Br. vel.
1.
(1990) . 146, 129
CAUSES OF DEATH AND ILLNESS IN THE NATIVE SHEEP OF NORTH RONALDSAY, ORKNEY . I. ADULT SHEEP DAVID P . BRITT*t and JOHN R. BAKERt *Department of Veterinary Parasitology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA; t Department of Veterinary Pathology, University of Liverpool, Veterinary Field Station, Leahurst, Neston, Wirral, L64 7TE
SUMMARY
Post-mortem examinations on 71 native sheep found dead on the island of North Ronaldsay, Orkney in four visits between April 1983 and July 1985 were carried out. The sheep in this almost feral flock have access to a small area of unmanaged moorland pasture but are otherwise restricted to the foreshore where they subsist largely on Laminaria spp. and other seaweeds . Young adult animals died largely of heavy parasite burdens combined with inadequate nutrition, while the older sheep often starved because of severe dental disease precipitated by heavy deposits of tartar on the cheek teeth-rarely seen in sheep on a more conventional diet . Other underlying metabolic conditions, such as the extensive mineralization of the kidney medulla in many mature sheep, may be debilitating . The pathological findings suggest that adaptation to the peculiar environmental rigours and dietary restrictions on North Ronaldsay is less complete than has previously been assumed .
INTRODUCTION
North Ronaldsay sheep, survivors of the old indigenous Orkney breed, are amongst the smallest sheep of the British Isles, standing about 18 inches at the shoulder and of light build . The sheep are not feral animals but remain in the ownership of the present day islanders who differ in the amount of attention which they give to the sheep . The animals are confined to the shore and a few areas of unimproved grassland for much of the year by a wall running the circumference of the island . Most of the food is seeweed . According to the North Ronaldsay Native Sheep Regulations 1902 (cited by Fenton, 1969) the population of native sheep on North Ronaldsay should be 2302 (Tribe & Tribe, 1950 ; Fenton, 1969) ; since then the numbers have fluctuated at around 4000 (Ryder, 1968 ; Hall, 1975) . In general, management input has declined with the dramatic reduction in the numbers of human inhabitants of North Ronaldsay, from a maximum of 442 (Vernon, 1979) to about 80, many of whom are not involved in work with the sheep . $Present address : Department of Allied Health Sciences and Nursing, Kuwait University, P .O. Box 31470, 90805 Sulaibikhat, Kuwait . Correspondence to John R. Baker .
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Published information about mortality and morbidity in these animals is sparse and undetailed . Tribe & Tribe (1950) commented that the sheep `are very healthy and suffer from few diseases, most of the deaths being caused by exposure or drowning' . They made specific reference to a few diseases or disease agents : braxy `uncommon', gid `only a few isolated cases', ticks `entirely absent', worms `exceptionally few', footrot `never troublesome' and bloat `unknown' . Hall (1975) mentioned `a fairly high incidence of liver fluke' . W . B . Carstairs (personal communication), veterinarian to the island, also drew attention to the problems of liver fluke and other helminth infestations which have, perhaps, grown in importance since the observations of Tribe & Tribe . METHODS The data are based on four visits made to North Ronaldsay within 28 months : April 1983 ; October 1983 ; May 1984 ; and July/August 1985 . Seventy-one freshly dead sheep found during at least one full circuit of the island on each of these four visits were subject to post-mortem examination . The carcases were weighed, sexed, aged by inspection of the incisor teeth, examined for earmarks and then subjected to routine necropsy procedures. Inflammatory lesions were plated on blood agar and filmed on slides prior to shipment to the university and identification by routine methods . Samples for histological examination were preserved in 10% formalin prior to sectioning and staining by routine methods . The dry matter of kidneys was estimated by drying to constant weight in a hot-air oven at 80°C . The dry tissue was then ashed in a muffle furnace at 600°C for 8 hours . The ash was dissolved in concentrated hydrochloric acid and, after suitable dilution, calcium, magnesium and copper were estimated using atomic absorption spectrophotometry, sodium and potassium by emission spectrophotometry and phosphorus by the method of Gormorri (1942) . Counting of coccidial oocysts and helminth eggs, sporulation of coccidial oocysts and culture of strongyloid nematode larvae were all carried out by standard methods . Oocysts and larvae were identified using the Ministry of Agriculture, Fisheries and Food (1979) manual . Lungworm larva were recovered directly from 5 g faecal samples by the Baermann technique with overnight incubation . Adult helminths were removed from the gastrointestinal tract at post-mortem examination and preserved in 10% formol saline . Samples of the contents of the abomasum, small intestine and caecum/colon were also collected . Because of difficulties in transportation, and because these organs were often damaged or incomplete, small volumes only were collected which precluded reliable quantitative estimations of helminth burdens . Adult Dictyocaulus were collected from trachea and lungs ; visible Mullerius lesions were confirmed on histological sections stained with haematoxylin and eosin . Fasciola were recovered from infected livers by opening the bile ducts and slicing and squeezing the tissue . Cysts of Sarcocystis gigantea were recorded on gross specimens at post-mortem examination . Small samples of heart and other muscles were examined for merozoites of S . tenella by trypsin digest of the tissue based on the method of Jacobs & Melton (1957) . Samples of the three Laminaria seaweed species on which the sheep principally feed were collected from the shore in October 1983 and May 1984 . The species were identified on the basis of features described by Thomson (1983) . The samples were diced and ground and three aliquots of each sample were analysed by methods routinely applied to grass and grass products (Ministry of Agriculture, Fisheries and Food, 1973) .
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RESULTS Observations on the live sheep A census of the live sheep carried out in October 1983 revealed a population of 4219 with a possible estimated error of ± 100 . The condition of the sheep was generally worse in the spring than at other times of year . Indeed, in October, 1983 many animals appeared quite fat and showed new wool growth, but even at this time there were signs of incipient ill-health . A high proportion of the droppings were diarrhoeic and some sheep had extensive faecal soiling of the fleece . Some sheep were coughing and a few were lame . In the spring most animals were thin, most coughed when moved and several showed evidence of skin irritation . During the visit at midsummer 1985 the condition of the sheep varied with their location on the island, and in particular those at the northern extremity were in poor condition .
Table I Permanent incisors in juvenile and adult sheep examined post mortem
No . permanent incisors
0 2 4 6 7 8
Broken mouthed Not recorded
No . sheep
17 11 9 4 8 9
12 1
Observations on the dead sheep Seventy-one adult and juvenile sheep were examined post mortem : 33 in April 1983, six in October 1983, 21 in May 1984 and 11 in July 1985 . The state of eruption or loss of the permanent incisor teeth of these animals is shown in Table I, which indicates two peaks of mortality : one in young adults, the other among aged sheep . The bodily condition of the sheep examined was generally poor (Table II), 79% were thin or emaciated at the time of death . The sexes of the sheep is given in Table III which also gives data on pregnant, barren and nursing ewes during the breeding season . The pregnancy rate was 80% . The difference between the number of males (including castrates) and females in the sample is not significant and suggests that the adults on the shore are in an approximate ratio of 1 :1 . Primary causes of death The primary causes of death are listed in Table IV . Dental disease, malnutrition and starvation account for nearly 60% of deaths . Dental disease was characterized by the
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Table II Bodily condition of juvenile and adult sheep post mortem Condition
No .
