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Pattern of distribution of the American bullfrog Rana catesbeiana in Europe

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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.
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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.
References
Albertini G (1970) Sulla diffusione della rana toro (Rana
catesbeiana Shaw) importata nel mantovano. Atti
Mem Accad Agricolt Sci Lett Verona 20(1968–
1969):67–106
Albertini G (1983) La Rana catesbeiana Shaw nella bassa
pianura reggiano-modenese. Atti Mem Accad Agri-
colt Sci Lett Verona 33(1981–1982):125–154
Albertini G, Lanza B (1987) Rana catesbeiana Shaw, 1802
in Italy. Alytes 6:117–129
Araujo MB, Thuiller W, Pearson RG (2006) Climate
warming and the decline of amphibians and reptiles in
Europe. J Biogeogr 33:1712–1728
Austin JD, Lougheed SC, Boag PT (2004) Controlling for
the effects of history and nonequilibrium conditions in
gene flow estimates in northern bullfrog (Rana cates-
beiana) populations. Genetics 168:1491–1506
Beebee TJC, Griffiths RA (2005) The amphibian decline
crisis: a watershed for conservation biology? Biol
Conserv 125:271–285
Berger L, Rick Speare R, Daszak P, Earl Green D,
Cunningham AA, Louise Gogging C, Slocombe R,
Ragan MA, Hyatt AD, McDonald KA, Hines HB,
Lips KR, Marantelli G, Parkes H (1998) Chytridi-
omycosis causes amphibian mortality associated with
population declines in the rain forests of Australia
and Central America. Proc Natl Acad Sci USA
95:9031–9036
Bosch J, Martine
´
z-Solano I, Garcia-Paris M (2001) Evi-
dence of a chytrid fungus infection involved in the
decline of the common midwife toad (Alytes obstet-
ricans) in protected areas of central Spain. Biol
Conserv 97:331–337
Detaint M, Coı
¨
c C (2001) Invasion de la Grenouille
taureau (Rana catesbeiana) en France: Synthe
`
se
bibliographique, suivi 2000–2001, perspectives. Cis-
tude Nature, Le Haillan
Detaint M, Coı
¨
c C (2006) La Grenouille taureau Rana
catesbeiana dans le sud-ouest de la France. Premiers
re
´
sultats du programme de lutte. Bull Soc Herpetol
France 117:41–56
Ferri V (2006) Rana catesbeiana Shaw, 1802. In: Sindaco
R, Doria G, Razzetti E, Bernini F (eds) Atlas of
Italian amphibians and reptiles. Polistampa, Firenze,
pp 330–333
Garner TWJ, Perkins MW, Govindarajulu P, Seglie D,
Walker S, Cunningham AA, Fisher MC (2006) The
emerging amphibian pathogen Batrachochytrium
dendrobatidis globally infects introduced populations
of the North American bullfrog, Rana catesbeiana.
Biol Lett 2:455–459
Gasc JP, Cabela A, Crnobrnja-Isailovic J, Dolmen D,
Grossenbacher K, Haffner P, Lescure J, Martens H,
Martı
´
nez Rica JP, Maurin H, Oliveira ME, Sofianidou
TS, Veith M, Zuiderwijk A (1997) Atlas of the
amphibians and reptiles in Europe. Societas Herpe-
tologica Europaea & Museum National d’Histoire
Naturelle, Paris
Hanselmann R, Rodriguez A, Lampo M, Fajardo-Ramos
L, Aguirre A, Kilpatrick M, Rodriguez JP, Daszak P
(2004) Presence of an emerging pathogen of amphib-
ians in introduced bullfrogs Rana catesbeiana in
Venezuela. Biol Conserv 120:115–119
Kats LB, Ferrer RP (2003) Alien predators and amphibian
declines: review of two decades of science and the
transition to conservation. Divers Distrib 9:99–110
Kolar CS, Lodge DM (2001) Progress in invasion biology:
predicting invaders. Trends Ecol Evol 16:199–204
Lanza B, Ferri V (1997) Rana catesbeiana. In: Gasc JP,
Cabela A, Crnobrnja-Isailovic J et al (eds) Atlas of
the amphibians and reptiles in Europe. Societas
Herpetologica Europaea & Museum National d’His-
toire Naturelle, Paris, pp 132–133
Lever C (2003) Naturalized amphibians and reptiles of the
world. Oxford University Press, New York
American bullfrog Rana catesbeiana in Europe
123
Lips KR, Brem F, Brenes R, Reeve JD, Alford RA,
Voyles J, Carey C, Livo L, Pessier AP, Collins JP
(2006) Emerging infectious disease and the loss of
biodiversity in a neotropical amphibian community.
