ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043
Neotropical Helminthology, 2018, 12(2), jul-dic:201-211.
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
TEMNOCEPHALIDS ON TRACHEMYS DORBIGNI (DUMÉRIL & BIBRON, 1835) (TESTUDINES,
EMYDIDAE): IMPLICATIONS OF ANTHROPOGENIC ENVIRONMENTS AND TURTLE'S GENDERS
IN SYMBIOTIC RELATIONSHIPS
TEMNOCÉFALOS SOBRE TRACHEMYS DORBIGNI (DUMÉRIL & BIBRON, 1835) (TESTUDINES,
EMYDIDAE): IMPLICANCIAS DE LOS AMBIENTES ANTROPOGÉNICOS Y LOS GÉNEROS DE LAS
TORTUGAS EN LA RELACIÓN SIMBIÓTICA
*Laboratório de Parasitologia de Animais Silvestres, Instituto de Biologia, Departamento de Microbiologia e Parasitologia,
†
Universidade Federal de Pelotas. Caixa Postal 354, 96010-900, Pelotas, RS, Brazil; Laboratório de Biologia de Parasitos de
Organismos Aquáticos, Instituto de Ciências Biológicas, Universidade Federal do Rio Grande. Avenida Itália, Km 08, s/n,
Caixa Postal 474, 96201-900, Rio Grande, RS, Brazil.
* Corresponding author: E-mail: phrybio@hotmail.com
* † *
Carolina Silveira Mascarenhas ; Renato Zacarias Silva & Gertrud Müller
ABSTRACT
Keywords: Brazil – freshwater turtles – rural area – Temnocephala – turtle's genders – urban area
We studied the association between epibiont helminths temnocephalids and the freshwater turtle
Trachemys dorbigni (Duméril & Bibron, 1835), comparing urban and rural environments and turtle's
genders. Sixty specimens of T. dorbigni were collected in urban canals and rural lakes at two locations in
Rio Grande do Sul, southern Brazil. Temnocephala pereirai Volonterio, 2010 and Temnocephala sp.
(Temnocephalidae) were found associated with T. dorbigni only in rural environments. There was a
positive relationship between epibiont helminths and males of T. dorbigni, suggesting that the population
dynamics of these helminths can be related to the behavior or reproductive condition of T. dorbigni.
Neotropical Helminthology
201
Volume12,Number2(jul-dec2018)
ÓrganooficialdelaAsociaciónPeruanadeHelmintologíaeInvertebradosAfines(APHIA)
Lima-Perú
VersiónImpresa:ISSN2218-6425VersiónElectrónica:ISSN1995-1043
RESUMEN
Palabras clave: Brazil – género sexual de las tortugas - Temnocephala - tortuga de agua dulce - zona rural - zona urbana
Se estudió la asociación entre los helmintos epibiontes de Temnocephalidae y la tortuga de agua dulce
Trachemys dorbigni (Duméril & Bibron, 1835), comparando los ambientes urbano y rural, y el género
sexual de las tortugas. Sesenta especímenes de T. dorbigni fueron recolectadas en canales urbanos y lagos
de la zona rural de dos localidades de Rio Grande do Sul, extremo sur de Brasil. Los epibiontes,
Temnocephala pereirai Volonterio, 2010 y Temnocephala sp. (Temnocephalidae), fueron encontrados
solamente en las tortugas de la zona rural. Se observó una relación positiva entre helmintos epibiontes y
los machos de T. dorbigni, sugiriendo que la dinámica poblacional de los helmintos esté relacionada con el
comportamiento y la condición reproductiva de T. dorbigni.
T e m n o c e p h a l a B l a n c h a r d , 1 8 4 9
(Temnocephalida,Temnocephalidae) consists of
31 nominal endemic species of the Neotropical
Region, associated with freshwater organisms such
as crustaceans (Damborenea & Cannon, 2001;
Amato et al., 2003, 2006; Volonterio, 2007; Seixas
et al., 2011; Seixas et al., 2018), insects
(Damborenea & Cannon, 2001; Amato & Amato,
2005; Amato et al., 2007, 2011), molluscs
(Damborenea & Cannon, 2001; Damborenea &
Bursa, 2008; Garcés et al., 2013; Seixas et al.,
2015) and freshwater turtles (Damborenea &
Cannon, 2001; Volonterio, 2010; Seixas et al.,
2014).
