Caiguiria himantopae n. sp. (Digenea: Heterophyidae) and Other ...

Comp. Parasitol. 72(1), 2005, pp. 22–27

Caiguiria himantopae n. sp. (Digenea: Heterophyidae) and Other Endohelminths from the Black-Necked Stilt, Himantopus mexicanus (Recurvirostridae), from the Galveston Area of the Texas Gulf Coast, U.S.A. NORMAN O. DRONEN,1,3 CHARLES K. BLEND,2

AND

ALISHA J. DAVIS1

1 Laboratory of Parasitology, Department of Wildlife and Fisheries Sciences, Texas A&M University, 2258 TAMU, College Station, Texas 77843-2258, U.S.A. (e-mail: [email protected]) and 2 Department of Biology, Gordon College, 255 Grapevine Road, Wenham, Massachusetts 01984, U.S.A. (e-mail: [email protected])

One of 2 black-necked stilts, Himantopus mexicanus, collected from Galveston, Texas, U.S.A., was infected with 60 Caiguiria himantopae n. sp. (Heterophyidae). The new species most closely resembles Caiguiria crassa but differs from it in having a Y-shaped excretory vesicle that lacks lateral branches off the vesicle stem rather than a saccate vesicle with additional lateral branches; ceca that terminate at the level of the ovary rather than extending posteriorly to the testes; and placement of the seminal receptacle on the midline of the body occupying the anterior aspect of the intertesticular space rather than sinistral and some distance ahead of the left testis. Dicranotaenia himantopodis was the only endohelminth found that had been previously reported from black-necked stilts. Allopyge sp., Ascocotyle sp., and Chevreuxia sp. were also found and are new host records. KEY WORDS: Allopyge sp., Ascocotyle sp., black-necked stilt, Caiguiria himantopae, Cestoda, Chevreuxia sp., Dicranotaenia himantopodis, Digenea, Galveston, Gulf of Mexico, Himantopus mexicanus, Nematoda, Recurvirostridae, Texas, Trematoda, U.S.A. ABSTRACT:

The black-necked stilt Himantopus mexicanus (Mu¨ller, 1776) is an uncommon shorebird found in grassy marshes, mud flats, pools, and shallow lakes ranging from western and southern North America through Central America and the West Indies to northern South America and the Galapagos (Robinson et al., 1999). This species is infrequently found along the Texas Gulf coast but occurs in somewhat greater numbers inland in the state (Pulich, 1988). Hinojos and Canaris (1988) surveyed 35 blacknecked stilts from El Paso County, Texas, U.S.A., and reported 7 cestodes (Acoleus vaginatus [Rudolphi, 1819], Davainea himantopodis [Krabbe, 1869], Diplophallus polymorphus [Rudolphi, 1819], Eurycestus avoceti Clark, 1954, Hymenolepis himantopodis [Krabbe, 1869], Hymenolepis sp., and Infula macrophallus Coil, 1955), 5 trematodes (Cloacitrema michiganensis McIntosh, 1938, Cyclocoelum lanceolatum [Wedl, 1858], Notocotylus sp., Parastrigea mexicana Coil, 1957, and Tanaisia fedtschenkoi Skrjabin, 1924), and 7 nematode taxa (Capillaria anatis [Schrank, 1970], Capillaria contorta [Creplin, 1839], Capillaria mergi Madsen, 1945, Capillaria sp., Chevreuxia americana Schmidt, 1968, Eustrongylides mergorum [Rudolphi, 1809], and Splendidofilaria sp.). These authors also provided a checklist of parasites

