Parasites of Cervids (Mammalia)

Proc. Helminthol. Soc. Wash. 51(2), 1984, pp. 196-204

Evolution of the Elaphostrongylinae (Nematoda: Metastrongyloidea: Protostrongylidae) Parasites of Cervids (Mammalia)

THOMAS R. PLATT Department of Biology, University of Richmond, Richmond, Virginia 23173

ABSTRACT: The phylogenetic relationships of the Elaphostrongylinae were evaluated by cladistic analysis. Ela- phostrongylus cervi is considered the most plesiomorphic member of the subfamily and is the sister-group of Parelaphostrongylus. Parelaphostrongylus, which consists of P. andersoni, P. odocoilei, and P. tenuis, is monophyletic based on the presence of crura on the gubernaculum and a bifurcate gubernacular corpus. P. tenuis is the most plesiomorphic member of the genus and is the sister-group of a monophyletic muscleworm lineage composed of P. andersoni and P. odocoilei. Elaphostrongylus cervi originated in the nearctic, cospeciating with Rangifer. The current holarctic distribution of E. cervi is interpreted as colonization of more primitive cervids with the retention of broad coaccommodation within the family. The meningeal worm, P. tenuis, originated prior to the formation of extant species of Odocoileus. Cospeciation of the muscleworm ancestor with the ancestor of the extant species of Odocoileus resulted in P. andersoni in O. virginianus and P. odocoilei in O. hemionus. The extensive distribution of E. cervi, a generalist, can be attributed to its broad coaccommodation within the Cervidae, broad coaccommodation with and the ubiquitous nature of suitable molluscan intermediate hosts, and the absence of competitors in Eurasia. The distribution of P. tenuis, a specialist, in North America is attributed to the success of white-tailed deer and in part to the pathogenic effects of the meningeal worm in sympatric cervids. Two hypotheses for the current distribution of the species of Parelaphostrongylus are presented.

The Elaphostrongylinae (Protostrongylidae) onization as an alternative means of parasite ac- comprise a small but economically important quisition. group of nematode parasites of cervids. Although Recent studies of host-parasite evolution and commonly referred to as "lungworms," all species zoogeography have centered exclusively on the of the subfamily inhabit extrapulmonary sites in relationship between the parasite and the defin- the definitive host. Life cycles are complex, and itive host (Brooks, 1977, 1978, 1979b; Brooks terrestrial gastropods are used as obligate inter- et al., 1981; Chabaud and Bain, 1976). The role mediate hosts (see Anderson, 1968 for a review). of intermediate hosts however has not been given Coevolution of parasitic organisms with their equal attention. The following analysis of the hosts has been considered axiomatic. Cameron Elaphostrongylinae includes an evaluation of the (1964) stated, "parasites have obviously evolved role of the intermediate and definitive hosts as co-incidentally with their hosts" and that "par- they relate to the distribution and evolution of asite phylogeny and classification can only be the parasite. interpreted in terms of host phylogeny and clas- Materials and Methods sification." However, Inglis (1965) stated, "evolution of most groups of nematodes has tended Specimens of P. odocoilei were obtained from experimentally infected mule deer (Odocoileus h. hem- to occur in hosts with similar ecological require- ionus) as reported by Platt and Samuel (197 8a, b). Spec- ments." Brooks (1979a) recently reexamined the imens of P. tenuis were obtained from naturally infected concept of coevolution and identified two dis- wapiti (Cervus elaphus canadensis) in PennsyJvania. tinct components: coaccommodation, "the mu- Type specimens of P. andersoni were obtained from tual adaptation of a given parasite species and the USNM Helm. Coll., Beltsville, Maryland. Speci- mens of E. cervi were not available, and the description its host through time" and cospeciation, "clado- by Lankester and Northcott (1979) was used as a source genesis of an ancestral parasite species as a result of morphological characters. of or, concomitant with, host cladogenesis." This The direction of change of characters within the Ela- distinction forms an important framework for phostrongylinae was determined through the use of out-group comparison (Hennig, 1966; Wiley, 1981). the study of the evolution of host-parasite sys- As some parasitologists may not be familiar with the tems, as it emphasizes the historical relationship terminology of phylogenetic systematics, the following of host and parasite but does not disregard col- definitions are provided (following Wiley, 1981). Ple-

