Gulf and Caribbean Research

Volume 9 Issue 2

January 1995

Levinseniella deblocki, New Species (: : ) from Salt Marshes along the Eastern Gulf of Mexico with Notes on Its Functional Morphology and Life History

Richard W. Heard Gulf Coast Research Laboratory, [email protected]

John M. Kinsella

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Recommended Citation Heard, R. W. and J. M. Kinsella. 1995. Levinseniella deblocki, New Species (Trematoda: Digenea: Microphallidae) from Salt Marshes along the Eastern Gulf of Mexico with Notes on Its Functional Morphology and Life History. Gulf Research Reports 9 (2): 97-103. Retrieved from https://aquila.usm.edu/gcr/vol9/iss2/3 DOI: https://doi.org/10.18785/grr.0902.03

This Article is brought to you for free and open access by The Aquila Digital Community. It has been accepted for inclusion in Gulf and Caribbean Research by an authorized editor of The Aquila Digital Community. For more information, please contact [email protected]. Research Reports, Vol. 9, 2,97-103,1995 Gulf No. Manuscript received September 12.1994; accepted October 17,1994

LEVINSENIELLA DEBLOCKI, NEW SPECIES (TREMATODA: DIGENEA: MICROPHALLIDAE) FROM SALT MARSHES ALONG THE EASTERN GULF OF MEXICO WITH NOTES ON ITS FUNCTIONAL MORPHOLOGY AND LIFE HISTORY

Richard W. Heard’ and John M. Kinsella2 ‘InvertebrateZoology Section, Gulf Coast Research Laboratory, P.O. Box 7000, Ocean Springs, Mississippi 39566-7000, USA 22108 Hilda Avenue, Missoula, Montana 59801, USA

ABSTRACT Levinseniella (Austromicrophallus)deblocki, n. sp., was collected during parasitologic studies of homeothermic vertebrates from salt marshes along the coast of the eastern Gulf of Mexico. Because L. deblocki lacks a femalepouch, it belongs to the subgenus Monarrhenosproposed by Deblock and Pearson (1970). However, since Deblock and Pearson did not explicitly designate a type species for Monarrhenos,it is not available and is a ”en nudum. The next available name, Amtormicrophallus Szidat, 1964, a genus synonymized with LminseniellaStiles andHassall, 1901by Deblock (1978), is reinstatedas a subgenus toreceive the species lacking a female pouch and previously assigned to Monarrhenos. The adult of L. deblocki is found in the lower digestive tracts of the clapper rail (Rallus Zongirostris), rice rat (Oryzomys palustris), and raccoon (Procyon lotor). Morphologically, L. deblocki appears to be most similar to L. polydactyla Deblock and Rose, 1962, known from Europe, and L. ophidea (Nicol, Dameree, and Wootton, 1985), described from a freshwater habitat in California. Differences in the life cycle, habitat type, and geographic distribution, plus a combination of distinctive morphological characters (presence of lappets on the oral sucker, number of genital pockets, and body size) separate L. deblocki from the other members of the subgenus Austromicrophallus. The metacercarial stage of L. deblocki occurs in the gonads of fiddler (Wca spp.) and the fist intermediate host appears to be a hydrobud gastropod (Heleobops sp.). Observations on living and preserved specimens fixed in copula indicate that the genital atrium functions as an eversible hermaphroditic organ bearing the male papillae and metraterm. The genital hooks or “Jagerskiold’s bodies” appear to function as holdfast structures during copulation.

