Resumen

Palabras clave: tortuga pintada - Telorchis corti - Telorchis achavali.

Trachemys dorbigni es nativo de Uruguay, Argentina y Brasil, en el territorio brasileño es

abundante en el extremo sur del país. Para la investigación de la fauna de helmintos de T. dorbigni

se examinaron sesenta tortugas de ambientes acuáticos de zonas urbanas y rurales de dos

municipios de Rio Grande do Sul, Brasil. Durante la investigación se encontraron Telorchis

achavali y Telorchis corti (Digenea). Este es el primer registro de T. achavali en Brasil.

201

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

TELORCHIS SPP. (DIGENEA: TELORCHIIDAE) IN TRACHEMYS DORBIGNI (DUMÉRIL &

BIBRON, 1835) (TESTUDINES: EMYDIDAE) IN SOUTHERN BRAZIL

TELORCHIS SPP. (DIGENEA: TELORCHIIDAE) EN TRACHEMYS DORBIGNI (DUMÉRIL &

BIBRON, 1835) (TESTUDINES: EMYDIDAE) EN EL SUR DE BRASIL

1 1

Carolina S. Mascarenhas * & Gertrud Müller

Abstract

Trachemys dorbigni, the Brazilian slider turtle, is native to Uruguay, Argentina and Brazil. In

Brazil the species is abundant in the southern region. This research investigated the helminth

fauna of this species. We examined sixty chelonians from aquatic environments of urban and rural

areas in two municipalities in the State of Rio Grande do Sul, Brazil. During the research we found

Telorchis achavali and Telorchis corti (Digenea). This is the first record of T. achavali in Brazil.

Keywords: Brazilian slider turtle - freshwater turtle - Telorchis corti - Telorchis achavali.

Suggested citation: Mascarenhas, CS & Müller, G. 2013. Telorchis spp. (Digenea: Telorchiidae) in Trachemys dorbigni (Duméril

& Bibron, 1835) (Testudines: Emydidae) in southern Brazil Neotropical Helminthology, vol. 7, n°2, jul-dec, pp. 201 - 210..

1 Laboratório de Parasitologia de Animais Silvestres, Departamento de Microbiologia e Parasitologia (DEMP), Instituto de Biologia (IB), Universidade Federal

de Pelotas (UFPel), Campus Universitário, caixa postal: 354, CEP 96010-900, Pelotas, RS, Brasil. *E-mail: phrybio@hotmail.com.br

Neotrop. Helminthol., 7(2), 2013

2013 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line

INTRODUCTION

Trachemys dorbigni (Duméril and Bibron,

1835), the Brazilian slider turtle, is restricted in

its distribution to the southern countries of South

America, occurring in Brazil, Uruguay and

Argentina (Fritz & Havaš, 2007), and are found

inhabiting fluvial ecosystems, such as dams,

rivers, ponds, and wetlands (Quintela &

Loebmann, 2009). In the Brazilian territory, the

species is native to the State of Rio Grande do

Sul; however its distribution has been expanded

to other Brazilian states, probably due to the

illegal trafficking of wild animals (Bujes &

Verrastro, 2007; Quintela & Loebmann, 2009)

Telorchiidae Looss, 1899 (Digenea) is

compound with five subfamilies, among them

the Telorchiinae Looss, 1899 which is

represented by five genera, and Telorchis Lühe,

1899 is the type genus. The species of Telorchis

usually parasitize the intestine of amphibians

and reptiles, especially turtles from North

America, South America, Europe, and Asia

(Font & Lotz, 2009).

In freshwater turtles from the Neotropical

Region 25 species of Telorchis (Lenis, 2009)

have been reported. In T. dorbigni there have

been records of Telorchis dubius Mañé-Garzon

& Hollman-Spector, 1968 and Telorchis

achavali Mañé-Garzon & Hollman-Spector,

1973 (Mañé-Garzon & Hollman-Spector, 1968;

Mañé-Garzon & Hollman-Spector, 1973) in

Uruguay and Telorchis corti Stunkard, 1915 was

reported in Brazil (Pesenti et al., 2009). In this

context, the current study aims report the

presence of Telorchis spp. in Trachemys

dorbigni in Brazil.

