DISEASES OF AQUATIC ORGANISMS Vol. 37: 221-230,1999 Published September 14 Dis Aquat Org Distribution patterns of marine bird digenean larvae in periwinkles along the southern coast of the Barents Sea Kirill V. Galaktionovl, Jan Ove ~ustnes~l* 'Zoological Institute of the Russian Academy of Sciences, White Sea Biological Station, Universitetskaja nab., 1, St Petersburg, 199034, Russia 'Norwegian Institute for Nature Research, Department of Arctic Ecology, The Polar Environmental Centre. 9296 Tromse, Norway ABSTRACT: An important component of the parasite fauna of seabirds in arctic regions are the flukes (Digena).Different species of digeneans have life cycles whch may consist of 1 intermediate host and no free-living larval stages, 2 intermediate hosts and 1 free-living stage, or 2 intermediate hosts and 2 free-living larval stages. This study examined the distribution of such parasites in the intertidal zones of the southern coast of the Barents Sea (northwestern Russia and northern Norway) by investigating 2 species of periwinkles (Littorina saxatilis and L. obtusata) which are intermediate hosts of many species of digeneans. A total of 26020 snails from 134 sampling stations were collected. The study area was divided into 5 regions, and the number of species, frequency of occurrence and prevalence of different digenean species and groups of species (depending on life cycle complexity) were compared among these regions, statistically controlling for environmental exposure. We found 14 species of digeneans, of which 13 have marine birds as final hosts. The number of species per sampling station increased westwards, and was hlgher on the Norwegian coast than on the Russian coast. The frequency of occur- rence of digeneans with more than 1 intermediate host increased westwards, making up a larger pro- portion of the digeneans among infected snails. This was significant in L. saxatilis. The prevalence of different species showed the same pattern, and significantly more snails of both species were infected with bgeneans with complicated Life cycles in the western regions. In L. saxatilis, environmental expo- sure had a statistically significant effect on the distribution of the most common digenean species This was less obvious in L. obtusata. The causes of changing species composition between regions are prob- ably (1) the harsh climate in the eastern part of the study area reducing the probability of successful transmission of digeneans with complicated life cycles, and (2) the distribution of different final hosts. KEY WORDS: Seabirds - Parasites - Trematoda . Digenea . Barents Sea. Distribution INTRODUCTION constitute an important part of the seabird parasite fauna in the area (Belpolskaya 1952, Galaktionov 1995, The distributions of seabird parasites are not well 1996). known in arctic regions. In the Barents Sea area Most seabird digeneans have complicated life cycles (northwestern Russia and northern Norway) there with 1 or more intermediate hosts. This should be have been no studies of the broad-scale geographical taken into account in analyses of the geographical dis- variation in the distribution of such organisms, but tribution of helminths (Hoberg 1996, 1997).A record of small-scale studies have shown that flukes (Digenea) adult digeneans in individual seabirds does not neces- sarily mean that completion of the life cycle of the spe- cies is possible at the location where the bird was cap- 'Addressee for correspondence. tured, since the bird may have become infected in a E-mail: [email protected] different area. More reliable information about the dis- O Inter-Research 1999 Resale of full article not permitted 222 Dis Aquat Org 37: 221-230, 1999 tribution of the digenean fauna may be gained from the different regions, controlling statistically for envi- examining the larval composition of the intermediate ronmental exposure. hosts, particularly the first host, which are intertidal and upper-subtidal gastropod molluscs such as peri- winkles Littorina spp. These molluscs are distributed MATERIALS AND METHODS widely along the intertidal zone of northern seas and play an important role as the first intermediate host for The coastline investigated stretched from Novaya many common seabird digeneans (Chubrick 1966, Zemlya to Tromsa, and included the White Sea (Fig. 1). James 1968, 1969, Werding 1969, Podlipajev 1979, This coast has a very harsh climate, especially in the Lauckner 1980, 1984a, 1987, Irwin 1983, Matthews et arctic eastern parts (e.g. Loeng 1991, Andalsvik & al. 1985, Galaktionov & Dobrovolskij 1986, Kristoffer- Loeng 1991). We divided the coastline into 5 different sen 1991, Galaktionov 1993). regions, which could be naturally distinguished. The most typical life cycles of digeneans involve 2 Region A was Novaya Zemlya and Vaygatch