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Helminth Parasites in Ringed Seals (Pusa hispida) From Svalbard, Norway withSpecial Emphasis on Nematodes: Variation with Age, Sex, Diet, and Location ofHostAuthor(s): Carina E. Johansen, Christian Lydersen, Paul E. Aspholm, Tore Haug, and Kit M. KovacsSource: Journal of Parasitology, 96(5):946-953. 2010.Published By: American Society of ParasitologistsDOI: http://dx.doi.org/10.1645/GE-1685.1URL: http://www.bioone.org/doi/full/10.1645/GE-1685.1

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HELMINTH PARASITES IN RINGED SEALS (PUSA HISPIDA) FROM SVALBARD, NORWAY

WITH SPECIAL EMPHASIS ON NEMATODES: VARIATION WITH AGE, SEX, DIET, AND

LOCATION OF HOST

Carina E. Johansen, Christian Lydersen, Paul E. Aspholm*, Tore Haug�`, and Kit M. Kovacs§Norwegian Polar Institute, N-9296 Tromsø, Norway. e-mail: Kit.Kovacs@npolar.no

ABSTRACT: Complete gastrointestinal tracts from 257 ringed seals (Pusa hispida) from Svalbard, Norway, were examined for helminthparasites. Three different helminth groups were recorded (acanthocephalans 61.1%; nematodes 38%; cestodes 0.9%). Acanthoceph-alans (Polymorphidae) and cestodes (Anophryocephalus and Diphyllobothrium sp(p)., as well as unidentified species, were confined tothe intestines. The anisakid nematodes Phocascaris phocae, Pseudoterranova sp(p)., Anisakis sp(p)., and Phocascaris/Contracaecumsp(p). were recorded in both stomachs and the anterior part of the small intestines. The abundance of nematodes and acanthocephalansvaried significantly with sampling location of the seal hosts. This is likely due to the relative prevalence of Arctic versus Atlantic waterin the different fjord systems, which strongly influences the age class and species of fish available as prey for the seals. Adult maleringed seals had significantly higher abundances of nematodes than did adult females or juveniles. Adult males also had significantlyhigher abundances of acanthocephalans than did adult females, but were not significantly different from juveniles in this regard.Nematode abundance increased significantly with age of male hosts, but this trend was lacking in female seals. Infection parametersappeared to be related to differences in the age of polar cod (Boreogadus saida) exploited by male, female, and juvenile seals.

The ringed seal (Pusa hispida) is the most abundant of the arctic

seals. This species has a circumpolar distribution and is generally

found in close association with sea ice (Reeves, 1998). Ringed

seals are the most abundant marine mammal in Svalbard,

Norway (Lydersen, 1998), where they occupy the land-fast ice

of the many fjords of this archipelago during the months of the

year when annually-formed sea ice is present, especially during

their breeding and molting periods in spring (Krafft et al., 2006);

the rest of the year, ringed seals are more mobile and often spend

time pelagically along the southern edges of the polar ice pack

(Gjertz et al., 2000; Freitas et al., 2008).

Studies of the diet of ringed seals from Svalbard have shown

that these seals feed on a wide variety of prey organisms, but that

the most important prey species is the polar cod (Boreogadus

saida). Several species of crustaceans, such as the krill Thysa-

noessa inermis and the amphipod Parathemisto libellula, can be

important seasonally, particularly to juvenile seals (Gjertz and

Lydersen, 1986; Lydersen et al., 1989; Weslawski et al., 1994;

Labansen et al., 2007). Despite the many dietary investigations of

ringed seals from Svalbard and elsewhere in the Arctic, almost

nothing is known about the helminth parasite communities found

in their gastrointestinal tracts (GIT). Little research has been

conducted on helminth parasites in ringed seals from the Arctic in

general, and samples sizes in available studies tend to be small

(Vik, 1986; Adams, 1988; Popov et al., 1993; Treshchev and

Popov, 1993; Measures and Gosselin, 1994). However, several

ecologically-oriented parasitological studies that have been

conducted on ringed seals in the Baltic Sea have resulted in

interesting suggestions regarding the foraging ecology of the seals

and the relationships (or the lack thereof) between parasite and

host densities (Valtonen et al., 2004; Sinisalo et al., 2006, 2008).

The purpose of the present paper is to describe the helminth

fauna found in the GITs of ringed seals collected at various

locations in the High Arctic Archipelago of Svalbard. Patterns of

variation in the occurrence of helminth parasites with host age,

sex, diet, and location are examined.

