A Comparison of the Parasites of Wild and Domestic Pigs in New Zealand.
[Read before a meeting of the Wellington Branch, February 17. 1954; received by the Editor, February 19, 1954.]
Twenty-Two wild pigs and the carcases and viscera of numerous domestic pigs were examined to determine the presence and intensity of parasitic infestation. Forty wild pig faecal samples were examined for eggs and cysts. Fifteen species of parasites and an anaplasma-like body were encountered during this survey. The following parasites are recorded from both groups of pigs. The figures given without brackets refer to pigs of the wild group, while those bracketed refer to the domestic group: Balantidium coli 61.9% (40%), Eimeria debliecki 4.7% (68%). Anaplasma 6.6% (70%), Cysticercus tenuicollis 4.7% (50.8%), Hyostrongylus rubidus 28.5% (48%), Ascaris suum 42.8% (1.2%), Metastrongylus elongatus 66.6% (26%), Choerostrongylus pudendotectus 38% (16%), Haematopinus suis 68.1% (49.3%), and Sarcoptes scabiei var. suis 4.5% (36%). Oesophagostomum dentatum infested 14.2%, and Demodex phylloides was present among the wild group. Echinococcus granulosus (10%), Fasciola hepatica (present), Trichuris suis(20%) and Globocephalus urosubulatus (4%) infested only the domestic group.
The environmental habitats of both groups of pigs are correlated with the incidence and intensity of infestations of the parasites, and where possible, with the life history of the parasites and the viability of the eggs. Sex ratios of nematodes are given and where possible egg counts recorded. Females were usually present in greater numbers than males. Adult specimens of M. elongatus, C. pudendotectus and A. suum were cultured in vitro in several media, and the egg-production of 5 worms of A. suum was observed. Specimens of A suum survived longest in Baldwin and Moyle's culture fluid maintained at body temperature. Specimens of M. elongatus and C. purendotectus survived longest in Ringer's solution held at room temperatures. and least in cultures maintained at body temperatures. Graphs have been prepared illustrating these survival periods.
Results obtained by other workers on the incidence of similar parasites in New Zealand and other countries, are compared with those obtained during this survey. The incidence and intensity of parasitic infestations of pigs in New Zealand is correlated with the habits of the wild and domestic animals in their respective habitats, the varying environmental factors, and the viability of resting and infective stages of the parasites.
The presence of both wild and domestic pigs in New Zealand offers a unique opportunity for a comparative study of the parasites of two isolated groups of the one host living under different environmental conditions. Wild pigs inhabit areas showing wide topographic and climatic variations, while domestic pigs are bred under comparatively uniform conditions. Both groups must be considered as being only relatively isolated from one another, however, since those pigs introduced to New Zealand in the latter half of the 18th century by De Surville, Cook and others, have been increased in number and cross-bred with pigs escaped from the farms of early settlers. This records the parasitic fauna of both wild and domestic pigs and the effect of the contrasting habitats.
Wild pigs for this study were secured from four widely separated areas by organised pig-hunting trips, over a period of 12 months. Twenty-two animals thus secured were examined for the presence and intensity of parasitic infestations. Domestic pigs were examined at J. C. Hutton's Bacon Factory, Ngauranga, and as many were seen as time would permit over a period of 16 months.
Material from both groups was preserved for examination later in the laboratory. Owing to varying conditions under which this material was obtained as well as the possibility of seasonal infestation of parasites, periodicity of egg-laying and cyst formation, the incidence of species recorded among both wild and domestic pigs should be regarded as approximate only.
Faeces taken from the rectum of slaughtered wild and domestic pigs, and 40 wild pig faecal samples, were subjected to a saline centrifugal flotation technique to obtain eggs and oocysts for the detection of infestations, for viability experiments, and for egg-counts. The viability of eggs and developmental stages of some parasites were investigated where possible, and the effect of the environment on viability and developmental stages was correlated with the incidence of parasites of wild and domestic pigs.
As a result of the comparative isolation of both groups in their respective habitats, some parasites were restricted to or present in greater numbers in only one of these groups of animals. Two of three species of ectoparasites, one of two cestodes, four of seven nematodes, two protozoa and an anaplasma-like body were common to both groups. Only two species of parasites have been recorded previously from wild pigs in New Zealand. The presence of another ten species is recorded here, while three more species are added here to the list of domestic pig parasites in this country. A comparison made between the incidence of individual parasites among domestic pigs of New Zealand and the incidence of some parasites of pigs of other countries, shows a wide variance. This variance is due to the dissimilar environmental conditions of individual countries.
Habits and habitats, diet and the presence of other animals which are intermediate or primary hosts, influence the presence of parasites among wild and domestic pigs. The conclusions reached therefore, upon the incidence of parasites among animals of both groups, are of economic importance in relation to the distribution and prevalence of swine parasites throughout New Zealand.
Members of Cook's first expedition in 1769 were informed that the Maoris had no pigs amongst them and that their ancestors had brought none with them. According to Fell, Garrick, et al. (1953), Crozet, writing in his journal of the French expeditions of 1769 and 1772, reports pigs to be absent from New Zealand. Angus (1847) states that the first pigs were left on the Islands of New Zealand by Spaniards. However, Thomson (1922) records that pigs were first introduced when De Surville of the French expedition presented two small animals to the Maori Chief at Doubtless Bay in December, 1769.
During Cook's second voyage, on June 2, 1773, Captain Furneaux released one boar and two sows in Queen Charlotte Sound in the South Island. Later in that year, November 2, following a visit to the Polynesian Islands where he probably obtained pigs, Cook released two pairs at Cape Kidnappers in the North Island. On November 8, 1774, one boar and one sow were released by Cook “next without” Cannibal Cove in the Queen Charlotte Sound, and off
Motuara Island on February 24, 1777, Cook presented a pair of pigs to a Maori Chief. Cook states, “I have at different times left in New Zealand not less than ten or a dozen hogs, besides those put on shore by Captain Furneaux.” It is thought that most of the first pigs introduced either died or were caught before they became wild and were eaten by the natives. From about 1790 onwards there are records of many importations of pigs into New Zealand; for example in 1793 Lieutenant King of New South Wales presented North Island Maoris with pigs that he obtained from Norfolk Island.
The principal reason for Cook's introduction of pigs was to provide food for sailors. The pigs established themselves in very great numbers, and soon became a source of food to the Maoris, to settlers, visitors and whalers, as well as sailors. Because the Maoris were fond of pigs and because of the poor fencing conditions of the early farmers, these animals were assisted in their spread, becoming distributed over most of New Zealand.
Thomson (1922) is of the opinion that, although in later years wild pigs had their numbers augmented and their breed modified by pigs which escaped from settlers, the “Captain Cook” type remained dominant and is still to be found in most of the wild parts of the country in great abundance. Although 22 wild pigs were caught and about the same number seen during the course of collecting material for this thesis, not one resembled the above type. Thomson also states that the wild pigs in the North Island are different from those in the South Island, because the former are largely the progeny of animals given to the natives in later years. Wodzicki (1950) records some authors as stating that Europe is the place of origin of the first wild pigs in New Zealand, but other authors, as has already been mentioned, claim that pigs were obtained from Pacific Islands visited by Cook on his way to New Zealand, and so are indirectly European. The black Berkshire is believed to have been the dominant breed of pig of the early days, and black is still the commonest colour of the wild pig found in most parts of New Zealand. Pigs of both Islands did not differ much in appearance, and black is by far the commonest colour; but in the North Island, rust-coloured pigs, a Tamworth characteristic, were seen, and black and pinkish coloured pigs were collected. In the South Island, black pigs were seen and collected and a greyish coloured pig was also taken. Information from reliable pig-hunters report the presence of small numbers of slatey-blue coloured pigs in Marlborough Sounds.
Wodzicki (1950) has established the population densities of wild pigs infesting areas in New Zealand on data collected in 1946. One pig to two acres is regarded as a heavy infestation, one pig from two to seven acres as a medium infestation, and where there is less than one pig to seven acres, as a light infestation. On the basis of his population density map, pigs collected for this thesis from the Hawke's Bay areas can be regarded as coming from heavily infested country. Pigs collected from Castlepoint and material collected from Mount Holdsworth, Otaki Forks and Orongorongo Valley, come from lightly infested country. Pigs from Marlborough Sounds, Awatere Valley and the Medway area come from medium infested country.
The topographical features of the areas where wild pigs were collected varied greatly from bracken-covered rocky slopes to swampy flat land, scrub-covered slopes and flat land, and forested slopes.
Surveys of domestic pigs for worm parasites have been carried out in New South Wales by Kauzal (1930), and in Queensland by Roberts (1934a). Results of numerous surveys of domestic pigs for one particular parasite have been examined and will be recorded in the subsequent discussions. Young (1938) lists helminth parasites of domestic pigs and Whitten (1949) records parasites of domestic pigs and one species, Demodex phylloides, of wild pigs in New Zealand. O'Connor (1923) during his researches in the Western Pacific, reports several parasites infesting pigs inhabiting the islands which he visited. Wodzicki (1950) records one ectoparasite, Haematopinus suis, among wild pigs in New Zealand.
Wild pigs were collected in the Marlborough Sounds and the Awatere Valley, Marlborough Province, Kereru and the Whakararas, Hawke's Bay Province, and Castlepoint, Wairarapa. Droppings and earthworms from wild pig rootings were collected from the Orongorongos and Otaki Forks, Wellington Province, and from Mount Holdsworth, Wairarapa. The animals were shot, or caught by dogs and stuck with a knife. One pig caught alive unharmed, at Castlepoint, was kept in captivity for three months.