Over fat Good Moderate Thin Emaciated
0 13 2
0 18 3
8 48
11 68
Total
71
100
Table III Sex of juvenile and adult sheep examined post mortem Sex
No.
%
Males Male castrates Females Not recorded
11 20 39 1
28 55 1
71
100
16
In May, 1984, in the middle of the lambing season, the adult females examined were divided into three groups on the basis of reproductive status : Females Pregnant Nursing Barren
7
47
5 3
33 20
15
100
(80% pregnancy rate in this sample) .
formation of massive amounts of tartar on the cheek teeth either all along the tooth row or restricted to, or most conspicuous on, the lower premolars, at which site the tartar even extended across the occlusal surface (Table V, Fig. 1) . The condition has already been described (Baker & Britt, 1984) and the correlation of incidence and severity with increased age of sheep and the significant association of the condition with emaciation has been noted . Extremely severe cases of periodontal disease, with alveolar recession and tooth loss, occurred in 25% of the sheep examined (Fig . 2) . Starvation/malnutrition, and parasitic gastroenteritis were major causes of death among young adults . The lethal cases of pneumonia occurred at all ages ; Pasteurella septica was isolated from five of the cases investigated bacteriologically.
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Table IV Primary causes of death in juvenile and adult sheep* Condition
Dental disease/starvation Starvation/malnutrition Parasitic gastroenteritis Pneumonia Drowning Trauma Cerebrocortical necrosis Fluke infestation Renal tubular necrosis Necrotic enteritis Pulmonary adenomatosis Myocarditis Glomerulonephritis Not diagnosed
Males
Females
Total
%
7 8 4 4 3 1 0 1 1 1 1 1 0 2
18 9 5 3 2 1 2 0 0 0 0 0 1 5
25 17 9 7 5 2 2 1 1 1 1 1 1 7
35 24 13 10 7 3 3 1 1 1 1 1 1 10
* Some animals had more than one primary cause of death . Table V Tartar on cheek teeth of adult sheep Extent of deposits
No . sheep affected
% Sheep affected
Absent Light Moderate Heavy
9 11 21 23
14 17 33 36
Total
64
100
Fig. 1 . Sheep maxilla showing large deposits of tartar on the anterior cheek teeth with swelling of the adjacent gum indicating gingivitis.
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The miscellaneous causes of death recorded from one or two carcases only are probably not related to the peculiar problems of survival faced by this flock but the two deaths due to trauma occurred on the western cliffs and were probably the result of falls .
Fig. 2. Naturally macerated sheep mandible found on the shore . There has been ante-mortem loss of the two central cheek teeth due to alveolar infection and recession and an associated osteomyelitis, as indicated by the swollen porous bone in this region and a discharging tooth root abscess ; the discharging sinus is visible .
Secondary causes of death The secondary causes of death (Table VI) show that various parasitoses were extremely common . In a few cases the decision as to whether the presence of gastrointestinal nematodes or flukes should be considered primary or secondary was reached somewhat arbitrarily but heavy infections have been included as primary causes of death while lighter infections may have been important contributory factors in several other animals . Dental tartar was the most common of the non-parasitic conditions and, again, it was to an extent arbitrary whether this should be considered primary or secondary . Where tartar deposition was `moderate' or `mild' and unaccompanied by evidence of severe periodontal disease, its role in mortality has been considered of secondary importance . Excessive wear was observed on the anterior aspect of the incisor teeth of eight sheep (Fig . 3) . Renal medullary mineralization occurred in nearly half the sheep and was weakly correlated with increasing age . The affected kidneys had pale streaks in the medullary tissue . An analysis of the kidneys is given in Table VII . Ash and dry weight values are similar to those of normal sheep without gross evidence of renal mineralization, but calcium, phosphorus and copper levels in the sheep from North Ronaldsay were higher than in kidneys of grass-fed sheep used for comparison, and the sodium content was less . The 12 secondary cases of pneumonia were mild, affecting a small proportion of the lung volume . Five cases were examined bacteriologically and small numbers of Pasteurella septica were recovered from one of them .
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MORTALITY IN ADULT SHEEP IN ORKNEY
The remaining 37 secondary conditions are of general interest, and of undoubted significance to the affected sheep, but contribute little to an understanding of the special problems of the flock . Table VI Secondary causes of death and other lesions in juvenile and adult sheep* Condition
Parasite infestations Melophagus ovinus Cysticercus tenuicollis Sarcocystis giganlea Dictyocaulus filaria Muellerius capillaris
Mixed parasitic gastroenteritis Sarcocystis tenella Damalinia ovis Moniezia expansa Fasciola hepatica Trichuris ovis
Calcified pelvic mass Cysticercus ovis
Non-parasitic conditions Dental tartar Renal medullary mineralization Bald knees Pneumonia Peridontal disease Worn incisors Pleural adhesions Calcified lung lesions Mesenteric lymph node abscesses Hepatic microabscesses Lumpy wool disease Trauma Peritoneal adhesions Deformed trachea Pulmonary collapse Renal cysts Renal scars Abomasal ulcers Sand in alimentary canal Broken teeth Retained deciduous teeth Displaced incisors
No. sheep affected
% Sheep affected
42 32 30 30 29 22 15 13 11 10 9 5
59 45 42 42 41 31 21 18 16 14 13 7
2
3
38 32 17 12 12 8 7 7 5 5 4 4 3 2 2 2 2 2 2 2 2 2
54 45 24 17 17 11 10 10 7 7 6 6 4 3 3 3 3 3 3 3 3 3
The following abnormalities were recorded from one carcase only : amorphous globosus, bald knees with subcutaneous abscesses, bald pasterns, blind teats, calcified mass in neck muscle, conjunctivitis, cryptorchidism, dystokia, endometritis, excessive wear of feet, fat necrosis, infected lesions associated with hobbling, inhaled foreign material, lymphosarcoma, milk in stomach (adult), myocarditis, necrotic fat in peritoneum, overgrown hooves, renal melanosis, string in rumen, senile myocardial pigmentation, wool ball . * The numbers are minimal because several of the carcases had organs missing due to the activity of scavenging birds .
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Sheep incisor teeth showing wear on the anterior surfaces of the central teeth . This may be due to eating the cortex of Laminaria stapes or possibly to eating mussels .
Fig. 3 .
Table VII Analyses of kidneys with medullary mineralization North Ronaldsay sheep
Control sheep
18 90 ± 2 . 61 1 . 12 ± 0 . 08 6 . 02 ± 1 . 12
18 . 72 ± 1 . 41 1 .10 ± 0 . 13 5 . 85 ± 0 . 35
Dry weight as % wet weight Ash weight as % wet weight Ash weight as % dry weight Mineral composition of ash (%) : Calcium Copper Magnesium Phosphorus Potassium Sodium
3.2± 1 .4
0 . 11 ± 0 . 23 1.3 ± 5.0± 16 . 7 ± 16 . 1 ±
0.3 1.8 1.9 2.4
0. 6 ± 0 . 03 ± 1.5 ± 2.3± 13 . 8 ± 22 . 4 ±
0. 2 0 . 08 0. 2 0. 4 4. 0 3. 1
* Clun cross ewes on lush grass .
