Bacteriological screening of Trachemys scripta

Biologia, Bratislava, 59/Suppl. 14: 201—207, 2004
Bacteriological screening of Trachemys scripta elegans
and Emys orbicularis in the Po plain (Italy)
Christiana Soccini & Vincenzo Ferri
Centro Studi Arcadia, via dello Statuto 13, I–01016, Tarquinia, Viterbo, Italy; tel.:+39 0766 857100,
e-mail: [email protected]
SOCCINI, C. & FERRI, V., Bacteriological screening of Trachemys scripta
elegans and Emys orbicularis in the Po plain (Italy). Biologia, Bratislava,
59/Suppl. 14: 201—207, 2004; ISSN 0006-3088.
Since 1999, introduced Trachemys scripta elegans from artificial and natural
water bodies in the Po plain (North Italy) were bacteriologically screened.
From 2001 onwards, a survey of Emys orbicularis was started in the same
area. 15 carcasses and 349 cloacal swabs from T. s. elegans, and 100 cloacal
swabs from E. orbicularis have been studied. Most samples yielded positive
bacteriological results. Besides bacteria known as pathogens for chelonians
(e. g. Aeromonas hydrophila, Citrobacter freundii, Pseudomonas spp., Edwardsiella tarda), ubiquitous bacteria occurring in water and soil have been
identified.
Key words: Emys orbicularis, Trachemys scripta, bacteriology, Italy.
Introduction
and Mauremys leprosa (Schweigger, 1812) (SER1986; MARTINEZ-SILVESTRE et al., 1997;
SERVAN & ARVY, 1997; ARVY & SERVAN, 1998;
CADI & JOLY, 2000, 2003). Sliders are now in Italy
by far more common and better known to the public than the native E. orbicularis (FERRI, 1995).
Because of the irreversible alteration of the
wetlands of the Po valley and Venetian plain, E.
orbicularis is either extinct or on the brink of
extinction throughout northern Italy. Its decline
in Piedmont, Liguria, Lombardy and parts of the
Veneto began well before the introduction of T. s.
elegans (FERRI, 1995; SEMENZATO et al., 1998).
Today, as a number of authorities plan and conduct reintroduction or population recovery programmes for E. orbicularis, especially in protected
areas along northern rivers (FERRI, 1999, 2000,
unpubl. data), there is an increasing need for studies on the impact of exotic turtles on the vitality
and survival of native and reintroduced pond turtle populations.
VAN,
The release of thousands of red-eared sliders, Trachemys scripta elegans (Wied, 1839) in all kinds
of natural and artificial waters since 1970 is the
largest known case of introducing a foreign reptile species. Almost all countries in South Europe, Saudi Arabia, Southeast Asia, South Africa,
and North America have been affected by this introduction, which resulted in some cases in established, reproducing populations (NEWBERRY,
1984; WARWICK, 1985; MOLL, 1995; DE ROA &
ROIG, 1997; ARVY & SERVAN, 1998).
Hence, widespread concern has arisen about
the potentially negative impact of sliders on native fauna and in particular on native chelonian
species. It has been shown that high numbers of
sliders occur in localities where new individuals
are released repeatedly. These can compete with
native freshwater turtles, especially if these are already endangered, like Emys orbicularis (L., 1758)
201
Table 1. Study sites and estimated numbers of Emys orbicularis and Trachemys scripta elegans for 2002 and
year of first record of T. s. elegans for each site.
Site code
Site
Wetland type
LAGBS
Bosco in Città (Public Gardens)
Abandoned “Cabassi” sand
pits in Via delle Forze Armate
Villa Reale in the Gardens of
the Monza Public Park
Fontanile dei Frati
Fontanile Laghetto del Parco
Arcadia (pond in public park)
Fontanile Nuovo di Bareggio
Ducos urban park
Ducos/San Polo urban park
Torrazzuolo di Nonantola ecological regeneration area
Villa Sorra Gardens
Regenerated artificial Milan MI
lake
Regenerated artificial Milan MI
lake
Artificial urban ponds Monza MI
Former phreatic spring Binasco MI
Former phreatic spring Bareggio MI
CAVFA
LAGMON
FONBIN
FONARC
FONNOV
DUCOS1
DUCOS2
ARETOR
VILSOR
Phreatic spring
Artificial urban pond
Artificial urban pond
Regenerated irrigated
basin
Regenerated artificial
lakes
Since 1994, as part of the ARCADIA/Trachemys Project (FERRI et al., 1999a), data have been
collected on inter-specific interactions between T.
