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ISSN Versión impresa 2218-6425
ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2021, 15(2), jul-dic:211-215.
RESEARCH NOTE / NOTA CIENTÍFICA
¹Interdisciplinary Animal Health Research Centre (CIISA), Faculty of Veterinary Medicine, University of Lisbon, 1300-
477 Lisboa, Portugal
²BW Institute. Rua Profa. Sueli Brasil Flores n.88, Praia Seca, Araruama, RJ (CEP) 28970-000, Brazil
*Corresponding author: max@bwvet.com.br
Bruna Cavaco: https://orcid.org/0000-0001-94594679
Luis Madeira de Carvalho: https://orcid.org/0000-0002-7548-667X
Lais Modolo Conti: https://orcid.org/0000-0002-5183-182X
Max Rondon Werneck: http://orcid.org/0000-0002-5650-3649
Bruna Cavaco¹; Luis Madeira De Carvalho¹; Lais Modolo Conti² & Max Rondon Werneck²*
ABSTRACT
This note reports the occurrence of
Charaxicephaloides polyorchis
Groschaft &Tenora, 1978 collected
from a green sea turtle -
Chelonia mydas
(Linnaeus, 1758) from Brazil. Our specimen is larger than the
original description and the following descriptions, provide new information on this species. This
represents the first record with morphometric data of
C. polyorchis
in a green turtle from Brazil and the
third record with morphometric data of this trematode.
Neotropical Helminthology
211
doi:10.24039/rnh20211521199
REPORT OF
CHARAXICEPHALOIDES POLYORCHIS
GROSCHAFT & TENORA 1978 (DIGENEA:
PRONOCEPHALIDAE) IN A GREEN TURTLE -
CHELONIA MYDAS
(LINNAEUS, 1758) FROM
BRAZIL
RELATO DE
CHARAXICEPHALOIDES POLYORCHIS
GROSCHAFT & TENORA 1978 (DIGENEA:
PRONOCEPHALIDAE) DE UNA TORTUGA VERDE-
CHELONIA MYDAS
(LINNAEUS, 1758) EN
BRASIL
D
D
D
D
Keywords
: Brazil –
Charaxicephaloides polyorchis
–
Chelonia mydas
– Pronocephalidae
RESUMEN
Esta nota informa la ocurrencia de
Charaxicephaloides polyorchis
Groschaft & Tenora, 1978
recolectados de una tortuga marina verde –
Chelonia mydas
(Linnaeus, 1758) de Brasil. Nuestros
ejemplares son más grandes que la descripción original y las siguientes descripciones, proporcionando
nueva información sobre esta especie. Esto representa el primer registro con datos morfométricos de
C.
polyorchis
en una tortuga verde de Brasil y el tercer registro con datos morfométricos de este trematodo.
Palavras-Chave
:
Brazil –
Charaxicephaloides polyorchis
–
Chelonia mydas
– Pronocephalidae
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212
The worms of Phylum Plathyelminthes, Class
Trematoda, include a wide range of parasites,
namely belonging to subclass Digenea, which can
be found in a wide sort of terrestrial and aquatic
hosts. Particularly, the family Pronocephalidae
Looss, 1899, belonging to these class and subclass,
includes trematodes found in aquatic and marine
reptiles and in marine fish from different parts of
the world. Currently, 22 genera are accepted and 12
are known in sea turtles (Blair, 2005; Worms,
2021).
The genus
Charaxicephaloides
Groschaft &
Tenora, 1978 includes a single species (species
type:
C. Charaxicephaloides polyorchis
Groschaft
& Tenora, 1978) and, until now, is considered a
species of specialist parasite, reported only in green
sea turtles, -
Chelonia mydas
Linnaeus, 1758, from
Cuba (Groschaft & Tenora, 1978), Costa Rica
(Santoro
et al.
, 2009) and Brazil (Gomes
et al
.,
2017). Despite that, there are only two reports with
morphometric data of this parasite to date (see
Groschaft & Tenora, 1978; Santoro
et al
., 2009),
being the present report, the third article to be
published with this information. This article aims
to expand the knowledge of
C. polyorchis
by
offering new morphometric data for the species.
