HELMINTH FAUNA OF ICE SEALS IN THE ALASKAN BERING AND CHUKCHI SEAS, 2006–15 Open Access

Ringed (Pusa hispida), bearded (Erignathus barbatus), spotted (Phoca largha), and ribbon (Histriophoca fasciata) seals are sea ice–associated Arctic phocids. In Alaskan (US) waters, ringed, bearded, and spotted seals are found in the Bering, Chukchi, and Beaufort seas (Burns 1970); ribbon seals are found in the Bering and Chukchi seas, and rarely in the Beaufort Sea (Burns 1981a). Movements of these seals are more restricted in winter than in spring, summer, and fall (Burns 1970; Lowry et al. 2000; Crawford et al. 2012). During summer months, ringed and bearded seals are widely distributed throughout their range (Burns 1981b; Burns et al. 1981), spotted seals inhabit coastal environments, often hauling out on land (Lowry et al. 2000), and most ribbon seals remain pelagic in the Bering Sea (Burns 1970). All four seal species are harvested for food by Alaska Native subsistence hunters from coastal villages, although ribbon seals are less common in the harvest (Burns 1981a).

Helminths of phocids have coevolved with their hosts such that most have minimal effects on healthy seals; however, some can be harmful (Raga et al. 2002; Leidenberger et al. 2007). There is evidence that individuals in poor health (e.g., poor body condition or compromised immune systems) tend to have a greater number and diversity of parasites (Harwood and Hall 1990; Geraci and Lounsbury 2002). Common phocid parasitic helminths include many nematode, cestode, trematode, and acanthocephalan species (Yurakhno 1971; Dailey 2001). Many of these parasitic helminths infect seal prey as larvae and are ingested by seals, and so helminth prevalence varies by seal species depending on prey selection. A change in parasite fauna within a host species could indicate a change in diet (Geraci and Lounsbury 2002).

Arctic marine waters are warming as sea ice decreases in extent and seasonal duration, and this is predicted to have negative effects on some Arctic marine mammal species (Laidre et al. 2008). A warming marine environment may favor some parasites (Harvell et al. 1999; Kovacs and Lydersen 2008), increasing the prevalence of existing parasites and allowing new species to become established through range expansion of host species (Burek et al. 2008; Kovacs et al. 2011). Newly introduced parasites could have significant health effects on naïve seal populations (Burek et al. 2008). In our study, conducted during 2006–15, we identified helminths in multiple tissues of ringed, bearded, spotted, and ribbon seals harvested for subsistence in the Bering and Chukchi seas of Alaska and compared our results to past studies.

Samples were collected from 141 ice seals (137 subsistence-harvested and four found dead) in Alaska during 2006–15, including 44 ringed, 74 bearded, 14 spotted, and nine ribbon seals. Most samples were collected during spring and fall from seals harvested for subsistence purposes from the coastal Alaskan communities of Hooper Bay, Gambell, Nome, Little Diomede, Shishmaref, Kotzebue, and Point Hope, in the Bering and Chukchi seas (Fig. 1). Of the four dead seals, two were ringed seals collected near Utqiaġvik during an unusual mortality event in 2011 (National Oceanic and Atmospheric Administration 2018), one was a ringed seal collected near Mekoryuk, and the last was a ribbon seal collected near Adak Island (Fig. 1).

