Published in collaboration with the University of Bergen and the Institute of Marine Research, Norway
Life cycles and transmission patterns of seabird digeneans in SW Iceland
Karl Skirnisson & Kirill V. Galaktionov
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SARSIA
Skirnisson K, Galaktionov KV. 2002. Life cycles and transmission patterns of seabird digeneans in SW
Iceland. Sarsia 87:144–151.
Flukes (digeneans) are common parasites of seabirds in Arctic and subarctic regions. This study
examined the distribution of such parasites in 1998 and 1999 in the intertidal zones of two study areas in
SW Iceland (Skerjafjördur and Grindavik) by investigating seven species of littoral snail, Littorina
saxatilis, L. obtusata, L. fabalis, Onoba aculeus, Hydrobia ventrosa, Epheria vincta and Nucella
lapillus, which are known to be Ž rst intermediate hosts of many species of digenean. A total of 2556
snails was collected and the intramolluscan stages of 23 seabird digenean species were identiŽ ed. The
local occurrence and abundanc e of Ž nal hosts, such as gulls, eiders and waders, largely explain
prevalence differences in the study areas. Seabird digeneans with life cycles involving two intermediate
hosts and one/two free-living larvae are more frequent in the Icelandic localities studied than in coastal
areas of northern Europe (Barents Sea, White Sea, northern Norway). This indicates that the
environmenta l conditions in the coastal ecosystem of SW Iceland are favourabl e for the transmission of
complex life cycles. Also, the abundance and diversity of both potential Ž nal hosts (birds) and second
intermediate hosts (littoral invertebrates and Ž shes) are considered to contribute to the richness of the
digenean fauna of SW Iceland.
Karl Skirnisson, Institute for Experimental Pathology, University of Iceland, Keldur, IS-112 Reykjavṍk,
Iceland.
E-mail: [email protected]
Kirill V. Galaktionov, White Sea Biological Station, Zoological, Institute of the Russian Academy of
Sciences, St Petersburg, Russia.
E-mail: [email protected] u
Keywords: Digenea; seabirds; snails; life cycles; Iceland.
INTRODUCTION
Seabird digeneans are one of the main parasitological
components of marine coastal ecosystems (Lauckner
1985, 1987; Bustnes & al. 2000). For some time now,
extensive studies have been carried out on the fauna
composition, life cycles, distribution patterns and
ecology of a number of seabird digeneans in Arctic
and subarctic regions of northwest Europe (Chubrik
1966; Kulachkova 1979; Podlipaev 1979; Galaktionov
& Marasaev 1990; Kristoffersen 1991; Granovitch
1992; Galaktionov 1993, 1995, 1996a, 1996b; Galaktionov & Bustnes 1995, 1999; Bustnes & Galaktionov
1999). However, only limited research has been carried
out on digenean parasites in Iceland (Brinkmann 1956;
Skirnisson & Jonsson 1996; Eydal & al. 1998; for a
review see Galaktionov & Skirnisson 2000).
Icelandic marine and coastal bird populations, especially sea-ducks, gulls and waders, are usually
characterized by high densities and high individual
numbers. For example, approximately one million
common eiders Somateria mollissima and hundreds of
thousands of big gulls Larus spp. winter along the cost
(Petersen 1998). Most marine and coastal birds regularly
visit the intertidal zone, where they rest or feed on
coastal invertebrates and Ž shes which may be intermediate hosts to digeneans. In Icelandic littoral and
sublittoral zones, organisms which act as intermediate
hosts occur in dense populations. This is especially true
in the western half of the country, where the most
extensive littoral zones are located (Ingolfsson 1996).
We commenced our study of digenean larvae in
coastal invertebrates of SW Iceland relatively recently.
Earlier, however, Sannia & James (1977) examined 14
species of intertidal and subtidal molluscs in Eyjafjördur
(N Iceland) and found intramolluscan stages of seven
digeneans. Eydal & al. (1994) examined the occurrence
of Cryptocotyle lingua. In our study (Galaktionov &
Skirnisson 2000), intramolluscan stages of 19 digeneans
from six species of intertidal snails collected in 1998
were reported. All the species found, except one, have
marine or coastal birds as Ž nal hosts.