196

P. andersoni P. odocoilei P. tenuis E. cervi

Figure 1. Male reproductive structures of the species of the Elaphostrongylinae. la-d, gubernacula, le-h, spicules. li-1, copulatory bursa. (Fig. b, c, e, f, i, 1, and k, original; Fig. la, redrawn from Prestwood [1972]; Fig. Ig, redrawn from Dougherty, 1945, Parasitology 36:199-208; Fig. Id, h, and 1, redrawn from Lankester and Northcott [1979].) siomorphic and apomorphic refer to the original and state and a 1, -1, or 2 for the apomorphic state. An derived states, respectively, of a pair of homologous outline and explanation for the decision of the deter- characters. Synapomorphies are "evolutionary novel- mination of character state polarity is presented below. ties" (derived characters) shared by two or more species forming a monophyletic group. Autapomorphies are 1. Crura of the gubernaculum.—The gubernaculum of derived characters restricted to a single species. Homo- the majority of the Protostrongylidae (sensu An- plasies are structurally similar characters that are derson, 1978) is complex, consisting of a corpus, thought to be of independent origin. crura, and capitulum. The gubernaculum of the re- As the sister-group of the elaphostrongylines is un- maining metastrongylids is simple, corpus only, or known, members of the Metastrongyloidea, excluding absent. Two states: crura absent (0); crura present the Protostrongylidae, were employed as the out-group. (1) (Fig. la-d). Each character was assigned a 0 for the plesiomorphic 2. Corpus of the gubernaculum.—The corpus is a solid

Table 1. Data matrix of the character state distribu- however in recognizing P. andersoni and P. ten- tion used in the analysis of the Elaphostrongylinae. uis, which are parasites of white-tailed deer, as a monophyletic group based on the position of Characters the branches of the dorsal ray. A single homo- Species 1 2 3 4 5 6 7 8 plasy, the presence of a compact dorsal ray, is E. cervi 0 0 0 0 0 0 0 1 shared by P. odocoilei and P. andersoni. P. tenuis 1 1 0 1 0 1 0 0 P. andersoni 1 1 1 0 1 1 1 0 Discussion P. odocoilei 1 2 0 0 1 0 -1 0 Although the two cladograms are equally parsimonius based on character distributions, the phylogeny in Figure 2a is preferred based on the piece in nonprotostrongylid members of the Meta- location of the adult worms in the definitive host. strongyloidea. Three states; solid corpus (0); distally Elaphostrongylus cervi, the most plesiomorphic notched corpus (1); distally split corpus (2) (Fig. la- species, has been reported from the meninges of d). the brain (Mitskevitch, 1964) as well as the con- 3. Spicules.—The distal end of the spicules in the ma- nective tissue of the skeletal muscles (Mitske- jority of metastrongylids is solid. Two states: solid (0); bifid (1) (Fig. le-h). vitch, 1964;LankesterandNorthcott, 1979) and 4. Spicular foramen.—A spicular foramen is only found occasionally deep muscle sites (Lankester and in P. tenuis. Two states: absent (0); present (1) (Fig. Northcott, 1979). Species of Parelaphostrongylus Ib). are more restricted in their site of maturation. 5. Shape of the dorsal ray.—The dorsal ray in the majority of nonprotostrongylids (excluding highly spe- Adult P. tenuis have only been found in close cialized forms with marked bursal reduction) is not association with the central nervous system (CNS) compact. Two states: not compact (0); compact bulb (Anderson, 1968). The muscleworms are re- (1) (Fig. li-1). stricted to the skeletal muscles and associated 6. Branches of the dorsal ray.—The branches of the connective tissue (Prestwood, 1972; Platt and dorsal ray in nonprotostrongylids (not exhibiting bursal reduction) are terminally placed. Two states: Samuel, 1978b). Therefore, following the phy- terminal (0); ventral (1) (Fig. li-1). logeny in Figure 2a, habitat specialization is a 7. Location of the dorsal ray.—The dorsal ray in non- direct process requiring no reversals or parallel- protostrongylids (not exhibiting bursal reduction) is isms. In the alternate phylogeny (Fig. 2b) neu- terminal. Three states: terminal (0); ventral (1); dor- rotropic behavior would have been lost in the sal (-1) (Fig. li-1). 8. Perityls.—Nonmovable lips are found in the ma- ancestral Parelaphostrongylus and then reap- jority of metastrongylids. Two states: present (0); peared in P. tenuis, or the muscleworms lost their absent (1). neurotropic behavior independently and P. ten- A summary of the distribution of character states is uis retained the behavior as a plesiomorphic trait. given in Table 1. Both of these scenarios require reversals or parallel evolution, hence Figure 2a is preferred. Results Strict adherence to the rules of phylogenetic Two equally parsimonius cladograms can be classification (Hennig, 1966) would result in a constructed based on the distribution of the syn- major change in nomenclature for the subfamily. apomorphies (Fig. 2). The first (Fig. 2a) recog- Application of the sequencing convention (Wi- nizes E. cervi as the most plesiomorphic member ley, 1979) would permit the inclusion of the four of the subfamily. Parelaphostrongylus is recog- species of elaphostrongylines in a single genus, nized as a monophyletic taxon on the basis of Elaphostrongylus Cameron, 1931.1 prefer to re- the presence of crura and a notched or distally tain the current nomenclature at the present time split gubernacular corpus (Fig. la-c). A muscle- for the following reasons. Pryadko and Boev worm lineage consisting of P. andersoni and P. (1971) reduced E. rangiferi Mitskevitch, 1958, odocoilei is monophyletic based on the presence and E. panticola Liubimov, 1945, to synonyms of a compact, bulbous dorsal ray (5). A single of E. cervi in the absence of morphometric cri- homoplasy, the ventral position of the branches teria to separate these forms. Additional inves- of the dorsal ray (6), is shared by P. tenuis and tigation, however may validate one or both of P. odocoilei. The alternative phylogeny (Fig. 2b) these species and would require the reinstate- also recognizes E. cervi as the most plesiomorph- ment of Parelaphostrongylus. In addition, both ic species and Parelaphostrongylus as monophy- taxa as currently defined are monophyletic based letic, as described above. Thi» phylogeny differs on criteria presented by Platnick (1977). Rec-

