Digeneans from Intertidal Molluscs of SW Iceland

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 parameters. 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. 89 3.6 19.9 Onoba aculeus Nucella lapillus Epheria vincta 3.6 1.8 0.3 4.1 0.3 0.3 0.3 0.5 2.1 2.9 0.3 2 33.3 0.9 0.4 2.8 4.3 1.4 0.9 0.2 4.1 0.9 1.1 4.8 4.1 0.6 0.9 2.2 1.4 0.5 1 1.8 2.5 0.4 6.8 1.8 4.3 0.2 6.2 Littorina saxatilis 1.70.32.3 Littorina obtusata Littorina mariae Onoba aculeus Nucella lapillus Littorina saxatilis Littorina obtusata Littorina mariae 1.40.3 0.2 0.3 0.8 1.5 1.1 3.6 6.6 VII 0.9 I 0.3 1.1 1.4 sp. 0.2 sp. 0.9 Prevalence (in%) of digeneans in the intertidal snails in SW Iceland. sp. 0.6 2.3 1 2.1 6.3 Individuals examined 483 332 92 213 153 416 290 44 112 196 80 Podocotyle atomon Metacercariae only Renicola Himasthla Sample siteSnail species Microphallus pygmaeus M. piriformes M. pseudopygmaeus SkerjafjordurM. triangulatus M. similis Cercaria islandica Cercaria littorina saxatilis Grindavik Maritrema linguilla Parorchis acanthus Renicola thaidus Cryptocotyle lingua Parvatrema homoeotecnum Himasthla Cercaria littorinae obtusata Notocotylidae gen. sp.Parapronocephalum symmetricum 1.4 Paramonostomum chabaudi Cercaria parvicaudata Table 1. 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). The ducts of gulatus metacercariae only once in Littorina obtusata the 2 anterior pairs are greatly swollen. In fully formed (L.) (Table 1). cercariae the entire secretory material is contained in The species Microphallus sp. I of Galaktionov the ducts, while the cytons of the glandular cells ap- (1980) (M. pseudopygmaeus Galaktionov, 1980) pear to be degenerate. The medial ducts are folded makes use of a wide range of the first intermediate into 2 loops, while the lateral ducts are folded into hosts, a feature which is very unusual for trematodes. 3 loops. The medial ducts extend posteriorly to the In Iceland intramolluscan stages of this species were middle of the body, while the lateral ducts reach the recorded in Littorina spp., Onoba aculeus and Epheria posterior third of the body. The cytons of the 2 pos- vincta (Montagu) (Table 1). In the Barents Sea, terior pairs of penetration glands are situated at their in addition to the above-named molluscs, daughter- posterior tips. The medial and lateral ducts are rela- sporocysts containing Microphallus sp. I were found tively narrow and are masked (except at their distal in Cryptonatica clausa (Broderip & Sowerby), Mar- regions) by the well-developed ducts of the anterior garites groenlandicus (Gmelin) and M. helicinus glands. The gland-ducts extend dorsally around of (Phipps) (see Galaktionov, 1986). It is most probable oral sucker and open at either side of the stylet. The that Metacercaria margaritae-groenlandicus I Sannia openings of the 2 posterior glands are situated close & James, 1977, identified in M. groenlandicus in Ice- to the stylet tip and those of the 2 anterior pairs are land, is in fact the same species (Galaktionov, 1986). situated posterior to them. In vivo observations of In the case of Microphallus sp. I (M. pseudopygmaeus) cercariae demonstrate that secretory material in the it is hard to tell whether we are dealing with one anterior gland-ducts is in the form of rough grains and species or a group of species which are extremely sim- in the posterior gland-ducts it is in the form of small ilar morphologically. This subject is currently the topic grains. of an on-going investigation. The flame-cell formula is 2[(2+2)+(2+2)]=16. The genital primordium takes the form of a com- pact group of cells in the posterior third of the larva body anterior to the bladder. The alimentary tract 91