MATERIALS AND METHODS

Complete GITs were collected from 257 ringed seals from northwesternSpitsbergen, Svalbard, Norway (Fig. 1) during the period 12 April–24May, 2002–2004. The seals were shot on land-fast ice at 5 differentlocations: (1) Wijdefjorden; (2) Kongsfjorden; (3) Forlandsundet & St.Jonsfjorden; (4) Billefjorden; and (5) Recherchefjorden & Van Keulenf-jorden. Collections were made in Wijdefjorden and Billefjorden in 2002and 2003, Forlandsundet & St. Jonsfjorden in 2003, and Kongsfjordenand Recherchefjorden & Van Keulenfjorden in 2004. Following extrac-tion, each GIT was tied with a string at the esophagus and rectum andpacked in a plastic bag. Samples were frozen immediately and kept frozenuntil laboratory analyses were performed. Reproductive organs and thelower jaw (with teeth) were also collected from each seal to determinestage of sexual maturity and age. The ringed seals were aged by countingcementum layers in decalcified, stained, longitudinal sections of canineteeth as described in Lydersen and Gjertz (1987). The ovaries wereanalyzed macroscopically for the presence of mature follicles, corporalutea, or corpora albicantia, all of which were taken as evidence of sexualmaturity in females. Testes were examined microscopically; the presence ofspermatozoa in the epididymis, or spermatogenesis in the seminiferoustubules, was taken as evidence of sexual maturity in males (Lydersen andGjertz, 1987).

In the laboratory, each GIT was thawed and separated into 3 parts;stomach with esophagus, small intestine (SI), and large intestine (LI).Then the SI, which had an average length of 14.3 m (±SD 2.4), was furtherdivided into 2 equal parts (SI anterior [SIa] and SI posterior [SIp]). Thestomach, SIa, SIp, and LI were analyzed separately. Each GIT section wascut longitudinally and thoroughly washed with lukewarm tap water indark plastic bowls; attached parasites were carefully removed from theGIT tissue using forceps. The contents of the various parts of the GITwere then washed over an interconnecting sieve system with mesh sizesranging from 2.0, 1.0, to 0.5 mm from top to bottom, respectively. Looseparasites were handpicked from the contents and preserved in 70%ethanol (Gibson, 1984) together with the parasites that were removed fromthe GIT walls.

Parasites were initially inspected using either a binocular light ordissecting microscope. In preparation for further analyses, the nematodeswere cleared for 2–4 min in a Petri dish that contained acetic acid. Theworms were then transferred to glycerol for further clearing for 2–15 min(Gibson, 1984). The clearing time varied depending on the size of thenematodes. The various species and stages of nematodes were determinedusing available keys (Myers, 1960; Berland, 1963; Grabda, 1976;Fagerholm, 1989; Host, 1990). The identified worms were categorized as3rd or 4th stage larvae, adult males (developed spicules), adult females

Received 7 May 2008; revised 8 October 2009, 19 April 2010; accepted 20April 2010.

* Bioforsk Soil and Environment Svanhovd, N-9925 Svanvik, Norway.{Department of Aquatic Biology, Norwegian College of Fishery Science,

University of Tromsø, N-9037 Tromsø, Norway.{ Institute of Marine Research, N-9294 Tromsø, Norway.}To whom correspondence should be addressed.

DOI: 10.1645/GE-1685.1

J. Parasitol., 96(5), 2010, pp. 946–953

F American Society of Parasitologists 2010

946

with eggs (developed eggs in uterus), and adult females without eggs (noeggs in uterus). Because the interlabia of Contracaecum osculatum appearafter the last molt, the larvae of Phocascaris spp. and C. osculatum aremorphologically indistinguishable (Berland, 1963; McClelland and Ron-ald, 1974; Likely and Burt, 1992); thus, 3rd- and 4th-stage larvae of these 2groups were merged. Anisakid nematodes that infest phocid seals maturein the seal’s stomach, but Phocascaris spp. also reach maturity in the SIa(Berland, 1963; Adams, 1988; Measures and Gosselin, 1994); thus, onlynematodes from the stomach and SIa were identified to species level.Nematodes found in the SIp and LI were simply counted (not identified)in order to have a more complete assessment of total parasite loads in theentire gut track at a time when helminth mortality is likely to besignificant. Clusters of larvae occurred in some seal stomachs, and theanterior parts of the nematodes were often firmly anchored in the center ofthe cluster such that larvae could not be extracted without sustainingdamage. Damaged larvae, lacking their boring tooth or lips, were pooledand categorized only as 3rd–4th stage larvae. Heads and tails of brokennematodes found in the stomach and SIa were identified and counted lastin each sample. Head or tail parts of broken nematodes found in SIp andLI were not identifiable; the number of broken parts was multiplied by0.67, a fraction based on the head-to-tail ratio found in the stomach andSIa, to estimate the number of worms represented by these fragments inthis GIT section. For clusters of nematodes in the stomach wall containingmore than 150 individuals, a random sample of approximately 40% of theworms was picked out and identified (all were counted). In the SIa, thenematodes were not found in large numbers and sub-sampling was notnecessary.