Proc Natl Acad Sci USA 103:3165–3170
Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100
of the world’s worst invasive alien species. A selection
from the Global Invasive Species Database. ISSG,
SSC and IUCN. Available at www.issg.org/book-
let.pdf
Pounds JA, Bustamante MR, Coloma LA, Consuegra JA,
Fogden MPL, Foster PN, La Marca E, Masters KL,
Merino-Viteri A, Pushendorf R, Ron SR, Sanchez-
Azofeifa GA, Still CJ, Young BE (2006) Widespread
amphibian extinctions from epidemic disease driven
by global warming. Nature 439:161–167
Shea K, Chesson P (2002) Community ecology theory as a
framework for biological invasions. Trends Ecol Evol
17:170–176
Smith MA, Green DM (2005) Dispersal and the meta-
population paradigm in amphibian ecology and con-
servation: are all amphibian populations
metapopulations? Ecography 28:110–128
Thiesmeier B, Ja
¨
ger O, Fritz U (1994) Erfolgreiche
Reproduktion des Ochsenfrosches (Rana catesbeiana)
im no
¨
rdlichen Landkreis Bo
¨
blingen (Baden-Wu
¨
rttem-
berg). Zeitschrift fu
¨
r Feldherpetologie 1:169–176
Veenvliet P, Veenvliet JK (2002) Review of the status of
Rana catesbeiana in the European Union. In: Adrados
LC, Briggs L (eds) Study of application of EU wildlife
trade regulations in relation to species which form an
ecological threat to EU fauna and flora, with case
studies of American bullfrog (Rana catesbeiana) and
red-eared slider (Trachemys scripta elegans). Unpub-
lished report to the European Commission, Amphi
Consult, Denmark
Yiming L, Zhengjun W, Duncan RP (2006) Why islands
are easier to invade: human influences on bullfrog
invasion in the Zhoushan archipelago and neighbor-
ing mainland China. Oecologia 148:129–136
G. F. Ficetola et al.
123

Supplementary resource (1)

Data
October 2007
Gentile Francesco Ficetola · Christophe Coïc · Mathieu Detaint · Matthieu Berroneau · Claude Miaud
... Bullfrog directly impacts native amphibians through predation and competition for resources and indirectly through the spread of deadly amphibian pathogens such as the fungi Batrachochytrium dendrobatidis and Saprolegnia ferax (Nori et al., 2011). B. dendrobatidis is the agent of chytridiomycosis (Garner et al., 2006), an infectious disease that is considered one of the main causes of ongoing global amphibian decline and extinction and L. catesbeianus may be infected by the fungus without developing the disease (Daszak et al., 2004;Ficetola et al., 2007a). Currently, little is known about American bullfrog impact on native species in Europe. ...
... Introductions of the species have been observed in Belgium, France, Germany, Greece, Holland, Italy, Spain, and the United Kingdom and established populations detected in Belgium, France, Germany, Greece, and Italy. Three successful eradications were reported, two of them (UK and Germany) by killing of individuals (both adults and tadpoles) and complete drainage of ponds and a third (also in Germany), by fencing the pond and consequently killing of individuals (Ficetola et al., 2007a). Initial introductions were probably due to pet trading and further expansion of bullfrogs occurred due to natural dispersal (short distances), or secondary human mediated translocations such as commercial farming initiatives (Ficetola et al., 2007a). ...