On securing the animals an examination routine was adopted. Blood for smears was taken from the knife wound in the neck and from the heart. The animal was then examined for ectoparasites. Lice, diseased portions of the hide, or scrapings from the skin and ears were preserved in 70% alcohol. Then organs, tissues and walls of the thoracic and abdominal chambers were examined for cysts. Smears of the mucous lining of the oesophagus, and of the outside contents of the stomach, duodenum, jejunum, small intestine, caecum, large intestine and rectum were fixed in Schaudin's fluid with 5% of glacial acetic acid. Scrapings from approximately similar areas of the above regions of the alimentary canal were preserved in 10% formalin. About 5 grams of rectal contents were secured for examination by the direct centrifugal flotation technique, Lane (1928), as recorded by Chandler (1950). In apparent infestations of Ascaris suum, the small intestine was freed from the mesentery and its contents forced out. Livers were examined for parasites. The presence of usually pale rectangular areas extending inwards from the edges of the lobes of the lung indicated an infestation of lungworm. Diseased portions of internal organs, tissues, etc., and intestinal nematodes were preserved in 10% formalin. When water was absent from the particular locality where the pigs were caught, dissecting instruments could not be cleansed thoroughly. In these circumstances all possible precautions were taken to avoid samples becoming contaminated.
Most of the domestic pigs examined at the slaughter-house of J. C. Hutton N.Z. Ltd. were bred at Carterton, Wairarapa. Several were from the Auckland and Wellington Provinces, and Manawatu. Due to the chain system in operation in the slaughter-house visited it was not possible to make individual examinations of domestic pigs. Blood smears were taken from the knife wound in the neck because by the time the heart was removed it was drained of blood. A number of pigs were examined for ectoparasitic infestation, a number of internal organs were examined for cysts, and a number of alimentary canals were examined using the same technique employed with those from the wild pigs. Because the small intestines were freed and cleansed of their contents prior to utilisation as sausage casings, a large number of pigs were examined for Ascaris infestation. Lungs
were examined for lungworm infestation and livers for liver-fluke infestation. Cestodes, nematodes and diseased portions of pigs were preserved in 10% formalin Specimens of Ascaris suum for culture purposes were transported from the slaughter-house to the laboratory in Ringer's solution heated to host temperature, in a vacuum flask.
Wild pigs were collected over a period of 12 months. They were difficult to catch and the number obtained is regarded by experienced hunters as being good for the six trips undertaken, the hunting usually being restricted to the week-ends. On two other trips, only faeces and earthworms were collected.
Domestic pigs were examined over a period of 16 months. During this time more than twenty visits were made to the slaughter-house.
Fresh faecal samples collected from various pig-infested areas visited were stored in small tins. Faeces were secured at good distances from each other so as to minimise the risk of collecting two or more samples from the same pig.
Fresh blood smears from pigs were allowed to dry and were then fixed in absolute methyl alcohol and stained in Giemsa. The edges and drawn out portions of individual smears were examined for half an hour each.
Infestations with the small mange ectoparasites Sarcoptes and Demodex were detected as follows:—
(1) Scrapings from the body or chopped up pieces of the hide were boiled in 5% caustic potash until most of the material had dissolved. The solution was centrifuged and the sediment washed and then centrifuged again. If ectoparasites were present, they were amongst the debris at the bottom of the tube.
(2) Scrapings from diseased or scabby portions of the body were mounted in polyvinyl alcohol (Salmon, 1949) and any mange parasites present were thus cleared for examination. Or scrapings from affected areas were examined microscopically for the presence of parasites.
Lice were mounted and cleared in polyvinyl alcohol.
The invaginated scolex and neck of cysticerci were cleared in polyvinyl alcohol. Microtome sections of an invaginated scolex and neck of a cysticercus and of the wall of an hydatid cyst were stained with Heidenhain's iron-haematoxylin and counterstained with a 1% solution of eosin in 95% alcohol (Bolles Lee, 1950), but the sections were left in each of the iron alum and haematoxylin solution for 12 hours. Evaginated scolices of cestodes and whole trematodes were progressively stained for several days with acetic acid alum carmine.
Smears of the mucous lining of the oesophagus and of the contents in contact with the epithelium of the alimentary canal—stomach, duodenum, jejunum, small intestine, large intestine, caecum and rectum—of 19 wild pigs and 25 domestic pigs were fixed in Schaudin's fluid to which had been added 5% of glacial acetic acid. The smears were then stained with Heidenhain's iron-haematoxylin for 12 hours.
The above named regions of the alimentary canal were slit open and scraped with the blade of a scalpel, and this material was examined in a petri dish over a white or black glass plate and then under a low power binocular microscope. When small worms, or larval stages of worms were present, a modification of
Whitlock's (1948) worm counting technique was employed. A weak aqueous solution of iodine was added to stain the scrapings and parasites a yellowish-brown colour. After 15 to 30 minutes a solution of sodium thiosulphate was added and this decolourised the debris and mucus before decolourising the worms, thus facilitating recognition of nematodes.
Smaller nematodes were placed in a 5% aqueous solution of glycerine, to which had been added 2% of Nipagin M and Nipasol T, in a covered watchglass kept warm. As the water evaporated from the solution and condensed on the glass covering, it was removed. Nematodes gradually cleared, and when fully cleared, the worms were mounted in glycerine jelly. Large nematodes, Ascaris suum, could not be cleared this way, but instead their anatomy was determined by dissection.
Faeces from 21 wild pigs and 25 domestic pigs, and 40 faecal samples collected from areas where wild pigs were hunted, were individually subjected to the following techniques:—
(1) A simple wet preparation from the outside of fresh stools was examined for living protozoa and larvae.
(2) Two preparations from the outside of each stool were stained with Gram's Iodine and examined for the presence of larvae, eggs and cysts.
(3) Simple flotation, using saturated sodium chloride solution, was employed for the detection of eggs and cysts in 12 faecal samples from wild pigs. Each faecal sample was ground apart in saturated sodium chloride solution, filtered through a wire gauze and the sediment washed with more solution. Coarse particles which would impede the flotation of any eggs present were thus removed. The filtrate was transferred to a tube and a coverslip placed over the mouth and left in contact with the surface of the liquid for 30 minutes. It was then removed with an upward pull, mounted on a slide and examined.
(4) All faecal samples were subjected to Lane's (1928) direct centrifugal flotation technique slightly modified. One gram of faeces was ground apart in water, filtered, and the sediment washed thoroughly. The filtrate was transferred to a centrifuge tube which was spun for 2 minutes at 2,600 r.p.m. The cloudy supernatant fluid was poured off, clean water added and the sediment in the bottom of the tube stirred. The solution was centrifuged again and the process repeated until the supernatant fluid was clear. This was then poured off, saturated sodium chloride solution added and the sediment thoroughly stirred. The tube was spun at 2,000 to 2,100 r.p.m. for 2 minutes and the eggs brought to the top were either removed with a platinum loop 5 mm. in diameter, or by adherence to a coverslip. The loop was inserted vertically under the surface of the liquid, brought to the horizontal, and the surface film removed with an upward movement, transferred to a microscope slide and examined. Or the level of the liquid was brought to the top of the tube and a coverslip placed over the mouth. After 5 minutes, the coverslip was removed, mounted on a slide and examined. Examinations were made using a 10x eyepiece and a 10x objective.
Using the fourth technique, satisfactory results were obtained in determining infestations of intestinal nematodes and protozoa by the presence of eggs and
cysts. This method was found to be particularly effective for detecting in faeces, eggs present in only small numbers.
When eggs or oocysts were required for individual culture, Method 4 was employed. The coverslip was removed from the mouth of the centrifuge tube, and turned over quickly. Eggs or oocysts were located microscopically in the fluid adhering to the coverslip and were transferred by a fine pipette to a staining block. The sodium chloride solution was washed away and the eggs or oocysts mounted in hanging-drop preparations and cultured.
To illustrate the intensity of infestation with Ascaris suum, egg counts were made using the technique recommended by the National Veterinary Medical Association of Great Britain (Anthony, 1946). Three grams of faecal material, either from the rectum or collected as droppings, were weighed out and placed in a glass-stopered bottle containing about ten glass beads. Forty-two cc. of water were added to the bottle, the stopper secured in place and the contents shaken until all the faecal material had been broken apart. By filtering the mixture the larger particles of debris were removed and the filtrate was retained in a flask. The larger particles of debris were discarded and the strained fluid shaken to obtain a uniform suspension of eggs. 0.15 cc. was removed with a pipette and placed on a microscope slide, covered with a ⅞ inch square cover glass, and the eggs present in that volume of liquid counted with the aid of a hand tally counter. The number of eggs obtained was multiplied by 100 to give the number of eggs present in one gram of the original faecal sample.
An experiment was carried out to show the egg production cycle of Ascaris suum. The faecal material was obtained three times daily for 7 days from wild pig No. 4 held in captivity. One gram of the sample was ground apart in water and the mixture made up to 50 cc. in a measuring cylinder. Ten cc. of this was diluted to 40 cc. and the cylinder shaken thoroughly to ensure an even distribution of eggs. Using a pipette some of this fluid was transferred to a McMaster's egg-counting slide, and eggs were counted in known areas on both sides of the slide and the average number of eggs estimated for a known volume of fluid. Where necessary, for example if results from individual samples varied widely, counts were repeated.
To test the viability of eggs under dry conditions, faeces containing eggs were dried by blowing warm air over them with an electrically driven pump. This air was warmed by being forced through spiral glass tubing immersed in water at a controlled temperature, and was conveyed through delivery tubing to a piece of combustion tubing in which the faecal sample was spread out. The sample was constantly broken apart and more air passed through until dry. Ascaris eggs were readily obtained from the dried faecal sample, for observation, but stomach worm eggs could not be recovered.
The viabilities of helminth eggs were further investigated. Eggs were cultured on microscope slides, in moist faecal samples and in hanging-drop preparations at low temperatures of -5.0 to 2.0°C, at room temperatures of 12.3 to 24.7°C, and at 37.0°C. To observe sporulation, oocysts were mounted in hanging-drop preparations maintained at room temperatures of 17.6 to 19.4°C. An attempt was made to determine the viability of lungworm eggs from their reaction to 1/1,000 aqueous solution of eosin, on the assumption that if they stained, the embryos would be dead. The reaction of eggs to the stain was not sensitive enough, and the experiment was abandoned.
To test the effect of presence or absence of oxygen on the development of Ascaris eggs, a faecal sample containing eggs was placed in a glass-stoppered bottle, covered with freshly boiled water, and sealed. A portion of the same faecal sample was exposed to the air and kept moist as a control, and eggs from it were examined periodically for development. Both cultures were maintained at room temperatures of 10·9 to 21·6°C.
