Digeneans from Intertidal Molluscs of SW Iceland
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Systematic Parasitology 47: 87–101, 2000. 87 © 2000 Kluwer Academic Publishers. Printed in the Netherlands. Digeneans from intertidal molluscs of SW Iceland Kirill V. Galaktionov1 & Karl Skirnisson2 1White Sea Biological Station, Zoological Institute of the Russian Academy of Sciences, 1 University Embankment, 199034 St. Petersburg, Russia 2Institute for Experimental Pathology, Keldur, University of Iceland, IS-112 Reykjavik, Iceland Accepted for publication 15th November, 1999 Abstract The fauna of digenean daughter-sporocysts, rediae, cercariae and metacercariae infecting molluscs Littorina spp., Onoba aculeus, Nucella lapillus and Epheria vincta has been studied in the Skerjafjordur and Grindavik regions of SW Iceland. In total, intramolluscan stages of 19 digenean species were recorded; 14 of them are new for Iceland and one of them, a microphallid named Cercaria islandica I, was unknown. A description of this new microphallid cercaria is provided. In addition, the identification and separation of the intramolluscan stages of some microphallid, renicolid and echinostomatid species are discussed. Consideration is given to difficulties encountered when identifying digenean species found on the coasts of European countries. Problems have arisen largely because larval and adult stages have been described and named independently and in isolation, synonyms are common and many “definitive” descriptions are inadequate or incomplete. Introduction mandoides Bloch from Icelandic waters. Presumably, future research will reveal additional species. Pioneer work on digeneans in Iceland was carried out Only three projects have been carried out on by Rees (1953), who reported eight species from six larval stages of digeneans in Iceland. Blair (1973) marine fish species caught in trawls off the east coast examined digeneans from freshwater molluscs. San- in 1948. A few years later Brinkmann (1956) pub- nia & James (1977) examined 14 species of in- lished details of digeneans collected in Iceland during tertidal and subtidal molluscs in Eyjafjordur (North 1955 from 18 fish, 16 bird and 2 mammalian species. Iceland) and found intramolluscan stages of seven He also reviewed the 24 digenean species, which he digeneans. Three of these larval stages were un- reported from Iceland at that time. described: Metacercaria margaritae-groenlandicus I Freshwater fishes were examined by Richter (Microphallidae), Cercaria littorinae-saxatilis VI and (1982) at the Institute for Experimental Pathology, Metacercaria nucellae-lapillus (Renicolidae). The University of Iceland. Since then a number of para- others belonged to species distributed widely in the sitological surveys of different final host species have coastal zone of northern Europe: Prosorhynchus revealed digeneans which had not previously been re- squamatus Odhner, 1905 (Bucephalidae), Microphal- ported from Iceland. Five digeneans were recorded lus pygmaeus (Levinsen, 1881) (Microphallidae), from the Arctic fox Alopex lagopus (L.) (see Skir- Renicola thaidus Stunkard, 1964 (Renicolidae) and nisson et al., 1993), eight from the common eider Podocotyle atomon (Rudolphi, 1802) (Opecoelidae). It Somateria mollissima (L.) (see Skirnisson & Jons- should be noted that Sannia & James (1977) sampled son, 1996) and at least five from large gulls Larus only one fjord in North Iceland and, with the exception spp. (Eydal et al., 1998). In addition, Eydal et al. of blue mussels, studied only a comparatively small (1996) reported Prosorhynchoides (Bucephaloides) sample of molluscs. The third investigation was by gracilescens (Rudolphi, 1819) from marine fishes Eydal et al. (1994), who examined the occurrence of and Olafsdottir (1999) reported 12 digeneans from Cryptocotyle lingua (Creplin, 1825) (Heterophyidae) the long rough dab Hippoglossoides platessoides li- in gastropods and marine fishes in coastal areas. 88 The present study continues the above-mentioned investigations. It covers the coast of SW Iceland where intertidal snails were collected from habitats with varying exposures and a wide range of ecological pa- rameters. We provide a list of the species recorded and emphasise descriptions of new microphallid cercariae. We have also revised descriptions of some daughter- sporocysts, rediae and cercariae, which are available in the current literature. Ecological aspects of this study will be considered in the another article (Skirnisson & Galaktionov, in prep.). Materials and methods Molluscs (Gastropoda, Prosobranchia) were collected from 11 intertidal sites in the region of Skerjafjor- dur and Grindavik, SW Iceland during August– September, 1998. Sample analysis took place in the Institute for Experimental Pathology, University of Iceland, at Keldur. The specimens collected were kept in a marine aquarium at 5 ◦C and dissected within 2 weeks of sampling. In each case the shell was removed and the molluscan soft tissues were carefully observed under a stereomicroscope. In total 2,411 intertidal gastropods belonging to six species were studied (Table 1). Digenean