Most studies on temnocephalids associated with
freshwater turtles are taxonomic studies.
Temnocephalids have been reported mainly in
turtles of the family Chelidae from South America.
In Brazil, Temnocephala brevicornis (Monticelli,
1889) has been reported in the chelids
Acanthochelys spixii (Duméril & Bibron, 1835)
(Yuki et al., 1993), A. radiolata (Mikan, 1820),
Mesoclemmys gibba (Schweigger, 1812),
Hydromedusa tectifera Cope, 1870 (Pereira &
Cuocolo, 1940) and H. maximiliani (Mikan, 1820)
(Pereira & Cuocolo, 1940; Novelli et al., 2009). In
addition, Temnocephala sp. has been reported from
H. tectifera (Soares et al., 2007). In Uruguay, T.
brevicornis, T. pereirai Volonterio, 2010 and T.
cuocoloi Volonterio, 2010 have been recorded in H.
tectifera (Cordero, 1946; Volonterio, 2010). There
has been only one record of T. brevicornis in H.
tectifera (Brusa & Damborenea, 2000) in
Argentina. In emydid turtles, there has been a
report of association of T. brevicornis and T.
pereirai with Trachemys dorbigni (Duméril &
Bibron, 1835) in Rio Grande do Sul State, Brazil
(Yuki et al., 1993; Seixas et al., 2014).
Species richness in the urban-rural gradient has
been increasingly studied to assess the impact of
urbanization on biodiversity. Typically, urban
landscapes have presented less biological diversity
than rural environments (Mckinney, 2002;
Kowarik, 2011). The loss of biological diversity
has been linked to several direct and indirect
human actions (Hero & Ridgway, 2006). Thus,
increased urbanization and agricultural activity
202
Neotropical Helminthology, 2018, 12(2), jul-dic
INTRODUCTION
MATERIAL AND METHODS
cause modification or loss of habitats (Mckinney,
2002; Hero & Ridgway, 2006). These factors are
considered the main threats to biodiversity (Brooks
et al., 2002). In southern Brazil, for example,
wetland ecosystems are undergoing rapid changes
and significant area loss due mainly to agricultural
activities and actions driven by urbanization, such
as landfills and garbage and sewage dumps
(Carvalho & Ozório, 2007).
Trachemys dorbigni (Duméril & Bibron, 1835)
occurs in Brazil, Uruguay and Argentina (Van Djik
et al., 2014). In Brazil, it is one of the most
abundant freshwater turtles in Rio Grande do Sul
State (Bujes et al., 2011). Trachemys dorbigni
often be found in heavily modified urban
environments, such as sewage systems, and in
agricultural environments such as rice field
drainage canals with pesticide residues (Bujes &
Verrastro, 2008; Fagundes et al., 2010). This
species is neither on the IUCN red list (IUCN,
2018) nor on the list of endangered species of
Brazilian fauna (ICMBio, 2016).
Studies of epibiont helminths associated with
freshwater turtles contribute to the knowledge of
the biology of the hosts and their habitats,
contributing to the conservation of species and of
the ecosystems that support these invaluable
relationships. In this context, this study aims to
analyze the association between epibiont
helminths (Temnocephalidae) and the freshwater
turtle, T. dorbigni, in relation both urban and rural
environments and turtle's gender.
Turtles were collected between July 2010 and
December 2012 in two distinct areas, one urban
and one rural, in the State of Rio Grande do Sul,
Brazil (Fig. 1). The sampling period encompassed
spring and summer months in the southern
hemisphere. Only two male hosts were sampled in
July 2010.
Sixty adult T. dorbigni were manually collected
with nets, and transported in plastic containers (56
liter) to the laboratory, where they were examined.
Mascarenhas et al.
Twenty-eight turtles (13 males, 15 females) were
collected in rural areas from four ponds at the
Centro Agropecuário da Palma of the Universidade
Federal de Pelotas (UFPel), located in Capão do
Leão county (31°48'01.1" S, 52°30'48.6''W) (Fig.