Figure 2. Cercaria islandica I. a, cercaria, living specimen from dorsal side, showing penetration glands and stylet; b,c, forebody of a heat-killed specimen, showing dorsal and lateral views of the stylet respectively. Scale-bars:a,50µm; b–c, 10 µm. primordium cannot be distinguished in fully formed Cercaria littorina saxatilis VII Newell, 1986 cercariae under observation in vivo. (Microphallidae) The life cycle of Cercaria islandica I is unknown. The second intermediate hosts are probably intertidal This cercaria was only recorded from Onoba aculeus crustaceans, and the final hosts are birds feeding in (Table 1). Daughter-sporocysts are oval, 117–184 the coastal zone. When compared with microphal- (150) × 100–120 (108). Cercariae (Figures 3a, 4) lid cercariae previously revealed from Littorina spp. occur in smaller numbers than those of the previous (Lebour, 1911; James, 1968a, 1969; Popiel, 1976; species. Body length is 88–108 (96) and body width Stunkard, 1983; Newell, 1986; Irwin et al., 1990; is 38–70 (50). The tail is about the same length as Ching, 1991; etc.), C. islandica I larvae are distin- the body, 85–105 (94) and its width is 7–10 (9). Oral guished by the well-developed ducts of the anterior sucker diameter is 22–28 (26). The stylet is 15–20 pairs of penetration glands. This feature permits iden- (16) long and 3–5 (4) wide at the base. It is lat- tification of these cercariae even in the course of a erally asymmetrical due to a diagnostic projection preliminary study. The stylet of C. islandica I cer- (Figure 3b,c). In fully formed cercariae, rough gran- cariae is similar with that in Cercaria littorina saxatilis ular secretory material is accumulated in the anterior VII Newell, 1986 (see below), but it differs by the regions of the ducts of the 2 anterior pairs of pene- absence of a projection. This projection is a char- tration glands. These ducts are situated dorso-laterally acteristic of Cercaria littorina saxatilis VII Newell, curving around the oral sucker. The posterior regions 1986 and it is clearly visible in side-view (Figure 1c). of the ducts, as well as the cytons, are degenerate It should be stressed that C. islandica I was only by the final stages of larval morphogenesis within the recorded from L. obtusata and L. mariae,anditwas daughter-sporocysts. The cytons of the 2 posterior absent from L. saxatilis (Olivi). pairs of penetration glands contain some small gran- ules and are situated in the middle of the larval body. Their narrow winding ducts terminate as openings on the each side of the stylet tip, anterior to the openings of the 2 anterior gland-ducts. The flame-cell formula is 92

tively. Also, the frontal and lateral profile of the stylet was the same. Perhaps Newell (1986) did not study the lateral profile in fully formed cercariae. Our observations show that the stylet projection is not formed in developing cercariae and that the tegumental glands [also mentioned by Newell (1986)] are still observed but not present in fully formed cercariae (Galaktionov & Malkova, 1994). Juvenile cercariae can swim actively in sea-water and may be easily mistaken for fully formed cercariae. Bearing this in mind, we have not declared our cercariae from O. aculeus (Iceland) as a previously undescribed but have identified them as Cercaria littorina saxatilis VII Newell, 1986. Our own evidence and evidence from the literature would suggest that O. aculeus is the most important first intermediate host for C. littorina saxatilis VII, and infection of L. saxatilis is only occasional. Despite numerous parasitological studies on L. saxatilis from the coasts of the British Isles, this cercaria has never been recorded (James, 1968a, 1969; Irwin, 1983; Matthews et al., 1985; etc.). In the present study, this also was the case. It has, however, been found in 5% of O. aculeus from the Barents Sea (Galaktionov, unpubl. data). De- spite numerous studies on L. saxatilis and L. obtusata, C. littorina saxatilis VII has never been recorded from these molluscs in the Barents Sea or Norwegian Sea (Galaktionov & Bustnes, 1999). It is significant that Newell (1986) recorded C. littorina saxatilis VII only once in an immature snail measuring 3 mm in length. In experiments on the Barents Sea Coast (Galak- tionov, unpubl. data) C. littorina saxatilis VII cercariae penetrated and encysted in the intertidal isopod Figure 3. Cercaria littorina saxatilis VII Newell, 1986. a, cercaria, Jaera albifrons (Leach). Considering the small size of dorsal view; b, stylet, dorsal view, c, stylet, lateral view. this crustacean, it is likely that waders feeding on the intertidal shore may represent the final hosts for this cercaria. 2[(1+1)+(1+1)]=8. The genital primordium is situated between the excretory bladder and the posterior penetration glands cytons. Alimentary tract primordia Maritrema linguilla (Jägerskiöld, 1909) could not be identified. (Microphallidae) Cercaria littorina saxatilis VII was originally identified by Newell (1986) but it should be noted This species was only recorded from O. aculeus (Ta- that his specimens were taken from Littorina saxatilis ble 1). The morphological features and size of the on the Isles of Scilly. The structure and morphom- daughter-sporocysts and cercariae corresponded pre- etry provided by Newell (1986) largely agrees with cisely with those of specimens taken from Littorina the observations recorded by us in Iceland. However, saxatilis from the Isles of Scilly by Newell (1986) some significant differences exist, and, for this rea- (Figure 5). Newell (1986) recorded M. linguilla in- son, we have provided the above description of the fection in L. saxatilis in all the coastal regions which larvae which we identified from Onoba aculeus.Inthe he studied, and sometimes its prevalence reached 31– cercariae studied by Newell (1986) the tail was little 37%. M. linguilla cercariae have also been recorded longer than the body: 110–140 and 80–115, respec- from L. saxatilis on the French coast (Richard, 1976). 93