Parasite studies : 1 . Gastrointestinal parasites
A majority of the faecal samples contained coccidial oocysts with highest, but still modest, counts in samples from young animals (up to 348 000/g) . Eimeria ovina and E. crandallis were the most numerous, other species present were E. ahsata, E. intricata, E. marsica, E. ovinoidalis, E. pallida and E . parva . Adult tape worms (Moniezia expansa) were found in the small intestines of 11 of the 71 sheep . From small volumes of abomasal contents examined from 28 sheep, Ostertagia spp . were found in 26 and Trichostrongylus axei in 22 . Larvae of Haemonchus were hatched from faecal egg culture on one occasion but no adult worms were recovered from abomasa . Trichostrongylus vitrinus and/or T. colubriformis were present in the small intestinal contents from 34 of 38 sheep . Other small intestinal worms found less frequently included Cooperia spp . (C. oncophora, C. mcmastert ) in 14 samples, Nematodirus filicollis in 10, N. battus, Bunostomum trigonocephalum and Strongyloides one each . Eggs of Strongyloides were seen in three faecal samples . Ostertagia spp .,
MORTALITY IN ADULT SHEEP IN ORKNEY
137
usually associated with the abomasum, were also recovered from 10 samples of small intestine contents . Eggs of Capillaria spp . were seen in seven faecal samples but no adults were found . Trichuris ovis were present in the caeca of 10 sheep and Chabertia ovina in the colon contents of four. Parasites studies: 2. Lungworms Adult Dictyocaulus filaria was found in the bronchi and lungs of 33 of 71 sheep, with heavy infections in yearlings . Nodules of Muellerius capillaris were present in the
subpleural tissue of 29, principally older animals . Small numbers of larvae of a third lungworm, Protostrongylus rufescens, were recovered from the faeces of four adult sheep . Parasite studies: 3. Tissue parasites Macrocysts of Sarcocystis gigantea were present in 27 of the 71 carcases . The cysts were
most often found in the oesophageal muscle (29/30) and tongue (22/30) . Prevalence of the parasite was closely related to the age of the host (Table VIII) . Examination of various tissues from 20 sheep for the microscopic cysts of Sarcocystis tenella suggests this parasite is also common in the flock (Table IX) . Table VIII Age-related prevalence of Sarcocystis gigantea macrocysts in 71 juvenile and adult North Ronaldsay sheep Age of sheep No . sheep No . sheep with macrocysts Sheep with macrocysts
< 3 years 27 0 0
3-5 years 24 10 42
> 5 years 20 17 85
Table IX Sarcocystis tenella cystozoites in tryptic digest preparations Total
Age of sheep No . of sheep No . samples with cystozoites/no . samples examined : diaphragm oesophagus heart
Up to 3 years 8
3 Years and above 11
19
0/2 3/7 4/7
0/3 2/4 10/11
0/5 5/11 14/18
Larval cestodes were a common finding, 32 sheep had from one to 10 cysts of Taenia hydatigena (Cysticercus tenuicollis) attached to the abdominal serosal surfaces ; several sheep showed calcified tracks caused by the migrating larvae in the liver . Single cysts of Taenia oais (Cysticercus oais) were present in the myocardium of two sheep, one of which had a similar, calcified, cyst in the neck muscles . Small, calcified nodules a few millimetres in diameter in the livers of seven and the lungs of two sheep and a larger calcified mass
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obstructing the pelvis of a ewe, were possibly of parasitic origin and could have been dead cysts of Echinococcus granulosus . However, this organism is thought not to occur in Orkney . Adult flukes, Fasciola hepatica, were recovered from the livers of 11 of the 71 sheep and Fasciola eggs were found in seven of the 55 faecal samples . Faecal egg counts were low, less than 100 eggs/g, and numbers of adults were small, from one to 26, most infected livers containing fewer than 10 . Parasite studies: 4. Ectoparasites Sheep keds, Melophagus ovinus, were a frequent finding ; of the 71 animals examined 42
were infected . The biting louse, Damalinia ovis, was seen on 13 carcases. Seaweed analysis
The vast bulk of Laminaria cast ashore and eaten by the sheep was L. digitata . L. hyper-
borea and L . saccharina were uncommon . In most areas, both stapes and attached fronds were washed ashore although on some occasions only stapes seem to have been deposited, especially on the south-east coast . The stape cortex was eaten by the sheep but the medullary tissue was ignored . Analysis of the nutritional content of the Laminaria species is given in Table X . Table X Analysis of the nutritive value of Laminaria species L . digitata fronds
October Dry matter (g/kg) 253 Nutrient constituents (g/kg dry matter) Crude protein 103 Ether extract 6 Crude fibre 90 Modified acid detergent fibre 258 Ash 113 May 86 Dry matter (g/kg) Nutrient constituents (g/kg dry matter) Crude protein 96 Ether extract 1 .4 Crude fibre 68 Modified acid detergent fibre 256 Ash 300
L. hyperborea
L . saccharina
fronds
staple cortex
staple medulla
fronds
228
191
152
200
115 3 104 318 215
152 5 116 437 250
50 1 127 388 331
147 5 85 269 179
167
286
148 2.6 141 404 287
115 1 .4 116 322 374
DISCUSSION The number of sheep present in October 1983, at 4219 ± 100, is close to the figures given by Ryder (1968) and Hall (1975), suggesting that the population has been stable for the last two decades . Under the North Ronaldsay Native Sheep Regulations, 1902, the
MORTALITY IN ADULT SHEEP IN ORKNEY
139
maximum number of sheep allowed is 2302 . A figure close to this was reported as early as 1790 (Fenton, 1969) and as recently as 1950 (Tribe & Tribe, 1950), indicating that the increase in numbers is a relatively recent phenomenon . The current sheep numbers probably represent the maximum carrying capacity of the island at a theoretical five linear yards of shore per animal . However, many areas of the western shore are barren cliffs and over a considerable proportion of the remainder seaweed was neither growing nor was it seen to be washed up . Observations in May 1984 indicated that only 2 . 2 miles of coast had significant quantities of Laminaria cast up, giving only 0 . 9 linear yards of food-bearing shore per sheep . In many areas the cast Laminaria extended down the shore for several yards below high-water mark and at spring tides fronds growing in shallow water were exposed, so that linear yardage gives an indication of crowding rather than a true picture of seaweed availability . The majority of intertidal seaweeds are wracks of various species eaten only sparsely by the sheep . An additional source of food is the 136 hectares of poor quality, unmanaged permanent pasture outside the dyke . With current sheep numbers, this gives a density of more than 30 sheep per hectare, greatly in excess of the carrying capacity of the best lowland pasture . The vegetation on these sites was virtually eaten to soil level each time the island was visited . Assuming that the current sheep population is stable and since few if any are taken by the islanders, deaths-other than neonatal mortalities-must approximate lamb production . Estimates, based on the rather limited data available, suggest an annual mortality rate in juveniles and adults of about 25% . Bodily condition of the sheep was poorest in the spring, improving through summer and autumn . A number of factors probably combine to produce the poor state of health around lambing time including stresses associated with severe winter weather, fetal growth and the demands of lactation, coupled with relatively little grass growth early in the year at these latitudes and the poor nutritive quality of Laminaria digitata fronds cast in the spring . The sparsity of previous reports of disease in the native sheep of North Ronaldsay has already been noted . The claim by Tribe & Tribe (1950) that the sheep `are very healthy and suffer from few diseases' is totally at variance with our experience . This, and the observation of `exceptionally few worms', indicate that important changes have occurred (probably associated with the increase in sheep numbers and a reduction in management of the flock) since the time of their investigation . However, we agree with most of their comments about specific conditions . The majority of the sheep died as young adults or in old age . The young died mainly of parasitism or starvation . Dental diseases and starvation associated with these problems were the main causes of death in the older animals, suggesting that tartar deposition was progressive and that periodontal disease was linked with ageing alveolar structure . We believe that dental tartar and periodontal disease resulted in pain on mastication leading to poor maceration of food and thus reduction in its digestibility (Baker & Britt, 1984) . Drowning was a rather unexpected cause of death and occurred in emaciated and fit sheep . Emaciated animals were probably too slow or feeble to escape the advancing tide if they ventured over-far from the shore to graze at low water or if they had fallen through rafts of Laminaria and other seaweeds which sometime formed . Because most of the sheep were unshorn, the weight of water in the fleece following accidental immersion could seriously impede efforts to escape even by the fit animals .