EC Pt

• 8 -- 4 - 6

2a 2b

Figure 2. Cladograms of the relationships of the Elaphostrongylinae. Numbers correspond to the presence of the apomorphic character states as outlined in the text. Numbers represent character states (Table 1 and text). A line followed by a number indicates an increased change. An X indicates a decreased change (see text and Table 1) (Ec = Elaphostrongylus cervi; Po = Parelaphostrongylus odocoilei-., Pa = P. andersoni; Pt = P. tenuis).

ognition of the first cladogenic event at the ge- on all continents except Australia and Antarc- neric level and subsequent events at the specific tica. Cervus and Mazama will be treated sensu level is clearly arbitrary. lato, consisting of the following: Cervus s.l. Any attempt to assess the evolutionary and (=Cervus, Darna, and Axis) and Mazama s.l. biogeographic history of a parasite with a com- (=Mazama, Blastocerus, Ozotocerus, Hippoca- plex life cycle must include an analysis of the melus, and Pudu). history and distribution of the intermediate There have been few attempts to formally re- host(s). There is some disagreement as to the construct the phylogenetic relationships of the time of origin of the current holarctic gastropod genera of cervids. Flerov (1950) presented a gen- fauna. All contemporary genera were present by eral evolutionary scheme for the cervids based the end of the Pliocene (Likhachev and Ram- on paleontological, as well as neontological data mermaier, 1952), however they may be sub- that is at variance with more traditional schemes stantially older (Taylor, 1960; Walden, 1963). (e.g., Lydeckker, 1898; Simpson, 1945). These The elaphostrongylines show some specificity follow Brooke's (1878) original designation of for the intermediate host (Panin, 1964; Lankester two primary lineages based on the type of re- and Anderson, 1968; Platt, 1978). A number of duction of the second and fifth metacarpals. Gif- species in two of the four suborders (Heterau- fin (1974) analyzed the phylogeny of the cervids rethra and Sigmaurethra) of the pulmonate order using cladistic methods in a more inclusive study Stylommatophora, are capable of serving as suit- of the relationships of the Artiodactyla. Her work able intermediate hosts. Therefore, it can be as- was based on a combination of gross cerebral sumed that a modern terrestrial gastropod fauna characters as well as noncerebral characters taken was present when modern cervids were becom- from the literature. Giffm (1974) did not use the ing established during the late Miocene and early condition of the metacarpals in her analysis, and Pliocene (Flerov, 1952) as suggested by Pryadko hence it serves as an independent test of that and Boev (1971). The continuity of the gastropod character. The results provide more support for fauna during the late Tertiary and Pleistocene the traditional classifications than that of Flerov would have given the elaphostrongylines a long (1952). association with, and relatively little selection The most parsimonius hypothesis of the origin pressure from, the intermediate host. Thus, the of the elaphostrongylines is a nearctic origin prior current distribution of these nematodes must be to the formation of Rangifer and the subsequent explained as a function of the evolution and dis- cospeciation of Parelaphostrongylus spp. with tribution of the definitive hosts. Odocoileus spp. (Fig. 3). E. cervi originated with The family Cervidae consists of 11-17 extant Rangifer, a northern-adapted, tundra specialist. genera, with representatives occurring naturally At the same time the ancestor of O. virginianus—