Earthworms from wild pig rootings, or as near to the rootings as possible, were collected from some of the wild pig infested areas visited. In the láboratory these earthworms were anaesthetised with a 2% aqueous solution of urethane, or killed with 70% alcohol, and the oesophagus and anterior circulatory system dissected out and removed. This material was teased apart and examined for lungworm larvae.
In order to investigate the life history of the lungworms Metastrongylus elongatus and Choerostrongylus pudendotectus, eggs of these species were added to four cultures of earthworms in petri dishes. The first three cultures each contained six earthworms, and the fourth culture contained three earthworms. Eggs for cultures Nos. 1 and 2 were obtained by chopping up adult worms of M. elongatus and C. pudendotectus. Earthworms exposed to eggs of M. elongatus and C. pudendotectus were transferred to soil free from lungworm eggs one day and three days after the seeding of their respective cultures. Adult female worms of both species were held in Ringer's solution at 37·0°C for three days. Eggs laid were placed on earthworm culture No. 3. Eggs for culture No. 4 were obtained by chopping up together adult female lungworms of both species. Earthworms of the last two cultures were held throughout the experiment in the soil to which the lungworm eggs had been added.
Balantidium coli Malmsten, 1856.
Infestations were recorded in 13 (61·9%) of the 21 wild pigs and in 10 (40%) of the 25 domestic pigs examined throughout the length of the alimentary canal. Two of 40 wild pig faecal samples contained cysts of B. coli. The trophozoite invariably parasitised the caecum. Frequently the large intestine together with the caecum was parasitised, but the numbers of animals in smears from the intestine were not as high as those from the caecum. Although numerous trophozoites were seen in caecal smears, often cysts were not present in rectal smears from the same pig, thus indicating that trophozoites encyst periodically.
The higher number of infested wild animals is possibly connected with the age factor, as a greater number of older wild pigs were examined and they would have had longer time therefore to acquire infestations. B. coli does not seem to have been previously recorded from pigs in New Zealand. While frequently reported in the literature from elsewhere it seems little attention has been paid to the incidence of this parasite in pigs. O'Connor (1923) records B. coli as occurring exclusively among the pigs of Samoa.
Eimeria debliecki Douwes, 1921.
Of 21 wild pigs examined, only one (4·7%) was infested Of 25 domestic pigs examined, 17 (68%) pigs were infested. Oocysts were not recovered from 40 wild pig faecal samples. The intensity of infestation was usually heavy, and when each 1 gram of faeces was treated by a slightly modified Lane's (1928) direct centrifugal flotation technique hundreds of oocysts were obtained on the first
coverslip. Biester and Murray (1929) have shown that after the initial infestation the number of oocysts passed in the faeces gradually decreases until few oocysts might be found on some days and negative findings on others. Therefore domestic pigs being closely herded together would have a greater chance of acquiring new infestations which would result in the continuous production of high numbers of oocysts.
Workers record the percentage of infestations of coccidia of swine as being high among most of the animals examined. Noller and Otter (1921) in Germany state 75% of pigs are infested. Munnik (1924) reports that 58% of swine in the Netherlands are infested. Coccidiosis occurs among 45·4% of some of the groups of swine in Russia, according to Yakimoff (1926 and 27). The above figures have been obtained from Biester and Murray (1929). Kauzal (1930) lists 54% of swine in New South Wales as being infested. Henry (1931) records 82% as being infested in America, while from the same country Spindler (1942) reports coccidiosis as probably the most important protozoan disease of swine.
Anaplasma Thelier, 1910.
Anaplasma-like bodies were present in 1 (6·6%) of 15 wild pigs and in 7 (70%) of 10 domestic pigs examined. All bodies lay within the red blood corpuscles. It could not be established that they occurred free in the plasma, although this has been reported previously by Gilruth (1909). In each half hour examination, the number of erythrocytes seen containing these bodies ranged from five to thirty. The higher percentage of infestation among the domestic animals my be due to the blood smears being secured from one series of pigs at slaughter rather than from random sampling. The pigs from which the smears were taken therefore had been in close association with one another, and possibly bred on the same farm.
Similar bodies have been described from pigs in New Zealand by Gilruth (1909). Porter (1915) states that anaplasma-like bodies probably have more than one origin. One such origin would be from the nucleus of the developing erythrocyte or erythroblast under the influence of haemolysis. Many infestations have been reported from apparently healthy pigs, but there seems to be nothing in the literature on the infestation rate for this “organism.”
Cysticercus tenuicollis Rudolphi, 1810.
Of 21 wild pigs examined 1 (4.7%) was infested. This animal had been kept in captivity for 3 months, and probably became infested during this period, since it was the only wild pig infested with C. tenuicollis and precautions were not taken to avoid such infestation. Of 59 domestic pigs examined, 30 (50.8%) were infested. This larval stage of Taenia marginata was commonly located on the great omentum and liver of the host. Heart, lungs, diaphragm, intestines, mesenteries and the wall of the abdominal cavity were other but less common locations.
The absence for the most part of the primary host, the dog, from the habitats of the wild pig, explains then the absence also of the bladderworm from these wild animals. However, hunters do take dogs into wild pig areas, and there is always the possibility of pigs acquiring infestations from infested pig-hunting dogs. The coprophagus habit of pigs favours the high occurrence, and the feeding of animal offal infested with C. tenuicollis to farm dogs, together with the close association of domestic pigs and dogs, also favours the occurrence as well
as the dispersal of this parasite. Rosen (1951) reports on the presence and absence of this parasite correlated with the presence and absence of the primary host. Although 90% of deer on the mainland of California were infested with bladderworm, deer on the neighbouring Santa Catalina Island were not infested. The deer had been transferred to this island from the mainland 20 years previously, and due to the absence of the coyote on the island the life cycle was broken so that the parasite was eliminated.
Roberts (1934a) records this parasite as being very common in sheep, and to a lesser extent in cattle and pigs, in Queensland. According to Whitten (1949), this is also the case in New Zealand. Young (1938) had listed the presence of this parasite in this country, and the New Zealand Medical Research Council Hydatid Bulletin (1938) lists it as present chiefly on the omentum, and also in or on the liver. According to Seddon (1950), Tinney (unpublished) in 1948 found 3.4% of 2,861 pigs infested in Victoria. Spindler (1951) records cystic tapeworms as being comparatively rare in pigs in America, or they have attracted little attention.
Echinococcus granulosus Batsch, 1786.
All of the 21 wild pigs examined were free of this parasite, and only 5 (10%) of 50 domestic pigs were infested. During this survey, cystic stages of E. granulosus were located deeply embedded in the liver, lungs and spleen of pigs. All cysts seen were sterile or degenerate, and in the absence of hooks or other characters were assigned provisionally to the above species.
The factors affecting the distribution and occurrence of E. granulosus are the same as those for C. tenuicollis. However, whereas the latter is relatively fast-growing, E. granulosus is regarded as slow-growing. Therefore the early ages of the domestic pigs examined would account for the low figure of infestation. It is likely that a higher number of animals was parasitised and that infestations were not recognised due to the developing cysts being deeply embedded in the host organs. Within this young age group, cysts were not large, and all those observed were sterile. Fairely and Penrose (1928) found the disease to be exceedingly uncommon in pigs under the age of 3 years, and that degenerate cysts occur frequently. They report an average infestation rate of a series of examinations of pigs in Victoria as 5%. According to Ross (1929), Cleland (1908) records 0.75% of 6,253 pigs infested in Australia, but Roberts (1934a) reports the parasite as being common in the liver and lungs of pigs in Queensland. E. granulosus has been listed as present in the pig in New Zealand, Young (1938). Whitten (1946) states that the incidence of hydatids increases with the age of the animal, and that 30% of cysts are fertile in pigs in New Zealand. In 1949 this author records hydatid disease as being common, particularly in old pigs, and that massive infestations are not uncommon. The prevalence of hydatids recorded during this survey is then similar to that found by other workers in this country and also in Australia.
Fasciola hepatica Linnaeus, 1758.
Preserved specimens obtained from the bile ducts in the liver of the pig are of a brown colour, presumably having been stained with bile. Liver fluke was not present in 21 wild pigs examined, or in 75 rejected livers of domestic pigs. Furthermore, liver fluke eggs were not present in any of the 40 faecal samples from wild pigs or in faeces taken from the rectum of 25 slaughtered domestic
pigs. Preserved specimens of the parasite were obtained, however, from a meat inspector who stated that he had seen pigs infested with liver fluke in New Zealand.
The distribution of the parasite is determined by the distribution of the intermediate hosts. In the past, F. hepatica has been responsible for the loss of an enormous number of sheep. In England in 1830, 2,000,000 were lost, and in Ireland in 1862, 60% of the sheep died. Again in 1879, over 300,000 sheep were lost in England. These figures have been obtained from Fantham et al. (1916). Recent workers in other countries record this parasite as occurring in only small percentages of the animals examined. Roberts (1934a) reports that F. hepatica has been collected on two occasions from the pig in Queensland. Diáz Marín and Irigoyen Ramírez (1951) record Fasciola present in 2% of pigs in Morocco. Spindler (1951) states that liver fluke is comparatively rare in pigs in America, or has attracted little attention. Whitten (1945) records the parasite in sheep, cattle and goats in fairly limited areas in New Zealand, but it does not seem to have been recorded previously from pigs in this country.
Hyostrongylus rubidus (Hassall and Stiles, 1892) Hall, 1921.
Six (28.5%) of 21 wild pigs examined, and 12 (48%) of 25 domestic pigs examined were infested with H. rubidus. Adult worms were usually located in the stomach of the host. One worm, however, was found in the scrapings from the duodenum of one pig, and 3 worms were found in the scrapings from the jejunum of 2 pigs. Approximately uniform areas, about 5 square inches, were scraped from the stomach of pigs examined. The highest number of worms recorded from one pig was 82, 25 of which were males and 57 females.
Ova recovered from faeces taken from the rectum of slaughtered domestic pigs were in an 8 to 16 cell stage. Further development was observed in hanging-drop preparations.