The acanthocephalans were identified to family based on availableliterature (Delyamure, 1968; Margolis and Kabata, 1989). The cestodes(all belonging to the Eucestoda based on scolex morphology [Delyamure,1968]) were small and fragile and only a few could be identified to genus(following Delyamure, 1968). Because so few cestodes were present in theringed seals, they were not included in statistical analyses of the data.

The diet of the ringed seals included in this study was investigated byLabansen et al. (2007). Polar cod was found to dominate the diet, andinformation on the fraction of various year classes of polar cod (based onmeasurements of otoliths) ingested by the individual seals was used in thisstudy to see if this factor had any impact on the observed parasite burdens.

Year classes of polar cod consumed were available from the GITs of 134ringed seals (n 5 134), including individuals from all 5 sampling locations.

Explanatory analysis and inferential statistics were conducted usingMicrosoft ExcelH (Microsoft Corporation, Redmond, Washington) andR 2.7.0 (R Development Core Team, 2008). The terms prevalence(percentage of seals infested), abundance (mean number of parasites perseal), intensity (number of parasites in each infested seal), and meanintensity (mean number of parasites in each infested seal) are based on thedefinitions of Margolis et al. (1982). Geographical location, sex, age, anddiet-related differences in the abundance of nematodes or acanthoceph-alans from the whole GIT were analyzed using generalized linear models(GLMs). GLMs were run on each seal category (adult male, adult female,and juvenile) and the 5 sample locations (AB 5 b1 seal category + b2

location) to test for sex, age, or geographical effect in abundance ofnematodes (or acanthocephalans; run with separate models). All of the257 ringed seals were included (n 5 257). Parasite abundance was thedependent factor in all of the models. Analysis of deviance was applied toall of the GLMs to test for significant effects of the different independentvariables (b). Nematode and acanthocephalan abundances were over-dispersed (the residual deviance was larger than the residual degree offreedom). To adjust for this, a quasi-poisson distribution of the error termwas assumed when running the GLMs. Additionally, GLMs were run totest for effect of year classes of consumed polar cod, expressed as afraction of old (2-yr-old and older polar cod) polar cod compared toyoung (year class ,2) polar cod found in GIT (AB 5 b1 fraction of olderpolar cod digested). A 2-way ANOVA was run on host-class (adult males,adult females, and juveniles) versus location. The statistical significancelevel was set at P # 0.05.

RESULTS

The seals in this study included 137 adult males, 76 adult

females, and 44 juveniles. All age–sex classes occurred at each

location, although they were not evenly distributed (n 5 257,

Table I). The ages of the seals ranged from 1–30 yr. A total of

53,159 helminth parasites was recorded in the GITs of these seals;

61.1% were acanthocephalans, 38.0% nematodes, and 0.9%

cestodes (Table II). The GITs of all but 1 of the ringed seals

had nematodes (prevalence 5 99.6%) (Table II). Nematode

intensity ranged from 1 to 602. All GITs contained acanthoceph-

alans (prevalence 5 100%) (Table II). Acanthocephalan intensity

ranged from 7 to 1,093. Only 30 ringed seals were infested with

cestodes (prevalence 5 11.7%) (Table II). Cestode intensity

ranged from 1 to 120. The helminth parasites were not evenly

distributed throughout the GIT of the ringed seals. The stomachs

contained only nematodes, while acanthocephalans were predom-

inantly found in the small intestines (Table II).

In total, 11,024 nematodes were found in the stomachs and SIa

(Table II). All of the identified nematodes belonged to the

Anisakidae; 228 of the 257 stomachs examined were infested

with nematodes (prevalence 5 88.7%) and 172 of the SIa

TABLE I. Numbers of ringed seals, Pusa hispida, collected from variousareas in northwestern Spitsbergen, Svalbard, sorted by age–sex categories.Wijd 5 Wijdefjorden, Kong 5 Kongsfjorden, FSJ 5 Forlandsundet & St.Jonsfjorden, Bill 5 Billefjorden, RVK 5 Recherchefjorden &Van Keulenfjorden.

