ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2019, 13(1), ene-jun:9-15.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
A NEW SPECIES OF COSMOCERCA (NEMATODA: ASCARIDIDA: COSMOCERCIDAE) FROM
GYMNOPHTHALMID LIZARDS OF WESTERN BRAZIL
UNA NUEVA ESPECIE DE COSMOCERCA (NEMATODA: ASCARIDIDA: COSMOCERCIDAE) DE
SAURIOS GIMNOFTÁLMIDOS DEL OESTE DE BRASIL
1Departamento de Química Biológica, Universidade Regional do Cariri – URCA, R. Cel. Antônio Luiz, 1161, Pimenta, CEP
63105-000, Crato, CE, Brazil. ORCID: 0000-0003-3641-8321
2UNESP – Univ Estadual Paulista, Campus de Botucatu, Instituto de Biociencias, Departamento de Parasitologia – Av. Bento
Lopes s/n. Distrito de Rubião Junior, CEP 18618-970 Botucatu, SP, Brasil. ORCID: 0000-0002-3426-6873
* Corresponding author: robsonavila@gmail.com
1,* 2
Robson Waldemar Ávila & Reinaldo José Da Silva
ABSTRACT
Keywords: Cosmocerca gymnophthalmicola n. sp. - Gymnophthalmidae - Neotropical - New species - Sauria - Squamata
Cosmocerca gymnophthalmicola n. sp., an intestinal parasite of the gymnophthalmid lizards
Alopoglossus angulatus (Linnaeus, 1758) and Cercosaura eigenmanni (Griffin, 1917) from western
st
Brazil is described and illustrated. Cosmocerca gymnophthalmicola n. sp. represents the 31 species
th
assigned to the genus, and the 11 to be reported in the Neotropical region. Moreover, C.
gymnophthalmicola n. sp. is the fourth species reported from lizard hosts, and is distinguished from other
species of the genus Cosmocerca by possessing 6 pairs of plectanes and by a combination of spicule and
gubernaculum length and by the absence of lateral alae in both sexes. The new species is more similar to C.
banyulensis, C. chilensis, C. longicauda, C. parva and C. rara in having 6 pairs of plectanes, but differ
from these species by larger spicules and absence of lateral alae in both sexes.
Neotropical Helminthology
9
Volume13,Number1(jan-jun2019)
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
Auspiciado por:
RESUMEN
Palabras clave: Cosmocerca gymnophthalmicola n. sp. - Gymnophthalmidae - Neotropical - Nueva especie - Sauria - Squamata
En este artículo se describe e ilustra a Cosmocerca gymnophthalmicola n. sp., un parásito intestinal de los
lagartos gimnoftálmidos Alopoglossus angulatus (Linnaeus, 1758) y Cercosaura eigenmanni (Griffin,
1917) del oeste de Brasil. Cosmocerca gymnophthalmicola n. sp. representa la 31ª especie asignada al
a
género, y la 11 en la región Neotropical. Por otra parte, C. gymnophthalmicola n. sp. es la cuarta especie
que tiene hospederos lagartos, y se distingue de otras especies del género Cosmocerca por poseer 6 pares
de plectanas y por una combinación de espículas y gubernáculo y por la ausencia de alas laterales en
ambos sexos. La nueva especie es más similar a C. banyulensis, C. chilensis, C. longicauda, C. parva y C.
rara en tener 6 pares de plectanas, pero se diferencian de estas especies por espículas más grandes y
ausencia de ala lateral en ambos sexos.
The nematode genus Cosmocerca Diesing, 1861 is
composed by 30 species (Bursey et al., 2015; Sou
et al., 2018). They are distributed worldwide, and
the Neotropical region harbors one third of the
known species, mostly described from amphibian
hosts (see Bursey et al., 2005; 2015).
To date, three species of Cosmocerca have been
described from lizard hosts, with two being from
gekkonids: C. zugi Bursey, Goldberg & Kraus,
2005 from Cyrtodactylus louisiadensis (De Vis,
1892) and C. leytensis Bursey, Goldberg, Siler &
Brown, 2015 from Cyrtodactylus gubaot Welton,
Siler, Linkem, Diesmos & Brown 2010 and C.
vricibradici Bursey & Goldberg, 2004 from the
gymnophthalmids Cercosaura (=Prionodactylus)
eigenmanni (Griffin, 1917) and C. oshaughnessyi
(Boulenger, 1885) (Bursey & Goldberg, 2004;
Bursey et al., 2015). The last species was described
from Ecuador and the Brazilian states of Rondonia,
Acre and Amazonas (Bursey & Goldberg, 2004),
neighbor states of Mato Grosso, where during
parasitological surveys we found an undescribed
species of Cosmocerca from gymnophthalmids,
which is described herein.