Here we examine the frequency of different transmission patterns of seabird digeneans in two locations
in SW Iceland and discuss the results relative to data
recently obtained in other coastal regions of Europe.
# 2002 Taylor & Francis
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Skirnisson & Galaktionov – Seabird digeneans in SW Iceland
Fig. 1. The geographica l location of the two study areas in SW
Iceland.
MATERIAL AND METHODS
In August and September 1998 and May 1999, seven
gastropod species, Littorina saxatilis (Olivi), L. obtusata (L.), L. fabalis (Turton), Onoba aculeus (Gould),
Hydrobia ventrosa (Montagu), Epheria vincta (Montagu), and Nucella lapillus L., comprising 2556 snails,
were collected at 12 intertidal sampling stations in
Skerjafjördur and Grindavik, SW Iceland (Fig. 1).
Littorina saxatilis was collected in the middle and
upper intertidal levels, where infection of the molluscs
with seabird trematodes is known to be maximal (James
1968; Robson & Williams 1970; Lauckner 1980;
Galaktionov 1993). The other molluscs were mainly
collected in the middle and low intertidal zones, i.e. in
their usual habitats.
Medium- and large-sized specimens were chosen for
dissection, as the probability of infection is highest in
these (Rothschild 1941; Robson & Williams 1970;
Curtis & Hurd 1983; Galaktionov 1985; Lauckner
1987; Granovitch 1992; Gorbushin 1997).
Skerjafjördur is an 8 km long, shallow fjord with
some sheltered creeks, approximately 18 km2 in area.
The outer parts of the fjord are characterized by
exposed rocky shores, but the shores in the inner part
are sheltered, with mud  ats uncovered at low tides in
the innermost creeks (Gardarsson & Adalsteinsdottir
1977, Ingolfsson 1977). The area is intensively used by
most seabird species occurring in Iceland (Petersen
1998).
Grindavik is a highly exposed triangle-shaped
creek, approximately 2 km wide and 2 km deep, with
steep, rocky shores covered with big boulders at
the upper limits of the intertidal zone. Walls composed of big boulders shelter the harbour of the
Ž shing village situated at the bottom of the fjord. The
145
area is an important temporary resting place for
waders during spring and autumn migration, but
common eiders and large and small larids are the
dominant bird species (Skarphedinsson & Einarsson
1989; Petersen 1998).
The snails were dissected and the sporocysts, rediae,
cercariae or metacercariae occurring in each snail were
identiŽ ed in vivo. The digeneans found were designated
into one of two groups according to their life cycle
(Galaktionov & Bustnes 1999). Species with a two-host
life cycle without free-living larvae were allocated to
group 1. Those with a three-host life cycle with a freeliving miracidium and/or cercaria were placed in group
2. The frequency of occurrence (as a percentage) was
calculated for both groups, so that only infected snails
were included in the calculations.
We also calculated the prevalence (as a percentage)
of snails infected by a particular parasite species and
tested for differences between sites using Fisher’s exact
test.
RESULTS
COMPOSITION OF THE DIGENEAN FAUNA
In total, intramolluscan stages of 23 seabird digenean
species were identiŽ ed (Table 1). They were Microphallus pygmaeus (Levinsen, 1881), M. piriformes
Galaktionov, 1983, Microphallus sp. I Galaktionov,
1980 (M. pseudopygmaeus Galaktionov, 1980), M.
triangulatus Galaktionov, 1984, M. breviatus Deblock
& Maillard, 1975, M. similis (Jägersköld, 1900), M.
claviformis (Brandes, 1888), Cercaria islandica I
Galaktionov & Skirnisson, 2000, C. littorina saxatilis
VII Newell, 1986, Maritrema linguilla (Jägersköld,
1909) (Microphallidae), Renicola thaidus Stunkard,
1964, C. parvicaudata Stunkard & Shaw, 1931 (Renicolidae), C. lingua (Creplin, 1825), C. concavum
(Creplin, 1825) (Heterophyidae), Parvatrema homoeotecnum James, 1964 (Gymnophallidae), Himasthla
elongata (Mehlis, 1831), H. continua Loos-Frank,
1967, C. littorina obtusata Lebour, 1911 (Echinostomatidae), Paramonostomum chabaudi van Strydonck,
1965, P. anatis Garkavi, 1965, Notocotylidae gen. sp.
