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

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1 Institute of Parasitology, Biology Centre CAS doi: Research Article Macroparasites and their communities of the European eel Anguilla anguilla (Linnaeus) in the Czech Republic František Moravec and Tomáš Scholz Abstract: Anguilla anguilla (Linnaeus) in the 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 ecological conditions. The parasite fauna of A. anguilla nematode Cucullanus egyptae as a species inquirenda. Keywords: nematode Anguillicoloides crassus (Kuwahara, Niimi et of eels Anguilla anguilla there were few helminthological studies on this species A. crassus, an agent of anguil licoloidosis, has seriously endangered both eel cultures with the problem of anguillicoloidosis, an increased inter est to study the parasite fauna of eels as a whole has also data on its parasite fauna are scarce, mostly published in of some helminth species parasitising eels (Moravec 1975, ogy and ecology of endohelminths parasitising eels in the otic species of helminth parasites, the nematode A. crassus and the monogeneans Pseudodactylogyrus anguillae (Yin P. bini This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

2 Table 1. List of the localities from where eels, Anguilla anguilla No. Locality Year(s) and month(s) Pond Pohorka near Lišov Within broad investigations on the helminth parasites of of the Institute of Parasitology, Czech Academy of Scienc es (previously the Czechoslovak Academy of Sciences), tained remain unpublished, even though they represent im portant information about the species composition of the tion of individual species and the diversity of their com munities in different localities. Based on the high number the most comprehensive studies on the parasites of this MATERIALS AND METHODS tions of eels Anguilla anguilla from the territory of the Czech emy of Sciences (previously the Czechoslovak Academy of Sci

3 Fig. 1. Table 1). belong to all of the three main river drainage systems in the Czech alive to the laboratory, where they were immediately killed and The parasites obtained were treated by usual helminthologi cal methods and these materials are mostly deposited in the Helminthological Collection of the Institute of Parasitology, group. RESULTS Composition of the fauna of macroparasites of Anguilla anguilla in the Czech Republic A total of 31 species of macroparasites was found in Gyrodactylus sp., Crepidostomum metoecus (Braun, 1900), Diplostomum spathaceum Cucullanus truttae Fabricius, 1794, Porrocaecum ensicaudatum Echinorhynchus truttae Argulus foliaceus Monogenea Gyrodactylus lucii Kulakovskaya, 1951 This is a parasite of Esox lucius Linnaeus and some G. lucii was found on this represents an accidental infection. Gyrodactylus sp. Numerous live and dead specimens of this parasite were A. anguilla is only an acciden tal host for this parasite. Pseudodactylogyrus anguillae and P. bini P. anguillae alone was recorded Page 3 of 17

4 Table 2. Occurrence of macroparasites in Anguilla anguilla (Lin ditional records from other countries are given in parentheses). Parasite Basin Basin Gyrodactylus lucii Gyrodactylus sp. Pseudodactylogyrus anguillae Pseudodactylogyrus bini Azygia lucii Crepidostomum metoecus Diplostomum spathaceum larv. (Metagonimus yokogawai larv.) Bothriocephalus claviceps Proteocephalus macrocephalus Triaenophorus nodulosus Anguillicoloides crassus Camallanus lacustris Camallanus truncatus Cucullanus truttae Daniconema anguillae (Hedruris androphora) Paraquimperia tenerrima Raphidascaris acus Salmonema ephemeridarum Spinitectus inermis Eustrongylides mergorum larv. Porrocaecum ensicaudatum larv. Acanthocephalus anguillae Acanthocephalus lucii Echinorhynchus truttae Neoechinorhynchus rutili (Paratenuisentis ambiguus) Pomphorhynchus laevis Piscicola geometra Glochidium gen. sp. larv. Ergasilus gibbus (?) Ergasilus sieboldti Argulus foliaceus Hydrozetes sp. Ergasilus gibbus Pseudodactylogyrus bini alone was found in P. anguillae and P. bini in the following Bohemian localities, where the propor tions of both species in samples were similar: Mácha Lake recorded in previous years) (prevalence of both species P. anguillae alone was re However, the presence of these parasites in other locali monogenean infections of eels in some localities. Both P. anguillae and P. bini are pathogenic gill para Anguilla japonica Temminck et A. anguilla both P. anguillae and P. bini are widespread in eel popula els of infection with P. anguillae and P. bini. The situation Trematoda Azygia lucii This trematode was found in the stomach of eels in two 9). Azygia lucii was previously reported from eels in the A. lucii is the northern pike, Esox lucius as a subsidiary host. It may be supposed that A. anguilla small pike and perch. The occurrence of A. lucii in eels seems to be in correlation with the feeding period of the Page 4 of 17