A juvenile female turtle (sex determined during
necropsy by viewing the ovary) measuring 52.7 cm
in curved carapace length and weighing 14.45 kg
was found alive in Praia da Barra (21°01'36"S,
40°48'40"W), municipality of Marataízes in the
state of Espírito Santo, Brazil. The turtle died
during the transport to rehabilitation center, and a
necropsy was performed thereafter. Several
trematodes were found in the stomach and in
urinary bladder.
The collected trematodes were preserved with
ethanol 70%, stained with carmine, and cleared
with eugenol. Morphometric data was collected
with the aid of a Global optics light microscope
using the S-EYE software program. Measurements
INTRODUCTION
are reported in micrometers, except when
indicated, with the mean and standard deviation
followed by the range in parenthesis. The
helminths were deposited in the Helminthological
Collection of the Instituto Oswaldo Cruz (CHIOC
number 38928) in the state of Rio de Janeiro,
Brazil.
The identification used in this report followed the
taxonomic proposal presented by Blair (2005) and
comparisons were made with the original
description by Groschaft & Tenora (1978) and the
redescription by Santoro
et al.
(2009).
Ethic aspects:
For this study formal consent is not
required.
During the necropsy, eight specimens of
C.
polyorchis
(Fig. 1) were found in the stomach of the
green turtle.
Description (Table 1, Fig. 1): Elongated body with
tapered anterior region, and posterior region with 2
conical projections; cephalic collar well
developed; oral sucker subterminal; oesophagus
short, cecal bifurcation at the level of the cephalic
collar margin; ceca ending near the posterior end of
the body, presenting numerous diverticula at
regular intervals that go close to the side of the
body; follicular testes ovoid to rounded in two
rows, ventral to the ceca, from genital pore to the
vitellaria; separated genital pore, to the left of the
body, male slightly anterior; small and transversal
cirrus sac; ovary round, on the right side of midline,
at the level of the end of the vitellaria; Mehlis' gland
round, postovarian; uterus occupying the entire
medial area of the body, between the ovary and the
cirrus sac, its coils do not extend beyond the main
body of the cecum; eggs presenting numbers polar
filaments.
Other pronocephalids were found in the same host
individual: six specimens of
Cricocephalus albus
(Kuhl & van Hasselt, 1822) Looss, 1899 (CHIOC
38929), one specimen of
Pronocephalus obliquus
Looss, 1899 (CHIOC 38936) and three specimens
of
Desmogonius
baldassinae
Werneck, Conti &
Blair, 2021 in stomach and three specimens of
Cavaco
et al.
MATERIAL AND METHODS
RESULTS
Neotropical Helminthology, 2021, 15(2), jul-dic
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213
Pyelosomum cochlear
Looss, 1899 in urinary
bladder (CHIOC 38937).
All specimens of
C. polyorchis
analyzed in the
present report had an evident cephalic collar, in
addition to have testicular follicles arranged in
double rows on each side, not separated by uterine
coils. These findings are compatible with the data
previously published by Blair (2005), in addition to
coinciding with the original description (Groschaft
& Tenora, 1978) and its redescription (Santoro
et
al
., 2009).
DISCUSSION
Our specimens have more developed and
elongated cecal diverticula, when compared to the
drawings by Groschaft & Tenora (1978), but with
characteristics closer to those mentioned by
Santoro
et al
. (2009). In addition, the genital pore is
on the left side of the trematode, as in Santoro
et al.
(2009).
However, in our specimens the Mehlis` gland is
located posterior to the ovary as well as in the
originals of Groschaft & Tenora (1978), but it
differs from the positioning presented by Santoro
et
al.
(2009). In our view, this is a morphological
change within the species and this does not
compromise the identification of the analyzed
specimens.
Charaxicephaloides polyoschis
in a green turtle from Brazil
Figure 1.
Charaxicephaloides polyorchis
Groshaft & Tenora, 1978 (Digenea: Pronocephalidae) collected in a
Chelonia mydas
(Testudines: Cheloniidae) from Brazil. Ventral view. Scale bar 3 mm.
