Selfcoelum lamothei, n. sp. (Digenea: Cyclocoelidae: Cyclocoelinae) de los sacos aéreos del playero de pico largo, Numenius americanus (Scolopacidae), del área del condado de Galveston, Texas, EUA
Charles K. Blend1* and Norman O. Dronen2
1Department of Biology, Gordon College, 255 Grapevine Road, Wenham, Massachusetts, 01984, USA.
2Laboratory of Parasitology, Department of Wildlife and Fisheries Sciences, Texas A & M University, 2258 TAMU, College Station, Texas 77843–2258 USA.
]]> *Correspondent:
Recibido: 27 julio 2007
Aceptado: 01 febrero 2008
Abstract
Fourteen specimens of a new species of cyclocoelid, Selfcoelum lamothei n. sp. (Digenea: Cyclocoelidae: Cyclocoelinae), from the air sacs of a long–billed curlew, Numenius americanus Bechstein (Scolopacidae), collected from the Galveston area, Galveston County, Texas, USA, were examined. The new species has an intertesticular ovary that forms a triangle with the testes, placing it in Cyclocoelinae Stossich, 1902. The new species is most similar to Selfcoelum capellum (Khan, 1935) n. comb., but differs from this species by lacking an oral sucker and by having a somewhat larger ovary, larger testes, a smaller posttesticular space, a larger cirrus sac, larger eggs, and the vitelline follicles of S. lamothei n. sp. are more bulky making the vitelline fields more laterally extensive, and more anteriorly distributed (reaching anteriorly to the level of the pharynx compared to the level of the cecal bifurcation) than those of S. capellum. The new species can be distinguished from the 2 species currently assigned to Selfcoelum Dronen, Gardner and Jiménez, 2006, S. brasilianum (Stossich, 1902) and S. limnodromi Dronen, Gardner and Jiménez, 2006, by having an intercecal uterus rather than having uterine loops that overreach the ceca laterally. The genus Selfcoelum should be emended to include those species where the uterus is either intercecal or where the uterine loops overreach the ceca laterally and those species with or without an oral sucker.
Key words: curlew, Numenius americanus, Selfcoelum capellum n. comb., Selfcoelum lamothei n. sp., Cyclocoelidae, Galveston, Texas.
]]> Resumen
Se examinaron 14 ejemplares de una nueva especie de ciclocélido, Selfcoelum lamothei n. sp. (Digenea: Cyclocoelidae: Cyclocoelinae) que es parásito de los sacos aéreos del playero de pico largo, Numenius americanus Bechstein (Scolopacidae), recolectados en el condado de Galveston, Texas, EUA. La especie nueva se caracteriza por presentar el ovario en posición intertesticular, formando un triángulo con relación a los testículos. Este rasgo sitúa a la nueva especie entre los Cyclocoelinae Stossich, 1902. Selfcoelum lamothei n. sp. es parecida a Selfcoelum capellum (Khan, 1935) n. comb., pero difiere de ésta por carecer de ventosa oral, por tener el ovario ligeramente más grande, un número mayor de testículos, menor espacio postesticular, una bolsa del cirro más grande, huevos de mayor tamaño, y vitelógenas más voluminosas arregladas en campos más extensos y distribuidas en la región anterior (alcanzando el nivel de la faringe en S. lamothei n. sp. y sólo hasta la bifurcación cecal en S. capellum). Asimismo, la especie nueva se distingue de las 2 especies asignadas a Selfcoelum Dronen, Gardner and Jiménez, 2006, S. brasilianum (Stossich, 1902) y S. limnodromi Dronen, Gardner and Jiménez, 2006, por tener el útero en posición intercecal y no lateralmente extendido más allá de los ciegos intestinales. El género Selfcoelum se debe enmendar para incluir las especies donde el útero está en posición intercecal, aquellas donde se extiende lateralmente más allá de los ciegos intestinales, y aquellas con ventosa oral ausente o presente.
Palabras clave: playero de pico largo, Numenius americanus, Selfcoelum capellum n. comb., Selfcoelum lamothei n. sp., Cyclocoelidae, Galveston, Texas.