5 A. lucii was not re corded. In addition to A. anguilla, Linnae us and Sander lucioperca (Linnaeus) were also recorded as subsidiary hosts of A. lucii A. lucii are various species of freshwater snails of the fami Crepidostomum metoecus (Braun, 1900) The only locality where this trematode was found in the C. metoecus are salmonids, Salmo trutta fario Lin Esox lucius Lota lota (Linnaeus) (Lotidae) or viatilis tion of adult trematodes while feeding on small salmonids C. metoecus in A. anguilla suggests a similar way of transmission, i.e. that the fected trout. In the same locality, C. metoecus was recorded S. trutta fario C. metoecus are bivalves (PisidiumGammarus pulex Ephemera Linnaeus, Cloeon Leach, Siphlonurus Diplostomum spathaceum Metacercariae of this trematode located in the eye lens of eels were recorded from the following localities belong ing to two main river drainage systems. D. spathaceum are common intestinal parasites of gulls (Larus spp.) and are ate host is the freshwater snail Lymnaea (Radix) peregra ovata ferent families (rarely also frogs) serve as the second in D. spathaceum cies (mainly cyprinids) in the former Czechoslovakia, but not from A. anguilla these parasites in eels represent a new host record. Taxonomic note:diplostomum studies that combined molecular and morphological data have revealed cryptic diversity in the Diplostomum species be that metacercariae from eels reported under the name D. spathaceum actually belong to more than one species of Diplostomum. Cestoda Bothriocephalus claviceps This cestode was recorded from eels in the following lo calities belonging to all three main river drainage systems: Page 5 of 17

6 Bothriocephalus claviceps was previously reported The present data show that B. claviceps is a common in eels all the year round. Although it is also present in B. claviceps eels and A. anguilla has so far been recorded as the only Bothriocephalus claviceps hosts (Scholz 1997). In this connection, it is necessary to B. claviceps from Triturus vulgaris (Linnaeus) 1990). However, no oncosphere development was observed these cestodes in their atypical amphibian host (newt). The source of B. claviceps infection for eels are either population biology of this cestode in eels of the Mácha who found that the highest values of prevalence and mean B. claviceps be small perch, B. claviceps the maturation cycles of B. claviceps local ecological factors, may be very different in other lo er months or nearly throughout the year in different locali Proteocephalus macrocephalus This species was recorded from the following localities present data indicate that P. macrocephalus is a common curring in eels mainly in larger rivers, water reservoirs and also found in some other localities. Anguilla spp.). The source of P. macrocephalus infection for eels are probably both infected copepod intermediate hosts It can be assumed that P. macrocephalus, as most other nounced seasonal maturation cycle, but no detailed data on the population biology of this species are available. Ac cording to Nie and Kennedy (1991a), growth and matu ration of P. macrocephalus occurred in early summer in

