J. Parasitol., 101(1), 2015, pp. 000–000
Ó American Society of Parasitologists 2015
A NEW ACANTHOCEPHALAN SPECIES (ARCHIACANTHOCEPHALA:
OLIGACANTHORHYNCHIDAE) FROM CERDOCYON THOUS, A CRAB-EATING FOX IN THE
BRAZILIAN PANTANAL WETLANDS
Ana Paula N. Gomes*†, Natalie Olifiers*, Joyce G. R. Souza‡, Helene S. Barbosa§, Paulo S. D’Andrea*, and Arnaldo
Maldonado Jr.*
* Laboratório de Biologia e Parasitologia de Mamı́feros Silvestre Reservatório, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Avenida Brasil, 4365
Manguinhos, Rio de Janeiro, RJ, CEP 21045-900, Brazil. † Curso de Pós-Graduação em Biodiversidade e Saúde, Instituto Oswaldo Cruz, Fundação Oswaldo
Cruz, Avenida Brasil, 4365 Manguinhos, Rio de Janeiro, RJ, CEP 21045-900, Brazil. ‡ Laboratório de Helmintologia Romero Lascasas Porto, Departamento
de Microbiologia, Imunologia e Parasitologia, Universidade do Estado do Rio de Janeiro, Avenida Professor Manoel de Abreu, 444/58 andar, Vila Isabel, Rio
de Janeiro, RJ, CEP 20511-070, Brazil. § Laboratório de Biologia Estrutural, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz, Avenida Brasil, 4365
Manguinhos, Rio de Janeiro, RJ, CEP 21045-900, Brazil. Correspondence should be sent to: [email protected]
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ABSTRACT: A new species of Oligacanthorhynchidae (Acanthocephala) Prosthenorchis cerdocyonis n. sp. is described from 17
specimens collected from the small intestine of the crab-eating fox Cerdocyon thous Linnaeus, 1766 (Canidae: Carnivora) found in the
Brazilian Pantanal wetlands. Specimens were studied using light and scanning electron microscopy. Characteristic features
distinguishing the new species from others already described are presented, such as size of the body, the position of lemnisci, size of the
eggs, host, and geographical distribution. Details of the body surface obtained by scanning electron microscopy, such as the presence
of 2 lateral papillae in the proximal region of the proboscis, the presence of barbs in hooks, and a robust and festooned collar, helped
to identify the species. Until now, specimens belonging to Prosthenorchis reported from Cerdocyon thous were not identified to species.
Furthermore, the new species is the first to be recorded in C. thous found in the Pantanal wetlands.
region of the Pantanal in Brazil. The animals were necropsied, and
acanthocephalans were collected from the small intestine of each fox for
taxonomic study. The study area is characterized by sandy soil with
mosaic vegetation of semi-deciduous forest with open grassy areas
(Rodela, 2006). Animal procedures were approved by the Brazilian
Federal Environmental Agency (IBAMA, first license #183/2005,
CGFAU/LIC; last license #11772-2).
Acanthocephalans were collected, washed in physiological saline
(0.95% NaCl), and stored in 70% alcohol. At the laboratory, only adult
specimens of both sexes were cleared in 90% phenol to study the hooks of
the proboscides. To describe the internal structures, the specimens were
stained with acid carmine, destained in acid (HCl) alcohol, dehydrated in a
graded alcohol series, cleared in methyl salicylate, and whole-mounted in
Canada balsam (modified from Amato, 1985). Identification of the genus
followed the key of Schmidt (1972). The description of Prosthenorchis sp.
was based on 17 specimens (7 males and 10 females). Measurements are in
millimeters unless otherwise stated. The range is followed by the mean in
parentheses. Specimens of Prosthenorchis sp. (CHIOC 17840 a–f, 10123;
Lima, 2009) and Prosthenorchis elegans (CHIOC 417, 418, 419, 421, 441,
442, 998, 7661, 8864, 10122, 16147; Machado Filho, 1950) deposited in the
Helminth Collection of the Oswaldo Cruz Institute (CHIOC) were used
for comparison.
Ultrastructural surface morphology was described for adult female and
male specimens using scanning electron microscopy (SEM). Specimens
were fixed for 1 hr at room temperature with 2.5% glutaraldehyde in 0.1
M Na-cacodylate buffer. After being washed in the same buffer, specimens
were post-fixed for 3 hr at room temperature in 1% osmium tetroxide in
0.1 M Na-cacodylate buffer. The material was then dehydrated in an
ascending acetone series, dried by the critical point method with CO2,
mounted with silver cellotape on aluminum stubs, and sputter-coated with
a 20-nm-thick layer of gold. Samples were examined using a Jeol JSM6390 LV microscope at an accelerating voltage of 15 kV at the Electron
Microscopy Platform of the Oswaldo Cruz Institute.
