The Superfamily Trichostrongyloidea
The Trichostrongyloidea is by far the largest superfamily among the bursate nematodes. Divided into 14 families and 24 subfamilies by Durette-Desset and Chabaud (1977, 1981) and Durette-Desset (1983) the group is distinguished from the hookworms and the strongyles by the fact that the buccal capsule is absent or greatly reduced and lips and corona radiata are vestigial or absent. The lateral lobes of the bursa are highly developed although the dorsal lobe may be considerably reduced. The host range of the trichostrongyloids is broad. Found in all terrestrial vertebrate groups, they are extremely diverse as parasites of mammals, especially bats, rodents and ruminants. They also occur in monotremes and Australian marsupials. They are much less common and diverse in amphibians, reptiles and birds.
Trichostrongyloids are essentially parasites of the stomach and intestine of their hosts. Nevertheless, species of the subfamily Dictyocaulinae (with Dictyocaulus) are widespread and successful parasites of the trachea and bronchi of ruminants and equines. Also, some rare genera occur in bile ducts (Hepatojarakus), nasal cavities (Nasistrongylus) and mammary glands (Mammanidula) of their hosts.
Herbivorous hosts usually acquire their trichostrongyloids by ingesting infective larvae contaminating their food. Infective larvae of species in ruminants, like those of the strongyles, have a tendency to climb in films of moisture on to vegetation, where they become available to the host.
Exsheathment, the process whereby an ingested ensheathed larva escapes from the cuticle of the second stage in the gut of the host, has been extensively studied in the Trichostrongyloidea (Sommerville, 1957; Rogers and Sommerville, 1963, 1968). The initial stimulus comes from the host and, depending on the species of nematode, may include dissolved gaseous carbon dioxide, undissociated carbonic acid or hydrochloric acid, and/or pepsin at a low pH. The larva responds to these stimuli by producing an exsheathing fluid, which arises from an area near the excretory gland and which attacks an encircling area of the sheath near the cephalic end. Typically the anterior end of the sheath detaches from the main body of the sheath like a cap, thus allowing the larva to escape.
In oral infections, exsheathed larvae may invade the gut mucosa and develop to the fourth stage before re-entering the lumen, where they mature. In species found in such hosts as rodents both oral and percutaneous infection may occur. In percutaneous infection larvae migrate by way of the lymph and blood to the heart and lungs. In lungs the parasite moults to the fourth stage which migrates up the trachea to the throat and gut, where it matures (e.g. Nippostrongylus brasiliensis).
There are some oddities in the development and transmission of the trichostrongyloids, however. In Dictyocaulus spp. infective larvae invade the gut wall and migrate by way of the lymphatics and blood to the lungs, where they mature. Larvae of Hepatojarakus malayae apparently follow the hepatic portal system to the liver, where they mature. Ollulanus tricuspis of the stomach of felines and pigs is autoinfective and is transmitted entirely by emesis. Undoubtedly other interesting surprises await discovery. Perhaps Mammanidula asperocutis of the mammary glands of Sorex spp. is transmitted through the milk.
The phenomenon of arrest or inhibition during development in the definitive host is an important part of the biology of many trichostrongyloids, especially those in lagomorphs and ruminants, and has been extensively investigated. Michel (1974) and Gibbs (1986) have published major reviews. In many trichostrongyloids third-stage larvae ingested by the host exsheath and invade the gut mucosa where they develop rapidly to the early fourth stage and then return to the gut lumen, where they mature in a few days. Some members of the genus Trichostrongylus (e.g. T. colubriformis and T. vitrinus) may remain as third-stage larvae in the mucosa. When arrest occurs, an unusually high percentage of larvae remain in the mucosa for prolonged periods without further development. Arrested development plays an important role in the transmission of some trichostrongyloids because it allows species with limited adult life spans to survive in the arrested stage during periods when external conditions are unsuitable for the development, survival and transmission of larval stages (Anderson et al., 1965; Blitz and Gibbs, 1972a,b; Michel, 1974). For example, in temperate regions where transmission cannot occur in winter, larvae acquired in autumn develop to the fourth stage in the mucosa and remain arrested until spring, when conditions are again favourable for transmission, whereupon they invade the lumen of the gut and grow to egg-producing adults. Arrested development also occurs in areas where there are periods of extreme dryness unsuitable for transmission (Williams and Bilkovich, 1971; Shimshony, 1974; Baker et al., 1981, 1984; Williams et al, 1983; Gatongi et al, 1998).