7 P. macrocephalus in A. anguilla ture worms during all months, with the highest numbers in Triaenophorus nodulosus the intestines of eels only twice in two localities belonging P.viatilis) harbouring the cestode plerocercoids and serving as the second intermediate host of T. nodulosus. Larval T. nodulosus in A. anguilla was previously reported by given) (see also Macko et al. 1993). Nematoda Anguillicoloides crassus Kuwahara, Niimi et Itagaki, 1974 This swimbladder nematode was recorded from the fol lowing localities belonging to two main river drainage sys tems. This pathogenic parasite of eels was introduced from many that belong to three main river drainage systems, A. crassus found in some other localities including those belonging The life cycle of A. crassus involves a copepod or os A. crassus infec A. crassus Camallanus lacustris This species was found in eels only in localities belong The nematode C. lacustris parasitises predominantly, whether the infective larvae of C. lacustris may develop further and attain maturity in A. anguilla, but eels often harboured gravid (larvigerous) females of this parasite. In C. lacustris prevalence and mean intensity markedly increased with the body size length. The intermediate hosts of C. lacustris are vari source of C. lacustris Page 7 of 17

8 hibit a pronounced seasonal cycle of maturation (Moravec Camallanus truncatus This species was found only in localities belonging to C. truncatus seem to Sander Oken (S. lucioperca and S. volgensis Similarly to C. lacustris, C. truncatus also occurs in many The intermediate hosts of C. truncatus are various spe main source of infection for eels. Cucullanus truttae Fabricius, 1794 Adults of this species (including ovigerous females) were recorded from eels in one locality belonging to the Cucullanus truttae is an intestinal parasite of salmonids, Salmo trutta fario. or Lota lota, which probably act only as postcyclic hosts (Moravec C. truttae was recorded from eels only C. truttae infection secondarily while occasional preying The intermediate hosts of C. truttae are larvae of dif brook lamprey Lampetra planeri (Bloch). However, after the metamorphosis of infected lampreys, the development of C. truttae larvae continues further in adult lampreys, in which the nematodes attain their full maturity and may C. truttae in the included ovigerous females, it is almost certain that the source of infection for eels was infected adult lampreys. C. truttae Daniconema anguillae This parasite of the serosa of swimbladder and intes tine of eels was recorded from the localities belonging to Daniconema anguillae is a Holarctic parasite of eels, occurring only in A. anguillaa. rostrata but it may be similar to that in the nematodes of the family sucking branchiurids (Argulus spp.), which may be also the source of D. anguillae larvae of D. anguillae occur, sometimes in considerable of infected eels (Molnár and Moravec 1994, Molnár and Paraquimperia tenerrima This nematode was recorded from the following locali ties: A. anguilla P. tenerrima seasonal cycles of occurrence and maturation (Chubb 1975, P. tenerrima ber and always gravid females with eggs were also present. The life cycle of P. tenerrima

9 serve as intermediate or paratenic hosts (Moravec 1975, Raphidascaris acus (Bloch, 1779) Adults of R. acus and larvae in the intestinal lumen of eels were found in the following localities belonging to one main river drainage system. Raphidascaris acus is a common and widespread para hosts of R. acus Esox lucius and the brown trout Salmo trutta fario, less often other species of salmonids, Lota lota,, Sander lucioperca or Anguilla anguilla R. acus larvae from a single eel The intermediate hosts of R. acus species and, in some localities, also amphipods of the ge nus Gammarus Fabricius, which are the source of infection intermediate paratenic hosts of R. acus, of which the lat R. acus (including ovigerous females) were recorded in eels only during late spring and early autumn, whereas samples collected in other seasons com responds to the pronounced seasonal maturation cycle of R. acus Salmonema ephemeridarum This nematode was found in an eel only once in a lo The nematode S. ephemeridarum is a stomach parasite Salmo trutta fario parasite is sometimes found in other, mostly predatory or S. ephemeridarum, i.e. small salmonids. Also in the present case, ap S. ephemeridarum infection secondarily by occassional preying upon small trouts. The intermediate hosts of S. ephemeridarum are dif Cottus gobio Linnaeus, Barbatula barbatula Spinitectus inermis This nematode was found in one locality belonging to 1). Spinitectus inermis A. anguilla. It occurs only locally and is a rather rare parasite of eels in most localities. The inter Eustrongylides mergorum Larvae of this parasite were recorded from the stomach E. mergorum ratenic hosts. Larvae of E. mergorum were reported from Porrocaecum ensicaudatum Larvae of this species were found in the intestinal lu 1994: 1/7, 3). Larvae of P. ensicaudatum were previously recorded from the intestine and pyloric caeca of Salmo trutta fario various birds mainly of the family Turdidae. It can be sup es after ingestion of their intermediate hosts, earthworms. culation of this parasite in the environment. Page 9 of 17