From July 2010 to December 2012, 60 turtles

were collected under license (n°23196) of the

Instituto Chico Mendes de Conservação da

Biodiversidade (ICMBio). Twenty-eight

specimens of T. dorbigni were captured in four

lakes in Centro Agropecuário da Palma

belonging to the Universidade Federal de

Pelotas (UFPel), which is located in the rural

area of the Municipality of Capão do Leão; the

other 32 chelonians were collected in channels

in urban areas of the Municipality of Pelotas, and

both municipalities are found in the State of Rio

Grande do Sul, Brazil.

The animals were manually captured with the

aid of netting and transported in plastic boxes

(56 L) to the laboratory, where the chelonians

were weighed and measured. After

morphometry the animals were anesthetized

with a combination of ketamine 10% and

xylazine 2%, and after analgesia they were given

an intrathecal injection of lidocaine

hydrochloride 2% (Amado et al., 1994), as

recommended by Resolution Nº 1000/2012 of

Brazilian Federal Board of Veterinary Medicine

(CFV, 2012). Fifty-six of these animals were

frozen for later necropsy, and the others were

necropsied after death. Their organs were

individualized and their content and mucous

membrane were examined. Some specimens of

Telorchis were fixed under light compression in

AFA (70°GL ethanol, formalin 37% and glacial

acetic acid) and preserved in 70°GL alcohol.

Others specimens were stained in Delafield's

hematoxylin or Carmine's Langeron, and

mounted as permanent slides in Canada balsam

and identified according Mañé-Garzon &

Hollman-Spector (1973) and MacDonald &

Brooks (1989).

The measurements are expressed in micrometers

(µm), unless otherwise specified. Means and

standard deviations appear in parentheses. The

ecological terms were used according to Bush et

al. (1997). The photomicrographs were taken

using an Olympus BX 41 Microscope, with a

camera adapter system. Representative

specimens of trematodes were deposited in two

collections: Coleção Helmintológica do

Instituto Oswaldo Cruz (CHIOC), Rio de

Janeiro State, Brazil, and in the Coleção de

Helmintos do Laboratório de Parasitologia de

Animais Silvestres from the Universidade

Federal de Pelotas (CHLPAS-UFPel), Rio

Grande do Sul State, Brazil. Representative

specimens of the hosts were deposited in the

Mascarenhas& Müller

Telorchis spp. in Trachemys dorbigni

202

MATERIALS AND METHODS

in the rural area; however, it occurred in only one

host.

Telorchis corti and T. achavali, described below,

are Digenea from the small intestine of T.

dorbigni in southern Brazil. Besides these two

species, specimens of Telorchis were found in

six hosts in the rural area, however, their specific

determination was not possible, due to the stage

of maturation of some specimens, they were

considered to be juveniles due to their immature

reproductive structures, and the low mean

intensity of the infection (2.16 helminths/host)

(Table 1).

collection at the Coleção Herpetológica do

Museu Carlos Ritter (CHMR-UFPel), Rio

Grande do Sul State, Brazil (Numbers 78 and

79).

Of the 60 hosts examined 48.3% were

parasitized by Telorchis spp. In the urban area

only T. corti were found; in the rural area T.

corti, T. achavali, and immature specimens of

Telorchis were found (Table 1). There was no

association between species in the same host in

the rural area. Telorchis corti was the species

with higher mean intensity and mean abundance

203

Neotrop. Helminthol., 7(2), 2013

Table 1. Prevalence, infection mean intensity and mean abundance of Telorchis corti, Telorchis achavali and

immature specimens of Telorchis spp. (Digenea: Telorchiidae) from Trachemsy dorbigni (Testudines: Emydidae) in

rural and urban environment in southern Brazil.

Urban (N = 32) Rural (N = 28)

Prevalence

(%) Mean intensity Mean abundance Prevalence

(%) Mean

intensity Mean

abundance

Telorchis corti 65.62 20.38 13.37 3.5 130 4.64

Telorchis achavali - - 0 3.5 3 0.1

Immature specimens of

Telorchis spp. - - 0 21.42 2.16 0.46

RESULTS

(419.79 ± 126.27) from posterior extremity.

