original type series of each and these new specimens were used to redescribe C. microcephalus. MATERIALS AND METHODS
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1 Comp. Parasitol. 77(2), 2010, pp Redescription of Centrorhynchus microcephalus (Bravo-Hollis, 1947) Golvan, 1956 (Acanthocephala: Centrorhynchidae) from the Groove-Billed Ani (Crotophaga sulcirostris) in Veracruz, Mexico DENNIS J. RICHARDSON, 1,4 SCOTT MONKS, 2 MARTÍN GARCÍA-VARELA, 3 AND GRISELDA PULIDO-FLORES 2 1 BC-BIO, Quinnipiac University, 275 Mt. Carmel Avenue, Hamden, Connecticut 06518, U.S.A. ( Dennis.Richardson@quinnipiac.edu), 2 Universidad Autónoma del Estado de Hidalgo, Centro de Investigaciones Biológicas, Apdo. Postal 1-69, C.P , Pachuca, Hidalgo, México ( smonks@uaeh.edu.mx; gpulido@uaeh.edu.mx), and 3 Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Circuito exterior s/n, Ciudad Universitaria, Copilco, Coyoacán, A.P / México, Distrito Federal, C.P ( garciav@servidor.unam.mx) ABSTRACT: Centrorhynchus microcephalus (Bravo-Hollis, 1947) Golvan, 1956 (Acanthocephala: Centrorhynchidae) originally was described as Gordiorhynchus microcephalus Bravo-Hollis, 1947 on the basis of 8 worms collected from the small intestine of a single great-tailed grackle (Quiscalus mexicanus) from the state of Puebla, Mexico. Acquisition of 48 specimens collected from the groove-billed ani (Crotophaga sulcirostris) in Tlacotalpan, Veracruz, Mexico permitted a more complete description of the species. Nine of 10 (90%) birds examined were infected with 2 13 individuals of Centrorhynchus microcephalus with a mean intensity of 5.3. Examination of the type material of Centrorhynchus crotophagicola Schmidt and Neiland, 1966 revealed this species, described from groove-billed anis and squirrel cuckoos (Piaya cayana) from Nicaragua, to be conspecific with C. microcephalus; thus, C. crotophagicola is considered a junior synonym of C. microcephalus. Centrorhynchus microcephalus is redescribed on the basis of the type material of G. microcephalus and C. crotophagicola,and the newly acquired specimens from Veracruz. This study constitutes the first report of C. microcephalus since its original description. Additionally, a single immature female of Centrorhynchus kuntzi Schmidt and Neiland, 1966 was collected from one ani, representing a new host record and the first report of C. kuntzi from Mexico. KEY WORDS: Centrorhynchus microcephalus, Centrorhynchus crotophagicola, Centrorhynchus kuntzi, groove-billed ani, Crotophaga sulcirostris, Acanthocephala. Centrorhynchus microcephalus was described by Bravo-Hollis (1947) as Gordiorhynchus microcephalus on the basis of 5 female and 3 male worms taken from the small intestine of a single great-tailed grackle (Quiscalus mexicanus) in the district of Matamoros, Puebla State, Mexico. Later, Golvan (1956) transferred this species to Centrorhynchus. A Central American species, Centrorhynchus crotophagicola Schmidt and Neiland, 1966, subsequently was described from groove-billed anis (Crotophaga sulcirostris) and squirrel cuckoos (Piaya cayana) collected at El Recreo, Río Escondido, Nicaragua. Acanthocephalans from 9 groove-billed anis collected near Tlacotalpan, Veracruz State, Mexico on 17 and 18 March, 2006 were consistent with both of these 2 species, which led to the reexamination of the type material of each. As a result, Centrorhynchus crotophagicola is declared to be a junior synonym of C. microcephalus and, since the original description was based on so few worms from a single bird, the 4 Corresponding author. original type series of each and these new specimens were used to redescribe C. microcephalus. MATERIALS AND METHODS Specimens of C. microcephalus were collected from hunter-shot birds (Cr. sulcirostris) and treated as described by Richardson (2006) except that those specimens stained in Mayer s carmalum were hydrated by passing through a graded series of 50%, 35%, and 15% ethanol and then into water (4 hr in each solution). Specimens were overstained in Mayer s carmalum, rinsed in water, and then passed sequentially through a series of 