Neotropical Helminthology, 2021, 15(2), jul-dic
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214
Variations also occurred for size, since our
specimens are larger than the largest flukes
described by Groschaft & Tenora (1978) and
Santoro
et al.
(2009). Possibly, the difference
between our specimens and the others already
described. Such findings likely correspond merely
to individual variations of the specimens.
Groschaft
et al.
(1977) describe seven different
species of trematodes collected from a green turtle
on a hawksbill sea turtle-
Eretmochelys imbricata
Linnaeus, 1766 from Cuba. In the present work, the
authors present morphometric and morphological
data of
C. polyorchis
, which apparently indicates
the same data as originally presented by Groschaft
& Tenora (1978), however the data of the body
length and width and the oral sucker were
presented with different values. Although
morphological and morphometric aspects are
available in different publications, there are no
records regarding the molecular biology of these
individuals, which could contribute to a better
understanding of this trematodes.
Santoro
et al.
(2009) redescribed
C. polyorchis
based on 35 specimens collected in the stomach of
green turtles from Tortugueiro National Park in
Costa Rica, the authors offer, in addition to new
morphometric data, broader descriptions of the
analyzed parasites.
Cavaco
et al.
Table 1.
Morphometric data of
Charaxicephaloides polyorchis
Groshaft & Tenora, 1978
(Digenea: Pronocephalidae) from
Chelonia mydas
(Testudines: Cheloniidae). Measurements in
micrometers as range (mean)
Groschaft
&
Tenora
(
197
8)
Santoro
et al.
(
2009
)
Present report
Locality
Cuba
Costa Rica
Brazil
Site of infection
Stomach (?)
Stomach
Stomach
N
4
35
4
Body length (mm)
4.05
–
4.12 (5.87)
4.6
–
6.2
(
5
.
5
)
11.39
–
12.86 (11.9)
Body width (mm)
1.41
–
1.51 (1.84)
1
.
2
–
2
(
1
.
6
)
3.15
–
3.65 (3.2)
Oral sucker length
0.436
–
0.717 (0.733)
0.433
–
0.714
(
0.590
)
0.840
–
0.998 (0.909)
Oral sucker width
0.499
–
0.748 (0.717)
0.624 (0.484
–
0.765)
0.930
–
1.01 (0.715)
Cephalic colar wide
-
0.8
–
2
.0 (
1.6
)
0.940
–
2.01 (1,4)
Oesophagus length
0.78
0.288
–
0.649
(
0.510)
0.460
–
0.720 (0.59)
Cirrus sac length
0.46
(
0.78
)
0.463
–
0.875
(
0.639)
0.547
–
0.630 (0.588)
Cirrus sac width
0.18
(
0.17
)
–
0.209
–
0.304 (0.256)
Follicles (diameter)
0.15
–
0.21
–
–
Testesc
left side (number)
18
–
25
14
–
24
21
–
26 (24)
Testes
right side
18
-
25
21
–
26
20
–
23 (21)
Follicles on
right side length
–
0.022
–
0.057
(
0.037
)
0.049
–
0.092 (0.071)
Follicles on right side width
–
0.024
–
0.062
(
0.038
)
0.070
–
0.106 (0.080)
Follicles on left side length
–
0.027
–
0.065
(
0.040
)
0.050
–
0.090 (0.074)
Follicles on left side width
–
0.027
–
0.067
(
0.041
)
0.064
–
0.083 (0.072)
Left testes length
–
0.103
–
0.237
(
0.158)
0.268
–
0.393 (0.329)
Left testes width
–
0.103
–
0.206
(
0.148)
0.276
–
0.417 (0.338)
Rigth testes length
–
0.112
–
0206
(
0.153)
0.273
–
0.406 (0.338)
Right
testes width
–
0.102
–
0.206
(
0.143)
0.267
–
0.379 (0.326)
Ovary length
0.234
(
0.187
)
0.196
–
0.309
(
0.252)
0.405
–
0.536 (0.484)
Ovary width
0.343
(
0.265
)
0.196
–
0.350
(
0.259)
0.420
–
0.512 (0.477)
Mehlis` gland length
–
0.175
–
0.309
(
0.248
)
0.364
–
0.530 (0.432)
Mehlis` gland width
–
0.175
–
0.381
(
0.285
)
0.397
–
0.538 (0.449)
Eggs length
0.034
–
0.038
0.024
–
0.049
(
0.034
)
0.029
–
0.034 (0.032)
Eggs width
0.015
–
0.018
0.012
–
0.022
(
0.016
)
0.012
–
0.018 (0.014)
Eggs
filaments length
0.35
0.270
–
0.310
(
0.290
)
–
Excretory vesicle length
–
0.270
–
0
.594
(
0.449
)
–
Excretory vesicle width
–
0.081
–
0.135
(
0.103
)
–
Neotropical Helminthology, 2021, 15(2), jul-dic
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215
Charaxicephaloides polyoschis
in a green turtle from Brazil
Gomes
et al
. (2017) analyzed 36 young specimens
of green turtle and reported the occurrence of
C.