3

previously reported from the black-necked stilt in North America. The following endohelminths from blacknecked stilts were not included in their checklist or have been published since its compilation: Choanotaenia rostellata (Fuhrmann, 1908) from Brazil (Fuhrmann, 1908); Cosmocephalus sp. from Cuba (Barus, 1966); Davainea minuta (Krabbe, 1869) from California, North Dakota, and Utah, U.S.A. (Burt, 1980; D. R. R. Burt and M. D. B. Burt, 1984); Eumegacetes garridoi Macko, 1994, from Cuba (Macko, 1994); Hofmonostomum himantopodis Harwood, 1939, from Puerto Rico (Harwood, 1939); Microphallus szidati Martorelli, 1986, from Argentina (Martorelli, 1986); and Caiguiria anterouteria Nasir and Dıáz, 1971, from Venezuela (Nasir and Dıáz, 1971). There are 3 nominal species in Caiguiria Nasir and Dıáz, 1971 (Heterophyidae [Leiper, 1909]): C. anterouteria from a kitten experimentally infected with metacercariae from the naturally infected guppy, Poecilia reticulata Peters, 1859 (as Lebistes reticulatus [Peters, 1859]), from San Juan de Macarapana, Venezuela (Nasir and Dıáz, 1971); Caiguiria crassa (Ostrowski de Nuń˜ez, 1995) from experimentally infected domesticated red junglefowl, Gallus gallus domesticus (Linnaeus, 1758) (as Gallus domesticus [Linnaeus, 1758]), from Argentina (Ostrowski de Nuń˜ez, 1995); and Caiguiria macrostomum (Travassos, 1928) from the Norway rat Rattus norvegicus (Berkenhout, 1976) from Brazil (Travassos, 1928).

Corresponding author. 22

DRONEN ET AL.—ENDOHELMINTHS FROM HIMANTOPUS MEXICANUS

Table 1. Summary of the helminths collected from the black-necked stilt Himantopis mexicanus from Galveston Texas, U.S.A., with their sites of infection and museum accession numbers. Endohelminth found Cestoda Dicranotaenia himantopodis Nematoda Chevreuxia sp. Trematoda Allopyge sp. Ascocotyle sp. Caiguiria himantopae n. sp.

23

RESULTS One cestode, 3 trematodes, and 1 nematode were found in this study (Table 1).

Site of infection

USNPC numbers

Caiguiria himantopae n. sp. (Figs. 1–3)

Intestine

095044

(Syn. C. anterouteria of Rietschel and Werding, 1978; Caiguiria sp. of Dronen et al., 2004).

Intestine

095046

Air sacs Intestine Intestine

094819, 094820 095045 095038-095043

Description

Dronen et al. (2004) redescribed C. anterouteria based on museum specimens, separating out C. crassa from the original materials used by Nasir and Dıáz (1971) in their description. Note that the original paratype of C. anterouteria (United States National Parasite Collection [USNPC 071428]) has been relabeled C. crassa. Also, the accession numbers of the voucher specimens at the USNPC originally identified as C. anterouteria by Fischthal and Nasir (1974) that are C. crassa have been assigned new accession numbers (USNPC 068108-094594; 072784-094595). During a survey of the parasites of wading birds from the Texas Gulf coast, a new species of Caiguiria was found in H. mexicanus. This new endohelminth from the black-necked stilt is described herein.

MATERIALS AND METHODS Two adult moribund black-necked stilts, H. mexicanus, collected from Galveston Bay, Texas, U.S.A., that died on 11 August 1977 and 14 September 1996 were examined for helminth parasites (U.S. Fish and Wildlife Service permit no. PRT 760668; Texas Parks and Wildlife Department permit no. TX SPH 0491253). Digeneans found were relaxed in saline, studied alive, heat fixed under slight coverslip pressure in alcohol–formalin–acetic acid, stained in Semichon’s carmine, and mounted in Kleermount or Canada balsam. Nematodes were fixed in warm 70% ethanol and cleared in a 50:50 solution of 70% ethanol and glycerine. Drawings were made with the aid of a drawing tube. Measurements are in micrometers (lm) and are presented as means followed by the range in parentheses unless otherwise stated. The holotype and paratypes were deposited in the USNPC, Beltsville, Maryland, U.S.A. The following specimens were examined: C. anterouteria USNPC 068108, 071427, 072784; C. crassa USNPC 094594, 094595; C. macrostomum the Natural History Museum, London, U.K., (NHM) 1997.6.9.1; Caiguiria sp. the Senckenberg Museum, Frankfurt, Germany, (SMF) 3583, 3584; C. americana USNPC 078871; C. lanceolatum USNPC 078879; H. himantopodis USNPC 078874.

