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Lagarocotyle salamandrae n. gen., n. sp. (Monogenoidea, Polyonchoinea, Lagarocotylidae n. ord.) from the Cloaca of Rhyacotriton cascadae Good and Wake (Caudata, Rhyacotritonidae) in Washington State

Delane C. Kritsky Idaho State University

Eric P. Hoberg United States Department of Agriculture, Agricultural Research Service, [email protected]

K. B. Aubry United States Department ofAgriculture, Forest Service, Pacific Northwest Research Station

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Kritsky, Delane C.; Hoberg, Eric P.; and Aubry, K. B., "Lagarocotyle salamandrae n. gen., n. sp. (Monogenoidea, Polyonchoinea, Lagarocotylidae n. ord.) from the Cloaca of Rhyacotriton cascadae Good and Wake (Caudata, Rhyacotritonidae) in Washington State" (1993). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 603. https://digitalcommons.unl.edu/parasitologyfacpubs/603

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. J. Parasitai.. 79(3), 1993, p. 322-330 © American Society of Parasitologists 1993

LAGAROCOTYLE SALAMANDRAE N. GEN., N. SP. (MONOGENOIDEA, POLYONCHOINEA, LAGAROCOTYLIDEA N. ORD.) FROM THE CLOACA OF RHYACOTRITON CASCADAEGOOD AND WAKE (CAUDATA, RHYACOTRITONIDAE) IN WASHINGTON STATE

D. C. Kritsky, E. P. Hoberg*, and K. B. Aubryt College of Health Professions, Idaho State University, Pocatello, Idaho 83209

ABSTRAcr: Lagarocotyle salamandrae n. gen., n. sp. (Lagarocotylidea n. ord., Lagarocotylidae n. fam.) is de­ scribed from the cloaca of the Cascade torrent salamander, Rhyacotriton cascadae Good and Wake (Rhyaco­ tritonidae), from the Lewis River and Wind River drainages of south-central Washington. Lagarocotyle n. gen. is characterized, in part, bya haptor armed with 16 hooks (14 submarginal, 2 subcentral), blind intestinal ceca, a large testis surrounding the germarium, an open male copulatory organ (not tubular), a dextroventral vaginal pore (at level ofcopulatory complex), and an egg lacking filaments; eyes, head organs, seminal receptacle, and haptoral anchors and bars are lacking. Lagarocotyle salamandrae is apparently specific for Rhyacotriton (not having been found in 2 sympatric species of Dicamptodon) and occurs within a limited range of the hosts' distribution, Prevalence varied from 21 % to 32% and intensity ofinfection from 1 to 5 worms/host. Phylogenetic analysis provided a hypothesis for the independent origin ofLagarocotylidea within Polyonchoinea (consistency index = 62.9%).