The family Oligacanthorhynchidae Southwell and Macfie, 1925,
includes 12 genera (Amin, 1985, 2013) and includes Prosthenorchis
Travassos, 1915. Species of Prosthenorchis have been reported as
follows: in South America as Prosthenorchis elegans (Diesing, 1851)
Travassos (1915) from primates; in Africa as Prosthenorchis lemuri
Machado (1950) from lemurs in Madagascar, Prosthenorchis
pardalis Southwell and Macfie (1925) from Felis pardus in Sierra
Leone, and Prosthenorchis fraterna (Baer, 1959) Schmidt, 1972,
from felid Panthera pardus in Congo; and in Asia as Prosthenorchis
sinicus Hu-Jiand, 1990, from a dog in China (Schmidt, 1972; Amin
et al., 2008; Amin, 2013).
The crab-eating fox, Cerdocyon thous, is a wild canid that
inhabits savannas and woodlands in South America (Silveira,
1999; Courtenay and Maffei, 2004). Cerdocyon thous (Linnaeus,
1766) has been the subject of a research program conducted by
Embrapa/Pantanal and the Institute Oswaldo Cruz Foundation
(FIOCRUZ-RJ) that studies the ecology and health of wild
carnivores in the Brazilian Pantanal wetlands. This research
program also includes the study of helminth parasites, and
specimens of helminths were made available to parasitologists at
Fiocruz by Embrapa/Pantanal researchers. Although specimens
of acanthocephalans have been reported from C. thous in Brazil
(Griese, 2007; Ruas et al., 2008; Vieira et al., 2008; Lima, 2009),
species of the genus Prosthenorchis had not been previously
identified.
In this report, we describe a new species of the genus
Prosthenorchis collected from the wall of the small intestine of
crab-eating foxes (C. thous) from the Pantanal wetlands, Mato
Grosso do Sul State, Brazil.
DESCRIPTION
Prosthenorchis cerdocyonis n. sp.
(Figs. 1–15)
MATERIALS AND METHODS
Two adult crab-eating female foxes (C. thous) were found dead in 2007
on Nhumirim Ranch (18859 0 S, 56839 0 W), located in the Nhecolândia sub-
General: Proboscis globular, armed with 36 hooks (12 rows of 3 hooks);
showing 3 different morphologies varying from robust hooks at top to
short hooks at bottom. Hooks are similar in size in both sexes. First type
of apical hook posteriorly curved, presenting complex manubria and root
immersed in matrix of proboscis, expanded laterally in T-shape, with top
of hook bearing chisel-shaped barbs. Second and third types of hooks in
Received 12 June 2014; revised 27 August 2014; accepted 26 September
2014.
DOI: 10.1645/13-321.1
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FIGURES 1–6. (1) Anterior part of Prosthenorchis cerdocyonis n. sp. presents a globular proboscis armed with hooks, 1 papilla in each side at the base
of proboscis, and neck surrounded by a festooned collar. (2) Three different hooks, the first one has strong roots with T-shape. (3) Posterior end of
female body. Va, vagina; Be, salient bell; Ut, uterine bell. (4) Male body with anterior and posterior testis, with 8 aggregated cement glands. (5) Eight
aggregated cement glands. (6) Lemnisci long, bent, and reaching the posterior of the body.
FIGURE 7. Egg ellipsoid shape and with 3 membranes, Outer
membrane (Om) is thick and granular, inner membrane (Im) is thin and
transparent, embryo (Em) is surrounded by a thin membrane, 2 poles (Po)
in each side.
proximal rows have small, discoid roots. The lengths of the anterior
hooks, measured from tip to posterior end, were 0.41–0.22 (0.32), 0.27–
0.08 (0.15), the lengths of the hook roots measured 0.28–0.11 (0.18), 0.06–
0.03 (0.05), and the posterior hooks measured 0.11–0.05 (0.08) with simple
roots.
One papillae on each side at base of proboscis, presenting elevated
border with smooth surface and medial pore; neck surrounded by robust,
irregular, festooned collar; cylindrical body curved ventrally, thick and
furrowed, not transparent, showing marked wrinkles transversely; long
lemnisci, sometimes bent on themselves, usually reaching the posterior
region of the body.