INTRODUCTION Living metacercariae were excysted in saline-typsin solution at 39OC; excystment usually occurred within 12 During parasitologic studies of homeothermic hours. Copulatingpairs of worms were obtainedbyplacing vertebrates from salt marshes along the coasts of the 50 to 100 excysted metacercariae together in warm saline northeastemandsoutheasmGulfofMexico, wediscovered (39°C). Copulating pairs were examined alive or were an undescribed species of the microphallid genus heat-killed in hot saline and fmed in AFA (with or without Levinseniella Stiles and Hassall, 1901. The adult stage of coverslip pressure). Some of the fmed copulating pairs this species occurred in the lower digestive tracts of clapper were separated for stained slide preparations, while others were mounted still copula. A Wild-20 drawing tube rail;, rice rats, and raccoons. The new species appears to in bemost closelyrelatedto L. polydactyla DeblockandRose, (camera lucida)aided in the preparation of the illustrations. 1962, known from Europe, and L. ophidea (Nicol et al., All measurements are in micrometers (m). 1985), described from a freshwater habitat in California. Type material (holotype and paratypes) are deposited in the National Parasite Collection of the US National Museum (USNM), Beltsville, Maryland. Additional MATERIALS paratypes in the collections of the Museum of the Gulf AND METHODS are Coast Research Laboratory (GCRL). Living and fixed specimens of excysted metaceriae from fiddlercrabs (Ucaspp.) and adults from naturally and RESULTS: experimentally infected vertebrate hosts were examined microscopically. Specimens were killed in hot saline with Genus LevinsenieUa Stiles and Hassall, 1901 and without coverslip pressure, then immediately fixed in MA,stained inErlich’shematoxylin, dehydrated, cleared, Synonyms. Austromicrophall us S zidat, 1964. and mounted in Permount (TM). Heardlevinseniella Y amaguti, 197 1.

97 HEARD AND ”SELLA

Subgenus Austromicrophallus Szidat, 1964, n.comb name available for those species lacking a female pouch and assigned to Monarrhenos sensu Deblock and Pearson Synonym. Monarrhenos Deblockand Pearson, 1970 (1970). Levinseniella anenteron andL. cupitanea areboth (p. 784) Nomen nudum. characterized by the absence of digestive ceca. Following Diagnosis. Species of Levinseniella lacking a female Overstreet and Perry (1972) and Deblock (1978), we pouch. consider the absence of digestive ceca to be ahighly derived Type species. Levinseniella (Austromicrophallus) character not warranting generic or subgeneric standing on anenteron Szidat, 1964. its own. Other species referred to Austromicrophallus: L. pellucida Jagerskitild, 1907; L. amnicolae Etges, 1953; L. Levinseniella deblocki, new species Polydactyla Deblock and RosC, 1962; L. byrdi Heard, Figure 1 A-G. 1968(a); L. hunterae’ Heard, 1968(b); L. munodactyla Deblock and Pearson, 1971; L. capitanea Overstreet and Synonyms. “Levinseniella sp. 2 (Heard, comm. Perry, 1972; and L. ophidea Nicol, Damaree, and Wootton, 6crite)”: Deblockand Pearson(197 1,p.787; “Levinseniella 1985; L. ucatanensis Carnaris and Ching, 1989. sp. 2 (Heard, communicaion Ccrite)”: Deblock (1971, p. Heard( 1968)dividedthegenus Levinseniellaintofour 449); “Levinseniellasp. 2 (HeardIn:Deblock and Pearson, groups based on the presence or absence of a female pouch 1971)”: Nicol et al. (1985, p. 182); Levinseniella sp. A and the relative number of atrial pockets (“male pockets” Heard (1976,pp.83-98); Levinseniella sp.: Kinsella (1988, of some authors) present. Deblock and Pearson (1970) pp. 276,277); Levinseniella sp.: Forrester (1992, [in part], proposed the subgenus Monarrhenos to receive the species p.95, 189). of Levinseniella that lack a female pouch. They did not, Description (based on 10 mature worms). Body however, explicitly designate a type species or give a elongate, 777 to 1020 long by 220 to 278 wide in posterior bibliographic reference to a proposed type species for their third of body. Tegument spinose; spines becoming smaller “new subgenus” as required under Article 13 of the and less conspicuous posteriorly, completely embedded in International Code of ZoologicalNomenclature. Therefore, hindbody tegument. Oral sucker subterminal with well- Monarrhenos cannot be considered an available name and developed ventrolateral papillae (lappets). Postoral is a nomen nudum. In his 1971 treatise, which was in press muscular ring immediately posterior to oral sucker. when Deblock and Pearson’s 1970 paper designating the Prepharynx 34 to 62 long. Pharynx 47 to 56 long by 43 to subgenus Monarrhenos was published,Yamaguti described 47 wide.Esophagus 136to2121ong.Cecae welldeveloped, themonotypicgenus Heardlevinseniella toreceive L. byrdi extending posterolateral and ending near lateral margins Heard, 1968. He characterized this genus by the absence of body at level of acetabulum. Acetabulum recessed, 75 to of a female pouch and the presence of a postoral muscular 98 long by 63 to 93 wide. Forebody 63 to 73% of body ring and oral lappets. Because there are several other length. species that lack a female pouch (Heard‘s Groups III and Testes immediately posterior to acetabulum, IV), have alargeoralsucker,andhavea“postoralmuscular symmetrical, usually wider long; right testis 38 to 67 ring,” Overstreet and Perry (1972) synonymized than long by 57 to 78 wide; left testis 44 to 58 long by 67 to 95 Heardlevinseniella with Levinseniella. Deblock (1978) wide. Seminal vesicle-pars prostatica complex surrounded redescribed Austromicrophallus anenteron Szidat, 1964, by membrane, retort-shaped, located intercecally a poorly-known monotypic species from gulls collected thin immediately anteriorto acetabulum; seminal vesicle 115 to along the coast of Patagonia (Szidat, 1964). Based on the 155 long by 46 to 75 wide; pars prostatica thick walled, presence of atrial pockets and the absence of a female 60 to 75 long by 42 to wide, surrounded by numerous pouch, Deblock (1978) synonymized the monotypic 50 prostatic cells. Male genitalpapillaa relatively small blunt Austromicrophallus Szidat, 1964 with Levinseniella and cone, 28 to 32 long by 28 to 30 wide at base, penetrated at placed A. anenteron in Monarrhenos. Thus base by ejaculatory duct, sperm duct opening at its tip. Austromicrophallus Szidat, 1964 is the oldest subgeneric Genital pockets sinistral to genital pore, 8 to 14 in number; embeddedinwall of eversiblegenital atrium; atrium, when not everted, with male papilla just under upper margin of genital pore; everted atrium protrudes through dilated Originally, Heard (1968b) named this species for Wanda S. Hunter, but genital pore, forming large large papilla-like structure, 95 incorrectly gave it the masculine ending “i” instead of the feminine “ae.” to 110 in diameter (Figure 1, B-E).