Introduction
The long–billed curlew, Numenius americanus Bechstein (Scolopacidae), is a wading bird that is most frequently found in prairies and grassy meadows near water. It is specifically found in marshes, wet fields, damp grasslands, and along ponds, lakes and some coastal marine areas (American Ornithologist's Union, 1983). Although it is not commonly found along the east coast of the USA, this species ranges from Alaska and southwestern Canada through the western USA and the Gulf of Mexico, to as far south as Costa Rica (American Ornithologist's Union, 1983). The parasite fauna of the long–billed curlew is somewhat diverse. At present 2 acanthocephalans, 1 acarinid, 7 cestode, 12 digenean, 5 mallophagan and as many as 8 nematode species have been reported from this host (Table 1). The only cyclocoelid previously reported from the long–billed curlew was Cyclocoelum obscurum (Leidy, 1887) (Dubois, 1959; Dronen and Badley, 1979; Lamothe–Argumedo and Orozco–Flores, 2000).
Selfcoelum Dronen, Gardner, and Jiménez, 2006 was established by Dronen et al. (2006) with the description of Selfcoelum limnodromi Dronen, Gardner, and Jiménez, 2006 from the air sacs of the long–billed dowitcher, Limnodromus scolopaceus (Say) (Charadriiformes: Scolopacidae), from Oklahoma, USA. There are currently 2 species assigned to Selfcoelum, Selfcoelum brasilianum (Stossich, 1902) Dronen, Gardner and Jiménez, 2006, originally described as Cyclocoelum brazilianum Stossich, 1902, from the abdominal cavity of the lesser yellowlegs, Tringa flavipes (Gmelin) (reported as Scolopax flaviceps Gmelin) from Brazil (Stossich, 1902), and the type species, Selfcoelum limnodromi.
Materials and methods
Ten long–billed curlews, N. americanus, collected from Galveston, Galveston County, Texas, USA between August, 1977 and October, 1978, and 2 long–billed curlews collected from Lake Bryan, Brazos County, Texas, USA in September, 1996 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 collected 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 from mounted specimens and are given in micrometers (μm) 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, USA. The following specimens from HWML were examined: Selfcoelum limnodromi (HWML 41212, 48162, 48163). Identification of digeneans to subfamily and genus was based on the key of Dronen (2007) and ecological terms used follow Bush et al. (1997).
]]>Description
Selfcoelum lamothei n. sp. (Figs. 1–3)
Description based on 10 specimens. Body large, tapered anteriorly, 17.3 (16.3–18.1) mm long by 3.6 (3.0–4.0) mm wide at widest point. Oral sucker and acetabulum absent. Mouth slightly subterminal; prepharynx 305 (220–350) long; pharynx well developed, 285 (270–300) long by 275 (260–300) wide; esophagus longer than prepharynx, 465 (390–550) long. Ratio of length of prepharynx to length of esophagus 1:1.5. Ceca generally simple, some specimens with irregular inner margins forming large bulges, uniting near posterior extremity to form cyclocoel. Testes smooth, spherical to subspherical, occasionally lobed, dextral to midline, arranged diagonally in intercecal region of posterior 1/7 of body. Anterior testis 0.815 mm (0.650–1.060) long by 1.035 mm (0.830–1.250) wide. Posterior testis 0.885 mm (0.785–1.000) long by 0.970 mm (0.870–1.250) wide. Intertesticular space 1.115 mm (0.650–1.700). Posttesticular space 0.915 mm (0.750–1.075). Cirrus sac 630 (550–700) long by 220 (190–270) wide. Seminal vesicle occupying posterior region of cirrus sac; proximal end of ejaculatory duct looping once before passing through small cluster of prostate cells to terminate at genital pore, which is postpharyngeal, at level of posterior 1/4 of pharynx, near midline of body. Ovary smooth, oval, 525 (480–600) long by 535 (470–590) wide, intertesticular and sinistral to midline of body, forming triangle with testes. Ratio of width of ovary to mean width of testes 1:1.9. Uterine seminal receptacle well developed, 560 (490–585) long by 220 (195–265) wide. Mehlis' gland immediately posterior to and overlapping posterior margin of ovary. Laurer's canal absent. Vitelline follicles bulky, more laterally extensive than usually seen in most cyclocoelids, distributed along ceca from level of pharynx to posterior extremity, not confluent posteriorly. Vitelline follicles approximately 145 (75–260) wide near anterior end; 480 (340–560) wide near lateral margins of midbody. Vitelline reservoir immediately posterior to Mehlis' complex. Uterus extensive, intercecal, extending from posterior level of pharynx to intertesticular area. Uterine seminal receptacle posterior to Mehlis' complex and immediately dorsal to vitelline reservoir. Eggs indistinctly operculate, measuring at distal end of uterus 145 (135–160) long by 65 (60–75) wide; miracidia oculate. Excretory vesicle Y–shaped; anterior extent of arms not observed. Excretory pore subterminal on dorsal surface of body.
