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Parasitic Enteritis Associated with the Camallanid Nematode Serpinema

microcephalus in Wild Invasive Turtles ( Trachemys , Pseudemys , Graptemys ,
and Ocadia ) in Spain

Article  in  Journal of Herpetological Medicine and Surgery · March 2015

DOI: 10.5818/1529-9651-25.1.48

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 Parasitic Enteritis Associated with the Camallanid
Nematode Serpinema microcephalus in Wild
Invasive Turtles (Trachemys, Pseudemys,
Graptemys, and Ocadia) in Spain
Albert Martínez-Silvestre1, DVM, MSc, PhD, DECZM (Herpetology), Acred. AVEPA
(Exotic Animals), David Guinea1, DVM, David Ferrer2, DVM, PhD, Nikola Pantchev3,
DVM, DrMedVet, FTA Parasitology
1. CRARC (Catalonian Reptile and Amphibian Rehabilitation Center), 08783 Masquefa, Barcelona,
Spain

2. Laboratori de Parasitologia, Facultat de Veterinària, Universitat Autònoma de Barcelona, 08193

Bellaterra (Cerdanyola del Vallès), Barcelona, Spain

3. IDEXX Vet Med Labor GmbH, 71636 Ludwigsburg, Germany

Abstract: This cross-sectional study characterized the prevalence of enteritis associated with Serpinema
microcephalus infections in the intestinal tracts of red-eared slider turtles (Trachemys scripta elegans), river
cooters (Pseudemys concinna), false map turtles (Graptemys pseudogeographica), and Chinese stripe-necked
turtles (Ocadia sinensis) in Spain. All four species (three American, one Asiatic) were introduced into Spain
through the pet trade. S. microcephalus is an Old World nematode that has been found to parasitize both
invasive and native turtles. This parasite causes a significant inflammatory reaction in the intestines of exotic
turtles that is not usually seen in native species. Parasites were detected in 27/70 turtles examined (38.6%;
95% confidence interval: 27.2–51%). Total worm counts ranged from 5 to 21. The nematodes were always
found in the enteric mucosa of the duodenum and jejunum. The lesions in the turtles varied but included
catarrhal to ulcerative enteritis and secondary hemorrhage surrounding the parasitized areas.

Key Words: enteritis, intestinal nematode, invasive species, Serpinema microcephalus, parasite.

Introduction with another species from the genus Serpinema, Serpinema

The presence of wild invasive freshwater turtles in Spain is
becoming increasingly common. In their native range, these
turtles may be exposed to a variety of parasites that are
habituated to them (Conboy et al., 1993); however, when
introduced into a new area, it is not always possible to pre-
dict how these hosts will respond to the parasites of that
region. The camallanid nematode Serpinema microcephalus
is an important parasite of turtles of the western Palaearctic
(Baker, 1979; Yildirimhan and Sahin, 2005; Hidalgo-Vila
et al., 2009), with high parasite prevalences reported in native
species (85.7%, Mauremys leprosa; 66.7%, Emys orbicularis)
(Hidalgo-Vila et al., 2009). However, in the same study, S.
microcephalus was also found to parasitize an invasive exotic
turtle (Trachemys scripta elegans), with a parasite prevalence
of 93.8% (Hidalgo-Vila et al., 2009). Furthermore, Hidalgo-
Vila et al. (2011) found pancreatitis in 3/19 T. s. elegans that
were infested with S. microcephalus. Affected animals had
central necrotic areas in their pancreas that were surrounded
by leukocytes that obstructed exocrine tissue and were asso-
ciated with parasite life stages. Moreover, blood screening of
3 females revealed eosinophilia and hyperglycemia, which
can be associated with both helminth infections and pancre-
atic disorders, respectively.
Under normal conditions, T. s. elegans and Chrysemys
picta are infected within their natural range in the Nearctic
trispinosum (Baker, 1979; Conboy et al., 1993; Hidalgo-Vila
et al., 2009; Oi et al., 2012). Asakawa et al. (2001) found S.
microcephalus (Ocadia sinensis, Siebenrockiella crassicollis)
and S. trispinosum (Graptemys geographica, T. s. elegans,
Chelydra serpentina) in pet turtles imported to Japan from
foreign reptile farms. Although S. microcephalus is regarded
as native in Japan, it could be detected in wild invasive T. s.
elegans at only one locality (Nerima). The prevalence of the
parasite in these turtles was 53.8%, and the mean parasite
density was 2.3 parasites/animal (Oi et al., 2012). Serpinema
trispinosum and S. microcephalus differ not only in regard to
their natural distribution but also based on their cephalic
structures (e.g., pattern of arrangement of longitudinal
ridges in the buccal capsule) (Baker,1979). There is no
molecular test available to distinguish these parasites from
one another.
The genus Serpinema belongs to the nematode superfam-
ily Camallanoidea. The latter includes 8 clearly related
­genera with approximately 150 species with a cosmopolitan
distribution. Nearly 40 of these parasites are found in
amphibians and reptiles (especially turtles), with the remain-
der primarily infecting fish (Anderson, 2000). Camallanid
nematodes are parasites of the stomach and intestinal tract.
At this time, there are two genera of camallanid parasites
that appear to be important in turtles, Camallanus (5 species
that infect turtles) and Serpinema (12 species that infect