polyorchis
collected in the stomach of 11.1% of the
hosts, however, no morphometric or
morphological data of the analyzed specimens
were presented.
In addition to
C. polyorchis
, specimens of
C. albus
,
P. obliquus
and
D. baldassinae
were found in the
stomach and
P. cochlear
in the urinary bladder.
These findings are not new and have been
described in the Brazilian region (Werneck &
Silva, 2015; Werneck
et al
., 2021).
So far, little is known about
C. polyorchis
, with less
than 50 individuals analyzed to date and it appears
that the species is restricted to green turtles in the
Neotropical region, being reported in green turtles
from Cuba (Groschaft
et al.
, 1977; Groschaft &
Tenora, 1978), Costa Rica (Santoro
et al.
, 2009)
and Brazil (Gomes
et al
., 2017).
The beach monitoring project in Espírito Santo is
part of the requirements established by the federal
environmental licensing process of the Brazilian
Environmental Agency (IBAMA), for the
exploration of oil and gas by PETROBRAS at the
Campos Basin presalt province. BW Institute is a
Non-Governmental Organization involved in
biology and veterinary medicine activities and one
of the main aims is to disseminate scientific study
results to contribute to the conservation of aquatic
organisms. We thank the comments of reviewers
that helped to improve our paper.
Conflict of interest:
On behalf of all authors, the
corresponding author states that there is no conflict
of interest.
ACKNOWLEDGMENTS
Blair, D. 2005.
Family Pronocephalidae Looss,
1899.
In
A. Jones, RA Bray & DI Gibson
(eds.).
Keys to the Trematoda
, Vol. 2. CAB
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Chelonia mydas
)
recolhidas no litoral do Espírito Santo
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Arquivo Brasileiro de Medicina veterinária
e Zootecnia, vol. 69, pp. 644-650.
Groschaft, J, Otero, AC & Tenora, F. 1977.
Trematodes (Trematoda) from Cuban
turtles,
Chelonia mydas
(L.) and
Eretmochelis imbricata imbricata
(L.)
(Testudinata – Chelonidae).
Acta
universitatis agriculturae, vol. 25, pp. 155-
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Groschaft, J & Tenora, F. 1978.
Charaxicephaloides polyorchis
Gen. Nov.,
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(Testudinata)
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Santoro, M, Brandmayr, P, Greiner, EC, Morales,
JA & Rodríguez-Ortíz, B. 2009.
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polyorchis
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Werneck, MR, Conti, LM & Blair, D. 2021.
Desmogonius baldassinae
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Parasitology Research, vol. 120, 2281-
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World Register of Marine Species. 2021.
Charaxicephaloides polyorchis
Groschaft
& Tenora, 1978. Accessed at:
https://www.marinespecies.org/aphia.php?
p=taxdetails&id=728066x
Received April 26, 2021.
Accepted June 22, 2021.
Neotropical Helminthology, 2021, 15(2), jul-dic