s. elegans and E. orbicularis in North Italy. Nine
years of counts and observations have confirmed
the high numbers and wide distribution of the
allochthonous species compared to the rare and
highly localized E. orbicularis, as well as the low
level of interaction of sliders with the native fauna
(AGOSTA & PAROLINI, 1999; FERRI & SOCCINI,
2001, 2003; GIANAROLI et al., 2001; PETTERINO
et al., 2001; PIOVANO & GIACOMA, 2002). Since
1999, a programme is underway to monitor the
state of slider populations in artificial and natural
water bodies, approved by the Conservation Committee of the Societas Herpetologica Italica (SHI)
in 1998 (FERRI et al., 1999b; FERRI & SOCCINI,
2001). The programme is conducted in cooperation with the laboratories of the Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia
Romagna (IZS) in Brescia. Some results of this activity are presented here.
The “Pond Turtle Diseases Monitoring Project” was launched with the following objectives:
(i) to perform a nationwide survey of introduced
T. s. elegans populations with more than 10 individuals by distributing a special report form; (ii)
to highlight possible negative effects linked to the
presence of T. s. elegans in potential habitats of E.
orbicularis, intensifying and promoting ecological
studies at syntopic localities for both species; (iii)
to set up a data base on diseases and associated
202
Town/city
and province
Emys Trachemys First record
Trachemys
0
75
1992
0
150
1992
0
150
1989
0
0
70
150
1984
1992
Bareggio MI
0
Brescia BS
0
Brescia BS
0
Nonantola MO 50
<10
100
120
0
1992
1985
1992
–
Castelfranco
Emilia MO
250
1990
150
micro-organisms known to occur in Italian chelonians (through consultation of all available scientific publications); (iv) to identify the causes of the
various diseases occurring in large percentages of
T. s. elegans found in the wild; (v) to develop a
standardized diagnostic procedure for recognition
of the various pathogenic micro-organisms; (vi) to
draw up an operational protocol aimed at identification, isolation and registration of the various
viral, bacterial and parasitic pathogens, enabling
optimum monitoring of the health of pond turtles.
The last four objectives form the basis of the cooperation with the IZS in Brescia.
Material and methods
Study areas and sampling
In the first phase (1999–2000), health monitoring was
carried out on groups of Trachemys scripta elegans
from urban and suburban ponds in the provinces of
Milan (six localities) and Brescia (two localities). Since
2001, syntopic sites for Emys orbicularis and T. s. elegans were studied, together with sites where only the
European pond turtle is present. A list and code of
these localities and estimated numbers of turtles (2002)
is presented in Table 1. Regarding E. orbicularis, individuals from the Cameri breeding centre were also
studied.
The study was carried out on: (a) water samples
from fish farm tanks or other water bodies in which
newly captured turtles were kept; (b) faecal samples
from captive turtles; (c) cloacal swabs from recently
captured or handed-over turtles; (d) carcasses of tur-
Table 2. Studied samples. (1) Sites only with Trachemys scripta elegans; (2) site with syntopic Emys orbicularis
and T. s. elegans. For site codes, see Table 1.
Carcasses
Cloacal swabs
Site code
Emys
Trachemys
Emys
Trachemys
LAGBS (1)
CAVFA (1)
LAGMON (1)
FONBIN (1)
FONARC (1)
DUCOS1 (1)
DUCOS2 (1)
VILSOR (2)
Captivity
Breeding centre
–
–
–
–
–
–
–
–
–
–
–
–
4
6
3
2
–
–
–
–
–
–
–
–
–
–
–
36
–
64
12
18
14
9
30
49
137
37
43
–
Total
–
15
100
349
Table 3. Findings of samples tested (FERRI & SOCCINI, 2001; SOCCINI, unpubl. data). “Various microbial flora”
= Citrobacter braakii, Klebsiella spp., Morganella spp., Proteus spp., etc.
Material examined
Emys
Cloacal swabs
Trachemys Cloacal swabs
Carcasses
Total Negative samples Samples positive for Typified microbial species
samples
various microbial flora (numbers of isolations)
100
4
349 46
15
3
4%
13%
20%
tles which died under natural conditions. The present
paper focuses on the latter two sample types.
Samples from turtles were taken in accordance
with the operational protocol worked out at the IZS in
Brescia in cooperation with the Centro Studi Arcadia:
(i) appropriate and non-harmful techniques of capture,
to be carried out with minimum handling and constraint of turtles, if possible under aseptic conditions
to prevent contamination; (ii) use of sterile swabs with
culture medium for the various materials to be examined; (iii) immediate forwarding of samples to the laboratory; in cases where this is impossible, samples to
be preserved at +4 ◦C awaiting shipment, which in all
cases must take place as early as possible. The following samples were studied:
Trachemys scripta elegans: 312 cloacal swabs and
15 carcasses from sites without E. orbicularis; 37 cloacal swabs from syntopic sites with E. orbicularis.
