Causes of mortality and morbidity in wild juvenile and adult grey seals (Halichoerus grypus)

Br. vet. -7. (1987) . 143, 203

CAUSES OF MORTALITY AND MORBIDITY IN WILD JUVENILE AND ADULT GREY SEALS (HALICHOERUS GRTPUS)

J . R . BAKER Department of Veterinary Pathology, University of Liverpool, Veterinary Field Station, Leahurst, Neston, Wirral L64 7TE

SUMMARY Juvenile and adult grey seals caught in fishery operations were subjected to postmortem examination . The 36 animals had 182 abnormalities . Parasites and parasite-related diseases of the gastrointestinal tract and respiratory system were common, as were skin, arterial, lung and liver diseases. Other systems were less commonly diseased . Nine animals, nearly all adults, found dead were investigated . Diseases of the digestive system killed three, reproductive system two, respiratory system two, a fall one, and sepsis one . Non-lethal diseases in these animals are also recorded as were those found in an animal dying of an anaesthetic accident . Diseases found in these animals are compared with previous records for this and other species of pinnipeds .

INTRODUCTION A crayfish fishery was established using tangle nets for a single season in 1984 in the southern Outer Hebrides (Scotland) and as a by-catch a number of grey seals were found enmeshed and drowned . The opportunity was taken to perform post-mortem examinations to investigate the causes of morbidity in this sample of `healthy' animals. References to surveys of seal mortality relate almost exclusively to animals found dead or dying on beaches (Table I) and while useful, they are not strictly comparable with the findings reported here . An exception is the work by Bergman & Olsson (1984) who incorporated in their paper details of grey and ringed seals caught as a by-catch of fishery operations in the Baltic . While there are some similarities between the pathology in the two populations, the differences are more striking . In the course of work on pup mortality from 1980 onwards, occasional dead juvenile and adult grey seals have been found . As the number of publications concerning the natural causes of death in this species is limited, it was thought that the lesions found in these animals were worthy of record . The findings in these two groups of animals will be compared with other reports of causes of morbidity and mortality in both grey and other species of seal .

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Table I References giving surveys of mortality and morbidity in various species of wild seals, excluding young pups Species

Age

References

Halichoerus grypus

(Grey Seal)

Adults Adults and juveniles

Phoca vituluna

Post-weaning pups Adult females Not stated

Appleby (1964) Farmer and Roberts (1970) Anderson, Bonner, Baker and Richards (1974) Baker (1980) van Haaften (1982) Bergman and Olsson (1984) Schroeder, Quadri, McIntyre and Walker (1973) Sweeney and Gilmartin (1974) Stroud and Roffe (1979) Britt and Howard (1983) van der Kamp (1985 personal communication) Stroud and Roffe (1979)

(Common Seal)

Eumetopias jubatus

Over three months Not stated

(Steller's sealion) Mironga augustirostris

Not stated

Adult males

Schroeder, Quadri, McIntyre and Walker (1973) Stroud and Roffe (1979) Stirling (1971) King (1973) Baker and McCann (in press)

Adult females

Bergman and Olsson (1984)

(Northern elephant seal) Leptomychotes weddelli

Adults

(Weddell Seal) Arctocephalus gazella

(Antarctic fur seal) Phoca Hispida

(Ringed Seal)

MATERIALS AND METHODS The bulk of this report is based on the post-mortem examination of thirty-four juvenile and two adult Grey seals caught and drowned in tangle nets laid for crayfish around the coasts of Barra and adjacent islands in the southern Outer Hebrides during the summer of 1984 . The bodies were stored frozen for up to two months prior to autopsy by routine methods together with limited histological, parasitological and bacteriological examinations . Ten dead adult Grey seals found elsewhere are also referred to : seven from North Rona in the Hebrides, two found washed up at West Kirby on the estuary of the Welsh Dee, and one on North Ronaldsay in the Orkneys . These animals were subjected to the same examinations as the main group . Some abnormal Grey seal vertebrae found on the island of Shillay in the Sound of Harris are also described .



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RESULTS

Morbidity The age and sex distribution of the Grey seals from Barra is presented in Table II . The abnormalities found during the post-mortem examinations, with the exception of the pathology of drowning, are given in Table III . Table II Grey Seals, Barra 1984-age frequency distributions

Age Class (years)

Frequency Males

0 1

Females

10

8

2 3 4 13 25

2 6 0 1 0 0

1 2 4 0 1 1

Total

19

17

* This includes 64 . 5kg .

one particularly heavy animal of 165

Weight Average Kg. Male Females

36 . 1 57 . 0 70 . 8 89 . 5 -

37 . 0 51 . 0 53 . 8 89 . 8* 126 . 5 145 . 0

Total 18

3 8 4 1 1 1 36

. 5kg, the average of the other three was

The most common disease was found to be infestation with gastric nematodes, due to and Porrocaecum decipiens and also with smaller numbers of Anisakis simplis . Often large numbers of nematodes were found in the oesophagus, mouth and nares, probably due to terminal vomiting, or post-mortem migration, and an unknown number of worms may have been lost in this way . The remaining nematodes were counted and the results grouped . Thirteen seals had less than 1000 nematodes, 20 had between 1,000 and 5,000, two had between 5,000 and 10,000 and the remaining one had over 10,000 . There was no correlation of numbers of nematodes with age except for those seals only a few months old which had below average numbers which ranged from between 169 to 1913 . The seals caught early in the year had a greater proportion of immature worms . These two factors are probably correlated and imply recent infection of young seals. Eighty-one per cent were infested with Corynesoma sp. which occurred throughout the small intestine but was commonest in the lower ileum . Infestations were considered to be light in 18 animals, moderate in 9 and heavy in only one ; 7 animals had none . Again there was no correlation between the level of infestation and the age of the animal . One five months old animal had a Corynesoma attached to the omentum in the peritoneal cavity . Pulmonary nematodes, a mixture of Otostrongylus sp. and Parafilaroids sp ., were detected on histological examination of sections approximately 1 . 5 cm square prepared from the dorsal posterior edge of the apical lobes of the lungs, the site with the heaviest infestation Contracaecum osculatum