(Notocotylidae), Parapronocephalum symmetricum
(Belopolskaya, 1952) (Pronocephalidae) and Parorchis
acanthus (Nicoll, 1906) (Philophthalmidae).
The richest parasite fauna were recorded in the
periwinkle L. obtusata (12 species) and L. saxatilis
(nine species), the most common gastropods in the
intertidal zone. Somewhat fewer digenean species were
found in O. aculeus (six species), H. ventrosa (six
species) and L. fabalis (Ž ve species). Nucella lapillus
**
0.3
1.4
2.1
0.3
1.4
0.3
0.3
4.3
0.4
ns
6.6
1.5
4.1
0.3
1
0.3
0.2
0.5
2.9
0.4
*
0.9
0.3
0.9
0.2
3.6
0.8
ns
ns
ns
G
(290)
ns
ns
**
*
ns
ns
p
Littorina obtusata
S
(332)
4.1
0.3
4.8
1.7
0.5
4.1
1.4
0.6
p
Numbers in parentheses are the numbers of individuals examined.
* p < 0.01, ** p < 0.001. ns, not signiŽ cant.
Microphallus pygmaeus
M. piriformes
M. pseudopygmaeus
M. triangulatus
M. breviatus
M. similis
M. claviformis
Cercaria islandica I
C. littorina saxatilis VII
Maritrema linguilla
Renicola thaidus
C. parvicaudata
Cryptocotyle lingua
C. concavum
Parvatrema homoeotecnum
Himasthla elongata
H. continua
C. littorina obtusata
Paramonostomum chabaudi
P. anatis
Notocotylidae gen. sp.
Parapronocephalum symmetricum
Parorchis acanthus
G
(416)
S
(483)
Littorina saxatilis
1.1
1.1
2.2
1.1
S
(92)
2.3
G
(44)
p
Littorina fabalis
1.4
2.8
0.9
0.9
0.9
1.4
0.9
3.6
1.8
1.8
ns
ns
ns
ns
S
G
p
(213) (112)
Onoba aculeus
2
33
3.6
20
ns
*
S
G
p
(153) (196)
Nucella lapillus
Table 1. Prevalence (as a percentage) of seabird digeneans in intertidal snails in Skerjafjördur (S) and Grindavik (G), SW Iceland.
2.5
G
(80)
Epheria vincta
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2.1
0.7
0.7
0.7
23.4
0.7
S
(145)
Hydrobia ventrosa
146
Sarsia 87:144-151 – 2002
Skirnisson & Galaktionov – Seabird digeneans in SW Iceland
and E. vincta had two and one species, respectively
(Table 1).
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LIFE CYCLES OF THE IDENTIFIED DIGENEANS
Six of the species (M. pygmaeus, M. piriformes, M.
pseudopygmaeus and M. triangulatus belonging to the
“pygmaeus” group of microphallids, plus M. breviatus
and P. symmetricum) have a two-host (snail–bird) life
cycle without free-living larvae (group 1). However, 13
of the remaining 17 species involve two intermediate
hosts and free-living miracidia and/or cercariae (group
2). The remaining four species, P. acanthus, Notocotylidae gen. sp., P. chabaudi and P. anatis, have twohost life cycles with free-living cercariae and all
occurred rarely except P. acanthus (Table 1).
The most common digeneans of seabirds in Iceland
are represented in groups 1 and 2. In L. saxatilis and L.
fabalis, the frequency of occurrence of group 1 and 2
digeneans was approximately 50:50 (Fig. 2). The
representatives of group 1, however, predominated in
E. vincta and H. ventrosa, but those of group 2 were
more frequently found in L. obtusata, O. aculeus and N.
lapillus (Fig. 2).
COMPARISON OF PREVALENCE IN SKERJAFJÖRDUR AND
GRINDAVIK
Periwinkles collected in Grindavik had a signiŽ cantly
higher prevalence of M. similis, C. lingua, C. parvicaudata and C. littorina obtusata than those observed
from the Skerjafjördur area (Table 1). On the other
147
hand, the prevalence in N. lapillus of R. thaidus was
signiŽ cantly higher in Skerjafjördur than in Grindavik.