Figure 3. Correspondence between the cladogram of the Elaphostrongylinae (dashed line) and Cervidae (solid line). Arrows indicate colonization of cervids by E. cervl (Cervinae; Ce = Cervus, El = Elaphrurus: Odocoilinae; Ca = Capreolus, Al = Alces, Ma = Mazama, Ra = Rangifer, Ov = Odocoileus virginianus, Oh = Odocoileus hemionus). ? indicates that elaphostrongylines are not known from these genera. Cladogram of Cervidae (excluding Hydropotinae and Muntiatinae) modified from Giffin (1974).

O. hemionus, a temperate and subtemperate gen- the muscleworm lineage (Figs. 2, 3). The vicar- eralist (Brokx, 1972), originated harboring the iant event responsible for this speciation event ancestor of Parelaphostrongylus spp. is unknown. It was not however, a response to Alternatively, the elaphostrongylines could be speciation in the host lineage (Fig. 3). Speciation regarded as eurasian in origin (Pryadko and Boev, in the muscleworm lineage followed the sepa- 1971). This would require strict cospeciation of ration of Odocoileus into a western population, the parasite and host with subsequent extinction O. hemionus, and an eastern form, O. virgini- of the parasites of Cervus s.l. through Mazama anus, as described by Brokx (1972). Vicariance s.l. preceding or as a result of colonization of could have been accomplished by the formation these hosts by E. cervi. There is no evidence to of the midwestern plains during the Pliocene support these extinctions, nor is the hypothesis (Clements and Chancy, 1937) or by a later re- testable in any way. A second alternative in- establishment of the plains during the Pleisto- volves the survival of E. cervi in the more prim- cene (Blair, 1958). itive cervids and recognizing E. cervi as ancestral The current distribution of elaphostrongylines to Parelaphostrongylus. However, since E. cervi can be explained as a function of dispersal is not plesiomorphic for all characters examined (mobilism), coaccommodation, and possibly it does not meet the minimum requirements of ecologic factors. Overlap between sister-taxa is an ancestor. The presence of E. cervi or an un- indicative of mobilism (Croizat et al., 1974). described species of Elaphostrongylus in South Elaphostrongylus cervi has an extensive distri- American cervids (Mazama s.l.) would falsify bution in Europe and Asia (see Kontramavichus the nearctic origin of the group, due to the geo- et al., 1976). Naturally occurring infections of E. graphic isolation of the hosts and the unlikely cervi have been reported from reindeer in New- possibility of long-distance dispersal of the foundland (Lankester, 1976; Lankester and nematode to the southern hemisphere. Northcott, 1979), which is evidence for a hoi- The second speciation event gave rise to the arctic distribution. Parelaphostrongylus is known neurotropic specialist P. tenuis, which exhibits only from North America (Anderson, 1972). P. narrow coaccommodation and is the ancestor of tenuis has been reported from a wide variety of