1A and Figs. 2A – B). Another 32 specimens (14
males, 18 females) were collected in canals in the
urban area of the city of Pelotas (31°46'16.9" S,
52°18'45.9'' W) (Fig. 1B and Figs. 2C – D).
The carapace and plastron, and skin-carapace and
skin-plastron junctions of each turtle were
examined for external helminths. Posteriorly, the
turtles were then sacrificed for study of internal
parasitic helminths. Turtle's genders were
determined during necropsy. This study was
licensed by the Instituto Chico Mendes de
Conservação da Biodiversidade (23196-ICMBio)
and was approved by the Ethics and Animal
Experimentation Commission (3026 -
CEEA/UFPel).
Epibionts were prepared according to Amato et al.
(1991), and were identified based on
morphological characteristics described by
Volonterio (2010) and Seixas et al. (2014).
Vouchers were deposited in the Coleção de
Helmintos do Laboratório de Parasitologia de
Animal Silvestres (545–568 CHLAPASIL-
UFPel). Some specimens were deposited in the
Coleção Helmintológica do Instituto Oswaldo
Cruz and in the Coleção de Invertebrados do
Instituto Nacional de Pesquisas da Amazônia as
vouchers of the morphological study carried out by
Seixas et al. (2014).
To analyze the association between epibiont
helminths and turtles, parasitological indices of
Bush et al. (1997) were adapted and interpreted as
ecological parameters of symbiotic interaction.
The mean intensity of infection was treated as
Mean Intensity (MI) of the non-parasitic
association between epibionts and turtles.
Prevalence (P%) and Mean Abundance (MA) were
used in the sense of Bush et al. (1997). These
measures can be used to represent population
patterns applicable to free-living populations; such
as population density and values of minimum and
maximum occurrence. These indices were
calculated for all sampled turtles, as well as for
turtle's genders (Male: M; Female: F). Thus, P%
and MI were compared between genders, whereas
203
Neotropical Helminthology, 2018, 12(2), jul-dic
RESULTS AND DISCUSSION
the P% values was compared by using the chi-
2
square test (χ) (p<0.05) in the software
Quantitative Parasitology (QP 3.0) (Reiczigel &
Rózsa, 2005), the MI values were compared by
using the Mann-Whitney test (p<0.05) in
“Paleontological Statistics – PAST 2.17” (Zar,
1999).
Among all examined turtles (N = 60), 25% were
positive for epibiont helminths, which belong to
Temnocephala (Temnocephalidae), T. pererai (Fig.
3) and Temnocephala sp. The association occurred
only in turtles from the rural area, where 53.6% (N
= 15/28) were positive (Table 1). A total of 2401 (6 -
1434) temnocephalids were collected on
freshwater turtles from rural area, unlike the turtles
of the urban area, where there was no association
between the epibionts and T. dorbigni. Helminths
were found on the skin of the neck, axillary,
inguinal and perianal areas, as well as the posterior
plastron lobe (Figs. 4A – E).
There was no significant difference in the
prevalence of epibionts among males and females
2
of the turtles (χ, p = 0.122) (Table 1). However,
temnocephalids showed significant differences in
their association with males and females measured
as to MI, which was higher in males (MI = 256.78
epibionts) than in females (MI = 15) (Mann-
Whitney U test, z= -3.126, p= 0.001). The
amplitude of epibionts on male turtles was 46 –
1434, whereas female turtles the amplitude was 6 –
29 epibionts (Table 1).
Degradation of freshwater environments may
influence the diversity of species occurring in these
environments as well as the population dynamics
of organisms living at different trophic levels
(Collier et al., 2016). Figure 2 shows the aquatic
environments of the rural and urban area where the
specimens of T. dorbigni were collected. The rural
ponds were ecosystems little impacted by human
intervention (Figs. 2A – B). In contrast, the urban
canals were extremely degraded by human
activities, such as deposition of trash and sewage
(Figs. 2C – D). The characteristics of the aquatic
environment in natural ecosystems have not been
covered by most studies of temnocephalids, which
Temnocephalids on Trachemys dorbigni
are largely of a taxonomic nature. It has been
reported that low levels of eutrophication are
important for the maintenance of T. brevicornis in
tanks (Pereira & Cuocolo, 1940).In this context,
the absence of temnocephalids in turtles from
urban area may be related to the degradation of
urban aquatic environments, negatively
influencing the occurrence of temnocephalids and
organisms that are part of the food web, in which
temnocephalids can be considered predators.
