Glypthelmins quieta (Stafford, 1900) Stafford, 1905

(Figs. 2–5)

Synonyms

Distomum quietum Stafford (1900): 403 –406, Fig. 4; Glypthelmins quieta Stafford (1905: 686–687); Glypthelmins subtropica Harwood (1936: 31, 36); Glypthelmins californiensis Rankin (1944, 31, 41); Glypthelmins proximus of Babero & Golling (1974: 212–213); Glypthelmins sera of Babero & Golling (1974: 213); Glypthelmins californiensis of León-Règagnon (1992: 152); Glypthelmins californiensis of Pulido-Flores (1994: 205–206) [in parti].

Taxonomic summary

Type-host: Stafford (1900) did not mention the host species, however, the same author in 1905 refers to the species Rana catesbeiana, R. virescens and Hyla pickeringii as hosts of G. quieta.

Habitat: Intestine.

Type-locality: Canada (Locality was not specified).

Type specimens deposition: Stafford (1900, 1905) did not mention the type of specimens that were actually deposited.

Diagnosis: The distinctive characteristic of this species is the presence of prominent peripharyngeal glands, which form acini when grouped. Glands extend from the anterior border of the pharynx to slightly beyond the caecal bifurcation. Additionally, this species possesses symmetrical or slightly oblique testes. Vitelline glands follicular in shape, and extend from the oesophagus to the 2nd third of the body length. Anterodorsally to the ventral sucker, the vitelline follicles converge medially. Uterus formed by several transverse uterine loops, occupying the intercaecal area with some loops extending into the caecal region.

Description: Body elongated with the maximum width in the post-testicular region. Anterior and posterior ends rounded, while the tegument is thick, with diminute spines along the body except in the posterior region. Scale-like spines on the body surface diminish in size and number in middle body, while a lack of spines is observed in the posterior third of body. Oral sucker subterminal, round; ventral sucker in the anterior 3rd of body, round, smaller than oral sucker, located anteriorly to testes, and just posterior to caecal bifurcation: oral sucker/ventral sucker ratio 1:0.63 length, 1:0.54 width. Mouth opening in the middle of oral sucker. Pharynx well-developed, prominent peripharyngeal glands at both sides of pharynx, forming bunches of follicles, extending from the anterior end of pharynx to the level of caecal bifurcation. Peripharyngeal glands open at the anterior border of oral sucker. Oesophagus long, slightly muscular, forming the caecal bifurcation. Caeca extend laterally to the posterior end of body. Left caecum slightly wider than the right one. Testes rounded, symmetrical, posterior to ventral sucker, and located at the middle level of body, intercecal. Right testis slightly anterior to left testis. Cirrus pouch well developed, straight, long, dorsal to ventral sucker, contains a bipartite seminal vesicle, followed by prostatic duct and cirrus. Cirrus short, unarmed, opens to the genital pore, which is located between the ventral sucker and the caecal bifurcation. Ovary rounded to oval, intercaecal, located posteriorly and to the left of ventral sucker. Seminal receptacle usually inconspicuous, rounded, located in the area between the ovary, ventral sucker and anterior testis. Uterus coiled, with numerous transverse loops occupying the region from the level of the anterior border of the testes to the posterior end of body, overlapping the caeca. Anterior to testes, uterine loops ascend dorsally to the ventral sucker, forming a muscular metraterm surrounded by glands and opening into the genital pore. Vitelline gland follicular. Vitelline follicles may extend anteriorly to anterior border of pharynx, the level of the oesophagus, or the level of the caecal bifurcation. Posteriorly, follicles reach the testicular region, and they run laterally to the margins of the body occupying the caecal and extracaecal region. Anteriorly to the ventral sucker, vitelline follicles are confluent. Eggs operculated, measuring 36–51 µm long by 14–21 µm wide. Excretory vesicle “I” shaped. Excretory pore located at the posterior border of body.

Host, geographic distribution and specimen deposition

Acris crepitans Baird. U.S.A.: West Lake Okoboji, Dickinson County, Iowa (Ulmer, 1970). Bufo americanus Holbrook. U.S.A.: Presque Isle, Aroostook, Maine (Bouchard, 1951).