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The high incidence of renal mineralization requires more detailed investigation . It may be due to highly efficient absorption of the metals found in our analyses, as demonstrated in this breed for copper (Wiener, Field & Smith, 1977), and/or unusually high dietary intake . In many of the sheep the skin on the anterior aspect of the carpal joints was bald, apparently due to abrasion caused by kneeling to feed ; many of the sheep spent long periods attempting to graze the sparse pasture and appeared to have adopted a kneeling posture to facilitate cropping of the consistently low growth . The worn incisors seen in eight sheep are believed to have resulted from eating the cortex of the tough Laminaria stapes. Many faecal samples contained comminuted mussel shells (Mytilus edulis) and one sample consisted almost entirely of this material . It is not known if ingestion of this material was accidental or deliberate . If the mussels were `grazed', this could result in tooth wear, and contribute to renal mineralization . The intestinal coccidia found comprised a mixture of species similar to those infecting sheep elsewhere . Total faecal oocyst counts were not high enough to suggest that the flock suffered serious effects from these organisms . The helminths recovered from the alimentary tract compare closely with the records from Scottish sheep given by Parnell et al. (1954) and earlier surveys cited in that work . Parnell and his colleagues found Ostertagia spp ., Trichostrongylus axes, Chabertia ovina, T. vitrinus, Nematodirus spp ., Capillaria spp . and Haemonchus contortus from nine North Ronaldsay sheep . The present study confirmed that proliferation of a wide range of parasitic helminths was successful on North Ronaldsay in spite of the constraints imposed by apparently unfavourable environmental conditions. Although there are significant differences in the pathogenicity of the various species of gastrointestinal nematodes recorded, heavy infestations with any combination can be responsible at least for loss of condition in the host and even death . The tapeworm, Moniezia expansa, is not considered a serious pathogen and this was confirmed in our studies . Larval cestodes, particularly migrating oncospheres of Taenia hydatigena, may have contributed to lack of thrift in infected lambs . Muellerius capillaris is found more frequently in Scottish sheep than other lungworms (Parnell et al., 1954) and is particularly common in adult sheep . Infection with Dictyocaulis filaria, the more important pathogen, is common in the native sheep of North Ronaldsay and appears to be an important cause of unthriftiness and an occasional cause of death in young adults . Fasciola hepatica is a major pathogen in sheep and the threat posed by the endemicity of this parasite on North Ronaldsay will continue in the absence of specific treatment of the sheep and as long as the habitats of the snail intermediate host persist . Infection with Sarcocystis tenella is a common condition in sheep throughout Britain . Ashford (1977) and Leguia & Herbert (1979) found almost 100% prevalence. Reported observations on the macrocysts of Sarcocystis gigantea in Britain are much less frequent (Ashford & Britt, 1983 ; Britt & Baker, 1983) . The prevalence of S. tenella amongst the North Ronaldsay sheep is probably similar to that in sheep elsewhere in Britain ; the prevalence of S. gigantea appears to be much higher . The role of both Sarcocystis species in natural disease in sheep remains to be established but lambs experimentally infected with S. tenella sporocysts develop a variety of clinical signs (Munday & Obendorf, 1984 ; O'Toole et al., 1986) . We have not been able to establish the importance of sarcocystosis in the North Ronaldsay flock but it would be unwise to assume that these parasites make no contribution to morbidity or mortality.
MORTALITY IN ADULT SHEEP IN ORKNEY
1 41
Neither the sheep ked, Melophagus ovinus, nor the biting louse, Damalinia ovis, is of major pathological significance, although heavy infestations with keds may give rise to anaemia (Soulsby, 1982) . Many of the live sheep were seen to be troubled by skin irritation, presumably caused by these parasites which were so frequent on the carcases . Rubbing to relieve this irritation caused fleece loss and a reduced resistance to cold which could be a significant threat to the well-being of sheep living in exposed conditions . Analysis of Laminaria species suggests that in October it provides an adequate diet as far as gross nutrients are concerned if available in sufficient quantity . L . digitata probably provides the bulk of the marine food in May, when the fronds are cast prior to the growth of new ones (Thomson, 1983) . The water content of the old fronds was found to be high . This bulky, wet material may well provide insufficient calories at the time of greatest demand . The poor nutritive value of seaweed in spring was noted by Hall (1975) although he suggested that the predominant species cast ashore was L . hyperborea, a species only washed up in small amounts during our study . The flock of North Ronaldsay sheep on North Ronaldsay comprises the largest group of animals of this rare breed and requires care in conservation . The flock exists in an almost feral state under conditions to which the animals have become less well adapted than earlier observers may well have implied . The present numbers of sheep and the reduced level of human intervention may have brought to light difficulties in adaptation to the environment which were previously not apparent. The present health status of the flock reveals a complexity of problems associated with dietary and other factors stemming from the unusual circumstances of their existence . Many of the diseases we have recorded in the sheep are preventable by the application of standard flock management procedures . All the problems could be relieved by reducing the size of the flock . Without such reduction, and in the absence of a larger work force and/or better facilities for handling the animals, it seems unlikely that the health of the flock will improve .
ACKNOWLEDGEMENTS The Animal Health Trust, Newmarket and the Universities Federation for Animal Welfare, Potters Bar provided financial support . We are also grateful to the following for help in the field and/or laboratory aspects of these investigations : Rosa and Carl Baker, Adam Britt, Dr T . L. J . Laurence, Ms S . Crozier, Mrs B . Harling, and Mr M . Savage . Ms Paula Jenkins prepared the photographs .
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(Accepted for publication 25 April 1989)
ANNOUNCEMENT
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1.