At low temperatures of 0.2 to 2.0°C, ova underwent further divisions, but except in one egg no embryo stage was reached. At room temperatures of 19·6 to 22·5°C, ova developed from the 8 or 16 cell stage to the fully formed motile embryo within 36 hours. Larvae hatched from some of these eggs, their survival time varied between one and three days, and they did not undergo ecdysis. When held at 37.0°C, ova underwent further divisions but did not reach the embryo stage. On removal from the frigidaire and oven to room temperatures of 17·3 to 22·5°C, ova did not recommence development.
The incidence of infestation is significantly higher among the domestic group. The difference may be due to the developing ova being more viable or the larval stages having a higher survival rate in the shelter of a pig sty than when exposed to a wide range of climatic conditions. Ova did not develop under extremes of temperature or survive drought. In hanging-drop preparations first-stage larvae appear to be structurally delicate and sensitive to the surrounding media. Alicata (1935) found that third-stage larvae were not very resistant to low temperatures or dry surroundings but would survive 2½ months in water at room temperatures.
Kauzal (1930) reports an infestation in New South Wales which was not higher than 8%. Clay (1938) found 52.4% of pigs in North Queensland infested with H. rubidus but Roberts (1940) recorded 37% of pigs in Queensland to be infested. Spindler (1942) states that this parasite occurs in 15% to 35% of
pigs in one section of U.S.A. The only earlier reference to stomach worm in New Zealand is that of Whitten (1949) who reports that it is a common infestation among pigs. The incidence of infestations among both groups of pigs obtained during this survey, then, falls within those obtained by workers in other countries.
Ascaris suum Goeze, 1782.
Nine wild pigs out of 21 were infested with A. suum. Of 1,025 domestic pigs examined, 13 were infested. Eggs of A. suum were present in 14 out of 40 faecal samples from wild pigs. The numbers of parasites harboured by the wild animals were usually higher, ranging from 2 to 37, compared with 1 to 3 in domestic pigs.
Material from wild pigs was examined more conveniently. In some of these pigs, worms were often located spread over areas of the small intestine. In other animals they were found bunched together and even doubled back upon themselves, thus almost blocking the canal. When the worms were first ejected from the intestine, they made slow movements from side to side.
Young pigs seemed more susceptible to infestation than old ones. Six of the nine infested wild hosts varied in age from about 1 to 4 months, two of the other three wild pigs were not quite fully grown, and the third was fully grown. Intensity of infestations were highest among young pigs. Immature specimens of A. suum were located in the small intestine of 2 wild pigs about 1 and 2 months old, but not one immature worm was found infesting older wild pigs, or any domestic pigs. Martin (1922 and 26) records similar observations and states that both young and old pigs are exposed to a similar amount of contamination, but that young pigs must be more susceptible to infestation.
Heavily infested pigs were in extremely poor condition. These animals showed signs of being stunted in growth and their bodies were thin and hair covering sparse. One wild pig about 3 to 4 months old was found to be infested with Ascaris when caught. This animal was held in captivity for 3 months. During that time it did not grow noticeably, coughing was frequent, and vomiting occurred on two occasions. Coughing could have been caused by Ascaris larvae migrating through the lungs, however, lungworms were also present. Vomiting could have been caused by obstruction of the intestine with worms, but when the animal was killed, only 12 specimens of A. suum were removed from the small intestine.
Viability Of Eggs
Every fertilised ovum seen in fresh faeces was undivided, and eggs for viability experiments were obtained therefore from faecal samples. The viability of eggs was tested under varying conditions of temperature and moisture, and the development to the active embryo stage was taken as a criterion of favourable conditions when seeking to determine the effects of topographic and climatic conditions upon survival.
Development in Dry Surroundings
In dry surroundings Ascaris ova remained viable for at least 40 days at low temperatures of 0·8 to 0 °C, because these ova developed when removed to room temperatures, and for at least 38 days at room temperatures of 17.3 to 24·7° C. They did not develop under extremely dry conditions such as obtained on glass
slides held at room temperatures of 14.4 to 22.5°C, or when held at 37·0°C. Similar results have been obtained by other workers. Martin (1926) observed that development of ova was slow at room temperatures and at very low temperatures the eggs may be killed. Although he kept ova in dry surroundings at -5.0 to 10.0°C for 25 months, development commenced when removed to warmer temperatures. Ross (1916) had found previously that the moisture requirement for the development of Ascaris ova was slight. He placed ova of A. lumbricoides on slides, exposed them to the sun, and found active embryos developed in 6 weeks. However, Roberts (1934b) states that ova in faeces exposed to the sun die if the faeces are allowed to dry out. Spindler (1940) states that undeveloped eggs both in water and when dried were less resistant to the effects of sunlight than fully developed eggs. It was also found by Jaskoski and Egan (1953) that aged, cleaved and motile embryonated eggs were less resistant to the ovicidal effect of detergent than fresh eggs.
Ova did not develop when held at temperatures of 37.8 to 38.8°C in dry surrounding for one week. Ransom and Foster (1920) incubated Ascaris eggs at 37.0°C until they dried out thoroughly. There was no further development after these eggs were moistened and transferred to a lower temperature.
Development In Moist Surroundings
Development did not take place with ova in moist faeces held at low temperatures of -1.5 to 1.0°C, but commenced when the ova were removed to warmer temperatures. Similar observations were made by Cram (1924) on the development of fresh Ascaris ova at low temperatures. He held these eggs at temperatures of -16.6 to -8.8°C for 40 days, and it was not until the eggs were removed to 24.0°C that embryos developed.
Development of ova in moist faeces held at room temperatures of 14.4 to 24.7°C was retarded until the faecal sample lost some of its moisture content. Numerous other workers have cultured eggs at room temperatures, and some have experimented with culture media. Alicata (1935) held eggs at room temperatures of 22.0 to 24.0°C in a 1% formalin solution, and eggs became embryonated 28 days after the culture was commenced. He found that ova developed quickest at about 33.0°C. Martin (1913) observed the optimum temperature for the development of ova to be about 33·0°C. Ransom and Foster (1920) cultured eggs at temperatures ranging from 33·0 to 34·0°C in a solution of 2% formalin. Eggs contained motile fully developed embryos after 10 days. Alicata (1935) incubated eggs in a 1% solution of formalin held at 33.0°C and fully developed embryos were observed after 12 to 15 days.
Even 7 months after becoming embryonated, Ascaris eggs in moist surroundings were seen to contain motile embryos. Embryos within eggs left in dried faeces for this length of time showed no signs of life. Roberts (1934b) states that eggs are viable for 28 months on moist soil. Davaine (1858), who first observed the developmental stages of ova of A. lumbricoides, claimed that eggs were still viable after 5 years.
Ova in moist faeces did not develop at 37.0°C. However, Martin (1913) cultured eggs at 38·0°C and he found that segmentation was extremely slow and irregular, with only one third of the eggs reaching the 2 blastomere stage. The ova then died.
Development Of Ova In Hanging-Drop Preparations
Ova were cultured at three temperature ranges, -5·0 to 0°C, 12.3 to 19.4°C and at 37.0°C. Ova did not develop past the 2 cell stage. Yet Wharton (1915a), also using tap water, observed that ova of A. lumbricoides in hanging-drop preparations develop as well as when exposed to the air.
Development Of Ova In The Absence Of Oxygen
Ova covered with water devoid of oxygen showed signs of inhibited development. However, in the presence of oxygen and under other favourable environmental conditions, the same ova later developed to the motile embryo stage. Oxygen is therefore necessary for the normal development of Ascaris ova. As early as 1885, Hallez had shown this. Ransom and Foster (1920) observed that ova did not develop when covered with water in a stoppered bottle. Wharton (1915a) states that ova placed in boiled water and covered with a film of oil failed to develop, but when these eggs were transferred to fresh water development commenced.
Results Of Egg-Counts From Faecal Samples
Using the technique recommended by the National Veterinary Medical Association of Great Britain, the numbers of eggs of A. suum per gram of faecal samples were estimated. Faecal material was obtained from the rectum of slaughtered wild pigs, and as droppings collected from wild pig habitats.
Table 1 lists, where possible, the numbers of eggs obtained in three counts and the averages of these three results, against the numbers of worms present in the small intestine of 9 wild pigs.
[The section below cannot be correctly rendered as it contains complex formatting. See the image of the page for a more accurate rendering.]
|Wild pig Nos.||Nos. of eggs per gram of faecal samples||Averages of the three counts||Nos. of worms present|
|13||No count obtained||—||1||1|
|17||No count obtained||—||2||1|
The lowest average number of eggs per gram of an original faecal sample was 470, and the highest 69,000. In the animal from which the former results were obtained, 5 mature female worms were present, and in the animal from which the latter results were obtained only 4 mature female worms were present. This indicates either that there is great variability of egg production, or that there are periods when worms do not lay eggs. Counts were not secured from wild pig No. 13 in which only 1 female worm was present, or from wild pig No. 17 because the worms had not yet reached maturity. In wild pig No. 14 only 8 of the 22 female worms were mature. The numbers of worms present in the small intestine of wild pigs Nos. 19 and 22 could not be estimated owing to shortage of time when in these wild pig areas.
Table 2 lists the numbers of eggs obtained in three counts and the averages of these three results for each of the 9 faecal samples. Samples 2 to 17 are from Marlborough Sounds and samples 20 and 21 are from the Whakararas, Hawke's Bay.
[The section below cannot be correctly rendered as it contains complex formatting. See the image of the page for a more accurate rendering.]
|Faecal sample numbers||Numbers of eggs per gram of faecal samples||Averages of the three counts|
The lowest number of eggs per gram of an original sample was 330, and the highest 17,100. As with counts obtained from faeces taken from the rectum of wild pigs, the number of eggs present in each sample varied widely.
Fertility of Eggs of A. Suum
Owing to their different appearance, fertile and infertile eggs were distinguishable. Percentages of fertile eggs in faeces from the wild pig held in captivity were estimated over a period of 8 days. Two counts were made from each sample and were obtained by use of the McMaster's egg-counting slide. Results are shown in Table 3.