Based on 10 adult specimens. With characteristics of genus. Body small, pyriform to slightly elongate, spinose, 565 (475–650) long by 330 (245–445) wide; forebody 265 (215–330) long; remnants of cercarial eyespots present near anterior end. Mouth subterminal; oral sucker unarmed, 54 (42–65) by 61 (50–70); prepharynx 40 (30–58) long; pharynx 43 (37–48) by 38 (35–58); esophagus longer than prepharynx, 55 (45–95) long; cecal bifurcation approximately 2/3 the distance down forebody; ceca moderately long, terminating about 2/3 the distance to posterior extremity. Ratio of widths of pharynx and oral sucker 1:1.6. Acetabulum approximately equal in size to oral sucker, partially embedded in parenchyma, 57 (50– 63) by 62 (58–64). Ratio of sucker widths 1:1.0. Testes smooth, transversely elongate, side by side, removed from posterior end by a short distance leaving a posttesticular space that occupies posterior 1/8 of body. Right testis 57 (55–70) by 102 (60–111); left testis 65 (45–100) by 97 (70–138). Male terminal genitalia simple, composed of a reduced pars prostatica, 87 (72–104) by 17 (15–19), and an ejaculatory duct. Cirrus absent. Prostate cells present, surrounding narrow isthmus just behind pars prostatica immediately followed by large seminal vesicle winding extensively between acetabulum and testes, 80 (53–103) by 97 (70–140). Acetabulogenital complex immediately preacetabular, composed of a transversely elongate genital atrium that receives a simple metraterm, proximal end of ejaculatory duct and gonotyl before opening ventrally at anterior margin of acetabulum through a large, slit-like genital pore. Gonotyl slightly sinistral to midline of body, composed of 10 folds, situated in an oval chamber, 44 (34–58) by 26 (23–31). Ovary smooth, transversely elongate, situated a short distance anterior to right testis, 62 (45–80) by 75 (55–88). Seminal receptacle spherical, on midline of body, 80 (53–103) by 97 (70–138), very extensive in fully developed specimens, often occupying entire intertesticular region. Laurer’s canal present, opening not observed. Vitelline follicles relatively large, 7 per side, individual

24

COMPARATIVE PARASITOLOGY, 72(1), JANUARY 2005

Figures 1–3. Caiguiria himantopae n. sp. from the black-necked stilt, Himantopus mexicanus. 1. Whole mount, ventral view. 2. Composite drawing of the terminal genitalia, ventral view. 3. Composite drawing of female reproductive system, ventral view. A, acetabulum; C, cecum; G, gonotyl; GP, genital pore; O, ovary; P, pars prostatica; R, seminal receptacle; S, seminal vesicle; T, testis; U, uterus; V, vitelline follicle; VD, vitelline duct.

follicles often subdivided, distributed from level of posterior margin of acetabulum to level of testes, overlapping testes laterally but not invading posttesticular space. Uterus extensive, largely postacetabular but having uterine loops on each side extending anteriorly to the level of pharynx, some loops overreaching ceca laterally approaching body wall, but not extending posteriorly in to posttesticular space. Eggs 18 (17–20) by 10 (8–12) (n ¼ 10). Excretory vesicle Y-shaped, branching at level of ovary, no secondary lateral branches off vesicle stem. Excretory pore subterminal.

Site of infection: Intestine. Prevalence and intensity: 50% (60 worms from 1 of 2 birds). Specimens deposited: Holotype USNPC 095038; paratypes (3 slides) USNPC 095039, 095040; voucher specimens USNPC 095041-095043. Other deposited specimens: SMF 3583, 3584. Etymology: The species designation reflects the genus of the host, Himantopus Brisson, 1760. Remarks

Taxonomic summary Type host: Recurvirostridae: H. mexicanus (Mu¨ller, 1776); black-necked stilt. Type locality: Vicinity of Galveston, Galveston County, Texas, U.S.A. (298189N; 948489W).

