ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2020, 14(2), jul-dic:175-181.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
INTESTINAL HELMINTHS OF HYLODES HEYERI HADDAD, POMBAL & BASTOS, 1996
(ANURA: HYLODIDAE) IN THE ATLANTIC FOREST, BRAZIL
HELMINTOS INTESTINALES DE HYLODES HEYERI HADDAD, POMBAL & BASTOS, 1996
(ANURA: HYLODIDAE) EN EL BOSQUE ATLÁNTICO, BRASIL
1Setor de Parasitologia, Instituto de Biociências, Campus de Botucatu, Universidade Estadual Paulista (UNESP), R. Prof. Dr.
Antônio Celso Wagner Zanin, 250, Distrito de Rubião Junior, CEP 18618-689, Caixa Postal 510, Botucatu, SP, Brazil.
2Instituto de Biologia, Universidade Federal da Bahia, Campus de Ondina, Salvador, BA 40170-115, Brazil.
3Universidade Federal de Uberlândia – UFU, Instituto de Ciências Agrárias, LMG-746, Km 1, Monte Carmelo, 38500-000,
MG, Brazil.
*Corresponding author: ednnapaulino@gmail.com
1* 1 2 3
Edna Paulino de Alcantara ; Cristiana Ferreira Silva ; Lucas Rodriguez Forti ; Drausio Honorio Morais &
1
Reinaldo José da Silva
Neotropical Helminthology
175
doi:10.24039/rnh2020142753
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
Volume14,Number2(jul-dec)2020
ABSTRACT
Cosmocercid nematodes are common parasites of amphibians and reptiles. Although it is a well-known
family, knowledge about its host diversity is lacking. Herein, we expand the knowledge of the anuran
parasitic fauna of the family Hylodidae and the geographic distribution of three species of cosmocercid
nematodes (Cosmocerca brasiliensis Travassos, 1925, Cosmocercoides sauria Strüssmann & Ávila,
Silva, 2010, and an unidentified cosmocercid species) found in two male torrent frogs Hylodes heyeri
Haddad Pombal & Bastos, 1996 Our report includes new data on the geographic distribution and the .
morphology of cosmocercid parasites and further enlightens the parasitic interactions of Neotropical
amphibians.
Keywords: amphibians – Cosmocercidae – endoparasites – Nematoda – new host
RESUMEN
Los nematodos cosmocercidos son parásitos comunes de anfibios y reptiles. Aunque es una familia bien
conocida, falta conocimiento sobre la diversidad de sus hospederos. En este documento, ampliamos el
conocimiento de la fauna parasitaria de anuros de la familia Hylodidae y la distribución geográfica de tres
especies de nematodos cosmocercidos (Cosmocerca brasiliensis Travassos, 1925, Cosmocercoides
sauria Ávila, Strüssmann & Silva, 2010 y cosmocercid) encontrados en dos ranas torrentes macho
Hylodes heyeri Haddad Pombal & Bastos, 1996. Nuestro reporte incluye nuevos datos sobre la
distribución geográfica y la morfología de los parásitos cosmocercidos y aclara aún más las interacciones
parasitarias de los anfibios neotropicales.
Palabras clave: anfíbios – Cosmocercidae – endoparasitos – nematoda – nuevos hospedadores
Both collected specimens of H. heyeri were
infected with at least one helminth parasite. In the
RESULTS
176
th
On September 16 , 2017, we collected two
specimens of H. heyeri by hand during visual
encounter surveys in two localities from São Paulo
State: one adult male specimen (snout-vent length
[SVL] 38.5 mm) from Parque Estadual da Caverna
do Diabo (-24.636329°S, -48.403442°W) in the
th
municipality of Eldorado and on September 13 ,
2017, and another adult male specimen (SVL 42
mm) from Parque Estadual do Turístico do Alto
Ribeira (-24.533361S°, -48.699261°W) in the
municipality of Iporanga, São Paulo State,
Southeast Brazil.
We searched all internal organs for helminths using
a stereoscope, soon after the frogs were euthanized.
After this, the hosts were fixed in 10% formalin,
preserved in 70% alcohol, and deposited at Museu
de Zoologia “Prof. Adão José Cardoso” at the
Universidade Estadual de Campinas (Unicamp),
Campinas, São Paulo, Brazil (under the codes
ZUEC-AMP 24061 and ZUEC-AMP 24023). The
nematodes found were cleared with lactophenol
and the taxonomic determination was conducted
by comparing morphological traits with published
descriptions (Vicente et al., 1991, Anderson et al.,
2009, Gibbons, 2010).