... Three successful eradications were reported, two of them (UK and Germany) by killing of individuals (both adults and tadpoles) and complete drainage of ponds and a third (also in Germany), by fencing the pond and consequently killing of individuals (Ficetola et al., 2007a). Initial introductions were probably due to pet trading and further expansion of bullfrogs occurred due to natural dispersal (short distances), or secondary human mediated translocations such as commercial farming initiatives (Ficetola et al., 2007a). Nonetheless Ficetola et al., 2010 reported that for Italy, bullfrog dispersal did not reach its maximum due to habitat fragmentation, presence of barriers such as roads/urbanizations and changes in land use decreasing water availability (in ponds, wetlands, rice fields, etc). ...
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... We searched for literature on non-native populations of Hoplobatrachus tigerinus on Google Scholar (September 2018) by employing a combination of key words covering taxonomic variation (including the previous taxonomic combinations 'Rana tigerina' and 'Rana tigrina') and invasion status ('alien', 'introduced', 'non-native', 'exotic', 'non-indigenous' and 'invasive'). We also consulted local researchers and herpetologists, in both native and non-native ranges, for occurrence information where published literature was lacking (Ficetola et al. 2007a). Identified non-native populations were evaluated for their invasion stage (following Blackburn et al. 2011), dispersal pathways (of introduction and secondary transfers), impact (see section 'Impact Scoring' below), and management actions undertaken. ...
... predation of native vertebrates, Table 1; Hirschfeld and Rödel 2011;Pili et al. 2019). Similarities in the invasion process of Hoplobatrachus to the well-studied model species Lithobates catesbeianus (130 publications on its non-native populations; Ficetola et al. 2007a;van Wilgen et al. 2018) belonging to the same ''invasion syndrome'', should be leveraged to frame hypotheses and inform management (Novoa et al. 2020). ...
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Full-text available
Invasive amphibians have considerable ecological and socio-economic impact. However, strong taxonomic biases in the existing literature necessitate synthesizing knowledge on emerging invaders. The Indian bullfrog, Hoplobatrachus tigerinus, a large dicroglossid frog (snout to vent length: up to 160 mm), is native to the Indian sub-continent. Despite the high likelihood of invasion success for H. tigerinus, based on the species’ natural history traits and human use, the status of its non-native populations and global invasion potential has not yet been assessed. In this paper, we provide a profile of H. tigerinus as an invasive species to aid in risk analyses and management of existing populations. We review the available knowledge on non-native populations of H. tigerinus and model its potential distribution in the non-native range and globally; finally, we evaluate its ecological and socio-economic impact using standard impact classification schemes. We confirm successful invasions on the Andaman archipelago and Madagascar. The ensemble species distribution model, with ‘good’ predictive ability and transferability, predicts tropical regions of the world to be climatically suitable for the species. Considering potential for propagule pressure, we predict the climatically suitable Mascarene Islands, Malaysia and Indonesia, and East Africa to likely be recipients of bridgehead invasions. We assign the species two impact scores: both socio-economic and environmental scores were ‘moderate’ with ‘medium’ confidence levels in our assessment. Finally, this synthesis outlines the invasion process of the genus Hoplobatrachus, which is an emerging group of amphibian invaders.
... Whatever the specific route of entry, feral populations of non-native amphibians are currently extant throughout the UK, particularly in the South (Langton et al., 2011). American bullfrogs were a heavily imported species (Banks, 2000) that currently maintain a southern foothold in the UK, but have since been eradicated from a once more widespread distribution (Ficetola et al., 2007(Ficetola et al., , 2008. ...
