Wild Animals in New Zealand as Hosts of Echinococcus granulosus and Other Taeniid Tapeworms
G.K. Sweatman
R.J. Williams
By
and
Hydatid Research Unit, New Zealand Medical Research Council, Medical School, University of Otago
[Received by the Editor, June 21, 1962.]
Abstract
Laboratory and field observations have been made on the real and potential role of the 32 exotic mammals established in a feral state in New Zealand in the maintenance and distribution of Echinococcus granulosus. Taenia hydatigena, T. ovis and Multiceps multiceps. The domestic dog is the only significant carnivore in the maintenance of these tapeworms. T. hydatigena infected laboratory cats, but the worms did not fully develop. T. ovis reached a gravid state in immature cats in the laboratory, but 347 cats from the field were not found infected. A diet with considerable horse meat appeared to be be, ficial to the survival of T. ovis in cats. Mustelids were not infected experi ~ntally with either E. granulosus or T. hydatigena.
Hydatid infections were produced in the possum (lungs and body wall), wallaby (muscle), mouse (liver and lungs), rabbit (lungs and renal iat), and red deer (liver and lungs). One of two fallow deer becam infected with only a single hydatid cyst which aborted early in development. The hedgehog. Polynesian rat, black rat and Norway rat were inherently Natural infections of E. granulosus were seen only in feral goats and fer? 1 s ’ine, while T. hydatigena infections occurred in feral goats, feral swine, red deer, fallow deer, wapiti and thar.
Rabbiters’ dogs are sometimes infected with E. granulosus and T. hydatigena but the incidence of infection dropped from the first to the fifth dosing round of the current hydatid eradication campaign. Pig dogs have a particularly high incidence of E. granulosus and T. hydatigena compared with infections in farm dogs and may be related to the eating of infected sheep carrion rather than wild pigs.
Introduction
No quadrupedal mammals occurred among the indigenous animals of New Zealand. The Maori people introduced a Polynesian rat, the kiore, and an unaggressive Polynesian dog. The latter disappeared about the time settlement began by Europeans. The explorers Cook, de Surville and Fumeaux introduced sheep,
goats and swine in the latter half of the eighteenth century (Thomson, 1922), and during the following century numerous alien mammals were introduced from Europe, Asia, North America and Australia (Wodzicki, 1950; Riney, 1955). No fewer than 32 exotic species are truly feral today.
Some of these are hosts of taeniid tapeworms overseas, but conditions are so very different in New Zealand that, for purposes of the current eradication campaign against Echinococcus granulosus and Taenia hydatigena, it was imperative to ascertain unequivocally the real and potential role of all introduced mammals as hosts in their new environment. Particular attention has been given to E. granulosus because this tapeworm is thought to lack host specificity and on account of its public health significance, and to a lesser extent to T. hydatigena, T. ovis, and Multiceps multiceps because of their importance in New Zealand agriculture. There is little doubt that all four tapeworms are for the most part farm problems in New Zealand, but in Foster’s (1958) review of human hydatid patients admitted for the first time to public hospitals from 1946 to 1956 it was shown that “ forestry and allied workers ” constituted the occupational group with the highest annual infection rate. The possibility of sylvatic infections contributing to this fact indicated another reason for an assessment of the role of wild mammals.
Some of the alien mammals have catholic feeding habits, and sometimes rival sheep and other livestock for food. Red deer, feral goats, feral swine, rabbits, hares, house mice, possums and hedgehogs are in .this category, and these have produced phenomenal populations under New Zealand conditions that could conceivably aggravate their role as hosts of parasites. Nowadays, rabbits and hares are kept satisfactorily under control in most of the agricultural regions of New Zealand by groups of men employed as professional rabbiters. Teams of full-time deer-cullers, assisted by sportsmen, work in forested areas, but they, by contrast with the rabbiters, are few in number and accomplish little more than temporary amelioration.
The role of each mammal in the maintenance and transmission of taeniid tapeworms has been assessed according to (a) its susceptibility under laboratory and field conditions, (b) its longevity under field conditions in relation to the time required by the parasite to reach an infective stage, (c) its geographic location, (d) its proximity to agricultural practices, (e) in the case of intermediate hosts, the opportunity to ingest taeniid tapeworm ova in relation to their feeding habits, which may vary seasonally and according to population density, and (f) in the case of a definitive host, its access to intermediate hosts, both wild and domestic. The role of each mammal, or group of mammals, is summarised under its own subheading.
Materials and Methods
Wild animals used in the laboratory were collected from the field. Possums and wallabies were removed from their mothers’ pouch as “ joeys ” and raised on whole cow’s milk and baby’s food (Glaxo’s Farex) to which commercial milk-nuts, sheep-nuts, fruits and vegetables were added later. Red deer and fallow deer were collected from the forest before they were old enough to follow their mothers, which would probably be during the first two weeks of life. These were raised on a bottle using whole cow’s milk diluted 4 to 1 with water to which glucose was added at the rate of a dessertspoonful to a pint. Milk was continued until they were six months old. Solid foods were introduced gradually. These consisted of commercial sheep feed, including linseed cake, root-crops, grass and willow (Salix spp.) branches. Mustelids were collected in the field and were of unknown age.
Eggs of the various tapeworms teased from gravid worms and washed free of debris in tap-water usually with a microsieve were stored in a refrigerator for no longer than three weeks before use. Egg counts were estimated from replicate aliquot samples and are precise only to two significant figures. For administration to ungulates, the eggs were placed on moistened feed in a 000 gelatin capsule which in turn was placed in a larger capsule (size No. 11) with dry feed. This was given with a balling gun. Small animals were fed by stomach tube sometimes under ether anaesthetic.
RESULTS
I. Wild Definitive Hosts
In New Zealand there is one canid, one felid and three mustelids. Feral and semi-wild cats ( Felis catus ) have a more or less continuous distribution throughout most of the islands of New Zealand. Many feral cats appear to live on runhold country feeding mainly on rabbits, hares and mice, and others are found in forested areas where they predate birds, mice and rats. Feral cats are scavengers of sheep which have died, particularly in the high country, and many farm cats in New Zealand are fed on sheep either when it is butchered or subsequently. It seems possible therefore that from time to time cats ingest tapeworm cysts from sheep.
It has been shown repeatedly that adult worms of E. granulosus either fail to develop completely in cats or develop only partially and never produce eggs (Southwell, 1929; Ldrincz, 1933; Witenberg, 1933; Gemmell, 1959; Hutchison and Bryan, 1960). Stiles and Hassall (1912) in their Index-Catalogue noted T. hydatigena from the domestic cat, but Hall (1919) was unable to locate the reference in question and regarded the case as not proven. A more recent article by Wardle (1933) noted an unpublished report by Riddle of 4 of 70 vagrant cats in Winnipeg infected with T. hydatigena. The current New Zealand situation made it imperative to assess the validity of these reports and to determine the role of the cat in the maintenance of T. hydatigena.
Table I shows the results of the feeding of cysticerci of T. hydatigena to 8 immature cats, sometimes on three successive occasions, and their examination at autopsy 5 to 97 days later. The cats were fed on horse meat, bread, milk and mutton. Five of the 8 cats were found infected, and all worms occurred in the anterior quarter of the small intestine. In four cases, even after 28 days, the worms were only 4mm long and there was no indication of segmentation (Fig. 1). The worms were alive and firmly embedded in the gut mucosa. The remaining infected cat (No. 5) was autopsied at 14 days, a shorter period than some of the above infections, and it harboured 4 worms, the longest of which was 13mm and contained 31 proglottids proximal to a short unsegmented neck. No differentiation within the proglottids was apparent (Fig. 1). It seems clear that T. hydatigena , like E. granulosus, can infect some cats, but the worms fail to mature.
A further 4 immature cats were fed scoleces of M. multiceps from a cerebral coenurus removed from a hogget. None was infected at autopsy between 7 and 155 days later (Table I). Dogs, which served as controls, were infected successfully.
Because of the prevalence of T. ovis in New Zealand (Sweatman, 1962) and since both feral and farm cats probably eat more sheep carcass-meat than entrails, it has been significant to determine the role of cats in the transmission of this tapeworm. Pullar (1946) failed to infect a kitten with T. ovis , and another
species of tapeworm which forms muscle cysticerci, T. krabhei, has been fed to cats by Shaw, Simms and Muth (1934) and Olsen and Williams (1959) with negative results. Rollings (1945), however, reported T. krabhei in a bobcat (Lynx rufus ) in Minnesota. In an initial trial we successfully infected 3 of 4 immature cats with T. ovis which had been fed a total of 26 cysticerci (Table I). Ten worms were recovered at autopsy 4 to 62 days later, 3 of which had become gravid. Eggs from these worms infected lambs. The cats were maintained on a diet of horse meat, bread, milk and some occasional mutton. Since the diet of the host may have been significant in the survival of T. ovis, an additional 8 immature cats from 2 litters were randomized into 2 equal groups and placed on diets which differed only in their source of meat. One group received horse meat, bread and milk, while the other received mutton instead of horse meat. Six weeks after this regime was commenced, each cat was fed 6 cysticerci of T. ovis. The cats fed on horse meat began to excrete ova at 48 days, while no ova were excreted by the cats on mutton within their pre-autopsy period of 62 days. At autopsy (Table I) 3 of the 4 cats on horse meat were infected with a total of
11 gravid worms, and one of the 4 cats on mutton contained 2 worms which had reached a gravid state but had not shed any proglottids even after as long as 62 days. These results demonstrate that horse meat is highly beneficial, but not imperative, for the development of T. ovis in cats.