Monogenoideans are uncommon as parasites ychodactylus japonicus (Houttuyn) (Hynobiidae) ofcaudate amphibians. In the Pacific northwest, in Japan (Ozaki, 1948; Combes, 1965; Timofee­ only the ectoparasitic gyrodactylids, Gyrodacty­ va and Sharpilo, 1979). lus ensatus Mizelle, Kritsky and Bury, 1968, from Ancillary to studies concerning the habitat af­ Dicamptodon ensatus (Eschscholtz) (Dicampto­ finities of stream-breeding amphibians in the dontidae) and Gyrodactylus ambystomae Cascade Range of south-central Washington Mizelle, Kritsky and McDougal, 1969, from Am­ (Bury et al., 1991), specimens ofthe ecologically bystoma macrodactylum Baird (Ambystomati­ similar Cascade torrent salamander (Rhyacotri­ dae), are known (Mizelle et al., 1968, 1969), In ton cascadae Good and Wake), Cope's giant sal­ addition, 4 species of Sphyranura (Sphyranuri­ amander (Dicamptodon copei Nussbaum), and dae) parasitize the gills and skin ofNecturus ma­ Pacific giant salamander (Dicamptodon tenebro­ culosus Rafinesque (Proteidae) and Eurycea ty­ sus Good) were collected and examined for en­ nerensis Moore and Hughes (Plethodontidae) in doparasitic helminths. In the present paper, we North America (Prudhoe and Bray, 1982; Schell, describe a new monogenoidean occurring in the 1985), The only endoparasitic monogenoideans cloacae of Cascade torrent salamanders from 2 described from caudate amphibians are the ia­ disjunct localities in the Cascade Range ofsouth­ gotrematids, Euzetrema knoepffleri Combes, ern Washington. Comments on the phylogenetic 1965, and Euzetrema caucasica Timofeeva and relationships of the new species and the origins Sharpilo, 1979, from the urinary bladders ofEu­ of endoparasitism by monogenoideans in Cau­ proctus montanus (Savi) (Salamandridae) in Eu­ data are presented. rope and Mertensiella caucasica (Waga) (Sala­ mandridae) in western Asia, respectively; and the MATERIALS AND METHODS polystomatid, Pseudopolystoma dendriticum Salamanders were collected from 15 localities in the Cascade Range ofsouthem Washington (Fig. 1) during (Ozaki, 1948), from the urinary bladder of On- 7-30 August 1984 and included 117 R. cascadae (from 8 of 15 geographic sites), 31 D. copei (5 of 15 sites), and 40 D. tenebrosus (9 of 15 sites). An additional 25 Received 31 August 1992; revised II December 1992; R. cascadae were obtained at the Martha Creek site on accepted 4 January 1993. 17 October 1991. Age (Iarva vs. adult) ofsalamanders * United States Department of Agriculture, Agricul­ was determined using criteria presented by Nussbaum tural Research Service, Biosystematic Parasitology et al. (1983). Sampling techniques for collection ofsal­ Laboratory, BARC East 1180, Beltsville, Maryland amanders were as documented by Bury et al. (1991). 20705. Sorne necropsies, conducted shortly after collection, t United States Department ofAgriculture, Forest Ser­ provided living helminths that were fixed in hot buf­ vice, Pacific Northwest Research Station, 3625 93rd fered 10% formalin. Other helminth specimens, also Avenue SW, Olympia, Washington 98512. fixed in 10% formalin, were obtained from hosts that 322 KAITSKY ET AL.-L. SALAMANDRAE N. GEN., N. SP. 323

o 122 W

MT. RAINIER NAT 1ONAl PARK WASHINGTON

MT. SA 1NT • HElENS NAll. MONUMENT \ :.

*- ClEAR CREEK ~ * SI TE Â R. cascadae .* * R. cascadae and D. tenebrosus • o 46 N • R. cascadae and D. cope; ,,** ... • D. tenebrosus 1 1 MARTHA CREEK + D. cope; SITE N

FIGURE 1. Map showing localities in south-central Washington from which salamanders were obtained for parasitological studies. Symbols indicate salamander species (Rhyacotriton cascadae, Dicamptodon tenebrosus, and Dicamptodon copei) that were examined for parasites at each site; assemblages shown do not necessarily represent the actual species composition at each site. The Martha Creek and C1ear Creek sites are those from which Lagarocotyle salamandrae was obtained from Rhyacotriton cascadae.

