<'F&&J 7![7 Q767$K !777[ H"!7'MM9&+[&F'+'M*9J hosts (Scholz 1997). In this connection, it is necessary to 677 ![B. claviceps from !K7?76 '-[KTriturus vulgaris (Linnaeus) 7 H" x 'M<< " 'M!@ 'MM*"'MM*'MM<"| 'M<<'M!K K67@ @77 curring in eels mainly in larger rivers, water reservoirs and these cestodes in their atypical amphibian host (newt). GH<+[J The source of B. claviceps infection for eels are either HEM!JK_$K@ ![@ _7'MME7K H~$ 'M-M 'ME& 'ME9 'M<- also found in some other localities. Q]7'M7 ! It can be assumed that P. macrocephalus, as most other K!~= !>7@ [K nounced seasonal maturation cycle, but no detailed data on be small perch, H"'M!!7!!!@ ration of P. macrocephalus occurred in early summer in !K?|K K!?\$"$

;+'-E;+&& E'* '+'99''F;+'-+&& Moravec and Scholz: Macroparasites of Anguilla anguilla67 x4H'M*+J!P. macrocephalus in A. an- ?A. crassus infec@ guilla!~~!7!!@ 77!@ ture worms during all months, with the highest numbers in ![7A. crassus@ Q!7 H;+'&J

Triaenophorus nodulosus H'*<'J5 Camallanus lacustrisH'**EJ ~!K! This species was found in eels only in localities belong@ the intestines of eels only twice in two localities belonging ?767\$[! ?767G6xH~ H7'ME*'F';&-=!7'M*-'F''= 'ME- 'FE 'J \$ [ ! H 'M*E;F<'='M*E'F;9=~'M*E'F&'="!@ 'MM9E['F'E'J@ 7'M*E9F-*M-''*=Q!7'M*E&F-;M;E''= K[H77!P.- 'M** 'F' '= 'M** 'F; 9= "!7 'M** viatilis) harbouring the cestode plerocercoids and serving -+[*F'9'M;9-=~'M<''F';="!7'M<' as the second intermediate host of T. nodulosus. Larval 'F;;=7'M<;'F&'='M<;EF<'M<&= T. nodulosus in A. anguilla was previously reported by 'M<;-F<'M'+&='M<;'F-<=~'M<; 5$H'ME'J!$H 9;[-F';;MM-=~'M<;&FM;M*9='M<; given) (see also Macko et al. 1993). ;F*;M-9="!7'M<;9F<'M9&=_7'M<; ;F-;M-9='M<*&'[-F'E&M'-*='MM+ Nematoda ;F&;M*-='MM999[*F'E'M-;="!@ 7'MM-9'[MF;;'M9&''=Q!7;+++;F&&ME Anguillicoloides crassus Kuwahara, Niimi et Itagaki, &=;++&'F''<=;++&'F;;=~;++& 1974 'F';=Q!7;++9'F;'=Q!7;++-;F&&ME This swimbladder nematode was recorded from the fol@ -J=$\H!7'M<-'F9&J= lowing localities belonging to two main river drainage sys@ $KH'M<<--[EF'''M';E= tems. ~'MM-;+[9F;+'M;;J=K ?767?76|T$H~'MM' G6GH'M<<E['F'E9J= <+[

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!G!>@ 'M<'<['F';'='M<**['F'-'='MM9 hibit a pronounced seasonal cycle of maturation (Moravec ;-[9F'E'M;&*="!7'MM-'9[&F;;'M; 'M*M7"'M7 7! seasonal cycles of occurrence and maturation (Chubb 1975, x'MM'7J67P. tenerri- Daniconema anguillae x='M<* maK!M~"!@ This parasite of the serosa of swimbladder and intes@ ber and always gravid females with eggs were also present. tine of eels was recorded from the localities belonging to The life cycle of P. tenerrima![$K ?767\$[!H~ 77![