98 NEWMICROPHALLID TREMATODE

1

2

Figure 1. Levinseniellu deblocki, n.sp.- A, ventral view of entire, mature worm; B-E, ventral views of ventral mid-region of body illustrating acetabulum and associated terminal genitalia. B, hermaphroditic organ retracted, genital pore not dilated; C, genital pore dilated, hermaphroditic organ beginning to protrude from genital pore; D, hermaphroditic organ (everted genital atrium) completely protruded through genital pore; E, protruded hermaphroditic organ under coverslip pressure showing openings of male papilla and metraterm); F, lateral aspect of oral sucker, post oral ring, pharynx, and lateral lappets; G, apical view of specimen showing lateral lappets adjacent to oral sucker. Scales = 100 m, scale 1for A-E, scale 2 for F and G.

Ovary immediately anterior to right testis, dextral to atrium at base of male papilla. Eggs, 18 to 21 long by acetabulum, 57-73 long by 73-113 wide. Wtype, Laurer’s 11 to 13 wide. canal, and Mehlis’ gland located in intertesticular region. bladder U-~haped;~OE Subterminal, acinose, six seven relatively Excretory dorsal. Vitellariapost-testicular, to Flame cell formula 2[(2+2)+(2+2)]=16. large follicles on each side. Uterine loops not reaching Holotype (USNM 84540). anterior to testes. Metratenn beginning in intertesticular Paratypes. patatypes: 1Specimen~mRuZZuSlongirostr~s region, passing dorsally along sinistral side of (USNM 84541), 1 specimen fromRullu~longirostris (GCRL acetabulum, opening into dorsal portion of genital 1338); 1excystedmewmma . hm Ucupunuceu (CQU, 1339).

