ORIGINAL ARTICLE /ARTÍCULO ORIGINAL
COMMUNITY STRUCTURE OF PARASITES OF THE TREE FROG SCINAX
FUSCOVARIUS (ANURA, HYLIDAE) FROM CAMPO BELO DO SUL, SANTA
CATARINA, BRAZIL
ESTRUCTURA DE LA COMUNIDAD PARASITARIA DE LA RANA ARBORICOLA
SCINAX FUSCOVARIUS (ANURA, HYLIDAE) DE CAMPO BELO DO SUL, SANTA
CATARINA, BRASIL
1,2 1,3 1,2
Viviane Gularte Tavares dos Santos ; Márcio Borges-Martins & Suzana B. Amato
1 Departamento de Zoologia, Programa de Pós-graduação em Biologia Animal, Instituto de Biociências, Universidade
Federal do Rio Grande do Sul, Porto Alegre, 91501-970, Rio Grande do Sul, Brasil.
2 Laboratório de Helmintologia; Universidade Federal do Rio Grande do Sul, Porto Alegre, 91501-970, Rio Grande do Sul,
Brasil.
3 Laboratório de Herpetologia. Universidade Federal do Rio Grande do Sul, Porto Alegre, 91501-970, Rio Grande do Sul,
Brasil. E-mail: santosvgt@gmail.com; sbamato@ufrgs.br; borges.martins@ufrgs.br
Neotropical Helminthology, 2016, 10(1), ene-jun: 41-50.
ABSTRACT
Keywords: Acanthocephala - anurans - helminth parasites - hylids - Nematoda - tree frogs
Sixty specimens of Scinax fuscovarius (Lutz, 1925) were collected between May 2009 and
October 2011 at Campo Belo do Sul, State of Santa Catarina, Brazil, and necropsied in search of
helminth parasites. Only four helminth species were found: Pseudoacanthocephalus sp.
Petrochenko, 1958, Cosmocerca brasiliense Travassos, 1925, C. parva Travassos, 1925 and
Physaloptera sp. Rudolphi, 1819 (larvae). The genus of the female cosmocercids could not be
determined. Only 30% of the anurans were parasitized. Scinax fuscovarius presented low
prevalence, infection intensity, and parasite richness. Sex and size of S. fuscovarius individuals
did not influence the prevalence, abundance, and species richness of helminth parasites.
RESUMEN
Palabras clave: Acanthocephala – anuros - helmintos parásitos – hílidos – Nematoda – rana arborícola
Sesenta ejemplares de Scinax fuscovarius (Lutz, 1925) fueron colectados entre mayo de 2009 y
octubre de 2011 en Campo Belo do Sul, Estado de Santa Catarina, Brasil y necropsiados para el
estudio de sus helmintos parásitos. Fueron halladas solamente cuatro especies de helmintos:
Pseudoacanthocephalus sp. Petrochenko, 1958, Cosmocerca brasiliense Travassos, 1925, C.
parva Travassos, 1925 and Physaloptera sp. Rudolphi, 1819. Las hembras de cosmocércidos no
pudieron ser determinadas debido a la falta de caracteres taxonómicos. Solamente el 30% de los
anuros estuvieron parasitados. Scinax fuscovarius presentó baja prevalencia, intensidad de
infección y riqueza parasitaria. El sexo y el tamaño de S. fuscovarius no influyeron en la
prevalencia, abundancia y riqueza de especies de helmintos parásitos.
41
ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
42
research and showing that the parasite richness
is higher than that cited by Aho (1990).
Scinax fuscovarius (Lutz, 1925) occurs from
south to southern Brazil and eastern Argentina,
Paraguay and Bolivia. It is found in open areas
such as pastures. At night during the
reproduction season they are found in still
water (lakes, ponds and wetlands), while at
other periods they take refuge in trees. The
tadpoles are nektonic and feed on suspended
matter. As adults, males measure from 37 to 47
mm, and females from 42 to 48 mm (Kwet &
Di-Bernardo, 1999; Kwet et al., 2010). This
species is very abundant in several areas of
southern Brazil, nevertheless, little is known
about its parasite community structure. Being
an arboreal species, S. fuscovarius is a good
model to analyze if arboreal frogs have lower
helminth richness as proposed by Aho (1990).