Thesis
Ranavirus is a genus of large double-stranded DNA viruses (family Iridoviridae) that parasitise three taxonomic classes of poikilothermic vertebrates. They are important wildlife pathogens of conservation and economic concern, posing significant threat to amphibian biodiversity and aquaculture commerce. Despite substantial advances since their discovery in the 1960s, the evolutionary history of ranaviruses remains poorly characterised. The aim of this thesis is to advance the characterisation of Ranavirus evolutionary dynamics to contemporary standards. A large whole-genome dataset was collated and scrutinised, combining all publicly available material with a novel collection of isolate genomes. Cutting-edge microbial genomics tools were applied to gain insight into ranavirus genetic diversity, phylogeography, and genome evolution. Delineation of the Ranavirus pan-genome served as a foundation to conduct phylogenetic and population genetic analyses. Where the limitations of alignment-based methodologies were met, alignment-free techniques were employed to make full use of all genomic information. Phylogenetic reconstructions uncovered unique genetic diversity incompatible with current taxonomic demarcations amongst several lineages of Ranavirus. Pervasive genetic recombination was detected across the genus, and certain lineages contained a high degree of ancestral polyphyly. Recurrent patterns linked to animal trade and aquaculture were detected. Extensively polyphyletic viruses were isolated from captive animals, and population genetic analysis revealed ancestry components shared by ranaviruses isolated from farmed animals on separate continents. Finally, phylodynamic analysis suggests human-mediated translocation of FV3-like ranaviruses began more than a century before present. The inadequacies of current Ranavirus taxonomy are highlighted by this work, and suggests a substantial diversity remains to be characterised. The processes by which ranaviral genetic diversity is generated appears particularly dynamic, with significant contributions made via recombination between distinct linages. Altogether, this thesis underscores the vital impact trade and captive rearing of fish and herpetofauna have had on the global spread of ranaviruses and their processes of genetic diversification. Finally, these results suggest that anthropogenic influences commenced decades earlier than previously thought, likely upon the acceleration of modern globalisation.
... Bullfrogs are native to the eastern United States, but have been introduced to the western United States and Canada, South America, Asia, and Europe (Ficetola et al., 2007). This large frog species exerts a severe pressure on indigenous amphibian communities through fierce resource competition, gape-limited predation, and the transmission of novel pathogens, and is therefore ranked among the most destructive invaders worldwide (Lowe et al., 2000). ...
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Biological invasions contribute now more than ever to the global homogenization of fauna and flora. Large‐scale monitoring programs are, therefore, needed to detect incipient invasions and to evaluate management interventions. As conventional monitoring methods are constrained by large costs, environmental DNA (eDNA)‐based methods are increasingly recognized as valuable monitoring tools. However, accurately estimating species abundance from eDNA concentrations in natural systems remains challenging and consequently hinders their integration in management applications. Here, we used droplet digital PCR (ddPCR) in eDNA surveys to estimate the abundance of invasive American bullfrogs (Lithobates catesbeianus). We first introduced bullfrog tadpoles in natural ponds to assess the relationship between abundances and eDNA concentrations under field conditions. Next, we combined eDNA sampling with fyke netting in naturally colonized ponds to investigate whether bullfrog eDNA concentrations can estimate bullfrog capture success and conventional abundance measures obtained via depletion sampling. Finally, we evaluated eradication measures by comparing bullfrog eDNA concentrations before and after fyke netting. We found a strong linear relationship between the numbers of introduced tadpoles and eDNA concentrations (r2 = 0.988). Bullfrog eDNA concentrations were not only linearly related to the catch‐per‐unit‐effort (r2 = 0.739), but also to conventional abundance estimates (r2 = 0.716), particularly when eDNA concentrations were standardized for pond area (r2 = 0.834) and volume (r2 = 0.888). Bullfrog tadpoles were only captured when eDNA concentrations exceeded 1.5 copies µl−1, indicating that quantitative eDNA analyses enable the localization of breeding ponds. We found a significant reduction in eDNA concentrations after fyke netting proportional to the number of captured bullfrogs. These results demonstrate that eDNA quantification is a reliable tool that accurately estimates bullfrog abundance in natural lentic systems. We show that quantitative eDNA analyses can complement the toolbox of natural resource managers and facilitate the coordination of eradication campaigns targeting alien invasive species. By quantifying eDNA concentrations before and after a national eradication campaign, we demonstrate that quantitative eDNA analyses can (i) accurately predict the number of individuals that can be captured, (ii) locate breeding ponds that serve as dispersal hubs, (iii) evaluate the efficacy of eradication programs, and thus that this technique can be a valuable addition to the nature resource manager's toolbox. As such, we present a novel approach in which quantitative eDNA analyses can significantly contribute to the control of biological invasions.