Figure 4. Cercaria littorina saxatilis VII Newell, 1986, cercaria, living specimen from ventral side, showing penetration glands and stylet. Scale-bar:50µm.

We did not record this species in L. saxatilis in Iceland, which may be explained by speciﬁc ecological conditions in the intertidal zone of the island (Skirnisson, Galaktionov, in prep.). M. linguilla has never been revealed in Littorina spp. or in O. aculeus from the coasts of the Barents Sea and the Norwegian Sea (Chubrik, 1966; Podlipaev, 1979; Galaktionov & Bustnes, 1999; Galaktionov, Figure 5. Maritrema linguilla (Jägerskiöld, 1909). a, cercaria, liv- unpubl. data). Nevertheless, Littorina saxatilis in ing specimens from dorsal side, showing penetration glands and this region sometimes harbours daughter-sporocysts of stylet; b, c, forebody of a heat-killed cercaria, showing dorsal and Maritrema murmanica Galaktionov, 1989, containing lateral views of the stylet respectively. Scale-bars:a,50µm; b–c, both cercariae and encysted metacercariae at different 10 µm. stages of morphogenesis (Galaktionov, 1989). Fully formed cercariae of M. murmanica, which can swim Ligia oceanica (L.). No encystment within daughter- actively in sea-water, and their metacercariae are very sporocysts has been observed (Lebour, 1914; Newell, similar to those of M. linguilla described in the lit- 1986; Benjamin & James, 1987). Analysis of the erature (Deblock & Capron, 1960; Newell, 1986; specimens from Iceland has again demonstrated the Benjamin & James, 1987). However, M. murmanica similarities between M. linguilla and M. murmanica is very different in that it lacks a second intermedi- cercariae. The possibility that they are the one species ate host (Galaktionov, 1989). The second intermedi- which, under some environmental conditions involves ate host for M. linguilla is the intertidal crustacean a second intermediate host and under others does not, 94

Figure 6. Renicola thaidus Stunkard, 1964. a, heat-killed cercariae, ventral view; b, part of tumour-like structure formed by daughter-sporocysts in gonads of infected snails; c, metacercariae, encysted in mantle of snail infected with daughter-sporocysts producing cercariae. Scale-bars:a, 100 µm; b, 500 µm; c, 100 µm. must not to be ruled out. If this is the case, M. linguilla anterior part (up to the lateral projections) to the pos- and M. murmanica should be considered as synonyms. terior part is aproximately 1:1 (Figure 7a,b). There are This problem warrants further investigation. 5 pairs of penetration glands, situated in the forebody. Their ducts pass forward as 2 bundles situated laterally and dorsally to the oral sucker. The lateral bundle has Renicola thaidus Stunkard, 1964 (Renicolidae) 3 ducts which open medially and ventrally to the dor- solateral openings of the 2 medial ducts (Figure 7a). This species was recorded at all sites investigated. It In some specimens the number of ducts in each of the occurred in the predatory mollusc Nucella lapillus (L.) bundles is reversed, as recorded by Stunkard (1964). and its prevalence was higher than that of all the other The intramolluscan stages of R. thaidus from digeneans recorded in Iceland (Table 1). The cercariae N. lapillus in Iceland appear to occur in two forms, (Figure 6a) correspond perfectly to the ﬁrst description the exact status of which remains unknown. In form A by Stunkard (1964). The stylet structure and position the daughter-sporocysts are usually colourless, infect of the penetration gland openings seem to be the most the mollusc’s gonads and form tumour-like structures important diagnostic features. The stylet is compara- (Figure 6b). Cercariae of this form do not encyst in tively small, 8–10 × 2.5–3, the ratio of the length of its the same mollusc. Rather they are released and enter 95

Figure 7. Renicola thaidus Stunkard, 1964, cercaria. a, anterior end Figure 9. Cercaria parvicaudata Stunkard & Shaw, 1931, cercaria. to show openings of penetration glands; b, stylet, dorsal view. a, anterior end to show openings of penetration glands; b, stylet, dorsal view.