[The section below cannot be correctly rendered as it contains complex formatting. See the image of the page for a more accurate rendering.]
|Date||Percentages Fertile||Percentages Infertile|
In the above results, an average of 11·5% of the eggs examined were infertile. Eggs in the faecal samples from the wild pig were cultured and after an interval of 7 months examined for embryos. Only 9.3% of the eggs did not contain embryos.
According to Alicata (1935), Otto (1932) states that 15.9% of the eggs he examined were infertile.
Egg-Production Cycle of A. Suum
An experiment was made to investigate the egg-production cycle of A. suum Morning, afternoon and evening stools were obtained for 7 days from the captive wild pig. Results of these egg-counts are shown in Table 4, and a graph illustrating the cycle of egg-production has been prepared (Graph 1).
During the week, three peak periods of high egg-production occurred. The curve obtained by plotting egg-counts from the interior of stools approximately resembles that obtained from egg-counts from the exterior of stools. However, eggs were almost always present in greater numbers on the exterior portion of stools. This may have been due to the mucous coating around stools retaining eggs, or to the mechanism of stool formation. Egg-counts from the interior and exterior of each stool were identical or similar in only three cases.
Egg-production gradually increased throughout the time that the pig was in captivity. However, this could have been the result of more worms reaching maturity. About one month after the data for this experiment had been secured the pig was killed, and 4 adult females and 8 adult male specimens of A. suum were present in the small intestine. No immature worms were seen.
Experiments Involving the Culture in Vitro of Adult Specimens of A. Suum
Worms secured from the small intestine were brought from the slaughterhouse to the laboratory in Ringer's solution heated to host temperature, in a vacuum flask. Thirty-six adult specimens, 26 females and 10 males, were cultured in vitro; 12 in Ringer's solution, 12 in Tyrode's solution, and 12 in Baldwin and Moyle's culture fluid. The cultures were replaced with fresh solution and the worms observed every 12 hours. A graph has been plotted illustrating the survival period of these worms in the three solutions (Graph 2).
|Date||Weights of morning, afternoon & evening stools.||Morning Stools||Afternoon Stools||Evening Stools|
|4/6/52||50, 36 & 48 gm.||(1)||27.30||10,20||(1)||31,30||21,21||(1)||30,33||22.20|
|5/6/52||44, 35 & 45 gm||(1)||27,27||12,14||(1)||12,23||11, 8||(1)||17,17||12,12|
|6/6/52||27.32 & 50 gm||(1)||24,19||31,17||(1)||38,35||29,27||(1)||33,22||16,22.|
|7/6/52||49 & 42 gm||(1)||30,12||35,33||No stool was passed||(1)||26,26||27,13|
|8/6/52||57, 26 & 51 gm.||(1)||47·47.||35,35||(1)||58,54||34,21||(1)||39,39||30,32|
|9/6/52||18, 49 & 18 gm||(1)||33,34||29,20||(1)||29,36||20,36||(1)||32.33||44,45|
|10/6/52||59, 51 & 39 gm||(1)||49,50||31.32||(1)||21,17||31,20||(1)||30,32||25,35|
Most of the worms survived 4 to 8 days in the three culture media. The shortest period a worm survived was half a day, and the longest was about 17 days. Males and females survived for the same length of time, and the presence of glucose in Tyrode's solution did not increase the survival period. Worms exhibited weaving and coiling movements which gradually decreased in intensity, towards death of the animals. These movements were most vigorous on the addition of fresh culture fluids.
The culture in vitro of Ascaris has been undertaken by many workers Wharton (1915) kept Ascaris of man alive in Kronecker's solution from 5 to 12 days at temperatures ranging from 25·0 to 35·0°C. Hall (1917), at temperatures
of 27·5 to 30 0°C, kept pig Ascaris alive for 14 and 15 days in physiological salt solution and for 26 days in Kronecker's solution. Hobson (1948) kept Ascaris alive for 28 days in 30% sea water. In their culture fluid maintained at 38 0°C, Baldwin and Moyle (1947) kept Ascaris alive for 4 to 12 days. They state that starvation does not in all likelihood cause death of the worms. The cause of death is unknown.
During the experiment, worms in Ringer's solution and Baldwin and Moyle's culture fluid changed from their normal yellowish-pink colour to yellowish-white. The posterior end of the animals usually changed colour first. The new colour gradually worked towards the anterior end of the animals. If the worms survived long enough, the areas which had first changed colour became opaque and the muscular body lining usually became separated from the cuticle. In Tyrode's solution, however, they retained their natural colour for longer periods than worms in the other two culture media. Colour changes similar to the above have been noted by Laser (1944).
Egg production of 5 worms, Nos. 25, 26, 32, 34 and 35, were observed during the culture in vitro, and egg-counts were obtained. The results indicate a cycle of production and that the number of eggs laid decreases towards death of the animals. Worms Nos. 25 and 26 did not lay during the first 4½ hours in vitro, and when production did commence eggs were infertile, being normal in shape but with the contents completely filling the shell. Some of the eggs adhered together as though they had been passed out in chains. Eight days later, some eggs from worm No. 26 lacked the albuminous coat, and in other eggs this coat was very thin. Eggs from worms Nos. 32, 34 and 35 were fertile. In 34 and 35 most of the eggs were spherical and lacked an albuminous coat after 1 day in vitro. In worm No. 34 the albuminous coat was thin after 1 day and absent from most eggs after 2 days. Eggs from this worm were normal in shape. Wharton (1915b) made similar observations on the presence of the albuminous coat of eggs laid by A. lumbricoides cultured in vitro.
A. suum occurred in significantly greater numbers of wild pigs (42.8%) than in domestic pigs (1·2%), and the intensity of infestation was also greater in the wild animals. It is difficult to account for these widely varying incidences. The roaming habits of wild pigs would help spread the parasite among this group. However, the crowding together of domestic pigs should increase the chances of acquiring an infestation, and therefore result in a greater incidence. The results of the examinations do not indicate this at all. Furthermore, most of the domestic pigs examined were about 6 months old and most of the wild pigs examined were older and thus had more time to acquire infestations. However, it has been established by Ransom and Foster (1920) that the highest percentage of parasites occurs among 2½ to 5 months old pigs, and that beyond 5 months the percentage of infestation gradually decreases.
Roberts (1934b) states that eggs die if subjected to drying by the sun. This observation offers one explanation for the low percentage of infested domestic pigs because ova in faeces lying in open paddocks might be killed, or faeces might be removed if in shelters, but in areas covered with bush or scrub faeces would not be subject to desiccation so quickly, and not to such an extreme degree. Therefore the probability of ova developing would be greater in wild pig areas. This is in agreement with the high percentage of infestation found among wild pigs.
Many workers have found that ova of A. suum are viable under most environmental conditions. Observations made during this survey also prove the survival of these ova under varying conditions of temperature and humidity, and in the absence of oxygen.
Administration of anthelmintics to domestic pigs would lower the percentage of Ascaris infested animals, but wild pigs naturally would not be subjected to this treatment. The results obtained from the wild group, then, may give a truer indication of the incidence of this parasite in New Zealand.
Incidences of the parasite in other countries vary widely, but are much higher than those obtained from the domestic pigs in this country. In Wiltshire, England, Stewart (1921) found that 16.75% of the pigs examined were infested with Ascaris. In Wales, Jones (1926) records 52.6% of pigs infested. O'Connor (1923) observed Ascaris ova several times in the faeces of Samoan pigs. In New South Wales, Australia, Kauzal (1930) found 32% of pigs infested, but in Queensland, Roberts (1940) reports 19.9% of pigs examined to be infested. In Russia, 52.9% of pigs examined by Chilimoniuk (1951) were parasitised, and in Germany, Sprehen (1951) records 11.53% of pigs examined to be infested with Ascaris. The highest incidence in any country is that recorded by Spindler (1951) who states that 74% of pigs in U.S.A. harbour Ascaris. Young (1938) lists the presence of the parasite in New Zealand, and Whitten (1949) states that it occurs less frequently than is often thought in domestic pigs in this country. The incidence of A. suum among domestic pigs examined during this survey supports Whitten's statement, but differs significantly from those obtained by workers in other countries.
Trichuris suis (Schrank, 1788) Smith, 1908.
None of the 21 wild pigs examined were infested. Of 25 domestic pigs examined, 5 (20%) were infested. Eggs of T. suis were not present in any of the 40 faecal samples from wild pigs. It is difficult to explain the absence of T. suis from wild pigs. Infestations might have been found if more animals had been examined Most workers in other countries do not record very high incidences. O'Connor (1923) observed Trichuris ova several times in the faeces of Samoan pigs. In North Wales, Jones (1926) found 10.5% of pigs examined infested. Kauzal (1930) records T. trichiura occurring in 6.9% of pigs examined in New South Wales, and Roberts (1940) reports an incidence of 15.6% among pigs examined in Queensland, Australia. Infestations occur among 23% of pigs in South-eastern States of America, according to Spindler (1942). The highest incidence seen is reported by Chilimoniuk (1951) who found 82.3% of pigs infested during one examination in Russia. Young (1938) lists the presence of T. suis, and Whitten (1949) records T. trichiura as being common among pigs in New Zealand.
Confusion exists in the literature over the morphological differences of Trichuris suis of the pig, and Trichuris trichiura of man. Yorke and Maplestone (1926) recognised two distinct species. According to Chandler (1950), Schwartz concluded in 1928 that the whipworms of pig and man are identical.
Oesophagostomum dentatum (Rudolphi, 1803) Molin, 1861.
Three (14·2%) of 21 wild pigs examined were infested with O. dentatum, worms being recovered from scrapings of the large intestine All three pigs were secured from the Marlborough Sounds None of the 25 domestic pigs
examined were infested. Whitten (1949) reports O. dentatum as being uncommon in New Zealand. The incidence also approximates some of those obtained by workers in other countries. Jones (1926) found 10·5% of pigs in North Wales infested. In New South Wales, Australia, from a series of examinations in different areas, Kauzal (1930) records 12%, 15% and 20% of pigs infested. In Queensland, Roberts (1940) reports 31·2% of pigs infested. According to Spindler (1942), nodule worms are perhaps the commonest of the worm parasites of swine in America. O. dentatum was found to occur among 48·7% of pigs examined in Germany by Sprehen (1951). Young (1938) records the presence of this parasite in New Zealand.
