Zootaxa,Revision of the family Cyclocoelidae ...

Zootaxa 1563: 55–68 (2007) www.mapress.com / zootaxa/

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Copyright © 2007 · Magnolia Press

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ZOOTAXA

Revision of the family Cyclocoelidae Stossich, 1902 with the proposal of two new subfamilies and the description of a new species of Morishitium Witenberg, 1928 from the common snipe, Gallinago gallinago, from Texas, U.S.A. NORMAN O. DRONEN Laboratory of Parasitology, Department of Wildlife and Fisheries Sciences, Texas A&M University, 2258 TAMU, College Station, Texas 77843-2258. E-mail: [email protected]

Abstract Based on the definition of 6 basic body types in the group, the family Cyclocoelidae is revised with the erection of Skrjabinocoelinae n. subf. and Szidatitreminae n. subf., and the resurrection of the subfamily Hyptiasminae. Subfamily keys and keys to genera that accommodate the original 3 subfamilies (Cyclocoelinae, Ophthalmophaginae, and Haematotrephinae), the 3 additional subfamilies proposed, the 6 body types used in the revision, and the recently described genus Selfcoelum are provided. Morishitium texanense n. sp. is described from the common snipe, Gallinago gallinago, in Texas, U.S.A., the genus Neoallopyge is synonymized with Allopyge, and the genus Neohyptiasmus is synonymized with Morishitium. Key words: Curlew, Cyclocoelidae, Cyclocoelinae, Gallinago gallinago, Haematotrephinae, Hyptiasminae, key, Morishitium texanense n. sp., Neoallopyge, Neohyptiasmus, Ophthalmophaginae, revision, Scolopacidae, Skrjabinocoelinae n. subf., snipe, Szidatitreminae n. subf., Texas, U.S.A.

Introduction The common snipe, Gallinago gallinago (Linnaeus) (syns. the Old World snipe, Capella gallinago [Linnaeus] or Scolopax gallinago [Linnaeus], Wilson’s snipe, Gallinago delicate [Ord]) (Scolopacidae), is a common wading bird that is generally found in wet meadows and grassy areas, flooded fields, marshes, and along the shores of lakes and streams from tundra to temperate lowlands. In the New World, it ranges from northern Alaska and Canada, southward throughout North America to Columbia, Ecuador and Venezuela, South America (Walters, 1980; American Ornithologist’s Union, 1983). This species is also found in most of Eurasia, ranging from Iceland in the west, eastward through the British Isles, Scandinavia, Russia, and much of southern Europe to the west coast of the Atlantic ocean in the east (Walters, 1980; American Ornithologist’s Union, 1983; Rappole & Blacklock, 1994). This species was previously assigned to the genus Capella Frenzel, but was reassigned to the genus Gallinago Brisson by Mayr (1963). There is disagreement among ornithologists as to whether or not southern hemisphere species (the South American snipe, Gallinago paraguaiae [Veillot] and the puna snipe, Gallinago andina Taczanowski [South America], and the African snipe, Gallinago nigripennis Bonaparte [Africa]) are conspecific with G. gallinago (American Ornithologist’s Union, 1983). There have been a number of cyclocoelids reported from this species of scolopacid bird (Table 1).

Accepted by W. Sterrer: 15 Jul. 2007; published: 29 Aug. 2007

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TABLE 1. Cyclocoelids previously reported from the common snipe, Gallinago gallinago. Host

Parasite

Locality

Citation

Gallinago gallinago

Cyclocoelum capellum Khan, 1935

India

Bashkirova, 1950; Dubois, 1959; Khan, 1935; Macko and Feige,1960

C. cuneatum Harrah, 1922

U.S.A.

Harrah, 1922; Dubois, 1959; Witenberg, 1926

C. leidyi Harrah, 1922

U.S.A.

Harrah, 1922; Dubois, 1959; Witenberg, 1926

C. makii Yamaguti, 1933

Taiwan

Bashkirova, 1950; Dubois, 1959; Yamaguti, 1933*

C. mehrii Khan, 1935

India

Dubois, 1959; Khan, 1935

C. mutabile (Zeder, 1800)

Asia;Europe;U.S.A

Dubois, 1959

C. nochi (Wesley, 1943)

India

Wesley, 1943

C. obliquum Harrah, 1921

Siam

Bashkirova, 1950; Dubois, 1959; Harrah, 1921; Witenberg, 1926

C. obscurum (Leidy, 1887)

Vietnam;Indochina

Joyeux and Baer, 1927

C. vicarium (Arnsdorff, 1908)

Europe

Bashkirova, 1950

Haemototrephus capellae Yamaguti, 1933 Taiwan

*

Dubois, 1959; Macko and Feige, 1960; Yamaguti, 1933

H. cymbius (Diesing, 1850)

Africa;Brazil; U.S.A. Joyeux and Baer, 1927; Stossich, 1903; Witenberg, 1923; 1926

H. halli (Harrah, 1922)

U.S.A.

Selfcoelum brasilianum (Stossich, 1902)

Asia; Brazil; Europe; Joyeux and Baer, 1927 U.S.A.

Wardianum taxorchis (Johnston, 1917

Australia

Yamaguti, 1971

Wardianum triangulare (Harrah, 1922)

U.S.A.

Macko and Feige,1960

Wardianum wilsoni (Harrah, 1922)

U.S.A.

Dubois, 1959; Witenberg, 1926

Witenberg, 1926

Cited as 1935 in Yamaguti (1971).