... Grant et al. 2020), et en Europe la présence d'espèces exotiques, les changements climatiques et la disponibilité des habitats favorables apparaissent comme des pressions majeures (Falaschi et al. 2019). La Normandie n'accueille pas d'espèces d'amphibiens introduits ailleurs en France continentale comme la Grenouille taureau (Lithobates catesbeianus) ou le Xénope lisse (Xenopus laevis), connues pour impacter au moins à court terme les communautés d'amphibiens autochtones (Ouellet et al., 2012 ;Ficetola et al., 2006 ;Fouquet et al., 2006 ;Lillo et al., 2010). La Grenouille rieuse est la seule espèce allochtone rencontrée en Normandie (Barrioz et al. 2015). ...
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The alarming decline of amphibians in France: The documented example of Normandy. Amphibians are exposed to numerous pressures such as the disappearance and degradation of their terrestrial and aquatic habitats, the introduction of invasive species, diseases, and climate change, which lead to the disappearance or decline of populations. Many environmental assessments (e.g. European directives, red lists, etc.), or management practices in protected areas are based on the status of populations. In this context, a consortium (SHF, CPIE, ONF, RNF, CEFE) has developed protocols to assess trends in amphibian communities (or target species). Unlike the distribution atlas-type approaches already well developed in France, these new protocols (known as "POPAmphibien") are based on the site occupancy framework that model amphibian occurrence in aquatic sites, while correcting for the probability of species detection. This paper presents the results of the application of a POPAmphibien "community" protocol in Normandy, with the aim of describing the temporal trend of an amphibian community by carrying out three field surveys per year that considering the phenology of the different species. Between 2007 and 2018, 114 areas (sectors presenting several aquatic sites potentially colonised by amphibians) comprising 1255 aquatic sites were monitored using standardised methods. The trends for the 15 taxa monitored in Normandy show a decrease for nine of them (Alytes obstetricans, Bufo sp, Rana temporaria, Pelophylax kl. esculentus, Salamandra salamandra, Ichthyosaura alpestris, Triturus cristatus, Lissotriton helveticus and Lissotriton vulgaris), a stability for four species (Epidalea calamita, Pelophylax ridibundus, Hyla arborea and Triturus marmoratus) and an increase for two species (Rana dalmatina and Pelodytes punctatus). Habitat degradation, particularly in agricultural landscapes, and climate change (drying up of breeding sites) particularly affect species such as Salamandra salamandra and Rana temporaria. Management measures (over digging of ponds, protection of habitats) appear to be favourable to the populations of P. punctatus which are confined to dunes and coastal marshes under protection status. R. dalmatina is on the increase, particularly outside protected areas, probably due to its expansion northwards for at least fifteen years in connection with more favourable local climatic conditions and the presence of refuge micro-habitats. These are the first results obtained with this methodology, deployment on a national scale will enable increasing precise analyses of the factors influencing the dynamics of amphibian populations in France, including management practices.
... Additionally, adult bullfrogs can play a critical role as carriers of pathogens as ranaviruses, the chytrid fungus Batrachochytrium dendrobatidis as well as pathogenic bacteria [73][74][75][76] . Research to understand traits explaining advantages of an invasive species can guide strategies to prevent expansion of bullfrogs' distribution into temporary and permanent habitats where native amphibians and bullfrogs can co-occur 55,77 . ...