A total of 347 feral and farm cats were examined from throughout the two main islands of New Zealand. Many came from properties where T. ovis occurred in sheep and dogs. None of the cats was infected with T. ovis. In spite of the laboratory observations, the above findings, together with the fact that cats habitually bury their faeces, indicate that under field conditions cats are probably of no significance in the transmission of T. ovis. Gats in abattoirs and freezing works would be better situated than farm cats to ingest large numbers of T. ovis cysts, but would be less likely to spread the infection to sheep on pasture except in the case of sheep transferred in a salesyard transaction to a new owner and property.
Of the three mustelids in New Zealand, the European stoat ( Mustela erminea) and ferret ( Putorius putorius) occur not uncommonly, while the European weasel {M. nivalis ) appears to be rare. The stoat and weasel are probably widely distributed in both the North and South Islands of New Zealand, but there are several broad areas which apparently have no populations of ferrets (Marshall, 1961). Marshall states that these show a reasonably close relationship with areas having a mean annual rainfall of less .than 60 inches. This may be related to the greater dependence of ferrets on rabbits as a food item which are more closely allied to dry country stocked with wool and store sheep. In Marshall’s report observers commonly noted that, following effective rabbit control operations (see rabbit dogs), the stoat and ferret were more often seen feeding at carrion. This consisted predominantly of sheep, but deer, goats, possums, rabbits, hares and other types of carrion were observed also. It is possible, therefore, that mustelids periodically ingest cystic tapeworms.
Six ferrets and 3 stoats coincident with South Island pastureland were not infected with tapeworms, nor was it possible in the laboratory to infect two stoats or a ferret with either E. granulosus or T. hydatigena following the ingestion by each of a large number of hydatid brood capsules and scoleces and twelve cysticerci of T. hydatigena. Autopsies were carried out five days after exposure. Dogs, which served as controls, were infected successfully. It is assumed that similar findings for T. ovis and M. multiceps in the ferret and stoat would result, and also occur for the weasel. Mustelids in New Zealand would appear therefore to be of no consequence in the transmission of taeniid tapeworms.
It is a strange phenomenon that a country like New Zealand with such a variety of successful herbivorous mammals which support mustelids and feral cats should be almost completely free of feral dogs ( Canis domesticus). Wild dogs, as distinct from stray and the occasional “ killer ” dog, appear to occur only in the Kaingaroa State Forest of the North Island, where they apparently live on deer, pigs, rabbits, hares and the occasional wild horse carcass. It has been reported to us that in 1948 wild dogs in the forest were numerous and frequently seen. Packs varied in size, the largest seen consisting of 14 dogs. Their numbers have gradually decreased, apparently as a result of land development adjoining the forest. There are at least 4 reliable sight-records of red deer in the forest being attacked by wild dog packs.
One red deer from the Kaingaroa State Forest was infected with T. hydatigena, but it would be presumptuous to assume that a deer-dog cycle is being perpetuated without carry-over from a livestock cycle. Two dogs from the forest
were examined in 1960 and one was infected with three T. pisiformis, confirming rabbits or hares as a food item, but not pigs and deer.
The field and experimental observations on wild and feral carnivores in New Zealand demonstrate that none is significant in the transmission of E. granulosus, T. hydatigena, T. ovis or M. multiceps. All infections must depend primarily, if not exclusively, on the domestic dog. The significance of wild and semi-wild herbivores in the spread of these parasites to the domestic dog could therefore become important towards the end of the eradication campaign after the feeding of raw offal from sheep has stopped.
11. Wild Intermediate Hosts
Possum
The Australian brush-tailed possum ( Trichosurus vulpecula) occurs in large numbers and has a übiquitous distribution throughout most islands of New Zealand. The possum feeds mainly in the arboreal canopy of subclimax brush associations. Those which live primarily in overgrown gullies which interdigitate with pastureland have been seen feeding at night on nearby pastures and appear to be fond of some grass crops such as timothy ( Phleum pratense) . Some scrub habitats have become overcrowded, and the possums have spread onto grassland and in some cases have established themselves more or less permanently on runhold tussock country of the South Island. These are closely associated with sheep and dogs and may ingest taeniid tapeworm ova. Now that rabbits have been markedly reduced in most agricultural regions of New Zealand, many rabbiters collect possums to feed to their dog packs. Also, dogs kept in forestry camps and occasionally by the professional deer-culler are frequently fed on possums in addition to deer, pigs and goats. Therefore, the possibility of a sheep-dog-possum-dog-man cycle of E. granulosus required elucidation.
Twelve immature possums, collected from the field, were randomized into pairs, and by stomach tube were fed a single dose of 100, 300, 500, 1,000, 5,000 or 10,000 mature ova of E. granulosus. Four additional possums received 6 repeat doses of 100 E. granulosus ova on alternate days, while two others received 10 E. granulosus ova on six different occasions. All were autopsied four to twelve months later. Two possums were infected (Table II). One possum which had received 1,000 ova was found at months with two sterile cysts. One cyst was pulmonary and 13mm in diameter (Fig. 3), while the other had a diameter of 17mm and was attached to the abdominal wall at the junction of the diaphragm (Fig. 4). The cysts had thick laminated cuticles (Fig. 5) outside of which was a fibrous host reaction with limited surrounding degeneration. In some parts, the zone of fibrosis was distended with an inflammatory exudate predominately of lymphocytes and eosinophils, both in varying stages of degeneration. The cyst was obviously viable and healthy. The second possum had received 10,000 ova and was examined at 11 months. Seven thoracic cysts were present; six in the lungs (Fig. 2) and the other in the mediastinal septum. The last was 17mm and sterile, while the pulmonary cysts had diameters of 6, 7, 12, 13, 16 and 36mm. The 16 and 36mm cysts were the only ones which were fertile, and these contained moderate numbers of brood capsules with scoleces. The rostellar hooks (Fig. 10) on the scoleces were only slightly shorter (see murids) than those from normal hosts (Sweatman and Williams, 1962) and can be compared with hooks from a sheep cyst in Fig. 9. It seems likely that there would have been no difficulty in infecting dogs with the possum material.
Eight possums were fed a single dose of 5,000 ova of M. multiceps and each of 4 received 1,000 T. ovis ova. Control lambs were infected, but none of the possums contained cysts at autopsy 2 to 6 months later.
A total of 216 possums, mainly adults, were examined for natural infections from various localities of the South Island. None was infected, although most would have had access to sheep pastureland. This was suggested from the examination of the small intestines of 17 possums, eight of which were infected with immature Trichostrongylus colubriformis with up to 17 worms in one possum. This is a common nematode of sheep in New Zealand, and has been listed from this same species of possum in Australia (Mackerras, 1958). It seems likely, therefore, that although possums have access to taeniid tapeworm ova originating from dog faeces on pasture, the number of eggs available is insufficient to overcome the natural resistance of this host. It is apparent that wild possums in New Zealand are unlikely reservoirs of E. granulosus and other taeniid tapeworms.
Wallabies
Three species of Australian wallabies occur as three distinct local populations in New Zealand. The rock wallaby, Petrogale ?penicillatia, occurs in large numbers on the cliffs of Kawau, Rangitoto and Motutapu Islands in the Hauraki Gulf of the North Island. Near Rotorua on the mainland of the North Island, the dama pademelon, Protemnodon {= Thylogale) euginii, has increased in numbers in the last few years and is extending its range eastward. In the South Island, the red-necked wallaby, P. rufogrisea, now inhabits a large area primarily near Waimate, but it exists discontinuously in scrub country and overgrown gullies from the Waitaki River in the south and west to the Rangitata River 70 miles north. A small mob, not recorded by Wodzicki in 1950, now occurs on the western slopes of Mount Maude on Mount Burke Station at the south-western comer of Lake Hawea. These localities are mapped on Figs. 20 and 21. All three species live primarily in scrub country and contiguous pastureland.
In the laboratory, 4 immature red-necked wallabies were fed ova of E. granulosus. Two received a single dose of 10,000 mature ova, and each of the other two received 6 repeat doses of 100 ova on alternate days. Only one wallaby became infected (Table II). This animal received 10,000 ova, and when examined 17£ months after exposure had 2 cysts, one fertile and one sterile. The sterile cyst was 7mm in diameter and was lodged between the muscle and tibia on the left hind leg. The fertile cyst had reached a size of only 10 x Bmm and was attached to the external surface of the gracilis muscle of the left hind leg. Scoleces were not numerous, and some of the rostellar hooks on those present were markedly shorter (Fig. 12) than those from sheep (Fig. 9). Some of the wallaby scoleces, therefore, would not necessarily have been infective to dogs.
The collection of faeces excreted daily for 7 days following exposure with the eggs was made in the case of the two wallabies which received the single large doses of ova. The faeces was boiled, washed and examined for eggs of E. granulosus that might have been excreted unchanged using the salt floatation technique. Coccidia and nematode ova occurred, validating the technique, but no tapeworm eggs were seen. Since there were only two cysts at autopsy, does this not suggest that most of the eggs of E. granulosus hatched in the gut of the wallaby but failed to become established as cysts?
Two of these red-necked wallabies were also fed 10,000 M. multiceps and 1,000 T. ovis ova by stomach tube 4 months following their exposure to E. granulosus. One had received the low repeat doses of E. granulosus ova and the other wallaby had had the single large exposure. Control lambs became infected with M. multiceps and T. ovis but not the wallabies as seen at autopsy 5 and 10 months later.