This study aimed to: identify the helminth
parasites of S. fuscovarius; analyze the parasite
community structure; and increase the
knowledge of the biology of these species with
parasitological data.
Sixty S. fuscovarius specimens (28 females, 31
males, one specimen with undetermined sex),
were captured under license SISBIO (Number
026/2006), between June 2009 and December
2011, at the Municipality of Campo Belo do
Sul (27°59' 42.19”S, 50°53'27.92”W, ranges
between 700-900 m.a.s.l), located in the
Araucarias Plateau Region of the State of
Santa Catarina, southern Brazil.
The specimens were manually collected and
sacrificed with lidocaine Geyer® 2% (local
anesthetic), spread on the abdomen of the
animal and absorbed by the skin; they were
weighed and measured (snout-cloacal length).
The sex of the host was identified through the
There are a few factors, such as host habit and
diet that may influence parasite community
structure. Anurans are a much diversified
group of vertebrates with 7300 extant species
which can be fossorial, arboreal, terrestrial,
semi-aquatic or aquatic (Duellman & Trueb,
1994; Frost, 2014). Aho (1990) observed that
semi-aquatic anurans had a tendency to present
greater helminth richness; terrestrial and
aquatic anurans presented intermediate and
similar values, while fossorial and arboreal
anurans presented lower helminth richness.
There are some studies on anurans that
demonstrate a positive relationship between
the host habitat and the variability of the
parasite community structure (Hamann &
Kehr, 1998; Bolek & Coggins, 2000; Muzzal et
al., 2001; Bursey et al., 2001; Iannacone,
2003; León-Règagnon et al., 2005; Luque et
al., 2005; Brooks et al., 2006; Goldberg et al.,
2007; González & Hamann, 2008; González,
2009; Santos & Amato, 2010; Hamann et al.,
2010; Campião et al., 2010; Santos et al.,
2013). Aquatic and/or semi-aquatic anurans
tend to present a greater number of digenean
species, because most of the anuran digeneans
use aquatic or semi-aquatic arthropods as
secondary intermediate hosts (Prudhoe &
Bray, 1982).
The diversity of parasite communities of the
Neotropical anurans is unknown. Since this
region concentrates the largest number of
global anuran richness, an adequate
description of their parasite diversity is
important to better understand some patterns
that are not well defined. Luque et al. (2005),
Santos & Amato (2010), Santos et al. (2013)
and Chero et al. (2014) presented results of
recent studies on Rhinella icterica (Spix,
1824), Rhinella fernandezae Gallardo, 1957
and Telmatobius jelskii (Peters, 1863)
demonstrating the contribution of this kind of
INTRODUCTION
MATERIAL AND METHODS
Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Santos et al.
43
vouchered at the Helminthological Collection
of Instituto Oswaldo Cruz (CHIOC),
FIOCRUZ, Rio de Janeiro, Rio de Janeiro
State, Brazil. All hosts examined were
vouchered at the Amphibian Collection,
Herpetology Laboratory, Zoology
Department, Universidade Federal do Rio
Grande do Sul, Porto Alegre, Rio Grande do
Sul, Brazil.
A total of 35 helminths, representing an
average intensity of infection of 0.6 helminths /
host, were collected. Only acanthocephalans
and nematodes were found (Table 1). The
parasite community was composed of four
helminth species, Pseudoacanthocephalus sp.,
Cosmocerca parva Travassos, 1925 and
Cosmocerca brasiliense Travassos, 1925, and
one species was represented by only a larval
form, Physaloptera sp. Due to the lack of
taxonomic characters the female
Cosmocercidae Railliet, 1916 could not be
determined to genus and species.