Infections of P. homoeotecnum were considerably
more frequent in periwinkles in Grindavik than in
Skerjafjördur (Table 1), but the opposite tendency was
observed in O. aculeus, of which higher infection
prevalences were reported in Skerjafjördur than in
Grindavik (Table 1).
Furthermore, the prevalence of M. pygmaeus in L.
obtusata was signiŽ cantly higher in Grindavik than in
Skerjafjördur (Table 1).
DISCUSSION
COMPOSITION OF THE DIGENEAN FAUNA
About 96% of the 70 breeding bird species in Iceland
are of Palaearctic origin and only 4% originate from the
Nearctic (Petersen 1998). It was, therefore, not surprising that digeneans of American origin were not found in
the Icelandic gastropods. All the species found have
been shown to occur either exclusively in Europe or in
both Europe and America (M. pygmaeus, M. linguilla,
R. thaidus, C. parvicaudata, P. acanthus) (James 1969;
Pohley 1976; Lauckner 1980; Stunkard 1983; Ching
1991; Galaktionov & Bustnes 1999; Galaktionov &
Skirnisson 2000). The geographical distribution of the
recently described C. islandica I is unknown.
The biodiversity of Icelandic seabird digeneans is
comparable with that found in the Barents Sea,
Norwegian Sea and the White Sea, but signiŽ cantly
less than the biodiversity observed in more southern,
Fig. 2. Frequency of occurrence of two groups of seabird digenean species (group 1 = species
with a two-host life cycle without free-living larvae; group 2 = species with a three-host life
cycle with a free-living miracidium and/or cercaria) in intertidal molluscs (infected specimens
only) of SW Iceland. Standard error of proportion is shown.
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148
Sarsia 87:144-151 – 2002
boreal regions of Europe and America. A total of 26
intramolluscan stages of digeneans has been documented from periwinkles from the coast of the British Isles
and France (James 1969; Combescot-Lang 1976;
Lauckner 1980; Irwin 1983), but only 14 have been
found in the Barents Sea and White Sea (Galaktionov &
Bustnes 1999). For H. ventrosa, these numbers are 16
and eight species, respectively (Deblock 1980; KV
Galaktionov, unpublished results). Only three digeneans (M. pseudopygmaeus, P. homoeotecnum and C.
littorina saxatilis VII) have been found in O. aculeus
inhabiting Arctic sea coasts (KV Galaktionov, unpublished results), whereas six species were recorded in this
study.
The approximate 50:50 group 1:group 2 digenean
ratio in SW Icelandic periwinkles is different from that
reported for northern and more southern regions. In
northern regions group 1 species predominate, whereas
in southern regions group 2 digeneans predominate
(Galaktionov & Bustnes 1999). This pattern suggests
that two-host life cycles without free-living larval
stages are adaptive in environments with extreme
conditions (e.g. Arctic intertidal). Under “milder”
ecological conditions, an advantage in transmission
gains digeneans with free-living larva(e) and a second
intermediate host in their three-host life cycle (Galaktionov & Bustnes 1999; Galaktionov & Dobrovolskij
2000).
The distribution of the group 1 and group 2 digeneans
among O. aculeus and H. ventrosa in the present study
also supports the suggestion outlined above. In Iceland,
both snail species are considered to be at the limits of
their geographical distribution; O. aculeus is at the
southern limits of its distribution, whereas H. ventrosa
is at its northern limits.
Only one species, M. pseudopygmaeus (a group 1
representative), has been found in O. aculeus on the
coast of the White Sea. On the eastern Murman coast of
the Barents Sea, the group 1:group 2 ratio is 88 (108
infected snails):12 (15 infected snails) (KV Galaktionov, unpublished results). In SW Iceland, however,
six species were found in O. aculeus and the group 1:
group 2 ratio was 21:79. The reason for this difference
is probably the same as previously suggested for the
other periwinkles. We also presume that the higher
number of digenean species in Icelandic O. aculeus, and
the shift of the group 1:group 2 species ratio towards
group 2, re ect that the ecological conditions in SW
Iceland are more favourable for the transmission of
three-host life cycles with free-living larvae than in NW
Russia and NE Norway.