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Invasive species pose a major threat to global biodiversity. The effects of invasive species can be strongly influenced and potentially mediated by their reproductive characteristics, such as fecundity, egg production, and duration and number of reproductive events. Selection for smaller body size at first reproduction can also play a role in their establishment, facilitating colonization and spread. The American bullfrog, native to the eastern U.S. ( Lithobates catesbeianus ), is a species that has invaded more than 40 countries across 4 continents. This species has become especially prevalent in the western United States since its introduction in the early 1900s. This study characterized reproductive characteristics of bullfrogs with emphasis on the minimum size at which males and females reach sexual maturity in the Willamette Valley, Oregon, USA invasion range. We collected and dissected 121 individuals in 2013 and 2017, quantifying characteristics of sexual maturity including snout-vent length, total length, sex, tympanum diameter, presence of distended oviducts or eggs for females, and testes length and sperm activity in males. Our results showed that the minimum reproductive size of both males and females was smaller relative to bullfrogs in their native range as well as in populations across their invasive range. Reduction in size at reproductive maturity is likely impacting the invasive success of American bullfrogs and this study gives us insight on management actions to control the invasion. Applying this insight, managers can adjust their definition of reproductively active adults, increasing the target population of culling and other control methods.
... For example, bullfrogs in the Yellowstone River in southcentral Montana spread roughly ten times this distance in three years (Sepulveda et al. 2015a) and molecular evidence suggests that this spread was natural and not aided by human secondary translocations (Kamath et al. 2016). In southwest France, bullfrogs have spread to over 2,000 km 2 since their introduction in the 1960s but this spread was likely facilitated by secondary translocations (Ficetola et al. 2007a). The Snake and Gros Ventre Rivers are ~8 km and 1 km, respectively, from KWS-overland distances that bullfrogs in other systems have moved without the aid of human secondary translocations (e.g., 10 km overland in a week in southern Arizona [Suhre 2010] and 1.2 km between June and July in Missouri [Willis et al. 1956]). ...
Article
Introduced American Bullfrogs (Lithobates catesbeianus) have been present in Grand Teton National Park since approximately the 1950s, but little is known about their distribution and potential impacts. In this study, we surveyed the current bullfrog distribution and spatial overlap with sympatric native amphibians in the park, and characterized post-metamorphic bullfrog diets from July – September 2015. Despite surveys in multiple large rivers and floodplain habitats, we only documented bullfrogs in a geothermal pond and 5 km of stream channel immediately downstream of this pond. In these waters, bullfrogs overlapped with native amphibians at the downstream end of their distribution, and we did not document native amphibians in bullfrog stomach contents. Larger bullfrogs (SVL ≥ 96 mm) primarily consumed native rodents (especially meadow voles, Microtus pennsylvanicus), while smaller bullfrogs frequently consumed native invertebrates and less frequently consumed non-native invertebrates and fish. Taken together, these data indicate that the distribution and implications of the bullfrog invasion in Grand Teton National Park are currently localized to a small area, so these bullfrogs should therefore be vulnerable to eradication.
... Alien species, which were introduced by man outside their natural ranges, can strongly impact local environments and compete against native species, which can lead to their extinction (Kraus 2009(Kraus , 2015Bucciarelli et al. 2014). Several nonnative amphibian species are known in Europe, among which the most well known are the African clawed frog, Xenopus laevis (Daudin, 1802), and the American bullfrog, Lithobates catesbeianus (Shaw, 1802) (Ficetola et al. 2007;Measey et al. 2012). ...