10 Acanthocephala Acanthocephalus anguillae This acanthocephalan is reported from many species of preferred hosts seem to be numerous cyprinids (Moravec A. anguillae A. anguillae The life cycle of A. anguillae involves the intermediate host, Asellus aquaticus Linnaeus (Isopoda), in which the infective larval stage, the cystacanth, develops (Moravec A. anguillae infection for eels may be also paratenic) hosts. Acanthocephalus lucii This acanthocephalan species was recorded from eels in all of the three main river drainage systems. 5 1 This acanthocephalan occurs in many species of fresh ing on macrobenthic invertebrates, belonging to different seems to be (see A. lucii was previously reported from all three main river drain The life cycle of A. lucii involves an intermediate host, the freshwater isopod Asellus aquaticus (see Moravec fected intermediate host isopods (A. aquaticus) or prey P. ) harbour ing these parasites. Echinorhynchus truttae Adults of E. truttae are found mainly in the intestine and pyloric caeca of various salmonids, but also in some of this acanthocephalan are amphipods of the genera Echinogammarus Stebbing, Gammarus, Pontoporeia Kohlm and Pallasea E. truttae Gammarus fossarum source of E. truttae infection for eels are probably both the intermediate hosts (mainly Gammarus spp.) harbouring small trouts) which may become a prey for larger eels. Neoechinorhynchus rutili This species was recorded from localities belonging to two main river drainage systems. This acanthocephalan species is a widely distributed Holarctic parasite mainly of various cyprinids, but it fre N. ru- Page 10 of 17

11 tili Like in other congeneric species, the life cycle of N. rutili of Ostracoda, whereas some other invertebrates (leeches, observed, may apparently serve only as paratenic hosts ratenic or postcyclic hosts of N. rutili. It can be assumed that eels become infected with this acanthocephalan main Pomphorhynchus laevis This acanthocephalan species was recorded from eels Pomphorhynchus laevis was previously reported from eels of this locality by Moravec and Scholz (1991a,b). ferent families, but mainly in cyprinids. The life cycle involves an intermediate host, gammarids of the genera Echinogammarus, Gammarus, Pontogammarus Sowinsky and Corophium P. laevis infection either by feeding on gammarid interme diate hosts harbouring cystacanths or by preying on smal Hirudinea Piscicola geometra This species was occasionally found on eels in Mácha cies belonging to different families. Bivalvia Glochidium gen. sp. larv. der Unioida Stoliczka occurring as ectoparasites on many Anodonta cygnea Copepoda Ergasilus sieboldi casionally recorded from eels in 1975 basin). Ergasilus gibbus A. anguilla E. gibbus is able that, in this case, E. sieboldi E. gibbus. Branchiura Argulus foliaceus This temporary ectoparasite was found on eels in two former locality, a rare occurrence of A. foliaceus on eels A. foliaceus occurs on the skin Acariformes Hydrozetes sp. This ectoparasite was recorded on gills of an eel in the A. anguilla recorded in the present study roughly divided into the following groups: Anguilla Pseudodactylus anguillae and P. bini, the cestodes Bothriocephalus claviceps and Proteocephalus macrocephalus, and the nematodes Paraquimperia tenerrima, Anguillicoloides crassus, Daniconema anguillae and Spinitectus inermis. other families: the monogeneans Gyrodactylus lucii and Gyrodactylus sp., the cestode Triaenophorus nodulosus, the trematodes Azygia lucii and Crepidostomum metoecus, the nematodes Camallanus lacustris, C. truncatus, Cucullanus truttae, Raphidascaris acus and Salmonema ephemeridarum, the acanthocephalans Acanthocephalus anguillae, A. lucii, Echinorhynchus truttae, Neoechinor- Page 11 of 17