The majority of temnocephalids species feed on
small organisms such as bacteria, diatoms, protists,
rotifers, and nematodes found in, or around, the
host and, although they are mobile, they do not
normally leave their hosts. If experimentally
removed from their host, some individuals of
temnocephalids species die promptly, whereas
others survive for weeks (Goater et al., 2014).
Pereira & Cuocolo (1940) have reported the
consumption of small oligochaete, as well as the
inability of the temnocephalids to capture other
invertebrates such as copepod crustaceans. These
predatory characteristics are probably related to
displacement of the temnocephalids, which need a
solid surface to get around. Dioni (1967) classified
Temnocephala associated with Aegla spp. as
epibiont predators that feed directly on polychaetes
(Stratiodrilus), protozoa, oligochaetes, rotifers and
crustacean-associated remains. Thus, this author
classified temnocephalids as belonging to the top
of the epibiont organism food web.
Organisms that make up the temnocephalids diet
have been reported in association with T. scripta
(Schoepff, 1792) and Pseudemys concinna
(LeConte, 1830) from a North American
(Tumlison & Clark, 1996). The authors mentioned
Cyanobacteria, Chlorophyceae, Xanthophyceae,
Bascillariophyceae, Protozoa, Turbellaria,
Gastrotricha, Rotatoria, Nematoda, Oligochaeta,
Crustacea (Cladocera, Copepoda, Ostracoda) and
Insecta (chironomids) associated with the carapace
and plastron of turtles. Unlike turtles collected
from urban canals in the city of Pelotas, some rural
specimens showed algae and nematodes associated
with the carapace and plastron, pointing to an
eventual creation of a micro-habitat favoring an
epibiont food web for temnocephalids. The
absence of temnocephalids in urban turtles seems
to be linked to the degradation of the aquatic
environment. This degradation might act as a
204
limiting factor on the population dynamics of these
helminths that live on the turtle in direct contact
with the surrounding water and also because they
feed on other organisms associated with the turtle
carapace.
Although ecological indices suggest that these
helminths should occur on males and females, a
significant difference in MI of the epibiont
helminths between turtle's genders suggests a
closer association with males. It is likely that the
lower rate of association with females is related to
the behavior of females during the nesting period.
During this period, females leave the water in
search of suitable land for laying eggs causing
probably the death or detachment of
temnocephalids from their body surface.
Various aspects of reproductive biology of T.
dorbigni have been studied by Krause et al. (1982)
and Bager et al. (2007) at the Estação Ecológica do
Taim in Rio Grande do Sul State, Brazil, where the
nesting season extends from September to
February. The females start the nesting process by
leaving the water to search for a suitable place to
construct their nest; after a site has been chosen, it
is excavated with the hind limbs, followed by egg
laying and nest closing and then finally return to
water (Krause et al., 1982; Bager et al., 2007).
Krause et al. (1982) observed that the distance
between the nest and water ranged from 1-400 m
depending on soil characteristics; they also
observed that on their return to the water the
females made 10 to 60 min stops. Bager (2003) did
not directly estimate nesting time, but
hypothesized that it should last between two and
three hours. Furthermore, some T. dorbigni
females at Estação Ecológica do Taim had three
nesting cycles at 15 to 20 day intervals in the same
reproductive season (Bager et al., 2007).
The reproductive characteristics of T. dorbigni
suggest that female behavior can act negatively on
the association with temnocephalids. The lengthy
nesting process would cause the death of helminths
by friction with the ground during the opening and
closing of the nest, and the possibility of more than
one nesting cycle in the reproductive period.
Lengthy walking activity of female freshwater
turtles the search of suitable egg-laying sites have
been reported for Phrynops geoffroanus
Neotropical Helminthology, 2018, 12(2), jul-dic Mascarenhas et al.
Table 1. Prevalence (P%), Mean intensity (MI), Mean abundance (MA) and Amplitude (A) of temnocephalids
associated with males and females of Trachemys dorbigni in a rural environment of Rio Grande do Sul, Brazil.