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Table III Post-mortem findings in 36 Grey seals

Condition Gastric nematodes* Intestinal Corynesoma Pulmonary nematodes* Gastric ulceration Nasal mites Arterial wall calcification Non verminous pneumonia Liver abscess/hepatitis Abraded flippers Dental disease Persistent pseudourachus Liquifaction of blubber Alopecia Lymphadenitis Viral skin disease Skin ulcers (unknown cause) Trauma Dermatitis Meningeal abscess Thrombosed pulmonary artery Corynesoma in peritoneal cavity Umbilical ulceration Liver capsule thickening Pulmonary abscess Skin papilloma Pulmonary neoplasia Pulmonary calcification Gastric foreign body (Polythene) Bronchiolar cartilage ossification

Number Affected

% affected`

34 94"/) 29 81% 57% 20 17 47"/0 13 36% 10 28% 8 22% 7 19% 5 14% 4 11% 4 11 0/() 4 11% 4 11 0/0 3 8% 3 8% 2 6"/0 2 6% 2 6'/o 3% 1 1 3% 1 3% 1 3"/% 3% 1 1 3"/0 1 3% 1 3% 1 3% 1 3% 1 3"/%

* Presence or absence not recorded in one animal . +To nearest 1% . There were 5 . 06 abnormalities per animal .

in previous studies (Baker, unpublished) . Twenty animals were affected, with most of the parasites being present in the lung parenchyma but with smaller numbers in the finer airways . In most animals there was no host reaction to either dead or live nematodes, although in four seals dead parasites were enclosed in a mesh of fibrous tissue lightly infiltrated with lymphocytes with, in one case, eosinophils, and in another, histocytes . One seal had produced a reaction to only some dead parasites. Pulmonary nematodes were present in large numbers in nearly all the animals less than one year old ; older animals had fewer infestations and usually only single nematodes were found in sections from the lungs of these animals (Table IV) . Gastric ulcers were found ranging in numbers from one to more than twenty . Grossly the ulcers appeared deep and crateriform ; they were usually surrounded by an elevated



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Table IV Grey Seals - Barra 1984 Age frequency distribution of animals with and without

pulmonary nematodes Age class (years) 0 1 2 3 4 13 25

Affected animals 16 3 1

Unaffected animals 2 2 5 3 1 1

Not recorded

1

1

Animals less than 1 year old 88% infected . Animals more than 1 year old 29% infected .

or swollen rim of mucosa . The ulcerated areas were grey in colour without any gross evidence of inflammation . Ulcers occurred in all parts of the mucosa . In one animal three apparently healing ulcers were present and in another pus could be expressed from the ulcerated areas. Histologically, the ulcers were usually more extensive than was apparent grossly as the inflammatory reaction underran the surrounding mucosa and was responsible for the elevated rim surrounding most ulcers . Nematodes' heads were found deep in all the ulcers . They were usually surrounded by lymphocytes and by variable numbers of foreign body giant cells . Further away, there was marked fibrosis and diffuse infiltration with lymphocytes and histocytes, this extended into the inner muscle layer of the stomach . Very few eosinophils were present . The number of polymorphs was very variable, presumably dependant on the extent of secondary bacterial infection . Occasional nematodes' heads were present either at the base of the mucosa or below the muscularis mucosae, surrounded by inflammatory cells but not associated with ulceration . Gastric ulcers were slightly commoner in animals over one year (50%) compared with those under one year (41%) . Older individuals had more ulcers . Halarachne halichoeri was found in the nasal chamber of thirteen animals . No associated gross pathology was noted . An incidental finding when examining lung sections for nematodes was an arterial wall calcification in ten animals . Lesions were present in both pulmonary and bronchiolar arteries . The nodules of calcified material appeared to originate in the media and expand to lie below, or occasionally perforate through, the intima . The masses were irregularly spherical, measuring between 20 and 250 µm . They cause considerable disruption of the muscle and elastic layers, and frequently caused a narrowing of the vessel . They were not associated with either inflammation or thrombosis . There was no correlation between arterial calcification and age . Eight of the Grey seals showed evidence of non-verminous pneumonia . All but one case consisted of single pneumonic lobules infiltrated with lymphocytes and polymorphs

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in about equal numbers. Three cases also had considerable numbers of alveolar macrophages in the exudate. One case was detected macroscopically in the apical lobe of the right lung; histologically it extended across lobular boundaries, with considerable necrosis and a massive polymorph response. Pasteurella septica was isolated. Six of the eight cases were in animals less than one year old. One animal had a circumscribed pulmonary abscess. Liver abscesses and focal hepatitis were found in seven animals; the lesions were small, usually less than 2 mm in diameter and presented as white or pale yellow circumscribed foci below the liver capsule, or in the hepatic parenchyma. Five animals had abraded fore flippers with hair loss and minor skin lesions on the plantar surface; this was most severe over the interphalangeal joints. Four animals had dental disease: they were all over 24 years in age and included the two adults. There were two cases of excessive wear. In one animal the anterior aspect of the upper cheek teeth was very worn resulting in the apex of the teeth being sharply pointed, in the other all the incisors and the upper canines were considerably reduced in height. The third animal had six incisors in the lower jaw, four in the normal position and two posterior to the lateral incisors. In the remaining animal the left canine and the first two cheek teeth were missing from the mandible and the third cheek tooth was displaced laterally. Infection in the alveolae had spread to the mandible which was considerably expanded and had areas of lysis due to severe oesteomyelitis (Fig. 1).