Male holotype and 6 paratypes: Body 9.60–6.8 (8.53) long, 1.97–1.26
(1.58) wide. Globular proboscides 1.1–0.56 (0.9) long, 0.98–0.72 (0.86) wide,
bearing 36 hooks (12 spiral rows of 3 hooks). Collar 1.26–0.68 (0.84) long,
0.98–0.82 (0.88) wide, neck short, with longitudinal pleats. Two testicle
ellipsoids, located in anterior region. Anterior testis 1.0–0.87 (0.94) long,
0.49–0.29 (0.39) wide; posterior testis 0.9–0.65 (0.78) long, 0.45–0.41 (0.44)
wide (n ¼ 2). Behind testicles, 8 ellipsoid, aggregated cement glands. Group
of cement glands 1.23–0.96 (1.09) (n ¼ 2) long. Ejaculatory duct 1.21–0.88
(1.05) (n ¼ 2). Bursa located at end of body, 0.96 long (n ¼ 1). Long lemnisci
extend to posterior testis and reach the end of the body. Posterior region
with reproductive vestibule closed by retracted copulatory bursa.
Female allotype and 9 paratypes: Body 12.18–5.34 (7.67) long, 2.08–1.4
(1.71) wide. Globular proboscides 1.0–0.68 (0.87) long, 1.04–0.78 (0.95)
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FIGURES 8–15. External morphology of Prosthenorchis cerdocyonis n. sp. via scanning electron microscopy (SEM). (8) Lateral view of female body.
Pr, proboscis; Co, collar. (9–11) Proboscis armed with hooks and hooks with barbs on the tip, neck with 2 papillae in each side. Ho, hooks, Pa, papilla.
(12) Detail of papilla with elevated border and smooth surface and a medial pore. (13) Posterior region of female body, ventral view. (14) Posterior
region of male body and bursa retracted. (15) Bursa outside the body. Fe, female; Pa, papillae; Ho, hook; Ma, male; B, bursa.
wide, bearing 36 hooks (12 spiral rows of 3 hooks). Collar 1.16–0.34 (0.74)
long, 1.18–0.72 (0.97) wide. In most specimens, lemnisci covered by eggs.
Uterine bell 1.11–0.75 (0.90) long (n ¼ 3; Fig. 3). The eggs (n ¼ 22)
ellipsoidal, 0.1–0.074 (0.09) long, 0.07–0.03 (0.05) wide, with 3 membranes. Outer membrane thick, granular, with hyaline poles; inner
membrane thin, membrane covering embryo thin and transparent.
Posterior end of body possessing smooth vulvar vestibule with prominent
edges.
Taxonomic summary
Type host: Cerdocyon thous Linnaeus, 1766 (Crab-eating fox).
Type locality: Nhumirim Ranch (18859 0 S, 56839 0 W), Mato Grosso do
Sul State, Brazil.
Type material: Holotype: 1 male (CHIOC: 35804a); allotype: 1 female
(CHIOC: 35804b); paratype 5 females and 6 males (CHIOC: 35804c)
deposited in the Helminth Collection of the Oswaldo Cruz Institute
(Coleção Helmintológica do Instituto Oswaldo Cruz-CHIOC), Rio de
Janeiro, Brazil.
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FIGURES 8–15. Continued.
Etymology: The new species is named after the genus of the host.
Remarks
The genus Prosthenorchis was created by Travassos (1915) for
the type-species Prosthenorchis elegans (Diesing, 1851) (syn.
Echinorhynchus elegans) from Callithrix chrysoleuca Wagner,
1842 (Schmidt, 1972). Stunkard (1965) included the genus
Prosthenorchis in a new subfamily, Prosthenorchinae Travassos,
1917, together with 2 other species: Prosthenorchis luhei Travassos, 1917, a parasite from the carnivore Nasua nasua, and
Prosthenorchis avicola Travassos, 1917, a parasite from the bird
Nettion brasiliense.
In 1950, Machado Filho revised the species described by
Travassos and included 13 new species parasitizing primates,
carnivores, birds, and lizards from different geographic regions of
the world. Yamaguti (1963) revised the classification of the
Oligacanthorhynchidae, establishing the main characteristics of
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TABLE I. Morphometric comparison of 5 species of Prosthenorchis (measurements in millimeters).