99 HECARD AND -SELLA

Type host. Rallus longirostris Boddaert (clapper rail). marine isopod (Sphueroma hoockeri Leach) from France Site of infection. Intestinal ceca: (Deblock and Rose 1972). It is distinguished from L. Type locality. Upper Tampa Bay (June 1965). polydactyla by having an oral sucker with a pair of Mammalian hosts. Oryzomys palustris, rice rat (in ventrolateral lappets, a well-developed postoral muscular large intestine); Procyon lotor (L.), northem raccoon (in ring, and a greater range in the number of genital pockets large intestine). (8 to 14), compared with 10 to 12 in L. polydactyla. Localities. MarcoIsland (CollierCounty), Florida(P. lotor); Cedar Key (Levy County), Florida (0.palustris). I Etymology. This species is named for Professor OBSERVATIONS Stkphane Deblock in recognition of his many contributions to the study of the systematics and biology of the family Functional Morphology of the Terminal Genital during Microphallidae. Mating Second intermediatehosts(Ucaspp.). U.longisignalis Salmon and Atsaides - Little Dauphin Island (Mobile Observations on the possible function of the genital County), Alabama; Cedar Key (Levy County), Florida. U . atrium, the acetabulum, and the genital pockets or panacea NovakandSalmon-HomIsland, JacksonCounty, “Jggerski6ld’s bodies”w“adeo“thgpaisofL.&blocki. Mississippi.- U. pugilator (Bosc)- Cedar Key, Florida Copulating pairs of worms were obtained by placing 50 to (Kinsella, 1988). 1OOexcystedmetacercariaetogetherin warm saline (39°C). Metacercaria. Cysts spherical,350 to45Oindiameter When these specimens were examined after 1 to 2 hours, (from naturally infected Ucapanacea collected from salt usually 25% or more of them were found in copula . marshes adjacent to Big Lagoon on Horn Island, Study of living and permanently mounted specimens Mississippi). in copula demonstrated that during copulation, the entire Site of infection. Gonads (testes and ovaries). “genital atrium” everts to form a large hermaphroditic Taxonomic Remarks. The absence of a female pouch organ bearing the male papilla, the genital pockets and the places Levinseniella deblocki into the new subgenus opening of the metraterm (see Figure 1 B-E). When the Heardlevinseniella and the absence of a female pouch hermaphroditic organ was everted, the acetabulum rotated coupledwithmore than five genitalpockets(“male pockets”) 60 to 80” and partially retracted into the dextral wall of the places it in subgroup IV of Heard (1968a). In addition to body, leaving a deep cavity or “acetabular genital atrium” L. deblocki,four other species (L.polydactyla Deblockand large enough for the insertion of the genital organ of the Rok, 1962; L. hunterae2 Heard, 1968; L. capitanea partner. During copulation, the acetabulum of each worm Overstreet and Perry, 1972; and L. ophideaNicol, Dameree, functions as a true genital sucker by attaching to the lateral and Wootton, 1985) are presently referable to Heard‘s wall of the partner’s hermaphroditic organ. The genital subgroup. Levinseniella capitanea differs from pockets (Jlgerskio1d’sbodies)ofeachwormthenpartially Levinseniella deblocki by the former’s much larger size, evert and mesh with those of its partner. While in copula, more numerous genital pockets (11-2 l), and the absence of the terminal genitalia of each worm lies immediately a pharynx and digestive ceca. Both ecological and opposite that of its partner, allowing the male papilla of morphological differences distinguishL. deblocki from L. each worm to be inserted simultaneously into the opening ophidea. Levinseniella ophidea utilizes leeches as second of the other’s metraterm, thus facilitating the exchange of intermediate hosts, frogs and snakes as definitive hosts, sperm (cross-fertilization). Excysted worms maintained at and occurs in freshwater stream habitats (Nicol, Demaree, 39°C in saliie produced eggs withii 24 hours. and Wootton 1985). Morphologically, L. ophidea is distinctly larger than L. deblocki and lacks lappets on its Life oral sucker. The presence of amassivemale papilla and the History absence of a pair of well-developedventrolateral lappets on The adult stage of Levinsenielladeblockiappears tobe the oral sucker of L. hunterae separatesit from L. deblocki. a well-established parasite of both mammals and birds. Levinseniella deblocki appears to be most similar to L. Clapper rails serve as an avian host for L. deblocki along polydactyla, described from the metacercaria stage in a theGulfCoastofHorida(Heard1976). Althoughmammals havebeen experimentally infected with Levinseniella (see Bridgmanet al. 1972), the occurrence of L. deblocki in rice Originally. named this species for Wanda S. and raccoons from salt marshes along the Gulf Coast Heard (1968b) Hunter, but rats gave it the ending instead of the feminine of Florida established first records of the genus in incorrectly masculine ”i” “ae.“ the