Cercaria parvicaudata Stunkard & Shaw, 1931 (Renicolidae)

Daughter-sporocysts of this species were recorded in the molluscs L. saxatilis and L. obtusata (Table 1). They develop in the hemoecoel of the gonads and digestive gland of infected molluscs. Their colour ranged from white to yellow and orange. The cercariae (Figure 8) agree in detail with available descriptions (Stunkard & Shaw, 1931; Stunkard, 1950; James, 1968a). The stylet is slightly larger than that of R. thaidus, 11–13 × 3–4. The ratio of the length Figure 8. Cercaria parvicaudata Stunkard & Shaw, 1931, of the anterior part (up to the lateral projections) to heat-killed cercaria, ventral view. Scale-bar: 100 µm. the posterior part is c. 5:8 (Figure 9a,b). There are 6 pairs of penetration glands, the anterior ducts of which pass dorsally to the oral sucker and, in doing so, form the external environment. Form B daughter-sporocysts a diagnostic loop (Figure 9a). The openings of these are usually orange and occur in the mollusc’s gonads ducts are situated on either side of the stylet. and the digestive gland. Hundreds, or even thousands, Due to the remarkable morphological similarity of cercariae from these daughter-sporocysts encyst in and size parameters of their cercariae, Werding (1969) the infected mollusc (Figure 6c). Nevertheless, the cer- suggested that R. thaidus, Cercaria parvicaudata and cariae can swim and some of them leave the infected R. roscovita (Stunkard, 1932) (the latter two species mollusc. Besides differences in colour and location in use Littorina spp. as the first intermediate hosts) are the host, both form A and B daughter-sporocysts and synonymous. This point of view was not supported cercariae of R. thaidus have the same morphology and by Sannia & James (1977) or Stunkard (1983). Our metrical parameters. studies appear to confirm the validity of, at least, Stunkard (1964, 1983) mentioned that the bivalves R. thaidus. When compared with renicolid cercariae Mytilus edulis (L.), Argopecten irradianus (Lamarck) recorded from Littorina spp., they differ in stylet struc- and Gemma gemma (Totten) acted as second interme- ture and in the number and arrangement of the anterior diate hosts for R. thaidus. Adults were experimentally penetration gland-ducts. grown in gulls. Cercarial encystment in the first inter- It is more difficult to distinguish between R. mediate host was not recorded by Stunkard (1964) or roscovita and C. parvicaudata cercariae. The number Sannia & James (1977). Whether or not these forms of of penetration glands in R. roscovita is reported as R. thaidus have a taxonomic status or are induced by several (Stunkard, 1932), numerous (James, 1968a) host or environmental factors is open to speculation. or indeterminate (Werding, 1969). Stunkard & Shaw (1931) and James (1968a) recorded in C. parvicaudata 6 pairs of penetration glands. Stunkard (1950), when differentiating between these two species, noted that “except for the difference in color of the daughter sporocysts, the two species are almost identical” 96