Characteristics
Trunk
Length
Width
P. elegans
(Diesing, 1851)
Travassos, 1915
P. elegans
Machado, 1950
P. fraternal
(Baer, 1959)
Schmidt, 1972
P. lemuri
Machado, 1950
P. cerdocyonis
(present study)
15.0–20.0*
2.0–4.0*
25.0–50.0*
1.50–4.0*
45.0*
3.0*
12–15*
1.60*
7.67–8.53
1.58–1.71
0.50*
0.60*
0.89*
0.91*
–
–
–
0.58*
0.87–0.90
0.86–0.95
0.224*
0.167*
0.120*
0.64*
0.56*
0.46*
–
–
–
0.24*
0.10*
0.60*
0.32
0.15
0.08
0.150*
0.116*
–
0.13*
–
–
–
–
–
–
–
–
0.18
0.05
–
Lemnisci end over body end
Anterior region
Anterior region
Middle region
Eggs
Length
Width
0.78*
0.42–0.46*
0.63–0.77*
0.42*
0.60*
0.42*
Proboscide
Length
Width
Hook length
Type I
Type II
Type III
Hook root
Type I
Type II
Type III
Natural definitive vertebrate host Saimiri sciurea
Geographic distribution
Mystax ursulus/
Lemur fulvus
Challithrix chrysoleu
Brazil/Panamá
Brazil/Panamá
(South America/
(South America/
Central America)
Central America)
Reach posterior region
0.45–0.47*
0.26–0.28*
0.87
0.49
Panthera pardus
Cerdocyon thous
Madagascar (Africa) Ituri, Congo (Africa) Brazil (South America)
* Measured by the authors of the present paper based on manuscript description.
Media AþP media of measurements of anterior and posterior testis together.
the genus Prosthenorchis and considering their geographical
distribution.
Schmidt (1972) revised the class Archiacanthocephala, focusing
on Oligacanthorhynchidae and emphasizing the importance of
reviewing the family due to the vague description and incorrect
interpretation of the morphology of the species. Recently, Golvan
(1994) revised the nomenclature of the phylum Acanthocephala
and considered geographical distribution as a taxonomic criterion.
Amin et al. (2008), following Schmidt (1972), considered the
genus Prosthenorchis as having 3 species based on morphological
characteristics such as a festooned collar, ornamented proboscides, 3 different types of hooks, and tips of hooks with barbs.
The 3 representative species are Prosthenorchis elegans (Diesing,
1851) Travassos, 1915, Prosthenorchis lemuri Machado, 1950,
and Prosthenorchis fraterna (Baer, 1959) Schmidt, 1972; other
species previously belonging to the genus Prosthenorchis, which
had no collar, have been relocated to other genera from the
Oligacanthorhynchidae family (Schmidt, 1972; Golvan, 1994;
Amin et al., 2008). Recently, Amin (2013) considered 2 other
species as belonging in the genus: Prosthenorchis pardalis
(Southwell and Macfie, 1925) and Prosthenorchis sinicus HuJiand, 1990.
In addition, Amin et al. (2008) described a new genus,
Paraprosthenorchis, in the Oligacanthorhynchidae family. The
genera Paraprosthenorchis and Prosthenorchis are closely related
because these genera are the only ones that have festooned collars
in the family. Otherwise, the genus Paraprosthenorchis has ornate
proboscides, does not have 12 rows of 3 hooks, has hooks without
barbs, does not have complex and large hook roots, has collars
with about 35 festoons, and does not have subterminal gonopores
(Amin et al., 2008).
Characteristics found in the new species described in the present
report, including the number of hooks, number of festoons, and
size of the body, were not observed in the genus Paraprosthenorchis, which justifies the inclusion of the new species described
here in the genus Prosthenorchis.
The main characteristics that distinguish Prosthenorchis cerdocyonis n. sp. from P. elegans, P. fraterna, and P. lemuri are size of
the body, position of the lemnisci, number of festoons, size of the
egg, and host and geographical distribution (Table I). However,
the lemnisci of P. cerdocyonis n. sp. and P. fraterna also reach the
posterior end.
Nevertheless, Prosthenorchis cerdocyonis n. sp. is distinguished
from P. elegans and P. lemuri by it is small trunk and long
lemnisci reaching the posterior end and from P. fraterna and P.
lemuri by the size of the egg, which is larger than that of other
species (Table I), and geographic distribution, since those species
occur in Africa.
