ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
HELMINTHS OF CHIASMOCLEIS ALBOPUNCTATA (BOETTGER, 1885) (ANURA:
MICROHYLIDAE) AND DENDROPSOPHUS NANUS (BOULENGER, 1889) (ANURA: HYLIDAE) IN
CERRADO, SOUTHEASTERN BRAZIL
HELMINTOS DE CHIASMOCLEIS ALBOPUNCTATA (BOETTGER, 1885) (ANURA:
MICROHYLIDAE) E DENDROPSOPHUS NANUS (BOULENGER, 1889) (ANURA: HYLIDAE) EM
UMA ÁREA DE CERRADO, CENTRO-OESTE DO BRASIL
HELMINTOS DE CHIASMOCLEIS ALBOPUNCTATA (BOETTGER, 1885) (ANURA:
MICROHYLIDAE) Y DENDROPSOPHUS NANUS (BOULENGER, 1889) (ANURA: HYLIDAE) EN
CERRADO, SURESTE DEL BRASIL
ABSTRACT
Keywords: Anurans – Diversity Conservation – Helminthology – Parasitology – Wild Animals
Brazil is the country with the largest amphibian richness in the world with about 1,136 described species, of
which 1,093 are anurans. However, related studies on the knowledge of the associated helminth fauna are
scarce, representing only 8% of anurans. This study aimed to identify the parasite communities, and their
parasitic parameters in two amphibian species: Chiasmocleis albopunctata (Boettger, 1885) and
Dendropsophus nanus (Boulenger, 1889) found in eastern Mato Grosso do Sul State. The hosts were collected
through pitfall traps with drift fences (PTDF) and the Active Search method at the breeding sites, euthanized,
and the helminths removed and identified. A total of 172 amphibians were collected: 70 individuals from C.
albopunctata (Boettger, 1885) and 102 individuals from D. nanus (Boulenger, 1889). Of this total, 84 were
parasitised by at least one taxon. The total number of helminths found was 675. Here we report ten helminth
taxa, including two new records for the D. nanus host species, and five records for C. albopunctata host
species. Thus, this study represents an important contribution to the knowledge of parasite and host diversity,
since the amount of existing studies is insufficient and not representative.
Neotropical Helminthology
295
Neotropical Helminthology, 2019, 13(2), jul-dic:295-304.
Postgraduate Program in Biological Sciences (Zoology), São Paulo State University (UNESP), Institute of Biosciences of
Botucatu, 18618-970, Botucatu, São Paulo, Brazil.
Corresponding author. Phone: +55 1199895-0656. E-mail: alinibparra@gmail.com. *This work was funded by the
Foundation for Research Support of the State of São Paulo – FAPESP (grant number Fapesp 2014/26923-0; Fapesp
2012/20978-2).
2Postgraduate Program in Ecology, Institute of Biology, State University of Campinas (Unicamp), Natural History Laboratory
of Brazilian Amphibians (LaHNAB), Campinas, São Paulo, Brazil. ³Postgraduate Program in
Biological Sciences (Zoology), São Paulo State University (UNESP), Institute of Biosciences of
4
Botucatu, Botucatu, São Paulo, Brazil. Federal University of Grande Dourados,
Faculty of Biological and Environmental Sciences, Dourados, Mato Grosso do Sul, Brazil.
5São Paulo State University (UNESP), School of Natural Sciences and Engineering, Ilha Solteira, Department of Biology and
Zootechny, Phone: +55 1837431964. ORCID: 0000-0003-4389-916X.
1* 2 3
Alini Beloto Parra ; Mariana Retuci Pontes ; Murilo Souza Queiroz ; Rodney Murillo Peixoto
4 1,5
Couto & Luciano Alves dos Anjos
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
Volume13,Number2(jul-dec2019)
Brazil is the country with the largest amphibian
diversity in the world with about 1,136 species
described, of which 1,093 are anurans (Martins-
Sobrinho et al., 2017; Segalla et al., 2019).
However, related studies on the knowledge of the
associated helminth fauna are scarce, representing
only 8% of anurans (Campião et al., 2014, 2016;
Graça et al., 2017). Given that Brazil has a rich
helminth fauna, with about 164 taxa (57% of the
rates found for South America) (Campião et al.,
2014; Graça et al., 2017), faunal surveys are
necessary since the vast majority of anurans have
not had their helminth fauna described (Graça et
al., 2017). Faunal surveys are urgently needed
because the number of newly discovered
organisms is disappearing faster than new
organisms are described (Greene & Losos, 1988;
Dobson et al., 2008; Muniz-Pereira et al., 2009).