A total of 93 red-necked wallabies from the mob contiguous with or overlapping sheep pastureland near Waimate were not infected with the three tapeworms above or with T. hydatigena. Six rock wallabies from Motutapu Island were uninfected also. These animals, however, were examined before the experimental observation was made of muscular hydatid cysts, and although the entrails of the wallabies were examined, only a few were skinned out and examined subcutaneously. Infections may therefore have been missed. Durie and Riek (1952) reported the lowest incidence (2 of 26) of hydatid cysts in the red-necked wallaby among the 6 macropodids which they examined in north-eastern Australia where the cycle is completed in the dingo (Canis dingo). They reported only pulmonary infections and presumably did not examine muscle tissue, so the incidence may have been higher than their figures suggest. As in New Zealand, the rock wallaby and dama pademelon have not been seen infected in Australia,
The combined laboratory and field observations suggest that wallabies under New Zealand conditions may be of limited practical significance in the maintenance of E. granulosus but not the other taeniid tapeworms. Since wallabies have increased in numbers and distribution, are eaten by dogs, and are hosts of E. granulosus in the laboratory and in the field in Australia,* they must always be considered in the regions where they occur as a possible reason for a local breakdown in control.
Murids
One species of mouse and three species of rats have been introduced into New Zealand. The two European rats, the Norway rat ( Rattus norvegicus) and the black rat ( Rattus rattus) are found in both country and city. It is generally accepted that both are refractive to infection with E. granulosus, and this has been confirmed by us for the type of E. granulosus in New Zealand. Eight Norway white rats (Wistar strain) and four black rats were fed ova of this tapeworm and were not infected as shown at autopsy 4 to 11 months later.
A third species of rat, the kiore ( Rattus exulans) was introduced into New Zealand from Oceania by the Maori people in pre-European times. This rat reached plague proportions in some districts of the South Island on at least six occasions in the latter half of the last century (Watson, 1956). Subsequently its numbers dropped to such an extent that it was considered extinct by Thomson in 1922. In 1956, however, Watson (1956) reported kiore living on nine off-shore islands, and at two localities in Fiordland National Park in the South Island. The kiore is frugivorous, feeding extensively in winter on beech mast and berries, and is found principally in forest and scrub of high-lying country on the summits of ranges and spurs away from agricultural regions. In low numbers the kiore
is of no concern, but because of its potential as a plague pest, four were collected and fed ova of E. granulosus. None was infected. The kiore, like the Norway and black rats, appears therefore to be unsuitable for the development of hydatid cysts.
Many mice (Mus muscuius) live permanently outdoors in New Zealand in tussock and other grassland country. No natural infections of E. granulosus have been found in mice in overseas countries or by us in 29 mice collected on runhold country of the South Island. Experimentally, however, the laboratory white mouse, which is the same species, has been reported as occasionally infected. Deve (1949) observed primary hydatid cysts in the lungs and pleura of experimental mice. In New Zealand, Batham (1957) stated that “. . . usually only about a quarter of mice developed cysts . . that were fed 10 gravid proglottids per mouse. Yamashita, Ohbayashi and Konno (1956) infected mice using eggs of worms from dogs fed cysts from Australian sheep. A few hydatid cysts were seen by them in 2 of 20 white mice autopsied four months following exposure. All cysts seen by the above workers were apparently sterile. We successfully infected 5 of 20 white mice, each of which had been fed 10,000 eggs of E. granulosus by stomach tube (Table II). Only 1 or 2 cysts occurred in each infected animal. Almost all were hepatic cysts (Fig. 6), but one infected a lung and another was loose in the abdominal cavity. Only in the mouse with the longest period of infection (13 months) had scoleces developed. The scoleces occurred in groups attached directly to the germinal membrane without first occurring in brood capsules. The rostellar hooks on scoleces from both cysts were underdeveloped and smaller than those from sheep (Fig. 13). Scoleces from both cysts were fed to a pup which was uninfected at autopsy 3 months later. This suggests that scoleces with underdeveloped hooks are not infective. Even fully infective cysts in mice after this period of time would probably be insignificant under field conditions since the longevity of mice is only up to 1£ years (Rensch, 1959) and few sheep dogs eat mice. These data suggest that the house mouse, like the different rats, is of no practical significance in the maintenance of E. granulosus.
Leporids
Fig. 22 shows that European rabbits ( Oryctolagus cuniculus) and European hares ( Lepus europaeus) have a fairly übiquitous distribution on the two main islands of New Zealand. The rabbit and hare distributions are based on those of Wodzicki (1950). Under New Zealand conditions, rabbits are capable of reaching phenomenal population densities but for the most part only on dry grassland, which agriculturally, is primarily run-country used in the production of wool and store sheep.
Infections of E. granulosus have been seen in experimental rabbits, but there appears to be no authentic report of infected rabbits or hares in the field. In the laboratory, Deve (1949) gave massive doses of E. granulosus eggs to 14 rabbits and infected six. Infections were not produced, however, in rabbits by Clunies Ross (1929). We have confirmed Deve’s observations by successfully infecting 6 of 11 white laboratory rabbits which are the same species as the wild rabbit in New Zealand. These rabbits were two months old at the time of exposure and received by stomach tube either a very large number of ova or 5,000 ova (Table II). Only the former were infected. Three of the infected rabbits died 10 and 13 months after exposure, probably as a result of the heavy pulmonary infections. The other three infected rabbits were autopsied after about the same period of infection without having shown any symptoms. Almost all cysts occurred in the lungs, and Fig. 7 shows a heavy pulmonary infection while Fig. 8
shows 2 cysts in renal fat. Table II shows that scoleces occurred in 13 hydatid cysts and all were in the animals with 10 to 14 month infections, while some other cysts of the same age were sterile. The rostellar hooks in the scoleces of the rabbit cysts (Fig. 11) were of comparable size and development to those of sheep cysts (Fig. 9) and in contradistinction to the mouse infection noted previously, those from the rabbit proved infective to a dog.
In spite of these laboratory infections in rabbits, a thorough examination of 100 wild rabbits and a less thorough examination of 6,000 wild rabbits in the North Island by Bull (1953) were all uninfected with this parasite. Neither did we find any hydatid cysts in 107 rabbits nor in 35 hares from different parts of the South Island. These findings are corroborated by Sweet’s {in Clunies Ross, 1929) observation of 1,200 European rabbits In Australia found negative for E. granulosus.
It seems possible that the contrast between the field and laboratory observations is related to the number of eggs ingested. In the laboratory rabbits, very large numbers of ova administered at one time produced an infection. These two conditions would not likely be met in the field. By contrast, one of 3 sheep became infected after ingesting as few as 10 ova (Sweatman, Williams, Moriarty and Henshall, 1962). Assuming the feeding behaviour of sheep and rabbits to be similar, it can be concluded that the threshold of infection is higher for rabbits than for sheep.
Hedgehog
The European hedgehog ( Erinaceus europaeus ) is the only insectivore to have been liberated in New Zealand. It has a wide distribution throughout the country and is abundant in sand dunes, gardens, orchards and pastures, in the city as well as on the farm (Brockie, 1958). Some dogs are regular predators of the hedgehog and do not generally find their dorsal spines a deterrent to kill. A large number of hedgehogs are killed on the highways, and these attract stray and working dogs.
A total of 119 hedgehogs from farming regions were not infected. In the laboratory it was not possible to infect 37 hedgehogs with mature eggs of E. granulosus administered in single large doses (10,000) or in repeat small doses (10 to 100) given on alternate days for two weeks. Autopsies were made from 4 to 11 months following exposure. Nor was it possible to infect 4 hedgehogs with either T. ovis or M. multiceps. In each case, lambs used as controls became infected. It seems clear that the hedgehog is inherently resistant to taeniid tapeworms.
Cervids
No fewer than 9 species of deer have been successfully introduced into New Zealand. Their present geographic distribution, chances of spread, social habits, feeding habits and part played in the diet of domestic and wild dogs are related to their real and potential role in the maintenance and spread of taeniid tapeworms. Figs. 20 and 21 show the present distribution of the different deer in (a) those parts of New Zealand covered by mountain, forest and shrub and only sparsely inhabited by man; (b) areas with low human habitation associated primarily with runhold country on natural (South Island) and culture (North Island) steppe land producing wool and store sheep; and (c) areas of intensive sheep (fat lamb) and dairy farming with a high human population. The distribution of the deer species in Figs. 20 and 21 is basically that noted by Wod-
zicki (1950; 1961), but has been brought up to date from current information provided by the New Zealand Forest Service.
Two of the deer species are indigenous to Europe. One of these, the red deer ( Cervus elaphus) , is the only cervid which has at the present time a fairly übiquitous distribution in the three major islands of New Zealand that corresponds closely to the distribution of forest, shrub and runhold country shown as (a) and (b) in Figs. 20 and 21 with the exception of the south-east comer of the South Island and the peninsula of North Auckland Land District where red deer do not occur. The red deer is essentially a forest dweller (Fig. 16) in New Zealand, but some have been observed some miles from a forest on steppe high country not unlike those Scottish red deer that inhabit only the open highlands (Matthews, 1952) or the North African race, C. elaphus barharus, which occupies open treeless country in Tunisia and Algeria (Murie, 1951). Tussock and
other native grasses cover 34% of the South Island of New Zealand (Hilgendorf, 1935), while the country as a whole is 23% forested (15,396,000 acres). About 80% of the forest is commercially inaccessible. Almost all of this is indigenous beech-podocarp-hardwood forest and Crown Lands where large herds of red deer occur. Of the merchantable 20% of the forest, 14% is indigenous forest and 6% exotic forest, mainly Pinus radiata. Red deer also abound in these regions, but being more accessible, are hunted more rigorously by both the full-time deer-culler and sportsman.
The number and distribution of red deer in New Zealand are generally on the increase, particularly in Fiordland National Park. Red deer along river flats and on tussock country frequently graze land used by dogs and sheep. Also it is not uncommon, particularly in winter, for red deer to feed on swedes ( Brassica rapa ) and other root-crops, to be shot at night, and for the offal to be left in places readily accessible to stray and working dogs.
