Digenetic Trematodes of Dermochelys coriacea From the

Digenetic Trematodes of Dermochelys coriacea From the Southwestern Atlantic Ocean
Max R. Werneck1, Luciana Verissimo2, Paula Baldassin3, Fiorella Gagliardi4, Eduardo Tadashi5, Juçara
Wanderlinde2, Cecília Baptistotte2, Maria T.D. Melo2, Eduardo H.S.M. Lima2, Berenice G. Gallo2
& Reinaldo J. da Silva6
Centro Universitário Módulo, Av. Frei Pacífico Wagner n.º 653, Centro Caraguatatuba, São Paulo, 11660-903, Brazil (E-mail:
[email protected]); 2Fundação Pró-Tamar, Rua Antônio Athanazio da Silva n.º 273, Bairro Itagua, Ubatuba, São Paulo,
11680-000 Brazil; 3Instituto Oceanográfico- Universidade de São Paulo, Praça do Oceanográfico, nº 191, São Paulo-SP, 05508-900,
Brazil; 4Karumbé, Av. Giannattasio 30.5 Km. El Pinar, Canelones, Uruguay; 5Departamento de ecologia e zoologia da Universidade
Federal de Santa Catarina- Av. Eduardo Marques Bairro Trindade CEP: 88040-970 Florianópolis-SC, Brazil; 6Departamento de
Parasitologia, Instituto de Biociências, UNESP, 18618-000 Botucatu, São Paulo, Brazil.
1
The leatherback turtle Dermochelys coriacea Vandelli, 1761 is the
largest of all sea turtles. The species inhabits pelagic tropical, subtropical and temperate environments from the Pacific, Atlantic and
Indian oceans, where its primary prey items are jellyfish, tunicates
and soft-bodied invertebrates (Márquez 1990).
Parasitological surveys of D. coriacea are still rare and the data
found in the literature concerns only about seven hosts (Manfredi
et al. 1996; Eckert et al. 2009). Five trematode species were found
parasitizing this species: Pyelosomum renicapite, Calycodes anthos,
Cymatocarpus sp., Enodiotrema instar and Enodiotrema carettae.
Here we summarize the helminth fauna of D. coriacea specimens
from the Southwestern Atlantic region.
Eight dead D. coriacea specimens (7 from Brazil and 1 from
Uruguay), were obtained from January 2005 to November 2006,
from strandings on the shoreline (n = 4), from incidental capture in
gillnets (n = 2), and from rehabilitation centers (n = 2). The mean
curvilinear carapace length (CCL) was 135.7 ± 14.1 SD cm (range
= 111.0 to 155.5 cm). At necropsy, the gastrointestinal tract was
removed and immediately processed, except in one case in which
it was frozen for later analysis. The esophagus, stomach, small
intestine and large intestine were removed and examined separately.
The heart was collected from four animals for analysis according to
the method described by Snyder & Clopton (2005) and simplified
by Werneck et al. (2006).
The trematodes were fixed in Alcohol-Formalin-Acetic Acid
solution under slight coverslip pressure for 10 min, and then
transferred to 70% alcohol for further processing. Specimens found
were stained with carmine, cleared with creosote, and analyzed
in a computerized system for image analysis (Leica Qwin Lite
3.1). After identification, the specimens were deposited in the
Helminthological Collection at the Instituto de Biociências (CHIBB)
at the Universidade Estadual Paulista, Botucatu, São Paulo, Brazil.
The trematode species were identified by following Yamaguti
(1971), Threlfall (1979), Almor et al. (1989), Manfredi et al. (1998)
and Jones et al. (2005).
Four (50%) D. coriacea specimens were parasitized by
trematodes. Only parasites of the digestive system were collected
from the small and large intestine. Trematodes of the species P.
renicapite were present in all four animals. In the Uruguayan
specimen, parasites of the species C. anthos were also observed.
Parasites of the family Spirorchiidae were not found in the four
heart samples analyzed.
