T tenuis Mehlin 1846

T. tenuis (syn. T. pergracilis) is reported as a parasite of the caeca mainly of grouse and geese which consume terrestrial vegetation. It is well known as a parasite of Lagopus lagopus and L. mutus in northern Europe. The status of reports of T. tenuis in the New World requires clarification since the species in the bobwhite quail (Colinus virginianus) formerly identified as T. tenuis (syn. pergracilis) is now recognized as a distinct North American species, T. cramae Durette-Desset et al. (1993). The assessment of the species reported in domestic geese in North America (Cram and Cuvillier, 1934; Cram and Wehr, 1934) should be clarified since the worms may have been misidentified as T. tenuis. However, T. tenuis could have been introduced into the USA, since Cram and Cuvillier (1934) reported that 'a flock of pheasants which had been imported from England and were held in captivity suffered from the effects of heavy infestations with Trichostrongylus tenuis, whereas pheasants reared on the premises showed no clinical evidence of disease'. The nematode has been reported in L. lagopus and L. mutus in Norway (Holstadt et al., 1994); intensities were higher in L. lagopus than in L. mutus.

The first observations on the development and transmission of T. tenuis were contained in a report of a Committee of Inquiry on Grouse Disease published in 1911 in the UK (Lovat, 1911). In 1912 an abridged, popular version was edited by Leslie and Shipley (1912). Within this latter volume the problem of grouse diseases consists of chapters (IV, V, VII and VIII) contributed, respectively, by Wilson, Wilson and Leslie, Shipley and Shipley and Leiper (Wilson et al., 1912). The authors related the prevalence, intensity and pathogenicity of T. tenuis to 'grouse disease' and well-known fluctuations in red grouse (Lagopus lagopus scoticus) on grouse moors in the UK. New investigations have confirmed most of the basic findings of the 1911 report, and added new dimensions to our understanding of the disease and how it might be managed on moorlands for grouse shooting.

The 1911 report noted that adults of T. tenuis were extremely thin, transparent and difficult to see with the naked eye even though males were 8 mm and females 10 mm in length. The cephalic end of the worms penetrated deeply into the caecal mucosa. Eggs were about 75 X 46 mm in size and were passed in faeces of grouse in the morula stage with 64 cells. In moist faeces and at suitable temperatures eggs reached the first stage, which hatched in about 36-48 h; larvae were about 360 mm in length. The first moult occurred in 36-48 h and the second in 8-16 days, depending on the temperature. Heather (Calluna vulgaris) is the staple food of adult red grouse and it was demonstrated experimentally that sheathed infective larvae crawled to the tips of moist heather and accumulated there in drops of water during misty weather. It was also shown that larvae could withstand desiccation on the tips of heather. Two adult grouse were given infective larvae in water. One bird died of aspiration pneumonia but the other became emaciated and died and many T. tenuis were found in its caeca. The authors concluded, as did Cobbold earlier, that T. tenuis was the causal agent of a disease that regularly killed grouse, mainly in spring and they speculated on the factors responsible for its seasonality.

Prevalence in adult grouse is 100% and chicks acquire infections soon after their diet turns from insects to vegetation. The prepatent period is about 7—8 days. Birds do not develop protective immunity and since worms are fairly long-lived intensities can be extremely high (up to 9000-10,000 individuals) (Hudson and Dobson, 1989; Shaw and Moss, 1989b).

Watson et al. (1987, 1988) showed that T. tenuis threaded themselves into the caecal mucosa with anterior and posterior ends protruding into the lumen. As noted earlier by Wilson (in Leslie and Shipley, 1912), the worms caused trauma, atrophy and flattening of the epithelial cells, which would probably interfere with the normal digestion of heather and other plant material.