15%, 35%, 50%, 70%, and 85% ethanol (4 hr in each). From 85% ethanol, specimens were destained and further treated as described by Richardson (2006). Microscopic observations and measurements were made as described by Richardson (2005, 2006). Drawings were made as described by Richardson and Barger (2006). Terminology for plane shapes follows Clopton (2004). Measurements are given as the range followed by the mean in parentheses; all values are in micrometers unless otherwise stated. The type series of G. microcephalus (5 C. microcephalus) was obtained from the Colección Nacional de Helmintos (CNHE), Instituto de Biología, Universidad Nacional Autónoma de México, Mexico City (II-11; holotype CNHE-557 [male], paratypes CNHE-621 [3 males: B, C, E; and 2 females: A, D]), and the U.S. National 164
2 RICHARDSON ET AL. REDESCRIPTION OF CENTRORHYNCHUS MICROCEPHALUS 165 Parasite Collection in Beltsville, Maryland, U.S.A. (USNPC 37052). The type series of C. crotophagicola was obtained from the U.S. National Parasite Collection, U.S. National Museum, Beltsville, Maryland, U.S.A. (USNM [holotype, male]; USNM [allotype female]; USNM and [paratypes]). RESULTS AND DISCUSSION Survey data Nine of 10 (90%) groove-billed anis were infected with 2 13 adult individuals of C. microcephalus. In all, 14 male and 34 female worms were collected (mean intensity 5 5.3). A single immature female of Centrorhynchus kuntzi Schmidt and Neiland, 1966 (CNHE-7075) was collected from 1 bird. This constitutes the first report of C. kuntzi from this host and the first report of this acanthocephalan from Mexico. Centrorhynchus microcephalus (Bravo-Hollis, 1947) Golvan, 1956 Syn. Gordiorhynchus microcephalus Bravo- Hollis, 1947; Centrorhynchus crotophagicola Schmidt and Neiland, 1966 Description based on 16 male and 16 female specimens (Figs. 1 9) General: Trunk roughly cylindrical, elongate, with slight constriction anteriorly; usually widest anterior to constriction. Neck (52) long and (384) wide. Proboscis cylindrical with constriction at insertion of receptacle; (696) long by (258) wide just anterior to insertion of receptacle, (244) at insertion of receptacle, (343) at base. Insertion of receptacle located 68 89% (76%) of distance posterior from apex of proboscis to base. Proboscis armed with (usually 30 33) longitudinal rows of (usually 16 or 17) hooks and spines. Anterior 7 10 (usually 8 or 9) hooks in each row (37) long (usually 33 39) with long simple roots. Rootless spines, 5 9 (usually 7 9), posterior to hooks. Apical hooks finely to narrowly semifalciform, semiluniform, or semicrescentic, (36) long (usually 31 42); remainder of anteriad hooks semifalciform, semiluniform, or semicrescentic to narrowly semifalciform, semiluniform, or semicrescentic, (39) long (usually 36 42). Spines very deeply to very depressed semifalciform, semiluniform, or semicrescentic, (29) long (usually 28 31). Basal-most spines almost always semifalciform to very depressed semifalciform. Proboscis receptacle double-walled, mm (1.3) long. Lemnisci about equal, mm (2.4) in length, extending mm (1.1) beyond posterior end of receptacle, posterior ends attached to body wall. Cerebral ganglion located mid-receptacle, just posterior to neck, narrowly elliptoid to elliptoid, (168) long by (66) wide. Male: Mature males mm (24) long by mm (1.2) wide at widest point. Length-to-width ratio (19.4):1. Proboscis (681) long by (249) wide just anterior to insertion of receptacle, (235) at insertion, (337) at base. Two testes, elliptoid, rarely broadly orbicular, approximately equal in size, 672 1,372 (1,019) long by (666) wide. Four elongate cement glands (Figs. 7, 8) begin immediately posterior to end of posterior testis, similar in length but with 1 or 2 glands slightly shorter than the others, mm (14.6) long. Saefftigen s pouch mm (3.7) long. Entire male system occupying (anterior end of anterior testis to genital pore) % (90.1%) of trunk length. Copulatory bursa large, globular when extended. Female: Gravid females mm (33) long by mm (1.6) wide at widest point. Length-towidth ratio (21.4):1, usually 18 