The Parasite Fauna of Arctogadus Glacialis (Peters) (Gadidae) from Western and Eastern Greenland

Polar Biol (2008) 31:1017–1021 DOI 10.1007/s00300-008-0440-1

ORIGINAL PAPER

The parasite fauna of Arctogadus glacialis (Peters) (Gadidae) from western and eastern Greenland

Marianne Køie · John Fleng SteVensen · Peter Rask Møller · Jørgen Schou Christiansen

Received: 8 January 2008 / Revised: 29 February 2008 / Accepted: 9 March 2008 / Published online: 26 March 2008 © Springer-Verlag 2008

Abstract In all 155 specimens of the high Arctic codWsh Keywords Arctogadus · Boreogadus · Greenland · Arctogadus glacialis examined for metazoan parasites, 55 Parasites specimens were from southern and northern BaYn Bay, western Greenland, and 100 specimens from north-eastern Green- land and Scoresby Sound. A total of 20 parasite taxa were Introduction recorded. A new myxozoan Gadimyxa arctica was found in southern BaYn Bay and Scoresby Sound. The gadid myxo- The codWsh Arctogadus glacialis (Peters) has a circumpolar zoan Zschokkella hildae, the digeneans Gonocerca phycidis distribution, with only few specimens caught south of the and Lecithaster gibbosus, the gill copepod Haemobaphes cycl- Arctic Circle. It has not been examined for parasites before. opterina and third-stage larvae of the nematodes Anisakis sim- The aim of the present study is to provide knowledge of the plex and Hysterothylacium aduncum were found in Scoresby parasite fauna and to relate it with the host food items and Sound only. The digenean Hemiurus levinseni and third-stage to compare the parasite fauna of A. glacialis with that of the larvae of the nematode Contracaecum sp. were found at all closely related Boreogadus saida (Lepechin). four stations. The nematodes Ascarophis spp. were found at three stations. The parasite fauna of A. glacialis from Scoresby Sound was very similar to that of 50 specimens of the closely Materials and methods related Boreogadus saida from the same area. Specimens of A. glacialis (Peters, 1874) (Gadidae) were collected from 2000 to 2005 at two stations in western and two stations in eastern Greenland waters. The number, locality, depth, date of capture, and size ranges of the M. Køie (&) · J. F. SteVensen examined specimens are listed in Table 1. Figure 1 shows Marine Biological Laboratory, the collecting stations for this study. Those from southern University of Copenhagen, 3000 Helsingor, Denmark Y W e-mail: [email protected] Ba n Bay (station 1) were caught by jigging during a eld V course party from the Arctic Station, Qeqertarssuaq; those J. F. Ste ensen Y e-mail: [email protected] from northern Ba n Bay (station 2) were bottom-trawled during a Wsh survey conducted by Greenland Institute of P. R. Møller Natural Resources. The specimens from eastern Greenland Zoological Museum, Natural History Museum of Denmark, (stations 3 and 4) were caught by bottom trawling during University of Copenhagen, Universitetsparken 15, 2100 Copenhagen, Denmark the TUNU-I and TUNU-II expeditions (Christiansen 2006). e-mail: [email protected] All Wsh were frozen immediately upon capture and transported frozen to the Marine Biological Laboratory, J. S. Christiansen Helsingor. Norwegian College of Fishery Science, W University of Tromso, 9037 Tromso, Norway In the laboratory the sh were thawed and the external e-mail: [email protected] surface of all A. glacialis, including nostrils, gills and mouth 123 1018 Polar Biol (2008) 31:1017–1021

Table 1 Sampling stations of Arctogadus glacialis and Boreogadus saida Station Position Depth Number Length (cm), Weight (g), Date (m) examined range, mean range, mean

1 Southern BaYn Bay, western Greenland 70°41ЈN, 51°56ЈW 20–50 5 35–40, 37 462–755, 580 7.07.00 2 Northern BaYn Bay, western Greenland 75°37ЈN, 66°10ЈW 492–576 50 16.0–24.0, 19.5 34–139, 69.4 24.09.04 75°40ЈN, 65°28ЈW 3 Greenland Sea, northeastern Greenland 75°24ЈN, 11°45ЈW 504 25 11.0–19.5, 13.2 10–53, 15.2 5.10.03 4 Scoresby Sound, eastern Greenland 71°09ЈN, 24°57ЈW 485 75 14.0–22.0, 17.7 18–75, 37.5 4.10.05 Scoresby Sound, eastern Greenlanda 70°30ЈN, 25°27ЈWa 620a 50a 13.5–19.5, 16.6a 20–47, 29.0a 4.10.05a a Sampling stations of Boreogadus saida