This is especially true in areas such as the Cerrado,
which has a very large diversity of species, mainly
endemic, but has a high degree of degradation
recorded, being constantly impacted by anthropic
activities which causes extinction of biodiversity,
invasion of exotic species, soil erosion, and
296
RESUMEN
Palabras clave: Anuros – Conservación de la Diversidad – Helmintología –Parasitología – Animales salvajes
Brasil es el país con la mayor riqueza de anfibios del mundo con alrededor de 1.136 especies descritas, de
las cuales 1.093 son anuros. Sin embargo, los estudios relacionados sobre el conocimiento de la fauna de
helmintos asociados son escasos, y representan solo el 8% de los anuros. Este estudio tuvo como objetivo
identificar las comunidades de parásitos y sus parámetros parasitarios en dos especies de anfibios:
Chiasmocleis albopunctata (Boettger, 1885) y Dendropsophus nanus (Boulenger, 1889) que se
encuentran en el este del estado de Mato Grosso do Sul. Los hospedadores fueron recolectados a través de
trampas de caídas con cercas de deriva (PTDF) y por el método de búsqueda activa en los sitios de
reproducción, sacrificados, y los helmintos fueron removidos e identificados. Se recolectaron un total de
172 anfibios: 70 individuos de C. albopunctata (Boettger, 1885) y 102 individuos de D. nanus (Boulenger,
1889). De este total, 84 fueron parasitados por al menos un taxón. El número total de helmintos
encontrados fue de 675. Aquí informamos diez taxones de helmintos, incluidos dos nuevos registros para
la especie hospedadora D. nanus y cinco registros para la especie hospedadora C. albopunctata. Por lo
tanto, este estudio representa una contribución importante al conocimiento de la diversidad de parásitos y
huéspedes, ya que la cantidad de estudios es insuficiente y no representativa.
INTRODUCTION fragmentation of habitats (Klink & Machado,
2005; Myers et al., 2000).
Anurans are animals widely diverse in their ways
of life and can spend their lives close to bodies of
water, as well as use them only in the larval stages
and breeding periods. They can even live in
environments with low water availability. Anurans'
way of life has a great influence on their parasitic
composition, just as parasites are major
determinants of this host group. However,
amphibian helminths constitute a poorly sampled
group in taxonomic survey studies (Anjos, 2011;
Campião et al., 2014).
Knowledge of the associated helminth fauna is
important in understanding the ecological
interactions between the various species of a
community, understanding the ecosystem
functions (McCallum & Dobson, 1995; Poulin &
Morand, 2000, 2004), biogeography (Rohde,
2005), and environmental quality assessment of
ecosystems (Thomas et al., 2005). Projects related
to environmental conservation and recovery
require knowledge of ecology and the systematics
of organisms and ecosystems (Scott et al., 1987).
Given these assumptions, knowledge of wildlife
Neotropical Helminthology, 2019, 13(2), jul-dic Parra et al.
297
fauna, associated parasites, and ecological
interactions is an important tool for conservation,
recovery, and rational use of the environment
(McCallum & Dobson, 1995; Poulin & Morand,
2000; Santos, 2003; Thomas et al., 2005, 2009).
This study aimed to reduce the gap in the
helminthological knowledge of anurans by
identifying parasite communities and their
parasitic parameters in two amphibian species
Chiasmocleis albopunctata (Boettger, 1885) and
Dendropsophus nanus (Boulenger, 1889) in an
area of Cerrado Biome, found in eastern Mato
Grosso do Sul state in the Midwest region of Brazil.
Study Area
The collections were performed in an area of the
Gallery Forest adjacent to the Stream of Véstia, at
UNESP Research and Extension Teaching Farm
(FEPE), Ilha Solteira Campus (20 ° 21'48” S, 051 °
24'17” W), Selvíria Municipality, Mato Grosso do
Sul State, Brazil.
Host Collection
The hosts were collected through six sets of Pitfall
Traps with Drift Fence (PTDF) (Corn, 1993),
consisting of a Y-shaped fence with a centre bucket
and a bucket at each “Y” vertex, usually in places
near anuran breeding sites. We also used the
searching in breeding sites method described by
Scott & Woodward (1994), which consists of
systematically walking around and through the
given collection site and searching for the animals
of interest (Halliday, 2006). In this work, the active
search collections were always performed by an
average of three people for three consecutive hours
(from 20:00 to 23:00 hours). The collections took
place monthly between September 2013 and
November 2015 (SisBio 36667-2; CEUA no.
06/2014).
At UNESP's Ecology Laboratory of Parasitism
(Lecop), the hosts were euthanised with sodium
thiopental solution. All internal organs, the
cellomatic cavity, and hind limb musculature were
evaluated for the presence of helminths.
The hosts were deposited at the Museum of
Zoology “Adão José Cardoso” State University of
Campinas (ZUEC).