Anterior testes 130 – 470 (280.83 ± 93.15) long

by 90 – 470 (261.25 ± 99.75) wide and posterior

testes 140 – 480 (300.41 ± 103.1) long by 90 –

450 (251.66 ± 94.57) wide. Cirrus sac extending

from the anterior region of the acetabulum at the

anterior margem of ovary. Seminal vesicle

bipartite. Genital pore ventral, immediately pre-

acetabular, intercecal, mediano or slightly

sinistral. Ovary spherical 100 – 250 (167.91 ±

46.71) long by 80 – 300 (175.83 ± 64.05) wide,

intercaecal, median. Distance between ovary

and acetabulum 1100 – 2430 (1590.83 ± 382.51)

and distance between ovary and anterior testes

1700 – 4500 (2851.04 ± 859.85). Seminal

receptacle, Laurer's canal, and Mehli's gland

presents. Uterus between ovary and anterior

testes. Vitelline follicles in continuous

longitudinal lateral rows, extending from

Telorchis corti Stunkard, 1915 (Figs. 1 - 6)

Description. Based on 24 helminths. Body

elongate 4.8 – 11.25mm (7.43mm ± 1.89) long

by 250 - 930 (581.66 ± 219.33) wide (the level of

the ovary). Oral sucker subterminal, 75 – 202.5

(123.33 ± 31.31) long by 95 - 210 (136.56 ±

29.98) wide, prepharynx short, pharynx

muscular with 60 – 110 (74.1 ± 11.7) long by 60 -

120 (83.47 ± 17.46) wide. Oesophagus 210 –

460 (299.16 ± 77.56) long. Double caeca,

unbranched, extending back to posterior body at

a distance 75 – 200 (122.91 ± 31.37) from

posterior extremity; distance from the

bifurcation of the caeca to the anterior extremity

350 – 1000 (608.08 ± 176.91). Acetabulum

intercaecal, 85 – 225 (159.47 ± 42.2) long by

77.5 – 200 (136.84 ± 39.11) wide (19 specimens

measured). Testes oval to spherical, vertical and

intercaecal and situated at a distance 200 – 650

204

Mascarenhas& Müller

Telorchis spp. in Trachemys dorbigni

Laurer's canal not observed. Mehli's gland

present. Uterus between ovary and anterior

testes. Vitelline follicles extending from the

middle portion of the cirrus sac to near zone

pretestes, occupying the middle third of the

body. Eggs 30 – 32.5 (31.66 ± 1.44) long by 15 –

17.5 (16.66 ± 1.44) wide. Excretory pore

situated in posterior extremity.

Host: Trachemys dorbigni (Duméril & Bibron,

1835), Brazilian slider turtle

Infection site: small intestine

Collection site: Centro Agropecuário da Palma,

Capão do Leão, Rio Grande do Sul, Brazil

(31°48'01.1”S - 52°30'48.6”W).

D e p o s i t e d s p e c i m e n s : 5 0 5 - 5 0 7

(CHLPAS/UFPel).

According to MacDonald & Brooks (1989), T.

corti is the most problematic species of the

genus, and 13 synonyms have been suggested.

The species occurs in several hosts, shows a

wide geographic distribution exhibiting a high

degree of intra-specific variation.

Moravec & Vargas-Vázquez (1998) considered

that T. corti is conspecific with Telorchis

attenuata Goldberger, 1911 reported in

Trachemys scripta (Schoepff, 1792) in Mexico

(Moravec &Vargas-Vázquez, 1998). The

identification of the species found in T. dorbigni

in southern Brazil was done according to the

description and the key proposed by MacDonald

& Brooks (1989).

In South America, T. corti was reported

parasitizing the small intestine of Trachemys

callirostris (Gray, 1856) in Colombia, with

lower indexes to those found for this helminth in

T. dorbigni in Brazil (Table 1). In the Colombian

chelonian T. corti occurred in 0.76% of the hosts

with intensity of 18.5 and abundance of 0.14

(Lenis & Vélez, 2011).

In Brazil, T. corti was reported in a specimen of

T. dorbigni that was run over and killed on a

highway in the Municipality of Capão do Leão,

posterior extremity cirrus sac to near zone

pretestes, occupying the middle third of the

body. Eggs 27.5 – 38 (31.87 ± 2.29) long by 15 –

20 (18.27 ± 1.54) wide. Excretory vesicle

Y–shape; pore terminal.

Host: Trachemys dorbigni (Duméril & Bibron,

1835), Brazilian slider turtle

Infection site: small intestine

Collection site: Pelotas, Rio Grande do Sul,

Brazil (31°46'16.9”S - 52°18'45.9”W;

31°46'24.3” S - 52°19'13.8” W; 31°46'22.0”S -

52°19'04.2”W; 31°45'44.3”S - 52°19'46.7”W;

31°45'48.6”S - 52°19'47.0''W); Centro

Agropecuário da Palma, Capão do Leão, Rio

Grande do Sul, Brazil (31°4750.0” S -

52°29'43.0” W).