(1990) . 146, 129
CAUSES OF DEATH AND ILLNESS IN THE NATIVE SHEEP OF NORTH RONALDSAY, ORKNEY . I. ADULT SHEEP DAVID P . BRITT*t and JOHN R. BAKERt *Department of Veterinary Parasitology, Liverpool School of Tropical Medicine, Pembroke Place, Liverpool, L3 5QA; t Department of Veterinary Pathology, University of Liverpool, Veterinary Field Station, Leahurst, Neston, Wirral, L64 7TE
SUMMARY
Post-mortem examinations on 71 native sheep found dead on the island of North Ronaldsay, Orkney in four visits between April 1983 and July 1985 were carried out. The sheep in this almost feral flock have access to a small area of unmanaged moorland pasture but are otherwise restricted to the foreshore where they subsist largely on Laminaria spp. and other seaweeds . Young adult animals died largely of heavy parasite burdens combined with inadequate nutrition, while the older sheep often starved because of severe dental disease precipitated by heavy deposits of tartar on the cheek teeth-rarely seen in sheep on a more conventional diet . Other underlying metabolic conditions, such as the extensive mineralization of the kidney medulla in many mature sheep, may be debilitating . The pathological findings suggest that adaptation to the peculiar environmental rigours and dietary restrictions on North Ronaldsay is less complete than has previously been assumed .
INTRODUCTION
North Ronaldsay sheep, survivors of the old indigenous Orkney breed, are amongst the smallest sheep of the British Isles, standing about 18 inches at the shoulder and of light build . The sheep are not feral animals but remain in the ownership of the present day islanders who differ in the amount of attention which they give to the sheep . The animals are confined to the shore and a few areas of unimproved grassland for much of the year by a wall running the circumference of the island . Most of the food is seeweed . According to the North Ronaldsay Native Sheep Regulations 1902 (cited by Fenton, 1969) the population of native sheep on North Ronaldsay should be 2302 (Tribe & Tribe, 1950 ; Fenton, 1969) ; since then the numbers have fluctuated at around 4000 (Ryder, 1968 ; Hall, 1975) . In general, management input has declined with the dramatic reduction in the numbers of human inhabitants of North Ronaldsay, from a maximum of 442 (Vernon, 1979) to about 80, many of whom are not involved in work with the sheep . $Present address : Department of Allied Health Sciences and Nursing, Kuwait University, P .O. Box 31470, 90805 Sulaibikhat, Kuwait . Correspondence to John R. Baker .
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Published information about mortality and morbidity in these animals is sparse and undetailed . Tribe & Tribe (1950) commented that the sheep `are very healthy and suffer from few diseases, most of the deaths being caused by exposure or drowning' . They made specific reference to a few diseases or disease agents : braxy `uncommon', gid `only a few isolated cases', ticks `entirely absent', worms `exceptionally few', footrot `never troublesome' and bloat `unknown' . Hall (1975) mentioned `a fairly high incidence of liver fluke' . W . B . Carstairs (personal communication), veterinarian to the island, also drew attention to the problems of liver fluke and other helminth infestations which have, perhaps, grown in importance since the observations of Tribe & Tribe . METHODS The data are based on four visits made to North Ronaldsay within 28 months : April 1983 ; October 1983 ; May 1984 ; and July/August 1985 . Seventy-one freshly dead sheep found during at least one full circuit of the island on each of these four visits were subject to post-mortem examination . The carcases were weighed, sexed, aged by inspection of the incisor teeth, examined for earmarks and then subjected to routine necropsy procedures. Inflammatory lesions were plated on blood agar and filmed on slides prior to shipment to the university and identification by routine methods . Samples for histological examination were preserved in 10% formalin prior to sectioning and staining by routine methods . The dry matter of kidneys was estimated by drying to constant weight in a hot-air oven at 80°C . The dry tissue was then ashed in a muffle furnace at 600°C for 8 hours . The ash was dissolved in concentrated hydrochloric acid and, after suitable dilution, calcium, magnesium and copper were estimated using atomic absorption spectrophotometry, sodium and potassium by emission spectrophotometry and phosphorus by the method of Gormorri (1942) . Counting of coccidial oocysts and helminth eggs, sporulation of coccidial oocysts and culture of strongyloid nematode larvae were all carried out by standard methods . Oocysts and larvae were identified using the Ministry of Agriculture, Fisheries and Food (1979) manual . Lungworm larva were recovered directly from 5 g faecal samples by the Baermann technique with overnight incubation . Adult helminths were removed from the gastrointestinal tract at post-mortem examination and preserved in 10% formol saline . Samples of the contents of the abomasum, small intestine and caecum/colon were also collected . Because of difficulties in transportation, and because these organs were often damaged or incomplete, small volumes only were collected which precluded reliable quantitative estimations of helminth burdens . Adult Dictyocaulus were collected from trachea and lungs ; visible Mullerius lesions were confirmed on histological sections stained with haematoxylin and eosin . Fasciola were recovered from infected livers by opening the bile ducts and slicing and squeezing the tissue . Cysts of Sarcocystis gigantea were recorded on gross specimens at post-mortem examination . Small samples of heart and other muscles were examined for merozoites of S . tenella by trypsin digest of the tissue based on the method of Jacobs & Melton (1957) . Samples of the three Laminaria seaweed species on which the sheep principally feed were collected from the shore in October 1983 and May 1984 . The species were identified on the basis of features described by Thomson (1983) . The samples were diced and ground and three aliquots of each sample were analysed by methods routinely applied to grass and grass products (Ministry of Agriculture, Fisheries and Food, 1973) .
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RESULTS Observations on the live sheep A census of the live sheep carried out in October 1983 revealed a population of 4219 with a possible estimated error of ± 100 . The condition of the sheep was generally worse in the spring than at other times of year . Indeed, in October, 1983 many animals appeared quite fat and showed new wool growth, but even at this time there were signs of incipient ill-health . A high proportion of the droppings were diarrhoeic and some sheep had extensive faecal soiling of the fleece . Some sheep were coughing and a few were lame . In the spring most animals were thin, most coughed when moved and several showed evidence of skin irritation . During the visit at midsummer 1985 the condition of the sheep varied with their location on the island, and in particular those at the northern extremity were in poor condition .
Table I Permanent incisors in juvenile and adult sheep examined post mortem
No . permanent incisors
0 2 4 6 7 8
Broken mouthed Not recorded
No . sheep
17 11 9 4 8 9
12 1
Observations on the dead sheep Seventy-one adult and juvenile sheep were examined post mortem : 33 in April 1983, six in October 1983, 21 in May 1984 and 11 in July 1985 . The state of eruption or loss of the permanent incisor teeth of these animals is shown in Table I, which indicates two peaks of mortality : one in young adults, the other among aged sheep . The bodily condition of the sheep examined was generally poor (Table II), 79% were thin or emaciated at the time of death . The sexes of the sheep is given in Table III which also gives data on pregnant, barren and nursing ewes during the breeding season . The pregnancy rate was 80% . The difference between the number of males (including castrates) and females in the sample is not significant and suggests that the adults on the shore are in an approximate ratio of 1 :1 . Primary causes of death The primary causes of death are listed in Table IV . Dental disease, malnutrition and starvation account for nearly 60% of deaths . Dental disease was characterized by the
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Table II Bodily condition of juvenile and adult sheep post mortem Condition
No .
Over fat Good Moderate Thin Emaciated
0 13 2
0 18 3
8 48
11 68
Total
71
100
Table III Sex of juvenile and adult sheep examined post mortem Sex
No.