Yamaguti (1971) recognized 3 subfamilies in Cyclocoelidae Stossich, 1902: Cyclocoelinae Stossich, 1902 where an external seminal vesicle was absent, the buccal cavity was funnelshaped, the ceca were simple (not diverticulate), and where cercariae encysted within the rediae in which they developed; Promptenovinae Yamaguti, 1971 where an external seminal vesicle was present and the buccal cavity was tubular; and Typhlocoelinae Harrah, 1922 where the external seminal vesicle was absent, the buccal cavity was funnel-shaped, the ceca were diverticulate, and where cercariae encysted in the tissue of the snail outside the rediae in which they developed. Yamaguti (1971) recognized 22 genera in the family. In Cyclocoelinae, he recognized 19 genera: Allopyge Johnston, 1913; Bothrigaster Dollfus, 1948; Contracoelum Witenberg, 1926; Corpopyrum Witenberg, 1923; Cyclocoelum Brandes, 1892; Cycloprimum Witenberg, 1923; Haematoprimum Witenberg, 1923; Haematotrephus Stossich, 1902; Harrahium Witenberg, 1926; Hyptiasmus Kossack, 1911; Morishitium Witenberg, 1928; Ophthalmophagus Stossich, 1902; Prohyptiasmus Witenberg, 1923; Skrjabinocoelum Kurashvili, 1953; Spaniometra Kossack, 1911; Szidatitrema Yamaguti, 1971; Transcoelum Witenberg, 1923; Uvitellina Witenberg, 1923; and Wardianum Witenberg, 1923. In Promptenovinae, he recognized only Promptenovum Witenberg, 1923, and in Typhlocoelinae, he recognized Tracheophilus Skrjabin,1913 and Typhlocoelum Stossich, 1902. In their recent key, Kanev et al. (2002a) revised the Cyclocoelidae recognizing 3 subfamilies: Cyclocoelinae where the ovary was located between the testes; Ophthalmophaginae Harrah, 1922 where the ovary was posttesticular; and Haematotrephinae Doll-

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DRONEN

fus,1948 where the ovary was pretesticular. These authors did not recognize Promptenovinae, assigning Promptenovum to Ophthalmophaginae (Kanev et al., 2002a). They also followed Bittner & Sprehn (1928) in recognizing Typhlocoelidae Harrah, 1922 as a family separate from Cyclocoelidae (Kanev et al., 2002b). These authors simplified these 3 subfamilies in Cyclocoelidae by synonymizing many of the genera previously accepted by Yamaguti (1971). They considered Cycloprimum to be synonymous with Cyclocoelum and Transcoelum to be synonymous with Hyptiasmus recognizing only Allopyge, Cyclocoelum, Hyptiasmus, Morishitium, Neohyptiasmus Kanev, Radev, & Fried, 2002, Prohyptiasmus, and Skrjabinocoelum as valid genera within the Cyclocoelinae. They considered Bothrigaster and Contracoelum to be synonymous with Spaniometra recognizing Ophthalmophagus, Promptenovum, Spaniometra, and Szidatitrema as valid genera in Ophthalmophaginae. They also considered Corpopyrum, Haematoprimum, Harrahium, and Wardianum to be synonymous with Haematotrephus recognizing Haematotrephus, Neohaematotrephus Kanev, Radev, & Fried, 2002, and Uvitellina as valid genera in Haematotrephinae. Yamaguti (1971) did not recognize Geowitenbergia Dollfus, 1948, Philoculum Savinov, 1958, Receptocoelum Lal, 1939, or Stossichium Witenberg, 1928 as valid genera, but Kanev et al. (2002a) considered Geowitenbergia to be synonymous with Ophthalmophagus, Philoculum to be synonymous with Allopyge, Receptocoelum to be synonymous with Cyclocoelum, and Stossichium (as originally proposed by Yamaguti, 1971) to be synonymous with Prohyptiasmus. Neocyclocoelum Feizullaev, 1980 and Porphyriotrema Duggal & Toor, 1986 were described after Yamaguti (1971), but Kanev et al. (2002a) considered Neocyclocoelum to be synonymous with Morishitium and Porphyriotrema to be synonymous with Cyclocoelum. More recently, Neoallopyge Dronen & Blend, 2005 was erected by Dronen & Blend (2005) with the description of Neoallopyge americanensis Dronen & Blend, 2005 and Selfcoelum Dronen, Gardner, & Jiménez, 2006 was established by Dronen et al. (2006a) with the description of Selfcoelum limnodromi Dronen, Gardner, & Jiménez, 2006. Dronen (2007) reestablished the genus Wardianum with the description of Wardianum catoptrophori Dronen, 2007. The genus Morishitium was established by Witenberg (1928) with the reassignment of 2 species of cyclocoelids: Cyclocoelum vagum Morishita, 1924 (type species) from the golden pheasant, Chrysolophus picta (Linnaeus), and Cyclocoelum distomatum Morishita, 1924 from the sparkling pheasant, Phasianus scintillans Gould, that had been described by Morishita (1924) from Japan. In addition to these 2 species, Yamaguti (1971) listed 8 species in the genus: Morishitium bivesiculatum (Prudhoe, 1944) from the Ceylon or great Indian green barbet, Megalaima zeylanicus (Gmelin) (reported as Thereiceryx zeylanicus Gmelin), from Ceylon (Prudhoe, 1944); Morishitium dollfusi (Timon-David, 1950) from the European or black-bellied magpie, Pica pica (Linnaeus), from France (Timon-David, 1950); Morishitium dumetellae (Zeliff, 1943) from the grey catbird, Dumetella carolinensis (Linnaeus), from Pennsylvania, U.S.A. (Zeliff, 1943); Morishitium ominosum (Kossack,1911), originally described as Hyptiasmus ominosus Kossack, 1911 from the grey crane or trane, Grus cinerea Bechst, from Germany (Kossack, 1911); Morishitium petrowi (Oganesov, 1959) from the common blackbird, Turdus merula Linnaeus from Azerbaidzhan (Oganesov, 1959); Morishitium sinhaldripa (Fernando, 1950) from the Ceylon jungle fowl, Gallus lafayetti Lesson, from Ceylon (Fernando, 1950); Morishitium straightum (Khan, 1935) from the greenshank, Tringa nebularia (Gunnerus) (reported as Glottis nebularia Gunnerus), from India (Khan, 1935); and Morishitium undulatum (Canavan, 1943) from the Manchurian crane, Grus japonensis (Müller) (reported as Megalornis grus lilfordi Müller), from Siberia (Canavan, 1934). Of these 10 species, both M. ominosum and M. undulatum (originally described as Allopyge undulates Canavan, 1934) have been placed in Allopyge (Dronen & Blend, 2005). Gupta & Gupta (1979) described Morishitium raushi Gupta & Gupta, 1979 from G. gallinago (reported as Capella gallingo) from Kanpur, India. Fischthal & Kuntz (1981) described Morishitium taiwanense Fischthal & Kuntz, 1981 from the Formosan hill partridge, Arborophila crudigularis (Swinhoe), from Taiwan. The purpose of the present study is to revise the family Cyclocoelidae and provide additional information concerning members of Morishitium and the cyclocoelids of scolopacid birds.