had been frozen immediately after collection. Mono­ outgroup analyses. The matrix is available through the genoideans were stained in Semichon's acetic carmine University ofNebraska State Museum (HWML 35904). or Gomori's trichrome, dehydrated in a graded series Diagnoses ofthe family and order ofthe new species of ethanol, and mounted (as whole mounts) in Per­ are c1adistic in nature. Numbers in parentheses refer mount. A few specimens (stained or unstained) were to respective characterchanges shown in the c1adogram mounted in Gray and Wess' medium for study ofscler­ and postulated by Boeger and Kritsky (1993). otized structures. Measurements (ail in micrometers), made with the aid of a calibrated filar micrometer, RESULTS represent straight-Iine distances between extreme points Descriptions and are presented as a mean followed by the range and sampIe size (n) in parentheses. Type specimens are Lagarocotylidea n. ordo deposited in the helminth collections ofU.S. National Class Monogenoidea Bychowsky, 1937 Museum (USNM), USDA, ARS, BeItsvilIe, Maryland, Subclass Polyonchoinea Bychowsky, 1937 and the University of Nebraska State Museum Diagnosis: Polyonchoinea; oral sucker absent (19); (HWML), Lincoln. subsurface microtubules absent in spermatozoa (20)­ For phylogenetic analysis, coded character states of postulated (based on phylogenetic analysis); vas defer­ the new species were added to the data matrix offam­ ens looping left intestinal cecum (33); accessory piece ilies of Polyonchoinea utilized by Boeger and Kritsky present in copulatory complex (34); egg filament(s) ab­ (1993) in development of their hypothesis on mono­ sent. genoidean phylogeny. The resuIting matrix was used Remarks: Lagarocotylidea shares sister-group re­ to evaluate hypotheses on evolutionary relationships lationships with Montchadskyellidea Lebedev, 1988, ofthe species from salamanders utilizing Phylogenetic and the taxon containing Dactylogyridea and Gyro­ Analysis Using Parsimony (PAUP; Version 2.4.1; D. dactylidea (Fig. 9). II may he differentiated from L. Swofford, Illinois Natural History Survey, Cham­ Montchadskyellidea by having a ventral mouth (sub­ paign). Seventy-two character states comprising 28 terminal in Montchadskyellidea), an intercecal ger­ transformation series were used in the analysis. Polar­ marium (looping right intestinal cecum in Montchad­ ization ofhomologous series was as provided by Boeger skyellidea), a ventrolateral vagina (midventral in and Kritsky (1993) based on outgroup and functional Montchadskyellidea), and 16 hooks (14 in Montchad- 324 THE JOURNAL OF PARASITOLOGY, VOL. 79, NO. 3, JUNE 1993