Voucher helminth specimens were deposited in the
Helminthological Collection of the Institute of
Biosciences, São Paulo State University – UNESP
(CHIBB), in the municipality of Botucatu, São
Paulo, Brazil.
Ethics aspects: The collections were authorized by
Instituto Chico Mendes de Conservação da
Biodiversidade – ICMBIO for collecting
permission (ICMBio permit 57611-2). The
procedures were approved by the Ethics
Committee on the Use of Animals (CEUA #126) of
the Institute of Biosciences, São Paulo State
University – UNESP.
Nematodes are typical macroparasites of
amphibians (Koprivnikar 2012). The et al.,
interaction between these two animal groups is an
outcome of their coevolutionary history and the
biological constraints of host species (Campião et
al., 2016). Unfortunately, we have a long way to go
to a comprehensive perspective on the complexity
of the interactive network between frogs and
helminths. One important step to reduce this gap is
by searching for descriptive notes about the
occurrence of hosts, which also generates data on
the geographical ranges of the parasites (Toledo et
al., 2018).
While Cosmocercidae nematodes are a common
parasite of amphibians (Campião 2014), the et al.,
list of hosts they interact with is not fully known.
Therefore, focusing on poorly studied groups of
frogs in parasite research is a promising approach
to reveal new interactions (Campião ., 2015).et al
Here we study helminths in a torrent frog species of
the family Hylodidae, which is composed of 47
species (Segalla 2019). (Fitzinger, et al., Hylodes
1826) is the most diverse genus of Hylodidae and
includes 26 species, all endemic to Brazil (Frost et
al., et al., Hylodes heyeri 2020; Segalla 2019).
Haddad Pombal & Bastos, 1996 was described
from the municipality of Eldorado, São Paulo
State, but occurs in other localities in Paraná and
Santa Catarina State (Lingnau, 2004; Araújo et al.,
2010; Monteiro et al., 2014). It is a diurnal species
exhibiting vocal activity and visual signals on
rocks of typical Atlantic forest streams (Haddad et
al., 1996; Lingnau & Bastos, 2007; de Sá et al.,
2016).
Despite the high number of Hylodidae species,
their parasites are rarely studied, with only one
report of a filarial parasite infecting H. heyeri
(D'Bastiani 2018).et al.,
Here we describe the infection of with H. heyeri
cosmocerciid nematode species, expanding our
knowledge of the anuran parasitic fauna of the
family Hylodidae and the geographic distribution
of these helminths. Besides, we provide a brief
morphological description of cosmocerciid
parasites.
INTRODUCTION
Neotropical Helminthology, 2020, 14(2), jul-dic
MATERIAL AND METHODS
Paulino-de-Alcantara et al.
177
small intestine of the individual from Iporanga, we
found one specimen of Cosmocerca brasiliensis
Travassos, 1925 (CHIBB 8852). The nematode had
a small and slender body, spicules of 210.9 mm,
gubernaculum measuring 195.3 mm, and three
precloacal and four postcloacal pairs of caudal
papillae, and 11 pairs of rosettes (Figure 1; Table
1). More detailed morphometry was not
performed, because the anterior part of the body
was cut and separated for later molecular analysis,
which unfortunately was not successful. However,
the measurements performed on the posterior part
of the body were consistent with previous C.
brasiliensis description (Table 1).
In the large intestine of the host specimen from
E l d o r a d o , w e f o u n d o n e a d u l t m a l e
Cosmocercoides sauria Ávila, Strüssmann &
Table 1. Morphometric comparison of Cosmocerca brasiliensis. All measurements are in micrometers, except where
stated.
Parameter Present study Data from
Travassos (1931)
Data from
Dyer & Altig (1976)
Sex (N = individuals)
Male
(N=1)
Male
Female
Male
(N=5)
Female
(N=8)
Length (mm)
-
5.5
9
2.24–3.99
9.67–12.67
Width -
52
96
180–270
320-490
Pharyngeal portion
-
48–72
48–72
39–47
68–81
Esophagus
-
60–92
060–92
400–509
780–960
Corpus -
- - - -
Istimus -
- - - -
Bulb -
100–170 100–170
78–96
140–169
Excretory pore
-
- - 258–390
450–660
Nerve ring
-
- - 122–231
260–327
Spicules
210.9
150–200 - 158–185
-
Gubernaculum
195.3
- - 140–156
-
Rosette 11 pares
9-11 pairs - 8 pairs
-
Caudal papillae
0:3:4
-
-
Anus -
28-32
56-70
-
-
Vulva from anterior end
(mm)
-
-
-
-
3.8-5.1
Tail 228.8
-
-
530- 740
Eggs - - 0.90 x 54 - 62-93 x 31
55
Neotropical Helminthology, 2020, 14(2), jul-dic Helminths of Hylodes heyeri
Silva, 2010 (CHIBB 8853) and seven adult
cosmocerciid females (CHIBB 8854). The C.