Culture of Ova of O. dentatum
Ova which were in various stages of development but had not reached the embryo stage were placed in hanging-drop preparations and held at room temperature of 21·5°C. Within 24 hours eggs contained immotile embryos.
Globocephalus urosubulatus Alessandrini, 1909.
Only 1 of 25 domestic pigs examined was infested, and none of the 21 wild pigs were infested. Adult worms were obtained from the scrapings of an area of the small intestine. The rare occurrence of this parasite in New Zealand has been noted previously by Whitten (1949). O'Connor (1923) has recorded this parasite present in Samoa.
Metastrongylus elongates (Dujardin, 1845) Railliet and Henry, 1911; and Choerostrongylus pudendotectus (Wostskow, 1905) Skrjabin, 1924.
Two species of lungworm, M. elongatus and C. pudendotectus, infest both the wild and domestic pigs in New Zealand. Seventeen wild pigs out of 21 examined for lungworm were infested. Of the seventeen, 14 were infested with M. elongatus, 8 with C. pudendotectus, and 5 were infested with both species. Of 50 domestic pigs examined for lungworm, 14 were infested; 13 with M. elongatus, 8 with C. pudendotectus, and 7 with both species. Lungworm eggs were found in 11 of 40 wild pig faecal samples. Ten samples contained eggs of M. elongatus, 2 contained eggs of C. pudendotectus, and one contained eggs of both species. A total of forty-five earthworms of several species collected from most of the wild pig areas visited were examined for the presence of lungworm larvae. None were infested.
Pale rectangular areas extending inwards from the edges of the lobes of the lungs indicated lungworm infestation. When the animals were heavily infested these patches were spread over a greater part of the surface of the lung. Adult worms were located in the bronchioles, bronchi, and in the trachea in one case only, but numbers were greatest nearest the edges of the lobes of the lungs. The lung tissue in these areas was often harder than normal, and almost always paler in colour. By transecting these areas, worms could be seen frequently packing the air passages.
The age groups of the wild pigs examined varied from several weeks to years. Mature worms were found in a young pig only several weeks old. However, the intensity of infestation in this case was low. Conversely, some of the biggest and oldest wild pigs examined were heavily infested. Infested domestic pigs examined were mostly about 6 months old. In some groups of pigs the percentage of
infestation was high, in others it was low. For example, one of the 21 pigs examined during one day was infested, and 9 of 12 pigs examined one day several months after were infested.
Viability of the Embryos
When eggs were being secured for observation from an adult specimen of C. pudendotectus which had been cleared in aqueous glycerine and then mounted in glycerine jelly for 5½ months, embryos were seen to be active within some eggs. When forced out of the shells, several embryos were found to be ensheathed in the cuticle of a previous molt. This latter observation is in contrast to that recorded by Alicata (1935) who states that embryos do not undergo additional development before being ingested by an intermediate host. This author also claims that embryos do not hatch until ingested by a suitable host. However, embryos which had hatched in the absence of an intermediate host were observed during this survey when adult lungworms were cultured in vitro. Towards the end of their survival period, the body wall of worms ruptured and structures disintegrated. Numerous embryos apparently liberated from eggs while inside the female reproductive organs, appeared in the culture media. The presence of these “larvae” were first noticed in Ringer's solution held at about 30.0°C.
Development of the Larvae of M. elongatus and C. pudendotectus In Lumbricus rubellus And/Or Allobophora longa
The four cultures were maintained at temperatures which varied from 10.8 to 20.4°C. Motile first-stage lungworm larvae of M. elongatus were located within the earthworms, 60 hours after seeding culture No. 1. Seventy-two hours after seeding culture No. 2 motile first-stage larvae of C. pudendotectus were recovered from the teased out oesophageal and circulatory system of some earthworms. Ten days after the initial infestation of the earthworms, one was dissected and a first-stage larva was seen, the measurements of which exceeded those of the previously mentioned first-stage larvae of C. pudendotectus. One month after culture No. 3 was seeded with lungworm eggs of both species, lungworm larvae were recovered. The measurements of one larva approximated those obtained by Alicata (1935) for second-stage larvae of C. pudendotectus 15 days old. No lungworm larvae were recovered from earthworms in culture No. 4.
Earthworms for these experiments were obtained from the garden of a city dwelling. Unknowingly, two species, Lumbricus rubellus and Allobophora longa, were incorporated in this work. At the conclusion of the experiments it was found that six earthworms out of twenty-one became infested, a ratio of 1 to 3.5. Of twelve earthworms collected at random from the original source, four were specimens of L. rubellus and eight were specimens of A. longa, giving a ratio of 1 to 3. This ratio approximates the former, and indicates that earthworms of L. rubellaus became infested.
Culture In Vitro Of Adult Lungworms
Adult lungworms of both species, M. elongatus and C. pudendotectus, were cultured at room temperatures, 14·2 to 20.5°C, oven temperatures, 28.0 to 30.2°C, and at 37.0°C. The culture medium used in one series of experiments was Ringer's solution, and in another series Tyrode's solution. Twelve males and 12 females were placed in each petri dish, a total of 144 worms being observed during
the experiment. Observations were made and the culture media changed every 12 hours. Each series of experiments was repeated once. A graph has been plotted showing the survival time of the worms in Ringer's solution during one series of experiments (Graph 3). Tyrode's solution was also used because it was thought lungworms would be able to utilise glucose, one of its constituents, as food, and thus survive longer than those cultured in the physiological salt solution.
Lungworms exhibited weaving movements in the culture media, their activity being greatest at 37.0°C, and also were more active at all three temperatures when they were changed to fresh culture media. Towards death, movements became feeble, and the body wall of the lungworms, especially females, ruptured. Worms gradually lost their opaqueness and became semi-transparent. This may have been due to the utilisation and loss of body resources. A pythium-like fungus was noticed growing from some worms 7 to 9 days after the culture was started.
Results showed that the presence of glucose does not prolong survival in vitro; whereas the lungworms survived 10 days in Tyrode's solution, they survived 12 days in Ringer's solution. Worms survived longest at room temperatures and least when cultured at 37 0°C. This may have been due to food resources being utilised quickest at 37·0°C, due in turn to the increased metabolic rate. Death from starvation, therefore, would be earliest at the highest temperature. Both genera, and males and females of individual genera, survived for approximately the same length of time.
Intensity of Lungworm Infestation
Complete lungs were examined from 10 domestic pigs infested with lungworm. The percentage of males to the total number of lungworms present in each lung was estimated, and except for two instances males were present in lower numbers
than females (Graph 4). Lewis (1926) also found females to be more numerous than males, and a wide variation in the number of worms present, namely 5 to 407.
The percentage of infestation in the wild host was very much higher than in the domestic host. Of the wild pigs exammed, 80.9% were infested, but only 28% of domestic pigs examined were infested. Of the wild animals parasitised, 82.3% harboured M. elongatus, 47% C. pudendotectus, and 29.4% harboured both
|Lung Nos.||Total Nos. of Worms Present||Nos. of Males Present||Nos. of Females Present||% of Males|
genera. Among the infested domestic group, 92.8% were parasitised by M. elongatus, 57.1% by C. pudendotectus, and 50% by both species. Lungworm eggs were present in 27.5% of the faecal samples of wild pigs. Of that 27.5%, 90.9% of eggs were from the species M. elongatus, 18.1% were from the species C. pudendotectus, and 9.0% contained eggs of both species. Infestations with M. elongatus not only occurred more frequently than those of C. pudendotectus, but the intensity of infestation was also greater. Lewis (1926) found 50% of pigs examined in Central Wales to be infested with M. elongatus and M. brevivaginatus (M. brevivaginatus is a synonym of C. pudendotectus). He observed that generally both species were present in the lung together, and M. elongatus present in the greater number.
Both species of lungworm occurred in a signficantly greater number of wild pigs than domestic pigs, although favourable conditions for the spread of these parasites are common to both wild and domestic groups. Earthworms are distributed over most of this country, and Whitten (1949) reports that there is no available treatment in New Zealand to remove the adult worms from their final hosts. Therefore the infestations among pigs are natural. Kates (1941) determined that lungworm eggs have a marked resistance to continued low temperatures and a long survival in soil under favourable moisture conditions. Alicata (1935) states that several species of earthworms can act as intermediate hosts.
The higher percentage of infestation in the wild group can be correlated with the necesity for wild pigs to root more in the soil for their food. Therefore they
are more likely to eat earthworms harbouring infective lungworm larvae. Earthworms were observed among the stomach contents of several of the wild pigs examined. Schwartz (1936) says any measures which prevent pigs rooting will lessen lungworm infestation. He found that earthworms collected on hog-lots showed a high rate of infestation with lungworm larvae in various stages of development.
Climatic factors affect the survival of the embryonated eggs. Lungworm eggs in faeces from wild pigs, deposited in forested or scrub-covered areas, are not subjected to the drying and lethal effects of the sun's rays, whereas eggs in domestic pig faecal samples lying in open paddocks are exposed to extremes of the weather. Furthermore it is possible that domestic pigs are shifted regularly to avoid infested earthworms, or to allow the earthworms present to die off, or they may be kept in pens with concrete floors. According to Kates (1941), effective control measures would be to place pigs on well-drained pastures exposed to the sun.
Lungworm infestations of pigs in other countries have been reported by numerous workers as varying widely. Kauzal (1930) reports that 12% of the pigs examined in New South Wales were infested with Metastrongylids (2 species). Roberts (1940) found M. elongatus infesting the lungs of 3.7% of pigs, and C. pudendotectus in one pig only, in Queensland. Spindler (1942) reports lungworm as the most widespread of the parasites that infest swine. In South East America, he records 70% of swine to be infested, the two common forms being M. elongatus and C. pudendotectus. Díaz Ungría (1951) records C. pudendotectus infesting 60% and M. elongatus infesting 80% of the pigs examined in Venezuela. Young (1938) lists M. elongatus present in domestic pigs in New Zealand, and Whitten (1949) records M. elongatus and C. pudendotectus as being common in domestic pigs in this country.