CYCLOCOELIDAE REVISION

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Material and methods Four common snipe, G. gallinago, collected from Lake Bryan, Brazos County, Texas in September, 2001, were examined for helminths (U.S. Fish and Wildlife Service permits nos. PRT 760668 and SPR 1191436; Texas Parks and Wildlife Department permit no. TX SPH 0491253). Cyclocoelids were studied alive, relaxed in saline, heat-fixed under slight cover slip pressure in alcohol-formalin-acetic acid (AFA), stained in Semichon’s carmine or Harris’ hematoxylin and counter stained with eosin, and mounted in Canada balsam or Kleermount. Drawings were done with the aid of a drawing tube. Measurements are in micrometers (μm), and are given with the mean followed by the range in parentheses unless otherwise stated. Comparative measurements were taken from the original species descriptions unless otherwise stated. Representative specimens were deposited in the Harold W. Manter Laboratory of Parasitology (HWML), University of Nebraska, Lincoln, Nebraska, U.S.A. The following specimens from HWML, the United States National Parasite Collection (USNPC), Beltsville, Maryland, U.S.A., the Natural History Museum (NHM), London, England, and the Laboratory of Parasitology Collection (ND) at the Texas Cooperative Wildlife Collection, Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, Texas, U.S.A. were examined: Allopyge undulatus (USNPC 037166.00), Allopyge sp. (NHM 1979.3.1.9–10), Cyclocoelum bivesiculatum (NHM 1952.12.17.58–67, 1980.6.3.96–98, 1981.2.11.97, 1983.10.10.2), C. microstomum (NHM 1952.12.5.161), C. mutabile (USNPC 024905.00; NHM 1964.8.25.14–15, 1984.7.7.3, 1984.10.9.18–19, 1988.2.29.4, 1991.7.11.41), C. obscurum (USNPC 075304.00, 084775.00; NHM 1965.7.27.9–11, 1979.4.10.132–133, 1980.6.3.136–138, 1982.5.21.146, 1992.6.25.9–11; ND 77a-117a), C. (=Hyptiasmus) oculeus (NHM 1952.12.5.162–163), Cyclocoelum phasidi (NHM 1946.12.20.20–23), Cyclocoelum (=Morishitium) polonicum (NHM 1983.9.30.3–37), C. problematicum (NHM 1922.10.25.98–99), C. pseudocotylerus (NHM 1973.12.11.61–65), C. vanelli (NHM 1920.8.26.1–2), Cyclocoelum sp. (NHM 1956.9.16.400–401, 1956.11.16.125, 1977.3.28.118–124; HWML 11775, 41216, 42309; ND 71-226-1–6), Haematotrephus (=Cyclocoelum) kossacki (NHM 1975.2.24.117–119), H. (= Cyclocoelum) lanceolatum (USNPC 078879.00; NHM 1991.7.11.50), H. limnodromi (HWML 48259–61), H. selfi (HWML 48493, 48494, 48495, 48496), H. (= Cyclocoelum) tringae (NHM 1990.1.10.1–7), H. (=Cyclocoelum) vanelli (NHM 1970.8.26.1–2), Haematotrephus sp. (NHM 1953.10.8.3–5, 1975.2.24.117–119, 1982.5.20.42–56, 1982.5.21.109–111, 1982.5.21.117, 1986.7.14.11; HWML 43005b, 41280, 48497; ND 77-426-7), Ophthalmophagus bucephali (HWML 21790, 48164), Ophthalmophagus sp. (HWML 1501), Morishitium sp. (HWML 43005a, 43009, 42237; ND 77a-117–118), Neoallopyge americanensis (USNPC 094819.00, 094820.00), Neohaematotrophus sp. (HWML 11775, 30407, 43007), Selfcoelum limnodromi (HWML 41212, 48162, 48163), Szidatitrema yamaguti (HWML 48329–48331; USNPC 96975), Wardianum catoptrophori (HWML 48370), and unidentified cyclocoelids (NHM 1946.12.20.24–25).