European fallow deer ( Dama dama ) occur in a series of widely separated localities (Figs. 20 and 21) usually in forest or scrub areas overlapping or contiguous with agricultural regions. Within the last decade, the fallow deer near Fairlie, in the South Island, have extended their range to include the Upper Pareora River valley and South Opuha River valley. Another herd in the Greenstone River valley off Lake Wakatipu has spread about 35 miles south-west towards Lake Mavora and the lower Upukeroa River valley. In the North Island the fallow deer in Wellington Province have enlarged their local area of occupation in the last decade. The report of fallow deer by Wodzicki (1950) in the
Herbert State Forest, however, has not been substantiated from observations made during the past few years. Some fallow deer herds are attracted to alluvial river flats where they graze more than they browse (Fig. 17), especially in spring coincident with the lush growth of grass before many seedlings begin to develop in the forest. These high country catchments constitute part of a runholder’s property where sheep are grazed and mustered by dogs five or six times a year. The deer are shot regularly and fed to the dogs.
From Asia, the sika or Japanese deer ( Cervus nippon), the sambar deer (Cervus unicolor) and the Javan rusa deer {Cervus timoriensis) were introduced into different regions of the North Island of New Zealand, while a fourth Asiatic species, the chital or axis deer {Axis axis), was introduced into the indigenous rain forest among the fiords of the South Island. Although recent authentic reports of axis deer do not exist, it may be that a few still survive in semi-bush habitats in one region of Fiordland National Park (Fig. 21) where this species can graze as much as browse, meeting some of the requirements of the savannah where it lives in Asia.
The sika deer is a forest dweller and the one herd in the North Island is gradually increasing its range in the indigenous and exotic forests. Sambar deer, which have been introduced onto St. Vincent’s Island, Florida (Hosley, 1953), have survived by grazing more than browsing. In India, Brander (1923) indicated that sambar do browse, but their chief food is coarse grass growing along the banks of streams associated with thickly wooded hillsides in the vicinity of cultivation and that they avoid the deep forest. In New Zealand, in the four regions where they occur, sambar deer exist near swampy areas in the same general location as sheep, but cattle drive them away (Riney, 1957). Sambar appear to require a regular abundant supply of water which could inhibit their spread into the dry central region of the North Island. On runholds, sambar are fed to farm dogs. The single herd of Javan rusa deer in the North Island also occurs in a swampy, scrubby area bordering native forest.
From North America, the moose {Alces alces) and wapiti {Cervus canadensis) were introduced into districts of the rain-forest of the South Island, and the white-tailed deer {Odocoileus virginianus) was introduced onto Stewart Island and into an area of the South Island immediately north of Lake Wakatipu (Fig. 21). There is no agriculture and there are no dogs associated with these species. Moose are believed to be dying out in an unfavourable habitat concomitant with increased competition with red deer. The last moose known to have been shot occurred in 1958, and there was a sight-record of a live animal in 1959 along the Wet Jacket Arm of Fiordland.
Wapiti, which occur in a different region of Fiordland National Park, are promiscuous feeders and in the densely forested areas of New Zealand they apparently live mostly on arboreous food {in Poole, 1951). Because of competition and interbreeding with red deer, it may be just a matter of time before there is complete submergence of the wapiti as a distinct species.
The white-tailed deer on Stewart Island have spread throughout the dense forest of the island. Agriculture on Stewart Island is local and rudimentary and there is only one sheep flock, which is confined to a small district on the east coast. The white-tailed deer in the one locality of the South Island have shown in the last few years a marked increase and spread throughout the catchments at the north end of Lake Wakatipu, but are still fairly well removed from agricultural practices. The restricted movement of white-tailed deer in eastern
North America (Hosley in Taylor, 1956) is less apparent in New Zealand, but it would seem unlikely that the single herd on the South Island will spread far, particularly in competition with red deer.
Most deer herds in New Zealand have thrived to the point of over-popula-tion. It is under these conditions when browse foods become limited that most deer, particularly red deer and fallow deer, graze more extensively and frequent crop lands. Large deer herds which have outstripped their food supply are likely, therefore, to ingest more tapeworm eggs originating from dog faeces than a population in balance with its environment. It is also when deer are in excess that they are simply shot and left unbutchered and perhaps accessible to wandering dogs, and also when they are most likely to be used as a dog food on runholds. The habits of the different deer species, the success of their adaptation to New Zealand conditions, and their current and potential geographic distributions indicate that red deer, fallow deer and to a lesser extent sambar deer are the important deer species to evaluate in an eradication campaign directed against tapeworms primarily dependent on a livestock cycle.
Hydatid cysts have been reported in moose, white-tailed deer and wapiti in their North American habitat (Sweatman and Williams, 1962); in a fallow deer examined in the Philadelphia Zoological Gardens (Weidman, 1923); and in a red deer in Holland (Jansen, 1961); but no overseas reports have been found for any of the other cervids introduced into New Zealand.
Reports of T. hydatigena from overseas countries have been found for all the cervids introduced successfully into New Zealand except the sika deer (Houston, 1836; Hall, 1919; Meggitt, 1924; Hadwen, 1932; Joyeux and Baer, 1936; Machul’skii, 1950; Peterson, 1955; Severinghaus and Gheatum, 1956; Sweatman and Plummer, 1957; Sweatman, 1957; Campbell and Richardson, 1960).
In New Zealand, natural infections have been looked for in 57 red deer from various localities in the North and South Islands; 103 fallow deer from the Gaples River valley, Tapanui forest and Wellington herds; 4 sika deer from the Lake Taupo herd; 6 sambar deer from the herd in Wellington Province; 6 wapiti and 5 wapiti x red deer hybrids from Fiordland National Park. None was infected with E. granulosus or T. ovis, and the sika and sambar deer were also negative for T. hydatigena. One wapiti (possibly with some red deer intermixed) contained an omental cyst of T. hydatigena together with a kidney lesion which showed on histopathological examination a fairly recent focal nephritis and a most intense eosinophilic infiltration assumed to be indicative of a parasitic invasion, although no parasitic remnants were present in it. The wapiti was shot 25 miles from the nearest farm in an area accessible only by amphibian aircraft and where dogs have never been known to occur. A single cyst of T. hydatigena also occurred in the omentum, liver or heart of 6 red deer while another red deer contained 3 hepatic cysts in close juxtaposition. The animals were from widely separated areas of New Zealand (Figs. 20 and 21), but, unlike the wapiti, most were in regions accessible to agricultural practices. Two other red deer had a few liver “ white spots ”. Histologically these spots were granulomata with varying cellular preponderance. Lymphocytes, eosinophils and polymorph leucocytes were present in all of them. In one large spot with a considerable amount of central necrosis there was a small structure approximately 30ju. in diameter and containing several nuclei each approximately s ji in diameter (Fig. 15). This was probably an oncosphere of a taeniid tapeworm, possibly T. hydatigena or E. granulosus, in an early stage of differentiation.
Six of 67 (9%) and 4 of 6 fallow deer were infected with T. hydatigena from the Gaples River valley and Wellington herds respectively (Table IV). The Caples River valley is part of a runhold used by sheep and worked by dogs about 5 times a year and where fallow deer are fed regularly to the dogs. Most of these fallow deer were three years old or younger (Table III). Two brokenmouth ewes were examined in the valley, and both were infected with E. granulosus and T. hydatigena. The infections of T. hydatigena in both deer and sheep suggest that a bilateral cycle goes on between sheep, dogs and deer. Because the infections in the different species of deer were light, it would seem likely that exclusion of sheep as a dog food would result in the gradual dying out of the infections in the deer.
The absence of natural infections of E. granulosus in red and fallow deer was substantiated by observations in the laboratory. One of 2 fallow deer became infected with only a single hydatid cyst which was small and necrotic at autopsy 21£ months later (Table II). Only one hydatid cyst among 4 exposed red deer showed any indication of normal development (Table II). The other red deer either did not become infected or the cysts failed to develop. It was not possible to infect red and fallow deer with T. ovis (Sweatman and Henshall, 1962). We also fed 10,000 mature ova of M. multiceps to 2 fallow deer as well as 10,000 and 70,000 mature ova to 2 red deer. Control sheep became infected, but not the deer. It seems likely from both the field and laboratory observations that deer in New Zealand are involved occasionally in the maintenance of T. hydatigena but not the other tapeworms.
Chamois and Thar
In its native habitat, the chamois ( Rupicapra rupicapra ) has a discontinuous distribution from the mountains of Europe to Asia Minor, while the thar {Hemitragus jemlaicus ) is its counterpart south of the main range of Himalayan mountains. Both are gregarious, and in New Zealand the herds occur along the main mountain range of the South Island between 4,000 and 6,000 feet. Wodzicki (1950) outlined the 1947 distribution of chamois in the Southern Alps of the South Island as extending from Lake Rotoiti in the north to Lakes Wanaka and Hawea in the south. During the past few years, chamois have increased in numbers and have spread southward to within Fiordland National Park. In 1959, one was sighted on the Milford Track and others have been shot on the Thomson Mountains and Lower Livingstone Mountain range near Lake Te Anau about 100 miles south of the 1947 distribution of this animal. Wodzicki (1961) reported that the annual kill of chamois was over 4,000 animals.
Thar, like the chamois, live in the Southern Alps, but are distributed less widely. Large numbers of thar now occur as far north as the Rakaia River watershed and some occur as far south as Lakes Wanaka and Hawea. This is approximately 40 miles both north and south of the 1957 distribution shown by Wodzicki (1950).
In winter, chamois and thar sometimes come down well below 4,000 feet onto high country pastures competing not only with domestic livestock and each other, but also with red deer and feral goats. An extensive migration was made by a large number of thar into the foothills of Canterbury Province in the winter of 1959. In summer, some cattle and sheep are run on mountain pastures (Fig. 18) and are occasionally worked by dogs.