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Alien species can strongly impact local environments and compete against native species, which can lead to their extinction. Marsh frogs of the Pelophylax ridibundus complex are one of the most invasive amphibians in Northern Eurasia. It was previously thought that three water frog species of the genus Pelophylax (the marsh frog, P. ridibundus, the pool frog, P. lessonae and their hemiclonal hybrid, the edible frog, P. esculentus) inhabited Kaliningradskaya Oblast' along the Russian Baltic coast. However, based on our study of the intron-1 of the nuclear serum albumin gene, two other marsh frog species were detected (the Balkan marsh frog, P. kurtmuelleri, and the Anatolian marsh frog, P. cf. bedriagae) as well as putative hybrids between P. ridibundus and P. cf. bedriagae. The majority of individuals of P. ridibundus and hybrids between P. ridibundus and P. cf. bedriagae had mitochondrial (mt) DNA of P. lessonae, while all others featured the P. kurtmuelleri mtDNA. The prevalence of P. lessonae mtDNA haplotypes in populations of P. ridibundus from the Baltic Coast of Russia suggests that local individuals of the latter species originated from crosses between P. esculentus individuals. Two hypotheses could explain the records of P. kurtmuelleri and P. cf. bedriagae in the region. The establishment of local populations of the first species could have occurred via postglacial dispersal from the Balkan refugium. The origin of local P. cf. bedriagae could be an occasional introduction of individuals from the Ponto-Caspian region. Since our study is preliminary (19 individuals), in the future it would be important to continue the study of water frogs in Kaliningradskaya Oblast' and neighboring countries by applying multiple genetic markers. Additional genetic markers will enable researchers to study routes of dispersal and introductions of marsh frogs, to clarify peculiarities of their hybridization and distribution, and to evaluate the impact of P. kurtmuelleri and P. cf. bedriagae on the reproduction success of hybridogenous populations and abundance of local amphibians.
... Over the last two centuries this amphibious has been disseminated worldwide, mainly in Italy, France, Holland and Brazil [1,2]. Its meat was introduced to the human diet due to its rich nutritional value, which has been attributed to the presence of fatty acids and the high amount of essential amino acids, known to be responsible for several of its biological activities [3]. ...
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Bullfrog oil, an animal oil extracted from the adipose tissue of Rana catesbeiana Shaw, showed promising cytotoxic activity against melanoma cells and, therefore, has the potential to become a pharmaceutical active compound. However, there is a lack of information regarding the pathways involved in its pharmacological activity. Thus, the aim of this study was to investigate and elucidate the cytotoxic effect of this oil against A2058 human melanoma cells. The cytotoxic potential was evaluated by the MTT assay, the cell cycle analysis and the cell death assay. In addition, the apoptotic potential was investigated by (i) the DNA fragmentation using propidium iodide staining analysis, (ii) the evaluation of mitochondrial membrane potential and (iii) the determination of intracellular Reactive Oxygen Species (ROS) level. The results showed that the bullfrog oil was able to promote a time-dependent cytotoxic effect, decreasing cell viability to 38% after 72 h of treatment without affecting the cell cycle. Additionally, the bullfrog oil induced the apoptosis in A2058 cells, increasing up to 50 ± 13% of the intracellular ROS level, maintaining the DNA integrity and promoting an approximate decrease of 35 ± 5% in the mitochondrial membrane potential. It can be concluded that the in vitro cytotoxic effect of the bullfrog oil in A2058 human melanoma cells is mediated by oxidative stress that induces mitochondrial dysfunction, triggering the apoptosis. These unprecedented results highlight the pharmacological potential of bullfrog oil and provide important information to support studies on the development of new pharmaceutical products for complementary and alternative treatments for melanoma.
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The invasive species are of global concern, and the Invasive American Bullfrog (IAB; Lithobates catesbeianus) is one of the worst invasive amphibian species worldwide. Like other countries, South Korea is also facing challenges from IAB. Although many studies indicated impacts of IAB on native anurans in Korea, the actual risk at the specific level is yet to evaluate. Considering the putative invasiveness of IAB, it is hypothesized that any species with the possibility of physical contact or habitat sharing with them, will have a potential risk. Thus, we estimated and observed their home range, preferred habitats, morphology, behavior, and ecology. Then, comparing with existing knowledge, we assessed risks to the native anurans. We found a home range of 3474.2 ± 5872.5 m² and identified three types of habitats for IAB. The analyses showed at least 84% of native anurans (frogs and toads) were at moderate to extreme risks, which included all frogs but only 33% of toads. Finally, we recommended immediate actions to conserve the native anurans based on our results. As this study is the first initiative to assess the specific risk level from the invasiveness of L. catesbeianus, it will help the managers to set conservation priorities and strategies.
