RESEARCH NOTE / NOTA CIENTÍFICA
Abstract
The aim of the present study is to report the occurrence of Styphlotrema solitaria Looss, 1899
infecting sea turtles of the species Eretmochelys imbricata Linnaeus, 1758 found in the North Coast
of São Paulo State, Brazil. Only nine S. solitaria specimens were found in the hosts studied, with a
mean intensity of infection of 4.5. Since 2002, 14 specimens of E. imbricata from this region were
necropsied and the prevalence of S. solitaria was 14.2%. New variations on morphological data were
presented for this digenetic species. This is the first occurrence of S. solitaria in sea turtles from
Brazilian Coast, expanding the information on the helminth fauna of E. imbricata and the
geographical distribution of S. solitaria.
Key words: Brazil - Eretmochelys imbricata - sea turtles - Styphlotrema solitaria – Trematoda.
Suggested citation: Werneck, MR & Silva, RJ 2012. Styphlotrema solitaria Looss, 1899 (Digenea,
Styphlotrematidae) infecting Eretmochelys imbricata Linnaeus 1758 (Testudines, Chelonidae) in Brazil.
Neotropical Helminthology, vol. 6, nº 1, pp. 121 - 126.
Neotrop. Helminthol., 6(1), 2012
2012 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)
ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line
a b
Max Rondon Werneck* ; Reinaldo José da Silva
STYPHLOTREMA SOLITARIA LOOSS, 1899 (DIGENEA, STYPHLOTREMATIDAE) INFECTING
ERETMOCHELYS IMBRICATA LINNAEUS 1758 (TESTUDINES, CHELONIDAE) IN BRAZIL
INFECCIÓN POR STYPHLOTREMA SOLITARIA LOOSS, 1899
(DIGENEA, STYPHLOTREMATIDAE) EN ERETMOCHELYS IMBRICATA LINNAEUS 1758
(TESTUDINES, CHELONIDAE) EN BRASIL
a
bUNESP – Univ Estadual Paulista, Campus de Botucatu, Instituto de Biociências, Departamento de Parasitologia, Botucatu, São Paulo, Brazil.
*Corresponding author: Max Rondon Werneck, e-mail: max@bwvet.com.br
BW Consultoria e laboratório veterinário, Rua Ponciano Eugênio Duarte n.º 203, Bairro Centro, Ubatuba, São Paulo, 11680-000,Brazil.
Resumen
Palabras clave: Brasil - Eretmochelys imbricata - Styphlotrema solitaria - tortugas marinas - trematoda.
El objetivo de esta investigación es presentar la ocurrencia de Styphlotrema solitaria Looss, 1899 en
las tortugas marinas de la especie Eretmochelys imbricata Linnaeus 1758 encontradas en el litoral
Norte del Estado de São Paulo, Brasil. Apenas nueve especímenes fueron encontrados en los
hospederos analizados correspondiendo a una intensidad media de 4,5. Desde el año de 2002, 14
ejemplares de E. imbricata provenientes de esta misma región fueron necropsiados lo que
corresponde a una prevalencia de 14,2 %. Nuevas variaciones y datos morfológicos se presentan para
esta especie de digeneo. Esta es la primera ocurrencia de S. solitaria en las tortugas marinas
encontradas en el litoral brasileño, ampliando así la información sobre la helmintofauna de E.
imbricata y distribución geográfica de S. solitaria.
121
INTRODUCTION
The family Styphlotrematidae Baer, 1924 has a
considerable complexity due to the numerous
taxonomic changes over time. This family includes
only the genus Styphlotrema Odhner, 1911 with
two described species Styphlotrema solitaria
Looss, 1899, reported in sea turtles, and
Styphlotrema artigasi Kohn & Fernandes 1982,
reported in marine fish (Tkach, 2008).
The present study reports the first occurrence of S.
solitaria in the sea turtle Eretmochelys imbricata
from the Brazilian Coast.
Specimens of S. solitaria were collected from the
small intestine of two E. imbricata individuals
found dead after becoming entangled in a fish net
in the Northern Coast of the São Paulo State
(Southeastern Brazil) in 2009. The first host had a
curvilinear carapace length of 41 cm and weighed
7 kg and the second had a curvilinear carapace
length of 49 cm and weighed 12 kg.