Three adult specimens of Alopoglossus angulatus
(Linnaeus, 1758) (mean snout vent length = 50.20
mm, standard deviation 7.72 mm) and nine adult
specimens of Cercosaura eigenmanni (Griffin,
1917) (mean snout vent length = 34.86 mm,
standard deviation 5.48 mm) were analyzed. All
lizards were collected by hand, between May and
October 2002, during a faunal rescue program at
the site of construction of the reservoir of Guaporé
hydroelectric power plant, Vale de São Domingos
municipality, Mato Grosso State, Brazil.
Helminths found in the small and large intestine of
the lizards were fixed in a solution of alcohol-
formalin-acetic acid, cleared in lactophenol and
examined using an optical microscope.
The holotype and allotype of the new nematode
species described here were deposited in the
10
INTRODUCTION Coleção Helmintológica of the Instituto Oswaldo
Cruz (CHIOC 35867a and 35867b, respectively),
Rio de Janeiro State, Brazil. Paratypes were
deposited in the Coleção Helmintológica of the
Departamento de Parasitologia, Instituto de
Biociências (CHIBB 3122, 3128, 3130, 3136, 3138
and 3141), Universidade Estadual Paulista -
UNESP, Botucatu municipality, São Paulo State,
Brazil. Morphology was studied using a
computerized system of image analysis (LAS DIC,
Leica Microsystems, Wetzlar, Germany) and
illustrations were made with the aid of a drawing
tube in a Leica microscope.
The host lizards were fixed in 10% formalin,
preserved in 70% ethanol and deposited in the
Coleção Zoológica da Universidade Federal de
Mato Grosso, Cuiabá municipality, Mato Grosso
State, Brazil (A. angulatus – UFMT 5727, 5730 and
5735; C. eigenmanni - UFMT 842, 844, 845, 857,
5055, 5061, 6064, 5065 and 5067).
Morphological data are generally presented as
mean ± 1 standard deviation (minimum and
maximum) values. Measurements in µm, unless
otherwise noted.
This study was approved by the ethics committee
o f U n i v e r s i d a d e R e g i o n a l d o C a r i r i
(CEUA/URCA, process No. 00260/2016.1).
Necropsy revealed 14 nematodes in the small and
large intestine of 5 lizards. Two adult females of A.
angulatus had 1 and 4 nematodes each, and two
adult males and one female of C. eigenmanni
harbored three nematodes each. The nematodes
were found in the small and large intestine of 2
from the 3 examined specimens of A. angulatus, a
prevalence of 66.7%, and of 3 from the 9 examined
specimens of C. eigenmanni, a prevalence of
33.3%. After careful examination and comparison
with available descriptions of congenerics, it
became clear that nematodes found in A. angulatus
and C. eigenmanni belong to a previously
undescribed species of Cosmocerca.
Neotropical Helminthology, 2019, 13(1), ene-jun
MATERIALS AND METHODS
RESULTS
Ávila & da Silva
Cosmocerca gymnophthalmicola n. sp.
(Figs. 1A–D, 2)
Description: Small nematodes, with males smaller
than females. Lateral alae absent in both male and
females. Cuticle transversely striated. Mouth with
three lips, with the dorsal lip bearing two large
submedian papillae and the two ventrolateral lips
with one submedian papillae and one amphid each.
Esophagus starting with a short pharynx, elongated
body, small isthmus and valved bulb. Excretory
pore situated above the bulb in both male and
females. Tapered conical tail in both sexes. Male
with 2 large spicules, a relatively small
gubernaculum and two rows of plectanes on
ventral surface.