skyellidea). It is separated from Dactylogyridea and otized. Testis 143 (103-163; n = 8) wide, 245 (144­ Gyrodactylidea by lacking an egg filament. 322; n = 8) long; vas deferens delicate; seminal vesicle fusiform, with delicate wall; prostatic reservoir vari­ Lagarocotylidae n. fam. able, usually filled with fine granular material; prostatic Diagnosis: With characters of Lagarocotylidea. glands not observed. Germarium pyriform, 85 (58­ 105; n = 9) long, 71 (51-88; n = 9) wide; uterusdelicate; Lagarocotyle n. gen. vagina unsclerotized, pore inconspicuous; vitellaria Diagnosis: Body divisible into cephalic region, trunk, comprising 2 dense bilateral bands, each Iying along peduncle, haptor. Trunk, peduncular surfaces with ir­ respective intestinal cecum; vitelline ducts indistinct. regularly spaced pustules; tegument thickened along Maximum of 1 egg in utero; egg 87 (72-116; n = 4) x trunk, peduncle. Terminal cephalic lobe; head organs 149 (122-179; n = 4), ovate. absent; cephalic glands unicellular, comprising 2 bi­ Type host andlocality: Rhyacotriton cascadae Good lateral groups anterolateral to pharynx, opening via 2 and Wake, Rhyacotritonidae; tributary ofMartha Creek, subterminal bilateral pores near base ofcephalic lobe. Wind River drainage, Gifford Pinchot National Forest, Eyes, pigment granules absent. Mouth midventral; 12.4 km N, 4.6 km W of Stevenson, Skamania Co., pharynx present; esophagus short to nonexistent; bi­ Washington (121°57'24"W, 45°47' 16"N; elevation 610 lateral esophageal glands dorsal to pharynx; wall of m) (17 August 1984; 17 October 1991). bifurcated intestine cellular; ceca nonconfluent poste­ Additional record: Rhyacotriton cascadae; tributary riorly. Gonads ventral to level of ceca; testis U- or ofClear Creek, Lewis River drainage, Gifford Pinchot H-shaped, surrounding germarium with anterior National Forest, 34.4 km S, 1.0 km W ofRandle, Ska­ branches. Vas deferens looping left intestinal cecum, mania Co., Washington (l21°58'16"W, 46°13'25"N; el­ dilated distally to form seminal vesicle; seminal vesicle evation 1,000 m) (21 August 1984). ventral to left cecum; prostatic reservoir dorsal to cop­ Specimens studied: Holotype, USNM 82691; 38 ulatory complex, with delicate wall. Copulatory com­ paratypes, USNM 82692, HWML 35902, 35903. plex sclerotized, comprising articulated male copula­ Etymology: The specific name refers to the host tory organ, accessory piece, prostatic canal. Oviduct group from which the species was collected. short; uterus containing maximum of 1 egg; vaginal Remarks: Numerous characters support placement pore dextroventral at level ofgenital pore; seminal re­ ofthis species as a member ofPolyonchoinea. Among ceptacle absent; vitellaria present; egg operculate, lack­ them, presence ofa sclerotized male copulatory organ, ing filaments. Haptor cup-shaped, armed with 16 un­ a ventral mouth, and 8 pairs of hooks (7 submarginal, hinged hooks (14 submarginal, 2 subcentral); hook with 1 subcentral) appear most significant. In addition, the slender shank, protruding thumb, weil developed do­ cellular structure of the intestinal wall supports place­ mus; anchors, bars absent. Internai parasites ofaquatic ment of the species in this subclass. Staining and amphibians. mounting techniques used in this study suggest that Type species: Lagarocotyle salamandrae n. sp. only 1 type of gut cell is present in L. salamandrae, Etymology: The generic name is from Greek (La­ which is consistent with findings from studies on the garos = empty + kotyle = cup-shaped cavity) and refers uItrastructure ofcecal cells in most other polyonchoi­ to the haptor lacking anchors and bars. neans: E. knoepjJIeri by Bekkouche et al. (1974); Cal­ Remarks: Lagarocotyle is monotypic. icotyle kroeyeri Diesing, 1850, by HaIton and Stranock (1976); and Tetraonchus monenteron (Wagner, 1857) Lagarocotyle salamandrae n. sp. by Junchis (1988). In contrast, the gut of Gyrodactylus (Figs.2-5) eucaliae Ikezaki and Hoffman, 1957 (Polyonchoinea) Description: Body 885 (605-1,230; n = 16) long, fu­ is syncytial (Kritsky and Bourguet, unpubl. obs.), which siform; trunk with nearly parallel margins, greatest width apparently represents a derived state. The structure of 314 (254-398; n = 18). Cephalic lobe broad, directed the intestinal walls of members of the subclasses Po­ slightly anteroventrally. Pharynx spherical, 152 (92­ Iystomatoinea and Oligonchoinea is also derived and 188; n = 17) in diameter; cells of intestinal wall low comprises 2 cell types, 1 of which is involved in di­ columnar (Figs. 6-8). Peduncle broad; haptor ovate, gestion of blood (see Rohde [1980) for review). La­ cup-shaped, 214 (158-257; n = 18) wide, 152 (126­ garocotyle salamandrae, along with most other 177; n = 10) long. Hooks similar; each 28 (26-30; n polyonchoineans, apparently exhibits the symplesio­ = 42) long, with prominent depressed thumb, short morphic state for Monogenoidea. A cellular gut com­ point, heavy shaft, uniform shank; domus about 0.8 prising a single cell type also occurs in rhabdocoels shank length. Male copulatory organ 45 (38-50; n = (Holt and Mettrick, 1975) and sorne digeneans and 31) long, evenly curved, open along entire length, re­ aspidobothreans (Dike, 1967; Rohde, 1971; Hatha­ sembling tip ofhypodermic needle; accessory piece 55 way, 1972; and others). (51-63; n = 32) long, comprising variably cavernous Two features distinguish L. salamandrae. Appar­ basal rod, terminal recurved hook; prostatic canal 88 ently the egg filament(s), generally present in mono­ (75-111; n = 34) long, elongate, tubular, heavily scler- genoideans, have been secondarily lost. AIthough the

FIGURES 2-5. Lagarocotyle salamandrae n. gen., n. sp. 2. Ventral view of holotype. 3. Hook. 4. Egg. 5. Copulatory complex (ventral view). ap, accessory piece; cg, cephalic gland; eg, esophageal gland; i, intestinal cecum; mco, male copulatory organ; 0, germarium; p, pharynx; pc, prostatic canal; pr, prostatic reservoir; sv, seminal vesicle; t, testis; u, uterus; v, vaginal pore; vi, vitellaria. KRITSKY ET AL.-L. SALAMANDRAE N. GEN .• N. SP. 325

