First records for Europe of the non-native turtles
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Herpetology Notes, volume 14: 303-307 (2021) (published online on 09 February 2021)
First records for Europe of the non-native turtles
Kinosternon subrubrum Bonnaterre, 1789 and
Pelomedusa olivacea (Schweigger, 1812) in a
suburban wetland in central Italy
Vincenzo Ferri1,2, Corrado Battisti3,*, Christiana Soccini1, and Riccardo Santoro4
Kinosternon subrubrum Bonnaterre, 1789 is a North colonisation of these ecosystems (Da Silva and Blasco,
American semi-aquatic freshwater turtle found primarily 1995; Martinez-Silvestre et al., 2001; Shiau et al., 2006).
in the mid-Atlantic and southeastern regions of the United Here, we provided the first records of K. subrubrum and
States (Powell et al., 2016). This primarily carnivorous P. olivacea in a suburban wetland remnant in central
species prefers lentic freshwater systems, but it also has Italy. These are the first records for Europe, outside the
been reported to inhabit brackish marshes (Frazer et respective native geographical ranges of both species.
al., 1991; Wilson et al., 1999; Ernst and Lovich, 2009; Study area. The study area is the Palude di Torre Flavia
Meshaka et al., 2017). Its longevity in the wild is thought (Battisti, 2006), a 40-ha wetland managed as a protected
to exceed 30 yrs (Gibbons, 1983). nature reserve (Special Protection Area IT6030020,
Pelomedusa olivacea (Schweigger, 1812) is a according to EU Directives 79/409 and 2009/147/EU)
freshwater turtle native to Benin, Burkina Faso, Niger, that is located in the Latium region along the Tyrrhenian
Nigeria, and Senegal (Vargas-Ramírez et al., 2010, 2016; coast of central Italy (41.9624°N, 12.0461°E; Fig. 1).
Wong et al., 2010; Fritz et al., 2014; Petzold et al., 2014). This ecosystem is the remnant of a larger wetland,
It is primarily carnivorous, feeding on amphibians (adults drained and transformed in the second half of the 20th
and larvae), fish, crabs, ticks, molluscs, birds, and small Century and embedded in an agricultural and urbanized
mammals. The species occupies marshes, temporary landscape (40 km from Rome, 2 km north of Ladispoli
pans, pools, or puddles and shows a high vagility, moving – a town with about 40,000 inhabitants). This wetland
great distances (Boycott and Bourquin, 2008). is characterized by a seminatural patchiness with ponds
Both of these species are included among the freshwater and channels, reedbeds (Phragmites australis), flooded
turtles held worldwide as pets, although with less meadows, dunes, and patches of Carex hirta, Juncus
frequency compared to large traded species, such as acutus, and Cyperaceae (Guidi, 2006). The area was
Trachemys scripta (Ferri and Soccini, 2008; Tapley et managed for fish farming until 2004 (pisciculture of
al., 2011; Masin et al., 2014). However, as with many mullet fry, Mugil cephalus, Chelon ramada, and C.
other pet species, these turtles are sometimes released by saliens). The water supply comes largely from rainfall
their owners into ponds or urban and suburban wetlands (Mesomediterranean Xeric Region; Tomaselli et al.,
(e.g., Masin et al., 2014), thereby potentially inducing 1973) and from an artificial intake controlled by the park
agency managing this reserve (‘Città Metropolitana di
Roma Capitale’ Agency). Inflow from surrounding areas
is scarce. The area may suffer major hydrological stress,
11
Via Valverde 4, 01016 Tarquinia, Italy. especially in late spring–summer (May–September).
2
Evolutionary Biology and Zoology, Department of Biology,
Fires of reedbeds (either controlled or not) are recurrent,
University of Rome II ‘Tor Vergata’, Via Cracovia 3, 00133
Rome, Italy.
occurring mainly in late summer.
3
‘Torre Flavia’ Long Term Ecological Research Station, Città Sampling. From 1997, when the Palude di Torre
Metropolitana di Roma, Via Tiburtina 691, 00159 Rome, Italy. Flavia was protected as a nature reserve, a large number
4
Via Eugenio Maccagnani 55, 00148 Rome, Italy. of researchers periodically and randomly sampled the
*
Corresponding author. E-mail: c.battisti@ macrofauna in the water channels (Battisti, 2006). During
cittametropolitanaroma.gov.it the months of May–July in the years 2016–18, we carried
© 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. out a time-constrained systematic sampling survey (SSS;
304 Vincenzo Ferri et al.
Figure 1. Location of Torre Flavia wetland in central Italy, where Kinosternon subrubrum and Pelomedusa olivacea were recorded.
Dodd, 2010) focused on freshwater turtles. Sampling and lakes of Rome, six non-native freshwater turtles were
was carried out along three transects (total length: 550 m) recorded, but not these species (Di Santo et al., 2017).
randomly located inside the study area. Research effort These records are also the first records of apparently
was about 12 h. Specimens were identified following free-ranging individuals for Europe. Records outside
Petzold et al. (2014). The collected specimens were their non-native range exist for areas outside of Europe
deposited in the zoological collection of Vincenzo Ferri (for Kinosternon subrubrum see Ceballos and Fitzgerald,
(Natural Museum of Sant’Oreste, Rome, Italy). 2004; for Pelomedusa sp., see Fujisaki, et al., 2010 and
Romagosa, 2014). In the case of P. subrufa, a non-native
Results population is known from Spain (Bugter et al., 2011).