Results Family Cyclocoelidae Stossich, 1902 Diagnosis: Medium-sized to large flatworms, lanceolate, body often tapered anteriorly and rounded posteriorly. Oral sucker, if present, usually poorly developed. Acetabulum generally absent, but reported in some species. Mouth subterminal, prepharynx generally shorter than esophagus, ceca frequently simple, inner wall sometimes irregular, undulating in overall appearance in some species, united near posterior extremity to form characteristic cyclocoel. Testes oval to elongate, borders smooth or irregular, tandem to diagonal, rarely side by side, usually located near posterior end, but may be equatorial to preequatorial in some species. Genital pore near midline of body, prepharyngeal, pharyngeal or postpharyngeal. Cirrus sac present, inclosing seminal


DRONEN

vesicle, extending posteriorly to level of posterior aspect of esophagus to immediately postbifurcal. Ovary oval to elongate, intertesticular, pretesticular or posttesticular, forming a triangle or in a straight line with testes. Uterus intercecal to extracecal, uterine seminal receptacle (“receptaculum seminis uterinum” of Yamaguti [1933]; “receptacle seminalis uterinum”of Harrah [1922]) present in some species. Vitellaria follicular, ventral and somewhat lateral to ceca, vitelline fields reaching to, or beyond, cecal bifurcation anteriorly, confluent posteriorly or not. Excretory vesicle generally Y-shaped, branches extending anterior to level of pharynx or beyond, reticulate where known. Excretory pore usually somewhat subterminal opening on dorsal surface, may approach being terminal in some species. Life cycles, where known, utilize either freshwater or terrestrial snails, polyembryony produces tailless cercariae that encyst in either the rediae where they were produced or in the tissue of snails. Adults in body cavity, lungs, air sacs, nasal and infraorbital sinuses, or hypothalamus of birds, occasionally in mammals. Type genus: Cyclocoelum Brandes, 1892.

Key to subfamilies of Cyclocoelidae Stossich, 1902 1a. 1b. 2a. 2b. 3a. 3b. 4a. 4b. 5a. 5b.

Ovary forming a triangle with the testes..................................................................................................... 2. Ovary nearly in a straight line with testes................................................................................................... 4. Ovary intertesticular ......................................................................... Cyclocoelinae Stossich, 1902 (Fig. 1). Ovary pretesticular or posttesticular ........................................................................................................... 3. Ovary pretesticular to opposite anterior testis ............................. Haematotrephinae Dollfus, 1948 (Fig. 2). Ovary posttesticular or opposite posterior testis........................................ Szidatitreminae n. subf. (Fig. 3). Ovary posttesticular ....................................................................Ophthalmophaginae Harrah, 1922 (Fig.4). Ovary intertesticular ................................................................................................................................... 5. Testes tandem to nearly tandem.......................................................... Hyptiasminae Dollfus, 1948 (Fig. 5). Testes nearly side by side........................................................................Skrjabinocoelinae n. subf. (Fig. 6).

Subfamily Cyclocoelinae Stossich, 1902 (Syns. Cyclocoeliinae Witenberg, 1923) Diagnosis: With the characteristics of the family. Ovary oval, intertesticular (ranging from level of posterior end of anterior testis to anterior end of posterior testis), forming triangle with testes. Testes spherical to subspherical, tandem to diagonal, usually smooth, occasionally irregular. Genital pore prepharyngeal (ranging from anterior end of pharynx to midlevel of prepharynx) or postpharyngeal (ranging from midlevel of pharynx to near level of cecal bifurcation). Vitelline fields not confluent posteriorly. Uterus intercecal or with uterine loops overreaching ceca laterally. Type genus: Cyclocoelum Brandes, 1892.

Key to the genera of Cyclocoelinae Stossich, 1902 1a. Genital pore prepharyngeal.............................................................................. .Cyclocoelum Brandes, 1892 (Syns. Cycloprimum Witenberg, 1923; Mediopharyngeum Witenberg, 1923; Antepharyngeum Witenberg, 1923; Receptocoelum Lal, 1939; Porphyriotrema Duggal & Toor, 1986). 1b. Genital pore postpharyngeal ...............................................Selfcoelum Dronen, Gardner, & Jiménez, 2006.



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FIGURES 1–6. Six basic body types found in cyclocoelids. 1. Body type 1 for Cyclocoelinae; ovary intertesticular forming a triangle with the testes; represented by Selfcoelum limnodromi adapted from Dronen et al. (2006a). 2. Body type 2 for Haematotrephinae; ovary pretesticular to opposite the anterior testis forming a triangle with the testes; represented by Heamatotrephus limnodromi adapted from Dronen et al. (2006b). 3. Body type 3 for Szidatitreminae n. sub.; ovary postesticular to opposite posterior testis forming a triangle with the testes; represented by Szidatitrema yamagutii adapted from Dronen et al. (2006c). 4. Body type 4 for Ophthalmophaginae; ovary postesticular in a longitudinal straight line with the testes; represented by Ophthalmophagus bucephali adapted from Dronen & Blend (2007). 5. Body type 5 for Hyptisaminae; ovary intertesticular in a longitudinal straight line with the testes; represented by Allopyge americanensis n. comb. adapted from Dronen & Blend (2005). 6. Body type 6 for Skrjabinocoelinae n. subf.; ovary intertesticular in a transverse row with the testes; represented by Skrjabinocoelum petrowi Kurashvili, 1953 adapted from Kurashvili (1953). Abbreviation: T, testis.