Taxonomic summary
Type host: the long–billed curlew, Numenius americanus Bechstein, 1812 (Scolopacidae).
Site of infection: air sacs of lungs.
Type locality: vicinity of Galveston, Galveston County, Texas, USA (29°18' N latitude, 94°48' W longitude).
Prevalence: 33% (4 of 12 birds).
Intensity: 2–5 per infected bird.
]]> Mean intensity: 2.5.Type specimens: holotype HWML 48562; paratypes (2 specimens) 48563.
Etymology: the species is named in honor of Dr. Rafael Lamothe–Argumedo in recognition of his many contributions to our knowledge of the helminths of vertebrates from the wild.
Remarks
The new species is assigned to Cyclocoelinae Stossich, 1902 because it has an intertesticular ovary (ranging from the level of the posterior end of the anterior testis to the anterior end of the posterior testis) that forms a triangle with the testes (Dronen, 2007). The testes in the new species are tandem to slightly diagonal and usually smooth; the vitelline fields are not united posteriorly; and the uterus is intercecal further supporting placement of this new species within Cyclocoelinae. Within Cyclocoelinae, Dronen (2007) recognized 2 genera: Cyclocoelum Brandes, 1892 containing those species with a prepharyngeal genital pore (ranging from anterior end of pharynx to midlevel of prepharynx), and Selfcoelum, containing those species with a postpharyngeal genital pore (ranging from midlevel of pharynx to near level of cecal bifurcation). The new species possesses a postpharyngeal genital pore that is at the level of the posterior 1/4 of the pharynx supporting placement of this new taxon in Selfcoelum.
While this new species is most similar to species of Selfcoelum by having a postpharyngeal genital pore, it differs from nominal species in the genus in having an intercecal and intertesticular uterus extending from the posterior level of the pharynx to the area between the testes, rather than having uterine loops that overreach the ceca laterally. Therefore, the generic diagnosis of Selfcoelum should be emended to include those species where the uterus is either intercecal or where the uterine loops overreach the ceca laterally. There are currently 2 species assigned to Selfcoelum, S. brasilianum and S. limnodromi. The new species can be distinguished from both of these species by having an intercecal uterus. A third species, Cyclocoelum capellum Khan, 1935, described from the air sacs of the common snipe, Capella gallinago (Linnaeus), from India (Khan, 1935), has an intertesticular ovary that forms a triangle with the testes (Cyclocoelinae). Dubois (1959) synonymized this species with C. obscurum, the only other cyclocoelid reported from N. americanus (see Table 1); however, we do not support this synonymy. Based on the data for both C. capellum and C. obscurum provided by Dubois (1959, p. 78–79), C. capellum differs from C. obscurum in the former species having a larger body (17.0–25 mm vs 6.0–13 mm long) and a smaller egg (120–130 by 64–68 vs 138–162 by 70–94). In addition, we noted that unlike species of Cyclocoelum where the genital pore is prepharyngeal, C. capellum has a postpharyngeal genital pore as is typical of species of Selfcoelum (Dronen, 2007). We have therefore reassigned C. capellum to Selfcoelum, as Selfcoelum capellum (Khan, 1935) n. comb. Unlike S. brasilianum, S. limnodromi, and S. lamothei n. sp., S. capellum possesses an oral sucker; therefore, the generic diagnosis of Selfcoelum should be emended to include either the presence or absence of an oral sucker.
Of the 3 nominal species now considered in Selfcoelum, the new species is most similar to S. capellum in body size (17.0–25 mm), the size of the uterine seminal receptacle (300–400 by 150–200), the width of the pharynx (275), and because S. capellum also has an intercecal uterus and a uterine seminal receptacle ("receptaculum seminis uterinum" of Yamaguti [1933]; "receptacle seminalis uterinum"of Harrah [1922]). It differs from S. capellum by having a somewhat larger ovary (370–500), larger testes (1.003 mm approximate mean width of testes; 1:1.9 ratio of width of ovary to mean width of testes compared to 790; 1:1.7), a smaller posttesticular space (1.200 mm), a larger cirrus sac (400 by 170), larger eggs (120–130 long by 64–68 wide), and the vitelline follicles of S. lamothei n. sp. are more bulky making the vitelline fields more laterally extensive, and they are more anteriorly distributed (reaching anteriorly to the level of the pharynx compared to the level of the cecal bifurcation) than those of S. capellum.