During the necropsy, the esophagus, stomach,
small and large intestines were removed. The
contents were washed and sifted (battery of sieves
with mesh sizes of 14, 60 and 100). The contents
were then examined under a stereomicroscope.
Helminths (n = 9) were fixed in an alcohol-
formalin-acetic acid solution, stained with
chlorhydric carmine, cleared with eugenol and
analyzed using a computer system for image
analyzes (QWin Lite 3.1 – Leica). Morphometric
values (in millimeters) were expressed as mean
and range (minimum – maximum). The helminths
were deposited in the Coleção Helmintológica do
Instituto de Biociências (CHIBB) of the
Universidade Estadual Paulista, Botucatu, São
Paulo State, Brazil (CHIBB 6194, 6200, 6213 and
6216). All collections were authorized by federal
licenses for activities with scientific purposes
(SISBIO 12421-1 and 12431-2).
Werneck & Silva
Styphlotrema infecting Eretmochelys in Brazil
MATERIAL AND METHODS
RESULTS AND DISSCUSION
Styphlotrema solitaria (Fig. 1-5) specimens
presented the following characteristics: parasite
small; extremities oval-shaped (Fig. 1); tegument
without spines (Fig. 2); oral sucker small and
subterminal (Fig. 3); pharynx present; esophagus
non-sinuous, terminating in cecal bifurcation in
initial third of body; ceca thin, slightly sinuous,
terminating in middle third of body; acetabulum
round and in middle third of body between cirrus
sac and metraterm; testis with irregular shape,
occupying equatorial region of body; cirrus sac of
little volume, occupying area on left side of
acetabulum; ovary oval-shaped, anterior to left
testicle, uterus long and quite sinuous, initiating
near ovary, running long course toward posterior
region of body and returning to more central region
of parasite, terminating in genital pore near cirrus
sac in initial third of body; vitellaria with
numerous small follicles extending from
equatorial region to testicle level and to posterior
region of cecum; excretory system consisting of
one pore in posterior region of body and single
trunk extending to region near testicle, where it
forks and ends in cecum fundus laterally to
acetabulum (Fig. 4); eggs oval-shaped (Fig. 5).
Figure 1. Styphlotrema solitaria Looss, 1899 (Digenea,
Styphlotrematidae) from Eretmochelys imbricata
(Testudines, Chelonidae) in Brazil (Bar: 1 mm).
122
Table 1. Morphometric data (in millimeters) of Styphlotrema solitaria (Digenea, Styphlotrematidae) of
Eretmochelys imbricata (Testudines, Chelonidae) from Brazil.
Neotrop. Helminthol., 6(1), 2012
Variables Groschaft et al. (1977) Present Study
Host Eretmochelys imbricata Eretmochelys imbricata
Locality Gulf of Guanahacabides, Cuba São Paulo State, Brazil
Site ESO, EST, INT SI
Number of parasites 99 (20 measured) 9 (4 measured)
Total length 2.09 – 3.21 4.86 ± 0.14 (4.70 – 4.99)
Total width 0.78 – 1.48 1.78 ± 0.12 (1.60 – 1.85)
Oral sucker length 0.133 – 0.198 0.275 ± 0.023 (0.254 -0. 306)
Oral sucker width
0.133 – 0.207
0.318 ± 0.018 (0.301 ± 0.335)
Pharynx length
0.052 – 0.103
0.116 ± 0.06 (0.111 – 0.124)
Pharynx width
0.089 – 0.148
0.165 ± 0.09 (0.154 – 0.171)
Esophagus length
0.089 – 0.170
0.344 ±0.028 (0.312 – 0.369)
Esophagus width
0.022 – 0.029
-
Acetabulum length
0.148 – 0.288
0.355 ± 0.017 (0.340 -0. 380)
Acetabulum width
0.133 – 0.244
0.345 ± 0.024 (0.309 – 0.361)
Right testis length
0.163 – 0.288
0.502 ± 0.037 (0.471 – 0.556)
Right testis width
0.170 – 0.370
0.493 ± 0.116 (0.412 – 0.666)
Left testis length
0.133 – 0.370
0.486 ± 0.028 (0.452 – 0.520)
Left testis width
0.177 – 0.303
0.514 ± 0.067 (0.425 – 0.590)
Cirrus pouch length
0.333 – 0.888
1.172 ± 0.046 (1.107 – 1.209)
Cirrus pouch width
0.103 – 0.199