Haematopinus suis Linnaeus.
Of 22 wild pigs examined for lice, 14 (68.1%) were infested, and the eggs of the parasite adhered to the hairs of another pig. Of 75 domestic pigs examined, 37 (49.3%) were infested. The intensity of infestation generally was greater among the wild group. Lice were located on the fore and hind quarters and in and especially behind the ears. Specimens were held at room temperatures ranging from 15.7 to 21 6°C. Most survived 2 days off the host.
A slightly higher percentage of wild pigs than domestic pigs was infested. The age factor does not seem to effect the incidence of this ectoparasite. Liee were observed on wild pigs about a few weeks old, presumably having been acquired from infested mothers, and they also parasitised some of the oldest wild pigs examined. Close grazing of pigs and bad sanitary conditions would favour high occurrence of these ectoparasites. Bedford (1932) has carried out experiments on the transmission of, and infestation with, ectoparasites. He found that as a result of improved conditions of the host, parasites were lost. Dietary deficiencies among the wild group might cause a lowered resistance of the host to infestation, hence the higher incidence among wild pigs. However, it is thought that wild pigs, having ready access to wallow holes and not being closely penned together, have a greater chance of ridding themselves of ectoparasites, or at least being freer of them.
The incidence of infestations among both groups agree with those obtained by other workers. Whitten (1949) states that H. suis is a very common parasite of domestic pigs in New Zealand. Wodzicki (1950) reports that most of the wild pigs in New Zealand, especially piglets and weaker animals, sometimes harbour considerable numbers of lice (H. suis).
Sarcoptes scabiel var. suis Gerlach, 1857.
Of 22 wild pigs examined for ectoparasites, only one (4.5%) was infested with Sarcoptes. The hair covering of this animal was thin and the hide was wrinkled and covered with prominent crusts of dead skin. The mange parasite was located under these crusts. Of 50 domestic pigs examined, 18 (36%) were infested. The area parasitised was mostly the skin within the ears. Female specimens were present in greater numbers than males among scrapings from the skin of most of the pigs infested. Specimens of Sarcoptes were held at room temperatures of 18.6 to 19.6°C. Most of the specimens survived 2 days away from the host. However, Imes (1942) claims that this parasite may retain its viability for four weeks or longer when away from the host, during mild weather.
Infestations with Sarcoptes occurred among significantly greater numbers of domestic pigs than among wild pigs. The incidence of this ectoparasite among both groups is in contrast to the incidence of H. suis among the same two groups of animals. However, the factors influencing the occurrence of this mange parasite would be the same as those influencing the occurrence of the louse. It is difficult, therefore, to explain the different incidences of both ectoparasites.
In America, Imes (1942) states that a large number of pigs are infested with Sarcoptes, and in New Zealand Whitten (1949) records it as occurring infrequently among domestic pigs.
Demodex phylloides Csokor, 1879.
Of 22 wild pigs and 50 domestic pigs examined, none were infested with D. phylloides. This parasite is recorded here from a piece of infected hide of a wild boar obtained from the Department of Parasitology, Wallaceville Agricultural Research Station.
Imes (1942) states that it is difficult to transmit this mange, and that many animals are apparently immune This possibly explains the absence of the parasite during this survey. It has been previously recorded from both wild and domestic pigs in New Zealand by Whitten (1949).
Fifteen species of parasites and an anaplasma-like body were recorded during this survey of wild and domestic pigs. Except for B. coli, E. debliecki and F. hepatica, Whitten (1949) records these parasites present in domestic pigs in New Zealand. The three exceptions mentioned do not seem to have been previously recorded from pigs in this country. Whitten also lists the presence of the kidney worm Stephanurus dentatus. and the thorny-headed worm Macracanthorhynchus hirudinaceus. Gilrnth (1909) reported the presence of anaplasma-like bodies in the erythrocytes of domestic pigs. H. suis and D. phylloides are the only parasites recorded previously from wild pigs in New Zealand.
Few workers have carried out complete surveys for domestic pig parasites in other countries, and there appear to have been no surveys for parasites of wild
pigs. However, there is an extensive literature on pig parasites of which the greater part comparises studies on individual species. The data presented in the latter have been compared, under the appropriate headings, with those obtained during the course of this work, and the incidence of some parasites among pigs of this and other countries varies widely. Two reasonably isolated groups of the same host in the one country are involved in this survey, and it is found here that the distribution and the incidence and intensity of infestation of parasites among both groups are influenced by different habits, environmental factors and the presence of other animals.
The habits of animals are largely influenced by the conditions under which they are reared. My observations and those of reliable hunters indicate that wild pigs in their natural habitat are clean animals. In well-established, small, piginfested areas covered with scrub or bush such as exist in parts of Marlborough Sounds, wild pigs apparently adhere to definite stooling areas. The use of stooling areas would tend to restrict the distribution of parasitic eggs and cysts passed in the faeces. However, this restricted distribution would be comparatively insignificant because wide-spread distribution of the parasites can be effected by the roaming habits of these pigs.
Close pennmg of animals and poor sanitary conditions should favour a higher incidence of nematode and protozoan infestations among domestic pigs than among wild animals. H. rubidus, E. debliecki and Anaplasma infested significantly greater numbers of domestic pigs examined, while T. suis and G. urosubulatus were restricted to this domesticated group. However, M. elongatus, C. pudendotectus, A. suum and B. coli parasitised a higher percetage of the wild pigs examined, and O. dentatum occurred only in the wild group. The intensity of infestation of A suum was also higher among wild pigs than among domestic pigs.
The higher incidence and intensity of infestation of A. suum may be explicable in terms of the viability of the ova under various climatic conditions. According to Roberts (1934b), Ascaris ova remain viable when sheltered from the sun, and thus faeces deposited in bush-covered areas are protected. It was found in the laboratory that ova also remain viable for several weeks when subjected to varying conditions of coldness and humidity. Even after reaching the embryo stage they are found to survive for several months under favourable conditions of humidity.
Wild pigs frequent wallow holes, and the absence of faeces within and around these holes was noted. As wild pigs have ready access to such mud baths, one would expect them to be freer of ectoparasites than domestic pigs If this is the case, close grazing of domestic pigs and the absence of wallow holes should result in a higher occurrence of ectoparasites among this group. This might explain the higher incidence of sarcoptic mange, but lice parasitised a slightly higher percentage of wild pigs and the intensity of infestation with ectoparasites among this group was also greater.
Generally, pigs are not very particular about the nature and condition of their food. Their diet is largely determined by availability. Furthermore, they are said to be coprophagus (Chandler, 1950); but faeces were not encountered among the stomach contents of any pigs examined. The habit of eating faeces, if those from dogs infested with the adult Taenia marginata are also involved, would explain the high frequency and often heavy intensity of infestation of the larval stage, C. tenuicollis, among domestic pigs. Since domestic pigs are usually milk-
fed and fattened for market as early as possible, their adequate food supply apparently allows them to acquire greater resistance than wild pigs to some parasitic infestations. Such almost certainly explains the low incidence of H. suis and A. suum among domestic pigs.
Wild pigs are forced to root more in the soil for food, whereas domestic pigs are supplied with food and have less occasion or need to root. Therefore chances of acquiring infestations by eating earthworms infested with infective lungworm larvae are greater among pigs of the wild group than among those of the domestic group. This can reasonably explain the occurrence of both species of lungworm, M. elongatus and C. pudendotectus, in significantly greater numbers of wild pigs.
The presence of other animals from which infestations are acquired, for example, primary or intermediate hosts, determines the distribution of some pig parasites. Dogs are in close association with domestic pigs but absent from, or only temporary intruders of the habitats of wild pigs. Hence the absence of E. granulosus and C. tenuicollis (except for the captive wild pig) from the wild pigs examined is not surprising. The absence of F. hepatica from the pigs of both groups examined is almost certainly due to the non occurrence of the intermediate molluscan hosts in areas where wild pigs were caught and areas where the domestic pigs examined were reared.
Allowance should be made for the possibility that some farmers employ anthelmintics to rid pigs of intestinal nematodes, and dipping to remove ectoparasites. Most of the sarcoptic infestations were in the ears, and it is probable that either the dipping fluid failed to cover the skin within the ears or that this region is a favourable site for infestation.
Finally, by far the greater majority of domestic pigs examined were about 6 months old. The age group of the wild pigs examined ranged from several weeks to years. Most of the animals of this group, then, had a longer time to acquire infestations, and this can be correlated with the higher incidence of some parasites. The young ages of the domestic pigs examined can be associated with the relatively low figure of animals infested with the slow growing cysts of E. granulosus. Ransom and Foster (1920) found that the highest percentage of intestinal infestation with A. suum is in pigs 2 ½ to 5 months old. Although 6 of 9 wild pigs infested with A. suum were under 5 months old, and therefore at the most susceptible ages for infestation, it seems that A. suum is more prevalent among wild pigs than domestic pigs.
Because of the system in operation of dressung the pigs at the slaughter house, individual animals could not be examined for all parasites, but it was possible to examine individual wild pigs completely, and the number of parasitic species and the intensity of infestation of some species were obtained. A small wild sow about 2 months old was parasitised with four species of nematodes–A. suum, H. rubidus, M. elongatus and C. pudendotectus; one protozoan—B. coli; and two ectoparasites—H. suis and S. scabiei Thirty-seven specimens of A. suum almost blocked the alimentary canal and the whole surface of the body of the animal was covered with sarcoptic mange. Both species of lungworms occupied many of the bronchi and bronchioles of the lung. If this animal had been released, it is extremely doubtful whether it would have overcome these intense infestations and survived. Although other wild pigs were infested by a variety of parasites, these were generally light infestations, and in the course of this study it became doubtful that parasites could exercise any significant control over the numbers of wild
pigs, even though it was apparent that several of the smaller wild pigs were stunted in growth.
Chandler (1950) states that civilization has diminished the variety and intensity of many human parasites, but for domestic animals, domestication and increasing concentration have meant increasing parasitization. This latter statement has been found to be true only with respect to certain parasites of domestic pigs. Other parasites occur in greater numbers among wild pigs.