Fig. 1. Grey seal mandible with severeosteomyelitis and tooth loss resulting from periodontal disease(X0.55).

Four animals had a persistent pseudourachus indicated by a slender but strong band of fibrous tissue running from the apex of the bladder to the umbilicus. No pathology was associated with this remnant of foetal tissue. Liquified blubber was found in four animals, all between two and four years of age and all in one batch of seals received on the 31st August, 1984. The condition only affected parts of the blubber and was found on the left thoracic wall (the largest lesion, 30X20 cm), the inner aspect of the right forearm, the ventral aspect of the neck and over the left hip (the smallest lesion was 6 cm in diameter). On cutting these areas, a clear oil ran from the tissues leaving behind an open fibrous mesh representing the supporting tissue. The affected areas were rimmed by a zone of hyperaemia. Histology confirmed



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that the fibrous stroma was present and scanty remnants of ruptured adipose cells were found . No evidence of inflammation, other than engorged blood vessels, was found . Four animals had areas of alopecia . These were circular, up to 1 cm in diameter, without hair but otherwise normal ; two animals had single lesions, one had two, and the fourth had eleven . They were found on both dorsal and ventral aspects of the body and on the dorsal surface of the flippers . Histologically, the epidermis was normal but all the adnexal elements were absent except for occasional sebaceous glands . The cause of these lesions was not established but they may follow the skin lesions described below . Three animals had a skin disease which may have been viral in origin . Grossly, these presented as slightly depressed rough, bald areas, one to two cm across, scattered over the seal's skin - affected animals having between two and five lesions . Histologically, these were areas of hyperplastic, very folded epidermis with large accumulations of surface squames . In the epithelial mid-zone large vacuoles were present in the cytoplasm, often containing hazy basophilic bodies . The formation of the vacuole caused margination of the nuclear remnant . Similar vacuoles were sometimes found in normal areas of epidermis but they were much smaller, both in size and number, without inclusions and were not causing displacement of the degenerating nucleus . Within the lesions ballooning degeneration was seen in parts of the germinal layers, and small numbers of nuclei in these areas had acidophilic inclusions . These lesions were associated with loss of most adnexal elements in the dermis : those small nests of sebaceous cells persisting, occasionally became cystic . Keratin pearls and epidermoid cysts were associated with the deepest foldings in some diseased areas . In one instance a heavy mixed bacterial flora was present on the surface of the lesion . One seal had a flat papilloma-like lesion on the plantar surface of a hind flipper which was histologically similar to the above lesions except that it protruded above the surrounding skin, was thicker, and lacked the apparent intranuclear inclusions . Enlarged lymph nodes were found in three animals, being the submaxillary, mesenteric and inguinal. No evidence of inflammation was found in the areas drained by these nodes . Two animals showed evidence of trauma . One had a large bruise over the lateral chest wall which had occurred two to four days before death . The other animal had a 29 cm long scar on the left flank . The same two animals also had areas of dermatitis : the former on the lateral aspects of both wrists, and the latter immediately posterior to the scar . Histologically, the first animal showed accumulations of polymorphs around the sebaceous glands, some of which were showing early cystic changes presumably associated with duct blockage. The same acute inflammatory reaction was also associated with some hair follicles and dermal blood vessels . Small areas of superficial epidermal necrosis were also seen . The second animal had loss of hair follicles although other adnexal structures were still present . An intense, somewhat focal, inflammatory reaction consisting of polymorphs and lymphocytes was present in the deeper parts of the dermis . In both cases gram positive coccobacillary organisms were present . Two animals had skin ulcers on the fore flippers, one on the leading edge and the other on the dorsal surface . They were between 5 and 8 mm across and had a `punched out' appearance with sharp edges . The surrounding tissue was hyperaemic . A number of conditions occurred only once . A meningeal abscess was found on the ventral aspect of the spinal cord at the atlanto-occipital articulation . A small core of pus,



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4 mm in diameter and bacteriologically sterile, was surrounded by marked fibrosis ; the lesion was not large enough to cause spinal cord compression . A thrombosed pulmonary artery was found incidentally in a lung sectioned for nematode investigation and was not associated with lesions in the surrounding tissue . The single case of umbilical ulceration occurred in an animal less than one year old . The ulcer was deep, exposing the underlying tissue but it was only 4 mm in diameter . One animal had plaques of fibrous thickening of the diaphragmatic aspect of the liver capsule, there was no underlying hepatic pathlogy and the cause was not established . One animal had a tumour 15 mm in diameter, a white mass in the anterior lobe of the right lung, this was associated with an enlargement of the associated lymph node, which was 30 mm across, white and without apparent structure . Due to freezing, it was not possible to identify the tumour with certainty, but it was probably a bronchogenic carcinoma . The affected animal was ten months old . A small 50 µµm diameter laminated calcified mass was found incidentally in the lungs, as was a case of bronchiolar cartilage ossification found incidentally . All the cartilage was involved, the ossification appearing to start in the middle of the segments whence spreading peripherally . A piece of clear polythene sheet was found in the stomach of one animal . Mortality The ages, sexes and sources of the ten adults referred to in this section are given in Table V and a summary of findings in Table VI . Three animals were found dead on North Rona during October, 1980, all in good bodily condition . A cow died of internal haemorrhage following rupture of the broad ligament of the uterus on the left side with severance of the enlarged blood vessels ; the animal having been pregnant in the left horn of the uterus . Unidentified gastric nematodes were present in moderate numbers ; large numbers of Halarachne halichoeri were present in the nasal chambers . A bull was found at the base of a 15 foot cliff presumably having fallen over it during a territorial dispute . Both pleural cavities were full of blood and the lungs were collapsed . The blood had

Table V Sexes, ages and sources of adults examined Age Sex

(years)