No overseas reports have been found of taeniid tapeworms in the thar. Simpson (1945), however, placed the thar in the same Tribe as sheep and goats, and Wolfe (1939) demonstrated that these three animals have very close serological affinities. It was not surprising therefore to find a single cyst of T. hydatigena attached to the abdominal body wall of a thar taken along the upper reaches of the Rangitata River on a high country pasture covered periodically by working dogs. The rostellar hooks on the cysticercus were of the length (128 [i and 200jx for the small and large hooks respectively) and morphology typical of this parasite in other hosts and would presumably have been infective to dogs.
Chamois are reported to be hosts of T. hydatigena and M. multiceps in Europe (Meggitt, 1924; Joyeux and Baer, 1936; Brumpt, 1949; Frauchiger and Fankhauser, 1957). Frauchiger and Fankhauser (1957) stated that in Germany M. multiceps seldom occurred in domestic animals and conjectured that the primary cycle was a sylvatic one between chamois, and perhaps deer, with the fox as the definitive host. However, these authors did not report any infections in either deer or foxes. As noted elsewhere (see cervids) neither red nor fallow deer, both European species, were infected experimentally with M. multiceps. Thornton (1949) has remarked that in Switzerland the chamois affected by M. multiceps leave the rocks on which they no longer feel secure. Animals with nervous symptoms would probably attract and be more susceptible to attacks from marauding dogs possibly facilitating the spread of M. multiceps. In the current study, one chamois near a mountain pasture used by cattle, and three other chamois from country covered by shepherds, dogs and sheep were examined but none was infected.
Wild and Semi-feral Goats
Goats (Capra hircus) are widely distributed throughout New Zealand, and in many regions have reached pest proportions and require periodic destruction. The annual kill of goats has reached as high as 70,000 animals (Wodzicki, 1961). Although goats browse wherever possible, they graze extensively, particularly at the margin of scrub country (Fig. 19). Feral goats are readily mustered, and on some farms are used as a source of dog food. More often than not, goats in the high country are shot and left unbutchered in areas accessible to wandering dogs.
Tapeworm cysts reported in goats in other parts of the world include E. granulosus, M. multiceps (Hall, 1919; Joyeux and Baer, 1936), M. gaigeri (Hall, 1916), T. hydatigena, T. ovis and T. saginata (Joyeux and Baer, 1936). M. gaigeri has been seen only in India and Ceylon (Rao et al., 1957). It is possible that the T. saginata record could be T. ovis, but since the former has no rostellar hooks it should not, if properly examined, be easily confused with T. ovis. T. saginata has not been seen in cattle or man in New Zealand except in recent immigrants.
Examination was made of 1,195 semi-feral goats from six properties, of which five were in the North Island and one in the South Island. Table HI shows .the ages of some of the goats examined in one herd. The goats were mainly adult animals (Table HI), but about 10%, if infected, would have been too young to have any hydatid cysts large enough to be obvious under field conditions. The lungs, liver, omentum, mesentery and heart of all the goats were examined for E. granulosus, T. hydatigena, T. ovis and possibly M. gaigeri. A perfunctory examination of the carcasses was made for cysts of T. ovis, and 149 brains from
the Whaiterinui, south Wairoa and Huntly herds were examined for M. multiceps or possibly E. granulosus. Table IV shows that E. granulosus occurred in the lungs and livers of 5% of 153 goats in one herd, 14% of 14 animals in another herd, and 1% of 212 goats in a third herd. Four of the 15 hydatid cysts had diameters of 25, 25, 23 and 22mm. This is larger than the size required for the production of brood capsules and scoleces in other hosts (Sweatman and Williams, 1962), but only one (23mm) of the goat cysts contained scoleces. In it, there were no brood capsules, and the four scoleces which did occur were attached directly to the germinal membrane. One of the other large cysts and also two small ones were filled with gelatinous material rather than hydatid fluid. These observations suggest that the goat can serve as a host of E. granulosus, but that the parasite is not particularly successful in it.
Total number of Rabbit Destruction Boards in Hydatid Control Authorities = 204 Average number of Rabbit Destruction Boards in Hydatid Control Authorities = 4.4 Total number of Rabbit Destruction Boards surveyed for dog tapeworms = 135 Other numbers on Fig. 22 (Roman face) = Hydatid Control Authorities without Rabbit Destruction Boards.
Animals from the three herds with E. granulosus were also infected with a 24%, 86% and 40% incidence of T. hydatigena. This tapeworm also infected 17% and 20% of goats in two other herds in which E. granulosus was absent.
Only one animal, in the Huntly herd, was infected with cardiac cysts of T. ovis. Multiceps spp. were not found. It is clear that the goat is an important reservoir of T. hydatigena, and is sometimes infected with E. granulosus and T. ovis.
Feral Horses, Cattle and Sheep
Small herds of feral horses are found in clearings in forest plantations only on the central plateau of the North Island. Feral cattle also occur in the same forest and there are small groups elsewhere in the country. Feral sheep occur locally in both the North and South Islands, and about 2,000 of these are shot annually (Wodzicki, 1961).
No feral horses, cattle or sheep have been examined for cystic tapeworm infections by us, but feral cattle and sheep are indisputable potential, if not real, hosts. Farm horses in New Zealand have not been seen infected with E. granulosus and Williams and Sweatman (1962) have shown that the type of E. granulosus in horses in the United Kingdom and possibly elsewhere is biologically and morphologically distinct from the type in New Zealand sheep, cattle and swine. Horses are therefore of no consequence in the epizootiology of hydatid disease in New Zealand.
Feral Pigs
Feral pigs ( Sus scrofa ) occur in marginal farmland, fern and scrub country throughout the North and South Islands, Poor Knights Islands, Great Barrier Islands, Chatham Islands, and Auckland Islands, but not on the other small offshore islands or on Stewart Island. Wodzicki (1961) presented data indicating that 20,000 to 30,000 feral pigs are killed annually.
Perfunctory autopsies of 251 feral pigs from the North Island and of 242 from the South Island were carried out. An hepatic cyst of E. granulosus was collected from a pig in the South Island and cysticerci of T. hydatigena were collected from 5 wild pigs in the South Island and 2 in the North Island. Only a single cyst occurred in each pig with the exception of one animal infected with 3 cysticerci. In 1953, Ineson reported that none of 21 wild pigs from the North Island and from the Marlborough Sounds of the South Island was infected with either E. granulosus or T. hydatigena. It seems clear that, in spite of their nomadic habits, feral pigs constitute only a minor reservoir of E. granulosus and T. hydatigena under New Zealand conditions.
111. Domestic Definitive Hosts Associated With Wild Animals Certain classes of dogs in New Zealand have close affinity with wild herbivores. For the most part these are used for rabbit destruction and hunting pigs. Rabbit Dogs
Rabbit Boards operate in most regions of New Zealand to reduce the numbers of rabbits and hares to a low level. Dogs are used extensively, and since they operate on a number of farms the rigid control of their diet becomes paramount in a campaign directed against E. granulosus and T. hydatigena.
Information on rabbit dogs was obtained by a questionnaire sent to the pertinent Hydatid Control Authority which also provided us with the incidence of infections of E. granulosus and T. hydatigena as determined by the National Hydatid Testing Station. Infections were based on the examination of faecal samples following the oral administration of arecoline hydrobromide, an assess-
ment of which was presented elsewhere (Sweatman, 1962). There are 204 rabbit boards in New Zealand, 135 of which form the bases of the following conclusions. The information was received from 29 of the 46 Hydatid Control Authorities with rabbit boards.
Table V shows that up to 27 Rabbit Boards occur in each Hydatid Control Authority. Rabbit boards employ from 1 to 21 rabbiters (average 3.4) and are responsible for areas of 13,000 to 4,335,000 acres (average 184,850) of generally rugged terrain. Each board contains 1 to 23 packs of rabbit dogs with each pack numbering 1 to 20 dogs (average 8). Usually each rabbiter works with 5 to 6 dogs at a time.
The working habits and feeding of rabbiters’ dogs is similar throughout the country. Rabbit dogs are used more or less continuously during the year. All Hydatid Control Officers reported that rabbiters feed their dogs with care and are aware of the dangers of feeding raw offal. The main food items are rabbits and hares. Frequently unbutchered sheep, cattle and horses are donated by farmers. Of the 135 reporting rabbit boards, possums are fed by 19; wallabies by 1; feral goats by 10; and deer by 7. Carcass meat is fed raw. Some rabbiters feed cooked offal. When not working, each rabbit dog is chained to an independent kennel located in an area some distance from human habitation. Most rabbit dogs return to a base kennel (Fig. 14) after each day’s work, while other packs are temporarily housed and fed on the farm being worked. Of 177 packs of rabbit dogs, 108 always returned to a base-kennel each night; 57 almost always; 12 about half the time; and one pack was itinerant. When housed away from the base kennel, the dogs would be less likely to acquire an accidental infection of E. granulosus and T. hydatigena since the rabbiters transport the meat to their dogs and any butchering required is done at the base kennel beforehand. The greatest danger to dogs acquiring these infections is likely to occur when the ungulates are being butchered at the base kennel. Carcasses on pastures encountered by the working dog could be another possible source of infection.