Pelomedusa olivacea is widely traded in Rome as
After the devastating fire of 16 July 2017, we
a pet (V. Ferri, pers. obs.). Moreover, in Ladispoli (the
recorded a carcass of Kinosternon subrubrum in the
town closest to the wetland), there is a large community
reedbed (Fig. 2). Species identity was determined
of residents with Senegalese origin. It is possible that
by examining the remains of the carapace using
a turtle, whose range includes the country of origin of
characteristics reported by Iverson (1977). These
community members, may be held as a pet to memorialize
included a first vertebral that does not contact the
the homeland and may have escaped or been released.
second marginal, a ninth marginal not elevated above
It is most likely that either of these turtles are only
the preceding marginals, length and width of the
occasionally released, and there is no evidence for
second vertebral nearly equal, whereas the posterior
colonization. The area has high suitability for turtles,
vertebrals are wider than long. The straight carapace
given the high availability of trophic and spatial resources
length was 10.4 cm.
(Battisti, 2006). For the Torre Flavia wetland we have
During our surveys, we also recorded two carcasses of
obtained evidence of a rich community of non-native
Pelomedusa olivacea (Fig. 3). At the beginning of April
freshwater turtles, represented by at least 10 taxa at the
2017, the carcass of one large adult female was found
species and subspecies levels, including Graptemys p.
floating at the edge of a pond in an advanced state of
pseudogeographica (Gray, 1831), G. p. kohni (Baur,
putrefaction. The second specimen was an adult male
1890), Pseudemys c. concinna (Le Conte, 1830), P. nelsoni
that had been killed in the fire on 16 July 2017.
Carr, 1938, Trachemys scripta elegans (Wied, 1839),
T. s. scripta (Schoepff, 1792), T. s. troosti (Holbrook,
Discussion
1836), and Mauremys sinensis (Gray, 1834). Therefore,
Neither of these two freshwater turtles has previously these two observations corroborate the concern about the
been recorded in the Latium region (Bologna et al., 2000, release of pet animals into the wild.
2007; Scalera and Montinaro, 2014) or in Italy (Sindaco et The presence of so many invasive species implies a
al., 2006). In a large survey carried out on 31 urban ponds disruption or alteration of ecological relationships, but
First European Records for Kinosternon subrubrum and Pelomedusa olivacea 305
Figure 2. (a) Parts of the shell of an Eastern Mud Turtle (Kinosternon subrubrum) of undetermined sex, comprising
both skeletal and dermal bone. The specimen was apparently killed by a fire on 16 July 2017. (b) Reconstructed shell.
(c) Live specimen of Kinosternon subrubrum. Photos by Vincenzo Ferri (a, b) and courtesy of Austin’s Turtle Page (c).
this has yet to be observed in the study area (Amori and non-native species could also compete with the native
Battisti, 2008). It would be interesting to carry out studies Emys orbicularis (see Luiselli et al., 1997), which is also
on the food web to better understand the role of non- locally present.
native freshwater turtles, since this wetland is also home
to invasive populations of the crustacean Procambarus Among the freshwater species occurring in this
clarkii and the mosquitofish Gambusia holbrooki wetland, some (e.g., Pelomedusa) show a high risk
(Chiesa, 2006; Celauro, 2006), which are both potential of potential invasion outside their native range due
prey for turtles. Moreover, non-native freshwater turtles to climate matching, coexistence with humans, high
may represent a further trophic resource for large fecundity, and human tolerance (Kopecký et al., 2013;
predatory birds (e.g., waders, such as herons). However, Masin et al., 2014). In this regard, we suggest improving306 Vincenzo Ferri et al.
Figure 3. (a–e) Parts of the shell, comprising both skeletal and dermal bone, of two specimens of North-western African Helmeted
Turtle, Pelomedusa olivacea, retrieved from Torre Flavia wetland in central Italy. (a, b) Cranium of a large adult female, found
floating at the edge of a pond in an advanced state of putrefaction. (c) Lateral view, (d) carapace, and (e) plastron of the remains of
an adult male apparently killed by a fire on 16 July 2017. (f) Shown for comparison is a female subadult P. olivacea from the pet
market with origin in West Africa. Photos by Vincenzo Ferri and Guido Tavecchio.
control of commercial trade, local release, and Editore. 192 pp.
eradication projects promoted by the local park agency Boycott, R.C., Bourquin, O. (2008): Pelomedusa subrufa (Lacépède
1788) – helmeted turtle, helmeted terrapin. In: Conservation
(see Ferri and Soccini, 2008).
Biology of Freshwater Turtles and Tortoises: a Compilation
Project of the IUCN/SSC Tortoise and Freshwater Turtle
Acknowledgments. We thank Egidio De Angelis, Carlo Galimberti,
Specialist Group. Chelonian Research Monographs 5, p. 007.1–6.
and Narciso Trucchia, rangers of Monumento naturale “Palude di
Rhodin, A.G.J., Pritchard, P.C.H., Dijk, P.P. van, Saumure, R.A.,
Torre Flavia”, for their support. Luca Luiselli pre-reviewed a first
Buhlmann, K.A., Iverson, J.B., Eds., Lunenburg, Massachusetts,
draft of the manuscript. Hinrich Kaiser and an anonymous reviewer
USA, Chelonian Research Foundation.
provided useful comments and suggestions, which improved the
Bugter, R.J.F., Ottburg, F.G.W.A., Roessink, I., Jansman, H.A.H.,
first draft of the manuscript. We also thank Paolo Crescia for editing
Grift, E.A. van der, Griffioen, A.J. (2011): Invasion of the
the high-definition images
Turtles? Exotic Turtles in the Netherlands: a Risk Assessment.
Wageningen, The Netherlands, Alterra report 2186. 92 pp.
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