The family consists of 13 clearly related genera distributed mainly among Bovidae (sheep, goats, African antelopes) and Cervidae (deer). About half the known species are members of the genus Protostrongylus, some members of which occur in lagomorphs. Since protostrongylids are predominantly parasites of ruminants it is speculated that they are secondarily adapted to lagomorphs (Anderson, 1982). The family is distinguished from other metastrongyloids by unusually complex gubernacula and telamons (Boev, 1975).
Most protostrongylids occur in lungs, bronchi, bronchioles, alveolar ducts and alveoli (e.g. Cystocaulus, Muellerius, Neostrongylus, Protostrongylus, Varestrongylus). A few species are associated with veins distant from the lungs (e.g. Elaphostrongylus, Parelaphostrongylus). It is characteristic of all species in the family that female worms deposit unembryonated eggs, which develop into first-stage larvae in the lungs of the host. Eggs of species living distant from the lungs are deposited in veins and carried by the blood to the lungs via the right heart. Eggs are filtered from the blood and come to lie in capillaries, where they embryonate and become encapsulated by host response. First-stage larvae hatch from eggs, leave the area of inflammation, enter the airways and pass up the respiratory system and out in faeces of the host. First-stage larvae are generally long lived and resistant to drying and freezing temperatures.
First-stage larvae of protostrongylids fall sharply into two types. Larvae of species of Protostrongylus have rather long, tapered tails ending in a sharp point. In most other species which have been studied (Cystocaulus, Elaphostrongylus, Muellerius, Parelaphostrongylus, Varestrongylus) the tail has a more or less prominent posteriorly directed dorsal spine a short distance from the tail tip; this spine is said to be minute and difficult to distinguish in Neostrongylus linearis. The spine is shed with the cuticle of the first moult in the gastropod intermediate host. In addition, all first-stage larvae in the family seem to have well-developed lateral alae.
Hobmaier and Hobmaier (1929c) were the first to show that protostrongylid first-stage larvae (of Muellerius capillaris) would invade the foot of terrestrial gastropods and develop to infective third-stage larvae. The larvae moult twice and, in the foot, they retain the two shed cuticles of the first and second stage. These loose cuticles are rapidly discarded after the larvae are freed from snail tissue. Protostrongylids are not highly specific in their use of intermediate hosts and many species have been shown experimentally to develop in a wide range of terrestrial snails and slugs and even in aquatic species. Nevertheless, in any one region, only a few intermediate host species are probably important in natural transmission to the definitive host. The latter usually becomes infected by the accidental ingestion of gastropods crawling on vegetation. Some authors have reported that infective larvae leave the foot of snails and slugs and survive for considerable periods on vegetation, where they are transmitted to herbivores.
Other authors dispute this and the evidence seems to favour the opinion that the host normally becomes infected by ingesting gastropods.
Concurrent infections of two or more species may occur in an individual final host. In addition, first-stage larvae of species of the same genus, and even of different genera, may be morphologically indistinguishable. Since eggs of protostrongylids only embryonate in tissues of the final host, there is no obvious practical way to separate species for experimental work in many concurrent infections. Thus, in the following account, Protostrongylus kamenskyi and P. pulmonalis of lagomorphs are considered together, as are P. stilesi and P. rushi of Rocky Mountain bighorn sheep.