Seal category

Sampling location

TotalWijd Kong FSJ Bill RVK

Adult males 17 33 33 46 8 137

Adult females 11 34 8 19 4 76

Juveniles 2 28 1 12 1 44

Total 30 95 42 77 13 257

FIGURE 1. Map of Svalbard showing the sampling locations onSpitsbergen (sample sizes are in parentheses) and major ocean currentsinfluencing the biota of the fjords. The white areas on the map indicate thedistribution of land-fast ice during the sampling periods.

JOHANSEN ET AL.—HELMINTH PARASITES IN RINGED SEALS 947

contained nematodes (prevalence 5 66.9%). Larvae of Phocas-

caris/Contracaecum sp(p.) (92.6%) were much more numerous

than adult worms (Table III). They were especially numerous in

the stomachs where large clusters of larvae were attached to the

stomach walls. Prevalence, abundance, and mean and maximum

intensities for the various species of nematodes are described in

Table III.

Pseudoterranova and Anisakis specimens were not common, but

they occurred in ringed seals from all 5 sampling locations

(Table III). Twenty-eight of the 257 ringed seals investigated were

infested with Pseudoterranova; it occurred more commonly in the

stomach than in the SIa (Table II). Only 52 Anisakis were found,

in total, in 29 infested ringed seals. These parasites were slightly

more prevalent in the stomach as compared to the SIa (Table II).

The acanthocephalans from the GIT were all species within the

Polymorphidae. All but 1 of the 257 SIa examined were infested

with acanthocephalans (Table II). The intensity of infestation

ranged from 1–297. All of the 257 SIp were infested with

anthocephalans, with an intensity ranging from 2–364 (Table II).

Fewer acanthocephalans were found in the LI; the intensity of the

acanthocephalans in the LI ranged from 1–1,041.

All of the cestodes found (Table II) belonged to Eucestoda.

Identified species were all Anophryocephalus or Diphyllobothrium

spp. Most of the cestodes (90.1%) were found in the SIa

(Table II). Two adult males and 2 juveniles contained 70% of

the cestodes recorded in the GITs.

GLM analyses suggested that seal category (P , 0.01) and

location (P , 0.001) had significant effects on the abundance of

nematodes and acanthocephalans, with no significant interaction

between these variables (P 5 0.87). Adult males had the highest

abundances of nematodes and acanthocephalans, while adult

females and juveniles had similar, lower burdens (though adult

males were not statistically significantly different than juveniles

[P . 0.05] with respect to acanthocephalans) (Table IV).

Seals from Billefjorden had the highest abundance of nema-

todes, while seals in Recherchefjorden & Van Keulenfjorden had

the highest abundance of acanthocephalans. Only Billefjorden

and Forlandsundet & St. Jonsfjorden differed significantly with

respect to the abundance of nematodes (Table V). The situation

was somewhat more complicated for acanthocephalans. For this

group of parasites, Kongsfjorden had the lowest abundances and

was significantly different from all other locations (Table V), and

Recherchefjorden & Van Keulenfjorden, which had the highest

abundance of acanthocephalans, was also significantly different

from all other locations (Table V).

ANOVA results showed that the number of nematodes

increased significantly with increasing age for adult males (P ,

0.02), but not for adult females (P . 0.60). No relation between

host sex and age was found for the abundance of acanthoceph-

alans (P . 0.05). Additionally, ringed seals that had eaten a

higher proportion of older polar cod had a significantly higher

abundance of nematodes (P , 0.001); this factor did not have the

impact of the abundance of acanthocephalans (P . 0.72, Fig. 2).

DISCUSSION

The ringed seals in this study were collected late in the breeding

season and during the molt, which is a period when all age groups,

except pups of the year, are in a state of negative energy balance

(Ryg et al., 1990). Although the reduced food consumption

during this period of the year reduces general body condition, it is

a natural part of the annual cycle for all phocid seals. Many of the

animals included in this study were surveyed for Brucella spp.

infections, and were also subjected to a general health screening of

their serum chemistry, without finding any abnormal values

(Tryland et al., 2005, 2006), suggesting that they were generally in

good health.

The helminth parasites found in the ringed seals in this study

showed the same general pattern of distribution throughout the

GIT as has been found in studies of ringed seals conducted

elsewhere in the Arctic. Only nematodes were found in the

stomachs, while acanthocephalans, nematodes, and cestodes were

all found in various parts of the intestines (Vik, 1986; Adams,

1988; Popov et al., 1993; Treshchev and Popov, 1993).