Helminths Collection
Helminths were collected, fixed, and processed
following commonly employed methodologies
(Amato et al., 1991). The nematodes were clarified
with Aman's lactophenol (Andrade, 2000), and
species identification was based on articles and
classification keys (Vicente et al., 1990; Gibbons,
2010; Anderson et al., 2009). Trematodes were
submitted to the hydrochloric carmine staining
technique (Amato et al., 1991), diaphanized with
clove oil, and identified according to Fernandes &
Kohn (2014). Parasitic parameters such as
Prevalence (P) and Mean Infection Intensity (IMI)
were calculated according to Bush et al. (1997),
with the aid of the SigmaEstat 3.1 program.
The morphometric, morphological, and
photomicrograph data of the helminths were
obtained using a computerised LAS V4 image
analysis system (Leica Application Suite) adapted
to the DM 2500-Leica microscopes with phase
interferential contrast system.
The parasites were deposited in the
Helminthological Collection of the Department of
Parasitology, Institute of Biosciences, Paulista
State University (UNESP) (CHIBB 8798 - 8818),
Botucatu, State of São Paulo, Brazil.
Ethic aspects
All international, national, and institutional
guidelines applicable to the care and use of animals
were followed.
A total of 172 amphibians, 70 C. albopunctata
(Boettger, 1885) individuals and 102 D. nanus
(Boulenger, 1889) individuals were collected. Of
these, 84 were parasitised by at least one taxon (P =
48.8%). The total number of helminths found was
675, with a mean infection intensity of 5.8 ± 1.4 (1-
154).
In the host species C. albopunctata (Boettger,
1885), 214 helminths were found, of which 207
MATERIAL AND METHODS
RESULTS
Neotropical Helminthology, 2019, 13(2), jul-dic Helminths of Chiasmocleis and Dendropsophus
298
were nematodes, and seven were trematodes. The
overall prevalence was 62.8%, and the IMI was 2.8
± 0.3 (1-14). The nematodes were the most
prevalent helminths (97.7%) with an IMI of 2.8 ±
0.3 (1-14), while trematodes had a prevalence of
2.3% and a total of seven individuals collected in a
single host.
In the host species D. nanus (Boulenger, 1889), 461
helminths were found, of which 452 were
trematodes, five were acanthocephalans, and four
were nematodes. The total prevalence of helminths
was 39.2%, and the IMI was 11 ± 3.7 (1-154). The
prevalence of trematode infection in this host
species was 90% with an IMI of 12.2 ± 4.2 (1-154);
for acanthocephalans, the prevalence was 5% with
an IMI of 2.5 ± 1.5 (1-4), and for nematodes the
prevalence was 7.5% with an IMI of 1.3 ± 0.3 (1-2).
The taxa found in each host species, infection sites,
their prevalence (P) and mean infection intensity
(IMI), and abundance are described in Table 1.
Table 1. Parasitic parameters of nematodes and trematodes associated with anurans Chiasmocleis albopunctata
(Boettger, 1885) and Dendropsophus nanus (Boulenger, 1889). ID = Small Intestine; Cav = Cavity; GI = Large
Intestine; P = Overall Prevalence; IMI = Mean Intensity of Infection; SI = Site of Infection; E = stomach.
Chiasmocleis albopunctata
(Boettger, 1885)
Helminths P (%) IMI SI
Cosmocercidae 60.5 3.2 ± 0.46 (1-12) ID, IG, Cav
Aplectana
sp. 2.3 3 ID
Cosmocerca parva 67.4 2.5 ± 0.4 (1-14) ID, IG, Cav
Mesocoelium monas 2.3 7 ID
Larva of
Nematoda 2.3 1 IG
P (%) 58.6
IMI 5.2 ± 2.7
Dendropsophus nanus
(Boulenger, 1889)
Helminths
P (%)
IMI
SI
Cosmocercidae
7.5
1.3 ± 0.33 (1-2)
ID, IG
Lophosicyadiplostomum
sp.
85
13.1 ± 4.5 (1-154)
Rim
Cyst of
Trematoda digenea
2.5
1
Rim
Metacercaria unidentied
2.5
3
E
Neohaematoloechus neivai
2.5
2
Pulmão
Echinorhynchidae
5
2.5 ±
1.5 (1-4)
E, ID
P(%) 41.2
IMI 11.5 ± 24.5
Neotropical Helminthology, 2019, 13(2), jul-dic Parra et al.
299
Table 2. List of taxa found for each host species, highlighting what has been reported in the literature and what is
being reported for the first time.
Dendropsophus nanus
(Boulenger, 1889)
Family
Cosmocercidae Campião et al.