Hydrobia ventrosa has been reported from seven
sites along the southwest and west coast of Iceland
(Skirnisson 1977; Oskarsson & al. 1977; Ingolfsson
1994, 1996). We collected the snails in Skerjafjördur
from brackish ponds in salt marsh where environmental
factors are generally regarded as harsh and unstable. As
noted above, such conditions are not advantageous for
the transmission of digeneans with three-host life cycles
(group 2). The group 1:group 2 ratio for H. ventrosa
was 87:13. As already discussed, this result was
anticipated.
COMPARISON OF PREVALENCE IN SKERJAFJÖRDUR AND
GRINDAVIK
Differences in the prevalence of some of the digenean
species found in Skerjafjördur and Grindavik are
probably related to differences in the abundance,
distribution and occurrence of the Ž nal hosts, the
respective marine and shore bird species. In Grindavik,
there is a big Ž shing port and close to the harbour there
is a large aquaculture complex. The village is the centre
of an intensive Ž sh industry and throughout the year Ž sh
offal attracts large gulls (especially Larus marinus, L.
argentatus and L. hyperboreus) and small larids (L.
ridibundus and Rissa tridactyla) to the area. In
Skerjafjördur, however, there is no Ž sh industry and
local accumulations of larids are not as prominent as in
Grindavik. Various geese and duck species, especially
S. mollissima, are abundant in Skerjafjördur during all
seasons. In contrast, the only frequently observed
anseriform bird in Grindavik is S. mollissima.
Among the digeneans predominating in periwinkles
in Grindavik, M. similis and C. lingua are gull-speciŽ c
parasites (Lauckner 1985) and there is a high probability that C. parvicaudata and C. littorina obtusata
may be as well. The two latter species belong to the
genera Renicola and Himasthla, respectively, and their
intramolluscan stages are closely related to digenean
species, which are typical gull parasites (Galaktionov &
Skirnisson 2000). The high prevalence of gull digeneans observed in periwinkles sampled in Grindavik is
probably the result of the rich larid fauna in the area.
Comparable results have been described in other
regions of Europe (for a review see Bustnes &
Galaktionov 1999; Bustnes & al. 2000). Microphallus
piriformes, a representative of the group 1 digeneans, is
a frequently found gull digenean in periwinkles on the
coasts of north Europe, where the ecosystems are
in uenced by Ž shing activity (Bustnes & Galaktionov
1999). However, the prevalence of M. piriformes in
periwinkles in Grindavik was not higher than in
Skerjafjördur and the increased prevalence of gull
digeneans observed in Grindavik was due to group 2
digeneans. Comparable observations have been made,
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Skirnisson & Galaktionov – Seabird digeneans in SW Iceland
and seem to be typical, on seashores of western and
southern parts of Europe (Germany, France, Great
Britain, Northern Ireland) (Hoff 1941; Bartoli & Prevot
1976; James & al. 1977; Lauckner 1984; Matthews &
al. 1985). In these regions, M. similis, C. lingua and
representatives of the genera Renicola and Himasthla,
dominate in gulls, whereas M. piriformes occurs
extremely rarely (Hoff 1941; Bartoli & Prevot 1976;
Lauckner 1984, 1987; Matthews & al. 1985).
The differing prevalence of R. thaidus in N. lapillus
in the two study areas was probably due to the very high
infection (51%) observed at a single sampling station in
Skerjafjördur (Grótta). The snails there were found to
be preying on Balanus balanoides attached to large
concrete pillars. Gulls frequently rest on these pillars
and they probably promoted the unusually high local
infection rates observed.
Similar circumstances probably also gave rise to
local increases in the prevalence of P. homoeotecnum in
periwinkles sampled in Grindavik. One particular
sampling site took the form of a shallow sandy beach
strewn with stones and seaweed. Here Haematopus
ostralegus, the Ž nal host for the species (James 1964),
accumulates in large numbers to search for food. In
total, 17% of the L. saxatilis sampled at this site
harboured intramolluscan stages of the parasite. This
type of habitat rarely occurs in Grindavik, but it is quite
common in Skerjafjördur where H. ostralegus is also
more abundant (Petersen 1998).
The distribution of C. littorina saxatilis VII cannot be
discussed as its Ž nal host is unknown.