Arrested trichostrongyloid larvae tend to develop to adulthood in ewes during parturition and lactation. Thus, transmission is enhanced at a time when young animals with little or no immunity are available for infection for the first time (Kassai and Aitkin, 1967; Kassai, 1968; Dineen and Kelly, 1973; Gibbs, 1982; Gibbs and Barger, 1986). The synchronized maturation of arrested larvae in spring in lactating ewes results in the so called spring rise in numbers of eggs passed by the host (Taylor, 1935b), a phenomenon also referred to as the periparturient rise by Salisbury and Arundel (1970).
Some factors responsible for arrest have been recognized. Experiments have shown that an important genetic component is involved and it is possible, by experimental, selection to increase the percentage of larvae in a population that are liable to arrest (Watkins and Fernando, 1984, 1986a,b). Waller and Thomas (1975) noted earlier that Haemonchus contortus in northern England always arrests and that it is an obligatory part of its development. Seasonal factors are also important in some species: seasonal arrest has been likened to diapause in insects and apparently occurs in response to such stimuli as low and/or fluctuating temperatures in autumn or the presence of hot, dry conditions in summer acting upon the free-living stages, especially the third larval stage (Armour et al., 1969; Fernando et al., 1971; Blitz and Gibbs, 1972a; Hutchinson et al., 1972; McKenna, 1973; Armour and Bruce, 1974; Armour, 1978; Horak, 1981). Increasing moisture and variations in photoperiod (Gibbs, 1973; Connan, 1975; Cremers and Eysker, 1975) have also been suggested as possible stimuli initiating arrest.
In addition to factors extrinsic to the host, factors within the host have been suggested as causes of arrest, the most important being immunity (Dunsmore, 1961; Ross, 1963; Donald et al., 1964; Dineen et al., 1965a,b). Larvae entering ahost with an established population of adult worms are most likely to arrest (Fox, 1976; Gibson and Everett, 1976; Michel, 1978; Behnke and Parish, 1979; Snider et al, 1981; Adams, 1983; Smith et al., 1984). The number of arresting worms in a host may be related to the number of adult worms present (Dineen, 1978) in that, as adults become senescent and die, there is a relaxation of immunity and some arrested larvae then leave the gut wall to replace the lost adults. Thus, the host immune system might regulate the number of adult worms.
The possible effects of environmental factors (photoperiod, temperature, diet) on host physiology have been investigated to determine if the latter could be related to arrest but results have been inconclusive (Gibbs, 1986). Parasite interactions have also been suggested as possible initiators of arrest, including the intensity of larvae and/or adult worms in the host (crowding effects) (Schad, 1977) and the possible presence of pheromones or other parasite-related chemicals which might cause invading larvae to arrest in the gut wall (Michel, 1963; Gibbs, 1986).
Factors responsible for the cessation of arrest and the resumption of development are not well understood. As noted earlier, loss or decline in immunity in the host may result in the cessation of arrest. However, there is little evidence that a decline in immunity can break arrest initiated by environmental factors (e.g. seasonal arrest) (Gibbs, 1986) and it has been suggested that seasonally arrested larvae behave as though they are in diapause, in which case an 'internal clock' would break arrest at a predetermined time after its induction by some stimulus (Armour and Bruce, 1974; Horak, 1981).
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