McGladdery (1984) confirmed earlier observations that free-living third-stage larvae were negatively geotactic and positively phototactic. They readily ascended heather in moist conditions. Shaw et al. (1989) showed that eggs and early free-living stages were not resistant to desiccation or extreme cold. Eggs failed to develop at low temperatures and most third-stage larvae failed to survive winter on grouse moors. Connan and Wise (1994) reported that eggs of T. tenuis are rather sensitive to cold but that infective larvae are capable of withstanding winter temperatures on Yorkshire grouse moors. The larvae may, however, be susceptible to desiccation, especially on the tips of heather.

Shaw (1988) provided evidence that arrest occurs in third-stage larvae. Recently acquired third-stage larvae apparently retained the second-stage cuticle for a few days and could be distinguished from established exsheathed larvae. In August and September most larvae in grouse were in the fourth stage but some third-stage larvae were sheathed, indicating that transmission was taking place. In winter (November and December) ensheathed larvae were absent but exsheathed larvae were present, suggesting that few new larvae were being ingested during this period and that the exsheathed third-stage larvae were arrested. In spring (March and April) the proportion of third-stage larvae decreased significantly in the parasite population and sheathed larvae were absent, indicating that overwintering third-stage larvae had developed to fourth and adult stages when the output of eggs in the faeces of the birds increased. Shaw (1988) suggested that the more or less synchronized development of larvae in grouse resulting eventually in the 'spring rise' in worm egg production may contribute to the disease and mortality occurring in grouse in spring. Delahay et al. (1995) reported that short-term energy unbalance, weight loss and loss of condition occurred in grouse at the onset of the development of fourth-stage larvae to adults and up to the onset of patency.

Shaw and Moss (1989a) reported that prevalences of T. tenuis in red grouse in Scotland were high even at low grouse densities and that prevalence, intensity and aggregation were higher in older than younger grouse. Populations of adult worms could apparently survive for over 2 years. The output of eggs from the worms decreased with age of the worm population, especially in winter (November-December). Moss et al. (1993) analysed the numbers of eggs of T. tenuis passed in faeces of red grouse over 8 years and proposed that rainfall in the previous summer explained much of the year-to-year variation in egg numbers, probably because transmission is greater in wet than in dry summers. The data apparently do not support the hypothesis that cyclic-type population changes in grouse were caused by T. tenuis.

Hudson and Dobson (1997) examined and quantified transmission rates and density-dependent reductions in egg production of T. tenuis. The sustained cycles observed in long-term dynamics of the grouse populations suggest that density-dependent reductions in worm fecundity and establishment are absent or only operating at levels undetectable in field studies.

Moss et al. (1990) decided that there was no relationship between intensity of T. tenuis and fox predation (cf. Hudson, 1986a). Shaw (1990) noted that captive red grouse infected with T. tenuis started to lay later in spring and laid fewer eggs at a slower rate than uninfected hens. Hens infected in March exhibited inappetence a week postinfection and gained less weight than controls. This suggested the possible significance of developing larvae to the health of the birds, as noted also in spring, when arrested larvae proceed to develop (Shaw, 1988). Hudson et al. (1992) reported that grouse killed by predators had more caecal worms than birds that were shot. More birds were heavily infected in places where predator control was intense, leading to the possibility that predators select heavily infected over less heavily infected grouse. Dogs found fewer birds treated with oral anthelminthics than untreated birds. A modified model taking predation into account was proposed. Dobson and Hudson (1995) claimed that models demonstrated that small numbers of predators selectively removing heavily infected individuals may allow the size of the red grouse population to increase, since the predators reduce the regulatory role of the parasites.

Hudson (1986b) compared the productivity of red grouse treated with levamisole hydrochloride with untreated birds in the field. Treatment significantly increased the production of young birds and breeding success was related to decreased intensities of T. tenuis.

Several attempts have been made to model the red grouse - T. tenuis system. Watson et al. (1984) modelled changes in breeding density emphasizing overwinter survival, whereas Potts et al. (1984) and Hudson et al. (1985) modelled cyclic changes in bag records emphasizing winter survival and dispersal. The models support the conclusion that T. tenuis infections in red grouse reduce breeding production and that this is reflected in cyclic changes in the numbers of grouse shot in the autumn. Hudson et al. (1985) emphasized the importance of humidity in the survival of free-living stages and showed by modelling that the 'interaction of a long-lived free-living stage and parasite induced reduction in fecundity would be of prime importance in producing the cycles in grouse density'.