Heart, gall bladder, and stomach were collected whole, and tissue samples (at least 8×8 cm) were collected from the liver. The junction of the trachea and both bronchi was also collected with lung tissue attached. Intestinal contents were placed into 125-mL plastic bottles in the field (2006–08), and a 30-cm length of intestine was collected from both the small and large intestines, and contents were removed in the laboratory (2009–15). All samples were placed in individual plastic bags, frozen, and shipped to the Alaska Department of Fish and Game laboratory in Fairbanks, Alaska, where they were stored at –20 C. Stomachs were thawed, rinsed, and sorted in the Alaska Department of Fish and Game laboratory for diet analysis, and helminths were removed, placed in 100% ethanol (if collected during 2006–08), or refrozen at –20 C (if collected during 2009–15). Frozen tissues collected during 2006–09 from 48 seals were sent to the Alaska SeaLife Center (Seward, Alaska, USA), where helminths were removed and shipped to the parasitology laboratory at the University of Florida, College of Veterinary Medicine (UF; Gainesville, Florida, USA). During 2010–15, the frozen tissues from 93 seals were sent directly to the parasitology laboratory at UF, where helminths were removed, and tissues were examined individually and rinsed into a no. 50 standard sieve until the water ran clear. The remaining material was back flushed into a glass container, from which the helminths were recovered. When possible, fecal flotations and/or sedimentation methods were used to detect helminth eggs in intestinal contents (Zajac and Conboy 2012). Intestinal content was stored at 4 C until processed. Fecal flotations were performed with a minimum 1 g of intestinal content, when available, using a centrifuge and Sheather's sugar (specific gravity 1.26). A simple sedimentation was also performed using a minimum of 1 g of intestinal content, when available, and the protocols of Zajac and Conboy (2012) were modified to include the use of a liquid detergent solution (two drops of detergent in 500 mL of water) and resting periods of 30 min rather than 1 h. Helminths were cleared in lactophenol (nematodes, acanthocephalans) or stained using Harrishematoxylin staining (cestodes, trematodes) and identified to species when possible based on morphologic characteristics (Price 1932; Delyamure 1968; Hoberg et al. 1991; Gosselin and Measures 1997; Dailey 2001). Representative specimens were submitted to the University of Florida Museum of Natural History (Gainesville): Nematoda (UF 22–68), Platyhelminthes (UF 1062–1137), and Rotifera (Acanthocephala; UF 3–34).

Helminths were found in 100% (9/9) of ribbon, 99% (73/74) of bearded, 93% (13/14) of spotted, and 86% (38/44) of ringed seals sampled (Table 1). Helminths included species of nematodes, cestodes, trematodes, and acanthocephalans. Most helminths were found in the stomach and intestines (Table 2). Only bearded seals had helminths in all tissue types analyzed. No helminths were found in the heart, liver, or gall bladder of spotted or ribbon seals (Table 2). No adult helminths were found in the hearts of ringed seals (Table 2); however, unidentified nematode larvae were found in the heart of one ringed seal.

Anisakid worms (Nematoda: Anisakidae) were found in all seal species; bearded seals had the highest prevalence (96%, 71/74), followed by spotted (71%, 10/14), ribbon (67%, 6/9), and then ringed (20%, 9/44) seals (Table 1). Most were found in the stomach and intestines (Table 2); however, Anisakis sp. individuals were found in the lungs of two ribbon seals and one spotted seal, and worms of the Pseudoterranova decipiens complex were found in the lungs of one bearded seal and one ribbon seal. These worms probably migrated from the stomach and intestines postmortem (Goertz et al. 2019). Anisakis sp. were most common in ribbon (44%, 4/9) and spotted seals (21%, 3/14). Nematodes of the Contracaecum osculatum complex were most prevalent in bearded seals (28%, 21/74), but they were also found in two ribbon seals and one ringed seal (Table 1). Other nematodes of the genus Contracaecum that could not be identified to species were found in an additional 16 bearded seals and two ribbon seals. Worms of the P. decipiens complex were also most prevalent in bearded seals (91%, 67/ 74). The heartworm Acanthocheilonema (Dipetalonema) spirocauda was found in the heart of one bearded seal and the lungs of one spotted seal (Tables 1, 2). Lungworms from the Filaroididae family were found in 29% (41/141) of seals (11 ringed, 13 bearded, eight spotted, and one ribbon seal). Most of these were identified in lung tissue, but Parafilaroides (Filaroides) gymnurus was found in one ringed seal liver, and Parafilaroides (Filaroides) sp. was found in one bearded seal heart (Table 2). Prevalence of the lungworm P. (F.) gymnurus was highest in spotted seals at 57% (8/14), followed by ringed seals at 18% (8/44), ribbon seals at 11% (1/9), and bearded seals at 8% (6/74; Table 1). The lungworms Otostrongylus circumlitus and Otostrongylus sp. were found in ringed, spotted, and ribbon seals, with ribbon seals having the highest prevalence at 22% (2/9; Table 1). All five ringed seals and the spotted seal with O. circumlitus were pups. In contrast, the two ribbon seals with O. circumlitus and Otostrongylus sp. were adults.

