Pattern of distribution of the American bullfrog Rana catesbeiana in Europe

Abstract

Despite early reports of its presence, no recent data exist on the distribution of the American bullfrog in Europe, the causes
of introduction, or the trends of populations. We monitored the European situation at two spatial scales. In SW France, we
performed call surveys over 2,500 wetlands. We found bullfrogs over about 2,000km2, apparently the European area in which the strongest expansion of bullfrogs is taking place. In addition, we used questionnaires
to investigate the situation at the continental scale. At least 25 independent introductions occurred in Europe; eradication
attempts were successful three times, and bullfrog populations are present in five countries. Education programs and monitoring
are necessary to reduce the rate of introduction and to start management action as soon as possible.

Full text

REVIEW PAPER
Pattern of distribution of the American bullfrog Rana
catesbeiana in Europe
Gentile Francesco Ficetola Æ Christophe Coı
¨
c Æ
Mathieu Detaint Æ Matthieu Berroneau Æ
Olivier Lorvelec Æ Claude Miaud
Received: 28 August 2006 / Accepted: 14 November 2006
 Springer Science+Business Media B.V. 2006
Abstract Despite early reports of its presence,
no recent data exist on the distribution of the
American bullfrog in Europe, the causes of
introduction, or the trends of populations. We
monitored the European situation at two spatial
scales. In SW France, we performed call surveys
over 2,500 wetlands. We found bullfrogs over
about 2,000 km
2
, apparently the European area in
which the strongest expansion of bullfrogs is
taking place. In addition, we used questionnaires
to investigate the situation at the continental
scale. At least 25 independent introductions
occurred in Europe; eradication attempts were
successful three times, and bullfrog populations
are present in five countries. Education programs
and monitoring are necessary to reduce the rate
of introduction and to start management action as
soon as possible.
Keywords France  Invasion success  Rana
catesbeiana  Invasion causes  Monitoring 
Distribution  Invasive species  Community
richness
Introduction
The bullfrog Rana catesbeiana is native to eastern
North America, but has been introduced through-
out the world during the past two centuries
(Lever 2003). The bullfrog is considered to be
one of the most harmful invasive species, since it
negatively affects native amphibians through
competition and predation (Lowe et al. 2000;
Kats and Ferrer 2003; Beebee and Griffiths 2005).
Moreover, both native and introduced bullfrog
populations are frequently infected by the fungus
Batrachochytrium dendrobatidis (Hanselmann
et al. 2004; Garner et al. 2006). This fungus is
the agent of chytridiomycosis, an emergent
amphibian disease that causes extinction of
amphibian populations at a global scale (Berger
et al. 1998; Bosch et al. 2001; Lips et al. 2006;
Pounds et al. 2006). Since bullfrogs can be
Electronic supplementary material Supplementary
material is available in the online version of this article at
http://dx.doi.org/10.1007/s10530-006-9080-y and is
accessible for authorized users.
G. F. Ficetola (&)  C. Miaud
UMR CNRS 5553 LECA-GPB, Laboratoire
d’Ecologie Alpine, e
´
quipe Ge
´
nomique des
Populations et Biodiversite
´
, Universite
´
de Savoie,
73 376 Le Bourget du Lac cedex, France
e-mail: francesco.ficetola@unimi.it
C. Coı
¨
c  M. Detaint  M. Berroneau
Association Cistude Nature, Chemin du Moulinat,
33185 Le Haillan, France
O. Lorvelec
Equipe Gestion des Populations Invasives,
INRA-Unite
´
SCRIBE, Campus de Beaulieu,
35 042 Rennes Cedex, France
123
Biol Invasions
DOI 10.1007/s10530-006-9080-y

infected by B. dendrobatidis without developing
chytridiomycosis, the introduction of bullfrogs
can be an important vector of this disease
(Hanselmann et al. 2004; Garner et al. 2006).
Knowledge of the pattern of bullfrog invasion
is, therefore, extremely important in planning
conservation strategies aiming to control the
invasion.
Bullfrogs were introduced into Europe several
times during the 20th century. Up to the 1990s,
acclimatised bullfrog populations were recorded
in Italy, Holland, and France (Albertini and
Lanza 1987; Lanza and Ferri 1997). However,
since the end of the 20th century, several new
introductions have occurred and the European
situation has dramatically changed. Despite at-
tempts to clarify the distribution of introduced
bullfrogs (Lever 2003), no comprehensive reports
on the situation in Europe exist. We, therefore,
investigated the distribution of the bullfrog at
two spatial scales. First, we performed intensive
field monitoring to evaluate the distribution of
R. catesbeiana in western France, an area in which
bullfrog expansion in Europe is progressing
rapidly. In addition, we gathered information,
including data from both successful and failed
introductions, from herpetologists throughout
Europe to obtain a picture of the present situa-
tion at the continental scale.
Methods
Distribution in SW France
We performed field sampling in an area of
southwest France (35,500 km
2
) including six
departments: Gironde, Dordogne, Landes, Lot et
Garonne, Charente, and Charente Maritime
(Fig. 1). The study site was selected on the basis
of anecdotal records and preliminary surveys
(Detaint and Coı
¨
c 2001), and includes coastline,
lowland, and hills, with a high density of wetlands.
The study area was divided into a 10 · 10 km grid
(total: 355 squares) and we identified water bodies
for each square on the basis of 1:25000 IGN maps.
Since, during late spring–summer male bullfrogs
produce easily identifiable calls, we used calling
surveys to evaluate the distribution of the species.
We performed surveys in seven randomly selected
wetlands per square, from May to August of 2003,
2004, and 2005, and from May to June of 2006. In a
few cases, less than seven wetlands were present
and we monitored all wetlands. We performed
surveys at least 15 min after sunset, under suitable
weather conditions (no heavy rain or wind), and
each survey was repeated 15 days later. We
performed further additional surveys in squares
where we detected the presence of R. catesbeiana
(total: 2,505 wetlands surveyed). The reproduction
was determined on the basis of presence of
tadpoles or egg masses.
Distribution at the continental scale
Monitoring of bullfrogs at the continental scale is
not feasible; therefore, we used the community of
Fig. 1 (a) Distribution of introductions of R. catesbeiana
in Europe. Localities and outcome of introductions are
provided in the Appendix S1. (b) Distribution of
R. catesbeiana in SW France. Filled circles: present; open
circles: absent. Some points are superimposed
G. F. Ficetola et al.
123