(p. 142). R. roscovita daughter-sporocysts are lemon sporocyst develops within L. saxatilis and it produces or cream coloured, whereas C. parvicaudata daughter- a primary germinal sac, also known as a metacer- sporocysts are orange (Stunkard, 1950; James, 1968a, caria, which James & Bowers (1967) considered to be 1969). It is doubtful if daughter-sporocyst colour parthenogenetic. It produces parthenogenetic metac- can be adopted as a trustworthy diagnostic feature. ercariae of the second generation, daughter-germinal Daughter-sporocyst and redial colour is determined by sacs. In their turn, these produce metacercariae ca- the presence of β-carotine accumulated in both mol- pable of infecting the final host, the oystercatcher lusc tissues and parasites (Nadakal, 1960). Molluscs Haematopus ostralegus L. This interpretation of the accumulate it when feeding on algae and, conse- P. homoetecnum life-cycle was not supported by Cable quently, daughter-sporocyst and redial colour depends (1965), whose point of view was supported by Ching on the host’s food. Not surprisingly, Werding (1969) (1982) and Pearson (1992). They suggested that life- described white R. roscovita daughter-sporocysts. We cycles of gymnophallids possessing parthenogenetic also recorded some differences in colour of daughter- metacercariae (Gymnophallus australis Szidat, 1962, sporocysts from different specimens of molluscan P. homoeotecnum and C. margaritensis)involvetwo host. In conclusion, it would appear that the only trust- intermediate hosts. In the first host, probably bi- worthy criterion for distinguishing R. roscovita from valves, daughter-sporocysts develop. They produce C. parvicaudata cercariae is the number of penetra- furcocercariae which enter a second mollusc, a gas- tion glands. This is the feature by which we identified tropod or bivalve, to become metacercariae or primary C. parvicaudata in the present study. In order to sep- germinal sacs. The remainder of the developmental arate R. roscovita and C. parvicaudata cercariae, the process follows James’ scheme (1964). This point number of penetration glands in R. roscovita must be of view was confirmed by Galaktionov (1996a) dur- determinated precisely. ing experimental studies on the life-cycle of Cercaria margaritensis (Parvatrema sp.). That work demonstrated that daughter-sporocysts producing mobile fur- Parvatrema homoeotecnum James, 1964 cocercariae infected small intertidal bivalves Turtonia (Gymnophallidae) minuta (Fabricius) which acted as the first intermediate hosts. Perhaps the life-cycle of P. homoeotecnum James (1964) provided morphological details of Par- follows the same pattern. Before this can be con- vatrema homoeotecnum at different stages of its life- firmed, the first intermediate host of this species must cycle within the mollusc L. saxatilis. In our sam- be identified. ples, daughter-germinal sacs (the term applied by James, 1964) were recorded from L. saxatilis,as well as L. obtusata and Onoba aculeus (Figure 10a). Cercaria littorinae obtusatae Lebour, 1911 Mature daughter-germinal sacs contain only fully (Echinostomatidae) formed metacercariae. Young specimens contain germinal balls, furcocercariae and different developmen- Rediae containing cercariae of this species were only tal stages of metacercariae. Morphological features recorded in L. obtusata from Grindavik (Table 1). The and size parameters of the metacercariae correspond rediae are white, and mature specimens, producing perfectly to those given by James (1964). This proves cercariae, are 1000–2200 long by 240–550 wide. The that the organisms in question are P. homoeotecnum. redial pharynx is small, 67–87 in diameter, and the The species most likely to be confused with P. ho- alimentary tract is short and stretches a little past the moeotecnum is Cercaria margaritensis Ching, 1982. level of the birth pore (Figure 11a). The birth pore is Germinal sacs of C. margaritensis have been recorded situated in a small protuberance on the anterior region from the intertidal gastropod Margarites spp. (Ching, of the redial body. 1982; Galaktionov, 1996a). Our experience would The shape of cercariae is typical of those of Hi- suggest that intramolluscan stages of P. homoeotec- masthla spp. (Figure 11b). The body is 460–770 (556) num are easily distinguished from C. margaritensis by long and 130–240 (170) wide. The collar has 29 the presence of a pronounced tail stem in developing spines; two terminal spines, which are at a lower level furcocercariae (Figure 10b). on each side, are shorter (8) than the others (10) (Fig- According to James (1964), the P. homoeotec- ure 11c). The tail is 350–570 (426) long and 30–50 num life-cycle involves a single intermediate host. A (39) wide, and the oral and ventral suckers are 50–71 97

Figure 10. Parvatrema homoeotecnum James, 1964, photographs of living specimens. a, mature daughter germinal sac (metacercaria of the second parthenogenetic generation) contain fully formed metacercariae which are invasive to deﬁnitive host; b, different stages of cercaria and metacercaria development within the daughter germinal sac. Abbreviations: c, caecum; dc, developing cercaria; dm, developing metacercaria; m, fully formed metacercaria; os, oral sucker. Scale-bars: a, 100 µm; b, 50 µm.