The most numerous nematodes found in the ringed seals were

Phocascaris/Contracaecum sp(p.) larvae, which is again similar to

what has been documented for ringed seals from other Arctic and

sub-Arctic areas, i.e., Newfoundland and Labrador (Brattey and

Stenson, 1993), the southeastern Barents Sea (Treshchev and

Popov, 1993), Icelandic waters (Palsson, 1977), and Alaska

(Adams, 1988). Adult Phocascaris observed in this study lacked

interlabial knobs and, thus, were identified as P. phocae. This

species has a Holarctic distribution and has previously been

identified in ringed seals in the southeastern part of the Barents

TABLE II. Numbers (N), percent of total (%) and prevalence (P) ofnematodes acanthocephalans and cestodes found in the gastrointestinaltracts (GITs) of 257 ringed seals, Pusa hispida, from northwesternSpitsbergen, Svalbard. Larvae are 3rd- and 4th-stage Phocascaris–Contracaecum sp(p.). SIa 5 anterior part of small intestine, SIp 5posterior part of small intestine, LI 5 large intestine.

Helminth group GIT-compartments N (%) P

Nematodes .Stomach . . .

. Phocascaris phocae 52 0.6 6.2

. Pseudoterranova spp. 119 1.3 7.4

. Anisakis spp. 29 0.3 5.6

. Larvae 8,714 94.9 88.7

. Unknown 265 2.9 12.5

.Total 9,179 100.0 88.7

.SIa . . .

. Phocascaris phocae 308 16.7 16.0

. Pseudoterranova spp. 15 0.8 4.3

. Anisakis spp. 23 1.3 3.9

. Larvae 1,456 78.9 66.9

. Unknown 43 2.3 9.3

.Total 1,845 100.0 66.9

.SIp 3,891 100.0 86.4

.LI 5,314 100.0 93.0

.Whole GIT 20,229 38.0 99.6

Acanthocephalans .Stomach 0 0.0 0.0

.SIa 10,182 31.4 99.6

.SIp 17,211 53.0 100.0

.LI 5,064 15.6 90.7

.Whole GIT 32,457 61.1 100.0

Cestodes .Stomach 0 0.0 0.0

.SIa 426 90.1 11.7

.SIp 44 9.3 10.5

.LI 3 0.6 0.8

.Whole GIT 473 0.9 11.7

948 THE JOURNAL OF PARASITOLOGY, VOL. 96, NO. 5, OCTOBER 2010

Sea (Treshchev and Popov, 1993), northern Quebec, Canada

(Measures and Gosselin, 1994), and Alaska (Adams, 1988). Two

other species from this genus have been recorded in GITs of

ringed seals; P. cystophorae has been described from ringed seals

from the Sea of Okhotsk (Popov et al., 1993), Alaska (Adams,

1988), and Icelandic waters (Palsson, 1977), while P. netsiki was

found in ringed seals from the eastern Canadian Arctic (Lyster,

1940).

Members of Phocascaris and Contracaecum are common

parasites in Arctic seal species such as harp (Phoca groenlandica),

hooded (Cystophora cristata), and bearded seals (Erignathus

barbatus), in addition to ringed seals (Scott and Fisher, 1958;

Adams, 1988; Brattey and Ni, 1992; Brattey and Stenson, 1993;

Measures and Gosselin, 1994), and the species Phocascaris phocae

is common in these northern seals. Phocascaris decipiens has a

more boreal distribution and is more common in grey (Hali-

choerus grypus) and harbor seals (Phoca vitulina) (McClelland,

1980; Brattey and Stenson, 1993; Olafsdottir and Hauksson, 1997,

1998), but was found in this study in significant numbers. The

normal definitive hosts for Anisakis simplex are cetaceans

(Ugland et al., 2004); however, as shown here, some Anisakis

spp. can be found in phocid stomachs, though they rarely mature

in seal hosts (Brattey and Stenson, 1993; Marcogliese et al., 1996).

TABLE III. Prevalence, abundance, and mean and maximum intensity (no. of parasites in each infested host) of nematodes in the stomachs and the smallintestine (SIa) of 257 ringed seals, Pusa hispida, from various areas in northwestern Spitsbergen, Svalbard. Wijd 5 Wijdefjorden, Kong 5 Kongsfjorden,FSJ 5 Forlandsundet & St. Jonsfjorden, Bill 5 Billefjorden, RVK 5 Recherchefjorden & Van Keulenfjorden, (—) 5 not observed.