%
Males Male castrates Females Not recorded
11 20 39 1
28 55 1
71
100
16
In May, 1984, in the middle of the lambing season, the adult females examined were divided into three groups on the basis of reproductive status : Females Pregnant Nursing Barren
7
47
5 3
33 20
15
100
(80% pregnancy rate in this sample) .
formation of massive amounts of tartar on the cheek teeth either all along the tooth row or restricted to, or most conspicuous on, the lower premolars, at which site the tartar even extended across the occlusal surface (Table V, Fig. 1) . The condition has already been described (Baker & Britt, 1984) and the correlation of incidence and severity with increased age of sheep and the significant association of the condition with emaciation has been noted . Extremely severe cases of periodontal disease, with alveolar recession and tooth loss, occurred in 25% of the sheep examined (Fig . 2) . Starvation/malnutrition, and parasitic gastroenteritis were major causes of death among young adults . The lethal cases of pneumonia occurred at all ages ; Pasteurella septica was isolated from five of the cases investigated bacteriologically.
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Table IV Primary causes of death in juvenile and adult sheep* Condition
Dental disease/starvation Starvation/malnutrition Parasitic gastroenteritis Pneumonia Drowning Trauma Cerebrocortical necrosis Fluke infestation Renal tubular necrosis Necrotic enteritis Pulmonary adenomatosis Myocarditis Glomerulonephritis Not diagnosed
Males
Females
Total
%
7 8 4 4 3 1 0 1 1 1 1 1 0 2
18 9 5 3 2 1 2 0 0 0 0 0 1 5
25 17 9 7 5 2 2 1 1 1 1 1 1 7
35 24 13 10 7 3 3 1 1 1 1 1 1 10
* Some animals had more than one primary cause of death . Table V Tartar on cheek teeth of adult sheep Extent of deposits
No . sheep affected
% Sheep affected
Absent Light Moderate Heavy
9 11 21 23
14 17 33 36
Total
64
100
Fig. 1 . Sheep maxilla showing large deposits of tartar on the anterior cheek teeth with swelling of the adjacent gum indicating gingivitis.
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The miscellaneous causes of death recorded from one or two carcases only are probably not related to the peculiar problems of survival faced by this flock but the two deaths due to trauma occurred on the western cliffs and were probably the result of falls .
Fig. 2. Naturally macerated sheep mandible found on the shore . There has been ante-mortem loss of the two central cheek teeth due to alveolar infection and recession and an associated osteomyelitis, as indicated by the swollen porous bone in this region and a discharging tooth root abscess ; the discharging sinus is visible .
Secondary causes of death The secondary causes of death (Table VI) show that various parasitoses were extremely common . In a few cases the decision as to whether the presence of gastrointestinal nematodes or flukes should be considered primary or secondary was reached somewhat arbitrarily but heavy infections have been included as primary causes of death while lighter infections may have been important contributory factors in several other animals . Dental tartar was the most common of the non-parasitic conditions and, again, it was to an extent arbitrary whether this should be considered primary or secondary . Where tartar deposition was `moderate' or `mild' and unaccompanied by evidence of severe periodontal disease, its role in mortality has been considered of secondary importance . Excessive wear was observed on the anterior aspect of the incisor teeth of eight sheep (Fig . 3) . Renal medullary mineralization occurred in nearly half the sheep and was weakly correlated with increasing age . The affected kidneys had pale streaks in the medullary tissue . An analysis of the kidneys is given in Table VII . Ash and dry weight values are similar to those of normal sheep without gross evidence of renal mineralization, but calcium, phosphorus and copper levels in the sheep from North Ronaldsay were higher than in kidneys of grass-fed sheep used for comparison, and the sodium content was less . The 12 secondary cases of pneumonia were mild, affecting a small proportion of the lung volume . Five cases were examined bacteriologically and small numbers of Pasteurella septica were recovered from one of them .
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MORTALITY IN ADULT SHEEP IN ORKNEY
The remaining 37 secondary conditions are of general interest, and of undoubted significance to the affected sheep, but contribute little to an understanding of the special problems of the flock . Table VI Secondary causes of death and other lesions in juvenile and adult sheep* Condition
Parasite infestations Melophagus ovinus Cysticercus tenuicollis Sarcocystis giganlea Dictyocaulus filaria Muellerius capillaris
Mixed parasitic gastroenteritis Sarcocystis tenella Damalinia ovis Moniezia expansa Fasciola hepatica Trichuris ovis
Calcified pelvic mass Cysticercus ovis
Non-parasitic conditions Dental tartar Renal medullary mineralization Bald knees Pneumonia Peridontal disease Worn incisors Pleural adhesions Calcified lung lesions Mesenteric lymph node abscesses Hepatic microabscesses Lumpy wool disease Trauma Peritoneal adhesions Deformed trachea Pulmonary collapse Renal cysts Renal scars Abomasal ulcers Sand in alimentary canal Broken teeth Retained deciduous teeth Displaced incisors
No. sheep affected
% Sheep affected
42 32 30 30 29 22 15 13 11 10 9 5
59 45 42 42 41 31 21 18 16 14 13 7
2
3
38 32 17 12 12 8 7 7 5 5 4 4 3 2 2 2 2 2 2 2 2 2
54 45 24 17 17 11 10 10 7 7 6 6 4 3 3 3 3 3 3 3 3 3
The following abnormalities were recorded from one carcase only : amorphous globosus, bald knees with subcutaneous abscesses, bald pasterns, blind teats, calcified mass in neck muscle, conjunctivitis, cryptorchidism, dystokia, endometritis, excessive wear of feet, fat necrosis, infected lesions associated with hobbling, inhaled foreign material, lymphosarcoma, milk in stomach (adult), myocarditis, necrotic fat in peritoneum, overgrown hooves, renal melanosis, string in rumen, senile myocardial pigmentation, wool ball . * The numbers are minimal because several of the carcases had organs missing due to the activity of scavenging birds .
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Sheep incisor teeth showing wear on the anterior surfaces of the central teeth . This may be due to eating the cortex of Laminaria stapes or possibly to eating mussels .
Fig. 3 .
Table VII Analyses of kidneys with medullary mineralization North Ronaldsay sheep
Control sheep
18 90 ± 2 . 61 1 . 12 ± 0 . 08 6 . 02 ± 1 . 12
18 . 72 ± 1 . 41 1 .10 ± 0 . 13 5 . 85 ± 0 . 35
Dry weight as % wet weight Ash weight as % wet weight Ash weight as % dry weight Mineral composition of ash (%) : Calcium Copper Magnesium Phosphorus Potassium Sodium
3.2± 1 .4
0 . 11 ± 0 . 23 1.3 ± 5.0± 16 . 7 ± 16 . 1 ±
0.3 1.8 1.9 2.4
0. 6 ± 0 . 03 ± 1.5 ± 2.3± 13 . 8 ± 22 . 4 ±
0. 2 0 . 08 0. 2 0. 4 4. 0 3. 1
* Clun cross ewes on lush grass .