0.235 ± 0.037 (0.199 – 0.286)
Ovary length
0.111 – 0.177
0.254 ± 0.016 (0.239 – 0.273)
Ovary width
0.133 – 0.236
0.322 ± 0.010 (0.311 – 0.337)
Seminal receptacle length
-
0.231 ±0.07 (0.224 – 0.240)
Seminal receptacle width
-
0.284 ± 0.036 (0.238 – 0.322)
Left vitelline fields length 0.357 – 1.123 1.610 ± 0.271 (1.428 – 2.013)
Rigth vitelline fields length 0.357 – 1.123 1.666 ± 0.196 (1.546 – 1.958)
Egg length 0.038 – 0.049 0.047 ±0.003 (0.040 – 0.054)
Egg width 0.019 – 0.024 0.021 ± 0.002 (0.017 – 0.025)
Since the year 2002, 14 individuals of E. imbricata
from the Northern Coast of São Paulo State, Brazil,
have been necropsied. Specimens of S. solitaria
were found in only two hosts, corresponding to a
prevalence of 14.2% and the mean intensity of
infection observed was 4.5.
Only two species are known for the genus
Styphlotrema: S. solitaria, described infecting the
sea turtles Caretta caretta in the State of Florida,
USA (Luhman, 1935; Byrd et al., 1940) and Italy
(Santoro et al., 2010), and also in E. imbricata
from Porto Rico (Fischthal & Acholonu, 1976) and
Cuba (Groschaft et al., 1977). Styphlotrema
artigasi was described based on a single specimen
reported in Guavina guavina (Valenciennes,
1837), which is a marine fish of the family
Eleotridae found on the Coast of Rio de Janeiro
State, Brazil (Kohn & Fernandes, 1982).
Styphlotrema solitaria is a generalist species only
found in sea turtles. This species has been reported
in C. caretta in the Mediterranean, with a
prevalence of 4.5% and mean intensity of infection
of 9.0 (Santoro et al., 2010). In E. imbricata, this
helminth is reported with a prevalence of 14.2%
and mean intensity of infection of 6.0 (Fischthal &
Acholonu, 1976). The present data and those from
reports in the literature corroborates that this
species occurs with low prevalence in sea turtles.
The morphometric analysis of the specimens
reported herein (Table 1) reveals that all
measurements are larger than those described for
ESO - Esophagus; EST - stomach; INT- intestine, SI - Small intestine.
123
Figure 2. Tegument of Styphlotrema solitaria Looss, 1899
(Digenea, Styphlotrematidae) of Eretmochelys imbricata
(Testudines, Chelonidae) from Brazil.
Figure 3. Oral sucker of Styphlotrema solitaria Looss, 1899
(Digenea, Styphlotrematidae) of Eretmochelys imbricata
(Testudines, Chelonidae) from Brazil.
the specimens studied by Groschaft et al. (1977).
Only the measurements of length and width of eggs
are similar to those reported in both studies. These
data contribute to the morphological
characterization of this digenetic species.
Approximately 50 species of helminths distributed
among 10 families are recognized as parasites of E.
imbricata (Dyer et al., 1995). However, little is
known on the helminth diversity of this species in
Brazil, for which only Cricocephalus albus
(Travassos et al., 1969), Amphiorchis
caborojoensis and Carettacola stunkardi
(Werneck et al., 2008a) were reported.
Unfortunately little is known about the E.
imbricata helminthes found on the Brazilian coast,
this report describes the occurrence of the fourth
species of parasites reported in this host for this
region. Therefore further studies should be
performed to identify the E. imbricata helminthes
parasites found on the Brazilian coast.
This is the first report of S. solitaria in sea turtles on
the Brazilian Coast, contributing for the
knowledge of geographical distribution of S.
solitaria and also for the helminth fauna of E.
imbricata.
Figure 4. Excretory system of Styphlotrema solitaria Looss,
1899 (Digenea, Styphlotrematidae) of Eretmochelys
imbricata (Testudines, Chelonidae) from Brazil (Bar: 1 mm).