Nematode Variable All areas

Sampling areas

Wijd Kong FSJ Bill RVK

Phocascaris phocae .Prevalence 18.7 23.3 20.0 3.9 20.8 7.7

.Abundance 1.4 1.3 1.7 0.1 2.0 0.2

.Mean intensity 7.5 5.1 8.3 1.3 9.7 3.0

.Maximum intensity 68 22 37 2 68 3

.% adult male 24.2 17.5 24.7 — 25.8 33.3

.% adult female 45.3 35.0 44.9 100.0 46.5 66.7

.% immature 30.6 47.5 30.4 — 27.7 —

Pseudoterranova sp(p). .Prevalence 10.9 6.6 13.7 11.9 7.8 7.7

.Abundance 0.5 0.1 1.0 0.3 0.3 0.1

.Mean intensity 5.7 1.5 7.3 2.8 3.5 1.0

.Maximum intensity 32 2 32 5 8 1

.% 3rd-stage larvae 50.8 33.3 49.5 28.6 71.4 100.0

.% 4th-stage larvae 17.9 66.7 11.6 64.3 9.5 —

.% 3rd–4th-stage larvae 31.3 — 39.0 7.1 19.1 —

Anisakis sp. .Prevalence 11.3 6.7 13.7 11.9 6.5 7.7

.Abundance 0.2 0.1 0.2 0.2 0.3 0.2

.Mean intensity 1.8 1.0 1.6 1.6 3.8 2.0

.Maximum intensity 5 1 4 3 8 2

.% 3rd-stage larvae 37.9 50.0 47.6 0.0 36.8 100.0

.% 4th-stage larvae 20.7 — 9.5 62.5 63.2 —

.% 3rd–4th-stage larvae 41.4 50.0 42.0 37.5 100.0 —

Phocascaris/Contracaecum sp(p). .Prevalence 92.6 96.7 93.7 88.1 92.2 92.3

.Abundance 39.6 46.5 32.1 15.8 64.0 10.2

.Mean intensity 42.7 48.1 34.3 15.8 69.4 11.1

.Maximum intensity 525 309 343 18 525 33

.% 3rd-stage larvae 23.8 9.3 19.5 3.8 33.7 5.3

.% 4th-stage larvae 37.8 43.8 35.0 76.3 31.6 76.7

.% 3rd–4th-stage larvae 38.5 46.9 45.6 19.9 34.7 18.1

TABLE IV. Mean abundance of parasites among various age and sexgroups of ringed seals, Pusa hispida, collected from northwesternSpitsbergen, Svalbard.

Seal category

Mean abundance (±SE)

All helminths Acanthocephalans Nematodes Cestodes

Adult males 254.5 (13.6) 155.2 (9.7) 97.8 (8.9) 1.4 (0.8)

Adult females 148.2 (21.0) 92.6 (15.0) 55.1 (12.1) 0.3 (0.2)

Juveniles 156.8 (18.3) 97.5 (14.9) 54.6 (8.0) 4.7 (3.1)

TABLE V. Summary table of the P-values from the comparisonsinvestigating potential differences in abundance of the nematodes andacanthocephalans between the 5 sample locations. The P-values areadjusted according to a Bonferroni correction and significant P-values aregiven in bold. Wijd 5 Wijdefjorden, Kong 5 Kongsfjorden, FSJ 5

Forlandsundet & St. Jonsfjorden, Bill 5 Billefjorden, RVK 5 Recherch-efjorden & Van Keulenfjorden.

Area

Nematodes Acanthocephalans

Wijd Kong FSJ Bill RVK Wijd Kong FSJ Bill RVK

Wijd — — — — .— — — — — .—

Kong 1.000 — — — .— ,0.001 — — — .—

FSJ 0.151 0.354 — — .— 1.000 ,0.001 — — .—

Bill 1.000 0.186 0.001 — .— 1.000 ,0.001 1.000 — .—

RVK 0.419 0.728 1.000 0.104 .— 0.037 ,0.001 0.042 0.008 .—

JOHANSEN ET AL.—HELMINTH PARASITES IN RINGED SEALS 949

The most abundant helminth group found in the GITs of the

ringed seals was acanthocephalans, all of which belonged to the

Polymorphidae. Two genera from this family (Bolbosoma and

Corynosoma) have previously been recorded in ringed seals

(Dailey, 1975; Adams, 1988; Popov et al., 1993). Bolbosoma

nipponicium is the only species of this genus confirmed in ringed

seals; it has been found in low numbers in ringed seals from the

Sea of Okhotsk (Popov et al., 1993; Adams, 1998). Several species

of Corynosoma have been found in the intestines of ringed seals in

the Arctic (Delyamure, 1968; Dailey, 1975; Adams, 1988; Popov

et al., 1993; Treshchev and Popov, 1993).