Source

9 d d d d 4 d 9 9 9

37

North Rona North Rona North Rona North Ronaldsay West Kirby West Kirby North Rona North Rona North Rona North Rona

13 13

15 .8 18 . 5 1

16

28 23 16



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Table VI Lesions found in 10 grey seals

Gastric nematodes Nasal mites

10 7

Corynesoma

6

Dental disease Calcified pulmonary nodules Septic wounds Pulmonary nematodes Arterial calcification Pulmonary collapse Gastric ulceration Post-parturient haemorrhage, ruptured broad ligament Ruptured heart Skin ulcers Tongue ulcers Oesophageal ulcers Enteritis Deformed tracheal and bronchial cartilages Mastitis Pulmonary emphysema Pneumonia Focal thickening of hepatic capsule Endometritis Clostridial hepatopathy? Asphyxia due to airway mucus Ossification of bronchial cartilages

4 3* 2 2* 2* 2* 2 1 1 1 1 1 1 1 1 I 1 1 1 1 1 1

* The lungs of only five animals were examined histologically .

come from two tears in the left auricle, both 2 cm long and nearly parallel . The pericardium was ruptured and the left lung was bruised . There were small numbers of gastric nematodes, occasional Corynesoma sp ., in the small intestine, and large numbers of

Halarachne halichoeri . Another bull died as the result of an anaesthetic accident, discussed elsewhere (Barker & Gatesman, 1985) . The animal had three septic wounds, two 2 cm long close to the left eye and one 12 cm long dorsally between the shoulder blades . Two small shallow ulcers were present on the ventral surface close to the xyphoid cartilage . Approximately 50 percent of the dorsal surface of the tongue was ulcerated and the submucosa was very inflamed . Small numbers of gastric nematodes were present together with a light burden of Corynesoma sp. i n the small intestine . All four lower incisors had been lost some time before death, the upper central incisors were absent and the other teeth were very worn . A further four animals were recovered on North Rona in 1985 . Three were found dead and one seriously ill bull died under anaesthetic . The latter animal had light burdens of nasal mites and anaplocephalids and a moderate number of gastric nematodes . There were minor anomalies of the cartilages of the airways, some of the tracheal rings being



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bifid and some of those in the primary bronchi fused so that these airways were supported by sheets of cartilage rather than rings . The lungs showed areas of collapse and also emphysema . Large numbers of pulmonary nematodes were also seen, live ones causing no host reaction but dead ones associated with large granulomas . There were areas of acute bacterial pneumonia and small numbers of calcified nodules in the lung parenchyma . There was focal thickening of the hepatic capsule . One cow had small numbers of nasal mites and gastric nematodes and moderate numbers of Corynesoma . No lower incisors were present, the remaining teeth were very worn . An endometritis was present and death appeared to be due to a clostridial hepatopathy although putrifactive changes made a definite diagnosis difficult . Calcified nodules were present both in the lung parenchyma and in the walls of branches of the pulmonary arteries . A second recently parturient cow had light burdens of Corynesoma and gastric nematodes, eleven gastric ulcers of the type usually associated with gastric round worms, and large numbers of nasal mites . Death was due to asphyxiation due to the large amounts of mucus in the airways . Lung histology showed some ossification of the bronchial cartilages and a single collapsed lobule infiltrated with lymphocytes . Another cow which had recently given birth had no nasal mites and light burdens of gastric nematodes and Corynesoma ; three deep gastric ulcers were found . Death was due to acute bacterial mastitis . Lung histology revealed calcified nodules in the lung parenchyma and pulmonary arterial walls . A further cow died as a result of falling over a cliff edge and becoming jammed in a rock chimney ; the body was not recoverable . A fifteen year old male was found washed ashore on the island of North Ronaldsay in October 1983 . Large amounts of blubber were present . Death was due to a large area of sepsis and cellulitis extending from the left lower jaw down the neck and involving all the tissues dorsal to the oesophagus and terminating at the thoracic inlet . Streptococcus faecalis and a Corynebacterium resembling C. bovis were isolated from the lesion ; a gram negative rod was also present which was not recovered culturally . The lower central incisors had been lost and the laterals, which were very worn, were on the point of being shed due to periodontal disease . A large number of nematodes were present in the stomach and a moderate burden of Corynesoma sp. in the small intestine . Two Grey seals were found washed up at the same spot on the beach at West Kirby on the estuary of the Welsh Dee, a male in August, 1981, and a female in August, 1984 . The male was 20 months old and in poor condition, weighing 51 . 7 kg . Death was due to haemorrhagic enteritis but the cause of this was not discovered due to decomposition . Very small numbers of gastric nematodes were present and occasional Corynesoma sp . were found in the intestine . The female was aged 18 . 5 years and was in poor bodily condition, weighing 66 . 2 kg . There was extensive oesophageal ulceration, linear lesions up to 30 cm long being present predominantly in the proximal half of the organ, which was hyperaemic and had multiple small submucosal haemorrhages . Small numbers of gastric nematodes were found ; large numbers of Corynesoma sp . were present in the small intestine. Nematodes were also present in the pulmonary tissue and small calcified nodules were present in branches of the pulmonary artery, sometimes displacing the intima so that it protruded into the lumen of the vessel . In the lower jaw the left lateral and right central incisors were missing . Two lumbar vertebrae, numbers three and four, of an adult Grey seal were found on the island of Shillay . These were fused due to the formation of new bone between their