DRONEN

Subfamily Haematotrephinae Dollfus, 1948 Diagnosis: With the characteristics of the family. Ovary oval, pretesticular to opposite anterior testis, forming triangle with testes. Testes spherical to subspherical, tandem to diagonal, usually smooth. Genital pore prepharyngeal (ranging from anterior end of pharynx to midlevel of prepharynx) or postpharyngeal (ranging from midlevel of pharynx to near level of cecal bifurcation). Vitelline fields confluent posteriorly or not. Uterus generally with uterine loops overreaching ceca laterally. Type genus: Haematotrephus Stossich, 1902.

Key to the genera of Haematotrephinae Dollfus, 1948 1a. 1b. 2a. 2b. 3a. 3b.

Genital pore prepharyngeal............................................Neohaematotrephus Kanev, Radev, & Fried, 2002. Genital pore postpharyngeal ....................................................................................................................... 2. Vitelline fields confluent posteriorly .................................................................Uvitellina Witenberg, 1923. Vitelline fields not confluent posteriorly .................................................................................................... 3. Testes nearly side by side................................................................................ Wardianum Witenberg, 1923. Testes diagonal to tandem...........................................................................Haematotrephus Stossich, 1902. (Syns. Corpopyrum Witenberg, 1923; Haematoprimum Witenberg, 1923; Harrahium Witenberg, 1923).

Subfamily Szidatitreminae n. subf. Diagnosis: With the characteristics of the family. Ovary oval, posttesticular to opposite posterior testis, forming triangle with testes. Testes spherical to subspherical, tandem to oblique, usually smooth. Genital pore postpharyngeal (ranging from midlevel of pharynx to near level of cecal bifurcation). Vitelline fields not confluent posteriorly. Uterus generally with uterine loops overreaching ceca laterally. Type genus: Szidatitrema Yamaguti, 1971. Szidatitrema Yamaguti, 1971 – only genus currently in subfamily. (Syn. Szidatiella Yamaguti, 1958).

Subfamily Ophthalmophaginae Harrah, 1922 (Syn. Bothrigasterinae Dollfus, 1948) Diagnosis: With the characteristics of the family. Ovary oval, posttesticular in line, or nearly in line with testes. Testes spherical to subspherical, tandem smooth. Genital pore prepharyngeal (ranging from anterior end of pharynx to midlevel of prepharynx) or postpharyngeal (ranging from midlevel of pharynx to near level of cecal bifurcation). Vitelline fields confluent posteriorly or not. Uterus generally with uterine loops overreaching ceca laterally. Type genus: Ophthalmophagus Stossich, 1902. Key to the genera of Ophthalmophaginae Harrah, 1922. 1a. Genital pore prepharyngeal...................................................................... Ophthalmophagus Stossich, 1902 (Syn. Geowitenbergia Dollfus, 1948). 1b. Genital pore postpharyngeal ....................................................................................................................... 2. 2a. Vitelline fields confluent posteriorly ........................................................ Promptenovum Witenberg, 1923. CYCLOCOELIDAE REVISION


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2b. Vitelline fields not confluent posteriorly .......................................................... Spaniometra Kossack, 1911 (Syns. Bothriogaster Fuhrmann, 1904; Contracoelum Witenberg, 1926; Bothrigaster Dollfus, 1948).

Subfamily Hyptiasminae Dollfus, 1948 Diagnosis: With the characteristics of the family. Ovary oval, intertesticular (ranging from level of posterior end of anterior testis to anterior end of posterior testis), in line or nearly in line with testes. Testes spherical to subspherical, tandem to oblique, smooth to irregular. Genital pore prepharyngeal (ranging from anterior end of pharynx to midlevel of prepharynx) or postpharyngeal (ranging from midlevel of pharynx to near level of cecal bifurcation). Vitelline fields confluent posteriorly or not. Uterus intercecal or with uterine loops overreaching ceca laterally. Type genus: Hyptiasmus Kossack, 1911.

Key to the genera of subfamily Hyptiasminae Dollfus, 1948 1a. Genital pore prepharyngeal......................................................................................................................... 2. 1b. Genital pore postpharyngeal ....................................................................................................................... 3. 2a. Vitelline fields confluent posteriorly ................................................................. .Hyptiasmus Kossack, 1911 (Syn. Transcoelum Witenberg, 1923). 2b. Vitelline fields not confluent posteriorly ....................................................Prohyptiasmus Witenberg, 1923 (Syn. Stossichium Witenberg, 1928). 3a. Vitelline fields confluent posteriorly .....................................................................Allopyge Johnston, 1913 (Syns. Philoculum Savinov,1958; Neoallopyge, Dronen & Blend, 2005). 3b. Vitelline fields not confluent posteriorly ........................................................ Morishitium Witenberg, 1928 (Syns. Pseudhyptiasmus Dollfus, 1948; Neocyclocoelum Feizullaev, 1980; Neohyptiasmus Kanev, Radev, & Fried, 2005).

Subfamily Skrjabinocoelinae n. subf. Diagnosis: With the characteristics of the family. Ovary oval, intertesticular in line, or nearly in line, with testes. Testes spherical to subspherical, side by side or nearly side by side, in a transverse row, smooth. Genital pore postpharyngeal (ranging from midlevel of pharynx to near level of cecal bifurcation). Vitelline fields confluent posteriorly and at level of cecal bifurcation. Uterus generally with uterine loops overreaching ceca laterally. Type genus: Skrjabinocoelum Kurashvili, 1953. Skrjabinocoelum Kurashvili, 1953 – only genus currently in subfamily.

Subfamily Hyptiasminae Dollfus, 1948 Genus Morishitium Witenberg, 1928 Morishitium texanense n. sp. (Figs. 7–9) Type host: Scolopacidae: Gallinago gallinago (Linnaeus. 1758); common snipe.