;+'-E;+&& <'* '+'99''F;+'-+&& Moravec and Scholz: Macroparasites of Anguilla anguilla67 serve as intermediate or paratenic hosts (Moravec 1975, xH~'ME-'F&'JG[K ;+'&"x;++-J 7H'ME*J The nematode S. ephemeridarum is a stomach parasite Raphidascaris acus (Bloch, 1779) !?!7KSalmo Adults of R. acus and larvae in the intestinal lumen of trutta farioH;+'&J! eels were found in the following localities belonging to one parasite is sometimes found in other, mostly predatory or main river drainage system. [@ ?767G6xH_7 K[S. ephemeri- 'ME9'F;'=~'ME-'FE&="!7'ME-'F';= darum, i.e. small salmonids. Also in the present case, ap@ ~'MEE'F&&=~'ME*'F&'J=\$[@ S. ephemeridarum infection !H"!7'M*E;F-;M;*'-='M** secondarily by occassional preying upon small trouts. 'F; '= "!7 'M** *[ 'F'9 '= Q!7 'M** The intermediate hosts of S. ephemeridarum are dif@ 'F''=Q!7'M<''F''="!7'MM+'F-'J= !\ H?!J K \6\!\H'M<*'F; ! ! [ Cottus gobio Linnaeus, Barbatula ;J= 6 7 H~ 'M<< &'[ 9F'& barbatula H\J ! 'M&;J=6G!H_7'M<<'F' H;+'&J 'J= x! 6 |T$ H~ 'MM' 'F' &J= \6G7H'MM9&+[&F'+;M'< Spinitectus inermis H'<++J '+=_$KDH~'MM9'FM This nematode was found in one locality belonging to '=_7'MM9'F*'='MME*['F'9'J= $ ?767\$[!H@ 6"T7H"!7'MM9;F*'M;;J=_T !7'M*-'F'9="!7'M*E'F-';=Q!7 6H_7'MM9;E[brown trout Salmo trutta fario, less often other species of salmonids, Lota lota, , Sander lucioperca Eustrongylides mergorum H6'<+MJ or Anguilla anguillaH;+'&J|K@ Larvae of this parasite were recorded from the stomach ![!@ K7?76 ! 7! H ! [ 7\$[!H7'ME*'F' J!H'M<-J ;J ;*R. acus larvae from a single eel G[E. mergorum[@ H79+!J'&;>!\$ 7K [! ! Hx! 'ME

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Acanthocephala _6$ T6H'MM-&E[ MF;-;M;<MJ= Acanthocephalus anguillaeH'*<+J _ 6 7 x7$ K GK?767 6x7$H~'MMEEF<;–'9MJ x! 6 |T$ H!7 'M** &F- This acanthocephalan occurs in many species of fresh@ 'M'9*J=665$\H"!7 K[!K@ 'MM9'&[&F;9'M;'J=_T6 ing on macrobenthic invertebrates, belonging to different H_7'MM99-['9F&''M;-EJ=_$K@ !H;++9J seems to be DH_7'MM9*['F'-'=~ ! [ ? (see 'MMEM['F'''=_7'MME*['F'-'J=" ;++'J!67A. lucii 6TH'MM-;&[&F'&;M'E was previously reported from all three main river drain@ *J !_67H6MQ$ This acanthocephalan is reported from many species of \$"'M-EJQ767H"$6 K [ 7 ! 7 M5$'M-MJ?767H\$ preferred hosts seem to be numerous cyprinids (Moravec [!M'M*<'M<-J ;++9J ?7 6 7 67 The life cycle of A. lucii involves an intermediate host, A. anguillaeK!7!$ the freshwater isopod Asellus aquaticus (see Moravec H'M+'J ?7 6 D7 7 ;++9JG!7@ "!$H'M--J"\6 fected intermediate host isopods (A. aquaticus) or prey 7Q776@ [!!HP. ) harbour@ 7HK[J ing these parasites. H;++'J7NH'M*MJA. anguillae !Q76"$ Echinorhynchus truttae "$'*<< The life cycle of A. anguillae involves the intermediate G K ! ?7 host, Asellus aquaticus Linnaeus (Isopoda), in which the 6 7 x! 6 |T$ H!7 infective larval stage, the cystacanth, develops (Moravec 'M*<'F-'=~'M*M'F&'J ;++9JGA. anguillae infection for eels may be Adults of E. truttae are found mainly in the intestine 7![[H7 and pyloric caeca of various salmonids, but also in some also paratenic) hosts. [7!G! of this acanthocephalan are amphipods of the genera Echi- Acanthocephalus lucii H'*<+J nogammarus Stebbing, Gammarus, Pontoporeia Kohlm This acanthocephalan species was recorded from eels in and Pallasea H ;+'&J all of the three main river drainage systems. E. truttaeK67 ?7 6 7 \ 6 \! !!'ME;K!!Gamma- \H'ME9;F;'='M**'F'