Cestodes were found in three of four species; bearded seals had the highest prevalence (82%, 61/74), followed by spotted (29%, 4/14) and ringed seals (9%, 4/44). No cestodes were found in ribbon seals (Table 1). The most common family found in bearded seals was Diphyllobothriidae (78%, 58/74), of which two species were identified: Diphyllobothrium cordatum (8%, 6/74) and Diphyllobothrium lanceolatum (19%, 14/74; Table 1). The only other cestode identified to genus in bearded seals was Pyramicocephalus sp., found in two individuals (3%, 2/74). In contrast, Anophryocephalus sp. and Diphyllobothrium sp. were found in ringed and spotted seals (Table 1). Most of the cestodes were found in the stomach and intestines, but tetrabothriid tapeworms (Terabothriidae) were found in the lungs of one ringed seal and one spotted seal, and diphyllobothriid tapeworms (Diphyllobothriidae) were found in the liver of one bearded seal (Table 2).

Again, trematodes were primarily found in bearded seals (64%, 47/74), but they were also in two ringed seals (Table 1). No trematodes were found in spotted or ribbon seals. Almost all the trematodes found in bearded seals were Orthosplanchnus sp., 51% (38/74) of which could be identified as Orthosplanchnus arcticus, and they were more often found in bearded seal gall bladders (62%, 46/74) than livers (12%, 9/74; Table 2). One ringed seal had O. arcticus in the liver, and another had Phocitrema fusiforme in the intestines (Tables 1, 2).

Acanthocephalans were present in all four ice seal species and were most prevalent in spotted seals 64% (9/14), followed by ringed 61% (27/44), ribbon 33% (3/9), and then bearded seals 15% (11/74; Table 1). Most were found in the stomach and intestine; however, they were also found in the gall bladder of one ringed seal and the heart of one bearded seal (Table 2). Corynosoma hadweni (a synonym of Corynosoma wegeneri; Amin 2013), Corynosoma semerme, and Corynosoma strumosum were found most often in ringed and spotted seals (Table 1).

Juvenile helminths were found in ringed, bearded, and ribbon seals. Nematode juveniles, without the presence of adult worms, occurred most often in ringed seals (25%, 11/ 44), followed by ribbon (11%, 1/9) and bearded seals (1%, 1/74). A juvenile trematode was found in the gall bladder of one bearded seal, and juvenile acanthocephalans were found in the stomach of another bearded seal. Helminth eggs were also found, using flotation and sedimentation methods, from intestinal content of ringed, bearded, and spotted seals. Nematode eggs, without the presence of adult worms, were found in one ringed seal (4%, 1/28) and one bearded seal (2%, 1/56). Trematode eggs were found in ringed (14%, 4/28) and bearded seals (4%, 2/ 56), but not in spotted or ribbon seals. Cestode eggs were only found in bearded seals (9%, 5/56). Acanthocephalan eggs were found in two spotted seals (67%, 2/3) and one bearded seal (2%, 1/56).

We found no helminths new to the Bering-Chukchi Seas region during our 2006–15 study period, despite the predicted changes associated with the warming Arctic marine environment (Burek et al. 2008). In addition, we found no evidence of elevated numbers or increased diversity of helminths that would suggest seal health has declined during these environmental changes. Helminths were found in 94% (133/141) of the ice seals examined, all of which were common in phocids. Many are considered nonpathogenic; however, some, such as lungworms and heartworms (both nematodes), have the potential to cause morbidity or mortality to their hosts. Quantitative comparisons with previous studies from this region are problematic because of vagaries in tissues examined, taxonomic identification, and nomenclature; despite these issues, our conclusions hold.

Lungworms are not new in Alaskan waters. Fay et al. (1978, 1979) reported the occurrence of lung lesions in bearded, spotted, and ribbon seals from the Bering Sea caused by an unknown parasitic nematode. Lungworms were also confirmed or presumed in stranded ringed, bearded, and spotted seals from the Bering, Chukchi, and Beaufort seas collected between 2000 and 2017 (Goertz et al. 2019). In our study, four seals (three ringed and one spotted) that had adult lungworms, or larvae suspected to be lungworms, were necropsied; all had lung disease such as pneumonia, fibrosis, and congestion.

The presence of lungworms, however, does not always produce ill health. Gosselin et al. (1998) reported no detrimental effects on body condition associated with the occurrence of Parafilaroides (F.) spp. or O. circumlitus from Northwest Territories and eastern Canada. Otostrongylus circumlitus, however, is implicated in the death of two northern elephant seals (Mirounga angustirostris) by causing verminous pneumonia and severe respiratory distress (Stroud and Dailey 1978), which limits diving and foraging ability (Onderka 1989).