(2014, 2016)
Lophosicyadiplostomum
sp. Hamann &
González (2009)
Cyst
of
Trematoda Digenea Unidentied
Metacercaria unidentied Unidentied
Neohaematoloechus neivai First report
Family
Echinorhynchidae First report
Chiasmocleis albopunctata
(Boettger, 1885)
Family
Cosmocercidae
First report
Aplectana
sp.
First report
Cosmocerca parva
First report
Mesocoelium monas First report
Larva of Nematoda First report
We report here ten helminth rates and seven new
records, in addition to the host species C.
albopunctata (Boettger, 1885), which had not been
studied so far (Table 2).
The anuran D. nanus (Boulenger, 1889) is found
from Suriname and French Guiana, to Uruguay,
Argentina, Paraguay and Bolivia, and in Brazil it
occurs from the Northeast to the South (Frost,
2019). The registration of two new helminth taxa
for this species demonstrates the lack of studies in
this area.
Existing parasitological studies revealed 11
parasitic helminth taxa of D. nanus (Boulenger,
1889), these being Centrorhyncus sp., Unidentified
Acanthocephala, Contracaecum sp., Cosmocerca
p o d i c i p i n u s Baker & Vaucher, 1984,
Cosmocercoidea gen. sp., Cylindrotaenia sp.,
Creptotrema sp., Digenea gen. sp., Plagiorchiata
gen. sp, Diplostomidae gen. sp., and
Brevimulticaecum sp. (Hamann & Kehr, 1998;
González & Hamann, 2011; Aguiar et al., 2014;
Campião et al., 2014, 2016; Graça et al., 2017).
DISCUSSION The anuran D. nanus (Boulenger, 1889) has an
aquatic larval phase, remains in the vegetation near
the water as an adult, and uses the aquatic
environment in reproduction (Uetanabaro et al.,
2008). Proximity to water during the anuran life
cycle is highly related to the high prevalence of
trematode parasites (McAlpine, 1997; Muzzall et
al., 2001; Bolek & Coggins, 2001, 2003; Paredes-
Calderón et al., 2004; Hamann et al., 2006ab;
Schaefer et al., 2006; Todd, 2007; Toledo et al.,
2018), which explains the helminth fauna
described for D. nanus (Boulenger, 1889) in this
work. Thus, the use of water bodies during the life
cycle of D. nanus (Boulenger, 1889) contributed to
determining the parasite community of this anuran.
The Cosmocercidae family comprises of several
nematode species and have been reported in several
South American countries parasitising the
intestine, rectum, stomach, and lungs of their hosts.
Unidentified individuals of the family have been
reported in Dermatonotus muelleri (Boettger,
1885), Physalaemus nattereri (Steindachner,
1863) (=Eupemphix nattereri), Boana prasina
(Burmeister, 1856) (=Hypsiboas prasinus),
Lept odac tylu s latrans (Steffen, 1815),
Leptodactylus pentadactylus (Laurenti, 1768),
Neotropical Helminthology, 2019, 13(2), jul-dic Helminths of Chiasmocleis and Dendropsophus
300
Leptodactylus podicipinus (Cope, 1862),
Pethecopus azureus (Cope, 1862) (=Phyllomedusa
azurea), Rhinella crucifer (Wied-Neuwied, 1821),
Rhinella icterica (Spix, 1824) and Rhinella
diptycha (Cope, 1862)(=Rhinella schneideri)
(Campião et al., 2014). In the present study, for the
species D. nanus (Boulenger, 1889), individuals of
this family were found in the small and large
intestines of the anurans. Acanthocephalans,
belonging to the family Echinorhynchidae, have
been reported in Paraguay and Brazil parasitising
the intestine and body cavity of the hosts, being
some species from this family Acanthocephalus
a c u t i s p i n u s M a c h a d o F i l h o , 1 9 6 8 ,
Acanthocephalus caspanensis Fernandez and
Ibarra, 1989, Acanthocephalus correalimai
Machado Filho, 1970, Acanthocephalus ula Lent
and Santos, 1989 and Pseudoacanthocephalus
lutzi (Hamann, 1891) (Campião et al., 2014).
However, in this study, individuals of this family
were found in the small intestine and the stomach
o f t h e a n u r a n s . T r e m a t o d a
Lophosicyadiplostomum is an anuran parasite in its
larval phase and has been found in Argentina and
Brazil parasitising the kidneys of these hosts.