23:1. Contraction of genital muscles produces a shallow genital vestibule and distinct terminal digitiform process. Proboscis (714) long by (269) wide just anterior to insertion of receptacle, (254) at insertion, (351) at base. Reproductive tract (anterior end of uterine bell to genital pore) occupying 5 10% of trunk length. Fully embryonated eggs narrowly elliptoid to elliptoid, (47) long by (20) wide when measured through body wall. Fertilization membrane elongate, leaving spaces at polar ends of acanthors (called polar prolongations by Nickol [1983] and Richardson and Nickol [1995]). Taxonomic summary Type host: Quiscalus mexicanus (syn. Cassidix mexicanus) (great-tailed grackle). Type locality: Distrito de Matamoros, Puebla State, México. Site of infection: Small intestine. Date of collection (type series): Sep Accession numbers: Type series of C. microcephalus (Bravo-Hollis, 1947) Golvan, 1956: holotype
3 166 COMPARATIVE PARASITOLOGY, 77(2), JULY 2010 Figures 1 6. Centrorhynchus microcephalus. 1. Adult male. 2. Gravid female, outline of body. 3. Copulatory bursa of male. 4. Posterior end of female. 5. Proboscis. 6. Egg drawn through body cavity. (male), CNHE-557, 5 paratypes (3 males B, C, E and 2 females A, D), CNHE-621; allotype (female specimen in vial, originally designated as cotype by Bravo-Hollis, 1947), USNPC Type series of C. crotophagicola Schmidt and Neiland, 1966: holotype (male), USNPC 60776; allotype (female), USNPC 60777; 3 paratypes (2 males and 1 female), USNPC and Additional hosts: Crotophaga sulcirostris (groovebilled ani) (this study), Schmidt and Neiland (1966); P. cayana (squirrel cuckoos) (Schmidt and Neiland,
4 RICHARDSON ET AL. REDESCRIPTION OF CENTRORHYNCHUS MICROCEPHALUS 167 Figures 7 9. Cement glands and ducts of Centrorhynchus microcephalus. 7. Anterior end of cement glands from a male paratype (CNHE ; specimen C ). 8. Anterior end of cement glands from a male from Tlacotalpan, Veracruz, Mexico (CNHE-7074; specimen bearing original number VER-06-29). 9. Cement gland ducts from a male from Tlacotalpan, Veracruz, Mexico (CNHE-7074; specimen bearing original number VER ). Letters indicate individual glands and ducts. 1966); cystacanths from stomach walls of the lizards, Anolis lineatopus lineatopus (Jamaican gray anole) and Anolis sagrei (brown anole) (Bundy et al., 1987). Additional localities: Tlacotalpan, Veracruz State, Mexico (18u N; 95u W) (this study); El Recreo, Río Escondido, Nicaragua (Schmidt and Neiland, 1966); Jamaica (Bundy et al., 1987). Date of collection (this study): Mar Specimens deposited: CNHE-7074; USNPC ; HWML (Harold W. Manter Laboratory, Nebraska State Museum, University of Nebraska-Lincoln, Lincoln, Nebraska, U.S.A.). Remarks Richardson and Nickol (1995), after examination of the type series of G. microcephalus, supported Golvan s (1956) placement of G. microcephalus in the genus Centrorhynchus. Reexamination of the type material of Bravo-Hollis (1947) (consisting of the holotype, allotype, and 5 paratypes) for this study revealed that in all specimens the proboscis is at least partially retracted and inverted, as she noted in the original description. Furthermore, the mounted specimens exhibit varying degrees of distortion, presumably resulting from osmotic stress during preparation, a condition that is not obvious in Lamina III of the original description (Bravo-Hollis, 1947). Because of the condition of the type series, some measurements from this material were not included in the current redescription; however, a summary of measurements from the type series along with those from material collected in this study is given in Table 1. Five of 15 specimens collected in Nicaragua (3 males and 2 females) were used by Schmidt and Neiland (1966) to describe C. crotophagicola from Cr. sulcirostris and P. cayana as a new species. Data provided by the larger collection of material in the current study clearly overlaps measurements and armature data given both by Bravo-Hollis (1947) and Schmidt and Neiland (1966) for C. microcephalus and C. crotophagicola, respectively, thus supporting the synonymy of