Alicata, J. E., 1935. Early developmental stages of nematodes occurring in swine. U.S. Dept. Agric. Tech. Bull. 489.
Angus, G. F., 1847. Savage life and scenes in Australia and New Zealand. 2 vols. London, Smith, Elder & Co.
Anthony, D. J., 1946. Diseases of the pig and its husbandry. London, Baillière, Tindall & Cox.
Baldwin, E., and Moyle, V., 1947. An isolated nerve-muscle preparation from Ascaris lumbricoides. J. Exp. Biol. 23: 277–291.
Bedford, G. A. H., 1932. A synoptic check-list and host-list of the ectoparasites found on South African Mammalia, Aves and Reptiles. Rept. Vet. Res. S. Afr. (Pretoria) 18: 223–523.
Biester, H. E., and Murray, C., 1929. Studies in infectious enteritis of swine. IV. Intestinal coccidiosis J. Am. Vet. Med. Assn. 75: 705–740.
—— 1930. Ibid. V. Coccidiosis in swine, and studies on Eimeria debliecki and E. zurni. Ibid. 76: 624–627.
Chandler, A. G., 1950. Introduction to parasitology. New York, John Wiley and Sons, Inc.
Chilimoniuk, J., 1951. Obraz krwi prosiat w przebiegu zarobaczenia mieszanego. Medycyna Weterynaryjna 7 (1): 34–35.
Clay, A. L., 1938. A note on the prevalence and pathogenic importance of Hyostrongylus rubidus in pigs in North Queensland. Aust. Vet. Journ. 14 (5): 194–197.
Cook J., 1977. A voyage towards the South Pole and around the World. London. Printed for W. Straham & T. Cadell.
Cram, E. B., 1924. The influence of low temperatures and disinfectants on the eggs of the Ascaris lumbricoides. J. Agric. Res., Wash. 27: 167–175.
Davaine, C., 1858. Recherches sur le développement et la propagation du Trichocephale de l'homme et de l'ascaride lombricoide. Compt. Rend. Acad. de. Sc., Paris. 2: 1217–1219.
Diaz Marin, J., and Irigoyen Ramirez, A., 1951. Un nuevo caso de hallazgo copro-logico de huevos de Fasciola. Medicina Colonial, Madrid. 17 (2): 164–166.
Diaz Ungria, C., 1951. Estrongilosis broncopulmonar del cerdo en Venezuela. Memoirias de la Sociedad de Cicncias Naturales La Salle. 11 (29): 183–194.
Fairley, N. H., and Penrose, J. S., 1928. A survey of the incidence of hydatid disease in the heibivoia and poicines of Victoria. Aust. Med. Journ. 2: 640–644.
Fairley, N. H., and Wright-Smith, N. J., 1929. Hydatid infestation (Echinococcus granulosus) in sheep, oxen and pigs With special reference to daughter-cyst formation. J. Path. Bact. 32 (2): 309–335.
Fantham, H. B., Stephens, J. W. W., and Theobald, F. V., 1916. The animal parasites of man. London, John Bale, Sons & Danielsson Ltd.
Fell, H. B., Garrick, J. A. F., et al., 1953. The first century of New Zealand Zoology. Victoria University College Zoology Publications.
Gedoelst L., 1923. Le genre Metastrongylus Molin 1861. Bull. Soc. Path. Exot. 15: 622–630.
Gilruth, J. A., 1909. Contagious pneumonia in pigs (swine plague) associated with the presence of a haemoeba in the red blood corpuscles and blood plasma. 17th Rept. Dept. Agric. N. Z. 301–304.
Hall, M. C., 1917. The longevity of adult Ascarids outside the body of the host. Its bearing on anthelmintic treatment. J. Am. Med. Ass. 68: 772–773.
Hallez, P., 1885 Sur le développement des nématodes. Compt. Rend. Acad. d. Sc., Paris. 101: 170–172.
Henry, D. P., 1931. A study of the species of Eimeria occurring in swine. Univ. Calif. Publ. Zool. 36: 115–126.
Hobson, A. D., 1948. The physiology and cultivation in artificial media of nematodes parasitic in the alimentary tract of animals. Parasit. 38 (4): 183–227.
Imes, M., 1942. Mange of swine. U.S. Dept Agric. Yearbook of Agriculture, Keeping Livestock Healthy. 734–740.
Jaskoski, B. J., and Egan, T. P., 1953. Age resistance of swine ascarid eggs. Trans. Am. Micros. Soc. 72 (2): 179–184.
Jones, N., 1926. A preliminary survey of the nematode and cestode parasites of sheep in North Wales, October 1923 to September 1924. J. Helm. 4 (1): 31–35.
Kates, K. C., 1941. Observations on the viability of eggs of lungworms of swine. J. Parasit 27: 265–272.
Kauzai, G., 1930. A survey of the helminth parasites of swine in N. S. W. Aust. Vet. Journ. 6 (2): 51–56.
Laser, H., 1944. The oxidative metabolism of Ascoris suis. Biochem. Journ. 38 (4): 333–338.
Lee, Bolles, 1950. The microtomist's vade-mecum. London, J. & A. Churchill Ltd.
Lewis, E. A., 1926. Observations on the incidence of Metastrongylus brevivaginatus and Metastrongylus elongatus in pigs in Central Wales. J. Helm. 4 (3): 123–126.
Martin, A., 1913. Recherches sur les conditions du développement embryonnaire des nématodes parasites. Ann. d. Sc. Nat. Zool., Paris. Series 9. 18: 1–151.
Martin, H. M., 1922. The common intestinal roundworm of swine. Nebr. Agric. Exp. Sta. Circ. 17.
—— 1926. Studies on the Ascaris lumbricoides. College of Agriculture. Univ. Nebr. Agric. Exp. Stn. Res. Bull. 37.
New Zealand Medical Research Council, 1938. Department of Hydatid research and prevention. Bull. No. 2.
O'Connor, F. W., 1923. Researches in the Western Pacific. Mem. London Sch. Trop Med. 4 (4): 1–57.
Otto, G. F., 1932. The appearance and significance of the unfertilised eggs of Ascaris lumbricoides (Linn.) J. Parasit 18: 269–273.
Porter, A. 1915. On anaplasma-like bodies in the blood of vertebrates. Ann. Trop. Med. and Parasit. 9 (4): 561–568.
Ransom, B. H., and Foster, W. D., 1920. Observations on the life history of Ascaris lumbricoides. U.S. Dept. Agric. Wash. Bull. 817. 1–47.
Roberts, F. H. S., 1934a. Worm parasites of domesticated animals in Queensland. Qucenes. Agric. Journ. 41 (3): 245–252.
—— 1934b. The large roundworm of pigs, Ascaris lumbricoides L. 1758. Its life history in Queensland, economic importance and control. Dept. Agric. & Stock., An Health Stn. Bull. No. 1. 1940. The incidence, prevalence and distribution of the helminths infesting the lungs and alimentary tract of the pig in Queensland. Aust Vet. Journ. 16: 259–266.
Rosen, M. N., 1951. A noticeable absence of bladder worms in Catalina deel. Calif. Fish & Game. 37 (2): 217.
Ross, R., 1916. The life history of Ascaris lumbricoides. (Letter to editor). Brit. Med. Journ. 2: 60–61.
Ross, I. C., 1929. Observations on the hydatid parasite Echinococcus granulosus (Batsch, 1786) Rudolphi 1805, and the control of hydatid disease in Australia. C.S.I.R. Aust. Bull. 40: 1–63.
Salmon, J. T., 1949. New methods in microscopy for the study of small insects and arthropods Trans. Roy. Soc. N.Z. 77 (5): 250–253.
Schwartz, B., 1936. Controlling lungworms of swine. U.S. Dept. Agric. Leaflet No. 118.
Seddon, H. R., 1950. Helminth Infestations. Diseases of domestic animals in Australia Part 1. Aust. Dept. Health Service Publication (Division of Veteriary Hygiene) No. 5: 1–223.
Spindler, L. A., 1940. Effect of tropical sunlight on the eggs of Ascaris suis (Nematoda), the large intestinal roundworm of swine. J. Parasit, 26 (4): 323–332
—— 1942. Internal parasites of swine. U.S. Dept. Agric. Yearbook of Agriculture, Keeping Livestock Healthy, 745–786.
—— 1951. Effects of parasites on the growth of pigs. Vet. Med. 46 (11) 421–427.
Sprehn, C., 1951. Befall mit dem Knotchenwurm Oesophagostomum dentatum Rud. (Nematoda) als haufige Ursache des Ferkelsterbens in einem mittelfiankischen Beznk T [ unclear: ] e [ unclear: ] a [ unclear: ] tliche Umschau. 6 (23/24): 443–445.
Stewart, F. H., 1921. On the life history of Ascaris lumbncoides L. Part V. Parasit 13 (1) 37–47.
Thomson, G. M., 1922. The naturalisation of plants and animals in New Zealand Cambridge University Press.
Wharton, L. D., 1915a. The development of the eggs of Ascaris lumbrecoides Philippine Journ. Sc., Manila. Sect. B. Trop. Med. 10 (1): 19–23.
—— 1915b. The eggs of Ascaris lumbncoides. Philippine Journ. Sc., Manila. Sect. D. 10 (2): 111–115.
Whitlock, H. V., 1943 A method for staining small nematodes to facilitate worm counts. Aust., C.S.I.R. Journ. 21 (3): 181–182.
Whitten, L. K., 1945. Liver-fluke of sheep and cattle. N.Z. Dept. Agric. Bull. No. 248.
—— 1946. The hydatid disease. The prevention of hydatids. N.Z. Dept. Agric Bull. No. 272.
—— 1949. Parasites of pigs in New Zealand. N.Z. Dept. Agric.
Wodzicki, K. A., 1950. Introduced mammals of New Zealand. An ecological and economic survey. N.Z. Dept. Sc. & Ind. Res. Bull. No. 98.
Yorke, W., and Maplestone. P. A. 1926. The nematode parasite of vertebrats. London, J & A. Churchill.
Young, M. R., 1938. Helminth parasites of New Zealand. Imperial Bureau of Agricultureal Parasitology (Helminthology).