Recently, Amin (2013) included 2 new species: Prosthenorchis
pardalis and Prosthenorchis sinicus in the genus Prosthenorchis,
but their descriptions need more morphological details. Further-
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THE JOURNAL OF PARASITOLOGY, VOL. 101, NO. 1, FEBRUARY 2015
more, P. pardalis is considered as nomen nudum (Amin, 2013),
and P. sinicus does not show the robust collar, which is the main
characteristic of the genus as shown in the original description.
Consequently, P. pardalis and P. sinicus may not belong in
Prosthenorchis, and we suggest that these species require further
study.
Specimens of Prosthenorchis sp. (Lima, 2009) and P. elegans
(Machado Filho, 1950), from the Helminth Collection of the
Oswaldo Cruz Institute were not in good condition, and we could
only measure the size of the body in P. elegans.
In addition, the features of Prosthenorchis cerdocyonis n. sp.
were observed in greater detail via scanning electron microscopy,
and the morphologic characteristics such as barbs on hooks,
papillae, and collar were described. However, these characteristics
have not previously been described by SEM in great detail for any
other species of the Prosthenorchis genus, making comparisons of
these features difficult.
In the Pantanal biome, where the samples were collected from
the crab-eating fox in the present study, a significant portion of
the crab-eating fox diet is composed of arthropods (87%),
especially Coleoptera (57%) (Bianchi et al., 2014). This aspect
suggests that these arthropods may be the intermediate host of
Prosthenorchis cerdocyonis.
ACKNOWLEDGMENTS
We thank Rodrigo Mexas from the Image Production and Treatment
Service of Oswaldo Cruz Institute (FIOCRUZ) for helping with image
processing and final production; the curator of the Helminthology
Collection of FIOCRUZ, Dr. Marcelo Knoff, for making available the
specimens from the collection; and the staff of Embrapa Pantanal for
helping in the field and making the specimens of acanthocephalans
available. This study received financial support from FUNDECT,
EMBRAPA-MACRO, PAPES IV/IOC-FIOCRUZ, and CAPES. Arnaldo Maldonado Júnior has a fellowship from the National Council for
Scientific and Technological Development (CNPq). We thank the
anonymous reviewers, whose comments and suggestions helped improve
an earlier version of the manuscript.
NOTE FROM THE EDITOR
This paper is being published in fairness to the authors since it was in
the process of being accepted during the transition. However, readers are
reminded that the journal no longer publishes stand-alone single species
descriptions unless they are in the context of broader taxonomic,
phylogenetic, or biogeographical issues that significantly advance our
understanding of these aspects.
LITERATURE CITED
AMATO, J. F. R. 1985. Manual de Técnicas para a Preparação de Coleções
Zoológicas. 8. Platelmintos (temnocefálidos, trematódeos, cestóides,
cestodários) e acantocéfalos. Sociedade Brasileira de Zoologia, São
Paulo, Brazil, 11 p.
AMIN, O. M. 1985. Classification. In Biology of the Acanthocephala, D.
W. T. Crompton and B. B. Nickol (eds.). Cambridge University
Press, London, U.K., p. 27–72.
———. 2013. Classification of the Acanthocephala. Folia Parasitologica
60: 273–305.
———, N. V. HA, AND R. A. HECKMANN. 2008. New and already known
acanthocephalans mostly from mammals in Vietnam, with descriptions of two new genera and species in Archiacanthocephala. Journal
of Parasitology 94: 194–201.
BIANCHI, R. C., R. C. CAMPOS, N. L. XAVIER FILHO, N. OLIFIERS, M. E.
GOMPPER, AND G. M. MOURÃO. 2014. Intraspecific, interspecific, and
seasonal differences in the diet of three mid-sized carnivores in a large
neotropical wetland. Acta Theriologica 59: 13–23.
COURTENAY, O., AND L. MAFFEI. 2004: Crab-eating fox Cerdocyon thous
(Linnaeus, 1766). In Canids: Foxes, wolves, jackals and dogs. Status
survey and conservation action plan, C. Sillero-Zubiri, M. Hoffmann,
and D. W. Macdonald (eds.). IUCN/SSC, Cambridge, U.K., p. 32–
38.
GOLVAN, Y. J. 1994. Nomenclature of the Acanthocephala. Research and
Reviews in Parasitology 54: 134–205.