DRONEN

Type locality: Lake Bryan, Brazos County, Texas, U.S.A., 30° 24’ N latitude, 96° 13’ W longitude. Site of infection: Air sacs of lungs. Prevalence: 50% (2 of 4 birds). Mean intensity: 3 (2 in one bird and 4 in a second). Specimens deposited: Holotype HWML 48564; paratypes (2 specimens) 48565; vouchers (3 specimens) HWML 48566. Etymology: The species designation reflects the general geographical region from which the host bird was collected, Texas, U.S.A.

FIGURES 7–9. Morishitium texanense n. sp. from the common snipe, Gallinago gallinago. 7. Morishitium texanense n. sp., ventral view of adult. 8. Morishitium texanense n. sp., composite drawing of the anterior end, ventral view. 9. Morishitium texanense n. sp., composite drawing of female reproductive system, ventral view. Abbreviations: AT, anterior testis; C, Cecum; M, Mehlis’ glands of ootype; OV, ovary; P, Pharynx; SV, seminal vesicle; T, testes; U, uterus; V, vitelline duct; VF, vitelline field.



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Description: Based on 6 specimens. With characteristics of the genus. Body large, relatively narrow, tapered anteriorly, 10.6 (9.3–11.0) mm long by 2.0 (1.9–2.3) mm wide at widest point. Oral sucker and acetabulum absent. Mouth slightly subterminal; prepharynx 175 (150–220) long; pharynx well developed, 278 (250–270) long by 220 (210–230) wide; esophagus longer than prepharynx, 460 (350–600) long. Ratio of length of prepharynx to length of esophagus 1:2.6. Ceca with irregular inner margins forming numerous, small, blister-like pouches in most specimens (not figured), uniting near posterior extremity to form cyclocoel. Testes smooth, spherical to subspherical, occasionally lobed, tandem to somewhat diagonal, in intercecal region of posterior 1/3 of body. Anterior testis 528 (460–630) long by 452 (370–550) wide. Posterior testis 578 (410–690) long by 454 (350–550) wide. Intertesticular space 1,090 (650–1,370, or approximately 10% of body length). Posttesticular space relatively small, 550 (450–670, or approximately 5% of body length). Cirrus sac 510 (400–750 [approximately 5% of body length]) long by 158 (150–180) wide, enclosing bipartite seminal vesicle. Genital pore postpharyngeal, at level of posterior 1/3 of pharynx, near midline of body. Ovary smooth, oval, situated intertesticularly, in line with, or nearly in line, with testes, 255 (220–280) long by 248 (210–300) wide. Ratio of width of ovary to mean width of testes 1:1.8. Uterine seminal receptacle absent. Laurer’s canal absent. Vitelline follicles distributed along ceca from level of pharynx to posterior extremity, not confluent posteriorly. In some specimens, one side may be less extensive, reaching anteriorly only to level of cecal bifurcation, longer extent not consistently on left or right. Uterus extensive, intercecal, proximal end filled with sperm. Eggs 140 (130–155) long (n=40) by 72 (60–80) wide in anterior aspect of uterus; miracidia oculate. Excretory vesicle Y-shaped. Excretory pore nearly terminal on dorsal surface of body. Remarks. This species has an intertesticular ovary that forms a straight line with the tandem testes and is assigned to Hyptiasminae. The new species is assigned to Morishitium because it has a genital pore that is postpharyngeal and the vitelline fields are not confluent posterior. Of the 10 species that can currently be assigned to Morishitium, M. distomatum (Morishita, 1924), M. sinhaldripa, M. taiwanense, and M. vagum have both an oral sucker and an acetabulum, while M. bivesiculatum, M. dollfusi, M. dumetellae, M. petrowi, and M. straightum have only an oral sucker. Morishitium raushi is the only previously described species that is like Morishitium texanense n. sp. in that it lacks both an oral sucker and an acetabulum. The new species also differs from M. raushi by having a smaller body size (10.6 mm long by 2.0 mm wide compared to 21.9 by 3.6), a somewhat smaller pharynx (220 wide compared to 300), a shorter esophagus (460 compared to 1,520), a smaller ovary (248 wide compared to 520), smaller testes (453 mean width compared to 1,875), a smaller cirrus sac (510 long by 158 wide compared to 1,000 by 460), a smaller posttesticular space (550 long compared to 750), larger eggs (135–155 long by 60–80 wide compared to 110–140 by 50–60), and by lacking a true uterine seminal receptacle.

Discussion Characteristics commonly used to distinguish taxa within Cyclocoelidae Cyclocoelids pose a difficult challenge for the parasite taxonomist because generally there are relatively few dependable characteristic available in the cyclocoelids that can be used to determine the placement of a species in a genus, define genera, or distinguish subfamilies. Most species lack an oral sucker, very few are known to have a ventral sucker, and there tends to be a reasonably large range of variability seen in descriptive measurements, as well as in the appearance and placement of morphological features generally used to define taxa within the family. At the species level, cyclocoelids frequently occur in low numbers and descriptions of many species have been from a limited number of specimens (often as few as 1 specimen) from a single host species, generally collected from a restricted geographical area, and most species have usually been reported from relatively few sites within their hosts. Also, most measurements that have been used to describe existing species have large ranges, and most species within a genus are often very similar in overall appearance leav-