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dorsal articular processes, this being more marked on the right than the left . The fusion had occurred so that there was lateral curvature of the spine posteriorly to the left . There was also new bone on the ventral aspect of both bodies, that on L3 measuring 10 mmX15 mmX8 mm, that on L4 eroded after death . The posterior dorsal articular facets of L4 were abnormal, having a periarticular rim of new bone most marked ventrally and irregular pitting of the dorsal part of the facets . These changes probably resulted from a spinal injury . DISCUSSION Opportunities for surveys of the type reported here into causes of morbidity in freeliving wild pinnipeds are few and far between and no similar studies of animals caught in the wild have been published, with the exception of some animals in the survey by Bergman & Olsson (1984) . Two points concerning the age distribution of the seals from Barra are of interest . Firstly only two adults were caught, perhaps meaning that small numbers of adults are present in inshore waters in the summer, or that they are usually sufficiently strong to break out of the tangle nets . Henderson (1984) suggested that adult Hawaiian monk seals are able to escape from nets which entangled pups . Bergman & Olsson (1984) hypothesised that only sick animals are caught and drowned in fishing gear but this seems rather unlikely . Amongst the juveniles the one year age group is under-represented, perhaps due to a different distribution of this age group, or to low survival to this age following the 1982 breeding season ; however, there is no independent data to support this assumption . However, as the number of animals was small, the under-representation of this age group may be a chance effect . No common seals (Phoca vitulina) were present in the catch although these seals were known to be in the area . Surveys of the causes of morbidity and mortality in juvenile and adult Grey seals in the UK have been published by Appleby (1964) who reported very briefly on five animals (four of which were shot normal animals) ; Farmer & Roberts (1970) gave details of the pathology of two animals ; Anderson et al. (1974) provided detailed postmortem findings in four animals (three of which were shot when ill) ; and Baker (1980) gave details of five animals found dead . Van Haaften (1982) referred briefly to thirty Grey seals found stranded and dead on the coasts of the Netherlands, half of which were post-weaning pups . Bergman & Olsson (1984) reported both on grey seals found dead and those caught as a result of fishing operations . The other species in which surveys of the causes of mortality of juvenile and adult animals dying in the wild are given in Table I . The results are not strictly comparable with those given in the survey reported here as they are mainly based on animals washed ashore dead or dying rather than on an apparently random sample of `healthy' animals . The commonest abnormality in the present survey was the presence of gastric nematodes . Darley & Brownell (1972) recorded Anisakis similis, Contracaecum osculatum and Porrocaecum decipiens in Grey seal stomachs, while King (1983) confirms that these three genera occur at this site in Grey seals as well as in other pinnipeds . These findings concur with the present results . All five animals post-mortemed by Appleby (1964) in



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the Farnes and Orkney were infested with Anisakis and Contracaecum and four of the five from the Welsh Dee and Orkney examined by Baker (1980) had gastric nematodes . Young & Lowe (1969) examined twenty juvenile and adult Grey seals and all but one had gastric nematodes ; they found marked differences in the ratio of species present when comparing seals from the east coast of Scotland with those from the Orkneys, but the animals were of different ages . The exceptions to these findings were recorded by Anderson et al. (1974) who found no nematodes in four animals from the Welsh Dee and by Bergman & Olsson (1984) who found Anisakis in only one of fifty-five Grey seals from the Baltic . With the exception of these papers, the general consensus is that most Grey seals have gastric nematodes which concurs with the findings in other species . Eleven of thirteen Northern elephant seals were infested (Schroeder et aL, 1973) and in the same species parasites occurred in five of eight animals (Stroud & Roffe, 1979) . In California sealions, 51% were infested (Sweeney & Gilmartin, 1974) . According to Stroud & Roffe (1979) `almost every animal' in a batch of twenty three Common seals, eight Northern elephant seals, ten California sealions and twelve Steller sealions had gastric nematodes . However low levels have also been recorded ; Britt & Howard (1983) found only 5% of California sealions infested and in the survey by Schroeder et al. (1973) 6% had gastric nematodes and the same authors found a level of only 10% in Common seals . This variation may be due to the different localities from which the animals came or may be an age effect . Reijnders et al. (1981) indicated that the gastric nematodes Porracaecum decipiens and Contracaecum osculatum were rarely found in `young' Common seals and were more common in `older' ones . No evidence of such an age effect was seen in the present survey . Forty seven per cent of the seals in this survey had gastric ulcers with the anterior ends of nematodes deeply embedded . There was also a mixed inflammatory response suggesting a foreign body reaction and response to secondary bacterial invaders . No such lesions were mentioned in Grey seals either by Appleby (1964) or by Anderson et al. (1974) . Young & Lowe (1969) reported raised inflammatory areas in the fundus of two of eight mature Grey seals from Orkney and in nine of twelve from eastern Scotland . Although the latter animals had fewer nematodes, the proportion of the different genera differed between two localities . They considered Anisakis and Contracaecum to be the cause . Gastric ulcers have frequently been reported in the much studied California sealion ; Schroeder & Wedgeforth (1935) stated that most freshly caught animals had gastric ulcers, as did six animals shot in the wild - the ulcers being associated with Anisakis and Contracaecum. Ulcers have been associated with the same species by Dougherty & Herman (1947), Young & Lowe (1969), and Migaki, Dyke & Hubbard (1971) . In a survey of mainly juvenile animals by Sweeney & Gilmartin (1974) ten of fifty-one had gastric ulcers and in two cases these had perforated, leading to death from peritonitis, the cause being Contraceacum osculatum . Ridgeway, Geraci & Medway (1975) recorded `several' adults dying from peritonitis following perforation of Contracaecum osculatum induced gastric ulcers . Gilmartin et aL (1976) recorded that `most' adults have a minor degree of gastric ulceration, again due to Contracaecum osculatum . However no cases of gastric ulceration were recorded in fifty-six California sealions by Schroeder et al. (1973) . Parasite induced gastric ulceration occurs in many other pinnipeds, records include Walruses (Odobenus rosmarus) (Murie, 1968) ; Common seals (Schroeder et al., 1973 ; Stroud & Roffe, 1979) ; Northern elephant seals (Schroeder