D e p o s i t e d s p e c i m e n s : 4 8 1 - 5 0 4

(CHLPAS/UFPel), 37846 – 37850 (CHIOC).

Telorchis achavali Mañé-Garzon & Hollman-

Spector, 1973 (Figs. 7 - 12)

Description. Based on 3 helminths. Body

elongate 13.12 – 17.55mm (14.8mm ± 2.39)

long by 575 – 1125 (783.33 ± 298.25) wide (the

level of the ovary). Oral sucker subterminal 125

- 195 (167.5 ± 37.33) long by 155 – 220 (194.16

± 34.49) wide, prepharynx short, pharynx

muscular 77.5 – 125 (105.83 ± 25.04) long by

10.5 – 152.5 (128.33 ± 22.68) wide. Oesophagus

absent. Double caeca, unbranched, extending

back to posterior body at a distance 25 – 100

(66.66 ± 38.18) long from posterior extremity.

Acetabulum intercaecal 120 – 200 (166.66 ±

41.63) diameter. Testes spherical and vertical,

intercaecal situated in posterior extremity,

anterior testes 230 – 380 (306.66 ± 75.05) long

by 230 – 370 (310 ± 72,11) wide and posterior

testes 280 – 360 (316.66 ± 40,41) long by 280 –

360 (316.66 ± 40.4) wide situated 250 – 325 (300

± 43.3) from posterior extremity. Cirrus sac

muscular and well developed. Genital pore

ventral, median, intercaecal, pre-acetabular.

Ovary rounded, intercaecal with 340 – 500

(403.33 ± 85.04) long by 290 - 430 (383.33 ±

80.82). Distance between ovary and acetabulum

3750 – 5500 (4333.33 ± 1010.36) and distance

between ovary and anterior testes 5650 – 7600

(6458.33 ± 1016.83). Seminal receptacle and

DISCUSSION

Neotrop. Helminthol., 7(2), 2013

205

Figures 1 – 2. Telorchis corti stained with Langeron's carmine. 1 – Anterior region, oral sucker (os); pharynx (ph); Oesophagus

(oe); caeca (c) (bar = 70µm). 2 – Median region, genital pore (gp); acetabulum (ac); cirrus sac (sc) (bar = 82.5µm)

Figures 3 – 4. Telorchis corti stained with Langeron's carmine. 3 – Median region, seminal vesicle (sv); vitellaria (v); ovary (ov)

(bar = 150µm). 4 - Median region, ovary (ov); Mehli's gland (mg) (bar = 260µm).

206

Mascarenhas& Müller

Telorchis spp. in Trachemys dorbigni

Figures 5 – 6. Telorchis corti stained with Delafield's hematoxylin. 5 – Posterior region, uterus (u); anterior teste (at); posterior

teste (pt); caeca (c); vitellaria (v) (bar = 290µm). 6 - Posterior region, posterior teste (pt); caeca (c) (bar = 100µm).

Telorchis corti and T. achavali, as well as the

other species of Telorchis, have a tegument with

spines (Stunkard, 1915; Mañé-Garzon &

Hollman-Spector, 1973; Font & Lotz, 2009). We

did not observe spines in the specimens found in

T. dorbigni, which probably have been lost in the

freezing process of the hosts. We examined the

specimens that were prepared by Pesenti et al.

(2009), in which we could clearly observe the

spines, which are abundant in the anterior region

of the body. It is important to highlight that in

this case the Digenea were prepared shortly after

the death of the host.

Regarding the life cycle of the species of

Telorchis, Font & Lotz (2009) reported the

participation of pulmonate mollusks as the first

intermediate hosts in which the cercariae

develop; tadpoles and mollusks are the second

intermediate hosts where cercariae develop to

metacercariae. The parasites reach the sexual

maturity in amphibians and reptiles, which

become infected by eating tadpoles and

mollusks with metacercariae.

Rio Grande do Sul State. Sixty-eight helminths

were found parasitizing the small intestine of

that host (Pesenti et al., 2009).