the two species. Measurements from the type series of C. crotophagicola are given in Table 1. In addition to C. microcephalus, 5 species of Centrorhynchus have been described from North America; Centrorhynchus conspectus Van Cleave and Pratt, 1940; Centrorhynchus robustus Richardson and Nickol, 1995; C. kuntzi Schmidt and Neiland, 1966; Centrorhynchus spinosus (Kaiser, 1893) Van Cleave, 1924; and Centrorhynchus californicus Millzner, Among these species, C. microcephalus is most similar to C. kuntzi and C. spinosus in the number of hooks and spines per row and the number of anterior rooted hooks, which are 7 10, 7 9, and 8 11 for C. microcephalus, C. kuntzi, and C. spinosus, respectively. However, C. microcephalus differs markedly from these 2 species in the number of posterior rootless proboscis spines (C. microcephalus 5 9, C. kuntzi 14 18, and C. spinosus 13 17). In addition, as implied by the specific epithet, the proboscis of C. microcephalus is considerably shorter than that of any other North American species of Centrorhynchus. The length of the proboscis of C. microcephalus ranges from 599 to 810 long as opposed to 920 1,265 for C. conspectus, 950 1,345 for C. robustus, 816 1,709 for C. kuntzi, and 806
5 168 COMPARATIVE PARASITOLOGY, 77(2), JULY 2010 Table 1. Summary of morphometric data for the type series of Centrorhynchus microcephalus, from the original description of C. microcephalus (Bravo-Hollis, 1947), from the type series of Centrorhynchus crotophagicola, and from material collected in the present study from groove-bill anis in Vera Cruz, Mexico. Mean, when given, is in parentheses following range. All measurements are in micrometers unless otherwise stated. Character Our measurements from type series of C. microcephalus Measurements of Bravo-Hollis (1947) Our measurements from type series of C. crotophagicola Measurements of specimens collected in this study Trunk (mm) Length, male (20) (28) (24) Maximum width male (1.1) (1.4) (1.2) Length, female (37) (32) Maximum width female (1.1) (1.6) Length 4 maximum width Male (18.6) { (21.1) (19.2) Female 24.5 { (26.4) (20.2) Neck Length * { (57.3) (51) Width * { (400.7) (381) Proboscis Length * (662) (700) Width anteriorly * (233) (262) Width at receptacle insertion * { (225) (246) Width at base * { (351) (342) Location of proboscis receptacle (% posterior from apex to base) * Posterior 1/ (76) (76) Number of rows of hooks and spines * Number of hooks/row Number of larger rooted hooks 8 9 { Number of smaller rootless spines 7 8 { Length of apical hooks (31) { (38) (36) Length of larger rooted hooks (37) (38) (39) Length of roots of larger hooks * (37) (37) Length of smaller rootless spines (27) (30) (29) Proboscis receptacle length (mm) * (1.3) (1.3) Testis length , ,120 (1,057) 672 1,372 (1,010) Testis width (590) (683) Cement gland length (mm) (14.9) (14.6) Seafftigen s pouch length (mm) (3.8) (3.6) % trunk occupied by male system (91.7) { (90.3) % trunk occupied by female system * { Egg length (43) (50) (47) Egg width (21) (19) (20) * Specimens inadequate to obtain reliable measurement. { not given. 1,104 for C. spinosus. Specimens of C. californicus apparently have been lost and could not be located for examination. The most striking difference setting C. microcephalus apart from other North American species of Centrorhynchus is definitive host utilization. On the basis of the lack of subsequent finding of this acanthocephalan in the type host, the primary definitive host of C. microcephalus appears to be Cr. sulcirostris (Order Cuculiformes), although gravid female worms also have been reported from an adult grackle (Order Passeriformes). Other North American species of Centrorhynchus occur as adults in raptors of the orders Falconiformes, hawks and exceptionally eagles, and Strigiformes, owls. In Brazil, Centrorhynchus tumidulus (Rudolphi, 1819) Travassos, 1923 has been reported from the smooth-billed ani (Crotophaga ani) and the greater ani (Crotophaga major) (Westrumb, 1821). Centrorhynchus microcephalus, with rows of hooks and spines comprised of 7 10 hooks and 5 9 spines, differs from C. tumidulus, which has 26 rows