;+'-E;+&& Page 10 of 17 '+'99''F;+'-+&& Moravec and Scholz: Macroparasites of Anguilla anguilla67 tili K!7]H'MM+J casionally recorded from eels in 1975–'M** M S!K6H?767@ 'M<-='MM9'&[;F'E'=J=_$K J7"H'MM'7J6$ DH~'MM9;FM'M& ;=_7'MM9*[ 6HQ767J 'F'-'="!7'MM-99[*F'E'–-;=!@ Like in other congeneric species, the life cycle of N. ru- 7'MM-'F*'='MME*['F'9'=~'MMEM[ tili7! 'F''&=_7'MME-&[leeches, DH'MM-<['F';'J \[JKK G![7@ observed, may apparently serve only as paratenic hosts !67@ H;++9J77![@ K 7 5$H'M-MJ ! ratenic or postcyclic hosts of N. rutili. It can be assumed "$6HQ767J7 that eels become infected with this acanthocephalan main@ H'M<-J!\$[!H?76 77[ basin). [[ 6H'<*&J! Ergasilus gibbus ! '<&; [ Pomphorhynchus laevis H'**EJ A. anguilla67H?7 This acanthocephalan species was recorded from eels 67MJ|KE. gibbus is Q7 6 7 6$ 6 7$@K7@ !H'M! This ectoparasite was recorded on gills of an eel in the 'M*-M'M**H'M<-J \$[!H?767JH G$K![@ 'M<;'F*9J=[K7H'M<-J cies belonging to different families. Bivalvia A. anguilla recorded in the present study 6@[7 Glochidium gen. sp. larv. roughly divided into the following groups: G K Q7 H'J " [ K HAnguilla 67DK_6 J[H[7_@ $ T6H'MM-E['F'<'J 'M*EJ!Pseudodactylus anguillae and K76H'M+