Bufo microscaphus Cope: U.S.A.: Utah (Parry & Grundmann, 1965). Specimen deposition: USNPC: 85921.

Bufo woodhousii Girard: U.S.A.: Utah (Parry & Grundmann, 1965); 0.25 miles north of Davey; 5 miles south of Spencer, Nebraska, (Brooks, 1976b).

Hyla crucifer (= Pseudacris crucifer): U.S.A.: U.S.A. (Walton, 1938); Western Massachusetts (Rankin, 1945); Ohio (Odlaug, 1954); Michigan (Najarian, 1955); Fulton, Hancock, Lucas, Ottawa and Wood Counties, Ohio (Ashton & Rabalais, 1978).

Hyla crucifer crucifer Harper (= Pseudacris crucifer crucifer): Canada (Stafford, 1905).

Hyla pickeringii (= Pseudacris crucifer): Canada (Stafford, 1905).

Pseudacris nigrita (LeConte): U.S.A.: Athens, Georgia (Byrd & Maples, 1963a).

Pseudacris triseriata: U.S.A.: North America (Walton, 1946); West Lake Okoboji, Dickinson County, Iowa (Ulmer, 1970); Fulton, Hancock, Lucas, Ottawa and Wood Counties, Ohio (Ashton & Rabalais, 1978). Specimen deposition: HWML: 1090, 1210, 1211.

Rana blairi: U.S.A.: 3 miles south of Lincoln; 0.25 miles north of Davey; Waverly; 2 miles south, 1 mile west of Mead; 3 miles wets of Fremont; 1.5 miles north, 2.5 miles east of Burchard; 5 miles south of Genoa; 0.75 miles east of Ashland; 10 miles south of Humboldt; 0.75 miles north of Winslow; 1.5 miles south of Sprague; 0.5 miles south, 0.5 miles west of Oakland; 2 miles south, 2 miles east of Ceresco; 0.25 miles northwest of Callaway; 3 miles east of Guide Rock; 4.5 miles east, 0.75 miles north of Red Cloud; 2 miles north, 2 miles east of Davenport, Nebraska (Brooks, 1976b). Yuma County, Colorado; Cherokee County, Kansas; Douglas, Lincoln and Sarpy Counties, Nebraska & Carson County, Texas (Goldberg et al. 2000). Specimen deposition: USNPC: 88033, 88043, 88051, 88059; HWML: 20184–20186, 20188, 20189, 20191–20197, 20200, 20201.

Rana catesbeiana: Canada (Stafford, 1905; Walton 1938, 1947). Cuba: Provinz Habana, Binnen-fischereistation bei Loma de Tierra (Odening, 1968). U.S.A.: Urbana, Illinois (Miller, 1930); Cleveland County, Oklahoma (Trowbridge & Hefley, 1934); Illinois (Leigh, 1937); Louisiana (Bennett, 1938); Florida (Manter, 1938); U.S.A. (Walton 1938, 1947); Georgia (Parker, 1941); Amherst, Massachusetts; North Carolina; New England and Seattle, Washington and Gaspe Peninsula (Rankin 1944); (Leigh & Van Cleave, 1945); U.S.A. (Walton 1947); Virginia (Britt, 1947); Ohio (Odlaug, 1954); Michigan (Najarian, 1955); Winsconsin (Schell, 1962); Pocahontas State Park, Chesterfield County, Virginia (Campbell, 1968). West Lake Okoboji, Dickinson County, Iowa (Ulmer, 1970); Glendale, Daviess County; Willow Slough, Newton County; Tri, Kosciusko and Noble Counties, Indiana (Lank, 1971). Kansas, (Jinks & Johnson, 1971); Burke, Oconee, Screven, Chatham and Taliaferro Counties, Georgia, Terrebone and East Baton Rouge Parishes, Louisiana and Oktibbeha County, Mississippi (Sullivan, 1972); East Texas (Hollis, 1972); Ash Meadow, Nye County, Nevada (Babero & Golling, 1974); 9. 2 miles west of Lincoln; 1.5 miles north, 2.5 miles east of Burchard; 8 miles south, 2 miles east of Humboldt; 10 miles south of Humboldt; 0.25 miles west of Verdon; 0.5 miles north, 1 mile west of Atkinson; 5 miles north, 2 miles west of Springview; 1 mile north, 3.5 miles west of Guide Rock, Nebraska (Brooks 1976b); Georgia, Mississippi and Louisiana (Sullivan, 1976); Fulton, Hancock, Lucas, Ottawa, Ohio (Ashton & Rabalais, 1978); Arkansas (Rossen & Manis, 1976); Big Muddy River, Illinois (Andrews et al. 1992). Specimen deposition: USNPC: 66142, 72269, 72270, 82012, 84282, 84283, 84802, 84814; HWML: 19721, 20174– 20178, 20187, 20229, 20643, 20925, 20938, 20956, 22675, 31273.