Individuals of the genus have been reported in
Scinax nasicus (Cope, 1862), Lysapsus limellum
Cope, 1862 (=Pseudis limellum), and D. nanus
(Boulenger, 1889) (=Hyla nana) (Hamann &
González, 2009; Campião et al., 2014). In the
present study, this species was found parasitising
the kidneys. The trematode Neohaematoloechus
neivai (Travassos & Artigas, 1927), have been
found in Brazil and Venezuela parasitising the
lungs of their hosts (Campião et al., 2014;
Fernandes & Kohn, 2014), having already been
reported in Leptodactylus latrans (Steffen, 1815),
Leptodactylus labyrinthicus (Spix, 1824),
Leptodactylus pentadactylus (Laurenti, 1768),
Pseudis paradoxa (Linnaeus, 1758), and
Lithobates palmipes (Spix, 1824) (=Rana
palmipes).
In this study, with the registration of the trematode
Neohaematoloecus neivai (Travassos & Artigas,
1927) and acanthocephalans of the family
Echinorhynchidae, we increased the number of
helminth taxa of D. nanus (Boulenger, 1889) to 13.
The frog C. albopunctata (Boettger, 1885) is found
in Bolivia, Argentina, Paraguay, and the Midwest
and Southeast Regions of Brazil (Frost, 2019).
Although their distribution covers four different
countries, the associated helminth fauna of this
anuran has never been studied.
The species C. albopunctata (Boettger, 1885) is
considered terrestrial and uses the aquatic
environment only in the larval phase and during
breeding periods (Uetanabaro et al., 2008; Giaretta
et al., 2008). Contact with soil may favour
nematode infection (Barton, 1999; Bolek &
Coggins, 2000, 2003; Iannacone, 2003; Luque et
al., 2005; Sena et al., 2018; Toledo et al., 2018),
which explains this marked prevalence of these
helminths for this host species. Despite this
prevalence of nematodes, the richness of parasite
species for this host was low with only three
species identified.
For the species C. albopunctata (Boettger, 1885),
nematodes of the family Cosmocercidae were
found parasitising the body cavity of the hosts. For
the Cosmocerca parva Travassos, 1925 helminth,
there are studies indicating its presence in
Argentina, Brazil, Colombia, Paraguay, Guyana,
and Peru (Campião et al., 2014). These parasites
are found mainly in the intestine and rectum of their
hosts, and have been reported in several species of
various genera such as Ameerega, Colostethus,
Dendropsophus, Edalorhina, Elachistocleis,
H a m p t o p h r y n e , H y p s o b o a s , H y l o d e s ,
Leptodactylus, Odontophrynus, Oreobates,
Phyllomedusa, Physalaemus, Pristimantis,
Rhaeboophion, Scella, Procella, Rhinella,
Proceratophrys, Scarthyla, and Scinax (Campião
et al., 2014). In this study, we found Cosmocerca
parva Travassos, 1925 in the body cavity of the
hosts. Individuals of the genus Aplectana have
been documented in several South American
countries parasitising the stomach, intestine and
rectum of their hosts. Unidentified individuals of
the genus have been found parasitising
C e r a t o p h r y s C r a n w e l l i Barr io, 1980 ,
Dendropsophus microps (Peters, 1872),
Dermatonotus muelleri (Boettger, 1885),
Haddadus binotatus (Spix, 1824), Boana
albopunctata (Spix, 1824) (=Hypsiboas
albopunctata), Boana pardalis (Spix, 1824)
(=Hypsiboas pardalis), Leptodactylus bufonius
Boulenger, 1894, Leptodactylus chaquensis Cei,
1950, Leptodactylus elenae Heyer, 1978,
Leptodactylus fuscus (Schneider, 1799),
Adenomera marmorata Steindachner, 1867
Neotropical Helminthology, 2019, 13(2), jul-dic Parra et al.
301
(=Leptodactylus marmoratus), Leptodactylus
mystacinus (Burmeister, 1861), Leptodactylus
podicipinus (Cope, 1862), Leptodactylus syphax
Bokermann, 1969, Physalaemus signifier (Girard,
1853), Rhinella granulosa (Spix, 1824), Rhinella
icterica (Spix, 1824), Rhinella marina (Linnaeus,
1758), Scinax acuminatus (Cope, 1862), Thoropa
miliaris (Spix, 1824), and Trachycephalus
mesophaeus (Hensel, 1867) (Campião et al.,
2014). In this study, Aplectana sp. was found in the
small intestine of the host. The Mesocoelium
monas (Rudolphi, 1819) Trematoda, according to
Campião et al. (2014) and Fernandes & Kohn
(2014), have been found in Argentina, Brazil,
Colombia, Paraguay, Peru and Venezuela
parasitising the small intestine of their hosts, and
have been reported in Siphonops annulatus
(Mikan, 1822), Leptodactylus fuscus (Schneider,
1799), Leptodactylus mystaceus (Burmeister,
1861), Leptodactylus mystacinus (Burmeister,
1861), Leptodactylus latrans (Steffen, 1815),
Leptodactylus pentadactylus (Laurenti, 1768),
Rhinella arenarum (Hensel, 1867), Rhinella
crucifer (Wied-Neuwied, 1821), Rhinella icterica
(Spix, 1824), Rhinella marina (Linnaeus, 1758),
Rhinella diptycha (Cope, 1862) (=Rhinella
schneideri), Incilius nebulifer (Girard, 1854) and
Scinax nasicus (Cope, 1862). In the present study it
was also found in the small intestine of the host.