For a general review of the relationship of T. tenuis to red grouse, the reader is referred to Hudson and Dobson (1989).

Moss et al. (1996) pointed out that red grouse have unstable population dynamics and that if some cocks were removed during the increase phase it might prevent the usual cyclic decline. The results indicate that age structural changes and associated behaviour may result in cycles by affecting recruitment.

Watson and Shaw (1991) pointed out that T. tenuis is uncommon in ptarmigan (Lagopus mutus) yet cyclic-type declines also occur in this species in Scotland.

T. vitrinus Looss, 1905

T. vitrinus is a cosmopolitan parasite of the duodenum of sheep, goats, cattle and other ruminants; it is frequently associated with T. colubriformis and it has been reported in pigs and rabbits. According to Shorb (1939) eggs were 93-118 X 41-52 mm in size. Infective larvae were 622-796 mm in length. The tail was blunt with two small terminal tubercles (Dikmans and Andrews, 1933). According to Crofton (1965) eggs hatched in

19 h at 36°C, 24 h at 28°C, 48 h at 18°C and 7 days at 9-10°C. Rose and Small (1984) studied the survival of eggs and larvae under field conditions in England. Eggs and larvae developed from April to March but development was slow from October to March and mortality was high. In dry periods, mortality of preinfective stages was high, especially in short herbage. Infective larvae survived for up to 16 months on grass plots and survived severe winter cold. In the laboratory, eggs and larvae developed from 4 to 27°C and were killed by continuous freezing.

Eysker (1978) and Ogunsusi and Eysker (1979) reported arrested development in the third stage.

Subfamily Haemonchinae Haemonchus

Members of the genus are found in the abomasum of ungulates and one well-known species (H. contortus) is regarded as one of the most pathogenic helminths in domesticated animals. The genus was revised by Gibbons (1979) who placed some 15 described species or subspecies and varieties, including H. placei and H. contortus cayugensis, into synonymy with H. contortus (Rudolphi, 1803) which she regarded as a polymorphic species. Whitlock and Le Jambre (1981) reported bionomic and genetic differences which they believed justified the recognition of H. placei and H. c. cayugensis as distinct from H. contortus. They suggested that the latter represented a complex of sibling species. Jacquiet et al. (1997) used morphology of spicules to separate species. The general biology of H. contortus and the reported differences in biology between this species and H. placei are outlined below.

H. bedfordi Le Roux, 1926

The infective larvae of H. bedfordi from the impala (Aepyceros melampus) in South Africa were 615-718 mm in length (Anderson, 1995). The author contrasted larvae of H. bedfordi with those of H. contortus and H. placei.

H. contortus (Rudolphi, 1803)

The twisted stomach or wire worm is a red, blood-sucking parasite found in sheep, goats, cattle, bison and deer. White-tailed deer (Odocoileus virginianus) have been infected experimentally with H. contortus from sheep (Foreyt and Trainer, 1970) and McGhee et al. (1981) transferred H. contortus between white-tailed deer, lambs and calves. Morphologically the parasites from deer were indistinguishable from those in cattle and sheep. Conder et al. (1992) infected jirds (Meriones unguiculatus); growth was slow and incomplete in jirds but they did invade the stomach and some persisted for 14 days.

Ransom (1906) made some of the earliest observations on H. contortus. He noted that eggs in faeces were in 'various stages' of segmentation and that they developed and first-stage larvae (350 mm in length) hatched within 2 days at 16-20°C. Most larvae reached the sheathed infective stage in 10-14 days. Eggs and newly hatched larvae were not resistant to cold and desiccation, but infective larvae were highly resistant to drying and cold, including freezing temperatures. Infective larvae climbed to the tips of blades of grass in moist conditions and Ransom concluded that the definitive host became infected by ingesting larvae on herbage.