loo NEW MICROPHALLIDTREMATODE naturally infected mammals (Heard 1976; Kinsella 1988; and definitive hosts appears to be directly related to the Forrester 1992). presence of the suspected gastropod host, Heleobops sp. InformationonthelifecycleofL.deblockiisincomplete, but a hydrobiid (Heleobops sp.) from salt marshes on Horn Island, Mississippi, shed a microphallid cercaria that DISCUSSION appeared to be its larva. In an experiment, this cercaria penetrated U .longisignulis and formedcysts in the gonads A variety of malacostracan , and in one within 48 hours. Due to high mortality in the fiddler crabs instance a leech, hate been reported to be the second used in this experiment, development to the mature intermediate hosts for species of Levinseniellu. However, metacercarial stage did not occur. The suspected cercaria more detailed morphological and life history studies are of another microphallid Gynuecotyla sp. also occurs in needed, especially for species occurring in Eurasia, before Heleobops sp. from the same area. These two cercariae can many of these reports can be verified. be distinguished from each other by their stylet lengths. Amphipods and isopods have been reported as second The stylet length of the Levinseniellu-like cercaria was 17 m, intermediate hosts for several species of Levinseniellu whereas the stylet length of the Gynaecotyla-like cercaria (Villot 1875;Etges 1956;Ouspenskaia 1960,1963; Deblock was 22 m. and Rose 1962; Reimer 1963; Rebecq 1964; Heard 1970, The infected fiddler and vertebrate hosts of L. 1976; Galaktionov 1988; GalaktionovandMalkova1993). Besides deblocki, several other species of Levinseniella deblocki occurred sporadically in the higher salinity salt L. marshes along the edge of the eastern Gulf of Mexico. The are known to use decapods as second intermediate hosts distribution partem of these infected second intermediate (see Table 1).

TABLE 1

Decapod crustaceans reported as hosts of Levinseniellu.

Species of Levinseniella Second intermediate host(s) Reference( s) L. brachysoma sensu Palaemnetes punicis Balozet and Callot Balozet and Callot* (1939)

L. capitanea Callinectes sapidu Overstreet and Peny (1972) L. caracinides** Carcinides maenas Rankin (1939) L. conicostoma penicillatus Bridgman et al. (1972). Kifune and Tho(1972) L. cruzi sensu Palaemnetes argentinus Martorelli and Schuldt (1990) Mortonrelli and Shuldt Schuldt and Lunaschi [1985(1987)] Uca isignalis, panacea, Heard L. deblocki, n. sp. Ion U. (1976) [as L. sp A], U. pughtor, U. rapar Kinsella(1988) [as L. sp.], present report L. 4. ellucia'a Astacus lepodac~luseichwaldi Nikitina sensuhcitina (1983)

Levinseniella sp.*** Upogebia @nis Pearse (1945) Levinsmiella sp. Uca sp. Cable et al. (1960) Levinsmiella sp. C Rhithropanopeus harrisii Heard (1976) Levinseniella sp. Portunus pelgicus Shields (1992) Levinsmiella sp. Pachygrapsus tansversus Bush et al. (1993)

* **

101 HEARD AND &SELLA

Some of the earlier reports of Levinseniella us (RWH,unpublisheddata)examinedover100 specimens metacercaria in decapod crustaceans may be erroneous or of this mud shrimp from the Beaufort area and found no need confinnation. Balozet and Callot (1939) reported the microphallid metacercariae. shrimp, Palaemonetespunicis, from Tunisian waters as an Levinseniella ophidea is the only species known to use intermediate host of L. pellucida; however, Yamaguti noncmstacean second intermediate hosts. The metacercarial (1958, page 886) questioned the identity of their material, stage of this species was reported in four species of leeches indicating that it was probably a species of from a California freshwater stream habitat (Nicol et al., Ward, 1901. After studying the description and figure 1985). I given by Balozet and Callot, we concur with Yamaguti that the Tunisian specimens do not belong to the genus ACKNOWLEDGMENTS Levinseniella. Rankin (1939) suspected the green crab, Carcinides menus (L.),tobethesecondintermediatehost of L. carcinides Rankin, 1939, a species described from We wish to thank Robin M. Overstreet and Donald J. New England; however, this conjecture has not been Forrester for advice, encouragement, and material support confiied. The metacercariamentioned by him may have during this study. Jeff htz, Robin Overstreet, Jerry been Microphallus similis (Jtigerskiiild, 1900), reported McLelland,and JanBoydkindlyreadandmadeconsauctive from the same crab host by Stunkard (1957). Cable (1956) comments on the manuscript. The illustrationswere inked mentioned the presence of Levinseniellametacercariae in by Berylstory. Wealsowishto thankthe tworeviewersfor fiddler crabs from Puerto Rico, but this record has not been their constructive comments and sugestions. This work confiied. Pearse (1945), working at Beaufort, North was supported in part by NOM Office of Sea Grant, Carolina, reported a trematode metacercaria from the Department of Commerce under Grant No. 04-6-158- anomuran mud shrimp Upogebia afjriinis (Say) which he 44060 (RWH) and MH Training Grant T01-A1-0038-02 tentatively identified a species of Levinseniella. One of from the NIAID as (JMK).