All taxa found in C. albopunctata (Boettger, 1885)
have never been reported for this host species, as
this is the first study using this approach. Here we
highlight the five taxa record for this host species.
Additional studies with populations from other
locations may show different patterns from those
found here.
This study represents an important contribution to
the knowledge of the diversity of parasites and
hosts since the number of studies is insufficient and
not representative. It also helps to complement
information for ecosystem studies with a view to
facilitating conservation projects.
Foundation for Research Support of the State of
São Paulo – FAPESP (processes Fapesp
2014/26923-0; Fapesp 2012/20978-2). National
Council for Scientific and Technological
Development CNPq (process 474584/2013-5).
Laboratory of Ecology of Parasitism – LECOP.
ACKNOWLEDGEMENT
Aguiar, A, Morais, DH, Cicchi, PJP & Silva, RJ.
2014. Evaluation of Helminths Associated
with 14 Amphibian Species from a
Neotropical Island Near the Southeast
Coast of Brazil. Herpetological Review,
vol. 45, pp. 227-236.
Amato, JFR, Boeger, WA & Amato, SB. 1991.
Protocolos para laboratório – Coleta e
processamento de parasitos de pescado.
Imprensa Universitária – UFRRJ,
Seropédica, pp.81.
Anderson, R, Chabaud, A & Willmott, S. 2009.
Keys to the Nematode parasites of
vertebrates. CABI, Wallingford, CABI, pp.
463.
Andrade, C. 2000. Meios e soluções comumente
empregados em laboratórios. Editora
Universidade Rural, Seropédica, pp. 353.
Anjos, LA. 2011. Herpetoparasitology in Brazil:
what we know about endoparasites, how
much we still do not know. Neotropical
Helminthology, vol. 5, pp. 107-111.
Barton, DP. 1999. Ecology of helminth
communities in tropical Australian
amphibians. International Journal of
Parasitology, vol. 29, pp. 921-926.
Bolek, MG & Coggins, JR. 2000. Seasonal
occurrence and community structure of
helminth parasites from the Eastern
Am e r i ca n t o ad Bufo americanus
americanus, from Southeastern Wisconsin,
U.S.A. Comparative Parasitology, vol. 67,
pp. 202-209.
Bolek, MG & Coggins, JR. 2001. Seasonal
occurrence and community structure of
helminth parasites from the green frog,
Ra na c la m it a ns m e l a n o t a , f ro m
s o u t h e a s t e r n Wi s c o n s i n , U . S . A .
Comparative Parasitology, vol. 68, pp. 164-
172.
Bolek, MG & Coggins, JR. 2003. Helminth
Community structure of sympatric Eastern
BIBLIOGRAPHIC REFERENCES
Neotropical Helminthology, 2019, 13(2), jul-dic Helminths of Chiasmocleis and Dendropsophus
302
American toad, Bufo americanus, Northern
Leopard frog, Rana pipiens, and Blue-
spotted salamander, Ambystoma laterale,
from Southeastern Wisconsin. Journal of
Parasitology, vol. 89, pp. 673-680.
Bush, AO, Lafferty, KD, Lotz, JM & Shostak, AW.
1997. Parasitology meets ecology on its
own terms: Margolis et al. Revisited. The
Journal of Parasitology, vol. 83, pp. 575-
583.
Campião, KM, Morais, DH, Dias, OT, Aguiar, A,
Toledo, G, Tavares, LER & Silva, RJ. 2014.
Checklist of Helminth parasites of
Amphibians from South America. Zootaxa,
vol. 3843, pp. 1-93.
Campião, KM, Silva, ICO, Dalazen, GT, Paiva, F
& Tavares, LE. 2016. Helminth parasites of
11 anuran species from the Pantanal
wetland, Brazil. Comparative Parasitology,
vol. 83, pp. 92-100.
Corn, PS. 1993. Straingth-Line drift fences and
pitfall traps. In:Heyer, WR, Donnelly, MA,
McDiarmid, RW, Hayek, LC & Foster, MS
(eds). Measuring and monitoring biological
d i v e r s i t y : s t a n d a rd m e t h o d s f o r
amphibians. Smithsonian Institution Press.
Dobson, A, Lafferty, K, Kuris, A, Hechinger, R &
Jetz, W. 2008. Homage to Linnaeus: How
many parasites? How many hosts?