There has been a great deal of confusion regarding the assignment of species to 2 similar heterophyid genera, Caiguiria and Pygidiopsis Looss, 1907. Dronen et al. (2004) divided species of Pygidiopsis into 4 basic morphological types: genata type, summa type, macrostomum type, and piclaumoreli type. In the


genata type the oral sucker is armed with spines; the vitelline follicles fall well short of the level of the acetabulum anteriorly extending from the level of the ovary some distance in to the posttesticular space; and the uterus does not exceed the acetabulum anteriorly. The genata types include Pygidiopsis ardea Køie, 1990, Pygidiopsis australis Ostrowski de Nuń˜ez, 1996, Pygidiopsis genata Looss, 1907, Pygidiopsis marivillai Refuerzo and Garcia, 1937, and Pygidiopsis pindoramensis Travassos, 1929. In the summa type the oral sucker is unarmed; the vitelline follicles fall well short of the level of the acetabulum anteriorly extending from the level of the ovary some distance in to the posttesticular space; and the uterus does not exceed the acetabulum anteriorly. The summa types include Pygidiopsis pelecani Wang, 1982, Pygidiopsis phalacrocoracis Yamaguti, 1939, Pygidiopsis plana (Linton, 1928), and Pygidiopsis summa Onji and Nishio, 1916. In the macrostomum type the oral sucker is unarmed; the vitelline follicles reach the level of the acetabulum anteriorly extending posteriorly to the level of the testes but not extensively invading the posttesticular space; and the uterus extends anteriorly in to the preacetabular region. The macrostomum types include Pygidiopsis crassus Ostrowski de Nuń˜ez, 1995, and Pygidiopsis macrostomum Travassos, 1928. In the piclaumoreli type the oral sucker is unarmed; the vitelline follicles fall well short of the level of the acetabulum anteriorly extending posteriorly only to the level of the testes but not reaching the posttesticular space; and the uterus does not exceed the acetabulum anteriorly. Only Pygidiopsis piclaumoreli Dollfus and Capron, 1958, represents the piclaumoreli type. Dronen et al. (2004) found that members of Pygidiopsis belonging to the macrostomum type formed a natural group with C. anterouteria and assigned P. crassus to Caiguiria (Caiguiriinae Nasir and Dıáz, 1971) as C. crassa and they supported the assignment of C. macrostomum to Caiguiria as proposed by Nasir and Dıáz (1971), and Rietschel and Werding (1978), bringing the number of species in the genus to 3. Caiguiria himantopae has an unarmed oral sucker; vitelline follicles that reach the level of the acetabulum, anteriorly extending only to the posterior margin of the testes but not invading the posttesticular space; and, a uterus that reaches in to the region anterior to the acetabulum; therefore, it is placed in Caiguiria. The new species differs from previously described species in the genus in having a Y-shaped excretory vesicle that lacks lateral branches off the vesicle stem rather than having a vesicle with additional pairs of lateral branches. It differs from C. crassa in having ceca that terminate at the level of the ovary rather than