Fig. 1 Sampling stations. 1 Southern BaYn Bay oV Uma- nak, western Greenland. 2 Northern BaYn Bay, north- western Greenland. 3 Greenland Sea, northeastern Greenland. 4 Scoresby Sound, eastern Greenland

as well as the internal organs, eyes, body cavity and brain, once in a gallbladder of A. glacialis from Scoresby Sound. were examined. Smears of kidney, urine, urinary bladder It was not identical with S. sinuosa Shulman, 1953 described wall, bile and gall bladder wall were examined at high from the urinary bladder of B. saida from the White Sea. magniWcation (min. 10 £ 20). The various parasites were Wxed in Berland’s Xuid (glacial acetic acid: 40% formalde- Platyhelminthes: Digenea and Cestoda hyde, 19:1), cleared in lactic acid and mounted in glycerine jelly. The hemiuroid digeneans Hemiurus levinseni Odhner, 1905 (Hemiuridae), Derogenes varicus (Müller, 1784) (Derogen- idae) and Lecithaster gibbosus (Rudolphi, 1802) (Lecithas- Results teridae) were found in A. glacialis from four, three and one stations, respectively. They were all found in B. saida from The parasite fauna of A. glacialis from stations 1–4 are Scoresby Sound. Five digenean specimens that were found shown in Table 2. The parasite fauna from Scoresby Sound in the stomach of A. glacialis from station 3 were full of (station 4) was compared with that of B. saida from the eggs preventing a study of morphological details. They same station. were tentatively identiWed as either Genolinea sp. (Bunoco- tylidae) or Lecithophyllum sp. (Lecithasteridae). The eggs Myxozoa measured 25–30 £ 18–20 m and are thus smaller than those of known species of Genolinea and Lecithophyllum. A new species Gadimyxa arctica Køie et al., 2007 (see One specimen of Gonocerca phycidis Manter, 1925 (Dero- Køie et al. 2007) and Zschokkella hildae Auerbach, 1909 genidae) was found in the stomach of an 18.0 cm long (Myxosporea, Bivalvulida, Myxidiidae) were found in the A. glacialis from station 4. urinary system of A. glacialis (Table 2). Spores belonging Tetraphyllid larvae (Tetraphyllidea) and small pseudo- to Sinuolinea sp. (Bivalvulida, Sinuolineidae) were found phyllid larvae (Pseudophyllidea) were found free in the 123 Polar Biol (2008) 31:1017–1021 1019

Table 2 Records of metazoan parasites of Arctogadus glacialis from western and eastern Greenland compared with those of Boreogadus saida from Scoresby Sound Parasite taxa Arctogadus glacialis Boreogadus saida

1 Southern 2 Northern 3 Greenland 4 Scoresby Scoresby BaYn Bay, western BaYn Bay, western Sea, eastern Sound, eastern Sound, eastern Greenland [5] Greenland [50] Greenland [25] Greenland [75] Greenland [50]