'"N

3 326 THE JOURNAL OF PARASITOLOGY, VOL. 79, NO. 3, JUNE 1993

FIGURES 6-8. Photomicrographs (interference microscopy) of the wall of the intestine of Lagarocotyle sal­ arnandrae n. gen., n. sp. 6. Medial walls of terminal portions of the 2 intestinal ceca. 7. Lateral view of low columnar cells in the wall ofthe intestine. 8. Surface view ofIow columnar cells ofthe intestinal wall. Respective scale bars are in micrometers. male copulatory organ is sc\erotized in L. salarnandrae. 1); 31 (22%) of 142 R. cascadae coIlected from it is not tubular as usually always occurs in other mem­ aIl sites were infected. Twenty of 79 (40 adults; bers of Polyonchoinea. 391arvae) R. cascadae(prevalence 25%; intensity 1-5; mean intensity 1.9 ± 1.21) were found in­ Phylogenetic analysis fected at the Martha Creek site in 1984. Among Our hypothesis for the independent origin of these 20 hosts, Il were adult salamanders (prev­ Lagarocotylidea within Polyonchoinea sensu alence 27.5%; intensity 1-5; mean intensity 2.45 Boeger and Kritsky (1993) is provided in Figure ± 1.37) and 9 were larvae (prevalence 23%; in­ 9. The hypothesis, 1of17 trees produced through tensity 1-2; mean intensity 1.22 ± 0.44). On 21 PAUP analysis (CI = 62.9%), provides the most August 1984 at the Clear Creek site, 14 Cascade parsimonious explanation of transformation of torrent salamanders (6 adults, 8 larvae) were ex­ character states associated with the apparent 10ss amined, and 3 adults were found infected (prev­ of haptoral anchors and/or bars in L. salaman­ alence 21 %; intensity 1-3; mean intensity 2.0 ± drae. In that hypothesis, the symplesiomorphic 1.0). On 17 October 1991, 8 L. salamandrae ventral anchor pair is postulated to have been were obtained from 8 of 25 specimens of this 10st in Lagarocotyle prior to development ofthe species from the Martha Creek site (prevalence bar(s) ofthe polyonchoinean haptor (see Boeger 32%; intensity 1; 7 of 14 [50%] adults and 1 of and Kritsky, 1993). Il [9%] larvae infected). Individual infections of more than 1 worm typicaIly comprised both ju­ Prevalence and intensity venile and mature flukes, whereas gravid monog­ Lagarocotyle salamandrae was obtained from enoideans only occurred as single parasite infec­ R. cascadae at only 2 of the 8 10calities where tions. Cascade torrent salamanders were examined (Fig. Dicamptodon tenebrosus occurred in sympatry KRITSKY ET AL.-L. SALAMANDRAE N. GEN., N. SP. 327 with R. cascadae at 5 sites, including both Mar­ tha Creek and Clear Creek, and D. copei occurred o in sympatry with R. cascadae at 2 sites (Fig. 1). o ()) o o ()) :g ()) ()) Although D. tenebrosus and D. copei were ex­ :g 'Cl :g amined from these sites as well as from 4 and 3 o .:: ~ ()) € >­ ~ additional sites, respectively, where they were o :g ü 0> ü ü o o collected alone (Fig. 1), L. salamandrae was not o g Q ~ 'Cl obtained from either species. c Q. o ü o o o o0> o >. DISCUSSION 2 o -l o (!) Host-parasite evolution 6,57 42-45 The distribution of L. salamandrae presents an enigma with respect to the postulated phy­ logenetic relationships for hosts and parasites and 4(),41 the biogeographic history of the Pacifie north­ west during the Tertiary period. The higher-level systematics ofthe caudate Amphibia and the ab­ sence of helminths similar to Lagarocotyle in othersalamanders (or fishes) in the Pacifie north­ west confuses the development of testable hy­ FIGURE 9. Cladogram depicting the proposed evo­ lutionary relationships ofLagarocotylidea within Poly­ potheses for the association of this monogenoi­ onchoinea (Monogenoidea). Slashes with numbers re­ dean with Cascade torrent salamanders. Until fer to postulated evolutionary changes suggested by recently, Rhyacotriton and Dicamptodon were Boeger and Kritsky (1993). Evolutionary changes: 7, referred to Dicamptodontidae (see Tihen, 1958). mouth ventral; 8, sperm microtubules Iying along '/. ofcell periphery; 9, male copulatory organ sclerotized; Edwards (1976) supported this classification and 10, male copulatory organ muscular, elongate; Il, spines postulated a sister-group relationship for the Di­ of male copulatory organ absent; 12, 14 marginal, 2 camptodontinae (containing Dicamptodon) and central hooks (oncomiracidium); 13, 14 marginal, 2 the Rhyacotritoninae (containing Rhyacotriton) central hooks (adult); 14, 2 sperm axonemes, 1 re­ within the Dicamptodontidae, as basal members duced; 15, 14 marginal hooks (oncomiracidium); 16, 14 marginal hooks (adult); 19, oral sucker absent; 20, of the Ambystomatoidea. However, subsequent sperm microtubules absent; 21, single genital aperture consensus based on morphological characters and marginal; 33, vas deferens looping left cecum; 34, ac­ molecular-level analyses suggests that Dicamp­ cessory piece present; 35, mouth subterminal; 36, gut todontidae as conceived by Edwards (1976) is diverticula present; 37, germarium/oviduct looping right cecum; 38, 14 marginal hooks (adult); 39, 1 mid­ polyphyletic or paraphyletic (Larson, 1991; ventral "true" vagina; 40, egg tetrahedric; 41, 1 ventral Sever, 1991); the latter authors postulated Di­ bar; 42, 2 ventral bars; 43, 16 marginal hooks (oncomi­ camptodontinae to have a sister-group relation­ racidium); 44, 16 marginal hooks (adult); 45, hook ship with Ambystomatidae, whereas Rhyacotri­ hinged; 56, 2 pairs of ventral anchors; 57, sperm with toninae does not share clear affinities with any 1 axoneme. extant genus of salamanders (Larson, 1991) or may share a sister-group association with Pleth­ Peninsula ofWashington (Nussbaum et al., 1983). odontidae and Proteidae (Sever, 1991). Good and Studies by Good and Wake (1992) show that 4 Wake (1992) elevated Rhyacotritoninae to fam­ species occupy the range. They suggested that ily level based on analyses indicating that Rhy­ populations ofRhyacotriton became isolated from acotriton is phylogenetically isolated and has no one another 6-11 million years ago and that an­ clear sister-group relationship to any contem­ cestral Rhyacotriton may have been present in porary taxon including Dicamptodon and Am­ the northem coastal forest ecosystem since the bystoma. Thus, the evolutionary distinctiveness upper Oligocene or lower Miocene epochs with of Rhyacotritonidae (and potential status as a dispersal into the Cascades occurring 15-22 mil­ relict according to Duellman and Trueb [1986]), lion yearsago (Goodetal., 1987; Goodand Wake, rather than historical ecological associations, may 1992). Subsequent isolation of host populations account for its unique helminth fauna (see Mar­ may thus have coincided with the continued tec­ tin, 1966). tonie development in the northwest during the Rhyacotriton is endemic to the Pacifie coastal late Tertiary period (see Cole and Armentrout, region from northem Califomia to the Olympie 1979). However, it is apparent that the diversi- 328 THE JOURNAL OF PARASITOLOGY. VOL 79, NO, 3, JUNE 1993 fication ofRhyacotriton was associated with long­ drae is specific for R. cascadae and that it may term residence in the northwest since the mid­ inhabit a restricted range within the distribution Tertiary period. Lagarocotyle salamandrae is of the host genus. known only in 1 species, R. cascadae. from near Both larvae and adults of R. cascadae were the northern limits of its range. These distribu­ collected at Martha Creek in 1984 and 1991. In tions suggest that the parasite has experienced 1984, no substantial difference in the prevalence long-term isolation as a relict or was a colonizer or intensity of infection was apparent with re­ from another vertebrate host group. spect to age class of the salamanders. However, Llewellyn (1965) postulated that the plesio­ prevalence in adult salamanders was higher than morphic habitat for monogenoideans is the skin that of larvae at Clear Creek in 1984 (3 of 6 and/or gill surfaces of their respective hosts. Of adults; 0 of 8 larvae) and among the 25 sala­ monogenoideans