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& Wedgeforth, 1935 ; Schroeder et al., 1973 ; Stroud & Dailey, 1978 ; Stroud & Roffe, 1979 ; King, 1983) ; Galapagos fur seals (Zalophus californianus wollebaeki), (Schroeder & Wedgeforth, 1935) ; Northern fur seals (Callorhinus ursinus) (Keyes, 1965) ; Steller sealions (Stroud & Roffe, 1979, one of these animals bleeding to death from a gastric ulcer) ; Harp seals (Phoca groenlandica) (Wilson & Stockdale, 1970) ; and a Bearded seal (Erignathus barbatus) (Bishop, 1979) . While the general consensus is that parasites cause the ulcers, not all agree . Schroeder & Wedgeforth (1935) state that in California sealions ingestion of obsidian (volcanic glass) causes ulcers which are invaded by nematodes, and King (1983) refers to the ingestion of sharp-edged lava as a cause in Northern elephant seals . This explanation, however, could not be the case in Grey seals reported here for, while volcanic debris is common in the areas they inhabited, it is in the form of basalts which lack sharp edges . In the present survey 81% of the animals had Acanthocephalids of the genus Corynesoma in the small intestines ; the species was not established . Five species have been recorded in the Grey seal, these being C. strumosum, C. semerue, C. hadweni, C. falcatum and C. magdeleni (Darley & Brownell, 1972) . Appleby (1964) recorded five of five British Grey seals as being infected, while only one of five from the Welsh Dee was infested (Anderson et al. 1974) . Baker (1980) reported that four of six UK animals had this parasite ; in European Common seals they are `rarely found' (Reijnders, et al., 1981) . Helle & Valtonen (1981) found evidence of seasonal fluctuations in the numbers of C . semerue but not C. strumosum in Ringed seals (Phoca hispida) in the Baltic . As in the Northern fur seal (Keyes, 1965) the greatest numbers are found in the terminal ileum of the Grey seal . Usually these parasites appear not to cause gross pathological changes, as in the current survey . However, Baker (1980) found ulceration associated with a very heavy infestation . Bergman & Olsson (1984) found associated ulceration in 12 of 19 grey seals which may have been immunologically compromised . Laws (1953) reported a Southern elephant seal (Mironga leonina), with its intestine almost blocked by a tumour induced by one of these parasites . The specimen in the peritoneal cavity of one of the Grey seals reported here appears to be the first case of ectopia in this genus . Fifty-seven per cent of the animals in the present survey had pulmonary nematodes in the predeliction site, the posterior dorsal edge of the apical lobes . Burdens away from this site may have been missed in some animals . The infections were mixed ; both Ostostrongylus sp. and Parafilaroides sp . being present . Usually no inflammation was associated with the nematodes although occasional local reactions were produced in response to dead degenerate ones . Both Anderson et al. (1974) and Baker (1980) recorded three of five grey seals having pulmonary nematodes . King (1983) referred to Ostostrongylus s p . i n the lungs of Grey seals and suggested that this may be associated with severe pneumonia whilst van den Broek & Wensvoort (1959) concluded that Parafilaroides gymnurus caused bronchitis and catarrhal pneumonia in Common seals in which this parasite is an important cause of death . Also in the Common seal, Sweeney (1974) referred to respiratory distress associated with Osculatum circumlitus obstruction of the bronchi while Geraci (1978) and King (1983) both associated pulmonary nematodes with significant pneumonia . Menschel, Kraft & Schiefer (1966) described the histopathological changes associated with 0. circumlitus . Reijnders et al. (1981) confirmed the presence of these parasites but do not mention disease associated with them . In the California sealion P. decorus is common and frequently associated with disease in which



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a hypersensitivity reaction may play a part (Fleischman & Squire, 1970) . Howard, Britt & Matsumoto (1983) described two forms of pneumonia in this species, a suppurative form with secondary bacterial invaders and a granulomatous form in which these do not occur . Sweeney (1974) also recorded two forms, a mucoid type with nematodes only, and a purulent type when secondary bacteria invaded the lesion, as did Morales & Helmboldt (1971) . They also stated that it is a disease of young animals and the findings in Grey seals would support this . Sweeney & Gilmartin (1974) in a population of California sealions of similar age structure to the cases recorded here found 67% to be infected, while Schroeder et al. (1973) found 58% of predominantly young animals to be infected, similar figures to those recorded in the current survey and in contrast to the figures of four of thirty seven California sealions of mixed ages reported by Britt & Howard (1983) . Severe disease associated with pulmonary nematodes has been seen in Steller sealions (Stroud & Roffe, 1979 ; King, 1983), and Northern elephant seals (Stroud & Dailey, 1978) . The difference between these reports and the animals that are the subject of the present paper is that the former are based on animals dead or dying, while the latter was presumed to be a random sample of the population . Even allowing for this there was remarkably little disease associated with lungworms in the present survey . Nasal mites, Halarachne halichoeri, were found in 36% of the animals and were somewhat more common in animals more than one year old ; with the exception of two cases, the numbers of mites was small . No pathological changes were seen associated with the mites which agrees with the findings of Bonner (1972), Anderson et al. (1974) and of Baker (1980). However van Bree (1974) recorded a captive Grey seal that died of nasal obstruction due to these mites . Unlike Grey seals, all Southern elephant seals, except for very young animals, are infested with a Halarachne sp . (Laws, 1953) . Futhermore, unlike the Grey seals reported here, nasal mites were associated with the formation of bony nodules in the nose of Leopard seals (Hydrurga leptonyx) (King, 1983), and catarrhal rhinitis with ulceration and inflammation in Northern fur seals (Kim, Haas & Keyes, 1980) . Arterial wall calcification was found in 28% of the animals, all ages being affected ; this was an incidental unexpected finding of lung histopathology and might have been found in a larger number of seals if other sites had been examined . The lesions frequently protruded into the lumen of the vessels but were not associated with thrombus formation . The only previous report of arterial calcification in a Grey seal occurred in the left iliac artery of a young captive animal and was associated with thrombosis ; migrating larvae were considered a possible cause (Fiennes, 1966) . Bergman & Olsson (1984) found arteriosclerosis in 7 of 19 grey seals' aortas together with lipid streaks in an unspecified number . Prathap et al. (1966) studied aortas and coronary arteries from wild Weddell and Southern elephant seals and found fatty streaking in 96% and 22% respectively but there was no calcification . Arteriosclerosis has been described in a single Bearded seal by Bishop (1979) . In California sealions, Kelly & Jensen (1960) found aortitis with cholesterol deposits in three of seventy adults, and Stout (1969) found fat-free, non-calcified aortic lesions consisting mainly of smooth muscle fibres in six of seven California sealions and three of four Common seals . Thus the calcified lesions seen in the Grey seals appear to be unique . There was no correlation between the lesions and the presence of pulmonary nematodes .