;+'-E;+&& Page 11 of 17 '+'99''F;+'-+&& Moravec and Scholz: Macroparasites of Anguilla anguilla67 hynchus rutili, and Pomphorhynchus laevis, the hirudinean term observations. However, in this study, the numbers of Piscicola geometra, the crustaceans Ergasilus sieboldi >! ! ! ! and Argulus foliaceus, and the acariform Hydrozetes sp. impossible to make a reliable comparison of the parasite Since the present knowledge of the biology of most of !!7! the localities investigated. cycles remains unknown. It can be only assumed that for Nevertheless, the results obtained indicated marked dif@ some of them (Azygia lucii, C. truttae, R. acus, N. rutili, ferences in the numbers of parasite species recorded from A. anguillae, A. lucii, E. truttae, P. laevis, P. geometra, ! ! K@! 7 E. sieboldi and A. foliaceusJ?! !!!>!?7 [! 6 7 !7 H'~D$"$6$ Gyrodactylus sp.). [GG6@ H&JKK[@ x $6"T7 K![! ?7 x! 6 |T$ serving either as intermediate hosts (D. spathaceum, Glo- 6 7 G! $ K chidium sp.), paratenic hosts (E. mergorum) or accidental 5$ D5@ facultative hosts (P. ensicaudatum). $6\! A comparison of these groups shows that although \GT7NK H;E[JK@ \76$" $ "" $ xD 7[Anguilla spp., a great $x$\ !5!H*9[JK!7@[@ 56\ 7HE'[JH'&[J Kx!$~T\|@ interest that there is no trematode species among the eight dec. No parasites were recorded from eels in seven other [HK!K H7!KJ=K> and four nematodes) and that three of them (P. anguillae, K!@KG@ P. bini and A. crassus) represent introduced species. !K>!!@ G7 ; K [ ties. for AnguillaK?767 However, the species composition of parasites of eels !>HSpinitectus inermis), was usually different even if the same or similar numbers K!Q767 of these organisms were recorded from eels in different 767 >! @ neighbouring countries. In contrast, only one parasite spe@ !_6HP. anguillae, P. bini, [Anguilla spp. (Bothriocephalus claviceps) was re@ P. macrocephalus, P. tenerrima, A. crassus, C. lacustris _67K!7 and A. foliaceus), only three (A. crassus, P. tenerrima and with the fact that eels rather rarely occur in this drainage C. lacustrisJ K ! > !HQ$\$"'M-*JG@ ~D$"$K [\7 (C. metoecus, C. truttae and N. rutili) occurred, which were [>!Cucullanus truttae 7_6 K!?77K K~D$" salmonids, but not from eels in the two other river basins, Brook share the environment with the brown trout (Salmo where C. truttae7!H;++'J trutta fario) (C. metoecus and C. truttae are common para@ sites of salmonids), whereas no salmonids probably occur Parasite communities of A. anguilla in different _6 localities _[@[ It is well known that the formation of the parasite fauna [ @ [7!>=!! 7 &+M9+[ >@ \$[! ronment, whereas the effects of others are manifested only H&M[J_$KH&'[J!K !7K>! [@ !!+;-[!-+ fect of many factors enabling its sometimes complicated '++[_[!7@ developmental cycle to be completed. Therefore, an evalu@ uted species was the tapeworm B. claviceps recorded from !![ ;97!7= 777@ widely distributed were also the tapeworm P. macrocepha-

;+'-E;+&& ';'* '+'99''F;+'-+&& Moravec and Scholz: Macroparasites of Anguilla anguilla67 lus and the nematode P. tenerrima, recorded from 14 and cause other Rhabdochona [ '- K 7 ?7 may be accidentally found in A. anguilla serving as a post@ Q7 7 G K!7 ! cyclic host (e.g. R. paski'M;<!? A. crassusK!?7 M'M*9JRhabdochona anguillae seems to be re@ Q77H7J_!@ 7?!@ tode S. inermis was found in a single locality (Mácha Lake phologically very similar species, R. keralaensis Moravec, [!J!D. anguillae only in "7x!;+';[Anguilla H\$[!_T bengalensisH]JH;+';J 66JG!@[@ !H;++\$[! H;++!!7 [>@ within a given locality and between different localities, onomy of some species of Acanthocephalus Koelreuther, were not considered as they would be misleading. 1771 and Echinorhynchus '**E@ ?K[!7!K@ DISCUSSION A. rhinensis needs ? Anguilla an- [ guilla have been intensively studied, mainly during re@ 7@![ 7!? ?K[!@ !Hx='M<<"7 [7$! 'MM*;++-'MMMQ;++' localities, represented by the monogenean Gyrodactylus x;++'x;++;x anguillae ? 'ME+ ! Deropristis in- 'MM+;++-";++-6@ H'<-MJBucephalus anguillae$ 7$ 6$$ ;++E x! | $ Q ;++; ! Goezia ;++*|!;++

;+'-E;+&& Page 13 of 17 '+'99''F;+'-+&& Moravec and Scholz: Macroparasites of Anguilla anguilla67