Rana chiricahuensis Platz & Mecham: U.S.A.: Arizona (Goldberg et al. 1998). Specimen deposition: USNPC: 87074.

Rana clamitans: U.S.A.: Illinois (Miller, 1930); U.S.A. (Walton 1938). Massachusetts (Rankin, 1945); Island Presque, Aroostook, Maine (Bouchard, 1951); Michigan (Najarian, 1955); Pocahontas State Park, Chesterfield County, Virginia (Campbell, 1968); Dekalb & Oglethorpe Counties, Georgia and Warren County, New Jersey (Sullivan, 1972); Connecticut (Brooks, 1976b); Georgia and New Jersey (Sullivan, 1976); Red Cedar River, Baron and Dunn Counties, Wisconsin (Williams & Taft, 1980); Battle Creek, Michigan (Rannala, 1990, 1991, 1992). Specimen deposition: USNPC: 51635, 72268, 75450, 81462, 90977; HWML: 15355, 15379, 23829.

Rana dunni: México: Lago de Pátzcuaro, Michoacán (Pulido-Flores, 1994). Lago de Pátzcuaro and Lago de Zacapu, Michoacán (Razo-Mendivil et al. 1999; Pérez-Ponce de León et al. 2000). Specimen deposition: CNHE: 1561, 3273, 3274, 4687; HWML: 39954.

Rana magnaocularis: México: Sinaloa (Goldberg & Bursey, 2002); Coquimatlán, Colima (this study). Specimen deposition: CNHE: 5030; USNPC: 89820.

Rana megapoda: México: Manantiales de Cointzio, Michoacán (Razo-Mendivil, 1998: 1–50). Lago de Cuitzeo and Manantiales de Cointzio, Michoacán (Razo-Mendivil et al. 1999). Lago de Cuitzeo and Manantiales de Cointzio, Michoacán and Lago de Chapala, Jalisco (Pérez-Ponce de León et al. 2000). Specimen deposition: CNHE: 3406, 3346.

Rana montezumae: México (Walton, 1938); Ciénaga de Lerma, Estado de México (León-Règagnon, 1992; Razo-Mendivil et al. 1999; Pérez-Ponce de León et al. 2000); Xochimilco, Distrito Federal and Lago de Texcoco, Estado de México (Lamothe-Argumedo et al. 1997). Specimen deposition: CNHE: 1461, 1562, 1563, 3271, 3275–3279, 4686; HWML: 39955.

Rana neovolcanica: México: Manantiales de Cointzio, Michoacán, (Razo-Mendivil et al. 1999; Pérez- Ponce de León et al. 2000); Tapalpa, Jalisco. Specimen deposition: CNHE: 3272, 3416, 3421, 5028.

Rana palustris LeConte: U.S.A.: Isla Presque, Aroostook, Maine (Bouchard, 1951); Arkansas (McAllister et al. 1995). Specimen deposition: USNPC: 84217.