48 Journal of Herpetological Medicine and Surgery Volume 25, No. 1–2, 2015
t­ urtles) (Gagno, 2006; Kuzmin et al., 2011). Serpinema and
Camallanus are morphologically similar, and the majority of
Serpinema species were once described within the genus
Camallanus. In 1960, the genus Serpinema (Yeh, 1960) was
created to include turtle parasites with characteristic buccal
capsules that possess a gap between the dorsal and ventral
groups of ridges on each of the buccal capsule valves. This
separation has been further supported by Kuzmin et al.
(2011) with molecular data (28S rDNA) from Camallanus
spp. and Serpinema octorugatum.
The purpose of this study was to perform a cross-sectional
study to characterize the health status of 4 different species
of invasive aquatic turtles (T. s. elegans, Pseudemys con-
cinna, G. pseudogeographica, O. sinensis) in Barcelona,
Spain. Animals collected for the study were removed during
managed eradication projects and submitted for post-mortem
examination and histological analysis. A specific aim of the
study was to determine the prevalence of camallanid nema-
todes (S. microcephalus) in these non-native turtles and
characterize any pathology associated with the parasites.
Materials and Methods
During 2012 and 2013, an invasive aquatic turtle species
eradication program was performed in freshwater areas near
the city of Barcelona. The goal was to remove invasive tur-
tles from Mediterranean ecosystems. A total of 189 turtles
were captured during the program. Of this total, 70 turtles
were non-native invasive species, including 50 T. scripta, 9
P. concinna, 5 G. pseudogeographica, and 6 O. sinensis. All of
the non-native turtles were adults and had no obvious signs
of disease. The turtles were sacrificed using the humane pro-
tocols specified for reptiles (Forrest, 1998).
At necropsy, fresh samples of intestine were removed and
screened for the presence of parasites. Tissue sections from
intestine, liver, pancreas, lung, kidney, stomach, and spleen
(approximately 0.5–1 cm wide) were also collected and fixed
in 10% neutral buffered formalin, embedded in wax paraf-
fin, and sectioned at 3 µm. Sections were mounted on glass
slides, stained with hematoxylin-eosin, and examined
through bright-field microscopy.
All observed parasites were collected and fixed in 70% eth-
anol until referral to the laboratory of Parasitology, Faculty
of Veterinary Medicine, Autonomous University of
Barcelona. Parasites were washed, mounted, and observed
under a light microscope. Taxonomic keys were used to
identify the parasites (Baker, 1979).
Results
Parasites were detected in 27/70 turtles examined (38.6%;
95% confidence interval [CI]: 27.2–51%; Table 1). They were
found in 22 (31.4%, 95% CI: 20.5–42.3) T. s. elegans, 3 (4.3%,
95% CI: 0.1–9.8) P. concinna, 1 (1.4%, 95% CI: 0.1–3.7) G.
pseudogeographica, and 1 (1.4%, 95% CI: 0.1–3.7) O. sinen-
sis. Total worm counts ranged from 5 to 21. The nematodes
were always found in the mucosa of the duodenum and jeju-
num (Fig. 1). Adults were 5–10 mm in length and evident on
light microscopy based on their bright red color.
Because there are no apparent differences in male repro-
ductive structures in the posterior end of Serpinema species,
cranial structures were used to identify the nematodes.
Among them, the shape of the buccal valves and the number
Volume 25, No. 1–2, 2015
and width of ridges therein demonstrated that the species
present in all cases were S. microcephalus (Baker, 1979). The
shape of buccal valves in lateral view is significantly differ-