The high prevalence (4.1%) of the speciŽ c eider
parasite M. pygmaeus in L. obtusata sampled in the
149
harbour of the Grindavik Ž shing port might be
explained by the fact that, in March and April each
year, thousands of eiders are attracted to the harbour
when Ž shing boats land capelin and a huge amount of
capelin eggs and Ž sh remains are washed into the
harbour.
The examples of the distribution patterns of larval
digeneans in their molluscan hosts discussed above
underline the fact that many different factors have to be
considered when parasitological data are to be
explained. These factors range from those which are
macro-scale in nature (e.g. climate, occurrence of hosts
in the geographical regions studied) to local micro-scale
in uences (local distribution of intermediate and Ž nal
hosts in the habitat, host abundance, etc.).
This study shows that digeneans with a three-host life
cycle with a free-living larval stage(s) are more
common in the studied areas of SW Iceland than in
the coasts of northernmost Europe. We suggest that the
relatively milder climate (due to the Gulf Stream), as
well as the abundance and diversity of potential Ž nal
hosts (birds) and second intermediate hosts (littoral
invertebrates and Ž shes) promote complex trematode
life cycles in the intertidal zones of SW Iceland.
ACKNOWLEDGEMENTS
The project was partly Ž nanced by grants from the Icelandic
Republic Fund 1994–1999 and the NATO Science Fellowship.
We wish to thank Dr E. Karlsbakk and two anonymous
reviewers for comments on a draft of the manuscript . We also
thank Dr S.W.B. Irwin for comments and correction of the
English.
REFERENCES
Bartoli P, Prevot G. 1976. Relations antre le proŽ l du lisere
cotier les ressources alimentaires et le parasitisme de
Larus argentatus par deux especes de trematodes.
Travaux ScientiŽ ques Parc National Port Cros 2:29–
38.
Brinkmann A. 1956. Trematoda. The Zoology of Iceland 2(11).
34 p.
Bustnes JO, Galaktionov KV. 1999. Anthropogeni c in uences
on the infestation of intertidal gastropods by seabird
trematode larvae on the southern Barents Sea coast.
Marine Biology 133:449–453.
Bustnes JO, Galaktionov KV, Irwin SWB. 2000. Potential
threats to littoral biodiversity: is increased parasitism a
consequenc e of human activity? Oikos 90:189–190.
Ching HL. 1991. List of larval worms from marine invertebrates of the PaciŽ c coast of North America. Journal of
the Helminthological Society of Washington 58:57–68.
Chubrik GK. 1966. Fauna and ecology of trematode larva from
molluscs of the Barents and White Sea. In: Poljansky
YI, editor. Life-cycles of parasitic worms from northern
seas. Leningrad: Nauka Press. p. 78–159 (in Russian).
Combescot-Lan g C. 1976. Etudes des digeneanse s parasites de
Littorina saxatilis (Olivi) et de leurs effect sur cet hôte.
Annales de Parasitologie Humaine et Comparee 51:27–
36.
Curtis LA, Hurd LE. 1983. Age, sex, and parasites: spatial
heterogeneity in a sand at population of Ilyanassa
obsoleta. Ecology 64:819–828.
Deblock S. 1980. Inventaire des trématodes larvaires parasites
des mollusques Hydrobia (Prosobranches ) des côtes de
France. Parassitologia 22:1–105.
Eydal M, Gunnlaugsd óttir B, Skirnisson K. 1994. The
occurrence of the digenean Cryptocotyl e lingua in the
coastal environment of Iceland. Bulletin of the Scandinavian Society for Parasitology 4:15–16.
Eydal M, Gunnlaugsdóttir B, Olafsdóttir D. 1998. Gulls
(Laridae) in Iceland as Ž nal hosts for digenean
trematodes. Parasitology International (Suppl.) 47:302.
Downloaded by [Stanford University Libraries] at 04:50 18 September 2012
150
Sarsia 87:144-151 – 2002
Galaktionov KV. 1985. The infection of males and females of
the genus Littorina molluscs (Gastropod: Prosobranchia) by trematode parasites at the Barents Sea shore.
Parazitologiya 19:213–219 (in Russian).
