Chelonoidis chilensis

Rev. Ibero-Latinoam. Parasitol. (2010); 69 (2): 214-219
Comunicaciones
The ocurrence of gastrointestinal parasitism in
captive Argentinean Tortoise (Chelonoidis chilensis)
PELICHONE N.1, DEIS E.1, 2 and CUERVO P. 1, 2*
1
2
Parasitología y Enfermedades Parasitarias, Facultad de Ciencias Veterinarias y Ambientales, Universidad Juan A.
Maza. Mendoza, Argentina.
Área de Diagnóstico Parasitológico, Unidad de Práctica Veterinaria (UPV), Facultad de Ciencias Veterinarias y
Ambientales, Universidad Juan A. Maza. Mendoza, Argentina.
ABSTRACT
Three species of Neotropical tortoises inhabit Argentina, all of them considered nationally endangered.
Despite their conservation status, specific information available regarding pathogens and medicine is
scarce. Since gastrointestinal nematodes are frequently found in tortoises, the question arises about the
parasitological status of the tortoises inhabiting Argentina (particularly Chelonoidis chilensis, the most
frequent species in captivity). Thirty-three Argentinean Tortoises (C. chilensis), from Mendoza (Argentina)
were sampled for coproparasitological examination (Sheater’s sugar flotation technique, Ritchie’s formalinether sedimentation technique and Lumbreras’ rapid sedimentation technique). Epidemiological data was
also collected. Coprological results and epidemiological data were statistically analyzed..Twenty-three
(69.7%) animals were found positive to parasites (Families Pharyngodonidae and Ascarididae). Three
animals were only positive to “oxyurids”, and nine to “ascarids”, while 11 showed concomitant infections
with both families. No statistical differences were found in the posterior analysis..As far as we know there is
no published information regarding parasites of tortoises from Argentina or, specifically, from C. chilensis.
Results are similar to previous reports on other species, and further studies should be developed.
Key words: Chelonoidis chilensis, Argentinean Tortoise, gastrointestinal parasitism, “oxyurids”, “ascarids”.
RESUMEN
En Argentina existen tres especies de tortugas terrestres neotropicales, todas ellas consideradas en
peligro a nivel nacional. A pesar de su estado de conservación, la información específica disponible sobre
patógenos y medicina es muy escasa. Debido a que los nemátodes gastrointestinales son frecuentemente
hallados en tortugas terrestres, se plantea el interrogante sobre el estado parasitario de las tortugas terrestres
de Argentina (particularmente Chelonoidis chilensis, la especie más frecuente en cautiverio). Treinta y tres
Recibido: 22 de Julio 2010, Aceptado: 18 de Octubre 2010.
Corresponding: Pablo F. Cuervo
Address: Av. Acceso Este, Lateral Sur 2245, Guaymallén. Mendoza, Argentina.
Tel: 054-261-154708531
E-mail: [email protected]
214
GASTROINTESTINAL PARASITISM IN CHELONOIDIS CHILENSIS
ejemplares de Tortuga Terrestre Argentina (C. chilensis), de Mendoza (Argentina), fueron muestreadas
para examen coproparasitológico (Técnica de flotación simple con solución de azúcar, Sedimentación con
formo-éter y Sedimentación seriada rápida de Lumbreras). Además se colectó información epidemiológica,
y se analizaron estadísticamente los resultados obtenidos. Veintitrés (69,7%) animales fueron positivos a
parásitos (Familias Pharyngodonidae y Ascarididae). Tres individuos fueron positivos sólo a “oxiuros” y
nueve a “áscaris”, mientras que 11 mostraron infección concomitante de ambas familias. No se hallaron
diferencias estadísticamente significativas en los análisis posteriores. Hasta donde tenemos conocimiento,
no hay información publicada sobre los parásitos de tortugas terrestres de Argentina y, específicamente,
de C. chilensis. Los resultados obtenidos son similares a lo reportado para otras especies, pero se debe
continuar con el desarrollo de estudios futuros.
Palabras clave: Chelonoidis chilensis, Tortuga Terrestre Argentina, parasitismo gastrointestinal, “oxyuros”, “áscaris”.
INTRODUCTION
There are three Neotropical tortoises living in
Argentina: Chelonoidis carbonaria (Red-Footed
Tortoise), Chelonoidis donosobarrosi (Patagonian
Tortoise) y Chelonoidis chilensis (Argentinean Tortoise) (Richard, 1999). The last species may have
two subspecies: Chelonoidis chilensis chilensis y
Chelonoidis chilensis petersi (Rhodin et al., 2008),
although Chebez (2008) states that the subspecies
petersi is a sinonime of chilensis. C. chilensis is
considered Vulnerable by the IUCN Red List of
Threatened Species (2010), while the three species
are considered nationally endangered (Richard and
Waller, 2000; Ubeda and Grigera, 2003; Chebez,
2008).