6 RICHARDSON ET AL. REDESCRIPTION OF CENTRORHYNCHUS MICROCEPHALUS 169 of hooks and spines comprised of 13 hooks and 7 8 spines (Meyer, 1933). Cystacanths of C. crotophagicola also have been reported from the stomach walls of lizards, A. lineatopus lineatopus and A. sagrei from Jamaica. Those specimens originally had been reported as C. spinosus by Bundy et al. (1987), but Dimitrova and Gibson (2005) determined them to be C. crotophagicola and provided a description of the cystacanths. Since C. crotophagicola is now considered to be a junior synonym of C. microcephalus, these cystacanths should be assigned to that species on the basis of Dimitrova and Gibson (2005). However, additional information from cystacanths from either the type locality or the new locality reported herein would be beneficial. Bravo-Hollis (1947) initially assigned her specimens to Gordiorhynchus primarily on the basis of the presence of pronounced internal pseudosegmentation and the presence of a clitoris on female worms. Gordiorhynchus, erected by Meyer (1931), was characterized as having pronounced internal pseudosegmentation and the presence of one appendage (protuberance, or clitoris, sensu Bravo-Hollis, 1947) alongside the genital aperture, features separating this genus from Centrorhynchus. Witenberg (1932) determined that Gordiorhynchus was a synonym of Centrorhynchus, a view not generally shared by other systematists until Ward (1951, 1959) endorsed this decision, and pointed out that pseudosegmentation occurs across several genera of Acanthocephala. This synonymy was supported by Golvan (1956), who formally transferred the species of the former genus to Centrorhynchus. As mentioned by Bravo-Hollis (1947), the pronounced pseudosegmentation in C. microcephalus examined for this study is internal and appears to be a manifestation of the lacunar system. In the specimens that we examined pseudosegmentation is more pronounced in females than in males and the cavities (pseudosegments) appear to be open to the body cavity because eggs can be seen resting inside. However, this feature should be studied further using histological techniques. The number of cement glands in members of Centrorhynchus has never been established at the generic level. The diagnosis of Yamaguti (1963) listed the number of cement glands as 3 6 but the author commented that they were not well defined from their ducts. (Yamaguti, 1963; pg. 118). The diagnosis of Petrochenko (1958; pg. 197) specified 3 cement glands but mentioned that there were 4 in one East Asiatic species. However, in his descriptions of the species assigned to the genus he mentioned several species (C. conspectus, N. Am.; Centrorhynchus corvi Fukui, 1929, Japan, now assigned to Sphaerirostris pinguis [Van Cleave, 1918] Golvan, 1956; Centrorhynchus itatsinis Fukui, 1929, Japan, USSR [sic.]; Crotorhynchus magnus Fukui, 1929, Japan, USSR; and C. polymorphus Travassos, 1926, Brazil, possibly a member of Sphaerirostris [Dimitrova and Gibson, 2005]) that possessed 4 cement glands, although in the majority of descriptions the number of glands was not mentioned. Many of the species described from hosts from the Indian region have been described as having 2 3 cement glands (Datta, 1933; Rengaraju and Das, 1980; Gupta and Fatma, 1981; Nama and Rathore, 1982; Duggal et al., 1986) or as having 4 cement glands (see Soota and Kansal, 1972; Rengaraju and Das, 1975; Duggal et al., 1986). North American species have been described as having 4 cement glands (see Van Cleave and Pratt, 1940; Nickol, 1983; Richardson and Nickol, 1995). Part of the problem is, as Johnston and Edmonds (1948; p. 69) stated so succinctly in their description of Centrorhynchus horridus (von Linstow, 1897) Meyer, 1932, that the cement glands are pressed together, which makes counting them difficult. In the original description, Bravo-Hollis (1947; Lámina 1 p. 500, p. 503) referred to the cement glands as if they were a single rather than composite structure, but depicted multiple glands in the figure. Schmidt and Neiland (1966) described C. crotophagicola as having 3 cement glands and in their remarks mentioned that in their examination of the paratypes of C. microcephalus they had determined that there were 3 cement glands in males of that species. As stated above, counting the number of cement glands in whole mounts of males is difficult at best and it is impossible for many specimens, probably accounting for the fact that numerous authors have not provided the number of cement glands in descriptions of new species. Examination of the type material of both of these 2 species revealed that it was not possible to determine the number of cement glands in most of the specimens because the membranes separating the individual glands were not visible even with Nomarski differential interference contrast lighting. However, in each case that it was possible to count the glands, 4 glands were encountered and even when the number of glands could not be determined it was possible to count 4 ducts leading from the glandular tissue. In 1 paratype of C. microcephalus (CNHE ; specimen C ) it was possible to count 4
7 170 COMPARATIVE PARASITOLOGY, 77(2), JULY 2010 glands (Fig. 7) and in new material from Veracruz 4 glands (Fig. 8) and 4 ducts leading from the glandular tissue (Fig. 9) could be counted using differential interference contrast lighting. Even after determining the number of cement glands in a specimen using this lighting technique it often was impossible to recount the glands using normal Koehler illumination. In all specimens that were examined the glands and the ducts appeared to be flattened rather than cylindrical, but this must be verified in sectioned material. On the basis of our study of the type material of C. microcephalus and C. crotophagicola, we revise the description of C. microcephalus to include the presence of 4 cement glands. Finding that C. microcephalus has 4 cement glands, as do other North American species (see references cited above), suggests the possibility that this feature might be useful in a phylogenetic context. Whether there are 3 6 cement glands in Centrorhynchus or a fixed number of glands at a subgeneric level for particular clades of species, the question is interesting. However, until the number of cement glands can be established with certainty for each of the known species, it is not possible to have full confidence in counts reported for particular species. Whenever possible, observations from whole mounts should be validated using sectioned material. ACKNOWLEDGMENTS This work was supported financially by a summer research grant (2006) to D.J.R. from the School of Health Sciences, Quinnipiac University. Funds from the Programa de Mejoramiento del Profesorado (PRO- MEP) provided the opportunity for D.J.R. to visit S.M. and G.P.-F., Universidad Autónoma del Estado de Hidalgo, during the production of this manuscript. Tamara J. Cook served as the acting editor for this manuscript, arranging reviews and exercising full editorial discretion in addition to her continued service as Managing Editor of Comparative Parasitology, thereby allowing D.J.R. to contribute to the Helminthological Society of Washington through continued publication in Comparative Parasitology. LITERATURE CITED Bravo-Hollis, M Gordiorhynchus microcephalus n. sp., acantocephalo parasito de un pajaro (Cassidix mexicanus mexicanus Gmelin). Anales del Instituto de Biología de la Universidad Nacional Autónoma de México 18: Bundy, D. A. P., P. Vogel, and E. A. Harris Helminth parasites of Jamaican anoles (Reptilia: Iguanidae): a comparison of the helminth fauna of 6 Anolis species. Journal of Helminthology 61: Clopton, R. E Standard nomenclatural and metrics of plane shapes for use in gregarine taxonomy. Comparative Parasitology 71: Datta, M. N Acanthocephala from Nothern India. II. A new species of Centrorhychus (C. maryasis, sp. nov.) from a Himalayan bird, Urocissa melonacephala occipitalis (Blyth). Records of the Indian Museum 25: Dimitrova, Z. M., and D. I. Gibson Some species of Centrorhynchus Lühe, 1911 (Acanthocephala: Centrorhynchidae) from the collection of