Acanthocephalans were not determined to the
specific level because no males were found.
Besides the characteristics of the proboscis, it
is necessary to observe the morphology and the
n u m b e r o f c e m e n t g l a n d s o f
Pseudoacanthocephalus species.
Of the 60 anurans collected, only 18 were
infected with parasite species. Nematodes
accounted for 80% of the sample (three
species), and 20% were represented by one
acanthocephalan species. A total of 23
nematodes and 12 acanthocephalans were
collected. The nematodes infected 15 hosts
while acanthocephalans infected only three
hosts.
Only Cosmocercidae females showed
prevalence greater than 10% and were the
dominant parasites (d = 0.47) of the sample.
There was no influence of the sex of the host on
coloration of the vocal sac (dark in males) and
gonad examination of juveniles.
Helminths were collected and placed in
physiological saline solution 0.65%; they were
fixed, stained and/or diaphanized following
Amato & Amato (2010). The morphologic and
biometric study was performed using an
Axiolab Zeiss microscope. The ecological
descriptors, prevalence, infection intensity,
parasite abundance and richness followed
Bush et al. (1997).
Statistical analysis included only the parasite
species with prevalence greater than 10%
(Bush et al., 1997). The Mann-Whitney "U"
test was calculated to evaluate if the sex of the
host was influenced by parasite abundance and
richness. Fisher's exact test was used to
evaluate if the host's sex and size influenced
parasite prevalence. To evaluate if host size
could influence the prevalence of helminth
species, anurans were categorized as small or
large frogs.
The Spearman correlation coefficient (r )
s
evaluated the influence of size on the parasite
abundance and richness of the analyzed
helminth hosts. The Berger-Parker index (d)
was used with a numerical measure of
dominance (Nering & Von Zuden, 2010). The
representativity of helminth species richness
found was analyzed with the program
EstimateS 8.0 (Colwell, 2009) through the
collectors curve and the Chao 1 Index and ACE
("Abundance-based Coverage Estimator"),
estimators based on abundance that quantify
rarity, and estimators based on incidence, ICE
("Incidence Coverage Estimator-based") and
Jackknife. Female Cosmocercidae were not
considered in the species richness
representativity analysis since these specimens
did not show diagnostic characters that allow
separation between Cosmocerca and
Aplectana.
Representative helminth specimens were
Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016
RESULTS
Parasite of the tree frog Scinax fuscovarius
44
The collector curve (SOBs) did not reach the
asymptote; on the other hand, the estimators
used ACE, ICE, Chao 1 and Jacknife reached
stability (Figure 1), which indicates that 80%
to 100% of helminth species were sampled in
this study.
the prevalence (p = 0.30), abundance (“U” =
372; p = 0.34) and parasite richness (“U” =
436; p = 0.85), and the host size did not
influence the prevalence (p = 0.49), abundance
(r 0.14; p = 0.27) and parasite richness (r=
s = s
0.17; p = 0.19).
Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Santos et al.
Figure 1. Accumulated richness observed (SOBs) and estimated (ACE, Chao 1, ICE and Jacknife) of the helminth community of
Scinax fuscovarius, Campo Belo do Sul, State of Santa Catarina, Brazil.
Table 1. Prevalence, intensity, mean intensity, mean abundance and infection site of parasite helminths of Scinax
fuscovarius (n = 60), Campo Belo do Sul, State of Santa Catarina, Brazil.
Parasites Prevalence
Intensity
Mean
intensity Mean
abundance Infection site
(%)
±SD ±SD
Acanthocephala
Pseudoacanthocephalus sp.