12 hynchus rutili, and Pomphorhynchus laevis, the hirudinean Piscicola geometra, the crustaceans Ergasilus sieboldi and Argulus foliaceus, and the acariform Hydrozetes sp. Since the present knowledge of the biology of most of cycles remains unknown. It can be only assumed that for some of them (Azygia lucii, C. truttae, R. acus, N. rutili, A. anguillae, A. lucii, E. truttae, P. laevis, P. geometra, E. sieboldi and A. foliaceus by these parasites are obtained secondarily, upon feeding sites A. anguilla probably serves only as a postcyclic host (C. metoecus, C. lacustris, C. truncatus and S. ephemeridarum (T. nodulosus) or an accidental facultative host (G. lucii, Gyrodactylus sp.). serving either as intermediate hosts (D. spathaceum, Glochidium sp.), paratenic hosts (E. mergorum) or accidental facultative hosts (P. ensicaudatum). A comparison of these groups shows that although Anguilla spp., a great interest that there is no trematode species among the eight and four nematodes) and that three of them (P. anguillae, P. bini and A. crassus) represent introduced species. for Anguilla Spinitectus inermis), neighbouring countries. In contrast, only one parasite spe Anguilla spp. (Bothriocephalus claviceps) was re with the fact that eels rather rarely occur in this drainage Cucullanus truttae salmonids, but not from eels in the two other river basins, where C. truttae Parasite communities of A. anguilla in different localities It is well known that the formation of the parasite fauna ronment, whereas the effects of others are manifested only fect of many factors enabling its sometimes complicated developmental cycle to be completed. Therefore, an evalu term observations. However, in this study, the numbers of impossible to make a reliable comparison of the parasite the localities investigated. Nevertheless, the results obtained indicated marked dif ferences in the numbers of parasite species recorded from near Postoloprty (13 species each). Ten species of parasites dec. No parasites were recorded from eels in seven other ties. However, the species composition of parasites of eels was usually different even if the same or similar numbers of these organisms were recorded from eels in different P. anguillae, P. bini, P. macrocephalus, P. tenerrima, A. crassus, C. lacustris and A. foliaceus), only three (A. crassus, P. tenerrima and C. lacustris (C. metoecus, C. truttae and N. rutili) occurred, which were Brook share the environment with the brown trout (Salmo trutta fario) (C. metoecus and C. truttae are common para sites of salmonids), whereas no salmonids probably occur uted species was the tapeworm B. claviceps recorded from widely distributed were also the tapeworm P. macrocepha-

13 lus and the nematode P. tenerrima, recorded from 14 and A. crassus tode S. inermis was found in a single locality (Mácha Lake D. anguillae only in sites found in eels mostly depended on the character of the ment. within a given locality and between different localities, were not considered as they would be misleading. DISCUSSION Anguilla anguilla have been intensively studied, mainly during re lished dealing with these parasites and their communities cies of macroparasites were known to occur in eels from within the whole range of A. anguilla, may be estimated to be around 100. The number (31) of parasite species re corded from eels in the freshwater localities of the Czech recorded in freshwater localities in other countries, where about 10 (see e.g. Borgsteede et al 1999 for survey). The highest number (35) of macroparasites of eels was reported steede et al. 1999). Since the species composition of the parasite fauna of in the same localities (see above), the most interesting and eels (Anguilla spp.). It has been mentioned above that eight Rhabdochona anguillae cause other Rhabdochona may be accidentally found in A. anguilla serving as a post cyclic host (e.g. R. paski Rhabdochona anguillae seems to be re phologically very similar species, R. keralaensis Moravec, Anguilla bengalensis Acanthocephalus rhinensis from A. anguilla other hosts of this acanthocephalan remain unknown, be cause of its rarity in eels from the type locality, Amin et al. A. anguilla is only an accessory host that may play a marginal role in the circulation of this para site in the environment. Therefore, A. rhinensis cannot be onomy of some species of Acanthocephalus Koelreuther, 1771 and Echinorhynchus A. rhinensis needs localities, represented by the monogenean Gyrodactylus anguillae Deropristis in- Bucephalus anguillae Goezia anguillae Paratenuisentis ambiguus and the cope pod Ergasilus gibbus. It may be that also the nematode Cucullanus egyptae cently described from A. anguilla from off the coast of the not clearly distinguished by morphometrical features from species inquirenda. Taxonomic note: a new trematode species, Bucephalus anguillae (Bu cephalidae) from A. anguilla was also reported from eels in the coastal lagoons of Tuni G. Perca sp. and Sander sp., which was synonymised with Bucephalus polymorphus (A. anguilla) in northern Italy (Padova) near the Adriatic A. anguilla trematode species, one acanthocephalan species and one or copepods occurred in eels from freshwater localities. Of Page 13 of 17