The data on the infections of E. granulosus and T. hydatigena in rabbit dogs have been grouped according to Hydatid Control Authorities, Rabbit Boards and individual dogs, and are compiled according to the dosing round of the local Hydatid Control Officer (Fig. 23). Most Hydatid Control Officers have been operating for about a year, but some for two years. Hence, the earlier dosing rounds have a larger number of observations with the numbers falling to an insignificant level beyond the fifth dosing round. The first dosing round is not a true base-line since almost all the rabbit dogs were treated with arecoline hydrobromide by a voluntary hydatid worker or by the rabbiter before the first visit of the Hydatid Control Officer. In spite of this, Fig, 23 shows that the number of Hydatid Control Authorities with rabbit dogs infected with E. granulosus dropped from 56% to 39% from the first to the third dosing round with an upswing to 50% for the fourth round but a downswing to 31% for the fifth. The number of Rabbit Boards with dogs infected with E. granulosus dropped from 18% in the first dosing round to 9% in the fifth. The comparable figures for infected dogs dropped from 2.3% to 0.9% with a possible upswing in the sixth and seventh rounds. These data suggest a more or less gradual reduction in the number of rabbit dogs infected with E. granulosus, but the results are more obvious for T. hydatigena. As many as 86% of the Hydatid Control Authorities had at least one rabbit dog infected with this parasite in the first dosing round. This dropped to 56% by the fifth round. Fig. 23 shows a more or less regular
decline in the number of Rabbit Boards with dogs infected with T. hydatigena from 36% in the first round to 17% in the fifth. There is a suggestion of an even further decline in the sixth and seventh rounds. Concomitant with this, the number of infected dogs dropped from 5.0% to 1.9%.
It is clear that infected rabbit dogs occur throughout New Zealand. There is no correlation between infected dogs and a particular Rabbit Board or Hydatid Control Authority. A reduction in the number of infections in rabbit dogs with E. granulosus and T. hydatigena is apparent, but additional care is required if these tapeworms are to be eradicated. Farmers can assist greatly by insisting that all rabbit dogs brought onto their properties be free of infection. This insistence should apply especially to farmers whose own dogs are worm-free. Rabbiters, in their turn, could insist that farmers remove any dead sheep carcasses from the farm before they go onto the property. Rabbiters should be encouraged to butcher carcasses used for their dogs away from the base kennel perhaps within a fenced-in enclosure inside of which is a deep pit for disposal of the offal.
Pig Dogs
Information has been collected on dogs used for hunting wild pigs according to (a) number of dogs in a hunting pack, (b) annual kill, (c) feeding habits, (d) usual pack domicile, and (e) incidence of infections with E. granulosus and T. hydatigena.
A bull terrier/sheep dog cross constitutes the usual pig dog, but in addition, it is not uncommon for rabbit dogs to be used also for hunting pigs. Most pig dogs noted in this survey are domiciled in villages, towns and cities (Table VI) where there would be greater contact with man, but some live on farms and a few in forestry camps and Maori pas. Table VI shows that most dog packs consist of 2 or 3 animals and rarely as many as 10. Dog packs tend to be used for hunting about every week or fortnight, and the number of pigs killed ranges up to about 3 animals per hunt (Table VI). A few hunters claim that pig offal is repugnant to dogs, particularly when still warm. Some prevent their dogs from feeding at the kill because they believe it makes the dog sluggish and food away from home encourages wandering. However, the pig’s liver is often fed uncooked to the dogs after the hunt.
Dogs in 2 of 24 packs in one district were definitely known to be fed occasionally on raw wild pig offal. At home, these two packs were fed on kitchen scraps and commercial dog food. Infections of E. granulosus and T. hydatigena were seen in two different dogs in one of these packs, and T. hydatigena occurred in one animal in the other pack. It is at least possible, therefore, that these dogs acquired their infections from feral pigs. Dogs in forestry camps, although never seen feeding on pig offal, have been known to return to the site of the kill where they might acquire an infection. Two of 8 dogs in forestry camps were infected with T. hydatigena (Table VI), but in both instances it would be just as reasonable for the infections to have been acquired from feral goats or even deer, also perhaps by returning to the kill. Hunting dogs sometimes come across dead sheep on pasture, and could conceivably become infected from this source, particularly since the dogs are often starved the day before the hunt.
The samples in Table VI are not large, but whatever the source of infection is for the pig dogs, this table shows that the incidence of E. granulosus and
T. hydatigena in the dogs in a district ranged up to 30% and 56% respectively. This is even a higher rate of infection than that seen in sheep dogs on New Zealand farms (Gemmell, 1958; Forbes, 1961) in spite of the fact that most pig dogs for which we have returns live in villages and towns and are fed extensively on kitchen scraps and commercial dog food. It is evident that pig dogs should be regarded as of some importance as a source of infection for man and livestock. At some juncture in the eradication campaign it may be expedient to regard pig dogs as a special group and perhaps restrict their movements and treat them with arecoline hydrobromide at 6 week intervals.
IV. Relationship With Human Infection
Foster (1958) reported on 242 people admitted for the first time for hydatid disease into public hospitals in New Zealand from 1954-56. There were in proportion to the total population, twice as many of these people domiciled in country areas as in cities and four times as many in towns. These figures suggested that people in small towns contract hydatid disease more than those living elsewhere. The importance of infection on farms must not be underrated, but it may be more than just coincidence that pig dogs live primarily in towns and that these dogs, as indicated in this paper, have a higher incidence of E. granulosus and T. hydatigena than farm dogs. Both worms demonstrate the ingestion of considerable raw offal by pig dogs. The low incidence of these tapeworms in wild pigs, however, suggests that the source of infection for the pig dogs is more likely to be sheep from farms at the periphery of the towns than pigs killed at the hunt.
Foster (1958) demonstrated also that in spite of the fact that hydatid disease in New Zealand is believed ,to be associated essentially with sheep farms, the rates of infection of patients from 1946-56 in various occupations to the total number of people in those occupations placed farmers fourth with an annual rate of 9 per 100,000 people in that occupational group. Farm workers were placed in a separate category and had an annual rate of 7 infections per 100,000 people, very similar to that of farmers. The first three occupational groups were (1) forestry and related workers (18 per 100,000), (2) spinners, weavers and related workers (16 per 100,000), and (3) labourers (13 per 100,000). The striking prevalence of the disease in people domiciled in towns and in forestry workers requires an explanation in light of what we know now about infections in wild as well as domestic animals.
Assessment of the kind of data summarised by Foster is inherently difficult for various reasons. Forestry work is generally strenuous, which may induce symptoms which would go unseen in someone with a more sedentary position. Most of New Zealand’s merchantable forests are in the North Island and employ some Maori* labour (1,037 Maoris : 4,177 Europeans in the year 1956) in which the incidence of hydatid disease is five times higher than in Europeans anyway (Foster, 1958; Rose, 1960). Forestry workers are often transient workers. Of the 1,392 forestry men within the New Zealand Forestry Service in 1961 a total of 800 (57%) were casuals employed for different periods up to six months. Many of these casual labourers do seasonal work in freezing works and on farms where dogs infected with E. granulosus are common. The other difficulty with pure statistics is that perhaps as many as 10 years may elapse between acquisition
of an infection and its detection, during which time the patient may have changed jobs a number of times.
In spite of these difficulties, it is true that pig, deer and goat hunting is a most popular pastime in forestry camps. Dogs are kept by the forestry workers to assist in the hunt, and many dogs no doubt return to the site of the kill, where they may become infected. The dogs are often as transient as their masters and may bring their infections to the camp with them. Sanitary conditions and personal hygiene in many forestry camps are rudimentary, and it is just possible that these combinations of circumstances predispose the forestry worker to hydatid infection.
Acknowledgments
This study was made possible through the generous co-operation of the personnel of the New Zealand Forest Service as well as the Hydatid Control Officers throughout the country. The determination of the different species of wallabies in New Zealand was kindly carried out from specimens examined by Mr R. Kean, New Zealand Forest Service, Wellington, and Mr J. H. Calaby, Wildlife Survey Section, G.5.1.R.0., Canberra. Technical assistance was provided by Messrs G. D. Page, D, V. Weston, Miss L. A. Duncan and Mrs B. R. Clarke.
References
Batham, E. J., 1957. Notes on viability of hydatid cysts and eggs. N.Z. vet. J. 5, pp, 74-76.
de Beaufort, L. F., 1951. Zoogeography of the land and inland waters. London: Sedgwick and Jackson Ltd. 208 pp.
Brander, A. A. D., 1923. Wild Animals in Central India. London: Edward Arnold & Co.
Brockie, R. D., 1958. The ecology of the hedgehog (Erinaceus europaeus L.) in Wellington, New Zealand. M.Sc. Thesis, Victoria University of Wellington, 121 pp.
Brumpt, E., 1949. Precis de parasitologic. Paris: Masson et Gie, 1082 pp.
Bull, P. C., 1953. Parasites of the wild rabbit, Oryctolagus cuniculus (L.) in New Zealand. N.Z. J. Sci. Tech. 348, pp. 341-372.
Campbell, W. D., and Richardson, T., 1960. Stimulation of cysticercus evagination by means of surfactants. /. Parasitol. 46, p. 490.
Clunies Ross, 1., 1929. Observations on the hydatid parasite Echinococcus granulosus (Batsch, 1786) Rudolphi 1805 and the control of hydatid disease in Australia. Counc. Sci. Ind. Res. Bull. 40, 63 pp.
Deve, F., 1949. L’tchinococcose primitive (Maladie hydatique). Paris: Masson et Cie, 362 pp.
Durie, P. H., and Riek, R. F., 1952. The role of the dingo and wallaby in the infestation of cattle with hydatids (Echinococcus granulosus (Batsch, 1786) Rudolphi, 1805) in Queensland. Aust. vet. J. 28, pp. 249-254.
Forbes, L. S., 1961. Observations on a survey of the incidence of cestodes in dogs in the North Island of New Zealand. N.Z. vet. J. 9, pp. 77-78.