The prevalence and the numbers of cestodes found in this study

were low, which is a trend that is in accordance with previous

findings in ringed seals from the southeastern and western parts of

the Barents Sea (Vik, 1986; Treshchev and Popov, 1993) and

Alaska (Adams, 1988). Five species of Anophryocephalus have

previously been identified in ringed seals, i.e., A. anophryus, A.

inuitorum, and A. arcticensis are endemic to the Arctic and sub-

Arctic regions of the Atlantic Basin (Hoberg and Measures, 1994;

Hoberg, 1995), while A. skjabini and A. nunivakensis are both

endemic to the north Pacific Basin (Hoberg and Measures, 1994).

Additionally, 3 species of Diphyllobothrium (D. lanceolatum, D.

hians, and D. latum) have been found in ringed seals (Adams,

1988). Other cestodes known to infest ringed seals are Diplogo-

noporus fasciatus, D. tetrapterus, Pyramicocephalus phocarum,

Schistocephalus solidus, Trigonoctyle skrjabini, and Tetrabothrium

sp. (Dailey, 1975; Adams, 1988).

Analyses of the GIT contents of all the ringed seals included in

this study showed that their diet was dominated by polar cod

(Labansen et al., 2007). This species has a circumpolar

distribution and is one of the most abundant fish in the Arctic

(Falk-Petersen et al., 1986). It has been found to be the most

important prey species for ringed seals in Spitsbergen over a

period of decades (Gjertz and Lydersen, 1986; Lydersen et al.,

1989; Weslawski et al., 1994), as well as being very important prey

for ringed seals in other regions (see Reeves, 1998, for review).

Largely because the polar cod is not an important commercial

species for human consumption, little is known about its role as a

host for helminth parasites. However, larvae of A. simplex, P.

decipiens, and C. osculatum have been found in polar cod (Shults

and Frost, 1988; Paggi et al., 1991; Mattiucci et al., 1997), as well as

cystacanths of C. strumosum and C. semerme and plerocercoids of

Diphyllobothrium spp. (Karasev and Mitenev, 1993).

Labansen et al. (2007) identified the polar cod in their study

using otoliths; these structures can remain from 4 hr up to 2 days

in the GITs of ringed seals (Parsons, 1977; Helm, 1984). The

development time from the 3rd- to the 4th-stage larvae is about 2–

5 days for both P. decipiens (McClelland, 1982) and C. osculatum

(Fagerholm, 1989). Because most of the nematodes recorded in

this study were 3rd- or 4th-stage larvae, and polar cod heavily

dominated the diet of the hosts, it is reasonable to assume that

most of the nematodes were derived from this fish species. The

low number of identifiable adult A. simplex and P. decipiens

found in this study, and elsewhere, in ringed seals suggests that

this seal species is not an ideal definitive host for these parasites

(Palsson, 1977; Brattey and Stenson, 1993; Popov et al., 1993).

Abiotic factors such as ocean temperature are likely important

to the distribution and abundance of the anisakid nematodes.

When eggs of P. decipiens, C. osculatum, and P. phocae are passed

into the sea water with the host’s feces, they sink and are

consequently exposed to the bottom temperatures (Brattey, 1990).

Eggs of C. osculatum hatch at 0 C (L. Measures, pers. comm.), but

eggs and larvae (L1, L2, L3) of P. decipiens are sensitive to low

temperatures (McClelland, 1982; Burt et al., 1990) and will not

hatch at 0 C (Marcogliese et al., 1996; Measures, 1996). Eggs of P.

phocae are presumably cold tolerant, similar to C. osculatum, as

this parasite has a close phylogenetic relationship to C. osculatum

(Nadler et al., 2000) and also has a Holarctic distribution (Adams,

1988).