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Non-verminous lobular pneumonia occured in 22% of the animals, a condition previously recorded as either a cause or a contributory factor in death (Anderson et al., 1974 ; Baker, 1980) . In common seals over three months, pneumonia is the second most common cause of death (J . S . van der Kamp, personal communication, 1985) . It has also been a frequent cause of death or stranding in California sealions (Schroeder et al., 1973 ; Sweeney & Gilmartin, 1974 ; Gilmartin et al., 1976 ; Britt & Howard, 1983 ; Howard et al., 1983) and also in Northern elephant seals (Schroeder et al., 1973) . However, only rarely have the causal agents been established, Sweeney & Gilmartin (1974) list eleven different bacteria as causing pneumonia, implying that these are opportunist infections rather than specific pathogens . Liver abscesses and hepatitis occurred in 19% of the animals ; the lesions were all small and would have had no clinical effect . Non-parasitic hepatic disease has rarely been recorded in any species of juvenile or adult pinniped . Baker & Doidge (1984) found small hepatic abscesses in an Antarctic fur seal (Arctocephalus gazella), Sweeney & Gilmartin (1974) found `hepatic disease' in 8% of juvenile California sealions and Sweeney (1974) considered that non-specific liver abscesses occurred infrequently in this species . Skin diseases were seen on a number of seals, 14% had abraded flippers, 12% had areas of alopecia, 8% had a skin disease with inclusion bodies, suggesting a viral etiology, 6% had ulcers of unknown cause, 6% had areas of bacterial dermatitis, and single cases of umbilical ulcer and cutaneous papilloma were seen . The abrasions on the flippers were probably due to clambering over rocks . However, in Northern fur seals (Sawyer, 1976) similar lesions were thought to be due to San Miguel sealion virus and in California sealions (Nutting & Darley, 1980) Demodex sp . caused similar lesions on the flippers . Neither of these causes were looked for . The presumed viral skin disease appears not to have been recorded previously although it bore some resemblance microscopically to seal pox (Wilson & Poglayan-Neuwall, 1971 ; Okada & Fujomoto, 1984) . Umbilical lesions are common in Grey and Common seals and have been discussed by Drescher (1978) and Baker (1984) . The ulcers elsewhere were of unknown cause and small, unlike the ulcerative lesions in seals reported previously by Anderson et al. (1974) . Cutaneous ulceration was recorded in grey seals by Bergman & Olsson (1984) as were other skin lesions believed to be due to adrenocortical hyperplasia . Eight cases of dental disease were seen, four in the Barra seals and four in the animals found dead elsewhere . Excessive wear appears to be common in a variety of pinnipeds . Baker (1980) recorded a case in a Grey seal . Weddell seals use their teeth to keep the breathing holes open, causing abrasion and infection of the inner tooth structure which results in death (Bertram, 1940 ; Carrick & Ingham, 1962a ; Stirling, 1969 ; Stirling, 1971) . Walruses get very worn cheek teeth, probably due to ingestion of sand with their prey (King, 1983) . Antartic fur seals abrade the medial surface of their cheek teeth, probably on krill exoskeletons (Laws, 1984) and excessive wear on the same teeth has been recorded by King (1983) . Occasional California sealions wear the anterior aspect of the incisors removing shellfish from rocks (Morejohn, 1969) . However, none of these seems to fit the cause of wear seen in the Grey seals . No other cases of supernumerary incisors have been found in any species of pinniped, although variation in the number and structure of teeth appears not uncommon, at least in the Northern fur seal (Chiasson, 1955) . Periodontal disease, often with tooth loss and