Rana pipiens: U.S.A.: Illinois (Miller, 1930; Leigh, 1937, 1937b, 1946; Leigh & Van Cleave, 1945); Utah (Parry & Grundmann, 1965); U.S.A. (Walton, 1938; Rankin, 1944); Brazos County, Texas, West Lake Okoboji, Dickinson County, Iowa, (Ulmer, 1970); 1 mile north of Louisville; 5 miles north, 2 miles west of Springview; 7 miles north, 1 mile west of Springview; 12 miles east of Marsland; 10 miles north of Whitman; 12 miles west of Mullen; 0.25 miles northwest of Callaway; 5 miles north, 2 miles west of Springview Nebraska (Brooks, 1976b); Franklin County, Ohio; Alamance County, North Carolina and Franklin County, Tennessee (Sullivan, 1972); Arkansas (Rosen & Manis, 1976); White Earth River, Mountrail County, North Dakota and Southeast Nebraska (O’Grady, 1987). Barnes and Sargent County, North Dakota, Beadle and Manlin County, South Dakota (Goldberg et al. 2001). Specimen deposition: USNPC: 72271, 88785; HWML: 1209, 22473, 20179–20182, 20190, 20198–20199, 20897.

Rana pipiens sphenocephala Stejneger & Barbour: U.S.A.: Oklahoma (Trowdbridge & Hefley, 1934).

Rana psilonota: México: Atenquique, Jalisco. (This study) Specimen deposition: CNHE: 5029.

Rana septentrionalis Baird: U.S.A.: Isla Presque, Aroostook, Maine (Bouchard, 1951).

Rana spectabilis: México: Huitzo, Oaxaca (This study) Specimen deposition: CNHE: 4689.

Rana sylvatica LeConte: U.S.A.: Rose Lake Wildlife Area, Shiawassee and Clinton Counties, Michigan (Muzzall & Peebles, 1991).

Rana sphenocephala: U.S.A.: (locality not specified) (Walton, 1938).

Rana tarahumarae Boulenger: México: Yecora, Sonora (Bursey & Goldberg, 2001). Specimen deposition: USNPC: 89181.

Rana utricularia (= R. sphenocephala): U.S.A.: Vicinity of Nemo, Somerville County, Texas (O’Grady, 1987). Specimen deposition: USNPC: 84280, 84281; HWML: 20890, 20954.

Rana virescens (= R. sphenocephala): Canada: (locality not specified), (Stafford, 1905).

Rana yavapaiensis Platz & Frost: U.S.A.: Arizona (Goldberg et al. 1998). Specimen deposition: USNPC: 87080.

Rana sp.: México: Coquimatlán, Colima; Atenquique, Jalisco (This study). Specimen deposition: CNHE: 4688, 5031–5033.

Rana sp. form Colima: México: Coquimatln, Colima.

Rana spp.: Toronto, Canada: (locality not specified) (Cheng, 1959).

Frog: Canada: (locality not specified) (Stafford, 1900).

Frogs: U.S.A.: Georgia, Louisiana, Mississippi and North Carolina (Byrd & Maples, 1963a). Physa gyrina Say: U.S.A.: Seattle, Washington (Rankin 1944); Charlies Pond, North Carolina (Snyder & Esch, 1993).

Life cycle

As studied by Rankin (1944) and Leigh (1946), adults inhabit the intestine of a wide range of species of anurans. Embryonated eggs are expelled with the feces of the host. In the water, eggs are ingested by snails of the species Physa gyrina (Physidae), where they hatch and the miracidiuim rapidly transforms into mother and then daughter sporocysts. Within sporocysts, cercariae (xiphidocercarie type, possessing stylets) are formed. Cercariae leave the snail, swimming actively to the surface of the body water, looking for the second intermediate host, usually tadpoles. Once the host is detected, cercariae attaches to the skin to become encysted in the epidermis transforming into a metacercariae. Metacercariae is the infective stage to the definitive host. Frogs become infected when they eat their own skin during molting. The adult forms are established in the intestine of their definitive hosts.

GenBank

Cytochrome oxydase 1 gen (cox 1): AY278056 (383 pb); 18s ribosomal gene: AJ287517 (1951 bp); 5.8S ribosomal RNA gene and internal transcribed spacer (ITS2): AY278063 (413 pb); 28s ribosomal gene: AF433675 (1250 pb), AY222278 (1256 pb), AY278049 (1274 pb), DQ452535 – DQ452537 (1274).