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Some Aspects of the Taxonomy and Biology of Dracunculoid Nematodes Parasitic in Fishes: a Review

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Some Aspects of the Taxonomy and Biology of Dracunculoid Nematodes Parasitic in Fishes: a Review FOLIA PARASITOLOGICA 51: 1–13, 2004 REVIEW ARTICLE Some aspects of the taxonomy and biology of dracunculoid nematodes parasitic in fishes: a review František Moravec Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic Key words: Nematoda, Dracunculoidea, parasites, taxonomy, fish Abstract. The nematode superfamily Dracunculoidea includes 166 recognized species, of which 150 (90%) are parasitic in about 300 species of freshwater, brackish-water and marine fishes. Fish dracunculoids are placed in 31 genera (86% of all dracunculoid genera) belonging to eight of the nine dracunculoid families: Anguillicolidae, Daniconematidae, Guyanemidae, Lucionematidae, Micropleuridae, Philometridae, Skrjabillanidae, and Tetanonematidae; the genus Lockenloia is considered incertae sedis. Because of difficulties in studying fish dracunculoids, associated with their morphological and biological peculiarities, most species of these largely histozoic parasites are poorly known and males of the majority of species and of eight genera have not yet been discovered. It is apparent that the present classification system of dracunculoids as a whole does not reflect phylogenetic relationships and a taxonomic revision of this nematode group, based on detailed morphological (including SEM and TEM), life history and molecular studies of individual species, is quite necessary. Data on the biology of fish dracunculoids is scarce. In known cases, their life cycles involve copepods, ostracods or branchiurids as intermediate hosts and, sometimes, fish paratenic hosts are known to occur in dracunculoid species parasitizing as adults piscivorous definitive hosts. However, nothing is known about the life cycles of representatives of 20 genera. Some species of dracunculoids, particularly of philometrids, are highly pathogenic and are known as agents of serious fish diseases. During recent years, especially the importance of Philometra spp. parasitizing the gonads of many species of marine fishes has increased due in particular to the rapid development of marine aquaculture, because they may significantly decrease fish reproduction or even cause full parasitic castration. Therefore, further detailed studies on fish dracunculoids are significant not only from the theoretical viewpoint, but they may also have practical implications. Nematodes of the superfamily Dracunculoidea Stiles, The hosts of the numerous species of these nema- 1907, which are characterized by certain morphological todes are members of all main classes of vertebrates features and some biological peculiarities, represent a (fishes, amphibians, reptiles, birds, mammals) including large, diverse group of parasites with a worldwide man, but their highest species and morphological diver- distribution. Members are noted for the presence of a sity occurs in fishes. Some species parasitize a wide simple oval or triangular mouth surrounded by a vari- range of hosts, others exhibit a relatively narrow host able number of cephalic papillae usually arranged in specificity. The dracunculoids are mostly parasites of two circles (Fig. 1). The buccal capsule, if present, is various tissues and organ cavities and different species usually reduced (Fig. 2). The oesophagus is largely attack, for example, the skin and subcutaneous tissue, divided into muscular and glandular parts but may be body musculature, eyes, orbits, gills and the swim- entirely muscular (Fig. 3). Two spicules or a sclerotized bladder (in fishes), kidneys, gonads and the circulatory copulatory plate may be present or absent (Fig. 4). Most system, or are found in the body cavity of the host forms are viviparous. After fertilisation, females grow (Ivashkin et al. 1971, Chabaud 1975, Moravec 1994). markedly as first-stage larvae fill their uteri. In some The dracunculoid life cycles involve aquatic crusta- groups the vulva and anus atrophy in fully gravid ceans (copepods, ostracods or branchiurids) as inter- females and larvae are dispersed into the environment mediate hosts and, consequently, the transmission and by bursting as they come in contact with water, whereas the occurrence of these parasites in vertebrate definitive in others their larvae are released into the tissues. Many hosts is always associated with the aquatic environment. dracunculoids exhibit marked sexual dimorphism in Therefore, it is not surprising that the absolute majority which females are highly modified and considerably of dracunculoids is found in fishes, both freshwater and larger than the males. The body size of gravid females marine. Of the nine dracunculoid