11
Male (Figs. 1B, D; 2) based on 1 adult specimen
(Holotype, CHIOC 35867a): Length 2.2 mm;
width at midbody 171.7. Esophagus 260.7 long:
pharyngeal portion 34.8 long, corpus 225.9 long,
bulb length 86.9; bulb width 95.8. Nerve ring 40.8;
excretory pore 142.8 from anterior end. Tail 145.3
long, flexed ventrally. Spicules equal, heavily
sclerotized at anterior portion, 266.1 long, width at
distal portion 5.4. Gubernaculum V-shaped, 108.3
long, anterior portion heavily sclerotized with
width 10.8. Posterior end with six pairs of preanal
plectanes (Fig. 1D), with the last pair 52.8 from
anal aperture. Six plectanes on each side, disposed
parallel to long axis of body, consisting of complete
rosettes of 15–16 punctuations and underlying
supports (Fig. 2). One pair of rosette papillae closer
Figure 1. Cosmocerca gymnophthalmicola n. sp. (A) female allotype. Scale bar = 200 µm. (B) male holotype. Scale bar = 100 µm.
(C) anterior end of female, lateral view. Scale bar = 50 µm. (D) posterior end of male, ventral view. Scale bar = 50 µm. (E)
posterior end of male, lateral view. Scale bar = 50 µm.
Neotropical Helminthology, 2019, 13(1), ene-jun A new species of Cosmocerca
to the first pair of plectanes and 7 pairs of simple
papillae: One preanal pair closer to last pair of
plectanes; one adanal pair in the anterior lip of
anus; five postanal simple papillae, with 1
subdorsal pair and 4 ventral papillae (being two just
before the tail filament and two in the middle of tail
filament).
Female (Fig. 1A, C), based on 5 adult specimens
CHIOC 35867b, CHIBB 3130: Length 3.7 ± 0.9
mm (3.1–4.9 mm); width at midbody 279 ± 120.6
(197–458). Esophagus 314 ± 75 (262.8–425.6)
12
long; pharyngeal portion 58.3 ± 13.3 (47.6–77.6)
long, corpus 313.9 ± 75.1 (262.8–425.6) long, bulb
length 94.4 ± 11.1 (82.1–104.1); bulb width 107.7
± 23.1 (93.6–142.1). Nerve ring 93.2 ± 29.8
(71.5–136.6) from anterior end. Excretory pore
231.8 ± 48.7 (171.6–279.3) from anterior end.
Uteri prodelphic. Vulva 2.0 ± 0.4 mm (1.8–2.0)
from anterior end. Eggs (N = 20) oval, thin-shelled
with embryos, 57.8 ± 7.8 (42.9–68.0) long, 35.2 ±
3.9 (28.4–42.1) wide. Tail 243.6 ± 28.3
(231.7–267.6) long.
Figure 2. Plectanes ornamentation in Cosmocerca gymnophthalmicola n. sp. , ventral view.
Neotropical Helminthology, 2019, 13(1), ene-jun Ávila & da Silva
Taxonomic summary. Type host: Alopoglossus
angulatus (N ); Deposited in the orthern teiid
Universidade Federal de Mato Grosso (UFMT
5730); Collection date 3 October 2002.
Additional host: Cercosaura eigenmanni
(Eigenmann's Prionodactylus).
Type locality: Vale de São Domingos municipality,
Mato Grosso state, Brazil, longitude 58º 58' W,
latitude 15º 07' S.
Site of infection: Small and large intestine.
Voucher specimens: Instituto Oswaldo Cruz, Rio
de Janeiro, RJ, Brazil; Holotype No. CHIOC
35867a, adult male; Allotype No. CHIOC 35867b,
adult female; Coleção Helmintológica do Instituto
de Biociências, Botucatu, SP, Brazil; Paratypes, 4
adult females, CHIBB 3130, 1 juvenile female,
CHIBB 3136, 3 juvenile females, CHIBB 3138, 3
juvenile females, CHIBB 3128 and 2 juvenile
females, CHIBB 3122.
Etymology: The new species is named in reference
t o i n f e c t i n g l i z a r d m e m b e r s o f t h e
Gymnophthalmidae family.
From the other Cosmocerca species, the new
species is promptly distinguished from 18 species,
including six Australian and Oceanian species (C.
archeyi, C. australis, C. limnodynastes, C.
novaguineae, C. oroensis and C. zugi), one
Nearctic (C. acanthurum), four Neotropical (C.
cruzi, C. paraguayensis, C. podicipinus, and C.
travassosi), two Paleartic (C. sardiniae and C.
ornata), four Oriental (C. bengalensis, C. kalesari,
C. leytensis and C. microhylae) and one Sino-
Japanese species (C. japonica) by possessing 6
pairs of plectanes instead of 3–5 pairs of plectanes.