25

extending posteriorly to the testes and in having the seminal receptacle on the midline of body occupying the anterior aspect of the intertesticular space rather than being sinistral some distance ahead of the left testis. It differs from C. macrostomum in having an acetabulum that is approximately the same size as the oral sucker (sucker ratio 1:1.0) rather than being smaller than the oral sucker (1:0.7); has ceca that terminate at the level of the ovary rather than extending posteriorly to the testes; has smaller eggs (17–20 by 8– 12 compared with 24 by 13–16); and, is smaller (565 long as compared with 840). Caiguiria himantopae differs from C. anterouteria in having 10 folds in the gonotyl rather than 6 to 7 (Dronen et al., 2004, table 2). In their redescription of C. anterouteria, Rietschel and Werding (1978) appear to have confounded 2 taxa: C. crassa (cf. their fig. 10A) and C. himantopae (cf. their fig. 10B). A summary of the measurements of the specimens of C. himantopae that Riestchel and Werding (1978) deposited and identified as C. anterouteria was given in table 2 of Dronen et al. (2004) under ‘‘Caiguiria sp.’’ All specimens deposited in the SMF (3583, 3584) by Rietschel and Werding (1978) represent the taxon described herein as C. himantopae. DISCUSSION Although our small host sample size (2) may account at least in part for the low species diversity of helminths seen in the Galveston area (5 species), we found 4 new host records (Allopyge sp., Ascocotyle sp., Chevreuxia sp., and C. himantopae). This suggests possible differences between the trophic structures of the coastal plains of the Texas Gulf coast in contrast to the other ecological settings sampled in previous studies (i.e., high desert of El Paso, Texas, U.S.A.). The collection of a species of Allopyge Johnston, 1913, from the air sacs of a wading bird in North America represents an unusual situation in that species of Allopyge are normally found only in the nasal cavity and interorbital sinuses of cranes, and there is no previous report of this genus from North America (Kanev et al., 2002). There are 5 species of cyclocoels historically assigned to the genus Allopyge: the type species, Allopyge adolphi (Stossich, 1902), originally described as Cyclocoelum adolphi Stossich, 1902, from the grey crane, Grus grus Linnaeus, 1758, from Europe and likely from the grey heron, Ardea cinerea Linnaeus, 1758, in Siberia by Stossich (1902); Allopyge antigones Johnston, 1913, described from the Sarus crane, Grus antigone (Linnaeus, 1758) (as Antigone australasiana [Linnaeus, 1758]) from Australia by Johnston (1913); Allopyge ominosus

26

COMPARATIVE PARASITOLOGY, 72(1), JANUARY 2005

(Kossack, 1911) described from what was likely the grey crane (as ‘‘Grus cinerea Linnaeus, 1758’’) from Germany by Kossack (1911); Allopyge skrjabini Shakhtakhtinskiai, 1951 described from G. grus from Azerbaidzhan by Shakhtakhtinskiai (1951); and Allopyge undulatus Canavan, 1934, described from the Manchurian crane, Grus japonensis (Mu¨ller, 1776) (as Megalornis grus lilfordi Linnaeus, 1758), autopsied at the Philadelphia Zoological Garden by Canavan (1934). Haematotrephus lanceolatum (Wedl, 1858) is the only cyclocoel previously reported (as C. lanceolatum Wedl, 1858) from the blacknecked stilt in North America (Hinojos and Canaris, 1988); however, we have examined the specimen deposited by Hinojos and Canaris (1988), and our species is clearly not a species of Haematotrephus Stossich, 1902. Using the most recent key for cyclocoelids by Kanev et al. (2002), H. lanceolatum is in the subfamily Haematotrephinae Dollfus, 1948, not Cyclocoelinae Stossich, 1902, where Allopyge is assigned because the ovary of H. lanceolatum is pretesticular. The ovary of our species is intertesticular, placing it in Cyclocoelinae. Further, the testes in our specimens are tandem to slightly diagonal; the genital pore is postpharyngeal; and, the vitelline fields are united posteriorly: characteristics of species of Allopyge. Our species differs from all previously described species in Allopyge in that 2 uterine loops on each side extensively invade the posttesticular space; there are no intertesticular uterine loops; and, our species is a parasite in the air sacs of Recurvirostridae (avocets, stilts) in the New World rather than being found in the nasal cavities and interorbital sinuses of Gruidae (cranes) from the Old World. It is probable that our specimens represent an undescribed genus that is similar to Allopyge. There were only 2 specimens of Ascocotyle sp. found in 1 black-necked stilt. The specimens were somewhat damaged during fixation, but they have vitellaria extending anteriorly to the level of the ovary; a double row of spines on the oral sucker; and the oral suckers in these specimens have the characteristic posterior lobe of species of Ascocotyle Looss, 1899. Observations of living specimens indicated that they are most similar to Ascocotyle tenuicollis Price, 1935; however, unlike A. tenuicollis, the esophagus is longer than the prepharynx in our specimens. There have been 2 species of Chevreuxia Seurat, 1918, that have been reported from black-necked stilts: C. americana (Hinojos and Canaris, 1988) and Chevreuxia revoluta (Rudolphi, 1819) (Barus, 1966; Barus and Hernandez, 1971). Although we found only females in this study, our specimens of Chevreuxia sp.