Galaktionov KV. 1993. Trematode life cycles as component s of
the ecosystem (an attempt to analyse by example of
representative s of the family Microphallidae). Kola:
ScientiŽ c Centre of the Russian Academy of Science
Publications (in Russian).
Galaktionov KV. 1995. Long term changes of composition of
the seabird helminth fauna on the Seven Island archipelago (eastern Murman). In: Skjoldal HR, Hopkins C,
Erikstad KE, Leinaas HP, editors. Ecology of fjords and
coastal waters. Amsterdam: Elsevier Science. p. 489–
496.
Galaktionov KV. 1996a. Life cycles and distribution of seabird
helminths in Arctic and subarctic regions. Bulletin of
the Scandinavian Society for Parasitology 6:31–49.
Galaktionov KV. 1996b. Impact of seabird helminths on host
populations and coastal ecosystems. Bulletin of the
Scandinavia n Society for Parasitology 6:50–64.
Galaktionov KV, Bustnes JO. 1995. Species composition and
prevalence of seabird trematode larvae in periwinkles at
two littoral sites in North Norway. Sarsia 80:187–191.
Galaktionov KV, Bustnes JO. 1999. Distribution patterns of
marine bird digenean larvae in periwinkles along the
southern Barents Sea coast. Diseases of Aquatic
Organisms 37:221–230.
Galaktionov KV, Dobrovolskij AA. 2000. An ecological
approach to the analysis of trematode life-cycle evolution. Bulletin of the Scandinavia n Society for Parasitology 10:13–18.
Galaktionov KV, Marasaev SF. 1990. Distribution of trematode infection in the Barents Sea. In: Matishov GG,
editor. Ecology and biological productivity of the
Barents Sea. Moscow: Nauka Press. p. 37–47.
Galaktionov KV, Skirnisson K. 2000. Digeneans from intertidal molluscs of SW Iceland. Systematic Parasitology
47:87–101.
Gardarsson A, Adalsteinsdottir K. 1977. Rannsóknir õ´ SkerjaŽ rdi. I. Botndýralõ´f. Fjölrit 9. Reykjavõ´k: Lõ´ffrædistofnun Háskólans. 83 p.
Gorbushin AM. 1997. Field evidence of trematode-induce d
gigantism in Hydrobia spp. (Gastropoda: Prosobranchia). Journal of the Marine Biological Association of
the United Kingdom 77:785–800.
Granovitch AI. 1992. The effect of trematode infection on the
population structure of Littorina saxatilis (Olivi) in the
White Sea. In: Grahame J, Mill PJ, Reid DG, editors.
Proceedings of the third international symposium on
littorinid biology. Malacological Society of London. p.
255–263.
Hoff CC. 1941. A case of correlation between infection of snail
hosts with Cryptocotyle lingua and the habits of gulls.
Journal of Parasitology 27:539.
Ingolfsson A. 1977. Rannsóknir õ´ SkerjaŽ rdi. II. Lõ´frõ´ki fjöru.
Fjölrit 10. Reykjavõ´k: Lõ´ffrædistofnun Háskólans. 94 p.
Ingolfsson A. 1994. Species assemblages in saltmarsh ponds in
western Iceland in relation to environmenta l variables.
Estuarine, Coastal and Shelf Science 38:235–248.
Ingolfsson A. 1996. The distribution of intertidal macrofauna
on the coast of Iceland in relation to temperature. Sarsia
81:29–44.
Irwin SWB. 1983. Incidence of trematode parasites in two
populations of Littorina saxatilis (Olivi) from the north
shore of Belfast Lough. Irish Naturalist’s Journal
21:26–29.
James BL. 1964. The life cycle of Parvatrema homoeotecnum
sp. nov. (Trematoda: Digenea) and review of the family
Gymnophallidae Morozov, 1955. Parasitology 54:1–
41.
James BL. 1968. The occurrence of larval Digenea in ten
species of intertidal prosobranc h molluscs in Cardigan
Bay. Journal of Natural History 2:329–343.
James BL. 1969. The Digenea of the intertidal prosobranc h
Littorina saxatilis (Olivi). Zeitschrift für Zoologie,
Systematik und Evolutionforschun g 7:273–316.