Emys orbicularis: 64 cloacal swabs from a breeding centre; 36 cloacal swabs from syntopic sites with
T. s. elegans (Tab. 2).
Laboratory tests
The procedures and techniques used for observation,
isolation, and identification of micro-organisms were
those commonly used in routine practice in the Departments of Diagnostics, Specialized Bacteriology, Microbiology and Electron Microscopy at the IZS in Brescia.
11
57
4
91
266
8
Bacteriological, virological and parasitological tests
were performed (NIEDDU et al., unpubl. data).
Results
Before discussing the results from laboratory analyses, it is important to recapitulate the environmental situation at the study sites. Most sites
are characterized by serious degradation of water
quality: water in advanced stage of eutrophication
and very limited transparency, because of limited
in/outflow and circulation and a direct or indirect link with polluted streams or rivers (localities
LAGMON, FONBIN, DUCOS1; Tab. 1). Chemical analyses revealed the presence of high levels
of nitrates, phosphates, and iron cations. The water quality at the other sites is comparatively fair,
thanks to constant water exchange (LAGARC,
FONNOV, DUCOS2, LAGBS), a large water body
(CAVFA), or rich aquatic vegetation (ARETOR,
VILSOR).
Autopsies of 15 T. s. elegans which had died
in the wild revealed in all cases underfeeding. In
all stomachs and intestinal tracts, no food was
present. The turtles were in a more or less gen-
203
Table 4. Typification results for microbial species of Trachemys scripta elegans from sites without Emys orbicularis (FERRI & SOCCINI, 2001; SOCCINI, unpubl. data; cloacal swabs: n = 312, carcasses: n = 15). % of samples
refers to number of cloacal swabs or tissues.
Bacterial strain
Source
Aeromonas spp.
Aeromonas caviae
Aeromonas sobria
Cloacal swab
Cloacal swab
Cloacal swab
Intestine (15)
Cloacal swab
Cloacal swab
Cloacal swab
Cloacal swab
Cloacal swab
Cloacal swab
Cloacal swab
Liver (15)
Lung (15)
Cloacal swab
Cloacal swab
Skin (9)
Intestine/faeces (15)
Liver (15)
Cloacal swab
Cloacal swab
Uterus (3)
Cloacal swab
Lung (15)
Cloacal swab
Cloacal swab
Intestine (15)
Cloacal swab
Cloacal swab
Cloacal swab
Aeromonas hydrophila
Edwardsiella tarda
Salmonella thompson
Salmonella typhimurium
Salmonella arizonae
Steptococcus spp.
Pseudomonas diminuita
Pseudomonas spp.
Providencia stuardi
Escherichia coli
Serratia odorifera
Serratia liquefaciens
Citrobacter freundii
Pasteurella haemolitica
Yersinia kristensenii
Hafnia alvei
Clostridium perfrigens
Enterobacter agglomerans
Enterobacter cloacae
No. of isolations
% of samples
>5
>1
20
20
10
>1
>1
>1
1
>1
>1
7
7
4
16
11
27
7
>1
>1
33
6
7
>1
1
7
1
1
>1
12
2
62
3
31
2
1
1
3
2
2
1
1
13
50
1
4
1
1
2
1
20
1
1
3
1
4
4
2
Table 5. Typification results for important microbial species from Trachemys scripta elegans from syntopic sites
with Emys orbicularis (FERRI & SOCCINI, 2001; SOCCINI, unpubl. data; n = 37, cloacal swabs).
Bacterial strain
Aeromonas sobria
Aeromonas hydrophila
Escherichia coli
No. of isolations
Percentage of total samples
25
21
2
68
57
5
eral state of anaemia. Anatomical-pathological examinations revealed pulmonary (n = 7), enteric
(n = 4), and hepatic lesions (n = 4). Approximately half of the carcasses showed lesions of the
shell (Septicaemic Cutaneous Ulcerative Disease
= SCUD). Virological and parasitological examinations yielded negative results. The bacteriological tests were positive (Tab. 3). Tables 4 and 5
summarize for T. s. elegans the most important
typified microbial species and their frequency of
isolation. Findings from E. orbicularis from sites
204
with or without T. s. elegans are given in Tables
6 and 7.