Ecological
indices
Turtle’s genders
N=28
Male (N=13) Female (N=15)
P%
53.6
69.2 40.0
MI (± SD)
160.06 (± 357.93)
256.78a (± 444.82) 15b(± 8.07)
MA (± SD)
85.75 (± 270.26)
177.77 (± 383.56) 6 (± 9.01)
A
6 -
1434
46 -
1434 6 -
29
Figure 1. Trachemys dorbigni in southern Overall layout of the collection environments in the study of epibionts associated with f
Brazil. A – Detail of the Centro Agropecuário da Palma (UFPel), rural area of Capão do Leão, State of Rio Grande do Sul. B –
®
Detail of the urban area of Pelotas, Rio Grande do Sul. Source: site Google Earth (©2014 Google – Extracted and modified the
Images ©2014 Digital Globe).
Neotropical Helminthology, 2018, 12(2), jul-dic Temnocephalids on Trachemys dorbigni
N – number of turtles examined; SD – standard deviation; a, b indicate differences between turtle’s gender (Mann-
Whitney U test, z= -3.126, p= 0.001)
205
Figure 2. Aquatic environments where the specimens of Trachemys dorbigni were collected in southern Brazil. A – B. Ponds in a
rural area of Capão do Leão, Rio Grande do Sul State, Brazil. C – D. Canals of the urban area of Pelotas, Rio Grande do Sul, Brazil.
Neotropical Helminthology, 2018, 12(2), jul-dic Mascarenhas et al.
206
ACKNOWLEDGEMENTS
Figure 3. Temnocephala pererai stained with carmine Langeron. A. ph – pharynx, vi – vitellarium, at – anterior testes, pt –
posterior testes, ad – adhesive disc. B. The arrow shows cirrus.
(Schweigger, 1812) (Guix et al., 1989). This chelid
species can repeat this process several times,
abandoning sites considered inappropriate and
looking for new ones, returning to the water body
and leaving it repeatedly during both pre and post
laying periods (Guix et al., 1989). These authors
reported that the nesting time (from the moment the
female leaves water until its return) can last up to
90 min.
A field observation made during turtle collection
that may strengthens our argument on the
relationship between of the turtle's genders and
epibionts is the fact that many T. dorbigni males
had their shell covered with algae (Figs. 4A – E),
unlike the females. This suggests that males remain
in aquatic habitat and these behaviors allow a more
positive association with temnocephalids and their
epibiont prey community. These aspects may be
reflected in P%, MI and MA values in this study.
Bager (2003) commented that males probably do
not frequently leave the water when they are in
favorable environments with respect to food
availability, sun exposure areas, and water volume.
It seems likely that recolonization of female T.
dorbigni by temnocephalids occurs at the end of the
nesting season through direct contact with males
(in copulation), and/or the through the viable eggs
hatching deposited by epibionts on female turtles.
These processes that occur after nesting could
provide continuity of the association between
temnocephalids and T. dorbigni females. Although
the freshwater turtles in this study were captured
during the reproductive period of the species, it is
difficult to determine how much influence of the
behavior and reproductive condition have on the
epibiont helminths population dynamics.
We would like to thank the Instituto Chico Mendes
de Conservação da Biodiversidade (ICMBio) for
the permission to capture the turtles (23196-
ICMBio); to Coordenação de Aperfeiçoamento do
Pessoal de Nível Superior (CAPES) for the
scholarship for CSM and financial support
(process number 032/2010). Special thanks to
Marco Antônio A. Coimbra, Samantha A. Seixas,
Joaber Pereira Jr., Mariana de Moura Mendes, and
Jéssica D. Souza for their assistance.
Neotropical Helminthology, 2018, 12(2), jul-dic Temnocephalids on Trachemys dorbigni
207
208
Figure 4. A - V Trachemys dorbigni with temnocephalids. B - Posterior lobe of plastron with epibionts (circle). entral view of male
C - temnocephalids (arrows). D - Region between the carapace and plastron near the tail with eggs of Region between the
carapace and plastron with helminths near the tail Region between the carapace and plastron with (circle). E - temnocephalids
near inguinal area (circle).
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