Foster, F. H., 1958. Hydatid disease in New Zealand. N.Z. med. /. 57, pp. 562-571. Frauchiger, E., and Fankhauser, R., 1957. Verglerchende Neuropathologic das Menschen und der Tiere. Berlin; Springer-Verlag. 451 pp.
Gemmell, M. A., 1958. Cestode problems of domestic animals and man in the South Island of New Zealand. N.Z. med. J. 57, pp. 442-458.
South Wales as definitive hosts of Echinococcus granulosus (Batsch, 1786) Rud. 1801, and their role in the spread of hydatidiosis in domestic animals. Aust. vet. J. 35, pp. 450-455.
Hadwen, S., 1932. No title. /. Parasitol. 19, p. 83. Hall, M. C., 1916. A new and economically important tapeworm Multiceps gaigeri from the dog. /. Amer. vet. med. Assoc. 50, pp. 214-223.
in North America. Proc. U.S. Nat. Mus. 55, pp. 1-94.
Hilgendorf, F. W., 1935. The grasslands of the South Island of New Zealand. N.Z. Dept. Sci. Ind. Res. Bull. 47, 24 pp.
Hosley, N. W., 1953. Fluctuations of the United States big game populations during the last decade. Proc. 7th Pacific Sci. Cong. 4, pp. 620-626.
Houston, J., 1835. An account of hydatids in the omentum of an Axis deer; with observations on their pathological changes. Dublin J. Med. Chem. 8, pp. 268-281.
Hutchison, W. F., and Bryan, Mildred W., 1960. Studies on the hydatid worm Echinococcus granulosus. I. Species identification of the parasite found in Mississippi. Amer. J. trop. Med. Hyg. 9, pp. 606-611.
Ineson, M. J., 1953. A comparison of the parasites of wild and domestic pigs in New Zealand. Trans, roy. Soc. N.Z. 82, pp. 579-609.
Joyeux, Ch., and Baer, J. G., 1936. Faune de France, 30, Cestodes. Paris: Lechevalier et fils. 613 pp.
Lorincz, F., 1933. A macska szereperbl az echinococcosis teryeszteseben. Orvosi Hetilap, 77, pp. 532-536.
Maghui/skii, S. N., 1950. (Helminths of elk of Buriat Mongolia) (in Russian). Doklad. Akad. Nank. S.S.R. 73, pp. 1313-1315.
Mackerras, M. Josephine, 1958. Catalogue of Australian mammals and their recorded internal parasites I-IV. Proc. Linn. Soc. N.S.W., 83, 101-160.
Marshall, W. H., 1961. Ecology of mustelids in New Zealand. Animal Ecology Division, Dept. Sci. Ind. Res., Inform. Ser. No. 1, 24 pp.
Matthews, L. H., 1952. The new naturalist: British mammals. London: Collins. 410 pp.
Megoitt, F. J., 1924. The cestodes of mammals. London: (printer not stated). 282 pp.
Murie, O. J., 1951. The elk of North America. Harrisburg and Washington: The Stockpole Co. and Wildlife Management Institute, 376 pp.
Olsen, O. W., and Williams, Jesse E., 1959. Cysticerci of Taenia krabbei in mule deer in Colorado. /. wildlife Mgmt. 23, 119-122.
Peterson, R. L., 1955. North American moose. Toronto: Univ. Toronto Press. 280 pp.
Poole, A. L., 1951. Preliminary reports of the New Zealand-American Fiordland expedition. N.Z. Dept. Sci. Ind. Res. Bull. 103, 99 pp.
Pullar, E. M., 1946. A survey of Victorian canine and vulpine parasites. I. Material and methods used in the investigation. 11. Taenia multiceps. Taenia ovis and Echinococcus granulosus. Aust. vet. ]. 22, pp. 12-21.
Rao, S. R., Bhatavdekar, M. Y., and Detha, K. T., 1957. Morphology and development of Coenurus gaigeri Hall in a ewe with particular reference to the taxonomy of the genus Multiceps. Bombay vet. Col. Mag. 6, pp. 12-18.
Rensch, 8., 1959. Evolution above the species level. London: Methuen and Co. Ltd., 419 pp.
Riney, T., 1955. Identification of big game animals in New Zealand. Dominion Museum Handbook, No. 4, 26 pp.
pp. 26-27.
Rollings, C. T., 1945. Habits, foods and parasites of the bobcat in Minnesota. /. wildlife Mgmt. 9, pp. 131-145.
Rose, R. J., 1960. Maori-European standard of health. Dept. Health, Special Report No. 1, 48 pp.
Severxnghaus, G. W., and Cheatum, E. L., 1956. Life and times of the white-tailed deer, pp. 57-186 in Taylor, W. P., 1956. The deer of North America. Harrisburg and Washington: The Stockpole Go. and The Wildlife Management Institute.
Shaw, J. N., Simms, B. T., and Muth, O. H., 1934. Some diseases of Oregon fish and game and identification of parts of game animals. Oregon agric. exp. Station Bull. 322, 23 pp.
Simpson, G. G., 1945. The principles of classification and a classification of mammals. Amer. Mus. Nat. Hist. Bull., Vol. 85, 350 pp.
Southwell, T., 1927. Experimental infection of the cat and the fox with the adult Echinococcus. Ann. trop. Med. Parasitol. 21, 155-163.
Stiles, C. W., and Hassall, A., 1912. Index-catalogue of medical and veterinary zoology. Subjects: Cestoda and Cestodaria. U.S. Pub. Health and Mar. Hosp. Serv. Hyg. Lab. Bull. 85, 467 pp.
Sweatman, G. K., 1952. Distribution and incidence of Echinococcus granulosus in man and other animals with special reference to Canada. Canad. J. pub. Health 43, pp. 480-486.
Canad. J. comp. Med. vet. Sci. 21, pp. 65-71.
and Henshall, T. C., 1962. Canad. J. Zool. (in press).
and Plummer, P. J. G., 1957. The biology and pathology of the tapeworm Taenia hydatigena in domestic and wild hosts. Canad. J. Zool. 35, pp. 93-109.
and Williams, Rosemary J., 1962. Unpublished data. Williams, R. J., Moriarty, K. M., and Henshall, T. C., 1962. Res. vet. Sci. (in press).
Taylor, W. P., 1956. The deer of North America. Harrisburg and Washington: The Stockpole Co. and The Wildlife Management Institute.
Thomson, G. M., 1922. The naturalization of animals and plants in New Zealand. Cambridge: Cambridge University Press, 607 pp.
Thornton, H., 1949. Textbook of meat inspection. London: Baillifere, Tindall and Cox, 659 pp.
Wardle, R. A., 1933. The parasitic helminths of Canadian animals. I. Gestodaria and Cestoda in Canadian animals. Canad. J. Res. 8, pp. 317-333.
Watson, J. S., 1956. The present distribution of Rattus exulans (Peale) in New Zealand. N.Z. J. Sci. Tech. 37, pp. 560-570.
Weidman, F. D., 1923. In Fox, H. Diseases of captive wild mammals and birds. Philadelphia: J. B. Lippincott Go., 631 pp.
Williams, Rosemary J., and Sweatman, G. K., 1962. Unpublished data. Witenberg, G., 1933. Zur Kenntnis der Verbreitung von Echinokokkus und Trichinen in Palastina. Arch. Schiffs-u. Tropen-Hyg. 37, pp. 37-41.
Wodzigki, K. A., 1950. Introduced mammals of New Zealand. N.Z. Dept. Sci. Ind. Res. Bull. 98j 255 pp.
La Terre et la Vie 1, pp. 130-157.
Wolfe, H. R., 1939. Serological relationships among Bovidae and Gervidae. Zoologica 24, pp. 309-321.
Yamashita, J., Ohbayashi, M., and Konno, S., 1956. Studies on echinococcosis. IV. Experimental infection of the white mouse. Japanese J. vet. Res. 4, pp. 123—128.
Dr G. K. SweatmaNj Department of Tropical Health, American University of Beirut, Lebanon. Miss R. J. Williams, Hydatid Research Unit, N.Z. Medical Research Council, Medical School, Dunedin.
* Present address: Department of Tropical Health, American University of Beirut, Lebanon.
* It would seem logical to assume that the type of E. granulosus in dingoes and wallabies in north-eastern Australia is identical with the type of hydatid in sheep and dogs and that the sylvatic infections became established in post-European times following their transfer from domestic animals. There are, however, two hosts capable of perpetuating a hydatid cycle known from Pleistocene deposits in Queensland. These are the dingo (Canis dingo) and the New Guinea pig (Sus papuensis). The former is very much a dog. The New Guinea pig is akin to the European Sus scrofa and hence to Palaearctic stock and not to Malayan pigs (de Beaufort, 1951). It seems likely, as de Beaufort implies, that Aboriginal man was accompanied by the pig as well as the dingo when he invaded Australia. If so, hydatid infections may have become established in Australia at that time also, and, being a peripheral population, may have established independent genetic characters. Although it is remote, the possibility of a distinctive sylvatic hydatid cycle in Australia is not completely out of the question.
not at group
* This represents a lower figure than that indicated by the total number of cysts, since some individuals were infected at more than one site. An infected animal usually had one cyst, sometimes two, and rarely as many as five.
X Includes cysticerci attached to biliary ligaments as well as those at the surface of the liver, but does not include haemorrhagic streaks or caseous lesions caused by migrating T. hydatigena.
f Lung; diaphragm; inside heart auricle; external surface of pericardium.
consist only may
* A Maori is classified as a person with half or more Maori blood.