Discussion
398 of 449 cloacal swabs (89%) and three of 15
carcasses (20%) were positive for micro-organisms
(Tabs 3–7). Several of the identified bacteria are
known chelonian pathogens. Citrobacter freundii
was identified as principal micro-organism causing
SCUD. Serratia bacteria may become established
Table 6. Typification results for important microbial species from Emys orbicularis from sites without Trachemys
scripta elegans (FERRI & SOCCINI, 2001; SOCCINI, unpubl. data; n = 64, cloacal swabs).
Bacterial strain
Aeromonas sobria
Aeromonas hydrophila
Pseudomonas diminuta
Escherichia coli
Enterobacter spp.
No. of isolations
Percentage of total samples
12
32
2
13
1
19
50
3
20
2
Table 7. Typification results for important microbial species from Emys orbicularis from syntopic sites with
Trachemys scripta elegans (FERRI & SOCCINI, 2001; SOCCINI, unpubl. data; n = 36, cloacal swabs).
Bacterial strain
Aeromonas sobria
Aeromonas hydrophila
Escherichia coli
Enterobacter agglomerans
Serratia liquefascens
No. of isolations
Percentage of total samples
19
5
5
1
1
52
14
14
3
3
on already existing lesions. The lytic action of Serratia permits C. freundii to infect deeper parts of
the shell and body, resulting in clinic symptoms
like crater ulcers in the necrotic tissue, hepatic
necrosis and, when the lesions invade the deeper
layers of the shell, the death of the animal through
septicaemia (FRYE et al., 1977).
Aeromonas hydrophila appears to be responsible for numerous deaths linked to anorexia and
septicaemia (MAS = Motile Aeromonas Septicaemia) in freshwater turtles (REICHENBACHKLINKE & ELKAN, 1965). Aeromonas are ubiquitous bacteria, present in all water. If freshwater turtles show clinical symptoms from an
Aeromonas infection, something has happened to
make them susceptible to bacterial invasion. Common causes are poor water quality and overcrowding. Stress elimination may be sufficient to resolve
the outbreak of the disease in captivity.
The pathogenic role of Pseudomonas spp. remains uncertain. However, it is likely that it causes
problems for turtles subjected to thermal stress.
We believe that Pseudomonas causes anorexia and
blepharo-conjunctivitis (lesions noted in four T.
s. elegans from DUCOS1 site; see also HOLT et
al., 1994). Edwardsiella tarda is another microorganism, responsible for latent intestinal infections. It occurs as an opportunist pathogen in various reptiles (QUINN et al., 1994). The role of other
bacteria (Tabs 4–7) remains unclear. They are frequently present as commensals in the gastroenteric
system of freshwater turtles.
In some samples, bacterial examination revealed the presence of micro-organisms which may
be pathogens for humans: Aeromonas, Citrobacter,
Enterobacter, Klebsiella, Proteus, Serratia, and
Salmonella spp. Until now it is a matter of debate whether infected turtles are a risk for public health. The majority of samples with these
bacteria correspond to T. s. elegans collected at
the most polluted and most degraded sites (LAGMON, FONBIN, DUCOS1). At these localities,
the highest rate of dead or dying turtles was
recorded.
There is also a significant correlation between
the origin of turtles and the occurrence of clinical
symptoms of SCUD. Observations over nine years
at collection points for abandoned pet turtles (ARCADIA/Trachemys Project) revealed that only
7% of all turtles are affected at the time when
they are released. This percentage rises to 47%
at sites in the province of Milan where environmental conditions are best and to 97% where they
are worst. The percentage is very low at sites in
the province of Brescia (2%) and falls virtually to
zero in the province of Modena. Among 68 captured T. s. elegans, 66% showed obvious signs of
weight loss, 12% appeared stable and only 22%
had apparently gained weight (SOCCINI & FERRI,
unpubl. data).
The results also highlight the difficulties of
exotic turtles to adapt after their release into degraded sites, where health problems might result
mainly from dietary and environmental contami-
205
nation (PIOVANO et al., 2001; PIOVANO & GIACOMA, 2002). A further interesting aspect is the
decrease of T. s. elegans after the winter season in the studied water bodies. The individuals
in artificial and urban sites in Milan (LAGPAL)
and Brescia (DUCOS1) seem to be reduced to
50% after winter. In semi-natural sites (FONBIN,
FONARC), this rate is lower (approx. 10–20%).
LUISELLI et al. (1997) reported similar observations for juvenile T. s. elegans from colonies in
artificial ponds in Central Italy.
Acknowledgements
We are grateful to D. NIEDDU, A. LAVAZZA, L.
PAROLINI and A. IMPERIALE (Istituto Zooprofilattico
Sperimentale della Lombardia e dell’Emilia Romagna,
Brescia) for their essential work.
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