Figure 11. Cercaria littorinae obtusatae Lebour, 1911. a, redia, living specimen; b, cercaria, ventral view of living specimen; c, forebody of heat-killed cercaria, showing collar spines. Abbreviations: bp, birth pore; c, caecum; p, pharynx. Scale-bars: a–b, 200 µm; c, 10 µm. 98

(58) and 75–105 (88) in diameter, respectively. The cum did not extend to the mid-body. Absence of colour pharynx is elongate and 25–46 (34) × 16–30 (21). in the redia is an additional helpful feature, as H. elon- Ascending branches of the main excretory canal form gata rediae are usually orange (Lebour, 1911; James, 10–15 conjugate branches between the ventral sucker 1968a; Werding, 1969). In conclusion, it should be and the pharynx on each side. noted that C. littorinae obtusatae was only recorded Lauckner (1983, p. 700) stated that “...the situ- from L. obtusata, even though many more L. saxatilis ation regarding specific determinations in the genus than L. obtusata were dissected in Grindavik (Table 1). Himasthla is chaotic, particularly with respect to the Significantly, both Lebour (1911) and Chubrik (1966) larval forms”. Due to extreme morphological similar- recorded C. littorinae obtusatae from only L. obtusata. ity between representatives of this genus at all stages Many features described in the available morpho- of their life-cycles, this remains true today. Among metric data (Lebour, 1911; Stunkard, 1966; Werding, those species using littorinids as their first intermedi- 1969) for H. elongata, H. littorinae and C. littorinae ate host, H. elongata (Mehlis, 1831) (see Stunkard, obtusatae cercariae practically overlap. C. littorinae 1966; Loos-Frank, 1967; Werding, 1969; Lauckner, obtusatae differs from H. littorinae in that it has larger 1980, 1983; etc.) is the most studied. Its cercariae have collar spines: its large spines are 17 long and its small often been misidentified as H. leptosoma (Creplin, corner spines are 11 long (Stunkard, 1966). There 1829) (for references see: Lauckner, 1983). Neverthe- is no information about the size of collar spines for less, H. leptosoma is a different species (Loos-Frank, H. elongata cercariae. According to one illustration 1967), and, according to Sellin (1970; cited after De- (figure 12, p. 315 in Werding, 1969) all spines are the block, 1980), its first intermediate host is Hydrobia same size. This appears to contradict information from ulvae (Pennant). It is, on the other hand, possible that Lebour (1911) and James (1968a), who pointed out H. elongata and H. secunda Nicoll, 1906 are syn- that the two spines at each end of collar, which are on onyms. Echinostomatid rediae and cercariae identified a lower level, are much shorter than the others. Un- as H. secunda were originally identified in Littorina like the first description of C. littorinae obtusatae by littorea (L.) (see Lebour, 1911). Lebour (1911), the tails of the cercariae of this species, In addition to H. elongata, intramolluscan stages which we observed, exceeded half of the body length. of Cercaria littorinae obtusatae Lebour, 1911 (see It should be remembered that our measurements were Lebour, 1911; Chubrik, 1966) and H. littorinae carried out on heat-killed specimens and this could Stunkard, 1966 develop inside littorinids. James be responsible for the difference. In living larvae, the (1968a) proposed an identification key for rediae and length of the contracted tail is approximately half of cercariae of these species. Unfortunately, the features the body length. which James (1968a) used did not always correspond to the earlier descriptions. For example, James (1968a) noted that the caecum of H. littorinae rediae did not Concluding remarks extend to the mid-body, whereas Stunkard (1966) noted that it extended more than one-half the length There have been very few recent studies on the fauna of body. According to James (1968a), the caecum of of intramolluscan stages of digeneans in marine mol- C. littorinae obtusatae rediae extended to the mid- luscs. This applies to all European coasts and it is body and this disagrees with Lebour’s data (1911), illustrated by the fact that the present study adds 14 which especially stressed that it did not extend to the species to the fauna of larval stages of adult Digenea mid-body, even in young individuals. Chubrik (1966) in intertidal molluscs in Iceland. This brings the total identifying rediae of C. littorinae obtusatae in Lit- number of species recorded (including those identified torina obtusata at the Barents Sea also noted this earlier by Sannia & James, 1977; Eydal et al., 1996; feature. Discrepancies such as these make diagnosis Skirnisson & Jonsson, 1996) to 22. With the exception of the intramolluscan stages of Himasthla even more of Prosorhynchus squamatus and Podocotyle atomon, baffling. the adults of which infect fishes, the final hosts for One of the species, which we observed in Ice- these digeneans are marine and coastal birds. Annu- land, was C. littorinae obtusatae. Its identification ally, approximately 70 bird species breed in Iceland, was based on redial features, such as small pharynx but only a proportion of