LITERATURECITED

Balozet, L. and J. Callot. 1939. Trematodes de Tunisie. 3. Deblock, S. and J.C. Pearson. 1970. Contribution B l’d’ktude Superfamily Heterophyoidea. Arch Inst Pasteur Tunis des microphallidae Travassos, 1920 (Trematoda). XXII. 28: 34-63. De deux Levinseniella d’Australie dont un nouveau: Lev. (Monarrhenos)monodactyla Esai de clk diagnostique des Bousfield,E.L. andR.W.Heard. 1986. Systematics,distributional . ecology, and some host-parasite relationships of espkes du genre. Ann Parasitol Hum Comp 45:773-791. Uhlorchestia unleri (Shoemaker) and U .spartinophila n. Deblock, S. and F. Ros6.1962. Contribution a la connaissance sp. (Crustacea: Amphipoda) endemic to salt marshes of the des Microphallidae Travassos, 1920 (Trematoda) des Atlantic coast ofNorth America. JCrustaceanBiol6(2):284- Oiseaux de France. VIT. Description de Levinseniella 274. Polydactyla nov. sp. Vie Milieu 13:773-783. Bridgman. J.F., Otagaki, I. Shitanda, and Tada. 1972. Etges, F. J. 1953. Studies on the life histories of K. K. obstipum (Vancleave andMueller, 1932)andLevinseniella Nine metacercariae (Microphallidae: Trematoda) from of the Japan Inland Sea, Kagawa Prefecture. amnicolae n. sp. (Trematoda: Microphflidae). J Parasitol including the description of Levinseniella conicostoma n. 39643-662. sp. Shikoku Christian Coll Treatises 23:35-61. Forrester, D.J. 1992. Parasites and diseases of wild mammals in Bush, A.O.. R.W. Heard, Jr., and R.M. Overstreet. 1993. Florida. Univ Press Fla, Gainesville. 459 p. Intermediate hosts source communities. J Zoo1 as Can Galaktionov, K.V. 1988. [Cercariae and metacercariae of 71: 1358-1363 Levinseniella brachysoma (Trematoda, Microphallidae) Cable, R.M.. R.S. Connor, and J.W. Balling. 1960. Digenetic from invertebrates in the White Sea. Parazitologikya trematodes of Puerto Rican shore buds. Scientific Survey 22:304-311. of Puerto Rico and Virgin Islands 17(Part 2):187-254. Galaktionov. K.V. and 1.1. Malkova. 1993. Development of the Deblock, S. 1971. Contribution B 1’6tude des Microphallidae alimentary track during morphogenesis of the metacercaria Travassos, 1920 XXIV. Tentative de phylogknie et de of Levinseniella brachysoma. J Helminthol 67(2):87-93. taxonomie. Bull Mus Natl Hist Nat 3‘ serie, nV, Zoo1 Heard, R.W. 1968a. Parasites of the clapper rail, Rallus 7: 353-468. Zongirostris Boddaert. I. The current status of the genus -. 1978. Invalidation du genre Austromicrophallus Szidat, Levinseniellawith the description of Levinseniellabyrdi n. 1964 (Trematoda: Micropahallidae). Ann Parasitol Hum sp. (Trematoda: Microphallidae). Proc Helminthol Soc Comp 53(1):47-52. Wash 35(1):62-67.