5
1 to 8
4,00 ± 3,61 0,2 ± 1,10 Small intestine
CHIOC 38283; 38284
Nematoda
Cosmocercidae
16,6
1 to 2
1,80 ± 1,87 0,3 ± 1,00 Small/large
intestine
CHIOC 38157
Cosmocerca parva
2
1
1 0,03 ± 0,18 Small/large
intestine
CHIOC 38158
Cosmocerca brasiliense 2 1 1 0,03 ± 0,18 Small/large
intestine
CHIOC 38159
Physaloptera sp. (larvae) 1,66 1 1 0,02 ± 0,13 Stomach
CHIOC 38160
CHIOC = Helminth Collection of Instituto Oswaldo Cruz, with the numbers of representative specimens.
0
1
2
3
4
5
6
7
8
1 2 3 4 5 6 7 8
Species richness
Number of hosts
Sobs
ACE
Chao 1
ICE
Jacknife
45
Rhinella icterica
Terrestrial
Leptodactylus latrans
Semi-aquatic
Physalaemus cuvieri
Terrestrial
Scinax
fuscovarius
Arboreal
Digenea
Digenea
Digenea
Acanthocephala
Catadiscus cohni
Catadiscus cohni
Metacercária
(larva)
Pseudoacanthocephalus sp.
Rudolphitrema rudolphi
Catadiscus pygmaeus
Eucestoda
Nematoda
Eucestoda
Catdiscus inopinatus
Cylindrotaenia americana
Cosmocercidae
Cylindrotaenia americana
Catadiscus uruguayensis
Monogenea
Cosmocerca parva
Plerocercóide
(larva)
Gorgoderina parvicava
Polystoma cuvieri
Cosmocerca brasiliense
Acanthocephala
Gorgoderina megacysta
Nematoda
Physaloptera sp. (larva)
Cistacanto (larva)
Choledoscystus elegans
Strongyloides sp.
Nematoda
Rauschiella linguatula
Cosmocercidae
Strongyloides sp.
Eucestoda
Cosmocerca rara
Rhabdias fuelleborni
Cylindrotaenia americana
Cosmocerca parva
Cosmocercidae
Plerocercóide
Cosmocerca cruzi
Cosmocerca rara
Nematoda
Aplectana elenae
Cosmocerca brasiliense
Aplectana elenae
Oxyascaris oxyascaris
Nematoide não identificado
Strongyloides sp.
Rhabdias elegans
Cosmocercidae
Cosmocerca rara
Cosmocerca parva
Cosmocerca cruzi
Cosmocerca brasiliense
Aplectana elenae
Oxyascaris oxyascaris
Table 2. Parasite richness of anurans collected in the municipality of Campo Belo do Sul, State of Santa Catarina, Brazil.
Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Parasite of the tree frog Scinax fuscovarius
46
prevalence.
In this study, the three parasite species (C.
brasiliense, C. parva and Physaloptera sp.)
showed low prevalence and infection intensity.
On hylids the low vagility and the arboreal
habit probably contributes to a low infection
occurrence by nematodes with cutaneous
penetration (Hamann et al., 2010).
The genus Pseudoacanthocephalus
Petrochenko,1956 includes only parasite
species of amphibians and reptiles. In South
A m e r i c a , t h e r e a r e r e c o r d s o f
Pseudoacanthocephalus lutzi (Hamann, 1891)
(= Acanthocephalus lutzi (Hamann, 1891); =
Acanthocephalus saopaulensis Smales, 2007)
in Brazil (Hartwich, 1956; Pinhão et al., 2009),
Argentina (Lajmanovich & Ferrato, 1995),
Peru (Tantaléan, 1976), Uruguay (Cordero,
1933; Hartwich, 1956) and Paraguay (Smales,
2007). The infection by this acanthocephalan
occurs by the ingestion of an arthropod;
Arredondo & Pertierra (2009) suggest that
aquatic insects are the intermediate hosts of P.
lutzi.
Hamann et al. (2010) analyzed the parasite
community structure of Scinax nasicus from
Corrientes, Argentina, and found that this host
had high richness of helminth parasite species,
with 21 species. However, only seven species
were adult forms while the others were larval
forms. The results observed by these authors
demonstrate the important role that this anuran
species plays in the food chain, occupying an
intermediate position between the parasite and
its definitive hosts (snakes, birds and
mammals).