Three species have number of plectanes higher
than the new species, the Neotropical C.
brasiliense (9 to 11 pairs; Travassos, 1931), the
Oceanian C. tyleri (9 pairs) and the Oriental C.
ishaqui (11 pairs) (Bursey et al., 2015; Sou et al.,
2018).
Besides the number of plectanes (seven pairs), two
Neotropical (C. uruguayensis, and C. vrcibradici),
one Panamanian (C. longispicula) and one
Paleartic species (C. commutata) have the spicule
size smaller than the new species species (155–180
13
DISCUSSION
µm) except C. longispicula (Bursey et al., 2015).
Cosmocerca gymnophthalmicola n. sp. can also be
distinguished from C. longispicula by both smaller
size of spicules and gubernaculum (300 and 138
µm in C. longispicula; Moravec & Kaiser, 1994),
absence of lateral alae (present in C. longispicula;
Moravec & Kaiser, 1994) and also by lesser
somatic papillae number (numerous in C.
longispicula; Moravec & Kaiser, 1994) and size of
eggs (72–81 µm long, 45–48 µm wide in C.
longispicula; Moravec & Kaiser, 1994).
Finally, five species are known to possess 6 pairs of
plectanes (Bursey et al., 2015): three from
Neotropical region (C. chilensis, C. parva and C.
rara) and two from the Paleartic (C. banyulensis
and C. longicauda). Of these, C. parva, C. rara and
C. banyulensis have variable number of plectanes
(5–7 in C. parva, 6–7 in C. rara and 5–6 in C.
banyulensis), but as we found only one male we do
not know if there is variation in the number of
plectanes in the new species; however, the new
species can be differentiated from these species by
the larger spicules (90–110 in C. parva, 200 in C.
rara and 10 in C. banyulensis), absence of lateral
alae (present in both C. parva, C. rara and C.
banyulensis), and gubernaculum length (larger
than C. parva with 95–108 and 80 in C. banyulensis
and smaller than C. rara with 206; Mordeglia &
Digiani, 1998; Bursey et al., 2005). Cosmocerca
gymnophthalmicola n. sp. can be distinguished
from C. chilensis by the larger spicule (80; Bursey
et al., 2015) and by possessing 7 pairs of simple
papillae, being one preanal, one adanal and five
postanal (numerous preanal, two adanal and four
postanal in C. chilensis, Lent & Freitas, 1948).
From C. longicauda, the new species is
distinguished by possessing larger spicule (92) and
smaller gubernaculum (190) and also by absence of
lateral alae (present; Bursey et al., 2015).
th
Cosmocerca gymnophthalmicola n. sp. is the 31
th
species assigned to the genus, and the 11 species
recorded for the Neotropical region (Falcón-Ordaz
et al., 2007; Bursey et al., 2015; Sou et al., 2018).
Species of Cosmocerca are known to infect mainly
frogs (over 88% of the species; see Bursey et al.,
2005, 2013), and C. gymnophthalmicola n. sp. is
the fourth species of the genus reported to have a
reptilian definitive host. Species of Cosmocerca
are monoxenous, with larvae actively infecting the
hosts by penetration of integument (Anderson,
Neotropical Helminthology, 2019, 13(1), ene-jun A new species of Cosmocerca
14
2000). Bursey & Goldberg (2004) suggested that
high prevalence of infection by Cosmocerca in
gymnophthalmid lizards is due to time spent in wet
leaf litter by these hosts. The recently discovery of
many species of cosmocercids infecting
gymnophthalmid lizards elsewhere in South
America (e.g. Cosmocercoides sauria in Iphisa
elegans – Ávila et al., 2010; Cosmocerca
vrcibradici in Alopoglossus angulatus, and A.
atriventris – Goldberg et al., 2007) may
corroborate this prediction.
We are grateful to Marcos André de Carvalho, who
provided access to lizards for dissection. This study
had financial support by FAPESP (#2016/50377-
1). RWA thanks Conselho Nacional de
Desenvolvimento Científico e Tecnológico
(CNPq; CNPq-PROTAX #440496/2015-2). #
309125/2017-O). Finally, we thank Paulo Emilio
Santos Costa for the final artwork.
ACKNOWLEDGEMENTS
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g e n u s , n e w s p e c i e s o f C e s t o d a
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