the Natural History Museum, London. Systematic Parasitology 62: Duggal, C. L., S. Solomon, and S. Ambardar On some acanthocephalans parasitizing birds of Punjab. Research Bulletin of the Panjab University (Science) 37: Golvan, Y. J Le genre Centrorhynchus Lühe, 1911 (Acanthocephala-Polymorphidae). Revision des espèces européennes et description d une nouvelle espèce africaine parasite de Rapace diurne. Bulletin de l Institut Français d Afrique Noire, Séries A 18: Gupta, V., and S. Fatma On five new species of the genus Centrorhynchus Lühe, 1911 (Acanthocephala: Centrorhynchidae Van Cleave, 1916) from avian and amphibian hosts of Lucknow, Uttar Pradesh. Indian Journal of Helminthology 33: Johnston, T. H., and S. J. Edmonds Australian Acanthocephala, No. 7. Transactions of the Royal Society of South Australia 72: Meyer, A Gordiorhynchus, ein neues Acanthocephalen-genus mit innerer ovarialer Pseudosementierung. Zooloische Jahrbücher. Abteilung für Systematik, Ökologie und Georaphie der Tiere 60: Meyer, A Acanthocephala. Pages in Dr. H. G. Bronns, Klassen und Ordnungen des Tier-Reichs, Leipzig. Bd 4, 2 Abt., 2 Buch, 1 Lief. Nama, H. S., and G. S. Rathore The acanthocephalan genus Centrorhynchus occurring in Indian birds with description of two species from Rajasthan. Indian Journal of Helminthology 34: Nickol, B. B Centrorhynchus kuntzi from the USA with description of the male and redescription of C. spinosus (Acanthocephala: Centrorhynchidae). Journal of Parasitology 69: Petrochenko, V. I Acanthocephala of domestic and wild animals. Vol. II. Translated from Russian by the Israel Program for Scientific Translation, Jerusalem, Israel, p. Rengaraju, V., and E. N. Das On some new species of avian Acanthocephala from India. Indian Journal of Helminthology 27: Rengaraju, V., and E. N. Das A new species of the genus Centrorhynchus Lühe, 1911 (Acanthocephala) from India. Records of the Zoological Survey of India 76: Richardson, D. J Identification of cystacanths and adults of Oligacanthorhynchus tortuosa, Macracanthorhynchus ingens, and Macaracanthorhynchus hirudinaceus based on proboscis and hook morphomet-
8 RICHARDSON ET AL. REDESCRIPTION OF CENTRORHYNCHUS MICROCEPHALUS 171 rics. Journal of the Arkansas Academy of Science 59: Richardson, D. J Life cycle of Oligacanthorhynchus tortuosa (Oligacanthorhynchidae), an acanthocephalan of the Virginia opossum (Didelphis virginiana). Comparative Parasitology 73:1 6. Richardson, D. J., and M. A. Barger Redescription of Oligacanthorhynchus major (Machado-Filho, 1963) Schmidt, 1972 (Acanthocephala: Oligacanthorhynchidae) from the white-lipped peccary (Tayassu pecari) in Bolivia. Comparative Parasitology 73: Richardson, D. J., and B. B. Nickol The genus Centrorhynchus (Acanthocephala) in North America with description of Centrorhynchus robustus n. sp., redescription of Centrorhynchus conspectus, and a key to species. Journal of Parasitology 81: Schmidt, G. D., and K. A. Neiland Helminth fauna of Nicaragua. III. Some Acanthocephala of birds, including three new species of Centrorhynchus. Journal of Parasitology 52: Soota, T. D., and K. C. Kansal The helminth fauna of Andaman and Nicobar. Acanthocephala. Records of the Zoological Survey of India 66: Van Cleave, H. J., and E. M. Pratt A new species of the genus Centrorhynchus (Acanthocephala) from the barred owl. Journal of Parasitology 26: Ward, H. L The species of Acanthocephala described since Part I. Journal of the Tennessee Academy of Science 26: Ward, H. L The status of the acanthocephalan genus Centrorhynchus. Journal of Parasitology 45:149. Westrumb, A. H. L De Helminthibus acanthocephalis. Commentatio historicoanatomic adnexo recensu animalium, in Museo Vindobonensis circa helminthes dissectorum et singularum speciarum harum in illis repertarum. Hanoverae Helwig Witenberg, G Akanthocephalen studien. II. Uber das system der Akanthocephalan. Bollettino di Zoologia, Publicato dall Unione Zoologica Italiana 3: Yamaguti, S Systema Helminthum: Acanthocephala. Wiley Interscience Publications, New York. 423 pp.
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