C. ocreatus (Railliet and Henry, 1907)
This is a parasite of the alveoli, alveolar ducts and bronchi of sheep and goats in Europe, Africa and Asia. According to Gerichter (1951) first-stage larvae were 390-420 mm in length; according to Davtyan (1949) they were 380-480 mm in length. The tail tip was bent dorsally and ended in a proximal tubular piece with tiny spines and a long, sharp, dagger-like piece. There was a curved dorsal spine on the tail as in M. capillaris. First-stage larvae invaded and developed in a variety of gastropods as follows: Abida frumentum, Agriolimax agrestis, A. schulzi, Cathaica semenovi, Cepaea hortensis, C. vindobonensis, Chondrula septemdentata, Cochlicella acuta, Ena asiatica, E. eleonorae, Euparypha pisana, Fruticicola rubens, Helicella barbesiana, H. candicans, H. joppensis, H. obvia, H. vestalis, Helix cavata, H. pometia, Jaminia potaniniana, Levantina caecariana, L. hierosolima, Limax flavus, L. maximus, Monacha syriaca, Monachoides umbrosa, Parachondrula aptycha, Retinella nittelina, Theba carthusiana, T. pisana and Zebrina detrita (see Boev, 1940, 1975; Joyeux and Gaud, 1946; Davtyan, 1948; Gerichter, 1951; Kassai, 1957; Zdarska, 1960). Manga-González and Morrondó-Pelayo (1990) showed that numerous species of snails were suitable intermediate host of combinations of C. ocreatus and Muellerius capillaris (i.e. Cernuella cespitum arigonis, Helicella itala, H. ordunensis, Cochlicella barbara, Cepaea nemoralis and Helis aspersa). Mixtures of larvae from C. ocreatus and Neostrongylus linearis developed in C. cespitum arigonis, H. ordunensis and C. nemoralis.
According to Zdarska (1960) first-stage larvae reached the infective stage in gastropods in 28 days at 26-28°C. Kassai (1957) claimed that the infective stage was reached in 20-46 days at 18-22°C. Gerichter (1951) stated that the first moult occurred 13-14 days and the second 15-17 days postinfection; an additional 1-2 days were required for larvae to become infective. At this time they were 750-790 mm in length and the tip of the tail had a button-like appendage.
According to Davtyan (1949) and Sagoyan (1950) infective larvae invaded the small intestine and colon of the final host and were found in mesenteric lymph nodes 36-40 h postinfection. Larvae apparently reached lungs by way of the hepatic portal system or lymph vessels. The parasite moulted twice in lung interstitial tissue (6-7 and 13 days after infection) and then moved into alveolar ducts. Worms matured by 28-30 days and unembryonated eggs were laid. The prepatent period was 40-44 days; Gerichter (1951) gave the prepatent period as 42 days.
Some authors believe that infective larvae leave molluscs and that sheep and goats become infected when they ingest free larvae on vegetation. Other authors (Azimov et al., 1973) question this and believe that the only route of infection is by the ingestion of gastropods, since the latter do not normally shed larvae.
Members of the genus have been reported from red deer (Cervus elaphus), sika deer (C. nippon), reindeer (Rangifer tarandus) and moose (Alces alces) in Europe and the eastern CIS. Pryadko and Boev (1971) and Kontrimavichus et al. (1976) recognized a single species consisting of: (i) E. cervi cervi in Cervus elaphus in Scotland and presumably western Europe; (ii) E. cervi panticola in C. elaphus, C. elaphus sibiricus, C. elaphus brauneri, C. nippon and Alces alces in eastern Europe and the Far East (e.g. Altai); and (iii) E. cervi rangiferi in Rangifer tarandus in Europe and the CIS. Steen et al. (1989) described a new species (E. alces) in moose in Sweden and distinguished it from E. cervi and E. rangiferi on the basis of some differences in morphology and the location in the host. In moose, worms are found epidurally rather than in the subdural and subarachnoid spaces as in reindeer. Halvorsen et al. (1989) provided some support for the proposal of Steen et al. (1989) when they were unable to transmit the parasite from red deer and moose to reindeer. Steen et al. (1997) transferred E. rangiferi to moose and E. alces to reindeer. Both species matured in the alternative host but produced fewer larvae than in the usual host, to which they were well adapted. Reindeer infected with E. alces developed patent infections after 39-130 days. In moose the prepatent period of E. alces was 39-73 days. E. rangiferi infections were patent in moose after 133 days. Lankester (1977) transmitted E. rangiferi from caribou (R. t. caribou) in Newfoundland to Alces alces, raising the possibility that this is a single species (see Kutzer and Prosl, 1975) and perhaps distinct strains. Gibbons et al. (1991) restudied specimens and concluded that three species should be recognized, namely E. cervi, E. rangiferi and E. alces. We prefer to use subspecies designations at this time to distinguish E. cervi from western Europe and E. cervi from the Far East.
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