>[7$! @[! one (P. ambiguusJ?@ 6777@ !!HGK$'M<*J HG7;J7 G@[ KKK? variable in different localities and mostly depends on the >!Ligula intestinalis (Linnae@ ! [ 7 '*-S. contortus maturing in turtles, one locality to another and with respect to the characteris@ [@7!7$@ tics of the environment. In addition to the parasite species @K ! ! ! @[ cestodes (GrillotiaΣGRJ!@ parasites were found in this host in freshwater localities in atodes, such as Anisakis simplex H6 '<+MJ Hys- >!!Bunodera lu- terothylacium spp. or Pseudoterranova decipiens (Krabbe, ciopercaeH'**EJCrepidostomum farionis (Müller, '<* many local representatives of the then State Fishery and the Czech thaster Lühe, 1901, Lecithochirium Lühe, 1901, Limnoder- Union of Sport Fishery for their permission to sample the eels. etrema 'M<* Podocotyle Q5'<9-J ! Thanks are also due to many technicians of the Institute of Parasi@ nematodes (e.g. species of Cucullanus Müller, 1777 and "5$ D5 Hysterothylacium Ward et Magath, 1917), acanthocepha@ K[K$7>! ! Echinorhynchus spp. and Acanthocepha- GK7] loides incrassatusH'<-

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ǃǅǂǍǍǂǉ \]@ ǂǂǎǐǖǓǊ ;++; Bu- ǐǓǈǔǕǆǆǅǆ | |ǂǆǏǆǏ _\ Qǆ Ǔǆǆ ~ \ǊǔǊǕǔǊǏǂ cephalus anguillae$$¯Q;++; O.I. 'MMM?HAnguilla anguil- HQJAnguilla anguilla (L.). Syst. la\J|!&E;-'M;E+ -&;+*M;'* ǉǖǃǃ~1975: A review of seasonal occurrence and maturation ǃǅǆǍ@]ǉǂǇǇǂǓǂǔǉǕǂǓ@6ǃǅǆǍ@]ǂǃǆǓ6ǐǓǔǚ !K[@ xǆǉǍǉǐǓǏ|Ǎ^ǖǓǂǊǔǉǚǐǉǂǎǎǆǅ";+'9Cu- *'M cullanus egyptae sp. nov. (Nematoda, Cucullanidae) infecting ǉǖǃǃ~'M<;"!K ?Anguilla anguilla? [! !6''&&9-*M&9E- ;+'M;M; ǎǊǏ_GǉǊǆǍǆǏǻǏǅǆǓǍǆǎGǂǓǂǔǄǉǆǘǔǌǊ| ǐǏǏǆǆǍǚ ~~ ǄǂǓǕǉǚ Gx 'M! ǍǂǔǄǐ@ǐǔǕǂǂǍǕǼǏǌǐǗǤ]ǆǐǓǈǊǆǗǂ""ǌǊǓǏǊǔǔǐǏ R Bothriocepha- x"ǄǉǐǍǛGxǐǔǕǂǅǊǏǐǗǂ;+'9 lus claviceps]'*<;HJ Arctic Circle: molecular, morphological and ecological evidence |!!E'9;&M9;M >DiplostomumHQQ!@ Qǚǌ 'ME9[K J~99*+&M*'- _!''M'M9HJ

;+'-E;+&& Page 14 of 17 '+'99''F;+'-+&& Moravec and Scholz: Macroparasites of Anguilla anguilla67

Qǚǌ\ǖǄǌǼ'M-E[ xǆǏǏǆǅǚ6ǊǕǄǉQ~1990: Colonization, larval survival and 67T7_$59-*'M-<+HJ epidemiology of the nematode Anguillicola crassus, parasitic in Qǚǌ\ǖǄǌǼ'M-*[ the eel, Anguilla anguilla~&E''*M'&' 67"7$!D' xǆǏǏǆǅǚ 6 ǐǓǊǂǓǕǚ ;++; \@! 7 *'M<;HJ richness and structure of helminth communities in eels, Anguilla Qǚǌ\ǖǄǌǼ'ME&6 anguilla\Q6"~|! !!["7$!D'' *E&'-M&;; -&MEMHJ xǐǅǆǅǐǗǤQǐǍǆȿǆǍQǓǐǖȁǌǐǗǤ~ǊǓǌȳ|ǚǑȪǂ ?ǓǈǆǏǔ6'ME'|![K"! \ǖǌǆȪ~"ǄǉǐǍǛG;+++_ !MK!5<'&*M H?@ 150. (In Czech.) J!'<"6~&+''+MM'''& ?ǓǈǆǏǔ6\ǐǎ~'M*+Q xǐǖǃǌǐǗǤǂǓǖȪ;+++G77HProterorhinus !&<&HJ marmoratus: Perciformes) as paratenic host of the nematode An- ǂǍǕǼǏǌǐǗǤ]ǆǐǓǈǊǆǗǂ"xǐǔǕǂǅǊǏǐǗǂǍǂǔǄǐ@ guillicola crassusHQJ|!&*9&M9- ǐǔǕǂ"ǄǉǐǍǛG"ǌǊǓǏǊǔǔǐǏx;+'9Diplostomum von xǟǊǆ 'M<< ? Anguilla anguilla (L.) !'<&;HQQ!J7@ !QK7$!_ >@ ;MM&M''< " ;<**–<+HJ !';;E

