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Helminth Fauna of Two Species of Physalaemus (Anura: Leiuperidae) from anUndisturbed Fragment of the Atlantic Rainforest, Southeastern BrazilAuthor(s): Gislayne M. Toledo , Aline Aguiar , Reinaldo J. Silva , and Luciano A. AnjosSource: Journal of Parasitology, 99(5):919-922. 2013.Published By: American Society of ParasitologistsDOI: http://dx.doi.org/10.1645/GE-3212.1URL: http://www.bioone.org/doi/full/10.1645/GE-3212.1
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J. Parasitol., 99(5), 2013, pp. 919–922
� American Society of Parasitologists 2013
Helminth Fauna of Two Species of Physalaemus (Anura: Leiuperidae) from an Undisturbed
Fragment of the Atlantic Rainforest, Southeastern Brazil
Gislayne M. Toledo, Aline Aguiar, Reinaldo J. Silva, and Luciano A. Anjos*, UNESP – Univ Estadual Paulista, Campus de Botucatu, Instituto deBiociencias, Departamento de Parasitologia, CEP: 18618-970, Botucatu, Sao Paulo, Brazil; *UNESP – Univ Estadual Paulista, Campus de Ilha Solteira, FIES,Departamento de Biologia e Zootecnia, CEP: 15385-000, Ilha Solteira, Sao Paulo, Brazil. Correspondence should be sent to: [email protected]
ABSTRACT: Two amphibian species, Physalaemus cuvieri and Physalaemus
olfersii, from Serra do Mar State Park, which is an old-growth
environment of the Atlantic Rainforest in southeastern Brazil, were
surveyed for endoparasites. Hosts were sampled in 2 ponds; each was
colonized by only 1 Physalaemus species. The overall prevalence of
helminths was high and similar in both amphibian species. The mean
intensity of infection in P. olfersii did not differ statistically from that in P.
cuvieri. Nine helminth species were found: 2 acanthocephalans, 1 cestode,
and 6 nematodes. Parasite richness in the 2 host species was similar. The
composition of helminth fauna differed but the 2 hosts shared the most
prevalent taxon of nematode (an unidentified species of Cosmocercidae).
All helminth species exhibited an aggregated distribution pattern in the
host species. The present results demonstrate relatively low species
richness and the dominance of generalist parasite species. This study
contributes to knowledge regarding the structure and composition of the
helminth community in anurans.
Species of Physalaemus Fitzinger, 1826 are leiuperid frogs, a genus
which includes 45 species (Frost, 2013) with broad geographic distribution
in the tropical region of the Americas from Mexico to South America
(Nascimento et al., 2005). A systematic review of the genus by Nascimento
et al. (2005) using morphometric analyses, external morphology, color
patterns, and bone characteristics defines 7 groups of species. Physalaemus
cuvieri Fitzinger, 1826 and Physalaemus olfersii (Lichtenstein and
Martens, 1856) are representatives of 2 different clusters, the P. cuvieri
group and P. olfersii group, respectively. Physalaemus cuvieri is a small-
bodied species with nocturnal behavior found in open areas near lentic
aquatic environments (Dixo and Verdade, 2006). This species is widely
distributed throughout the northeastern, central western, southeastern,
and southern regions of Brazil as well as in parts of Argentina and eastern
Paraguay (Frost, 2013). Physalaemus olfersii is found near bodies of water
in open forests or at the forest ecotone (Dixo and Verdade, 2006)
throughout southeastern and southern Brazil (Nascimento et al., 2005;
Frost, 2013).
Features of the natural history and ecology of host species, such as size,
sex, diet composition, and behavior, are suggested to be important
determinants in structuring amphibian parasite communities (Tucker and
Joy, 1996; Bursey et al., 2001; Goldberg and Bursey, 2002; Bolek and
Coggins, 2003; Hamann, Gonzalez et al., 2006; Schaefer et al., 2006;
Santos and Amato, 2010). Moreover, characteristics of the preferred host
environments are considered as key factors with respect to parasite
colonization (Zelmer et al., 1999; Kehr et al., 2000; Muzzall et al., 2001;
Zelmer et al., 2004; Goater et al., 2005; Haman, Gonzalez et al., 2006).
The aim of the present study was to conduct a survey of helminth fauna
associated with 2 amphibian species, P. cuvieri and P. olfersii, at 2 sites in
the Serra do Mar State Park in southeastern Brazil. These data will
hopefully contribute to knowledge regarding the composition and
structure of the helminth community parasitizing frogs in an area with a
high degree of species diversity and endemism.