TREMATODA
Pronocephalidae Looss, 1899
Pyelosomum renicapite Leidy, 1856
Measurements (mm): (n = 10) Body 17.0 (9.9–33.1) by 2.4
(1.7–3.6); Head collar evident with shallow incision midventrally;
Oral sucker 0.679 (0.410–0.871) X 0.753 (0.508–0.89); Esophagus
short; Ceca are narrow and with wide serpentine undulations, ending
near the posterior region; Ovary 0.525 (0.315–0.760) X 0,64 (0.340–
0.960), slightly submedian, lobulated, pretesticular; Right testis 1.29
(0.807–1.74) X 1.26 (0.670–1.82); left testis 1.182 (0.740–1.54)
X 1.224 (0.862–1.79), both irregularly lobulated, situated at the
posterior end; Genital pore situated on the left and after the cecal
bifurcation; Vitelline follicles extend from the midpoint of the body
to posterior ovary region; Cirrus sac, short and oblique into the
anterior end; Uterus in transverse coils, filling the major part of the
body; Eggs 0.035 (0.031–0.037) x 0.023 (0.020–0.027).
Host: Dermochelys coriacea
Locality and collection date: Mangaratiba, Rio de Janeiro State,
Brazil (23° 9' 10.64" S / 44° 0' 21.50" W), on October 19, 2005;
Florianópolis, Santa Catarina State, Brazil (27° 26' 8.33" S/ 48° 0'
44.97" W), on October 25, 2005; San José Kiyu - Uruguay (34° 44'
59.51" S / 57° 0' 31.58" W) on October 27, 2005; Almofala, Ceará
State, Brazil (3° 10' 41.67" S/ 39° 0' 20.55" W) on November 14,
2006.
Site of infection: Small and large intestine.
Prevalence: 4 of 8 (50%)
Intensity of infection ± SE: 24 ± 9.46
Number of helminthes collected: 72
Voucher specimens deposited: CHIBB 1667, 1668, 1670, 2014.
Calicodidae Dolfus, 1929
Calycodes anthos Braun 1899
Measurements (mm): (n = 1) Body slender and long 20.9 X 2.73;
Oral sucker ventral, subterminal, 0.96 X 1.07; Esophagus has two
lateral diverticles; Long muscular pharynx 0.82 X 0.77; The ceca are
straight and reach the posterior end; Ventral sucker well developed
and situated in the upper third of the body 1.16 X 1.27; Genital pore
is preacetabular situated left of midline; Cirrus pouch is long and
preacetabular; Uterus between the ventral sucker and testis; Ovary
anterior to testis situated to the right of the midline; Testis slightly
elliptical, tandem, anterior testis 1.09 X 0.88, posterior testis 1.43
X 1.05; Vitelline follicles are dispersed, occupying the lateral parts
of the body. Eggs oval 0.062 X 0.040.
Marine Turtle Newsletter No. 132, 2012 - Page 13
Host: Dermochelys coriacea
Locality and collection date: San José Kiyu - Uruguay (34° 44'
59.51" S / 57° 0' 31.58" W) on October 27, 2005.
Site of infection: Small and large intestine.
Prevalence: 1 of 8 (12.5%)
Intensity of infection: 1
Number of helminthes collected: 1
Voucher specimens deposited: CHIBB 1669
Mohan (1970) reported the occurrence of P. renicapite in a turtle
from the Indian Ocean. This parasite was later found in sea turtles
from the North Atlantic Ocean in Canada (Threlfall, 1979), France
(Almor et al. 1989), the Mediterranean Sea in Italy (Manfredi et
al. 1996), and in Puerto Rico (Dyer et al. 1995). Threlfall (1979)
found C. anthos and Cymatocarpus sp. in specimens from the North
Atlantic Ocean. Manfredi et al. (1996) also observed E. instar and
E. carettae in D. coriacea from the Mediterranean Sea.
No parasite of the circulatory system was observed in the hearts
of the specimens in this study. Helminths of the family Spirorchidae
have been previously found in sea turtles of the species Chelonia
mydas (L.), Caretta caretta (L.) and Eretmochelys imbricata (L.)
(Smith, 1997), but there are no previous studies on D. coriacea.
The morphometric analysis of the P. renicapite specimens was
based on the studies of MacCallum (1921), Threlfall (1979) and
Almor et al. (1989). The range for total length, oral sucker length,
ovary width and testicle length of specimens we observed was larger
than that reported in other studies. Analyses of the species C. anthos
were performed as established by Threlfall (1979) and Manfredi
et al. (1998), and showed that total length and width, oral sucker
length and width, pharynx length and width, as well as ovary width,
were larger than measurements reported previously. In both cases,
the differences may be due to individual variability and increases
in the range of species morphometry.