Zschokkella hildae – – – (8) 11% (14) 28% Myxidium sp. – – – (1) 1.3% – Sinuolinea sp. – – – (1) 1.3% – Gadimyxa arctica (1) 20% – – (5) 7% – Hemiurus levinseni (2) 40%1–3, 1.5 (10) 20%1–6, 2.3 (2) 8%1, 1 (44) 59% 1–40, 4.5 (33) 66% 1–15, 4.4 Derogenes varicus (3) 60%1–9, 5.3 (1) 2%, 1, 1 – (9) 12% 1, 1 (6) 12% 1–4, 2 Genolinea sp./ Lecithophyllum sp. – – (3) 12%1–3, 1.7 – – Gonocerca phycidis – – – (1) 1.3% 1, 1 – Lecithaster gibbosus – – – (14) 19% 1–22, 5.4 (10) 20% 1–8, 3.2 Tetraphyllid larva – – – (1) 1.3% 2, 2 – Pseudophyllid larva (2) 40%1–2, 1.5 – – (2) 2.7% 1–3, 1.5 (1) 2% 1, 1 Anisakis simplex larva – – – (11) 15% 1–4, 1.3 (2) 4% 1, 1 Contracaecum osculatum larva (4) 80%2–6, 4.5 (41) 82%1–7, 3.0 (9) 36%1–2, 1.3 (59) 79% 1–8, 2.5 (35) 70% 1–8, 2.1 Hysterothylacium aduncum larva – – – (1) 1.3% 1, 1 (2) 4% 1, 1 Ascarophis morrhuae (3) 60%1–3, 2.0 (40) 80%1–15, 4.8 – (11) 15% 1–3, 1.7 – Ascarophis 1 (5) 100%1–6, 2.2 – – – – Ascarophis 2 juvenile – – – (5) 7% 1–2, 1.4 – Ascarophis sp. juvenile – – – – (1) 2% 18, 18 Echinorhynchus sp. (1) 20%1, 1 – – – – Corynosoma sp. juvenile – – (2) 8%1, 1 (6) 8% 1–2, 1.2 – Clavella adunca – – – – (6) 12% 1–5, 1.7 Haemobaphes cyclopterina – – – (2) 3% 1, 1 (2) 4% 1, 1 The number of examined Wsh is in square brackets. The number of specimens infected is in brackets, the prevalence is shown in % and the ranges and mean intensities of infection (number of infected specimens per number of all infected specimens) are shown digestive system of A. glacialis from station 4, and 1 and 4, only undeveloped eggs. Ascarophis morrhuae (Van Bene- respectively. den, 1871) was found in the stomach and intestine of A. glacialis from both western and eastern Greenland. Nematoda, Acanthocephala and Copepoda One juvenile specimen of Echinorhynchus sp. (Ech- inorhynchidae) was found in the intestine of A. glacialis Encapsulated third-stage larvae of Anisakis simplex (Rudol- from station 1. Encapsulated juvenile specimens of Coryno- phi, 1845) (sensu lato) (Ascaridida, Anisakidae) were soma sp. (Polymorphidae) were found externally on the found externally on the pyloric caeca of A. glacialis from pyloric caeca of A. glacialis from eastern Greenland. station 4. The infected Wsh measured 16.0–22.0 cm, mean Haemobaphes cyclopterina (Fabricius, 1780) (Pennellidae) 18.9 cm. Third-stage larvae of Contracaecum sp. (Ascarid- was found on the gills of two specimens of A. glacialis ida, Anisakidae) were found at all stations. Up to 4.5 cm from station 4. long encapsulated larvae were found externally on the pyloric caeca and intestine and specimens a few mm long were sometimes found free in the stomach. A third-stage larva of Discussion Hysterothylacium aduncum (Rudolphi, 1802) (sensu lato) (Ascaridida, Raphidascarididae) was found once on the Arctogadus glacialis has a wide habitat range and occurs in caeca of a specimen of A. glacialis from Scoresby Sound. river mouths as well as far oVshore, and at depths ranging Mature H. aduncum was not found in the present study. At from 5 to 930 meters (Nielsen and Jensen 1967). The rather least three species of Ascarophis (Spirurida, Cystidicolidae) large eyes may suggest that A. glacialis is adapted to life at low were found. Most specimens were juveniles or harboured light levels, for instance below ice cover (Jordan et al. 2003). 123 1020 Polar Biol (2008) 31:1017–1021