ent between the 2 species of nematodes (Fig. 2). Serpinema
microcephalus have fewer (8–11) ridges than S. trispinosum
(15–19), and the ridges are markedly thicker and more
widely separated by the median zone of the valves, which
separates the long ridges into dorsal and ventral groups.
Short ridges are only rarely observed in S. microcephalus.
All of the parasitized turtles showed varying degrees of
enteritis (Fig. 3); 18 of the turtles had catarrhal enteritis
(non-suppurative, presence of mononuclear leukocytes:
lymphocytes and macrophages), 8 had hemorrhagic enteritis
(secondary hemorrhages were found surrounding the para-
sitized areas), and a single turtle had ulcerative enteritis
(a loss of mucosal layers with a lymphocytic proliferative reac-
tion and granulation tissue at the base of the ulcer) (Table 1).
Parasites were found in all affected sections of the intestine.
Intestinal pleats (17/27, 62.9%), gastritis (5/27, 18.5%), and
pancreatitis (2/27, 7.4%) were also found in some of the tur-
tles. All of the turtles had some degree of hepatic lipidosis. No
turtle was cachexic, but 2 animals were notably obese. No
other parasites (helminths) were detected within the intestines.
Discussion
Serpinema microcephalus is a helminth nematode from the
family Camallanidae that is characterized by a cephalic
structure with ridges in the buccal valves (Baker, 1979). It is
a common species in Old World turtles, while S. trispinosum
is common in North American turtles (Gagno, 2006), and
S. octorugatum is common in Asian turtles (Sharma et al.,
2002). In the native range of red-eared sliders, the Nearctic
region, S. trispinosum would be the most common nematode
to parasitize the turtles (Esch et al., 1979); however, in the
colonized areas of Spain that these turtles have invaded,
S. microcephalus is more common. The findings of this
study suggest that these two parasites indeed fill a similar
niche within these regions (Palearctic and Nearctic)
(Hidalgo-Vila et al., 2009).
Serpinema microcephalus is a heteroxenous parasite that
typically uses the Spanish terrapin, M. leprosa, as its defini-
tive host. In M. leprosa, S. microcephalus can be found in
high numbers without causing any clinical signs of disease
(Villaran and Dominguez, 2009). This nematode has also
been reported in the European pond terrapin (E. orbicularis)
(Yildirimhan and Sahin, 2005). The life cycle of Serpinema
has not been fully elucidated; however, it is likely similar to
that of Camallanus oxycephalus, a closely related nematode,
in which copepods (e.g., Cyclops spp., microcrustaceans,
zooplankton) serve as intermediate hosts and fish as
paratenic (transport) hosts (Conboy et al., 1993). Some
developmental steps in the parasite’s life cycle appear to be
similar among the species studied. For example, the first lar-
vae hatch in utero (Fig. 4) and are passed into the water
either via fecal material or from a ruptured, gravid female;
the gravid female may rupture after exiting the host’s anus
and reaching the water, thus releasing the larvae. Further
development into third-stage larvae occurs in intermediate
hosts (e.g., copepods or other crustaceans). When a suitable
final host (e.g., turtle) eats one of the infected copepods, the
life cycle is completed. However, it is also possible that a
paratenic host (e.g., snails, fish, amphibians) may eat the
Journal of Herpetological Medicine and Surgery 49
Table 1. Parasite and pathologic findings for 27 invasive turtle species captured in Barcelona, Spain.