Werneck & Silva
Styphlotrema infecting Eretmochelys in Brazil
124
ACKNOWLEDGMENTS
We would like to thank the Fundação de Amparo à
Pesquisa do Estado de São Paulo - FAPESP (Proc.
07/59504-7) for the financial support. The authors
wish to express their thanks to Paula Baldassin and
Monica Quezada for critical reading and
suggestions to improve the manuscript.
BIBLIOGRAPHIC REFERENCES
Byrd, EE, Parker, MV & Reiber, RJ. 1940.
Taxonomic studies on the genus
Styphlodora Looss, 1899 (Trematoda:
Styphlodorinae), with descriptions of four
new species. Transactions of the American
Microscopical Society, vol. 59, pp. 294-
326.
Neotrop. Helminthol., 6(1), 2012
Figure 5. Egg of Styphlotrema solitaria Looss, 1899
(Digenea, Styphlotrematidae) of Eretmochelys imbricata
(Testudines, Chelonidae) from Brazil.
Dyer, WG, Williams, EHJ, Bunkley-Williams, L &
Moore, D. 1995.
Fischthal, JH & Acholonu, AD. 1976.
Groschaft, J, Otero, C & Tenora, A. 1977.
Kohn, A & Fernandes, BMM. 1982.
Luhman, M. 1935.
Santoro, M, Badillo, FJ, Mattiucci, S, Nascetti, G,
Bentivegna, F, Isacco, G, Travaglini, A,
Paoletti, M, Kinsella, JM, Tomas, J, Raga,
JA & Aznar, FJ. 2010.
Tkach VV. 2008.
Travassos, L, Freitas, JFT & KOHN, A. 1969.
Werneck, MR, Gallo, BG & Silva, RJ. 2008.
Some digeneans
(Trematoda) of the hawksbill turtle,
Eretmochelys imbricata imbricata
(Testudines: Cheloniidae) from Puerto Rico.
Journal of Helminthological Society of
Washington, vol. 62, pp. 13-17. Some
digenetic trematodes from Atlantic
Hawksbill turtle Eretmochelys imbricata
imbricata (L.) from Puerto Rico. Journal of
Helminthological Society of Washington,
vol. 43, pp. 174-185.
Trematodes (trematoda) from cuban turtles,
Chelonia mydas mydas (L.) and
Eretmochelys imbricata imbricata (L.)
(Testudinata- Cheloniidae). Acta
Universitatis Agriculturae, vol. 25, pp. 154-
167. Styphlotrema
artigasi sp. N. (Plagiorchiidae), a new
trematode parasite of marine Fish.
Proceedings of the Helminthological
Society of Washington, vol. 49, pp. 31-33.
Two new trematodes from the
loggerhead turtle (Caretta caretta). Journal
of Parasitology, vol. 21, pp. 274-276.
Helminth
communities of loggerhead turtles (Caretta
caretta) from Central and Western
Mediterranean Sea: the importance of host's
ontogeny. Parasitology International, vol.
59, pp. 367-375.
Family Styphlotrematidae Baer,
1924. In: Bray, RA, Gibson, DI & Jones, A
(eds). 2008. Keys to the Trematoda. Vol.3.
CAB International, Cambridge, UK, pp.
421-423.
Trematódeos do Brasil. Memorias do
Instituto Oswaldo Cruz, vol. 67, pp. 1-886.
Spirorchiids (Digenea: Spirorchiidae)
infecting a Hawksbill sea turtle
Eretmochelys imbricata (Linnaeus 1758)
from Brazil. Arquivo Brasileiro de Medicina
veterinária e Zootecnia, vol. 60, pp. 663-
666.
125
Werneck & Silva
Styphlotrema infecting Eretmochelys in Brazil
Received February 13, 2012.
Accepted March 26, 2012.
Correspondence to author/ Autor para
correspondencia:
Max Rondon Werneck
BW Consultoria e laboratório veterinário, Rua
Ponciano Eugênio Duarte n.º 203, Bairro Centro,
Ubatuba, São Paulo, 11680-000,Brazil.
E-mail/ correo electrónico:
max@bwvet.com.br
126