Copyright © 2011, The Helminthological Society of Washington OF WASHINGTON, VOLUME 51, NUMBER 2, JULY 1984 201 locations in eastern North America (Anderson, tween mule deer and wapiti where E. cervi was 1956; Prestwood and Smith, 1969; Gilbert, 1973) present and the subsequent spread of E. cervi and as far west as western Manitoba (Bindernagel into areas occupied only by O. hemionus. and Anderson, 1972) and eastern Oklahoma The current pattern of distribution of muscle- (Carpenter et al., 1972; Kocan et al., 1982). The worm species is considerably more difficult to distribution of P. andersoni has been well doc- explain. The recent report of P. andersoni from umented in the southeastern United States British Columbia (Pybus and Samuel, 1981) oc- (Prestwood et al., 1974). Pybus and Samuel (1981) cupying an area of overlap with P. odocoilei in- have reported this species from white-tailed deer dicates a period of mobilism for P. andersoni in southeastern British Columbia. P. odocoilei associated with the expansion of the range of has been reported from central California (Hob- white-tailed deer. The timing of this movement maierandHobmaier, 1934;Brunetti, 1969), west- is unclear. Kramer (1972) hypothesized that the central Alberta (Platt and Samuel, 1978a), and white-tailed deer in British Columbia represent Vancouver Island, British Columbia (Platt, un- an autochthonous population that survived the publ.). last glacial period in western refugia. The current holarctic distribution of E. cervi The meningeal worm, P. tennis, has not been could be attributed to the colonization of more reported from white-tailed deer in western Can- plesiomorphiccervids(e.g.,v4/ces, Capreolus, and ada (British Columbia, Alberta, and western Sas- Cervus) (Fig. 3) as a result of a period of westward katchewan) despite intensive investigation (Bin- mobilism of Rangifer, broad coaccommodation dernagel and Anderson, 1972; Bindernagel, 1973; within the Cervidae, and the apparent absence Samuel and Holmes, 1974). There are two pos- of competitors in Europe and Asia. Natural in- sible explanations for the absence of P. tennis fections have been reported from five genera of from western North America. The first involves cervids (Anderson, 1968; Kontramavichus et al., two separate periods of mobilism from white- 1976; Kotrla and Kotrly, 1977). Larvae identical tailed deer; one, reaching the west coast and, to those described for other elaphostrongylines, preceding the last glaciation, which resulted in as well as other protostrongylids, have been re- deer harboring P. andersoni but not P. tennis, ported from caribou in Ontario and Manitoba and a later period of mobilism of white-tailed (Lankester et al., 1976), suggesting that E. cervi deer infected with P. tennis. If this scenario is is sympatric with P. tennis in some parts of its correct, P. tennis may eventually reach cervid range. White-tailed deer show no ill effects of populations in and west of the Rocky Mountains, infection with E. cervi in limited experimental as suggested by Bindernagel and Anderson (1972). trials (Lankester, 1976) or under field conditions A more parsimonius hypothesis may relate to (Kotrla and Kotrly, 1977). Although white-tailed differences in biological valence between the deer can harbor infections of E. cervi, competi- muscleworm species and P. tennis. Shostak and tion from P. tennis, which is extremely patho- Samuel (1979) demonstrated significant lowered genic to reindeer, could have resulted in com- infectivity of the first-stage larvae of P. tennis to petitive exclusion and may have prevented the gastropods after exposure to freezing conditions. introduction of E. cervi into populations of O. Larvae of P. odocoilei did not show a similar virginianus. decline in infectivity. Larvae of P. andersoni have The absence of neurotropic elaphostrongylines not been tested, however this species would be in mule deer from western North America may expected to have a response similar to its sister- be explained by a low tolerance of the proto- species, P. odocoilei, and to have the capacity to hemionus population for CNS-inhabiting species. survive freezing conditions. This would result in Experimental infections of P. tennis in mule deer an ecological limitation to the spread of P. tennis, resulted in paralysis and death of the host (An- but not P. andersoni, in accord with the general derson et al., 1966; Tyler et al., 1980). The ab- hypothesis proposed by Samuel and Holmes sence of CNS-inhabiting species could be further (1974). They stated that, "some ecological fea- tested by experimentally infecting mule deer with ture, possibly associated with drier conditions" E. cervi. The prediction being that mule deer prevented the westward spread of P. tennis. This would succumb to the infection or at least show would predict that P. tennis has reached the west- signs of CNS disturbance, thereby reducing host ernmost limits of its range and cannot move far- fitness. This would have prevented sympatry be- ther west without significant ecological changes