Proceedings of the National Academy of
Sciences, vol. 105, pp. 11482-11489.
Fernandes, BMM & Kohn, A. 2014. South
American trematodes parasites of
amphibians and reptiles. FIOCRUZ, Rio de
Janeiro, pp. 225.
Frost, DR. 2019. Amphibian Species of the World:
An Online Reference, Version 6.0. American
Museum of Natural History, New York,
USA, consulted in 16 of July of 2019,
<http://research.amnh.org/herpetology/am
phibia/index.html>
Giaretta, AA, Menin, M, Facure, KG, Kokubum,
MNC & Filho, JCO. 2008. Species richness,
relative abundance, and habitat of
reproduction of terrestrial frogs in the
Triângulo Mineiro region, Cerrado biome,
southeastern Brazil. Iheringia, Série
Zoologia, vol. 98, pp. 181-188.
Gibbons, LM. 2010. Keys to the nematode
parasites of vertebrates: Supplementary
volume. CABI Publishing, Wallingford,
Reino Unido, pp. 416.
González, CE & Hamann, MI. 2011. Cosmocercid
Nematodes of three species of frogs (Anura:
Hylidae) from Corrientes, Argentina.
Comparative Parasitology, vol. 78, pp. 212-
216.
Graça, RJ, Oda, FH, Lima, FS, Guerra, V,
Gambale, PG & Takemoto, RM. 2017.
Metazoan endoparasites of 18 anuran
species from the mesophytic semideciduous
Atlantic Forest in southern Brazil. Journal
of Natural History, vol. 51, pp. 705-729.
Greene, HW & Losos, JB. 1988. Systematics,
natural history, and conservation.
BioScience, vol 38, pp. 458-462.
Halliday, T. 2006. Amphibians. In:Sutherland, WJ
(ed). Ecological census techniques.
Cambridge University Press, Cambridge,
pp. 218-226.
Hamann, MI, González, C & Kehr, AI. 2006a.
Helminth community structure of the oven
frog Leptodactylus latinasus (Anura,
Leptodactylidae) from Corrientes,
Argentina. Acta Parasitologica, vol. 51, pp.
294-299.
Hamann, MI, Kehr, AI & González, CE. 2006b.
Species affinity and infracommunity
ordination of helminths of Leptodactylus
chaquensis (Anura: Leptodactylidae) in two
c o n t r a s t i n g e n v i r o n m e n t s f ro m
northeastern Argentina. Journal of
Parasitology, vol. 92, pp. 1171-1179.
Hamann, MI & González, CE. 2009. Larval
digenetic trematodes in tadpoles of six
amphibian species from Northeastern
Argentina. Journal of Parasitology, vol. 95,
pp. 623-628.
Hamann, MI & Kehr, AI. 1998. Variación espacio
temporal en infrapoblaciones de helmintos
y su relación con las fluctuaciones
poblacionales de Hyla nana (Anura,
Hylidae). Cuadernos de Herpetología, vol.
12, pp. 23-33.
Iannacone, J. 2003. Helmintos parasitos de
Atelopus bomolochus Peters 1973 (Anura:
Bufonidae) de Piura, Peru. Gayana, vol. 67,
pp. 9-15.
Klink, CA & Machado, RB. 2005. A conservação
do Cerrado Brasileiro. Megadiversidade,
vol. 1, pp.147-155.
Luque, JL, Martins, NA & Tavares, LER. 2005.
Community structure of metazoan parasites
of the yellow Cururu toad, Bufo ictericus
Neotropical Helminthology, 2019, 13(2), jul-dic Parra et al.
303
(Anura, Bufonidae) from Rio de Janeiro,
Brazil. Acta Parasitology 50: 215-220.
Martins-Sobrinho, PM, Silva, WGO, Santos, EG,
Moura, GJB & Oliveira, JB. 2017.
Helminths of some tree frogs of the families
Hylidae and Phyllomedusidae in an Atlantic
rainforest fragment, Brazil. Journal of
Natural History, vol. 51, pp. 1639-1648.
McAlpine, DF. 1997. Helminth communities in
bullfrogs (Rana catesbeiana), green frogs
(Rana clamitans), and leopard frogs (Rana
pipiens) from New Brunswick, Canada.
Canadian Journal of Zoology, vol. 75, pp.
1883–1890.
McCallum, H & Dobson, A. 1995. Detecting
disease and parasite threats to endangered
species and ecosystems. Trends in Ecology
and Evolution, vol. 10, pp. 190-194.
Muniz-Pereira, LC, Vieira, FM & Luque, JL. 2009.
Checklist of helminth parasites of
threatened vertebrate species from Brazil.
Zootaxa, vol. 2123, pp.1-45.