Parasite Gat Number Number Scoleces or Cysticerci Period of Infection (days) Number Worms at Autopsy Worm Length (mm) Number Proglottids T. hydatigena 1 3 2 1 5 0 1 18 1 25 2 8 5 1 4 0 1 32 .1 37 3 2 5 0 — . — 4 2 14 0 — — 5 7 14 4 13 31 9 28 9 24 5 2 6 6 19 2 4 0 4 0 7 5 28 2 4 0 4 0 8 5 97 0 — — M. multiceps 9 2 7 0 __ 10 10 11 0 — — 11 10 46 0 — — 12 10 155 0 — — T. ovis 13 10 4 0 _ 14 6 16 6 20 to 32 mature 15 5 59 1 — gravid 16 5 62 3 — 2 gravid ♦ 1 mature T. ovis 17 6 62 6 gravid Horse meat) 18 6 62 3 — gravid 19 6 62 0 — — 20 6 121 2 — gravid T. ovis 21 6 62 2 — gravid (Mutton) 22 6 62 0 — — 23 6 62 0 — — 24 6 62 0 — —
Table I EXPOSURE OF CATS TO T. HYDATIGENA, M. MULTICEPS AND T. OVIS.
Mammal Exposed Age (months) Animal Number Number Eggs Period Before Autopsy (months) Number Cysts Autopsy ofSite Infection Size cyst (mm) Scoleces Possum 4 1 1,000 H 2 Lung 13 Absent Abdominal 17 Absent Wall 2 10,000 n 7 Lungs 6-36 in Present Mediastinal 17 Absent Septum 3-16 See — 0 — — — Wallaby 9 1 10,000 17* 2 Muscle 10 Present Muscle 7 Absent 2-4 See — 0 — — — White 1 1 10,000 6* 1 Liver 6 Absent Mouse 2 10,000 9 2 Liver 15 Absent Liver 4 Absent 3 10,000 9 2 Liver 10 Absent Liver 4 Absent 4 10,000 10 2 Liver 10 Absent Lung 3 Absent 5 10,000 13 2 Liver 23 Present Abdominal 20 Present Cavity 6-20 10,000 9 0 — — — Laboratory 2 1 Numerous 8 ±50 Lungs 5-15 Absent Rabbit 2 Numerous 9 33 Lungs 8-24 Absent 3 Numerous 10 25 Lungs 10-25 in Present 2 Fat 9-23 in Present 4 Numerous 13 1 Lung 25 Absent 5 Numerous 14 2 Lung 4-6 Absent 6 Numerous 14 Lungs 6-25 7 7-11 5,000 3 0 — — — Fallow 4 1 10,000 21 0 — 4 2 10,000 21* 1 Liver 1 Absent Red 33 1 Numerous 7* 1 Lung 7 Absent 9 2 7,000 3 1,292 Lungs 1-2 Absent Kidney 21 3 Numerous 14 0 — — . 11 4 Numerous 14 0 — — —
Table II LABORATORY INFECTIONS OF MAMMALS WITH E. GRANULOSUS*
SPECIES Fallow Deer Red Deer Goat LOCATION Gaples Valley Highburn Valley R.D. 2, Huntly TIME November, 1958 December, 1958 September, 1959 DEVELOPMENTAL STAGE Fawn or kid 4 0 7 Two-tooth 16 4 14 Four- to six-tooth 38 3 19 Full mouth 9 0 24 Broken mouth 0 0 6 TOTAL 67 7 70
Table 111 DEVELOPMENTAL STAGE (AGE) OF SOME OF THE DEER AND SEMI-FERAL GOATS EXAMINED FOR CYSTS.
Location Number Animals Number granulosus E. % Animals Infected* T. Number Cysts Animals Infected* Lungs Liver Omentum LiverJ Otherf GOATS Whaiterinui 153 10 1 5 26 11 3 24 South 212 1 1 1 68 17 1 40 Islands Bay 630 0 0 0 ? ? ? 17 HuntlyR.D.2, 180 0 0 0 81 0 1 20 Stratford 14 2 0 14 11 6 0 86 Mount 6 0 0 0 1 0 0 — DEER Wellington 6 0 0 0 4 0 0 — ForestTapanui 30 0 0 0 0 0 0 0 ValleyGaples 67 0 0 0 5 0 1 9
Table IV INFECTION OF E. GRANULOSUS AND T. HYDATIGENA IN SOME H ERDS OF FALLOW DEER AND SEMIFERAL GOATS.
North Island South Island Hydatid Control Authority (H.G.A.) (Number on Fig. 22) Number of Rabbit Boards in H.G.A. Number of Rabbit Boards in Survey Hydatid Control Authority (H.G.A.) (Number on Fig. 22) Number of Rabbit Boards in H.G.A. Number of Rabbit Boards in Survey 4 1 1 46 1 0 8 2 0 49 6 6 9 4 4 50 2 2 13 2 2 51 4 4 14 1 0 53 7 5 15 1 1 54 3 0 16 4 0 56 1 0 18 3 0 57 3 1 19 4 4 60 2 0 20 2 2 61 1 0 24 1 1 63 3 2 25 2 2 64 2 2 26 4 0 65 2 • 0 27 2 0 66 4 3 32 1 1 67 5 5 33 2 0 68 10 0 36 2 2 69 18 17 37 2 2 70 17 17 38 2 2 71 8 8 39 7 0 72 5 5 40 1 1 73 10 6 42 3 0 74 27 22 43 2 0 75 6 5
Table V DISTRIBUTION OF HYDATID CONTROL AUTHORITIES, RABBIT DESTRUCTION BOARDS, AND NUMBER OF BOARDS SURVEYED FOR DOG TAPEWORMS.
Dunedin City u> » M V| 03 Gisborne City 09 03 tO 03 03 — 4. O O NS 03 22 Fig. on H.C.A. o « .► o w I 05 50-100 24 3 100 9 42 in Packs No. District 4. wo + oif 03 4. In w 'J io o Observed Packs No. 03 o> U1 ro S* ro ro K» 5* 071 071 I ro os . r* 4* ro 05 U5 wO Dogs No. Aver. S | l ro os !° »- 4* Packper -3 Os Os 2-4 1-3 2-1-3 2Range No. Dogs per Pack. ro 4* ro oo io I os ro 05 O' 1 4On Aver. No. Times Each Pack Hunted in i960 05 4* -4 ro ! ro O 03 03 I ro ro 05 ‘ u 5 S » W Aver. No. Pigs Killed per Pack in 1960 o o o o o o o «- o o o o 1 Maori Pa G o o o to o o SOUTH ISLi o 0 0)000 1 0 JO I Forestry Camp ? o >r o 03 o o to o o 1 3 co f p o Farm §. o ? o o o o *—* CO 4* 2 o o o> I > a c Village g 1 o 03 4* IO o IO o OMMUN | Town u f> pr 4o o o o o 03 o o o o o 1 City O O O O O N3 o MOWO^>No. Packs with E. granulosus o 0 0 0 0 4. o « o 4. o 4. W Total Dogs with E. granulosus ; nils 1 » 1 SI too % Dogs with E. 'granulosus o 141 o 1C O 1C o 0-^OH03 No. Packs with T. hydatigena o 4* O IO O 05 o - - o o w Total Dogs with T. hydatigena 1 13 13 ! 1 O ; On i • ro 1 4- w I Cr 05 1 — o B /r Dogs with T. hydatigena per Pack t 2-6 2 2 1-3 1-7 1-3 2-1-3 2Range No. Dogs per Pack. ro 4IO CO IO I 09 ro CO 071 I 4O" Aver. No. Times Each Pack Hunted in i960 CD 4“ ro | ro O 09 09 1 ro ro o 15 68 145 83 17 ? Aver. No. Pigs Killed per Pack in 1960 O o o o o o o ►- o o o o i Maori Pa G O O O IO o o SOUTH ISLy o O OS CS o o 1 0 7> | Forestry Camp S’ *■ o 09 o O IO o o 03 O 4. O OS 1 S vs FO Farm |. O ? o o o o ** 00 4* o "•-S-Ott | > C Village | o OS 4* IO O to o O K3 N3 03 fo 1 Town u f> fr 4o o o o o 09 O O O O O 1 City O o o o o so o *-> O 03 O 4. ►- No. Packs with E. granulosus o 0 0 0 0 4. o 03 O 4. 0 4. 03 Total Dogs with E. granulosus i IMIS 1 OS I SI too % Dogs with E. 'granulosus O io o io o io o O-^oSw No. Packs with T. hydatigena o 4- O IO o 09 o — — O O to 03 Total Dogs with’ T. hydatigena i ro io * I o ; ui i ’£> \ ro 071 I 4- 09 1 CT DO o> 1 — O e /r Dogs with T. hydatigena Aver. No. Dogs
Table VI RELATION BETWEEN PIG DOGS, PIG KILLS AND INFECTIONS OF E. GRANULOSUS AND T. HYDATIGENA
Permanent link to this item
https://paperspast.natlib.govt.nz/periodicals/TRSZOO19621120.2.2
Bibliographic details
Transactions of the Royal Society of New Zealand : Zoology, Volume 2, Issue 26, 20 November 1962, Page 221
Word Count
14,025Wild Animals in New Zealand as Hosts of Echinococcus granulosus and Other Taeniid Tapeworms Transactions of the Royal Society of New Zealand : Zoology, Volume 2, Issue 26, 20 November 1962, Page 221
Using This Item
In-Copyright Materials
In-copyright materials are made available under a Creative Commons Attribution 4.0 International licence. This means that you may copy, adapt and republish this material, as long as you attribute both the author and the Royal Society of New Zealand.
In-copyright taxonomic materials are made available under a Creative Commons Attribution No-Derivatives 4.0 International licence. This means that you may copy and republish this material, as long as you attribute both the author and the Royal Society of New Zealand.
For advice on reproduction of out-of-copyright material from this periodical, please refer to the Copyright guide.
Log in