Discussion
Dronen (2007) recognized 6 subfamilies in Cyclocoelidae Stossich, 1902: Cyclocoelinae; Haematotrephinae Dollfus, 1948; Hyptiasminae Dollfus, 1948; Ophthalmophaginae Harrah, 1922; Skrjabinocoelinae Dronen, 2007; and Szidatitreminae Dronen, 2007. Within Haematotrephinae, S. lamothei n. sp. is most similar to species of Haematotrephus Stossich, 1902 (syns. Corpopyrum Witenberg, 1923; Haematoprimum Witenberg, 1923; Harrahium Witenberg, 1923) in having a postpharyngeal genital pore, non–confluent vitelline fields posteriorly and diagonal testes forming a triangle with the ovary; however, the ovary of the new species is intertesticular while species of Haematotrephus have an ovary that is pretesticular to opposite the anterior testis. Within Hyptiasminae, the new species is most similar to species of Morishitium Witenberg, 1928 (syns. Pseudhyptiasmus Dollfus, 1948; Neocyclocoelum Feizullaev, 1980; Neohyptiasmus Kanev, Radev and Fried, 2005) in having a postpharyngeal genital pore, non–confluent vitelline fields posteriorly, and an intertesticular ovary; however, S. lamothei n. sp. has diagonal testes that form a triangle with the ovary whereas species of Morishitium have tandem testes that form nearly a straight line with the ovary. Of the species within Ophthalmophaginae, S. lamothei n. sp. is most like species of Spaniometra Kossack, 1911 (syns. Bothriogaster Fuhrmann, 1904; Contracoelum Witenberg, 1926; Bothrigaster Dollfus, 1948) in possessing a postpharyngeal genital pore and non–confluent vitelline fields posteriorly, but the new species has an intertesticular ovary forming a triangle with the testes and species of Spaniometra have a posttesticular ovary nearly in a straight line with the testes. Species of Skrjabinocoelum Kurashvili, 1953, the only genus within Skrjabinocoelinae Dronen, 2007, are similar to the new species in having a postpharyngeal genital pore and an intertesticular ovary; however, the testes are nearly side by side and form a straight line with the ovary in species of Skrjabinocoelum while the testes are diagonal and form a triangle with the ovary in the new species. Species of Szidatitrema Yamaguti, 1971, the only genus of Szidatitreminae Dronen, 2007, are similar to S. lamothei n. sp. in possessing a postpharyngeal genital pore, non–confluent vitelline fields posteriorly, and an ovary forming a triangle with diagonal testes; however, the new species has an ovary that is intertesticular whereas species of Szidatitrema have an ovary that is posttesticular or opposite the posterior testis.
]]> As mentioned above, Cyclocoelum obscurum (Leidy, 1887) Harrah, 1922, reported from the body cavity and air sacs of 2 long–billed curlews from Texas (Dronen and Badley, 1979; also see Dubois, 1959 and Lamothe–Argumedo and Orozco–Flores, 2000), represents the only other cyclocoelid documented from this host (Table 1). While C. obscurum and S. lamothei n. sp. are within Cyclocoelinae, species of Selfcoelum differ from species of Cyclocoelum in the former having a postpharyngeal genital pore and the latter having a prepharyngeal genital pore (Dronen, 2007).
Acknowledgments
We are 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, was instrumental in loaning us specimens of cyclocoelids. We also thank Eileen Harris, the Natural History Museum, London, for also allowing us to examine cyclocoelids and Dr. Agustín Jiménez, Harold W. Manter Laboratory, University of Nebraska, Lincoln, for lending us specimens of cyclocoelids from the HWML. Dr. Leasa Lutes, Department of Foreign Language and Linguistics, Gordon College, Wenham, Massachusetts helped with Spanish translation. This study was funded by a grant from the Schubot Exotic Bird Research Center, the Texas Veterinary Center, Texas A&M University, USA.
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