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ing relatively few characteristics apparent that can be used to show specific differences. In terms of generic diagnoses and placement of genera into subfamilies, not only is the taxonomist faced with large ranges of variability in many characteristic, but many of the commonly used distinguishing characteristics are difficult to see and/or interpret. Currently, there are 5 general characteristic states that have commonly been used either individually or in combination to place species into genera and subfamilies: 1. The placement of the ovary relative to the testes; 2. The position of the genital pore relative to the pharynx; 3. The posterior extent of the vitelline fields (confluent posteriorly or not); 4. The lateral extent of the uterine loops (uterus entirely intercecal or with loops surpassing the ceca laterally); and 5. The appearance of the testes (smooth or irregular). The placement of the ovary relative to the testes appears to be a reasonably dependable (little variability) characteristic, and one that is most visible and easy to interpret. However, this characteristic is not without some variability. In species currently assigned to Haematotrephinae, where the ovary is pretesticular, species vary from having the ovary clearly pretesticular to having it directly opposite to the anterior testis (e.g. Haematotrephus limnodromi Dronen, Gardner, & Jiménez, 2006). In species currently assigned to Cyclocoelinae, the position of the ovary can vary from being within the level of the intertesticular space to being nearly opposite the posterior testis (e.g. Selfcoelum limnodromi). In members of Ophthalmophaginae, the position of the ovary may vary from being clearly posttesticular to being opposite the posterior testis (Ophthalmophagus bucephali Dronen & Blend, 2007). Dronen et al. (2006a) suggested that at least some of the variability seen in the position of the ovary in cyclocoelids may be related to the amount of curvature of the body at the time of fixation, but that such variability is still seen even when large numbers of specimens of a species are available for examination is worth noting. The position of the genital pore relative to the pharynx is also a somewhat variable characteristic, and often this feature is difficult at best, to determine. Dronen et al. (2006a) and Dronen & Blend (2007) pointed out that the position of the genital pore is often difficult to see in cyclocoelids. In species like Selfcoelum limnodromi (11 specimens) (Dronen et al., 2006a) and Szidatitrema yamagutii Dronen, Craig, & Hammond, 2006 (over 90 specimens; 11 specimens and sections used in the species description) (Dronen et al., 2006c), where there have been large numbers of specimens to examine, the placement of the genital pore can vary from being located near the midlevel of the pharynx to being distinctly postpharyngeal. Historically, most authors have considered species with this range in the placement of the genital pore to have a postpharyngeal genital pore, as opposed to those where the genital pore is distinctly prepharyngeal (i.e. species assigned to Cyclocoelum or Ophthalmophagus). In examination of specimens from museums, it is clear that the placement of the genital pore can be quite difficult to interpret in the cyclocoelids. The posterior extent of the vitelline fields (confluent posteriorly or not) is a fairly dependable characteristic, although some species examined for this study had the vitelline fields of some specimens confluent posteriorly in species where they would have been expected not to be confluent (e.g. Haematotrephus limnodromi). Conversely, a few specimens of species of Allopyge examined (a genus where species would be expected to have vitelline fields confluent posteriorly) had vitelline fields that were not confluent. The lateral extent of the uterine loops (uterus entirely intercecal or with loops surpassing the ceca laterally) seems to be reasonably constant in some species within some genera (e.g. Cyclocoelum-intercecal); however, among species in other genera (e.g. Morishitium) the lateral extent of the uterine loops seemed to be agerelated. In some species (e.g. Szidatitrema yamagutii), smaller (younger) specimens have an intercecal uterus, while larger (older) ones have the cecal loops overreaching the ceca laterally, and in some specimens, almost reaching the body wall. Some species of Selfcoelum have an intercecal uterus, while in others the uterine loops overreach the ceca laterally. The appearance of the testes (smooth or irregular) seemed to be the least dependable of these 5 characteristics, as I found both irregular and smooth testes to be occasionally present in specimens of species of genera (e.g. Selfcoelum spp., Morishitium spp.) from all the current subfamilies. Rarely, one testes was irregular and