these species can be regarded (smaller than that of H. littorinae or H. elongata)anda as marine or coastal. However, marine or coastal short caecum. Even in the youngest specimens the cae- birds usually occur in large numbers and in dense 99 populations (Petersen, 1998) and this contributes to and some others (Sudarikov & Stenko, 1984; Skir- the rich fauna and relatively high infestation of inter- nisson & Jonsson, 1996) have been shown to be tidal molluscs with intramolluscan stages of digeneans common in these hosts, yet no intramolluscan stages (Skirnisson & Galaktionov, in prep.). of these species have been identified. It is also very Data provided in this study highlight problems as- strange that R. roscovita daughter-sporocysts, cer- sociated with the identification of even well known cariae and metacercariae are common in molluscs and widely distributed digenean larvae. Similar size from intertidal zones in the northern European seas parameters and the absence of contrasting charac- (Lauckner, 1980, 1983), whereas their adults have ters in daughter-sporocysts or rediae and cercariae of only been observed in experimentally infected herring closely related species (especially renicolids and echi- gulls (Werding, 1969; Sudarikov & Stenko, 1984). nostomatids) is sometimes compounded by contradict- Further complexity has arisen from the fact that the ing descriptions by different authors (some of these taxonomic status of the renicolid daughter-sporocysts have already been discussed). Without a thorough re- and cercariae Cercaria parvicaudata, C. emasculans vision of the literature, combined with experimental Pelseneer, 1906, C. brevicauda Pelseneer, 1906 and studies on the life-cycles concerned, identification of C. littorinae-saxatilis VI Sannia & James, 1977 iden- representatives of the genera Himasthla Dietz, 1909 tified from littorinids is unknown. This situation paral- and Renicola Cohn, 1904 infecting intertidal molluscs lels the one outlined above for rediae and cercariae in will remain difficult. the genus Himasthla. In some cases, specific features of the biology It is our opinion that the problems highlighted of the daughter-sporocysts or rediae, cercariae and above can only be resolved by experimental studies on metacercariae may have a significant role to play in digenean life-cycles associated with the sea coast. The species identification. This is illustrated when cercar- necessity for this type of study is particularly impor- ial encystment of M. linguilla and R. thaidus in their tant in regions where infection of intertidal molluscs first intermediate hosts is considered. It is possible that with intramolluscan stages of Digenea is increasing. under some conditions the cercariae of some species This phenomenon has largely resulted from an in- are not released, whereas under different conditions crease in seabird (mainly gull) numbers and changes they are. This is true for Gymnophallus choledochus in their feeding behaviour. The birds gather near places (Odhner, 1900): in summer its cercariae are shed from associated with human activity (fishing ports, coastal the molluscan host and penetrate polychaetes, whereas settlments, fish farms, etc.) and this results in in- in winter they encyst within their daughter-sporocysts creased parasite pressure on populations of intertidal in the first intermediate host, the bivalve Cardium ed- animals in adjacent coastal regions (Lauckner, 1985; ule (L.) (see Loos-Frank, 1969). Representatives of Matthews et al., 1985; Bustnes & Galaktionov, 1999). many digenean families found in the intertidal zone The acquisition of information enabling the precise (especially in the north) demonstrate an apparent trend identification of digenean species and a knowledge of to discard free-living stages from their life-cycles their intermediate and final hosts, become especially (James, 1968b; Deblock, 1977; Galaktionov, 1996b). important under these conditions. Bearing this in mind, it should not be surprising for one species to have both three-host and two-host life cycles under different ecological conditions. Acknowledgements In many cases it is impossible to correlate the data on intramolluscan stages with those of their adults. The project was financed by grants from the Ice- This is not so with Renicola thaidus, the adults of land Republic Fund 1994–1999, the NATO Science which were experimentally grown in gulls by Stunkard Fellowship and the Russian Foundation for Basic Re- (1964). On northern European coasts the prevalence search (grant N 98-04-49706). We wish to thank of this species in Nucella lapillus can be very high two anonymous reviewers for comments on draft of (Sannia & James, 1977; Podlipajev, 1979; Bustnes the manuscript. We also thank Dr S.W.B. Irwin for & Galaktionov, 1999; present study). Surprisingly, comments and correction of the English. adult R. thaidus has never been recorded in marine and coastal birds from this region. On the other hand, R. murmanicus Belopolskaja, 1952, R. somateria Be- lopolskaja, 1952, R. mollissimus Kulachkova, 1957 100

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