Muzzall, PM, Gillilland, MG, Summer, CS &
Mehne, CJ. 2001. Helminth communities of
green frogs Rana clamitans Latreille, from
southwestern Michigan. Journal of
Parasitology, vol. 87, pp. 962-968.
Myers, N, Mittermeier, RA, Mittermeier, CG, da
Fonseca, GAB & Kent, J. 2000. Biodiversity
hotspots for conservation priorities. Nature,
vol. 403, pp. 853-858.
Paredes-Calderón, L, León-Regagnon, V &
Gárcia-Prieto, L. 2004. Helminth
infracommunities of Rana vaillanti Brocchi
(Anura: Ranidae) in Los Tuxtlas, Veracruz,
Mexico. Journal of Parasitology, vol. 90, pp.
692-696.
Poulin, R & Morand, S. 2000. The diversity of
parasites. Quarterly Review of Biology,
vol. 75, pp. 277-293.
Poulin, R & Morand, S. 2004. Parasite
Bio div ers ity. Smithsonian Books,
Washington, pp.216.
Rohde, K (ed.). 2005. Parasitologia Marinha.
Publicação CSIRO, Collingwood IC 3066,
Austrália e CABI Publishing, Wallingford,
Reino Unido, pp. 565.
Schaefer, EF, Hamann, MI, Kehr, AI, González, CE
& Duré, MI. 2006. Trophic, reproductive
and parasitological aspects of the ecology
of Leptodactylus chaquensis (Anura:
L e p t o d a c t y l i d a e ) i n A r g e n t i n a .
Herpetological Journal, vol. 16, pp. 387-
394.
Santos, AJ. 2003. Estimativas de riqueza em
espécies. In: Cullen, LJR, Valladares-
Padua, C & Rudran, R (eds.) Métodos de
estudos em Biologia da Conservação &
Manejo da vida Silvestre. Ed. da UFPR,
Fundação o Boticário de Proteção à
natureza, Curitiba, pp. 19-41.
Segalla, MV, Caramaschi, U, Cruz, CAG, Garcia,
PCA, Grant, T, Haddad, CFB, Santana, DJ,
Toledo, LF & Langone, JA. 2019. Brazilian
amphibians: list of Species. Herpetologia
Brasileira, vol. 8, pp. 65-96.
Sena, PA, Conceição, BM, Silva, PF, Silva, WGO,
Ferreira, WB, Júnior, VAS, Moura, GJB &
Oliveira, JB. 2018. Helminth communities
of Pithecopus nordestinus (Anura:
Phyllomedusidae) in forest remnants,
Brazil. Herpetology Notes, vol. 11, pp. 565-
572.
Scott, JM, Csuti, B, Jacobi, JD & Estes, JE. 1987.
Species richness: a geographical approach
to protecting future biological diversity.
BioScience, vol. 37, pp. 782- 788.
Scott, NJ & Woodward, BD. 1994. Inventory and
monitoring. In: Heyer, WR, Donnelly, MA,
McDiarmid, RW, Hayek, LA & Foster, MS
(eds.). Measuring and monitoring
biological diversity – Standard methods for
amphibians. Smithsonian Institution,
Washington.
Thomas, F, Guégan, JF & Renaud, F. (eds.). 2009.
Ecology and evolution of parasitism.
Oxford University Press, USA.
Thomas, F, Renaud, F & Guégan, JF. (eds.). 2005.
Parasitism and ecosystems. Oxford
University Press, USA.
Todd, BD. 2007. Parasites lost? An overlooked
hypothesis for the evolution of alternative
reproductive strategies in Amphibians. The
American Naturalist, vol. 170, pp. 793-799.
Toledo, GM, Schwarts, HO, Nomura, HAQ,
Aguiar, A, Velota, RAMV, Silva, RJ &
Anjos, LA. 2018. Helminth community
structure of 13 species of anurans from
Atlantic rainforest remnants, Brazil.
Journal of Helminthology, vol. 92, pp. 438-
444.
Uetanabaro, M, Prado, CPA, Rodrigues, DJ,
Gordo, M & Campos, Z. (eds.). 2008. Guia
de Campo dos Anuros do Pantanal e
Neotropical Helminthology, 2019, 13(2), jul-dic Helminths of Chiasmocleis and Dendropsophus
304
Planaltos de Entorno. Ed. UFMS, Campo
Grande; Ed UFMT, Cuiabá, pp. 196.
Vicente, JJ, Rodrigues, HO, Gomes, DC & Pinto,
RM. 1990. Nematoides do Brasil. Parte II:
Nematoides de anfíbios. Revista Brasileira
Zoologia, vol. 7, pp. 549-626.
Received September 27, 2019.
Accepted November 30, 2019.
Neotropical Helminthology, 2019, 13(2), jul-dic Parra et al.