families, eight (89%) in different species ranges between 1 mm in Lucionema include the forms from fishes, whereas the family balatonense from European pikeperch to more than 1 m Dracunculidae Stiles, 1907 contains a few species in Philometra sp. from wreckfish (pers. comm. of C.J. This paper was presented at the 6th International Symposium on Fish Fennesy, Virginia Institute of Marine Science, USA). Parasites in Bloemfontein, South Africa, 22–26 September 2003. Address for correspondence: F. Moravec, Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic. Phone: ++420 387 775 432; Fax: ++420 385 310 388; E-mail: [email protected] 1 parasitic in amphibians (species of the monotypic Besides the practical importance of fish dracuncu- genera Kamegainema Hasegawa, Doi, Araki et Miyata, loids as pathogens, this nematode group represents a 2000 and Protenema Petter et Planelles, 1986), birds significant experimental group for testing theoretical (species of Avioserpens Wehr et Chitwood, 1934) and questions concerning the host – parasite relationships, reptiles and mammals (members of Dracunculus morphological adaptations to parasitism, biology, eco- Reichard, 1759); the Micropleuridae Baylis et Daubney, logy, zoogeography and phylogeny of these parasites 1926 contains four species of Micropleura Linstow, and their fish hosts, as also some questions of general 1906 from reptiles and two species of Granulinema biology. Moravec et Little, 1988 from fish (sharks) (Muller 1971, In view of their unusual location in the host’s body Petter and Planelles 1986, Moravec and Little 1988, and some morphological, physiological and biological Moravec et al. 1998a, 2004, Hasegawa et al. 2000). Of a peculiarities, the majority of dracunculoids remains total number of 36 valid genera of dracunculoid nema- poorly known and the classification within this parasite todes with 166 recognized species, 31 (86%) genera with 150 (90%) species are found in fishes. group is, besides trichinelloids, one of the most difficult According to Moravec et al. (1998a), the following and unsatisfactory in the Nematoda (Anderson 2000). dracunculoid families include adult forms from fishes: Anguillicolidae Yamaguti, 1935 (1 genus, 5 species), TAXONOMY AND CLASSIFICATION Daniconematidae Moravec et Køie, 1987 (3 genera, 4 The first fish dracunculoid was described by Zeder species), Guyanemidae Petter, 1975 (5 genera, 9 spe- (1803) as Filaria ovata (= Philometra ovata) from cies), Lucionematidae Moravec, Molnár et Székely, European cyprinids. During the 19th and especially 20th 1998 (1 genus, 1 species), Micropleuridae Baylis et century, the number of nominal philometrid species Daubney, 1926 (1 genus, 2 species), Philometridae Baylis et Daubney, 1926 (12 genera, 115 species), rapidly increased, but the identification of many of them Skrjabillanidae Shigin et Shigina, 1958 (4 genera, 7 remained questionable (Ivashkin et al. 1971). Most species), and Tetanonematidae Skryabin et Shikho- species descriptions were based solely on large-sized balova, 1948 (1 genus, 1 species); the monotypic dra- females, whereas conspecific males remained unknown cunculoid genus Lockenloia Adamson et Caira, 1991 because they often are very small, have a rare or tempo- with L. sanguinis Adamson et Caira, 1991 from sharks rary occurrence in the host, and usually locate in differ- has not been assigned to any family and is considered ent host tissue than the gravid female. incertae sedis. In the past, the majority of philometrids were as- The present author does not consider useful to pro- signed to the generally recognized genus Philometra vide a key to the families and genera of Dracunculoidea Costa, 1845. In 1963, Rasheed carried out a detailed or to list valid dracunculoid species in this paper, be- revision of members of this genus and, in attempt to cause important taxonomic changes are expected soon, make species identification easier, she created a taxo- as indicated by contemporary studies. The Dracunculoi- nomic system of Philometridae based principally on the dea will be dealt with in detail in the author’s mono- female morphology. Taking into account certain genera graph intended to be published within two next years. established by previous authors (Philonema Kuitunen- Dracunculoid nematodes are widely distributed Ekbaum, 1933, Ichthyofilaria Yamaguti, 1935, Philo- among freshwater, brackish-water and marine fishes, metroides Yamaguti, 1935, Nilonema Khalil, 1960, being reported from at least 300 fish species, belonging Rumai Travassos, 1960), she proposed two more new to 84 fish families and 25 orders. Some of them are genera, Buckleyella and Thwaitia, and a few new sub- highly pathogenic and are known to be agents of serious genera. diseases of fish with economic importance, where they The system of Rasheed (1963) is based
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