This report is the first helminthological analysis of D. coriacea
from the Southwestern Atlantic Ocean, and the first record of these
parasites in this region, thus contributing to the knowledge about
the helminth fauna of sea turtles and their geographical distribution.
Acknowledgments: Projeto TAMAR is affiliated with ICMBio, comanaged by the Fundação Pró-TAMAR, and officially sponsored
by PETROBRAS. We thank the Fundação de Amparo à Pesquisa do
Estado de São Paulo - FAPESP (Proc. 07/59504-7) for the financial
support. The authors are indebted to Marcelo Spiandorin, Ligia
Santana, Antônio Mauro Correa and “Popo” (fishermanfrom Kiyu),
for helping collect the samples. The authors express their thanks
to Prof. Oscar Castro, from the Departamento de Parasitología,
Facultad de Veterinaria, UDELAR, Uruguay for critical reading
and suggestions to improve the manuscript.
ALMOR, P., J.A. RAGA, E. ABRIL, J.A. BALBUENA & R.
DUGUY. 1989. Parasitime de la tortue luth, Dermochelys coriacea
(Linnaeus, 1766) dans les eaux europeennes par Pyelossomum
renicapite (Leidy, 1856). Vie Milieu 39: 57-59.
DYER, W.G., E.H. WILLIAMS & L. BUNKLEY-WILLIAMS.
1995. Digenea of the green turtle (Chelonia mydas) and the
leatherback turtle (Dermochelys coriacea) from Puerto Rico.
Caribbean Journal of Science 31: 269-273.
ECKERT, K.L., B.P. WALLACE, J.G. FRAZIER, S.A. ECKERT
& P.C.H. PRITCHARD. In press. Synopsis of the biological data
on the leatherback sea turtle, Dermochelys coriacea (Vandelli,
1761). U.S. Fish and Wildlife Service.
JONES, A., R.A. BRAY & D.I. GIBSON. 2005. Key to the
Trematoda v.2, CABI Publishing, London, 745 pp.
MACCALLUM, G.A. 1921. Studies in helminthology. Part 1
Trematodes. Zoopathologica 1: 202-204.
MANFREDI, M.T., G. PICCOLO, F. PRATO & G.R. LORIA.
1996. Parasites in Italian sea turtles I. The leatherback turtle
Dermochelys coriacea (Linnaeus, 1766). Parassitologia 38:
581-583.
MANFREDI, M.T., G. PICCOLO & C. MEOTTI. 1998. Parasites
of Italian sea turtles. II. Loggerhead turtles (Caretta caretta
[Linnaeus, 758]). Parassitologia 40: 305-308.
MARQUEZ, M.R. 1990. FAO Species catalogue. Sea turtles of
the world. An annotated and illustrated catalogue of sea turtle
species known to date. FAO Fisheries Synopsys. No. 125, Vol.
11 Rome, FAO. 81 pp.
MOHAN, R.S.L. 1970. Occurrence of the digenetic trematode
Astorchis renicapite (Leidy) (family: Pronocephalidae) in the
leathery turtle Dermochelys coriacea (Linné) from the Indian
Ocean. Journal of the Bombay Natural History Society 68: 489490.
SMITH, J.W. 1997. The blood flukes of cold-blood vertebrates.
Helminthological Abstracts 66: 255-294.
SNYDER, S. & R. CLOPTON. 2005. New methods for the collection
and preservation of spirorchiid trematodes and polystomatid
monogeneans from turtles. Comparative Parasitology 72: 102107.
THRELFALL, W. 1979. Three species of Digenea from the Atlantic
leatherback turtle (Dermochelys coriacea). Canadian Journal of
Zoology 57: 1825-1829.
WERNECK, M.R., J.H. BECKER, B.M.G. GALLO & R.J. SILVA.
2006. Learedius learedi Price, 1934 (Digenea, Spirorchiidae)
in Chelonia mydas Linnaeus, 1758 (Testudines, Chelonidae) in
Brazil: case report. Arquivo Brasileiro de Medicina Veterinária e
Zootecnia 58: 550-555.
YAMAGUTI, S. 1971. Synopsis of digenetic trematodes of
vertebrates. Keigaku Publishing Co., Tokyo, 1074 pp.
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