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osteomyelitis, is not rare ; cases have been recorded in Grey seals by Anderson et al. (1974) and Baker (1980) although the initiating factors are unknown . Beck (1985, personal communication) stated that 10% of Canadian grey seals have evidence of periodontal disease . Gingivitis and periodontal disease have been seen in Common seals (Stroud & Roffe, 1979 ; Reijnders et al., 1981) . Dental and jaw infections associated with tooth fractures during fighting are recorded in Elephant seals (Paulian, 1957 ; Carrick & Ingham, 1962b) . Four animals in the survey had a persistent pseudourachus . In a young Walrus (Cornell, Golden & Osborn, 1975) the presence of the same structure led to death, the bladder being pulled forward with secondary hydronephrosis and pyelonephritis . In the Grey seals reported here there was probably insufficient tension on the structure to lead to these sequelae . Four animals also had liquified blubber, clear oil running out of incisions, leaving only connective tissue beyond . As the affected areas were surrounded by a zone of hyperaemia the condition is assumed to have occurred in life . All four animals were caught in the late summer but the cause is unknown . Stedham, Casey & Keyes (1977) refer in passing to a similar condition in a Northern fur seal pup . Pulmonary neoplasia does not appear to have been recorded in Grey seals previously . However neoplasia of this type is not unknown in other pinnipeds . Howard, Britt & Simpson (1983) found five pulmonary neoplasms in about 1,500 California sealions and King (1983) mentioned a bronchial tumour in a Leopard seal . Three conditions are worthy of note in the seals which died of natural causes . The male from North Ronaldsay died of sepsis of the neck and one of the North Rona animals had septic wounds . As these occurred on sites of injuries received during fighting and as the bodies were recovered in the breeding season, it is reasonable to assume that they followed trauma during territorial disputes . Trauma with sepsis associated with fighting but without death has been recorded in several species of pinnipeds - Southern elephant seal (Laws, 1953), Ringed seal (Svenkernd, Rostad & Thorshaugh (1951), South American sealion (0taria byronia) (Vaz-Ferreira, 1981) and Weddell seals (Stirling, 1971) - and this would seem to be the usual course of events . However Baker & Doidge (1984) recorded two male Antarctic fur seals dying of sepsis during the breeding season . The female seal dying of an ulcerated oesophagus is of interest as no reference to any species of pinniped with a similar condition has been found but the tissues were too autolysed for meaningful histology . The cow, which died of asphyxia due to mucus in the airways, resembled a grey seal which died of a similar condition (Baker, 1980) and California sealions reported by Sweeney & Gilmartin (1974) . However, the previously reported cases had parasitic pneumonia as an underlying cause and no evidence of this was seen in the present case ; the reason for the massive mucus production remains obscure . Mastitis has been previously reported in single grey seals by Appleby (1984) and Baker (1980) and Baker et al. (1980) but in no case was the causal organism identified . Tongue ulcers due to self inflicted bites are common in Grey seal pups (Baker, 1984) but the tongue ulcers seen in the adult seem far too extensive to be due to this ; the cause is unknown . The fused Grey seal vertebrae are of interest as only extremely rarely are skeletal



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examinations included in autopsies . Zorab (1961) described two cases of ankylosing spondylosis in Mediterranian monk seals (Monachus monachus) but these were not similar to the present case . Van Bree (1974) described a case of atlanto-occipital ankylosis in a young Grey seal which he believed followed luxation of the joint at the time of birth. Morejohn (1969) described a vertebral column deformity and fusion in a California sealion with associated abnormalities of the pelvis and one femur . The published pictures suggest that the lesions were sequelae to osteomyelitis .

ACKNOWLEDGEMENTS

I wish to thank Dr J . Harwood, Director of the Sea Mammal Research Unit for the invitation to undertake the survey and for providing financial support for travel and laboratory costs . Members of staff of SMRU and Rosa and Rowena Baker kindly assisted with the post-mortem examinations . I am grateful to Mr J . Prime, also of SMRU, who very kindly aged all the animals by canine tooth section . I also wish to thank Mrs S . Spiller for capable technical assistance and Mrs B . Heap and Mrs L . Greatwich for typing the manuscript . REFERENCES ANDERSON, S. S ., BONNER, W . N ., BAKER, J . R . & RICHARDS, R . (1974) . Journal of the Zoological Society of London 174, 429. APPLEBY, E . C . (1964) . Diergeneesk 89, 201 . BAKER, J. R. (1980) . British Veterinary Journal 136, 443 . BAKER, J. R. (1984) . Journal of the Zoological Society of London 203, 23 . BAKER, J. R., ANDERSON, S . S., PRIME, J. H . & BAIRD, A . (1980) . British Veterinary Journal 136, 401 . BAKER, J. R. & DoIDGE, D . W . (1984). British Veterinary Journal 140, 210 . BAKER, J. R. & GATESMAN, T. J . (1985). Veterinary Record 116, 208 . BAKER, J. R . & MCCANN, T . S . (in press) . Journal of the Biological Society of London. BERGMAN, A . & OLSSON, M . (1984) . Proceedings from the Symposium on the Seals in the Baltic and Eurasian Lakes, Savolinna, Finland . BER'I RAM, G . C . L . (1940) . Scientific Report of the British Graham Land Expedition 1, 1 . BISHOP, L . (1979) . Journal of Wildlife Diseases 15, 285 . BONNER, W . N . (1972) . Oceanography and Marine Biology Annual Review 10, 461 . BRITT, J. O . & HOWARD, E . B . (1983). In Pathobiology of Marine Mammal Diseases Vol . 2 ed . E . B . Howard, p . 80. Boca Raton, Florida : CRC Press . CARRICK, R . & INGHAM, S . E . (1962a) . Journal of Population Dynamics and Utilization . CSIRO Wildlife Research 7, 198 . CARRICK, R . & INGHAM, S . E . (1962b) . CSIRO Wildlife Research 7, 102 . CHIASSON, R . B . (1955) . Journal of Mammalology 36, 562 . CORNELL, L . A ., GOLDEN, G . S . & OSBORN, K. G . (1975) . Journal of the American Veterinary Medical Association 167, 548 . DARLEY, M . D. & BROWNELL, R . L . (1972) . In Mammals of the Sea, ed . S . H . Ridgway, p . 538 . Springfield, Illinois : C . C . Thomas . DOUGHERTY, E . C . & HERMAN, C . N . (1947) . Helminth Society (Washington) 14, 77 . DRESCHER, H . E . (1978) . Saugetierkundliche Mitteilungen 26, 50 . FARMER, A . S . & ROBERTS, D . (1970) . On strandings of the Grey seal, Halichoerus grypus (Fabricius) in the south of the Isle of Man . Annual Report of the University of Liverpool Marine Biological Station, Port Erin, Isle of Man 83, 43 . FIENNES, R . N . T . W . (1966) . Journal of the Zoological Society of London 148, 363 . FLEISCHMAN, R . W . & SQUIRE, R . A. (1970) . Pathologica Veterinaria 7, 89 .



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