Parasite studies : 1 . Gastrointestinal parasites
A majority of the faecal samples contained coccidial oocysts with highest, but still modest, counts in samples from young animals (up to 348 000/g) . Eimeria ovina and E. crandallis were the most numerous, other species present were E. ahsata, E. intricata, E. marsica, E. ovinoidalis, E. pallida and E . parva . Adult tape worms (Moniezia expansa) were found in the small intestines of 11 of the 71 sheep . From small volumes of abomasal contents examined from 28 sheep, Ostertagia spp . were found in 26 and Trichostrongylus axei in 22 . Larvae of Haemonchus were hatched from faecal egg culture on one occasion but no adult worms were recovered from abomasa . Trichostrongylus vitrinus and/or T. colubriformis were present in the small intestinal contents from 34 of 38 sheep . Other small intestinal worms found less frequently included Cooperia spp . (C. oncophora, C. mcmastert ) in 14 samples, Nematodirus filicollis in 10, N. battus, Bunostomum trigonocephalum and Strongyloides one each . Eggs of Strongyloides were seen in three faecal samples . Ostertagia spp .,
MORTALITY IN ADULT SHEEP IN ORKNEY
137
usually associated with the abomasum, were also recovered from 10 samples of small intestine contents . Eggs of Capillaria spp . were seen in seven faecal samples but no adults were found . Trichuris ovis were present in the caeca of 10 sheep and Chabertia ovina in the colon contents of four. Parasites studies: 2. Lungworms Adult Dictyocaulus filaria was found in the bronchi and lungs of 33 of 71 sheep, with heavy infections in yearlings . Nodules of Muellerius capillaris were present in the
subpleural tissue of 29, principally older animals . Small numbers of larvae of a third lungworm, Protostrongylus rufescens, were recovered from the faeces of four adult sheep . Parasite studies: 3. Tissue parasites Macrocysts of Sarcocystis gigantea were present in 27 of the 71 carcases . The cysts were
most often found in the oesophageal muscle (29/30) and tongue (22/30) . Prevalence of the parasite was closely related to the age of the host (Table VIII) . Examination of various tissues from 20 sheep for the microscopic cysts of Sarcocystis tenella suggests this parasite is also common in the flock (Table IX) . Table VIII Age-related prevalence of Sarcocystis gigantea macrocysts in 71 juvenile and adult North Ronaldsay sheep Age of sheep No . sheep No . sheep with macrocysts Sheep with macrocysts
< 3 years 27 0 0
3-5 years 24 10 42
> 5 years 20 17 85
Table IX Sarcocystis tenella cystozoites in tryptic digest preparations Total
Age of sheep No . of sheep No . samples with cystozoites/no . samples examined : diaphragm oesophagus heart
Up to 3 years 8
3 Years and above 11
19
0/2 3/7 4/7
0/3 2/4 10/11
0/5 5/11 14/18
Larval cestodes were a common finding, 32 sheep had from one to 10 cysts of Taenia hydatigena (Cysticercus tenuicollis) attached to the abdominal serosal surfaces ; several sheep showed calcified tracks caused by the migrating larvae in the liver . Single cysts of Taenia oais (Cysticercus oais) were present in the myocardium of two sheep, one of which had a similar, calcified, cyst in the neck muscles . Small, calcified nodules a few millimetres in diameter in the livers of seven and the lungs of two sheep and a larger calcified mass
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obstructing the pelvis of a ewe, were possibly of parasitic origin and could have been dead cysts of Echinococcus granulosus . However, this organism is thought not to occur in Orkney . Adult flukes, Fasciola hepatica, were recovered from the livers of 11 of the 71 sheep and Fasciola eggs were found in seven of the 55 faecal samples . Faecal egg counts were low, less than 100 eggs/g, and numbers of adults were small, from one to 26, most infected livers containing fewer than 10 . Parasite studies: 4. Ectoparasites Sheep keds, Melophagus ovinus, were a frequent finding ; of the 71 animals examined 42
were infected . The biting louse, Damalinia ovis, was seen on 13 carcases. Seaweed analysis
The vast bulk of Laminaria cast ashore and eaten by the sheep was L. digitata . L. hyper-
borea and L . saccharina were uncommon . In most areas, both stapes and attached fronds were washed ashore although on some occasions only stapes seem to have been deposited, especially on the south-east coast . The stape cortex was eaten by the sheep but the medullary tissue was ignored . Analysis of the nutritional content of the Laminaria species is given in Table X . Table X Analysis of the nutritive value of Laminaria species L . digitata fronds
October Dry matter (g/kg) 253 Nutrient constituents (g/kg dry matter) Crude protein 103 Ether extract 6 Crude fibre 90 Modified acid detergent fibre 258 Ash 113 May 86 Dry matter (g/kg) Nutrient constituents (g/kg dry matter) Crude protein 96 Ether extract 1 .4 Crude fibre 68 Modified acid detergent fibre 256 Ash 300
L. hyperborea
L . saccharina
fronds
staple cortex
staple medulla
fronds
228
191
152
200
115 3 104 318 215
152 5 116 437 250
50 1 127 388 331
147 5 85 269 179
167
286
148 2.6 141 404 287
115 1 .4 116 322 374
DISCUSSION The number of sheep present in October 1983, at 4219 ± 100, is close to the figures given by Ryder (1968) and Hall (1975), suggesting that the population has been stable for the last two decades . Under the North Ronaldsay Native Sheep Regulations, 1902, the
MORTALITY IN ADULT SHEEP IN ORKNEY
139
maximum number of sheep allowed is 2302 . A figure close to this was reported as early as 1790 (Fenton, 1969) and as recently as 1950 (Tribe & Tribe, 1950), indicating that the increase in numbers is a relatively recent phenomenon . The current sheep numbers probably represent the maximum carrying capacity of the island at a theoretical five linear yards of shore per animal . However, many areas of the western shore are barren cliffs and over a considerable proportion of the remainder seaweed was neither growing nor was it seen to be washed up . Observations in May 1984 indicated that only 2 . 2 miles of coast had significant quantities of Laminaria cast up, giving only 0 . 9 linear yards of food-bearing shore per sheep . In many areas the cast Laminaria extended down the shore for several yards below high-water mark and at spring tides fronds growing in shallow water were exposed, so that linear yardage gives an indication of crowding rather than a true picture of seaweed availability . The majority of intertidal seaweeds are wracks of various species eaten only sparsely by the sheep . An additional source of food is the 136 hectares of poor quality, unmanaged permanent pasture outside the dyke . With current sheep numbers, this gives a density of more than 30 sheep per hectare, greatly in excess of the carrying capacity of the best lowland pasture . The vegetation on these sites was virtually eaten to soil level each time the island was visited . Assuming that the current sheep population is stable and since few if any are taken by the islanders, deaths-other than neonatal mortalities-must approximate lamb production . Estimates, based on the rather limited data available, suggest an annual mortality rate in juveniles and adults of about 25% . Bodily condition of the sheep was poorest in the spring, improving through summer and autumn . A number of factors probably combine to produce the poor state of health around lambing time including stresses associated with severe winter weather, fetal growth and the demands of lactation, coupled with relatively little grass growth early in the year at these latitudes and the poor nutritive quality of Laminaria digitata fronds cast in the spring . The sparsity of previous reports of disease in the native sheep of North Ronaldsay has already been noted . The claim by Tribe & Tribe (1950) that the sheep `are very healthy and suffer from few diseases' is totally at variance with our experience . This, and the observation of `exceptionally few worms', indicate that important changes have occurred (probably associated with the increase in sheep numbers and a reduction in management of the flock) since the time of their investigation . However, we agree with most of their comments about specific conditions . The majority of the sheep died as young adults or in old age . The young died mainly of parasitism or starvation . Dental diseases and starvation associated with these problems were the main causes of death in the older animals, suggesting that tartar deposition was progressive and that periodontal disease was linked with ageing alveolar structure . We believe that dental tartar and periodontal disease resulted in pain on mastication leading to poor maceration of food and thus reduction in its digestibility (Baker & Britt, 1984) . Drowning was a rather unexpected cause of death and occurred in emaciated and fit sheep . Emaciated animals were probably too slow or feeble to escape the advancing tide if they ventured over-far from the shore to graze at low water or if they had fallen through rafts of Laminaria and other seaweeds which sometime formed . Because most of the sheep were unshorn, the weight of water in the fleece following accidental immersion could seriously impede efforts to escape even by the fit animals .