daughter- sporocysts, rediae, cercariae and metacercariae from infected molluscs were studied in vivo with a Leitz Di- alux 20B microscope. Photographs were taken with a Leica Wild MPS 32 photomicrography camera. Mea- surements were made on heat-killed specimens in sea-water under light coverglass pressure. Not less than 20 cercariae and daughter-sporocysts or rediae of × each species were measured. Measurements (length Figure 1. Cercaria islandica I. a, cercaria, dorsal view; b, stylet, width) are presented in micrometres with the mean in dorsal view, c, stylet, lateral view. parentheses. descriptions. Cercariae and metacercariae of Para- Results and discussion monostomum chabaudi Van Strydonck, 1965 (Noto- cotylidae), identified by Evans et al. (1997), but earlier The daughter-sporocysts, rediae, cercariae and metac- known as Cercaria lebouri Stunkard, 1932 was also ercariae of 19 digenean species were recorded in recorded and it is possible that they may have been the intertidal molluscs studied (Table 1). Intramol- the same species as Notocotylidae gen. sp. cercariae luscan stages of Microphallus similis (Jägerskiöld, recorded by us from Onoba aculeus (Gould). Unfortu- 1900) (Microphallidae), Cryptocotyle lingua (Creplin, nately, we were unable to study their morphological 1825) (Heterophyidae), Parapronocephalum sym- features in enough detail to establish their species metricum (Belopolskaja, 1952) (Pronocephalidae), with accuracy. The same applies to species of the Parorchis acanthus (Nicoll, 1906) (Philophthalmidae) genus Himasthla Dietz, 1909 taken from Onoba ac- and Podocotyle atomon (Rudolphi, 1802) (Opecoel- uleus. However, we have provided a more thorough idae) were identified directly from their definitive description of all the other digeneans recorded. Table 1. Prevalence (in%) of digeneans in the intertidal snails in SW Iceland. Sample site Skerjafjordur Grindavik Snail species Littorina saxatilis Littorina obtusata Littorina mariae Onoba aculeus Nucella lapillus Littorina saxatilis Littorina obtusata Littorina mariae Onoba aculeus Nucella lapillus Epheria vincta Individuals examined 483 332 92 213 153 416 290 44 112 196 80 Microphallus pygmaeus 4.1 0.9 1.1 4.8 4.1 M. piriformes 1.40.3 1.70.32.3 M. pseudopygmaeus 0.6 0.9 2.2 1.4 0.5 1 1.8 2.5 M. triangulatus 0.3 M. similis 0.8 1.5 1.1 3.6 6.6 Cercaria islandica I 0.3 1.1 1.4 Cercaria littorina saxatilis VII 0.9 3.6 Maritrema linguilla 0.9 1.8 Renicola thaidus 33.3 19.9 Cercaria parvicaudata 0.4 0.5 2.1 Cryptocotyle lingua 2.9 0.3 Parvatrema homoeotecnum 0.4 2.8 4.3 1.4 0.9 Himasthla sp. 0.9 Cercaria littorinae obtusata 4.1 Paramonostomum chabaudi 0.2 0.3 Notocotylidae gen. sp. 1.4 Parapronocephalum symmetricum 0.2 0.3 0.3 Parorchis acanthus 2 3.6 Podocotyle atomon 6.8 1.8 4.3 0.2 6.2 Metacercariae only Renicola sp. 0.6 2.3 1 2.1 6.3 Himasthla sp. 0.2 0.3 89 90 Microphallids of the “pygmaeus”group Cercaria islandica I (Microphallidae) (new (Microphallidae) cercarial form) In this group we have included a number of closely This cercaria was found in Littorina obtusata and in related species in the genus Microphallus Ward, 1901 L. mariae Sacci & Rastelli (Table 1). Vermiform and which have life-cycles devoid of second intermedi- oval daughter-sporocysts 180–570 (370) × 110–220 ate hosts (Galaktionov, 1980, 1983, 1984). In these (180) were recorded in the haemocoel of the diges- species the metacercariae develop within daughter tive gland and the gonad of the hosts. Our observa- sporocysts. Their final hosts are sea ducks (especially tions show that fully formed cercariae leave daughter- common eider) and gulls. Our studies have revealed sporocysts through their birth pores, emerge from their that the previously identified species “M. pygmaeus” molluscan hosts and swim actively in water. The body includes at least four individual species (Galaktionov, of fully formed cercariae is flattened dorso-ventrally 1980, 1983, 1984; Saville et al., 1997). At present it and is an elongate oval in outline when relaxed (Fig- is impossible to say for sure which of these species ures 1a, 2a). The surface is covered with small spines was recorded in Iceland by Sannia & James (1977). which decrease in size from the anterior to the pos- On northern European coasts M. pygmaeus (Levin- terior end of the body. Cercariae measure 103–135 sen, 1881) and M. piriformes Galaktionov, 1983, using (115) long and 48–73 (54) wide at mid-body. The tail periwinkles Littorina spp. as their intermediate hosts, is slightly shorter than the body and measures 88–120 are most widely-distributed (Table 1). Recently a com- (99) long and 8–13 (10) wide at the base. The oral parative morphological analysis of the metacercariae sucker is 28–40 (30) in diameter. The lanceolate stylet of these species was carried out by Saville et al. is slightly bent in dorso-ventral plane (Figures 1b,c, (1997). 2b,c) and measures 15–20 (17) long and 5–6 (5) wide The species Microphallus triangulatus Galak- at the base. tionov, 1984 is always rare. Iceland is not an exception There are 4 pairs of penetration glands (which is to the rule. We found sporocycts containing M. trian- typical for most microphallid cercariae).