Although Svalbard is a high Arctic archipelago, the coastal

waters of West Spitsbergen are influenced by relatively warm,

salty water from the West Spitsbergen Current (Fig. 1). This

current is the northernmost extension of the Norwegian Atlantic

Current and occupies the upper 600 m along the continental slope

from the south, moving northwards along the west coast of the

Svalbard Archipelago (Svendsen et al., 2002). Forlandssundet and

St. Jonsfjorden (Fig. 1) have an open coastal connection and are

highly influenced by Atlantic water. High species diversity and

low numbers of polar cod were found in the diet of ringed seals in

this area (Labansen et al., 2007), and the seals from this area were

found to have the lowest abundance of nematodes. Seals in

Billefjorden (Fig. 1) were found to have the highest abundance of

nematodes, and seals from this fjord had also consumed the

highest numbers of polar cod (Labansen et al., 2007), supporting

the hypothesis that polar cod might be an important host for

FIGURE 2. Abundance of nematodes (top) and acanthocephalans(bottom) in relation to the proportion of large polar cod (Boreogadussaida) in the diet of the ringed seal hosts.

950 THE JOURNAL OF PARASITOLOGY, VOL. 96, NO. 5, OCTOBER 2010

transferring nematodes to ringed seals. Recherchefjorden & Van

Keulenfjorden (Fig. 1) was the southernmost sampling location

and is probably also influenced strongly by Atlantic water. The

ringed seals from this location had the highest abundance of

acanthocephalans, while Kongsfjorden (Fig. 1), which has a

mixture of Atlantic and Arctic water, had the lowest abundance

of this group of parasites. Wijdefjorden on the northern coast of

Spitsbergen (Fig. 1) is the sampling location with the least

influence of Atlantic water in this study; it differed from

Kongsfjorden and Recherchefjorden & Van Keulenfjorden in

terms of acanthocephalan abundances, but was similar to other

regions in terms of nematode abundance.

Adult male ringed seals had significantly higher abundances of

nematodes compared to adult females and juveniles, and adult

males also had significantly higher abundance of acanthocepha-

lans compared to adult females. Because the parasites observed in

this study are transmitted by consumption of infested prey, any

sex- or age-related difference in the diet of the seals would likely

be linked to variation in parasite burdens. In the present study,

nematode abundance increased significantly with the fraction of

older polar cod consumed. Adult males and juveniles in this study

had consumed significantly more large (old) polar cod than had

the adult female seals (Labansen et al., 2007). According to Falk-

Petersen et al. (1986), large polar cod have a deeper distribution

than do the smaller polar cod, and smaller individuals (year class I

and II) dominate in shallow areas. Additionally, polar cod

associated with sea ice are year classes I and II (Lønne and

Gulliksen, 1989). During the period when the seals in this study

were collected, most of the adult females were probably more

restricted in their movements than were adult males, staying deep

inside the fast-ice habitat where they had nursed their pups. The

females had preyed on the youngest year classes of polar cod,

which may have been less infested with parasites. Most adult

males, and all juveniles, are generally less restricted in terms of

movements during the spring period, often being found on the

edges of the land-fast ice (Krafft et al., 2007) and, thus, have

greater opportunity to prey on the older year classes of polar cod

that are found in deeper waters and have more exposure to

helminth parasites.

Larval nematodes and Corynosoma spp. cystacanths tend to

accumulate with age within paratenic hosts (Grabda, 1991;

Sinisalo and Valtonen, 2003), and male ringed seals did have

increased worm burdens with age. But, this trend was not seen

among adult females, which experience much greater fluctuations

annually in condition because of the high costs of lactation, which

might influence their suitability as hosts.

In summary, nematodes and acanthocephalans were found to

be the most numerous helminth parasites in the GIT of ringed

seals from Svalbard. The abundance of these parasites was found

to vary with both sex and age of the seals as well as by geographic

sampling location. The occurrence of nematodes is, at least in

part, likely related to dietary differences among the various

groups of seals because of the different size–age of prey that they

respectively target. Polar cod might be of major importance in the

life cycle of Phocascaris spp. (and perhaps also of C. osculatum) in

the Arctic. However, additional information about helminth

parasites in polar cod and other possible prey groups in the diet of

ringed seals is needed before more definitive conclusions can be

reached regarding the sources of infestation of ringed seals.

Comparative data from other arctic sites would also be very

beneficial to track potential changes taking place in parasite

communities in the Arctic (Rausch et al., 2007), with the

increasing water temperatures and increasing occurrences of

temperate marine mammal species at higher latitudes, as they

extend their distributions northward in a warming climate.

ACKNOWLEDGMENTS

This study was supported by the Norwegian Polar Institute and theNorwegian Research Council. In addition, C.E.J. was supported bystudent grants from the Norwegian Polar Institute’s Arctic Scholarshipand the Roald Amundsen Centre for Arctic Research. We thank Aili LageLabansen, Helen Carlens, and Bjørn Krafft for help in the field and in thelab, and Raul Primicerio (NFH, University of Tromsø) for statisticaladvice.

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