Twenty-two specimens of P. cuvieri and 21 specimens of P. olfersii were
sampled under a license from the Brazilian environmental agency IBAMA
(Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais
Renovaveis, No. 18240-1/2009) in January 2010 at the Serra do Mar
State Park, ‘‘Nucleo Santa Virgınia’’ (238240S and 458030W), which is an
undisturbed area of the Atlantic rainforest located in the state of Sao
Paulo, southeast Brazil. The amphibians were sampled from 2 temporary
ponds separated by a distance of 2 km; 1 pond was inhabited by P. olfersii
and the other by P. cuvieri.
The frogs were captured during active searches at night, transported to
the laboratory, and killed with a sodium thiopental solution. The
specimens were necropsied and the gastrointestinal tract, lungs, kidneys,
liver, urinary bladder, body cavity, and musculature of the hind limbs
were searched for the presence of helminths.
Parasites were fixed in alcohol-formaldehyde-acetic acid and preserved
in 70% ethyl alcohol. For species determination cestodes and acantho-
cephalans were stained with carmine and cleared with creosote.
Nematodes were cleared with lactophenol and examined using temporary
mounts. The systematic determination of helminths followed the
approaches proposed by Yamaguti (1959, 1961), Travassos et al. (1969),
Schmidt (1986), Vicente et al. (1990), Anderson et al. (2009), and Gibbons
(2010). Morphological and morphometric measures were obtained using
the computerized LAS V3 image analysis system (Leica Application Suite,
Leica Microsystems, Wetzlar, Germany) coupled to a DM5000B
microscope (interferential phase contrast). Helminth species were depos-
ited in the Colecao Helmintologica do Instituto de Biociencias de
Botucatu (CHIBB) of the Universidade Estadual Paulista, state of Sao
Paulo, Brazil.
Overall prevalence, mean intensity of infection, and mean abundance
were calculated following the methods provided by Bush et al. (1997).
Mean helminth species richness also was calculated. The discrepancy index
(D) was estimated following the method described by Poulin (1993). This
index has a minimum value of zero (D¼0), when all hosts harbor the same
number of parasites, whereas aggregation is considered a maximum (D¼1) when all parasites are found in a single host. The Quantitative
Parasitology 3.0 program (Rozsa et al., 2000) was used to determine this
index. Student’s t-test was employed to determine significant differences
between mean intensity of infection between the host species, as
recommended by Magurran (1988). The Statistica 7.0 program (Statsoft
Inc., 2004) was used for the statistical analysis. Nonparametric multi-
response permutation procedures (MRPP) were run on the PC-Ord 4.0
program (McCune and Mefford, 1999) to determine similarity in the
composition and abundance of parasites in the amphibian species. The
Sorensen (Bray-Curtis) distance was used as the dissimilarity measure to
determine whether the findings were more similar than would be expected
if the samples were randomly distributed in the environment. Delta (A)
equals the maximum value (A ¼ 1) when all groups have the same
composition of species, A ¼ 0 when heterogeneity within groups equals
expectation by chance, and A , 0 when heterogeneity within groups is
greater than that expected by chance (McCune and Mefford, 1999). The
purpose of this test is to determine the concentration within groups
(similar to t- and F-tests) and does not depend on the assumption of
normality but rather on the internal variability of the data (Zimmerman et
al., 1985).DOI: 10.1645/GE-3212.1
919
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The overall prevalence of infection was 91% in P. cuvieri and 90% in P.
olfersii. Ninety-eight helminths were found infecting P. cuvieri with a mean
intensity of infection of 4.9 6 0.8 helminths/host. One-hundred forty-
seven helminths were collected from P. olfersii with a mean intensity of
infection of 7.7 6 1.7 helminths/host. No statistically significant difference
was observed between host species regarding mean intensity of infection
(Student’s t-test: t ¼�1.5112; df¼ 25; P ¼ 0.1437) (Table I).
Nematodes represented 99% of the total helminths in the component
community in P. cuvieri and 95.2% in P. olfersii. The component
community in P. cuvieri was composed of 5 taxa, i.e., larvae of an
unknown encysted nematode, an unidentified cosmocercid, Physaloptera
sp., Rhabdias sp. (Nematoda), and Acantocephalo saopaulensis (Acantho-
cephala). For P. olfersii the community component was also composed of
5 taxa: an unidentified cosmocercid, Ochoterenella sp., Oswaldocruzia
subauricularis (Nematoda), a cystacanth of Centhorhynchidae (Acantho-
cephala), and Cylindrotaenia americana (Cestoda). Data for the preva-
lence, mean intensity of infection, and site of infection for each helminth
species in P. cuvieri and P. olfersii are presented in Table II.