;+'-E;+&& Page 15 of 17 '+'99''F;+'-+&& Moravec and Scholz: Macroparasites of Anguilla anguilla67

ǐǓǂǗǆǄ 'M<+ Cucullanus truttae (Nematoda) in a _ǖǕǆǊǓǂǍ"ǍǗǂǓǆǛǈǍǆǔǊǂǔ6ǂǏǊǂǈǖǂ?"ǂǏ@ !;*;'*M;;E ǎǂǓǕǯǏ\;++;@!@ ǐǓǂǗǆǄ'M<-_! @K"|!&MM'MM* (Anguilla anguillaH\JJ!\$[! ǤǓ_'M<+GK!Bothriocephalus[ $&;''&M';- T&+'*salmon (Salmo salar) after its reintroduction into the guilla anguilla?9-;&&M;&< ?7 6 7 67 -+ "ǂǓǂǊǗǂ ǐǓǂǗǆǄ ǆǓǆǊǓǂ ǓǖǛ ;++;Q@ ;M<–304. velopment of Spinitectus inermis (Nematoda: Cystidicolidae), a ǐǓǂǗǆǄ;++9"!?@ parasite of eel, Anguilla anguilla?9M rope. Academia, Prague, 510 pp. ''! ?!?Anguilla anguil- observations on the development of Anguillicola crassus (Nema@ la, from four disconnected meanders from the rivers Leie and QJ[Anguilla anguilla (Pis@ "K!99';M'< J9''&<–'9< "ǄǉǐǍǛ G 'M!@ Leuciscus cephalus6$6$ ogy of Proteocephalus tapeworms (Cestoda: Proteocephalidae), "!--';–;< K[6@ ǐǓǂǗǆǄ"ǉǆǆǃǂ"xǖǎǂǓ;+';Rhabdochona (Rhab- 9-;*M9& dochona) keralaensis H67J! "ǄǉǐǍǛG|ǂǏǛǆǍǐǗǤ'MM<GK!]Proteo- nematodes in the Indian mottled eel Anguilla bengalensis benga- cephalus'<-<HJ lensis!-**9M<; ?"56;!''< ǐǓǂǗǆǄǌǐǓǯǌǐǗǤ'MM<!7 "ǄǉǐǍǛGxǆǑǓG'M<<G[[K!Pro- insects as new paratenic hosts of Anguillicola crassus (Nematoda: teocephalus macrocephalusH'<;-JH@ QJK!7Q_ J$&-'''M''; &9;'*–;;; "ǄǉǐǍǛGǐǓǂǗǆǄ1990: A record of gravid cestodes Both- ǆǖǎǂǏǏ'M<-"K!!7Anguillicola bei Aalen. riocephalus clavicepsH]'*<;J!KTriturus GK''&;; vulgarisH\JH!7J&*;<&M;<9 ǊǆxǆǏǏǆǅǚ61991a: Population biology of Proteocephalus "ǄǉǐǍǛGǑǂǌǖǍǐǗǤǏǤǃǆǍxǓǤǍǐǗǤ|ǂǏ@ macrocephalusHJ?Anguilla anguilla ǛǆǍǐǗǤ1997: A multidisciplinary approach to the systemat@ H\JK!~&<M;'MM;* ics of Proteocephalus macrocephalusH'<;-JH Ǌǆ xǆǏǏǆǅǚ 6 1991b: Seasonal population dynamics of J"&*'M'; Paraquimperia tenerrimaH\KJH!J? "ǉǆǂǓǔ~xǆǏǏǆǅǚ6;++-GParaquimpe- eel, Anguilla anguilla (Linnaeus) in three localities of southwest ria tenerrima?Anguilla anguilla. ?~&M99'M99M ~|!*M'EMM'*E ǊǆxǆǏǏǆǅǚ6'MM;Bothriocephalus clavi- "ǊǕǌǐ ~ ǂǍǕǼǏǌǐǗǤ "ǄǉǐǍǛ G ;++E $ cepsH]JHJ?Anguilla anguilla G!HQJ"$67@ H\J K ? ~ 9' lics. Academia, Prague, 111 pp. -;'M-&' "ǑǂǖǍ?'M;*_K!Rhabdo- _ǅǆǏǊǏǈx'M*E!@ chona|"M'ME&EME9' ogy. Adv. Parasitol. 14: 1–93. "ǖǓǆǔ"ǕǓǆǊǕ;++'?! 766]!';& '<-M'M'