Ringed seal pups in the western Canadian Arctic had a higher occurrence of O. circumlitus than older seals (Onderka 1989), which was also true for our study where 75% (6/8) of the seals with O. circumlitus were pups. Onderka (1989) found pups have microscopic lung fibrosis not seen in adults, suggesting that this parasite may reduce pup survival, possibly during their first winter when their movements are restricted under sea ice and they must use breathing holes.

We found lungworms P. (F.) gymnurus, Otostrongylus sp., and O. circumlitus in ribbon seals in the Bering-Chukchi Seas region, which were previously unreported there, although O. circumlitus has been reported in ribbon seals from the Sea of Okhotsk (Popov 1975; Shults and Frost 1988). We also found P. (F.) gymnurus in bearded seals from the Bering-Chukchi Seas region, which was previously unreported there, although Parafilaroides (Filaroides) krascheninnikovi, a synonym of P. (F.) gymnurus (Gosselin and Measures 1997), has been reported in bearded seals from the Sea of Okhotsk (Delyamure and Popov 1975). Parafilaroides (F.) krascheninnikovi has also been reported in ringed seals from the Gulf of Anadyr in the Russian Bering Sea (Yurakhno and Skryabin 1971; Yurakhno 1972; Yurakhno and Popov 1976) and from spotted seals in the Gulfs of Anadyr and Karaginsky (Delyamure et al. 1984).

We found the pathogenic heartworm A. (D.) spirocauda in a bearded seal at Little Diomede Island and in a spotted seal at Point Hope, but not in ringed or ribbon seals, although it has been reported in ringed (Yurakhno et al. 1968; Yurakhno 1972; Yurakhno and Popov 1976; Eley 1981) and ribbon seals (Fay et al. 1978; Eley 1981; Shults and Frost 1988) from the Bering-Chukchi Seas region. Heartworms are found in the right ventricle and pulmonary artery of the heart and can cause proliferative endarteritis and may completely occlude the pulmonary artery (Eley 1981; Measures et al. 1997). Heartworms are the only helminth we identified that are not transmitted by prey; they are thought to be transmitted by seal lice (Echinophthirius horridus), an ectoparasite (Leidenberger et al. 2007). None of the seals in our study, however, was known to have seal lice.

Several nematode helminths reported in the Bering-Chukchi Seas region in the past were not found in our study. We did not find species from the genus Phocascaris in ringed seals, although species of this genus have been found in this region (Yurakhno et al. 1968; Yurakhno 1972; Yurakhno and Popov 1976; Delyamure et al. 1976). We did not find the Contracaecum osculatum complex in spotted seals, although it was present in spotted seals in the past (Fay et al. 1978, 1979; Shults 1982; Delyamure et al. 1984).

We found cestodes in fewer seal species and at lower prevalence than reported in the past. We found Anophryocephalus sp., reported as a common seal cestode in the Bering Sea (Hoberg et al. 1991), in ringed (2%, 1/44) and spotted seals (29%, 4/14) only. We found Diphyllobothrium sp. in only one spotted seal (the necropsied individual mentioned earlier with lungworms and lung disease). We found no cestodes in ribbon seals, although they have been reported by others (Shults and Frost 1988). We found a lower prevalence (3%, 2/74) of the genus Pyramicocephalus in bearded seals in the Chukchi-Bering Seas region than past reports for Pyramicocephalus phocarum at 44% (4/9; Delyamure et al. 1976), 69% (9/13; Fay et al. 1979), and 100% (8/8; Fay et al. 1978). This cestode is reported as common throughout the Holarctic range of bearded seals (Rausch and Adams 2000). Our method of subsampling the intestines may have contributed to a lower occurrence; however, our sample size of bearded seals (74) was much larger than these previous studies (Delyamure et al. 1976; Fay et al. 1978, 1979), and so it seems unlikely that such a decrease in occurrence was related to our methods. Cestode eggs were only found in the intestinal contents of bearded seals.