European herpetologists as a source of primary
information about the distribution of bullfrogs.
First, we contacted the atlas committees and
members of the all the European herpetological
societies, and a large number of field herpetolo-
gists whom we knew to be interested in bullfrog-
related problems. Moreover, during the winter of
2005–2006 we posted e-mail messages asking
feedback from anyone knowing the presence of
bullfrogs in Europe. These messages were posted
on two major herpetological mailing lists: Herpnet
(479 subscribers, Europe-wide coverage) and
erpetologia (345 subscribers, mainly Italian
herpetologists). We particularly focused on the
Italian situation since Italy was the first country
where successful introductions of R. catesbeiana
occurred, and it is the country suffering the
largest number of introductions. Furthermore, in
several localities of northern Italy where the
species is historically known to be present (Al-
bertini and Lanza 1987), we performed additional
point counts and dip-netting to confirm the
bullfrog presence.
We subsequently sent questionnaires to all
people reporting current or past presence of
bullfrogs. The questions included the date and
the causes of introduction, the origin of individ-
uals, the current trend and status of the popula-
tion, and any available information about
eradication protocols. For areas of early intro-
duction and extinction, we also obtained data
from old literature and unpublished reports (Al-
bertini 1970; Veenvliet and Veenvliet 2002). We
considered as introduction events all cases in
which at least one reproduction was recorded, or
where a very large number of adults were
observed. We did not consider as introduction
events those in which only isolated adults were
observed.
Invasion success was classified as follows: 0,
extinct population; 1, established, but apparently
not invasive population (population did not
expand from the locality of introduction); 2,
invasive population (expansion from the locality
of introduction) (Kolar and Lodge 2001). We did
not quantify invasion success for populations
successfully eradicated after introduction.
Since it has been frequently assumed that
species-rich communities better resist invasion
than species-poor communities (Shea and Ches-
son 2002), we calculated the Spearman’s correla-
tion between invasion success and the number of
amphibian species present in the area, measured
as the number of species recorded in the same
grid square in the European herpetological atlas
(Gasc et al. 1997).
Results and discussion
Distribution in southwest France
The surveys detected the presence of R. catesbei-
ana in 123 out the 2,505 wetlands (Fig. 1b); we
observed successful reproduction in 30 wetlands.
Breeding populations of R. catesbeiana are pres-
ent in two geographic areas: Gironde (west of the
study area; at least 10 breeding wetlands, pres-
ence of the species in an area of about 1,800 km
2
)
and Dordogne (at least 20 breeding wetlands,
presence of the species in an area of about
200 km
2
). It should be noted that we did not
perform surveys in all the wetlands of the study
area; therefore, the real number of water bodies
where bullfrogs are present or breeding is prob-
ably larger than these figures.
The bullfrog distribution in the study area was
not continuous. For example, the populations in
the northwest corner of the study area (Dordo-
gne) are about 90 km from the other populations
(Fig. 1b), a distance far exceeding the possibility
of dispersal of this species estimated on the basis
of mark-recapture and microsatellite data (Austin
et al. 2004; Smith and Green 2005). This suggests
that secondary translocations into private wet-
lands as a pet or source of food (Albertini 1970;
Yiming et al. 2006) can substantially increase the
rate of expansion of this invasive species. Inter-
views of local people confirmed that, within the
study area, translocations were performed at least
in one case.
Our results show that R. catesbeiana is
present in a large area of southwest France,
and that this is the second largest area in
Europe where R. catesbeiana is present. More-
over, in this area, the bullfrog seems to be
particularly invasive compared to other Euro-
pean areas. For instance, in northern Italy,
American bullfrog Rana catesbeiana in Europe
123