parasitizing caudate amphibi­ manders examined from Martha Creek in 1991 ans, endoparasitic species are members only of (7 of 14 adults; 1 of II larvae). This suggests that the families Iagotrematidae, Lagarocotylidae, and L. salamandrae remains in the host for pro­ Polystomatidae, all comprising phylogenetically longed periods following infection. disparate taxa lacking sister-group relationships Each infected salamander at Martha Creek in (Boeger and Kritsky, 1993). Similarly, caudates 1991 was parasitized by a single, fully developed, ofthe families Hynobiidae, Salamandridae, and gravid specimen. However in 1984 (at Martha Rhyacotritonidae that serve as hosts for internai Creek and Clear Creek) multiple infections (2-5 monogenoidean parasites are also distantly re­ ftukes/host) were noted in 13 of 23 infected sal­ lated phylogenetically. Thus, these phylogenetic amanders (lI adults; 2 larvae); only 10 sala­ incongruences among the host and parasite taxa manders (3 adults, 7 larvae) were infected with are compatible with a hypothesis for multiple single worms. In multiple infections worms were origins (3 instances of independent derivation) consistently smaller and usually had not attained of endoparasitism by monogenoideans (urinary a comparable state ofdevelopment compared to bladder or cloaca) among caudate amphibians. those from single infections. Thus, in weil estab­ However, the occurrence of the 2 species ofEu­ lished infections only single gravid worms may zetrema in salamandrids from Eurasia may rep­ be present, suggesting the potential for compet­ resent a coevolutionary association. itive exclusion as a factor inftuencing intensity. Additionally, the occurrence of multiple infec­ Host-parasite ecology tions ofimmature ftukes in larval and adult hosts In a series of studies in western Oregon, 46 indicates that transmission ofL. salamandrae is specimens ofRhyacotriton species (originally re­ not limited to a particular age class of R. cas­ ported as R. olympicus Gaige but apparently in­ cadae. cluding both R. variegatus Stebbins and Lowe, Torrent salamanders, Rhyacotriton spp., are and R. kezeri Good and Wake based on geo­ among the most highly aquatic of the salaman­ graphic range, see Good and Wake [1992]) and ders occurring in the Pacific northwest, being approximately 136 D. cf. tenebrosus (reported as typically confined to the splash zone or shallows D. ensatus, see Good [1989]) were examined for of small, cold, mountain streams (Nussbaum et helminths (Lynch, 1936; Senger and Macy, 1952, al., 1983; Bury et al., 1991). Although a fully 1953; Lehman, 1954; Anderson et al., 1966; aquatic life history would not be required in the Martin, 1966). Although 4 species of Digenea host for transmission of L. salamandrae, pro­ were collected from these salamanders, endo­ longed contact with lotic habitats by the sala­ parasitic monogenoideans were not reported in manders (both larvae and adults) may enhance these studies. Additionally, parasitological stud­ the possibility for completion ofthe life cycle. In ies of Ascaphus truei Stejneger and Rana spp. contrast, giant salamanders (Dicamptodon spp.), occurring in sympatry with Rhyacotriton and Di­ although inhabiting streams as larvae, usually are camptodon spp. have not resulted in records for found in terrestrial habitats of moist coniferous endoparasitic monogenoideans (Pratt and forests as metamorphosed adults (Nussbaum et McCauley, 1961; Schell, 1964; Jansen and Van al., 1983). This difference in habitat preference Haaften, 1968). Although the number of sala­ and the distant phylogenetic relationship of Di­ manders examined for the current study was camptodon and Rhyacotriton may explain the small, our results and those of previous parasi­ absence ofL. salamandrae as a parasite ofgiant tological investigations suggest that L. salaman- salamanders. KRITSKY ET AL.-L. SALAMANDRAE N. GEN., N. SP. 329

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