Copyright © 2011, The Helminthological Society of Washington 202 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY or human intervention. Recent ecological studies genic effects of P. tennis in wapiti have been well (Kocan et al., 1982) provide circumstantial evi- documented (Carpenter et al., 1973; Trainer, dence for this hypothesis. Single or multiple pe- 1973). riods of mobilism of white-tailed deer would be The role of parasites in altering the range of consistent with this scenario. host organisms can only be approached circum- Success of the host(s) may also play a promi- stantially, as presented above. Range extension nent role in determining the distribution of the is undoubtedly a complex process involving a parasite. This is exemplified by the wide distri- variety of factors. Climate and concomitant bution of P. tennis and P. andersoni in North changes in vegetation during the Pleistocene have America. Range expansion of these species is been used to explain significant shifts in the dis- directly related to the success of the white-tailed tribution of a variety of mammals (Blair, 1958); deer and the wide availability of suitable inter- however, the possibility of a host-parasite com- mediate hosts. The case of P. tennis, which ex- plex acting as a selective agent must be consid- hibits narrow coaccommodation and is patho- ered where the evidence warrants. genic to ecologically similar hosts, is particularly Acknowledgments intriguing. I wish to thank: Dr. W. M. Samuel for his ad- Barbehenn (1969) proposed a "germ warfare" vice and encouragement during the preparation theory of species diversity as a mechanism for of this work; Dr. E. Giffin, Wellesly College, for the maintenance of a competitively inferior host permission to reprint her cladogram of cervid in the presence of a superior competitor. Coe vo- relationships. Editors of journals granted per- lution of the host-parasite complex would pro- mission to print illustrations: Parasitology, Fig- duce a more successful competitor than the host ure Ig; Journal of Parasitology, la; and Canadian alone. Barbehenn (1969), citing the work of Karns Journal of Zoology, Id, h and 1. Dr. A. Woolf, (1966), recognized Pnenmostrongylus (=Pare- Southern Illinois University, provided speci- laphostrongylus) tenuis-O. virginianus as a pos- mens of P. tennis to Dr. W. M. Samuel. This sible example of a host-parasite complex that work was supported by the Natural Sciences and could adversely affect sympatric ungulates. In- Engineering Research Council of Canada (Op- vestigations in Maine (Gilbert, 1973, 1974) and erating Grant A-6601 to W.M.S.) and the Uni- Ontario (Saunders, 1973) have provided circum- versity of Alberta (Dissertation Fellowship to stantial evidence for the reduction of moose (Alces T.R.P.). alces) populations in areas where they are sym- Literature Cited patric with white-tailed deer that have a high prevalence of infection of P. tennis. The patho- Anderson, R. C. 1956. Elaphostrongylus odocoilei Hobmaier and Hobmaier, 1934 in the cranial case logic effects of P. tennis infections in moose (An- of Odocoileus virginianus borealis Miller. Can. J. derson, 1964; Kurtz and Schlotthauer, 1966) Zool. 34:167-173. support his hypothesis. Kelsall and Telfer (1973) . 1964. Neurologic disease in moose infected suggested that P. tennis may have had a role in experimentally with Pneumostrongylus tennis from restricting the range of moose. Experimental in- white-tailed deer. Pathol. Vet. 1:289-322. . 1968. The pathogenesis and transmission of fections of P. tennis in reindeer have also proved neurotropic and accidental nematode parasites of lethal (Anderson, 1971) and Dauphine (1975) the central nervous system of mammals and birds. hypothesized that the failure of reindeer (Ran- Helm. Abstracts 37:191-210. gifer tarandus) to establish in Nova Scotia was . 1971. Neurologic disease in reindeer (Ran- gifer tarandus tarandus) introduced into Ontario. a result of the acquisition of P. tennis from res- Can. J. Zool. 49:159-166. ident white-tailed deer. . 1972. The ecological relationships of me- Wapiti (Cervus elaphus) were widely distrib- ningeal worm and native cervids in North Amer- uted in the northern and central United States ica. J. Wildl. Dis. 8:304-310. . 1978. No. 5, Keys to the genera of the super- following the last glacial period (Hall and Kelson, family Metastrongyloidea. in R. C. Anderson, A. 1959), however they are currently restricted to G. Chabaud, and S. Willmott, eds. CIH Keys to higher elevations in western North America and the nematode parasites of vertebrates. Farnham northern habitats where white-tailed deer do not Royal, Bucks, England. Commonwealth Agricul- typically occur. This tremendous reduction in tural Bureaux. , M. W. Lankester, and U. R. Strelive. 1966. range may be associated with the expansion of Further experimental studies of Pneumostrongy- the O. virginianus-P. tennis complex. The patho- lus tenuis in cervids. Can. J. Zool. 44:851-861.

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