Necropsy Location of Number of Type of

number Species parasites parasites enteritis Liver Other findings

433 T. scripta Duodenum 9 Catarrhal Hepatic lipidosis

435 T. scripta Duodenum 16 Catarrhal Hepatic lipidosis Gathered intestinal pleats

436 P. concinna Duodenum 15 Hemorrhagic Hepatic lipidosis Gastritis, gathered

intestinal pleats, obesity

437 T. scripta Duodenum Hemorrhagic Hepatic lipidosis Gathered intestinal pleats

438 T. scripta Duodenum 15 Catarrhal Gathered intestinal pleats

441 T. scripta Duodenum 12 Hemorrhagic Severe hepatic Gathered intestinal pleats

lipidosis

442 T. scripta Duodenum 18 Hemorrhagic Hepatic lipidosis Gathered intestinal pleats,

polyserositis

443 T. scripta Duodenum 20 Hemorrhagic Hepatic lipidosis Gathered intestinal pleats

444 T. scripta Duodenum 18 Hemorrhagic Hepatic lipidosis Gastritis, gathered

intestinal pleats, general
edema

445 P. concinna Duodenum 17 Catarrhal Hepatic lipidosis

448 T. scripta Duodenum 19 Catarrhal Hepatic lipidosis

449 T. scripta Duodenum 16 Ulcerative Hepatic lipidosis Gastritis

450 T. scripta Duodenum 18 Catarrhal Hepatic lipidosis Gathered intestinal pleats,

obesity

452 T. scripta Duodenum 8 Hemorrhagic Hepatic lipidosis Gathered intestinal pleats,

obesity

455 T. scripta Duodenum 19 Catarrhal

456 T. scripta Duodenum 20 Catarrhal Hepatic lipidosis Gathered intestinal pleats

458 T. scripta Duodenum 16 Catarrhal Hepatic lipidosis

480 T. scripta Duodenum 18 Catarrhal Hepatic lipidosis Gathered intestinal pleats

482 T. scripta Duodenum 21 Catarrhal Hepatic lipidosis Pancreatitis

484 T. scripta Duodenum 10 Catarrhal Hepatic lipidosis Pancreatitis

487 T. scripta Duodenum, 8 Catarrhal Hepatic lipidosis Gathered intestinal pleats

jejunum

490 G. pseudogeographica Duodenum 21 Hemorrhagic Severe hepatic Gathered intestinal pleats

lipidosis

493 T. scripta Duodenum 9 Catarrhal Hepatic lipidosis Gastritis

496 T. scripta Duodenum 15 Catarrhal Hepatic lipidosis Gastritis, gathered

intestinal pleats

497 T. scripta Duodenum, 5 Catarrhal Hepatic lipidosis

jejunum, ileum

512 P. concinna Duodenum 10 Catarrhal Severe hepatic Gathered intestinal pleats

lipidosis

518 O. sinensis Duodenum 9 Catarrhal Gathered intestinal pleats

50 Journal of Herpetological Medicine and Surgery Volume 25, No. 1–2, 2015
 Figure 1. Serpinema microcephalus anchored to the duodenal
mucosa of a river cooter (Pseudemys concinna). Bar = 1 cm.
Figure 2. Cephalic extremity showing ridges in buccal valves
(lateral view); specimen of Serpinema microcephalus (present
study) is on the right, and a specimen of S. trispinosum is on the
left (from the small intestine of an imported Chrysemys picta
belli).
Figure 3. Intestinal mucosa from a river cooter (Pseudemys
concinna). Note the presence of cross sections of parasite stages
(black arrows) in the mucosa and a lymphoplasmacytic infil-
trate (white arrow). Hematoxylin and eosin stain.
Volume 25, No. 1–2, 2015
Figure 4. Parasite uterus with first-stage larvae of Serpinema
trispinosum from a Trachemys scripta elegans (histology; hema-
toxylin and eosin stain; longitudinal section; 200×).
intermediate host, allowing for a fourth-stage larvae to
develop (Anderson, 2000). Until recently, the third-stage lar-
vae of S. trispinosum were only found to infect aquatic snails
and planktonophagous fish as paratenic hosts (Gonzáles
and Hamann, 2007). However, subsequent studies have
showed the presence of third-stage larvae in Lysapsus limel-
lum, an anuran from the family Hylidae, and another study
found third-stage larvae of S. trispinosum in 4 species of
adult aquatic damselflies (Wiles and Bolek, 2012). Based on
these findings, it is possible that captive turtles can become
infected with this parasite if intermediate hosts (e.g., micro-
crustaceans) are present in artificial ponds or aquariums
(Conboy et al., 1993). Many of these intermediate or
paratenic hosts are common in the diet of omnivorous fresh-
water turtles (Trachemys, Pseudemys). When the parasite
reaches the intestinal tract of the definitive host, it anchors
into the gastrointestinal mucosa to feed. In other European
countries where these turtles have been introduced, other
exclusive parasites of these ecosystems have been described,