In Argentina, tortoises have been traditionally
used for commercials purposes, principally as pets,
but also as part of subsistence economies (as bushmeat or as material for regional crafts) (Richard,
1999). But also deforestation, environment degradation and the competition for food with domestic
cattle (particularly goats) represent an important
threat to their conservation (Richard, 1999; Chebez, 2008).
Despite their conservation threat, information
available on the internal medicine and surgery of
these native species is almost inexistent. There are
a few documents about their biology and related
aspects, but fewer about medicine aspects (e.g.
Troiano, 1991); and when considering information
on parasites and parasitic diseases, specific published information is unavailable.
Since almost every reptile medicine textbook
Rev. Ibero-Latinoam. Parasitol. (2010); 69 (2): 214-219
coincide that gastrointestinal helminths are frequently found in quelonians (see McArthur et al.,
2004; Greiner and Mader, 2006; Jacobson, 2007),
the question arises about the parasitological status
of the tortoises inhabiting Argentina.
The aim of this study is to develop a parasitological survey on C. chilensis (the most common
species maintained in captivity in Argentina),
through coprological examination, particularly focused on nematodes.
MATHERIALS AND METHODS
The study was carried out during October, November and December of 2009, in central Mendoza
province (central-west Argentina. About 70% of the
province’s surface is occupied by the Monte Occidental phytogeographical region, characterized by
an arid warm temperate climate, with annual temperatures around 20ºC in the north and 13ºC in the
south. Rains are very scarce, fluctuating between
100 and 400 mm3, and commonly occurred during
summer (Parodi, 1964).
Feces samples from captive individuals of C.
chilensis (identified according to Chebez, 2008)
were collected and preserved in formol 4%. Feces
were analyzed with the Sheater’s sugar flotation
technique, Ritchie’s formalinether sedimentation
technique and the Lumbreras’ rapid sedimentation technique. Epidemiological data was collected
(sex, estimated age, living environment, presence
of other tortoises, presence of symptoms of gastrointestinal disease and previous treatments with
215
N. PELICHONE et al.
antiparasitics).
Gastrointestinal nematodes eggs were identified according to morphological characteristics
(Anderson, 2000; Foreyt, 2001; McArthur et al.,
2004; Greiner and Mader, 2006; Jacobson, 2007).
The differences between the coproparasitological
prevalences and the sexes, age classes (1-10, 11-20,
21-30, 31-40 and ≥ 41), living environments (access
to garden or tile floor) and presence of other tortoises
were evaluated using the c2 test and the Fisher’s
exact test or the Yate’s correction test (when needed).
Statistical analysis was performed using Statistix 7.0
- Analytical software for Windows, and p < 0.05 0.1 were used to indicate statistical significance.
Table1. Tortoises determined to be infected (+) or uninfected (-) at the coprological examination with
Pharyngodonidae and Ascarididae
Animal Age (years) Sex
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
28
11
45
15
3
5
20
40
18
30
5
20
25
5
20
30
20
38
33
30
10
10
15
30
30
20
15
17
3
20
22
33
42
M
M
F
F
Nd
Nd
M
M
F
F
M
F
M
Nd
F
F
F
M
M
M
M
M
M
M
F
M
F
M
Nd
M
M
F
M
Habitat
PoT
GS
AT
CE
P
A
G
G
G
G
G
TF
TF
G
G
G
G
G
G
G
G
TF
TF
G
G
G
G
G
G
TF
TF
TF
G
TF
G
G
G
G
G
Y
Y
Y
N
N
N
N
N
Y
Y
Y
N
Y
N
Y
N
Y
Y
Y
N
Y
Y
N
Y
Y
Y
N
Y
N
Y
Y
Y
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
N
+
+
+
+
+
-
+
+
+
+
+
-
+
+
+
-
-
+
-
-
-
+
+
+
+
+
-
+
-
+
+
-
+
-
+
-
-
-
-
+
-
+
+
+
-
+
+
-
-
-
+
-
-
-
+
+
-
-
-
-
+
-
+
+
-
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
PoT presence of other tortoise, GS gastrointestinal symptoms, AT previous antiparasitic treatment, CE coprological
examination, P Pharingodonidae, A Ascarididae, F female, M male, Nd not determined, G grass, TF tile floor, Y yes,
N no, + presence of parasites, - absence of parasites.