Due to the similarity of congeneric females of an unidentified
cosmocercid nematode, and the absence of males in several samples,
identification was not possible. Species determination is frequently based
on male characters such as spicule length, gubernaculum, and caudal
papillae.
Unidentified cosmocercids and larvae of Physaloptera sp. were the most
prevalent taxa in P. cuvieri whereas an unidentified cosmocercid, C.
americana, and O. subauricularis were the most prevalent taxa in P. olfersii
(Table II). The greatest mean intensity of infection in P. cuvieri was due to
larvae of an unidentified encysted nematode whereas an unidentified
cosmocercid was the most abundant in P. olfersii (Table II).
Parasites were recovered from the gastrointestinal tract, liver, lungs,
and body cavity. The gastrointestinal tract had the greatest richness and
abundance of nematodes in both host species. Unidentified cosmocercids
were found in the intestines of both P. cuvieri and P. olfersii. Rhabdias sp.
was found in the lungs of P. cuvieri alone and centhorhynchid cystacanths
were found in the liver of P. olfersii alone (Table II). Not surprisingly, the
discrepancy index revealed that all helminth species exhibited an
aggregated distribution pattern (Table II).
In P. cuvieri, in which there were 5 helminth taxa, the richness of
parasites ranged from 1 species (45% of the hosts), 2 species (45% of
hosts), and 3 helminth species (10% of hosts). Five helminth taxa were
identified in P. olfersii, with the majority of infected specimens harboring 1
helminth species (52.6%) and a slightly smaller percentage harboring 2
species (47.4%) (Fig. 1).
Mean parasite richness (Sm) in the 2 host species was similar (P. cuvieri:
Sm ¼ 1.5 6 0.2; P. olfersii: Sm ¼ 1.3 6 0.2). However, the permutation
analysis (MRPP) revealed that the helminth fauna found in the 2 host
species was different (A ¼ 0.047; P , 0.05).
The overall prevalence of parasites was high in both host species. This
high prevalence of infection may be related to the biology of the hosts,
which have a habitat that is terrestrial and cryptozoic and favors infection
by monoxenous life cycle nematodes by penetration of the skin or the
ingestion of eggs or larvae (Anderson, 2000). In addition, they use aquatic
calling sites in the breeding season which favors infection by heteroxenous
life cycle helminths, with higher exposure to cercariae or other potential
intermediate hosts (Hamann, Gonzalez et al., 2006; Hamann, Kehr et al.,
2006).
A high prevalence by cosmocercid nematodes was found in both host
species. These parasites infect their hosts either orally or by the active
penetration of larvae through the skin (Anderson, 2000).
Larvae of Physaloptera spp. are generally found in amphibians
(Goldberg et al., 1993), including Neotropical anurans (Bursey et al.,
2001; Goldberg et al., 2009). These parasites use insects and amphibians as
intermediate and definitive hosts; snakes, lizards, and birds are infected
when they consume anurans infected with larvae (Anderson, 2000). These
helminths were found in the stomach of P. cuvieri. The absence of these
parasites in P. olfersii may be associated with the lack of an appropriate
insect intermediate host in the pond sampled or with specialization on a
particular type of prey that is free of physalopterans.
Although acanthocephalans are less frequent in amphibian hosts
(Smales, 2007), 2 species of acanthocephalans were found in the present
TABLE I. Parameters of infection of helminth communities associated withPhysalaemus cuvieri and Physalaemus olfersii from Serra do Mar StatePark, ‘‘Nucleo Santa Virgınia,’’ municipality of Sao Luiz do Paraitinga,state of Sao Paulo, southeastern Brazil.
Parameters
Physalaemus
cuvieri
(n ¼ 22)
Physalaemus
olfersii
(n ¼ 21)
Overall prevalence (%) 91 90
Mean abundance 4.5 6 0.8 7.0 6 1.6
Mean intensity of infection (range) 4.9 6 0.8 (1–13) 7.7 6 1.7 (1–29)
Helminth richness 6 5
Mean richness (range) 1.5 6 0.2 (1–3) 1.3 6 0.2 (1–2)
TABLE II. Prevalence (P), mean abundance (MA), mean intensity of infection (MII), aggregation index (D), and site of infection (SI) of helminth speciesinfecting Physalaemus cuvieri and Physalaemus olfersii in Serra do Mar State Park, ‘‘Nucleo Santa Virgınia,’’ southeastern Brazil. *Site of infection: BC¼body cavity; S¼ stomach; LI ¼ large intestine; SI¼ small intestine; L¼ liver; Lu¼ lungs.