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The high incidence of renal mineralization requires more detailed investigation . It may be due to highly efficient absorption of the metals found in our analyses, as demonstrated in this breed for copper (Wiener, Field & Smith, 1977), and/or unusually high dietary intake . In many of the sheep the skin on the anterior aspect of the carpal joints was bald, apparently due to abrasion caused by kneeling to feed ; many of the sheep spent long periods attempting to graze the sparse pasture and appeared to have adopted a kneeling posture to facilitate cropping of the consistently low growth . The worn incisors seen in eight sheep are believed to have resulted from eating the cortex of the tough Laminaria stapes. Many faecal samples contained comminuted mussel shells (Mytilus edulis) and one sample consisted almost entirely of this material . It is not known if ingestion of this material was accidental or deliberate . If the mussels were `grazed', this could result in tooth wear, and contribute to renal mineralization . The intestinal coccidia found comprised a mixture of species similar to those infecting sheep elsewhere . Total faecal oocyst counts were not high enough to suggest that the flock suffered serious effects from these organisms . The helminths recovered from the alimentary tract compare closely with the records from Scottish sheep given by Parnell et al. (1954) and earlier surveys cited in that work . Parnell and his colleagues found Ostertagia spp ., Trichostrongylus axes, Chabertia ovina, T. vitrinus, Nematodirus spp ., Capillaria spp . and Haemonchus contortus from nine North Ronaldsay sheep . The present study confirmed that proliferation of a wide range of parasitic helminths was successful on North Ronaldsay in spite of the constraints imposed by apparently unfavourable environmental conditions. Although there are significant differences in the pathogenicity of the various species of gastrointestinal nematodes recorded, heavy infestations with any combination can be responsible at least for loss of condition in the host and even death . The tapeworm, Moniezia expansa, is not considered a serious pathogen and this was confirmed in our studies . Larval cestodes, particularly migrating oncospheres of Taenia hydatigena, may have contributed to lack of thrift in infected lambs . Muellerius capillaris is found more frequently in Scottish sheep than other lungworms (Parnell et al., 1954) and is particularly common in adult sheep . Infection with Dictyocaulis filaria, the more important pathogen, is common in the native sheep of North Ronaldsay and appears to be an important cause of unthriftiness and an occasional cause of death in young adults . Fasciola hepatica is a major pathogen in sheep and the threat posed by the endemicity of this parasite on North Ronaldsay will continue in the absence of specific treatment of the sheep and as long as the habitats of the snail intermediate host persist . Infection with Sarcocystis tenella is a common condition in sheep throughout Britain . Ashford (1977) and Leguia & Herbert (1979) found almost 100% prevalence. Reported observations on the macrocysts of Sarcocystis gigantea in Britain are much less frequent (Ashford & Britt, 1983 ; Britt & Baker, 1983) . The prevalence of S. tenella amongst the North Ronaldsay sheep is probably similar to that in sheep elsewhere in Britain ; the prevalence of S. gigantea appears to be much higher . The role of both Sarcocystis species in natural disease in sheep remains to be established but lambs experimentally infected with S. tenella sporocysts develop a variety of clinical signs (Munday & Obendorf, 1984 ; O'Toole et al., 1986) . We have not been able to establish the importance of sarcocystosis in the North Ronaldsay flock but it would be unwise to assume that these parasites make no contribution to morbidity or mortality.
MORTALITY IN ADULT SHEEP IN ORKNEY
1 41
Neither the sheep ked, Melophagus ovinus, nor the biting louse, Damalinia ovis, is of major pathological significance, although heavy infestations with keds may give rise to anaemia (Soulsby, 1982) . Many of the live sheep were seen to be troubled by skin irritation, presumably caused by these parasites which were so frequent on the carcases . Rubbing to relieve this irritation caused fleece loss and a reduced resistance to cold which could be a significant threat to the well-being of sheep living in exposed conditions . Analysis of Laminaria species suggests that in October it provides an adequate diet as far as gross nutrients are concerned if available in sufficient quantity . L . digitata probably provides the bulk of the marine food in May, when the fronds are cast prior to the growth of new ones (Thomson, 1983) . The water content of the old fronds was found to be high . This bulky, wet material may well provide insufficient calories at the time of greatest demand . The poor nutritive value of seaweed in spring was noted by Hall (1975) although he suggested that the predominant species cast ashore was L . hyperborea, a species only washed up in small amounts during our study . The flock of North Ronaldsay sheep on North Ronaldsay comprises the largest group of animals of this rare breed and requires care in conservation . The flock exists in an almost feral state under conditions to which the animals have become less well adapted than earlier observers may well have implied . The present numbers of sheep and the reduced level of human intervention may have brought to light difficulties in adaptation to the environment which were previously not apparent. The present health status of the flock reveals a complexity of problems associated with dietary and other factors stemming from the unusual circumstances of their existence . Many of the diseases we have recorded in the sheep are preventable by the application of standard flock management procedures . All the problems could be relieved by reducing the size of the flock . Without such reduction, and in the absence of a larger work force and/or better facilities for handling the animals, it seems unlikely that the health of the flock will improve .
ACKNOWLEDGEMENTS The Animal Health Trust, Newmarket and the Universities Federation for Animal Welfare, Potters Bar provided financial support . We are also grateful to the following for help in the field and/or laboratory aspects of these investigations : Rosa and Carl Baker, Adam Britt, Dr T . L. J . Laurence, Ms S . Crozier, Mrs B . Harling, and Mr M . Savage . Ms Paula Jenkins prepared the photographs .
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ANNOUNCEMENT
VIIIth International Congress of Virology To be held in Berlin 26-31 August 1990 . It will be preceded by an IUMS Symposium on new developments in diagnosis and control of infectious diseases from 24-26 August . Details of registration from : DER-CONGRESS Congress Organization Augsburger Strasse 27 D-1000 Berlin 30 Tel : 030-24 60 11 Details of scientific programme from : Institute for Clinical and Experimental Virology Free University of Berlin Hindenburgdamm 27 D-1000 Berlin 45 Tel : 030-798 36 95