such as hemoparasites or flukes in Austria (Hassl and
Kleewein, 2012). Moreover, there are already data on the
presence of S. microcephalus in natural habitats where
T. s. elegans have been introduced, such as Spain (Hidalgo
et al., 2009) and Japan (Asakawa et al., 2001; Oi et al., 2012).
Interestingly, there has been no report of a European turtle
species being infected with S. trispinosum even though they
are sharing their native waters with the foreign invaders (T.
scripta elegans) that harbor the parasite. This difference may
occur as a result of a more pronounced host specificity for S.
trispinosum compared to S. microcephalus or ecological fac-
tors, such as composition of intermediate or transport hosts,
within the habitat. Furthermore, there is only scarce infor-
mation regarding the pathogenicity of S. trispinosum in its
natural hosts. Conboy et al. (1993) found weight loss,
anorexia, and blood-stained, mucoid feces as clinical signs
associated with infection, while Marcus (1981) reported that
abscess formation within the gastrointestinal mucosa was
possible because of the deep attachment of the parasite
within these tissues.
Journal of Herpetological Medicine and Surgery 51
 Serpinema microcephalus has been found to induce patho-
logic lesions in non-native turtles in the past. For example,
parasitic pancreatitis was identified in T. s. elegans in the
Doñana National Park (Southern Spain) (Hidalgo et al.,
2011). Two animals sampled in the current study also showed
pancreatic lesions. In these cases, a mild granulocytic inflam-
matory infiltrate affecting up to 25% of the pancreatic
parenchyma was observed, although parasites were not seen
within the pancreatic tissue. However, all of the infected tur-
tles examined in the current study did have enteritis, includ-
ing one case that showed ulcerative enteritis with intestinal
perforation in the duodenum. In these cases, there was also
vascular neoformation with lymphocyte and eosinophil
migration to the parasites. Interestingly, the presence of S.
microcephalus is not known to be associated with inflamma-
tion in the Mediterranean turtles (M. leprosa or E. orbicu-
laris), where it is a common parasite (Villaran and
Dominguez, 1999; Yildirinham and Sahin, 2005). However,
based on the authors’ observations, this parasite generates a
significant reactive enteritis in Trachemys, Pseudemys,
Graptemys, and Ocadia. The relationship between hepatic
lipidosis and the abundance of parasites has not been fully
investigated; however, obesity and/or fatty liver could be
predisposing factors that debilitate and predispose the host
to more severe clinical disease. The gathered intestinal pleats
could be a response to the increase of peristalsis associated
with parasitism and the presence of gastrointestinal infec-
tion. The results of this study reinforce the generally held
belief that naive hosts translocated to a new ecosystem and
exposed to a new parasite can develop more severe lesions
than the typical host. This is an important consideration for
veterinarians and biologists working in reptile conservation
programs, as head-start animals and translocated animals
may be more susceptible to infectious and parasitic organ-
isms within those ecosystems.
The finding of S. microcephalus parasitizing P. concinna,
G. pseudogeographica, and O. sinensis is a new report. This is
the first time that these turtle species were found to serve as
an alternate host for this nematode in the Western Paleartic.
Given these preliminary results, it appears that a wide range
of parasitic relationships can be established in these new tur-
tle species in the European ecosystems they invade
(Martínez-Silvestre et al., 2011).
Acknowledgments: The authors wish to thank the
Generalitat de Catalunya (government of Catalonia, Spain)
for the legal permission to perform this research; the
Diputació de Barcelona, administrator of Parc del Foix, and
the Sant Cugat town hall for permission to develop the con-
trol programs to eradicate exotic turtles; and Joaquim Soler,
Silvia Merchan, and Isabel Verdaguer for their help in the
laboratory and with the necropsy procedures.
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