Helminth species
Physalaemus cuvieri (n ¼ 22) Physalaemus olfersii (n ¼ 21)
P (%) MA 6 SE
MII 6 SE
(Range) D SI* P (%) MA 6 SE
MII 6 SE
(Range) D SI*
Acanthocephala
Acanthocephalus saopaulensis 4.5 0.05 6 0.04 1 (1) 0.913 LI — — — — —
Centrorhynchidae (cystacanths) — — — — — 9.5 0.1 6 0.1 1 (1) 0.909 L
Cestoda
Cylindrotaenia americana — — — — — 14.3 0.2 6 0.2 1.7 6 0.7 (1–3) 0.848 SI
Nematoda
Nematode encysted (larvae) 13.6 0.77 6 0.53 5.7 6 2.7 (2–11) 0.89 S — — — — —
Cosmocercidae unidentified 81.8 2.7 6 0.5 3.3 6 0.5 (1–10) 0.447 SI, LI 90.5 6.3 6 1.5 6.9 6 1.6 (1–25) 0.491 SI, LI
Ochoterenella sp. — — — — — 4.8 0.05 1 (1) 0.909 BC
Oswaldocruzia subauricularis — — — — — 14.3 0.3 6 0.2 2.3 6 0.9 (1–4) 0.857 SI
Physaloptera (larvae) 40.9 0.77 6 0.25 1.9 6 0.4 (1–4) 0.667 S — — — — —
Rhabdias sp. 9.1 0.14 6 0.10 1.5 6 0.5 (1–2) 0.848 Lu — — — — —
920 THE JOURNAL OF PARASITOLOGY, VOL. 99, NO. 5, OCTOBER 2013
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study, i.e., adults of Acanthocephalus saopaulensis in P. cuvieri and the
cystacanth of a centhorhynchid in P. olfersii, affirming that amphibians
can act as either definitive hosts (Smales, 2007; Pinhao et al., 2009) or
second intermediate–paratenic hosts (Smales, 2007).
Centrorhynchid cystacanths have been reported in several amphibian
species (Rodrigues, 1986; Azevedo-Ramos et al., 1998; Goldberg and
Bursey, 2003; Hamann, Gonzalez et al., 2006; Goldberg et al., 2009;
Santos and Amato, 2010) whereas A. saopaulensis has been found in a
much smaller number of amphibian hosts (Smales, 2007; Pinhao et al.,
2009).
Cylindrotaenia americana is known from a wide variety of North
American and South American amphibians (Wardle and MacLeod, 1952;
Tantalean and Garcıa, 1989; Recharte, 1995; Rego, 1995; Bursey et al.,
2001; Goldberg et al., 2002) and was found in the small intestine of P.
olfersii in the present study.
The parasite fauna was composed of generalist species, as all taxa found
in both host species also infect other amphibian species and even different
families. According to Aho (1990), generalist parasites are the major
species composing helminth communities in amphibians. For example,
cosmocercids, O. subauricularis, and Rhabdias sp. found here are also
known to infect Rhinella icterica (Spix, 1824) (Pinhao et al., 2009),
Leptodactylus podicipinus (Cope, 1862) (Campiao et al., 2009), and
Rhinella fernandezae (Gallardo, 1957) (Santos and Amato, 2010) from
other localities in the Neotropics. Hosts in same locality, even those of
different species and genera, can share helminth taxa when exposed to
similar ecological conditions (Aho, 1990).
Therefore, the present findings are in agreement with a number of
studies regarding the community structure of helminths in amphibians
with relatively low species richness (compared with other vertebrate hosts)
and the dominance by generalist species (Aho, 1990; Boquimpani-Freitas
et al., 2001; Van Sluys et al., 2006; Campiao et al., 2009; Pinhao et al.,
2009; Klaion et al., 2011). These results contribute to knowledge on the
structure and composition of the helminth community in anurans. Further
studies should be carried out in the region to gain a better understanding
of the ecological relationships between amphibian hosts and their parasite
fauna.
The authors are grateful to Carla S. Cassini for help with the
manuscript and colleagues from the Laboratorio de Parasitologia de
Animais Silvestres (Lapas) – UNESP for help with the fieldwork. G. M.
Toledo and A. Aguiar thank the Conselho Nacional de Desenvolvimento
Cientıfico e Tecnologico (CNPq) for MSc. scholarships (130585/2011-4
and 130583/2011-1). L. A. Anjos thanks the Fundacao de Amparo a
Pesquisa do Estado de Sao Paulo (FAPESP) for the postdoctoral grant
(2008/50417-7). R. J. Silva is grateful to FAPESP for financial support
(2008/58180-6).
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