GRIESE, J. 2007. Helmintofauna de vertebrados atropelados em rodovias
da região de Botucatu, São Paulo. M.S. Thesis. Programa Pós
Graduação em Biologia Geral e Aplicada do Instituto de Biociências,
Campus de Botucatu, Universidade Estadual de São Paulo–UNESP,
São Paulo, Brazil, 75 p.
HU-JIAND, D. 1990. Une nouvelle espèce de Prosthenorchis (Oligacanthorhynchida: Oligacanthorhynchidae). Acta Veterinaria et Zootecnica
Sinica 21: 65–66.
LIMA, A. C. R. 2009. Helmintos Gastrointestinais de Cerdocyon thous
(Linnaeus, 1766); Smith, 1839 provenientes da área de caatinga do
estado da Paraı́ba, Brasil. M.S. Thesis. Faculdade de Ciências
Agrárias e Veterinárias, Universidade Estadual de São Paulo–
UNESP, Campus de Jaboticabal, São Paulo, Brazil, 61 p.
MACHADO FILHO, D. A. 1950. Revisão do gênero Prosthenorchis
Travassos, 1915 (Acanthocephala). Memórias do Instituto Oswaldo
Cruz 48: 495–544.
RODELA, L. G. 2006. Unidades de vegetação e pastagens nativas do
Pantanal da Nhecolândia, Mato Grosso do Sul. Ph.D. Thesis.
Universidade de São Paulo, São Paulo, Brazil, 222 p.
RUAS, J. L., G. MULLER, N. A. R. FARIAS, T. GALLINA, A. S. LUCAS, F. G.
PAPPEN, A. L. SINKOC, AND J. G. W. BRUM. 2008. Helmintos do
cachorro do campo, Pseudalopex gymnocercus (Fischer, 1814) e do
cachorro do mato, Cerdocyon thous (Linnaeus, 1766) no sul do Rio
Grande do Sul, Brasil. Revista Brasileira Parasitologia Veterinária
17: 87–92.
SCHMIDT, G. D. 1972. Revision of the class Archiacanthocephala Meyer,
1931 (Phylum Acanthocephala), with emphasis on Oligacanthorhynchidae Southwell et Macfie, 1925. Journal of Parasitology 58: 290–
297.
SILVEIRA, L. 1999. Ecologia e conservação dos mamı́feros carnı́voros do
Parque Nacional das Emas. M.S. Thesis, Universidade Federal do
Goiás, Goiânia, Brazil, 117 p.
SOUTHWELL, T., AND J. W. S. MACFIE. 1925. On a collection of
Acanthocephala in the Liverpool School of Tropical Medicine.
Annals of Tropical Medicine and Parasitology 19: 141–284.
TRAVASSOS, L. 1915. Revisão dos Acanthocephalos brasileiros. I. Fam.
Gigantorthynchidae Hamann, 1982 (Nota prévia). Brasil Médico 29:
105.
———. 1917. Contribuição para o conhecimento da fauna helmintológica
brasileira, XVII. Revisão dos acantocéfalos brasileiros. Parte I. Fam.
Gigantorhynchidae Hamann, 1982. Memórias do Instituto Oswaldo
Cruz 17(Suppl.): 5–62.
VIEIRA, F. M., J. L. LUQUE, AND L. C. MUNIZ-PEREIRA. 2008. Checklist of
helminth parasites in wild carnivore mammals from Brazil. Zootaxa
1721: 1–23.
YAMAGUTI, S. 1963. Acanthocephala. In Systema Helminthum, Vol. 5.
John Wiley and Sons Interscience, New York, New York, 423 p.
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Queries for para-101-01-16
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document and make changes on these pages. Please limit your corrections to substantive changes that affect
meaning. If no change is required in response to a question, please write ‘‘OK as set’’ in the margin. Copy editor
2. Author: Please verify spelling of new species name cerdocynis (vs. cerdocynys). Copy editor
3. Author: You cite Stunkard (1965) in the first paragraph of the Remarks section. This is not listed in the literature
cited list. Please provide full matching reference for the list or delete in-text citation. Copy editor
4. Author: Please check spelling of Challithrix chrysoleu in Table I. Should it be Callithrix chrysoleuca? Copy editor
5. Author: Provide supplement number for Travassos (1917) reference? Copy editor
6. Author: Please provide editors (if any) for Yamaguti (1963) reference. Copy editor
//titan/production/p/para/live_jobs/para-101-01/para-101-01-16/layouts/para-101-01-16q.3d Monday, 1 December 2014 6:12 pm Allen Press, Inc. Page 1