appear to represent a species not previously reported from the black-necked stilt and may represent an undescribed species. Chevreuxia sp. differs from C. americana in having a smaller body size (9,250 long by 115 wide compared with 11,000–17,000 by 203– 229); a smaller egg (27–30 long compared with 35– 36); a shorter tail length (165 long as compared with 190–197); a shorter distance from the anterior margin of the cuticular collarette to the anterior end (270 long compared with 425–510); and, a shorter vestibule length (150 long compared with 150–170) (Schmidt, 1968). Chevreuxia sp. differs from C. revoluta in having a smaller body size (9,250 long compared with 18,300); a somewhat smaller egg size (27–30 long compared with 32); and, a shorter tail length than C. revoluta (165 long compared with 170) (Schmidt, 1968; Yorke and Maplestone, 1969). ACKNOWLEDGMENTS We are indebted to Trudy Beltz of Texas City and Dr. Jackie Cole of Galveston, Texas, licensed bird rehabilitators, and Dr. Keith Arnold, Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, Texas, U.S.A., for providing black-necked stilts. We thank the Texas Parks and Wildlife Department and the U.S. Fish and Wildlife Service whose cooperation made this study possible. We are indebted to Dr. Eric Hoberg, Dr. Ralph Lichtenfels, and Patricia Pilitt, United States National Parasite Collection, Beltsville, Maryland, U.S.A., for providing specimens of Caiguiria, Chevreuxia, Cyclocoelum, and Hymenolepis and for their assistance in the differentiation of species of Pygidiopsis and Caiguiria. We also thank Mrs. Eileen Harris, the Natural History Museum, London, U.K., and Drs. Dieter Fiege and Micheal Tu¨rkay, the Senckenberg Natural History Museum, Frankfurt, Germany, for lending us specimens of Caiguiria or Pygidiopsis (or both). Special thanks to Dr. Rodney Bray, Department of Zoology, the Natural History Museum, London, U.K., and Dr. Robin Overstreet, the Gulf Coast Research Laboratory, Ocean Springs, Mississippi, U.S.A., for providing information concerning the structure of the male terminal genitalia in heterophyids. This study was funded by the Schubot Exotic Bird Research Center, the Texas Veterinary Center, Texas A&M University, College Station, Texas, U.S.A.

LITERATURE CITED Barus, V. 1966. Nema´todos para´sitos de Aves en Cuba. Parte I. Poeyana, Serie A 22:1–37.