Island. intermediate hosts. There may be 1 (cercaria) or 2 Region B was the White Sea and the tip of the Kanin (miracidia and cercaria) free-living stages in such life peninsula. Region C was the eastern Kola coast to the cycles. A genus with 2 free-living stages commonly Kola fjord (eastern Murman). Region D was the found in the Barents Sea is Himasthla, while digeneans with 1 free-living larval stage are Microphallus similis, Cryptocotyle lingua, and the genus Renicola. The second intermediate host may be omitted from the life cycle; the cercaria then encysts in the environment (e.g. the genus Noto- 7 cotylus). In some cases the metacer- canae mature inside sporocysts in the molluscan host that combine, to some extent, the function of both the first and the second intermediate hosts. Some of these life cycles are devoid of free-swimming larval stages (mira- cidia and cercaria) (Galaktionov 1993, 1996).A common group of digeneans with such life cycles are the micro- phallids of the 'pygmaeus' group (MicrophaLlus pygmaeus, M. pirifor- mes, etc.), which are common in the Barents Sea region (Chubrick 1966, Podlipajev 1979, Galaktionov & Do- brovolskij 1986, Galaktionov 1993). Our aim was to examine the distrib- ution of seabird digeneans with dif- ferent life cycle complexity in 2 spe- cies of periwinkles (Littorina saxatills and L. obtusata),along a climatic gra- dient on the southern coast of the Bar- ents Sea. The area stretched from the arctic Novaya Zemlya in the east to the milder coastal area around Tromse in the west (Fig. 1). We divided the area into 5 naturally sepa- rated regions (Fig. l) and compared the frequency Of Occurrence and Fig. 1. (a) Division of the study area into different regions (A to E) (see 'Materials prevalence of digenean species with and methods'), and (b) the distribution of sampling stations along the southern varying life cycle complexity among Barents Sea Coast Galaktionov & Bustnes: Digeneans in the Barents Sea 223 western Murman and Finnmark County Table 1. Sample sizes of periwinkles collected in different regions on the east of the Porsanger fjord. Region E was southern coast of the Barents Sea western Finnmark and Troms Counties (Fig. l). Species Region No. of No. of Mean no. SE Min Max. The areas surrounding Novaya Zemlya - locations individuals per site and Vaygatch have an arctic climate with LI ttonna sasatilis very low temperatures during the whole A 4 4 7357 167.2 11.5 40 344 year. Sea ice dominates from October to B 29 5240 180.7 30.2 50 785 June, and intertidal zones are covered by C 14 2846 203.3 26.4 98 450 ice (Loeng & Vinje 1979, Vinje & Kvam- D 27 3461 128.2 9.5 60 292 E 20 1950 97.5 4.1 40 130 bekk 1991). The climate in the White Sea Sum 134 20854 is milder, but the sea is frozen in winter L. obtusata (December to May) since the water in this B 8 1406 175.5 67.4 28 502 region has a low salinity (Lsnne et al. C 3 530 176.7 76.7 100 330 1997). The eastern Kola coast is usually D 14 1475 105.4 12.5 75 264 not frozen in winter. There are no large E 18 1755 97.5 3.0 48 110 Sum 43 5166 fjords in this region, and the intertidal zones are thus more exposed to wave action (e.g.Andalsvik & Loeng 1991).The western Murman and eastern Finnmark have more upper-mid intertidal zone (Golikov 1995).In regions B, fjords and the climate is milder, influenced by the C, D and E, L. obtusata is common in the middle and North Atlantic and coastal currents. Nevertheless the lower levels of the seaweed fronds (Golikov 1995). prevalent wind directions are more easterly than they Molluscs were collected by hand at low tide. The are further west. Troms and western Finnmark are sampling was done in the same manner and at the dominated by westerly winds, and are relatively mild same time of year (August and September) at all sites. compared to the other regions (Loeng 1991, Loeng et In this season the infestation of intertidal snails by al. 1992, Lernne et al. 1997). digenean larvae in arctic areas is at its highest The collection of the material was carried out from (Chubrick 1966, Galaktionov & Dobrovolskij 1986, 1978 to 1990 in Russia, and in 1992 and 1994 in Galaktionov 1992). Snails were dissected under a Norway. We collected totally 26020 snails of 2 species stereomicroscope, and the digenean larvae were iden- (Littorina saxatilis and L. obtusata) from 134 locations tified in vivo. For the analyses we recorded the pres- (Table 1). The sampling stations were evenly distrib- ence or absence of different digenean species in each uted along the coast in Norway (Fig. 1).In Russia, the mollusc. Double infections made up a very small pro- stations chosen were more clustered (Fig. 1) because portion (usually less than 1 %) of the infected snails, they were remote and access was much more difficult. and were therefore excluded from the analyses.