In Uruguay, two species were described, T.

dubios and T. achavali, parasitizing the small

intestine of T. dorbigni (Mañé-Garzon &

Hollman-Spector, 1968; Mañé-Garzon &

Hollman-Spector, 1973). The main

characteristic that distinguished T. corti (the

present study) from T. dubios (Mañé-Garzon &

Hollman-Spector, 1968) was that the latter have

a transversely elongate ovary. Also, T. dubios

(Mañé-Garzon & Hollman-Spector, 1968)

differed from T. achavali (the present study),

since the latter did not have an esophagus, the

ovary was spherical, and the cirrus sac was

muscular and well developed. In the present

study, T. achavali differed from T. corti mainly

because it was greater than T. corti, did not have

an esophagus, and its cirrus sac was muscular

and well-developed. This is the first record of T.

achavali in Brazil.

Figures 7 – 10. Telorchis achavali stained with Langeron's carmine. 7 - Anterior region, oral sucker (os); pharynx (ph); caeca (c)

(bar = 152.5µm). 8 – Median region, cirrus sac (sc); vitellaria (v) (bar = 210µm). 9 - Median region, vitellaria (v); cirrus sac (sc)

(bar = 210µm). 10 - Median region, uterus (u); ovary (ov) (bar = 430µm).

Neotrop. Helminthol., 7(2), 2013

207

208

Mascarenhas& Müller

Telorchis spp. in Trachemys dorbigni

and Elodea spp.). Pereira (1998), by analyzing

feces from nine individuals, recorded as food

items insects, grass, seeds, algae, fragment of

bones, and scales. The ingestion of mollusks was

reported by Hahn (2005) who studied the

stomach content of 75 turtles and reported that

85.27% of the diet was composed of plant matter

and 13.23%, and the total volume was

represented by animal matter (mollusks,

crustaceans, arthropods, Hirudinea, and

vertebrates). With regard to vertebrate as a

component of T. dorbigni's diet, Hahn (2005)

identified Anura, in two turtles, and

Characiformes in another. Bujes et al. (2007)

recorded T. dorbigni preying on the golden

mussel Limnoperna fortunei (Dunker, 1857), a

bivalve mollusk originating from Southeast Asia

and introduced into Rio Grande do Sul State in

the 1970s (Mansur et al., 2003). They also

analyzed the fecal content from eight specimens

and recorded the presence of gastropods,

crustaceans, plant matter, sand, and synthetic

material.

Studies on the diet may help investigations of

helminth fauna and vice versa. Lenis (2009)

studied digenetic helminths of T. callirostris and

Podocnemis lewyana Duméril, 1852, as well as

the diet of these hosts, through analysis of

stomach and intestinal contents of some

individuals, and collected limnic mollusks to

identify the possible intermediate hosts,

concluding that the omnivorous diet of T.

callirostris could favor the transmission of

digenetic helminths, for example, T. corti that

uses mollusks and tadpoles as intermediate

hosts.

Regarding T. dorbigni 's diet, there are studies

carried out in the State of Rio Grande do Sul,

Brazil, with individuals in captivity (Lema &

Ferreira, 1990) and in the wild environment

(Pereira, 1998; Hahn, 2005; Bujes et al., 2007).

Lema & Ferreira (1990) reported that chelonians

fed on snakes, frogs, teleosts, saurians,

caecilians, Oligochaeta, bovine meat, and

lettuce. Moreover, they observed the

consumption of floating plants (Eichornia spp.

Figures 11 – 12. Telorchis achavali stained with Langeron's carmine. 11 - Posterior region, uterus (u); anterior testes (at);

posterior testes (pt); caeca (c) (bar = 330µm). 12 - Posterior region, anterior testes (at); posterior testes (pt); caeca (c) (bar =

330µm).

Neotrop. Helminthol., 7(2), 2013

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209

During the collection of helminths we noticed

that some turtles ingested gastropod mollusks,

however, future studies should be conducted to

identify the food items that were part of the diet

of the turtles examined.

Special thanks to “Instituto Chico Mendes de

Conservação da Biodiversidade (ICMbio)” for

the permission (N° 23196); and to colleagues

Fabiana Fedatto Bernardon, Natasha Carvalho

Aires, Adriano Alves Menna; and, especially

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ACKNOWLEDGEMENTS

Correspondence to author/ Autor para

correspondencia:

Carolina S. Mascarenhas

Laboratório de Parasitologia de Animais Silvestres,

Departamento de Microbiologia e Parasitologia

(DEMP), Instituto de Biologia (IB), Universidade

Federal de Pelotas (UFPel), Campus Universitário,

caixa postal: 354, CEP 96010-900, Pelotas, RS,

Brasil.

E-mail / Correo electrónico:

phrybio@hotmail.com.br

Received June 3, 2013.

Accepted September 6, 2013.

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