Barus, V., and N. L. Hernandez. 1971. Nema´todos para´sitos de Aves en Cuba. Parte IV. Poeyana, Serie A 88:1–15. Burt, D. R. R. 1980. On Davainea minuta (Cestoda). Parasitology 81:xlv. (Abstract.) Burt, D. R. R., and M. D. B. Burt. 1984. On Davainea minuta Cohn: 1901 (Cestoda: Cyclophyllidea) and its variation in North American Recurvirostridae (Aves). Journal of Natural History 18:15–23. Canavan, P. N. 1934. On a trematode Allopyge undulatus n. sp. parasitic in Lilford’s crane (Megalornis grus lilifordi). Parasitology 25:117–120. Dronen, N. O., C. K. Blend, and A. J. Davis. 2004. Emendation of the subfamilies Caiguiriinae and Pygidiopsinae (Digenea) with a redescription of Caiguiria anterouteria (Digenea: Heterophyidae) and reassignment of Pygydiopsis crassus to Caiguiria. Zootaxa 417:1–12. Fischthal, J. H., and P. Nasir. 1974. Some digenetic trematodes of birds and a mammal from Venezuela. Proceedings of the Helminthological Society of Washington 41:178–183. Fuhrmann, O. 1908. Nouveaux Teńias d’oiseaux. Revue Suisse de Zoologie 16:27–73. Harwood, P. D. 1939. Notes on Tennessee helminths. IV. North American trematodes of the subfamily Notocotylinae. Journal of the Tennessee Academy of Science 14:421–437. Hinojos, J. G., and A. G. Canaris. 1988. Metazoan parasites of Himantopus mexicanus Muller (Aves) from southwestern Texas, with a checklist of helminth parasites from North America. Journal of Parasitology 74:326–331. Johnston, S. J. 1913. On some Queensland trematodes, with anatomical observations and descriptions of new species and genera. Quarterly Journal of Microscopical Science 59:361–400. Kanev, I., V. Radev, and B. Fried. 2002. Family Cyclocoelidae Stossich, 1902. Pages 131–145 in D. I. Gibson, A. Jones, and R. A. Bray, eds. Key to the Trematodes. Vol. 1. CABI Publishing and The Natural History Museum, London, U.K. ¨ ber Monostomiden. Zoologische Kossack, W. F. K. 1911. U Jahrbu¨cher Abteilung fu¨r Systematik, Geographie und Biologie der Tiere. Jena 31:491–590.

27

Macko, J. K. 1994. Taxonomy and systematics of eumegacetidids (Trematoda: Eumegacetidae) from Slovakia and Cuba. Helminthologia 31:163–174. Martorelli, S. R. 1986. Estudio sistematico y biologico de un digeneo perteneciente a la familia Microphallidae Travassos, 1920. 2. Desarrollo del ciclo biologico de Microphallus szidati en dos ambientes de condiciones ecologicas diferentes. Revista Iberica de Parasitologia 46:379–385. Nasir, P., and M. T. Dıáz. 1971. Studies on freshwater larval trematodes. XXVII. Partial life cycle of Caiguiria anterouteria gen. n., sp. n., subfam. n. (Trematoda: Digenea). Proceedings of the Helminthological Society of Washington 38:21–23. Ostrowski de Nuń˜ez, M. 1995. Life history of Pygidiopsis crassus n. sp. (Trematoda, Digenea, Heterophyidae) in the neotropical region. Memoires of the Institute of Oswaldo Cruz 90:13–19. Pulich, W. M. 1988. The Birds of North Central Texas. Texas A&M University Press, College Station, Texas. 438 pp. Rietschel, G., and B. Werding. 1978. Trematodes of birds from northern Columbia. Zeitschrift fu¨r Parasitenkunde 57:57–82. Robinson, J. A., J. M. Reed, J. P. Skorupa, and L. W. Oring. 1999. Black-necked stilt: (Himantopus mexicanus). Pages 1–32 in A. Poole and F. Gill, eds. The Birds of North America, No. 449. The Birds of North America, Inc., Philadelphia, Pennsylvania. Schmidt, G. D. 1968. Chevreuxia americana sp. nov. (Nematoda: Acuariidae) from the avocet, Recurvirostra americana, in Colorado. Parasitology 58:831–834. Shakhtakhtinskiai, Z. 1951. New trematode Allopyge skrjabini nov. sp. from the ocular orbit of the gray crane. Trudy Gel’mintologicheskoi Labortorii Akademiya Nauk, SSSR 5:165–167. (In Russian.) Stossich, M. 1902. Il Monostomum mutabile Zeder e le sue forme affini. Zoologisches Zentralblatt 9:406–407. Travassos, L. P. 1928. Informaç~oes sobre alguns Heterophyidae dos animaes domesticos do Brasil. Anais da Faculdade de Medicina da Universidade de Sañ Paulo 3:1–4. Yorke, W., and P. A. Maplestone. 1969. The Nematode Parasites of Vertebrates. Hafner Publishing Company, New York. 536 pp.