In the Northeast Water Polynya oV eastern Greenland they A. glacialis were similar to those described by Petter feed almost exclusively on pelagic prey (Süfke et al. 1998). (1970). Ascarophis 1 may include more than one species. Calanoid copepods dominated the diet of small Wsh, Most had characters similar to A. arctica Polyanski (1952) whereas amphipods and mysidaceans were relatively and A. Wliformis Polyanski (1952) as described by, e.g. important for larger Wsh. Truly benthic organisms were not Polyanski (1952) and Appy (1981). The cuticle of the pres- found and ice-related species were rarely recorded. In ice- ent worms had a faint striation. Polyanski (1952) described covered waters, however, it has been reported to feed on the cuticle of A. Wliformis as smooth, but Appy (1981) ice-associated organisms. The broad variety of food items found a faint striation in his material from the type host indicated an opportunistic pelagic feeding pattern. Gadus morhua. According to Appy (1981) A. Wliformis is Comparison of the four stations is somewhat biased by longer than A. arctica, has less distinct striations, a shorter the diVerences in sample size and body size of the hosts left spicule, eggs with Wlaments at one pole only, and (Table 1). All the metazoan parasites, apart from Gadimyxa shorter oesophagus and male tail relative to body length. arctica and Genolinea sp./Lecithophyllum sp., are general- Since all these features, apart from the eggs, are relative ist species found in several Wsh families. The high arctic and the present worms were immature they could not with digenean only found north of 75°N, and Gonocerca phyci- certainty be identiWed to species. Ascarophis 2 were all dis have completely unknown life cycles. It is likely that juveniles. They could not be identiWed as either A. morr- the infected A. glacialis has acquired G. phycidis at a huae or Ascarophis 1. They were very similar to Ascaro- greater depth than where it normally feeds. In Faeroese phis sp. found in various non-gadid Wsh from below 500 m waters G. phycidis gradually replaces Derogenes sp. at from the Faeroe Islands (Køie 1993). Larvae of Ascarophis depths from 400 to 500 m (Køie 2000). The molluscan host spp. develop in various malacostracan crustaceans includ- of Hemiurus levinseni is unknown, but should probably be ing amphipods, isopods, mysidaceans, shrimps and crabs found among bullomorph opisthobranchs (Køie 2000). (Petter 1970; Køie 1993; Jackson et al. 1997). The acantho- Derogenes varicus is apparently a collective name which cephalans Echinorhynchus sp. and Corynosoma spp. use may comprise several species (see Køie 2000). The Wrst amphipods as Wrst intermediate host. Corynosoma spp. may hosts are prosobranchs belonging to the Naticidae. A small use various Wsh as transport host and birds (e.g. cormorants opisthobranch acts as the Wrst intermediate host of Lecith- Phalacrocorax spp.) and/or seals (e.g. Phoca spp.) as the aster gibbosus (Rudolphi, 1802) (Lecithasteridae) in Dan- Wnal host. ish waters (Køie 2000); the Wrst intermediate host in arctic Arctogadus glacialis has acquired the infections with the waters is unknown since this snail does not occur in the hemiuroid digeneans and cestodes by eating planktonic Arctic. All the digeneans mentioned above use calanoid copepods and with Contracaecum sp., Hysterothylacium copepods as second intermediate hosts. Adult tetraphyllids aduncum, Ascarophis spp. and the acanthocephalans by occur in the spiral valve of elasmobranchs and holocepha- eating planktonic copepods and other crustaceans and, lids. Adult pseudophyllids occur predominantly in Wsh, but especially amphipods. Third-stage larvae of A. simplex also in other vertebrate groups, e.g. birds, seals and whales. were found in A. glacialis from station 4. Even though eup- Pelagic copepods act as the Wrst intermediate host of most hausiaceans, the main intermediate host of A. simplex, were tetraphyllids and pseudophyllids. Euphausiacians are the not recorded among the stomach contents of A. glacialis most important crustacean hosts of Anisakis simplex, and from north-eastern Greenland (Süfke et al. 1998) it is likely Wsh act as transport host with whales being the Wnal host. that they are among the food items of this species at station The present specimens of Contracaecum sp. were very sim- 4. The infected A. glacialis were not among the largest ilar to C. osculatum (Rudolphi, 1802). Crustaceans, mostly specimens. This indicates that the infection is probably not copepods, act as Wrst intermediate hosts, Wsh as second acquired by ingesting infected Wsh. intermediate hosts