14 one (P. ambiguus variable in different localities and mostly depends on the paratenic hosts. This group of parasites is highly variable as to the species composition, which differs considerably from one locality to another and with respect to the characteris tics of the environment. In addition to the parasite species parasites were found in this host in freshwater localities in Bunodera luciopercaecrepidostomum farionis (Müller, Nicolla gallica Phyllodistomum folium Sphaerostoma bramae (Müller, Pseudocapillaria tomentosa Philometra cyprinirutili acanthocephalan Acanthocephalus clavula sented by a large number of trematode species (e.g. species of Derogenes Lühe, 1900, Hemiurus Lecithaster Lühe, 1901, Lecithochirium Lühe, 1901, Limnoderetrema Podocotyle nematodes (e.g. species of Cucullanus Müller, 1777 and Hysterothylacium Ward et Magath, 1917), acanthocepha Echinorhynchus spp. and Acanthocephaloides incrassatusgnathia maxillaris Ligula intestinalis (Linnae Diplostomum spp. or the nematode larvae of Contracaecum spp., Cosmocephalus obvelatus (Creplin, Paracuaria aduncaspiroxys contortusstreptocara spp. Adults of all S. contortus maturing in turtles, cestodes (Grillotia atodes, such as Anisakis simplex Hysterothylacium spp. or Pseudoterranova decipiens (Krabbe, marine mammals. desirable to pay further attention to this highly interesting group of parasitic organisms. Acknowledgements. many local representatives of the then State Fishery and the Czech Union of Sport Fishery for their permission to sample the eels. Thanks are also due to many technicians of the Institute of Parasi REFERENCES Bucephalus anguillae Anguilla anguilla (L.). Syst. Cucullanus egyptae sp. nov. (Nematoda, Cucullanidae) infecting Anguilla anguilla Anguilla anguilla, in Acanthocephalus tion of the nematode Anguillicola crassus 1999: Anguillicolosis of the Anguilla anguilla Arctic Circle: molecular, morphological and ecological evidence Diplostomum O.I. Anguilla anguilla 1975: A review of seasonal occurrence and maturation Anguilla anguilla Anguilla anguilla morphologie et de la biologie de Proteocephalus macrocephalus Bothriocephalus claviceps Page 14 of 17