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the other smooth in a single specimen (e.g. Morishitium texanense n. sp.). Hyptiasminae, as a group, appears to have an unusual number of species where the testes are occasionally irregular. Definition of subfamilies In their definition of the 3 subfamilies within Cyclocoelidae, Kanev et al. (2002a) primarily used the position of the ovary relative to the testes (pretesticular, intertesticular, posttesticular). The placement of the ovary relative to the testes appears to be the least variable characteristics of the 5 listed above, and it is likely the most useful characteristic available in the cyclocoelids for determining subfamily status. The approach by Kanev et al. (2002a) represents an improvement over previous keys; however, in both the Cyclocoelinae and the Ophthalmophaginae, the way in which this characteristic has been applied has resulted in a mixture of more than one basic body morphology (type) in these subfamilies. In Cyclocoelinae, this application of the characteristic mixes those genera where the ovary forms a triangle with the testes (Cyclocoelum), with those where the ovary forms a straight line with the testes longitudinally (testes tandem to slightly diagonal) (Allopyge, Hyptiasmus, Morishitium, Neohyptiasmus, Prohyptiasmus), and those where the ovary forms a straight transverse line with the testes (Skrjabincoelum). Similarly in Ophthalmophaginae, species where the ovary is posttesticular to directly opposite the posterior testis forming a triangle with the testes (Szidatitrema) are mixed with those where the ovary is distinctly posttesticular forming a straight line with the testes (Ophthalmophagus, Promptenovum, Spaniometra). In the revised key proposed herein, genera are initially divided into 2 main groups: those where the ovary forms a triangle with the testes, and those where it is in a straight line with the testes. The first main group (where ovary forms a triangle with the testes) is further separated into 2 secondary groups: one where the ovary is intertesticular (represented by the subfamily Cyclocoelinae; body type 1 [Fig 1]), and a second secondary group where the ovary is either pretesticular or posttesticular. The second of these groups (where the ovary is either pretesticular or posttesticular) is divided into Haematotrephinae (body type 2 [Fig. 2]) where the ovary is pretesticular or opposite of the anterior testis, and Szidatitreminae n. subf. (body type 3 [Fig. 3]) where the ovary is either posttesticular or opposite to the posterior testis. The second main group above (where the ovary is in a straight line with the testes) is also further divided into 2 secondary groups: those where the ovary is posttesticular (represented by Ophthalmophaginae; body type 4 [Fig. 4]), and those where the ovary is intertesticular. The second secondary group (where the ovary is intertesticular) is divided into Hyptiasminae (body type 5 [Fig. 5]) where the testes are tandem to nearly tandem, and Skrjabinocoelinae n. subf. (body type 6 [Fig. 6]) where the testes are nearly side by side. This results in 6 subfamilies, each of which represents a specific body type, so that all the genera within a subfamily look similar. The revised key to subfamilies also emphasizes characteristics that are easily seen, tend to be less variable, and they are applied in a way that takes into account the variability that is evident in the specimens examined and in the literature. One possible objection to this new arrangement is that both Skrjabinocoelinae n. subf. and Szidatitreminae n. subf. are each represented by only a single genus; however, it is not unusual in most groups of organisms to have some lineages that are represented by single taxa; and new genera may be added to these subfamilies in the future. Definition and placement of Genera into subfamilies In the Cyclocoelinae, as defined by Kanev et al. (2002a), the orientation of the testes is used to separate out the genus Skrjabinocoelum, where the testes are in a transverse row, from the rest of the genera in the subfamily, where the testes are either diagonal or tandem. In my opinion, the unusual configuration of the ovary and testes that is seen in Skrjabinocoelum represents a unique body morphology (body type 6) that distinguishes it from the rest of the genera in the family, and therefore, I feel that it should be placed in its own subfamily, designated herein as Skrjabinocoelinae n. subf. These authors then distribute the remaining genera (where the testes are either diagonal or tandem) into 2 basic groups, those in which the genital pore is prepha-


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ryngeal (Hyptiasmus, Cyclocoelum and Prohyptiasmus) and those where the genital pore is postpharyngeal (Allopyge, Morishitium and Neohyptiasmus). Allopyge, Hyptiasmus, Morishitium, and Prohyptiasmus have body type 5, and are assigned herein to Hyptiasminae, as defined above. Neohyptiasmus also has body type 5, but based on examination of specimens and the literature, I consider the lobed nature of testes (irregular testes) to be too variable of a characteristic in the group to be used in defining this genus, and therefore, I consider it to be synonymous with Morishitium. Neoallopyge also has body type 5; however, based on the revised key proposed herein, I do not feel there is sufficient difference between it and Allopyge to support its retention, and therefore consider it to be synonymous with the later genus. In the key to genera within Cyclocoelinae of Kanev et al. (2002a), the only genus in this subfamily where the intertesticular ovary forms a triangle with the testes (body type 1) is Cyclocoelum, which is assigned to Cyclocoelinae. Using the revised key proposed herein, Selfcoelum (where the genital pore is postpharyngeal rather than prepharyngeal, as is seen in Cyclocoelum) must be placed in Cyclocoelinae with Cyclocoelum as a second genus, because it also has an intertesticular ovary that forms a triangle with the testes (body type 1). In the Ophthalmophaginae, as defined by Kanev et al. (2002a), Ophthalmophagus where the genital pore is prepharyngeal, is separated from the remaining 3 genera these authors have assigned to the subfamily (Promptenovum, Spaniometra, Szidatitrema), where the genital pore is postpharyngeal. Ophthalmophagus, Promptenovum, and Spaniometra have a posttesticular ovary that is in line, or nearly in line, with the testes (body type 4), and should be assigned to Ophthalmophaginae; however, species of Szidatitrema, where the ovary is posttesticular or opposite to the posterior testis and forms a triangle with the testes, represents a body type (body type 3) that is distinct from Ophthalmophagus, Promptenovum, and Spaniometra, and this genus should be assigned to Szidatitreminae n. subf., as defined above. In Haematotrephinae, as defined by Kanev et al. (2002a), Haematotrephus is separated from the remaining 2 genera (Uvitellina; Neohaematotrephus) because it has vitelline fields that are not united (confluent) posteriorly, rather than being united. Species of these 3 genera have an ovary that is pretesticular, or opposite to the anterior testis that forms a triangle with the testes (body type 2), and should be assigned to Haematotrephinae, as defined herein. The genus Wardianum has this same body type, and it should be assigned to this subfamily as a fourth genus.

Acknowledgments I am indebted to Dr. Keith Arnold, Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, Texas for providing birds. We thank the Texas Parks and Wildlife Department and the U.S. Fish and Wildlife Service whose cooperation made this study possible. Patricia Pilitt, United States National Parasite Collection, Beltsville, Maryland, U.S.A., was instrumental in loaning us specimens of cyclocoelids from the USNPC. We also thank Eileen Harris, the Natural History Museum, London, U.K., for allowing us to examine cyclocoelids from the NHM and Dr. Agustín Jiménez, Harold W. Manter Laboratory, University of Nebraska,Lincoln, Nebraska, U.S.A., for lending us specimens of cyclocoelids from the HWML. This study was funded by a grant from the Schubot Exotic Bird Research Center, the Texas Veterinary Center, Texas A&M University, College Station, Texas, U.S.A.

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