and seals as the Wnal host (Køie and Only stations 2–4 are comparable due to the relatively Fagerholm 1995). Hysterothylacium aduncum use various high number of A. glacialis examined and due to the nearly crustaceans as Wrst intermediate host, benthic and pelagic similar size of the examined Wsh. Those from the most invertebrates and Wsh as transport hosts and Wsh as Wnal northern stations 2 and 3 were infected with four parasite hosts (Køie 1993). species or taxa. Even though the sample size of A. glacialis The type host of Ascarophis morrhuae is Gadus morhua from station 4 was larger than those of the remaining sta- L. The species has been redescribed from Gadus spp by, tions, it is obvious that the parasite fauna here shows a e.g. Polyanski (1952) and Petter (1970). According to Poly- higher diversity with 17 parasite taxa. This probably indi- anski (1952) the eggs are provided with two long Wlaments cates a higher diversity of the benthic and pelagic inverte- at one end. Petter (1970) found in addition to the two long brate fauna at station 4 (Scoresby Sound) than in the other Wlaments a variable number of shorter and thinner Wlaments areas studied. B. saida from Scoresby Sound caught on the at both poles. The eggs of the present specimens from same day harboured 11 parasite taxa. The greatest diVerences 123 Polar Biol (2008) 31:1017–1021 1021 between the parasite fauna of the two gadids are the Christiansen JS (2006) TUNU-II expedition: marine Wshes of NE scarcity of Ascarophis spp. and absence of Corynosoma in Greenland—diversity and adaptation. Tech Rep, Univ of Tromsø, 28 pp B. saida from Scoresby Sound. Also notable is the absence Jackson CJ, Marcogliese DJ, Burt MBD (1997) Role of hyperbenthic of Clavella adunca in A. glacialis, a crustacean ectoparasite crustaceans in the transmission of marine helminth parasites. Can which is relatively common in other gadids from arctic and J Fish Aquat Sci 54:815–820 temperate areas. Jordan AD, Møller PR, Nielsen JG (2003) Revision of the Arctic cod genus Arctogadus. J Fish Biol 62:1339–1352 The great similarity between the parasite faunae of Køie M (1993) Nematode parasites in teleosts from 0 to 1540 m depth A. glacialis and B. saida shows that these closely related oV the Faroe Islands (the North Atlantic). Ophelia 38:217–243 species (Møller et al. 2002), with a few exceptions, are Køie M (2000) Metazoan parasites of teleost Wshes from Atlantic wa- susceptible to the same parasite species and that the two ters oV the Faroe Islands. Ophelia 52:25–44 Køie M, Fagerholm H-P (1995) The life cycle of Contracaecum oscul- species have a similar food habit. atum (Rudolphi, 1802) sensu stricto (Nematoda, Ascaridoidea, Anisakidae) in view of experimental infections. Parasitol Res Acknowledgments The specimens of Arctogadus glacialis and 81:481–489 Boreogadus saida used in this study were provided by Anders Køie M, Karlsbakk E, Nylund A (2007) A new genus Gadimyxa with D. Jordan and Peter V. Skov (MBL, Helsingør), Ole A. Jørgensen three new species (Myxozoa, Parvicapsulidae) parasitic in marine (DIFRES, Charlottenlund), Steen Knudsen (Zoological Museum, Wsh (Gadidae) and the two-host life cycle of Gadimyxa atlantica University of Copenhagen) and the personal of R/V Jan Mayen n. sp. J Parasitol 93:1459–1467 (TUNU-Programme, University of Tromso), R/V Paamiut (Greenland Møller PR, Jordan AD, Gravlund P, SteVensen JF (2002) Phylogenetic Institute of Natural Resources), and R/V Porsild (University of position of the cryopelagic codWsh genus Arctogadus Drjagin, Copenhagen). The Arctic Station course was Wnanced by the Carlsberg 1932 based on partial mitochondrial cytochrome b sequences. Po- Memorial Foundation for J.C. Jacobsen, the Elisabeth & Knud lar Biol 25:342–349 Petersens Foundation, the G. E. C. Gads Foundation, the Ole Kirks Nielsen JG, Jensen JM (1967) Revision of the Arctic cod genus, Arc- Foundation and the Palsboell Foundation. togadus (Pisces: Gadidae). Medd Grønland 184:1–26 Petter AJ (1970) Quelques spirurides de poissons de la région nantaise. Ann Parasit Hum Comp 45:31–46 References Polyanski YI (1952) Some new and little known parasitic Nematoda from the intestinal tract of marine Wshes. Trudy Zool Inst Leningr 12:133–147; (In Russian) Appy RG (1981) Species of Ascarophis van Beneden, 1870 (Nema- Süfke L, Piepenbutg D, von Dorrien CF (1998) Body size, sex ratio and W toda: Cystidicolidae) in North Atlantic shes. Can J Zool diet composition of Arctogadus glacialis (Peters, 1874) (Pisces: 59:2193–2205 Gadidae) in the Northeast Water Polynya. Polar Biol 20:357–363

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