We found fewer trematode species in fewer seal species than reported in the past. Trematodes were only found in ringed and bearded seals, although all four ice seal species are known hosts of trematodes (Delyamure and Yurakhno 1974; Delyamure et al. 1984; Adams and Rausch 1989). We found P. fusiforme in ringed seals only, but they have also been reported in ribbon and spotted seals (Shults 1982; Shults and Frost 1988). We did not find four species of Trematoda previously found in the Bering Sea, including Orthosplanchnus fraterculus in ribbon and bearded seals (Fay et al. 1978, 1979; Shults and Frost 1988), Orthosplanchnus pygmaeus in spotted seals (Delyamure et al. 1984), Pricetrema erignathi in bearded seals (Delyamure et al. 1976), and Microphallus orientalis in bearded (Delyamure et al. 1976), spotted (Delyamure et al. 1984), and ribbon seals (Yurakhno 1984).

Trematodes are known to cause thickening of the bile ducts of the liver in bearded seals (Bishop 1979). We found two adult bearded seals with O. arcticus or Orthosplanchnus sp. in their gall bladders, but not their livers; both had yellow blubber. Although the cause of yellow blubber is unknown, helminths blocking bile ducts may be responsible in some cases. One of these bearded seals was a 20-yr-old female that had an enlarged gall bladder and bile-colored ducts in the liver; however this animal appeared otherwise healthy, with thick blubber, had recently produced a pup, and was pregnant again when harvested.

We found Acanthocephala from the genus Corynosoma only. They were found in the intestines of all seal species (Table 2). We did not find Corynosoma hadweni in ribbon seals; however, it has been reported by Delyamure and Yurakhno (1974), Yurakhno (1984), and Shults and Frost (1988). We did not find Acanthocephala of the genus Bolbosoma; however, species of this genus have been found in ringed (Adams 1988), spotted (Fay et al. 1978, 1979; Shults 1982; Delyamure et al. 1984), and ribbon seals (Fay et al. 1978, 1979; Shults and Frost 1988), although the genus identification in spotted seals was contested (Delyamure et al. 1984).

Most helminths found in this study are acquired by eating infected prey (Dailey 2005). As such, species-specific seal diet likely contributes to parasite diversity and prevalence. Fish such as cod (family Gadidae), capelin (Mallotus spp.), and herring (Clupea spp.) are known to be intermediate hosts for the anisakid nematodes P. decipiens complex, Anisakis spp., and Contracaecum spp. (Sakanari and McKerrow 1989). Arctic cod (Boreogadus saida) or capelin, along with crustaceans and mollusks, may be intermediate hosts for O. circumlitus (Bergeron et al. 1997). Bearded seals are benthic generalists that feed on a wide variety of fish and invertebrates (Crawford et al. 2015), which may explain why they are host to a higher diversity of helminths and why most individuals host multiple helminth species. Given the prey diversity of these four seal species, it is not surprising that their helminth life cycles are largely unknown.

As marine waters warm and habitats change for prey, seals may be exposed to different helminths due to changes in the food web (Marcogliese 2001; Rausch et al. 2007; Jenkins et al. 2013). Crawford et al. (2015) reported an increase in the frequency of occurrence of Arctic cod, pricklebacks (family Stichaeidae), and flatfish (family Pleuronectidae) in the diet of bearded seals in Alaska in recent years (2003–12), none of which is new to the region; however, more of these prey species in the diet could increase the prevalence of helminths such as anisakid nematodes, Contracaecum spp., and acanthocephalans in bearded seals if these fish are intermediate hosts. On the other hand, changes in prey assemblages may be responsible for the lower prevalence of the cestode genus Pyramicocephalus observed in bearded seals and for the absence of several trematodes previously found in the Bering Sea. There are many unknowns ahead as the environment changes, and studies like this, which monitor helminths directly, will continue to be important.

This project was made possible by the willingness of hunters to contribute samples from their harvest, the support of their communities, local governments, and tribal councils. We appreciate the support from the North Slope Borough and the Ice Seal Committee. We would also like to thank Mark Nelson, Louise Biderman, and college interns from the Alaska Department of Fish and Game, Cristina Hansen (University of Alaska–Fairbanks), Alex Whiting (Native Village of Kotzebue), and Alaska SeaLife Center interns for their help with sample collection and processing. Sample collection and analysis were funded by the National Oceanic and Atmospheric Administration, National Marine Fisheries Service (projects NA05NMF4391187, NA08NMF4390544, and NA11NMF4390200). Samples were collected and analyzed under National Marine Fisheries Service research permits 358-1787 and 15324 issued to the Alaska Department of Fish and Game.