Veglia (1916) carried out a detailed study of H. contortus with special reference to the development and characteristics of the free-living stages. Eggs were 66.5-79.0 X 43.3-46.6 mm in size and with 24-26 blastomeres in fresh faeces; eggs deposited by females were usually in the four-cell stage and developed as they passed through the gut of the host. The optimal temperature for development was 20-30°C. In liquid cultures first-stage larvae hatched from eggs in 14-17 h at 26°C. First-stage larvae were 340-350 mm in length and had a valved oesophageal bulb and attenuated, sharply pointed tails. The buccal cavity was tubular. The genital primordium consisted of two cells. About 1 h after hatching, larvae commenced to feed. In 10-12 h, when larvae were 400-450 mm in length, the first lethargus and moult occurred and larvae recommenced feeding. Gamble et al. (1989) studied the second moult in H. contortus and suggested that the second cuticle is digested by 44-kDa zinc metalloprotease, possibly released from oesophageal glands. Prominent lateral alae made their appearance. The second lethargus and moult commenced 40 h after the first moult or 60-65 h after larvae had hatched. Infective larvae in faecal cultures were 754-756 mm in length (apparently this included the sheath) in 65 h at 26°C. The larva retained the second-stage cuticle with its pointed, attenuated tail. The tail of the larva within the sheath was conical and much less attenuated than that of the second stage. Prominent lateral alae were present. The genital primordium had 16 nuclei and the buccal cavity was elongated but closed anteriorly.

Veglia (1916) made extensive observations on the effects of various environmental factors on the behaviour of larvae and their survival. For example, larvae died at high temperatures (70-85°C) and in decomposed faeces. Eggs failed to develop when kept at 4°C and would not develop when returned to warmer temperatures. Mature larvae left faecal material and were highly resistant to desiccation, apparently in part because of the presence of lipid in the intestinal cells and because they tended to clump together. Infective larvae moved upwards in films of moisture, especially at night and at times of diffuse light, and were negatively heliotactic.

Attempts to infect lambs percutaneously were unsuccessful but after oral inoculation with infective larvae lambs passed eggs on average 15 days postinfection. Larvae exsheathed in the mouth and abomasum. In the latter they immediately began to feed as they lodged between villi. In 2 days larvae were 655-840 mm in length. The third lethargus started in 30-36 h postinfection and lasted for 12 h, during which the moult occurred; larvae (still 750-850 mm in length) escaped from the third cuticle through a longitudinal slit. A provisional buccal capsule was present in the early fourth stage which enabled larvae to attach to the mucosa and suck blood for the first time. Larvae caused small haemorrhages as early as 3 days postinfection. By day 7, sexes were easily distinguishable and males were 2.7-3.0 mm and females 3.7-4.0 mm in length. The fourth moult occurred in 9-11 days and was preceded by a lethargus of about 24 h. The adult buccal capsule was more globular than that of the fourth stage. Eggs were deposited by females in about 15 days.

Coyne and Smith (1992) noted that eggs did not develop at 5°C and the optimum temperature for full development was 20°C. They produced a model to estimate development and mortality rates from their experimental data.

Rahman and Collins (1990b) infected goats with 40,000 larvae and examined them at various days postinfection. More worms established themselves in the fundic than in the middle or pyloric third of the abomasum. Emergence into the lumen started between 7 and 11 days postinfection and by 4 days all worms had moulted to the fourth stage. By day 18 some (13.2%) females had eggs. In 21 days over half the females were gravid.