R. catesbeiana is present over some 5,000 km
2
,
but the present situation is very similar to that
recorded during the 1980s (Albertini and Lanza
1987; Ferri 2006). Moreover, Italian populations
were introduced during the 1930s, and were the
first acclimatised in Europe, while French pop-
ulations were introduced 30 years later (Alber-
tini and Lanza 1987; Detaint and Coı
¨
c 2001).
This first monitoring of the situation in south-
west France suggests an alarming expansion of
the species compared to other European areas.
The increasing abundance of bullfrogs in this
area also increases the risk that individuals will
be captured and translocated elsewhere.
Although breeding populations exist in only
three French areas (see below, Fig. 1a), isolated
individuals have been observed in several fur-
ther localities, suggesting that translocations
have been frequent.
To hinder this expansion, a large-scale eradi-
cation plan is currently ongoing in southwest
France, including direct capture and trapping of
both adults and tadpoles, and education of local
people to the problems caused by biological
invasions (Detaint and Coı
¨
c 2006).
Distribution at the continental scale
We found evidence of at least 25 different
introductions of R. catesbeiana in Europe
(Appendix S1; Fig. 1a). Introductions have been
observed in Belgium, France, Germany, Greece,
Holland, Italy, Spain, and the United Kingdom.
Free-ranging populations are present in Belgium,
France, Germany, Greece, and Italy. Therefore,
the situation is radically different from that
recorded in the 1990s, when populations were
present only in France, Holland, and Italy (Lanza
and Ferri 1997). Successful eradication was per-
formed in at least three cases, while in 11 further
cases, bullfrogs disappeared after the introduction
(Appendix S1). Two of the successful eradications
(UK, Germany-Bonn) coped killing of individuals
(both adults and tadpoles) and complete drainage
of ponds where the population was breeding. In
the third successful eradication (Germany-Stutt-
gart), a complete fencing of the breeding pond
was performed in addition to the killing of
individuals (Thiesmeier et al. 1994).
The first introductions occurred during the
1930s (Italy) and 1960s (France), but 60% of
introductions occurred during the 1980s and
1990s. At least two introductions apparently
occurred after 1997, the year when the introduction
of R. catesbeiana was forbidden in Europe (law of
the European Council 2551/1997) (Appendix S1).
Information about the causes of introduction is
frequently lacking; however, in most cases, bull-
frogs were introduced as pets or because of
personal initiatives with unknown causes. Only
five introductions were performed as attempts at
commercial farming. This is in contrast to obser-
vations in other continents, where the bullfrog is
usually introduced for the production of food
(Lever 2003; Yiming et al. 2006).
The history of the Italian invasions was more
complex than those depicted by our paper (Fig. 1;
Appendix S1), including multiple secondary
translocations. The early dynamics of the Italian
invasion has been described in detail by Albertini
(1970, 1983) and Albertini and Lanza (1987).
Population invasiveness was positively related
to the number of amphibians species recorded in
the community (r
s
= 0.479, N = 21, P = 0.028).
This is contrary to what would be observed if the
richest communities were more resistant to inva-
sion. Such a pattern can be accounted for if other
extrinsic factors are positively related to both
richness of native communities and environmental
suitability for R. catesbeiana (Shea and Chesson
2002). For example, climatic features such as
temperature and precipitation are extremely
important in determining the distribution of Euro-
pean amphibians (Araujo et al. 2006), and may
play a role also in the suitability of European
localities for R. catesbeiana. At least five bullfrog
populations from France, Italy, and the United
Kingdom are or were infected by the fungus
B. dendrobatidis (Garner et al. 2006). The positive
association of bullfrog invasions with areas of high
richness of amphibians is, therefore, a cause of
particular concern for the fate of native species.
Conclusion
Our study shows an alarming increase of the
presence of R. catesbeiana in Europe, probably
G. F. Ficetola et al.
123

caused by the combined effect of multiple intro-
ductions from North America, secondary trans-
locations within European countries, and natural
expansion. The number of countries where bull-
frogs are present has almost doubled during the
last 10 years (Lanza and Ferri 1997), and the
species is present over a large area of southwest
France. Legislation already forbids new introduc-
tions and environmental agencies promote erad-
ication plans. However, translocation performed
as personal initiatives seems to be the main cause
of introductions. It is, therefore, very difficult to
avoid concluding that new introductions will be
performed in the future. Moreover, eradication
can be difficult; the three successful actions have
been performed at early stages of invasion and by
means of strenuous destruction or fencing of all
breeding wetlands. Therefore, we suggest promo-
tion of educational programs to reduce the risk of
new introductions and translocations from estab-
lished populations. Careful monitoring is neces-
sary for the early detection and management of
newly established populations.
Acknowledgements We thank all the people who helped
during field sampling, and all the herpetologists who
provided information about the situation in Europe.
P. Veenvliet provided valuable unpublished information;
the comments of B.R. Anholt and A. Bonin improved an
earlier version of the manuscript. Monitoring of the French
populations is funded by La Fe
´
de
´
ration des AAPPMA de
la Gironde, de la Dordogne, du Lot et Garonne, Le Conseil
Ge
´
ne
´
ral de la Gironde, du Lot et Garonne et de la
Dordogne, l’Agence de l’Eau Adour-Garonne, la Re
´
gion
Aquitaine and the European Council.
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