James BL, Sannia A, Bowers EA. 1977. Parasites of birds and
shellŽ sh. In: Nelson-Smith A, Bridges EM, editors.
Problems of a small estuary. Proceedings of the Burry
Inlet Symposium, University College Swansea, 1976.
Swansea: Institute of Marine Studies and Quadrant
Press. p. 1–16.
Kristoffersen R. 1991. Occurrence of the digenean Cryptocotyle lingua in farmed Arctic charr Salvelinus alpinus
and periwinkles Littorina littorea sampled close to charr
farms in northern Norway. Diseases of Aquatic Organisms 12:59–65.
Kulachkova VG. 1979. Helminths as a cause of common
eider’s death in the top of Kandalaksha Bay. In:
Kischinski AA, editor. Ecology and morpholog y of
eiders in the USSR. Moscow: Nauka Press. p. 119–125
(in Russian).
Lauckner G. 1980. Diseases of Mollusca: Gastropoda. In:
Kinne O, editor. Diseases of marine animals, Vol. I.
Hamburg: Biologische Anstalt Helgoland. p. 311–424.
Lauckner G. 1984. Impact of digenean parasitism on the fauna
of North Sea tidal  at. Helgoländer Wissenschaftliche
Meeresuntersuchungen 37:185–199.
Lauckner G. 1985. Diseases of Aves (marine birds). In: Kinne
O, editor. Diseases of marine animals, Vol. IV, Part 2.
Hamburg: Biologische Anstalt Helgoland. p. 627–643.
Lauckner G. 1987. Ecological effects of larval digenean
infestation on littoral marine invertebrate populations.
International Journal for Parasitology 17:391–398.
Matthews PM, Montgomery WI, Hanna REB. 1985. Infestation of littorinids by larval digenea around a small
Ž shing port. Parasitology 90:277–287.
Oskarsson I, Ingolfsson A, Gardarsson A. 1977. Hydrobia
ventrosa recorded in Iceland. Náttúrufrædingurinn
47:8–15.
Petersen Ae. 1998. Íslenskir fuglar. Reykjavõ´k: Vaka-Helgafell. 312 p.
Podlipaev SA. 1979. Parthenities and larva of trematodes in
intertidal molluscs of the Eastern Murman. In: Poljanskii YuI, editor. Ecological and experimental parasitology, Vol. 2. Leningrad: Izdatel’stvo Leningradskog o
Universiteta. p. 47–101 (in Russian).
Pohley WJ. 1976. Relationships among three species of
Littorina and their larval Digenea. Marine Biology
37:179–186.
Robson EM, Williams IC. 1970. Relationships of some species
Skirnisson & Galaktionov – Seabird digeneans in SW Iceland
Downloaded by [Stanford University Libraries] at 04:50 18 September 2012
of Digenea with the marine prosobranch Littorina
littorea (L.). 1. The occurrence of larval Digenea in L.
littorea of the North Yorkshire coast. Journal of
Helminthology 44:153–168.
Rothschild M. 1941. The effect of trematode parasites on the
growth of Littorina neritoides (L.). Journal of the
Marine Biological Association of the United Kingdom
25:69–80.
Sannia A, James BL. 1977. The digenea in marine molluscs
from Eyjafordur, North Iceland. Ophelia 16:97–109.
Skarphedinsso n KH, Einarsson O. 1989. Fuglalõ´f á sunnanverdum Reykjanesskaga . In: Egilsson K, editor.
151
Náttúrufar á sunnanverdu m Reykjanesskaga. Reykjavõ´k: Náttúrufrædistofnun Íslands. p. 37–58.
Skirnisson K. 1977. Athuganir á lṍfrṍki Melabakka ṍ Hnappadalssýslu. Mimeographed manuscript . Reykjavõ´k: Lõ´ffraediskor Háskóla Íslands. 32 p.
Skirnisson K, Jónsson AA. 1996. Parasites and ecology of the
common eider in Iceland. Bulletin of the Scandinavian
Society for Parasitology 6:126–127.
Stunkard HW. 1983. The marine cercariae of the Woods Hole,
Massachusett s region, a review and a revision. Biological Bulletin 164:143–162.
Accepted 20 February 2001 – Printed 15 July 2002
Editorial responsibility: Egil Karlsbakk