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Heard, R.W. 1968b. Levinseniella hunteri sp. nov.. a new Ouspenakaia, A.V. 1963. Parasite fauna of marine benthic species of microphallid trematode from the Wilson plover, crustacea of the Barents Sea (in Russian). Publications of Charadrius wilsonia Ord. Proc Helminthol SOCWash Academy Sciences of the USSR, Moscow, Leningrad. 128 p. 35~140-143. Overstreet, R.M. and H.M. Perry. 1972. A new microphallid . 1970. Parasites of the clapper rail, Rallus longirostris trematode from the blue crab in the northern Gulf of Boddaert. II. Some trematodes and cestodes from spartina Mexico. Trans Am Microsc 91:436-440. marshes of the eastern United States. Proc Helminthol Soc Soc Pearse, AS. 1945. Ecology of Upogebia afSinis (Say). Ecology Wash 37~147-153. 26303-305. . 1976. Microphallid trematode metacercariae in fiddler Rankin, J.S. 1939. Studieson the trematodefamilyMicrophallidae crabs of the genus Uca Leach, 1814 from the northern Gulf Travassos, 1920. I. The genus Levinseniella Stiles and Mexico [dissertation]. Hattiesburg (MS): University of Hassall, 1901,anddescriptionof anew genus, Cornucopula. Southern Mississippi. 178 p. Trans Am Microsc Soc 58:431-447. Kinsella, J.M. 1988. Comparison of helminths of rice rats, Rebecq, J. 1964. Recherches systimatiques, biologiques et Oryzomyspalustris, from freshwater and saltwater marshes tkologiquessur lesformea 1arvairesdequelquesTri~odes in Florida. Proc Helminthol Soc Wash 55(2):275-280. de Camargue. Thhse Sciences, Aix-Marseille. 223 p. Kifune, T. and Y. Takao. 1972. On three species of the Reimer, L. 1963. Zue verhreitung der adulti und larvenstadien microphallid metacercariae found from a crab, der familie Microphallidae Viana, 1924, (Trematoda, Hemigrapsus penicillatus with descriptions of two Digenea) in der mittleren Ostsee. Z Parasitenk 23:253-273. new species (Trematoda: Microphallidae). Jpn J Schuldt,M. andL.1. Lunaschi. 1985(1987).Apreciacionesacerca Parasitol 21 3 18-327. : del la “castraci6n parasitaria”. An Soc Cientifica Argent Martorelli, S.R. and M. Schuldt. 1990. Encapsulaci6n de dos 215(48):29-37. metacercarias (Digenea:Microphallidae) en Cyrtograpsus Shields, J.D. 1992. Parasites andsymbionts of thecrab Portunus angulatus y Palaemonetes argentinus (Crustacea: pelagicus fromMoretonBay, eastern Australia. JCrustacean ). Rev Biol Trop 38(2A):295-304. Biol12(1):94-100. Nicol, J.T., R. Demaree, Jr., and D.M. Wootton. 1985. Stunkard, H.W. 1957. The morphology and life-history of the Levinseniella (Monarrhenos) ophidea sp.n (Trematoda: digenetic trematode, Microphallus similis (Jagerskiold, Microphallidae) from the westem garter snake, Thamnophis 1900)Baer, 1943. BiolBuU(WoodsHole,MA)112254-266. elegans and the bullfrog, Rana catebeiana. Proc Helminthol Szidat, L. 1964. Helminthologische Untersuchengen an dem SOC Wash 52(2):180-183. Argeniinischen Grossmoven Larus marinus dominicanus Nikitina, EN. [Helminths of Decapoda in the Krasnovodsk Lichtenstein und Lauras ridibkundus maculipennis Bay]. In: Biologisheskie resursy Kaspiiskogo Morya. M.S. Lichtenstein nebst nenen beobachtungen ueber die Art- Gilyarova and G.B. Zevina, Editors. Moscow, USSR Bildung bei Parasiten. Z Parasitenk 24:351-414. Izdatel’stvo Moskovskogo Universiteta 173-185 [in Vil1ot.M.A. 1875. Sur les migrations et les metamorphoses des Russian]. Trematodes parasites marins. CR Acad Sci (Paris) 81:475- Ouspenakaia, A.V. 1960. Parasitofaune des crustaces 477. benthiguesdelamerdeBarentz (Expos6 Preliminare). Ann Yamaguti, S. 1971. Synopsis of degenetic trematodes of Parasitol Hum Comp 35:221-242. vertebrates. Keigaku, Tokyo, Japan. 1800 p.

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