A number of authors have reported on the effects of environmental factors on the development and survival of eggs and larvae of H. contortus. For example, Rees (1950) emphasized the necessity for a favourable combination of temperature, humidity and light to initiate vertical migration of larvae on grass blades. Silverman and Campbell (1958) concluded that in Scotland H. contortus requires about an optimum of 2 weeks in summer for development of the egg to the third-stage larva. They noted that embryonated eggs were more resistant to adverse conditions than unembryonated eggs. For example, rapid dessication of faeces destroyed most eggs unless they were all embryonated. Rose (1963b, 1964) compared larval survival and availability on herbage of different heights and lushness. Narain and Chaudhry (1971) and Sood and Kaur

(1975) restudied the effects of temperature on development and Todd et al. (1976) reported that desiccation protected free larvae from death at storage below freezing temperatures but was harmful at temperatures above freezing. Gibson and Everett

(1976) concluded that in southern England the climate was not particularly favourable for the development and survival of the free-living stages of H. contortus. Hsu and Levine

(1977) related humidity and temperature to development of the free-living stages of H. contortus (and Trichostrongylus colubriformes). Jasmer et al. (1987) compared cold hardiness in H. contortus and Teladorsagia circumcincta.

H. contortus is noted for a marked propensity to arrest in the early fourth stage and the process is considered as the primary means of surviving winter in temperate climates. According to Blitz and Gibbs (1971b) arrested male larvae were at the stage equivalent to 3-4 days postinfection and the genital primordium was not differentiated whereas females were slightly more advanced and the genital primordium had started to develop. Cylindrical crystals of unknown significance were common in intestinal cells of arrested larvae; these crystals disappeared with development of larvae. Arrested larvae occurred on and not in the mucosa.

Dineen et al. (1965a), Soulsby (1966) and Michel (1968) suggested that arrest was related to high levels of resistance in lambs. Dineen et al. (1965a) showed that the percentage of arrested larvae of H. contortus increased in lambs given repeated doses of infective larvae.

Gibbs (1967), Connan (1968) and Muller (1968) showed that arrested larvae of H. contortus acquired in fall matured in spring and the worms contributed to the spring rise in eggs passed in faeces of sheep. Arrested larvae, transferred in winter to parasite-free lambs, failed to develop for 10 weeks and egg counts in the faeces of the host rose markedly as usual in April (Blitz and Gibbs, 1971a,b). In addition, a high percentage of infective larvae exposed to environmental conditions (14.25-12.50 photoperiod and mean temperature of 17°C) in September in Quebec, Canada, arrested (Blitz and Gibbs, 1972a). It was concluded that arrested larvae mature spontaneously in spring as if they have been in an environmentally induced diapause (Blitz and Gibbs, 1972b). Jacquiet et al. (1995) showed that in dry periods H. contortus is able to survive because adult worms can maintain their ability to produce eggs for up to 50 weeks.

Waller and Thomas (1975) studied H. contortus in lambs in northeast England. In late June small numbers of adult H. contortus were present. Subsequently the number of worms rose rapidly and the percentage of arrested worms increased monthly until it was 100% in September, October and November. There were no differences in worm numbers or percentage arrested in experimental and tracer lambs, suggesting that autumn climatic conditions and host immunity were not responsible for arrest in this strain of H. contortus.

Connan (1975) reported that chilling infective larvae (4°C) had no effect on the percentage of larvae arresting and that exposing larvae to autumn climatic conditions in East Anglia, England, was not necessary to induce a high percentage of larvae to arrest. Apparently a suitable stimulus was provided by keeping the culture in the dark at 25°C for 12 days. Mansfield et al. (1977) also concluded that temperature had no effects on inducing arrest in H. contortus. Eysker (1981) reported that exposure of infective larvae to 15-16°C induced arrest in sheep and that exposure to lower temperatures was much less effective. Connan (1978) reported that the number of larvae arresting in experimentally infected lambs varied positively with the water content of faeces in which larvae had been cultured and the time larvae were in the cultures (6 or 12 days). Two groups of sheep were allowed to graze on infected pasture: (i) from 10 to 27 September and (ii) from 22 November to 9 December. Both groups began to pass eggs between February and May and there was in both groups a sharp rise in egg counts in April, presumably because of the simultaneous maturation of arrested larvae.

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