Usually, the sex of the anuran does not
influence the structure of the parasite
community, once they are evenly distributed
between males and females. This pattern was
found on S. fuscovarius in which sex did not
influence the parasite richness, the helminth
prevalence and abundance. This result
Analysis showed that S. fuscovarius had low
parasite richness, which is probably related to
the species' habitat. The nematodes found
showed low prevalence and low infection
intensities, and most hosts were parasitized
with only one helminth species.
The parasite richness of S. fuscovarius is
different from those found in Rhinella icterica
(Spix, 1824) (Santos et al., 2013),
Leptodactylus latrans (Steffen, 1815) and
Physalaemus cuvieri Fitzinger, 1826,
collected on the same area (Table 2); all four
species have distinct habits. However, the
result obtained in this study corroborates
Hamann & Kehr (1998), Bursey et al. (2001),
Goldberg et al. (2002) and González &
Hamann (2008), which also found low values
of parasite richness on hylid anurans of South
America.
The nematode species C. parva and C.
brasiliense found in this study have direct
cycles (monoxenous) and infect their hosts
through cutaneous penetration. Species of
Physaloptera have an indirect cycle
(heteroxenous) and are commonly found in
anurans which, according to Anderson (2000),
act as paratenic hosts for Physaloptera species,
while lizards, snakes and mammals act as
definitive hosts.
According to Bursey et al. (2001), C.
brasiliense is the most common and greater
prevalence parasite species found on arboreal
anurans. Goldberg et al. (2007) working in the
State of Pará, Brazil found low prevalence
(10%) and an intensity equal to 1 for the
parasite C. brasiliense in the species
Dendropsophus cachimbo (Napoli and
Caramashi, 1999). González & Hamann
(2008) found C. parva and Physaloptera sp.
(larval form) in Scinax acuminatus at
Corrientes, Argentina, which also showed low
DISCUSSION
Neotropical Helminthology. Vol. 10, Nº1, ene-jun 2016 Santos et al.
47
Etiele Senna. To “Florestal Gateados” for
allowing the collection of specimens on their
property. Phillip J. Scholl for kindly reviewing
the English version To CAPES for the
scholarship granted to the first author. To
FAPERGS for the financial support granted to
this research.
.
corroborates other studies (Yoder & Coggins,
1996; McAlpine, 1997; Barton, 1999;
Goldberg et al., 2002; Hamann et al., 2006a,b;
Santos & Amato, 2010; Santos et al., 2013).
On the other hand, some authors suggest that
the host size influences the parasite richness
and the helminth prevalence and abundance
(Baker, 1984; McAlpine, 1997; Gillilland &
Muzzall, 1999; Bolek & Coggins, 2003; Chero
et al., 2016). In this study, however, this
correlation was not observed, since size did not
influence the parasite community structure of
S. fuscovarius, this result corroborates with
Chero et al. (2014). This result may indicate
that, regardless of size, all individuals are
susceptible to infection by Cosmocercidae.
The estimators did not reach an asymptote and
this result may be related to the low number of
infected anurans, but the estimated values did
not extrapolate and remained close to
observed. The parasite richness of S.
fuscovarius is, probably, between four and five
species.
The results obtained in this study was
corroborated by Hamann et al. (2010) who
suggested that the sit-and-wait strategy and the
particular diet of these anurans are determining
factors for the low parasite richness found. The
limited movement and the arboreal habit of
this species also contribute to the low
occurrence of nematodes that parasitize
anurans through cutaneous penetration. The
absence of digenetic is probably related to the
little contact of these anurans with the aquatic
environment.
Authors would like to thank the herpetologists
Rafael Balestrin, Patrick Colombo, Martin
Schossler, Daniel Bühler and Simoni Leonardi
for field assistence, and to Mariana Gliesh and
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Received February 22, 2016.
Accepted March 24, 2016.