;+'-E;+&& 'E'* '+'99''F;+'-+&& Moravec and Scholz: Macroparasites of Anguilla anguilla67

ǌǐǓǯǌǐǗǤ"ǄǉǐǍǛGǐǓǂǗǆǄ'MME" ǐǋǕǆǌ~'M*9![$@ monogeneans Pseudodactylogyrus anguillae and P. bini among "`$99'-'&M-';7 679&'--M'-E (In Czech.) ǑǂǌǖǍǐǗǤǂǄǌǐ~xǆǓǓǊǍǍǊQǆǛǇǖǍǊ";++;Q@ ǐǋǕǌǐǗǤ\'M-M7$K scription of Bucephalus anguillae n. sp. (Trematoda: Bucephali@ [6""$"T$~ dae), a parasite of the eel Anguilla anguilla (Anguillidae) from a ?$DD9+'M*M';&HJ 7$K"~<<&<;M&<* ǐǍǇ"ǎǯȪǆǌ~'M--?$K"75 ǓǤǎǆǌ 1901: Helminthen der an der zoologischen Station in $!D;<&M-M9'+HJ 7H!JK ǂǈǆǏǆǓ6'<-<?!7Distoma campanula \!''M9M''< Q5HGasterostoma Sieb.) und Monostoma biparti- GǂǓǂǔǄǉǆǘǔǌǊ|ǐǓǂǗǆǄ\ǂǎǂǕǉGǏǅǆǓǔx'M<* tum;9;-+M;-E Q7!K!@ ǊǍǍǆǎǔǆ~~'ME*G@7K@K ? Anguillicola crassus [K!Proteocephalus. Arch. Neer@ H!QJParatenuisentis ambiguus '*;$!Proteocephalus 1999: Parallel analysis of some heavy metals concentrations in macrocephalus H? J the Anguillicola crassusH!J?An- 9E;*MM;<& guilla anguillaH_J|!&E*MM<' ȄǤǓǔǌǤ ǆǃǆǔǤȦǐǗǤ ~ 'MMM7Q7@ GǷǓǏǒǖǊǔǕ'M&'Q!! K>Proteocephalus Camallanidae nebst weiteren Beiträgen zur Kenntnis der Anato@ macrocephalusHJE9MM-E !|!]7x@ ǊǕȟǂǏ6'M*M|![$ "!|";'M99' Q7! ǐǋǕǆǌ~'ME'|![ !$!! $*<'+M<'9HJ 7$Q'M*M'9<–'E;H 6J

6 ;' ~ ;+'- 'M ;+'- 7 &+ ~ ;+'-

Cite this article as: "G;+'-!!?Anguilla anguilla (Lin@ J67E;+&&

;+'-E;+&& Page 17 of 17