15 150. (In Czech.) Diplostomum von pography and ultrastructure of the tegument of Bucephalus anguillae Anguilla anguilla Diplostomum Anguilla anguilla) population from an Bothriocephalus claviceps tif de Bothriocephalus clavicepsanguilla anguilla Bothriocephalus claviceps Anguilla anguilla of helminth parasites of eels Anguilla anguilla munities in eels Anguilla anguilla 1990: Colonization, larval survival and epidemiology of the nematode Anguillicola crassus, parasitic in the eel, Anguilla anguilla richness and structure of helminth communities in eels, Anguilla anguilla Proterorhinus marmoratus: Perciformes) as paratenic host of the nematode Anguillicola crassus Anguilla anguilla (L.) of eels Anguilla anguilla in freshwater and marine habitats in Iceland in comparison with other parasite communities of eels in the occurrence of the digenetic trematode Sphaerostoma bramae Anguilla anguilla : 593 Eubothrium crassum 1993: Syn opsis of cestodes in Slovakia I. Cestodaria, Cestoidea: Caryo phyllidea, Spathebothriidea, Pseudophyllidea, Proteocephali M.P. Anguilla anguilla (L.) from three coastal Rhabdochona anguillae Daniconema anguillae sue of eel Anguilla anguilla 1995: Parasitological survey of some im Paraquimperia tenerrimaanguilla anguilla (L.) in Sterliadochona 371 Nat. Acad. Sci. Bohemoslov. Brno 5: : Some remarks on the development of Paraquimperia tenerrima Fac. Sci. Nat. Univ. Purk. Brun., Biol. 5, 4 (Year 1974): 135 Spinitectus inermis parasitic in eels, Anguilla anguilla Bohemoslov. 43: b: Occurrence of the endoparasitic helminths in pike (Esox lucius 193. Page 15 of 17

16 Cucullanus truttae (Nematoda) in a (Anguilla anguilla Anguillicola crassus hosts of Anguillicola crassus Atlantic salmon (Salmo salar) after its reintroduction into the 304. rope. Academia, Prague, 510 pp. 1993: Studies on the development of Anguillicola crassus Kuwahara, Niimi et Itagaki, Parasitol. 40: 39 observations on the development of Anguillicola crassus (Nema Anguilla anguilla (Pis 1997: Metazoan Daniconema anguillae gen. et sp. n., a a: Observations on the biology of Pomphorhynchus laevis 1991b: Occurrence of endohelmiths in chub, Leuciscus cephalus Rhabdochona (Rhabdochona) keralaensis nematodes in the Indian mottled eel Anguilla bengalensis bengalensis insects as new paratenic hosts of Anguillicola crassus (Nematoda: Anguillicola bei Aalen. 1991a: Population biology of Proteocephalus macrocephalusanguilla anguilla 1991b: Seasonal population dynamics of Paraquimperia tenerrima eel, Anguilla anguilla (Linnaeus) in three localities of southwest Bothriocephalus clavicepsanguilla anguilla ogy. Adv. Parasitol. 14: Bothriocephalus Anguilla anguilla (L.) Anguilla anguilla Anguilla anguilla from rivers Rhabdochona anguillaeanguilla anguilla velopment of Spinitectus inermis (Nematoda: Cystidicolidae), a parasite of eel, Anguilla anguilla composition and richness of intestinal helminth communities in the stocked population of eel, Anguilla anguilla, in Neusiedler 1997: Anguilla anguilla, from four disconnected meanders from the rivers Leie and intestinal helminths in perch () from the Mácha perch ( 1 Bothriocephalus claviceps ogy of Proteocephalus tapeworms (Cestoda: Proteocephalidae), Proteocephalus Proteocephalus macrocephalus 1990: A record of gravid cestodes Bothriocephalus clavicepstriturus vulgaris 1997: A multidisciplinary approach to the systemat ics of Proteocephalus macrocephalus Paraquimperia tenerrimaanguilla anguilla. lics. Academia, Prague, 111 pp. Rhabdochona

17 monogeneans Pseudodactylogyrus anguillae and P. bini among scription of Bucephalus anguillae n. sp. (Trematoda: Bucephali dae), a parasite of the eel Anguilla anguilla (Anguillidae) from a 1901: Helminthen der an der zoologischen Station in Anguillicola crassus Paratenuisentis ambiguus 1999: Parallel analysis of some heavy metals concentrations in the Anguillicola crassusanguilla anguilla Camallanidae nebst weiteren Beiträgen zur Kenntnis der Anato (In Czech.) Distoma campanula Gasterostoma Sieb.) und Monostoma bipartitum Proteocephalus. Arch. Neer Proteocephalus macrocephalus Proteocephalus macrocephalus Cite this article as: Anguilla anguilla (Lin Page 17 of 17