sauria male was 2.3 mm long and 205 mm wide at
midbody, with pharyngeal portion 20.4 mm long,
corpus 257.7 mm long, bulb length 55.3 mm, bulb
width 63.5 mm, nerve ring 103.6 from the anterior
extremity, excretory pore 174.8 mm from anterior
end. Its tapering tail was 59.5 mm long. Lateral
alae were present, gubernaculum 105.5 mm, equal
spicules 103.7 mm, and four pairs of rosette
papillae (Figure 2).
The seven cosmocerciid females presented 4.5–5.4
mm long and 409.3–506.2 mm wide, pharyngeal
portion 41.2–58.5 mm, esophagus total
693.6–720.1 mm, with corpus 484.7–498.8 mm,
isthmus 38.1–51,3 mm and bulb 99.7–124.8 x
135.7–151.9 mm, excretory pore 533.6–559.8
178
Figure 1. Posterior region of male Cosmocerca brasiliensis.
Figure 2. Posterior region of male Cosmocercoides sauria. Highlighted rossete.
Neotropical Helminthology, 2020, 14(2), jul-dic Paulino-de-Alcantara et al.
from anterior end, nerve ring 232.1–242 mm from
anterior end, vulva 2.2–3 mm from the anterior end, tail 374.5–401.8 mm long. Eggs were
63.6–73.6 x 33.7–47.4 mm (Figure 3).
179
brasiliensis parasitizing an anuran in São Paulo
State, expanding the geographical distribution of
this parasite and adding as a newly H. heyeri
reported host.
Cosmocercoides sauria has been described in the
small and large intestines of the gymnophtalmid
lizard Iphisa elegans elegans Gray, 1851 from the
municipality of Vale de São Domingos, Mato
Grosso State, Brazil (Ávila et al., 2010) and no
other report on the occurrence of this helminth has
been published. Therefore, here we report for the
first time the interaction between this parasite and
its amphibian host. Also, our record expands its
geographical distribution to the southeastern
region of Brazil.
In the same host infected with a male of C. sauria,
seven cosmocerciid adult female specimens were
also found. However, these females were not
identified as C. sauria since their morphometrical
data were inconsistent with the data reported by
this nematode species (Ávila et al., 2010) and so
characterizing a mixed infection.
Our results reinforce the necessity of more studies
on the parasitic fauna of Neotropical amphibians,
Our results contribute to the knowledge on the
parasitic interactions of Neotropical amphibians.
The three nematode taxa found in is an H. heyeri
important contribution to the poorly known
parasites of this frog family, as previously registers
of parasites in this species were limited to one
report of a filarial nematode (D'Bastiani et al.,
2018), while other helminth species have been
reported in other species of Hylodidae (Campião et
al., 2014).
Cosmocerca brasiliensis is an anuran intestinal
parasite and has been reported from Brazil,
Ecuador, Guayana, and Peru (Campião et al.,
2014). In Brazil, this nematode species was found
parasitizing the intestine of (Spix, Rhinella icterica
1824) in Santa Catarina State (Santos 2013)et al., ,
Dendropsophus cachimbo (Napoli & Caramaschi,
1999) in Pará State, and (Wied, 1821), Boana faber
Ischnocnema guentheri , (Steindachner, 1864)
Proceratophrys appendiculata (Günther, 1873),
Thoropa miliaris Rhinella (Spix, 1824), and
crucifer (Wied, 1821) in Rio de Janeiro State
(Campião 2014). This is the first record of et al., C.
DISCUSSION
Figure 3. Cosmocerciid female. (a-b) Anterior end, and (c-d) posterior end.
Neotropical Helminthology, 2020, 14(2), jul-dic Helminths of Hylodes heyeri
180
especially of hylodid frogs, a promising family to
find unknown host-parasites interactions.
We thank Joice Ruggeri for field assistance and
Judit Szabo for English review and improvements
on early versions of this manuscript. We thank
Conselho Nacional de Desenvolvimento Cientıfico
e Tecnológico (CNPq) for providing a research
fellowship for EPA (141322/2018-7), CFS
(140871/2017-9), DHM (313241/2018-0) and
R.J.S. (309125/2017-0). LRF (150041/2017-9),
and to the Coordination for the Improvement of
Higher Education Personnel (CAPES) for his
current post-doctoral fellowship.
ACKNOWLEDGMENTS
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