216
Rev. Ibero-Latinoam. Parasitol. (2010); 69 (2): 214-219
GASTROINTESTINAL PARASITISM IN CHELONOIDIS CHILENSIS
RESULTS
Thirty-three tortoises were included in the survey: 18 males, 11 females and four not determined;
seven ≤ 10 years old, 12 >10 years old, eight > 20
years, four > 30 years old and two > 40 years old;
25 have access to garden and 8 live in tile floor;
finally 21 live with other/s individual/s of C. chilensis, while 12 live alone. None of the animals
showed signs of gastrointestinal disease or were
previously dewormed (Table 1).
Eggs of oxyurids (Oxyurida: Pharyngodonidae)
(Figure 1) and ascarids (Ascaridida: Ascarididae)
(Figure 2) were identified in 23 (69.7%) of the
sampled tortoises. Three animals (9.1%) were only
positive to oxyurids, and nine (27.3%) only positive
to ascarids, while 11 (33.3%) showed concomitant
infection with both kind of eggs. Summarizing, 14
animals (42.4%) were found positive to oxyurids
and 20 (60.6%) to ascarids.
No statistical differences were found between
parasitological affection and sex, estimated age,
living environments or presence of other tortoises;
nor between type of parasite and the epidemiological
data. Only when applying p < 0.1, a correlation
between sex and presence of oxyurids is found, and
a weak association with males is inferred.
Figure 1. Eggs of Pharingodonidae (40x).
DISCUSSION
As far as we know, there is no published information regarding parasites of tortoises from Argentina or, specifically, of Argentinean Tortoise C.
chilensis. The high number of affected animals and
the type of parasites detected are coincident with
previous reports on other species around the world
(e.g. Nathanael et al., 2004; Tittoto de Oliveira et
al., 2005; Traversa et al., 2005).
Several authors state that herbivore reptiles
present a wider nematode fauna than carnivores
(Bowie, 1974; Roca, 1999). It is strongly suggested that these nematodes live in balance with
their hosts (Roca et al., 1988; Roca and Carbonell,
1993), causing no damage to the hosting reptile.
Gastrointestinal helminths are frequently found
in quelonians, being generally considered to be
nonpathogenic (Mitchell and Figueroa, 2005) and
rarely involved as significant pathogens (Jacobson,
2007). A tortoise, in good physiological condition,
Rev. Ibero-Latinoam. Parasitol. (2010); 69 (2): 214-219
Figure 2. Egg of Ascarididae (40x).
may harbor around 5000 and 20000 nematodes
(Petter, 1966). According to Petter (1966), Iverson
(1982) and Roca (1999) the colon of herbivore reptiles, usually with a dilated portion, provides a very
suitable microhabitat to the nematode population,
217
N. PELICHONE et al.
with abundant remains of undigested vegetal material. Furthermore, Roca (1999) suggests that the
massive amount of nematodes in the colon of tortoises have trespassed the parasitism’s barrier, constituting an endocomensalism or even a mutualism.
Quelonian’s nematodes, particularly Pharyngodonidae, usually have direct life cycles and the eggs
could be ingested due to geophagy or coprophagy,
habits frequently observed in these animals (Sokol, 1967, 1971; Iverson, 1982; Richard, 1999;
McArthur et al., 2004). When considering that,
in Argentina, captive tortoises usually inhabit in
reduced environments (with garden or tile floor),
re-infestations could explain the high affection observed.
No statistical association was observed when
contrasting the parasitological affection or type of
parasite with epidemiological data. Information on
epidemiology is scarce, not allowing major discussion. Traversa et al. (2005) only report a positive
association between intensity of oxyurids (epg,
eggs per gram) - animals ageing from 1 to 5 years
and oxyurid intensity (epg) - animals living in open
enclosure, but this data was not confirmed in the
present study.
Further identification of the parasites detected
was not achieved, since no necropsies or faecal
culture (Baermann technique, as suggested by Traversa et al., 2005) were implemented. The results
obtained, but not expected, justify futures studies
on the theme, particularly regarding the identification up to species level, performing necropsies
when feasible and a quantification of the parasite
burdens.
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Acknowledgements: We want to acknowledge MV. Mag.
Roberto Mera y Sierra, MV. Omar Gonzales Viera, MSc.
Diego Soler Trovar, MSc. Bernardo Mesa Cruz, MV. Javier
Origlia and Dr. Donato Traversa for their uninterested collaboration.
219