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Epidermal changes caused by a chytridiomycete fungus (Chytridiomycota; Chytridiales) were found in sick and dead adult anurans collected from montane rain forests in Queensland (Australia) and Panama during mass mortality events associated with significant population declines. We also have found this new disease associated with morbidity and mortality in wild and captive anurans from additional locations in Australia and Central America. This is the first report of parasitism of a vertebrate by a member of the phylum Chytridiomycota. Experimental data support the conclusion that cutaneous chytridiomycosis is a fatal disease of anurans, and we hypothesize that it is the proximate cause of these recent amphibian declines.
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Nonequilibrium conditions due to either allopatry followed by secondary contact or recent range expansion can confound measurements of gene flow among populations in previously glaciated regions. We determined the scale at which gene flow can be estimated among breeding aggregations of bullfrogs (Rana catesbeiana) at the northern limit of their range in Ontario, Canada, using seven highly polymorphic DNA microsatellite loci. We first identified breeding aggregations that likely share a common history, determined from the pattern of allelic richness, factorial correspondence analysis, and a previously published mtDNA phylogeography, and then tested for regional equilibrium by evaluating the association between pairwise F-ST and geographic distance. Regional breeding aggregations in eastern Ontario separated by less than or equal to100 km were determined to be at or near equilibrium. High levels of gene flow were measured using traditional 1 statistics and likelihood estimates of Nm. Similarly high levels of recent migration (past one to three generations) were estimated among the breeding aggregations rising nonequilibrium methods. We also show that, in many cases, breeding aggregations separated by tip to tens of kilometers are not genetically distinct enough to be considered separate genetic populations. These results have important implications both for the identification of independent "populations" and in assessing the effect of scale in detecting patterns of genetic equilibrium and gene flow.
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Aim We explore the relationship between current European distributions of amphibian and reptile species and observed climate, and project species potential distributions into the future. Potential impacts of climate warming are assessed by quantifying the magnitude and direction of modelled distributional shifts for every species. In particular we ask, first, what proportion of amphibian and reptile species are projected to lose and gain suitable climate space in the future? Secondly, do species projections vary according to taxonomic, spatial or environmental properties? And thirdly, what climate factors might be driving projections of loss or gain in suitable environments for species?
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During the summers of 1997, 1998 and 1999 mass mortality episodes of post-metamorphic common midwife toads (Alytes obstetricans) occurred in a protected area in central Spain. The population suffered a sharp decline, disappearing from 86% of the ponds where they were known to reproduce some years ago. Scanning electron microscopy and histological techniques revealed the presence of a chytridiomycosis infection in the skin of the toads. This evidence supports chytridiomycosis as the most plausible cause of the decline of the species in the area. This is the first report of an apparent chytridium-caused amphibian decline in Europe.
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Remark: this isn't the "real"atlas! This is a book Review of the Atlas; the author of the book Review is Tim Halliday.
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Over the last two decades, numerous studies have shown that alien predators contributed to amphibian population declines. Both experimental studies and correlative field surveys implicated alien species of fish, bullfrogs and crayfish as major contributors to amphibian population decline, and in some instances local extinction. Additional studies have demonstrated that alien predators also caused long-term changes in aquatic communities. Recent studies have examined the feasibility of removing alien predators, and provide some evidence that amphibian populations can recover. Applying information gained from past studies to the recovery of amphibian populations will be the challenge of future studies. International, national and local policies that regulate alien predators should be based largely on the body of scientific evidence already in the literature. Scientists need to be more involved with policy-makers to most effectively change laws that regulate alien predators.
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Amphibians are frequently characterized as having limited dispersal abilities, strong site fidelity and spatially disjunct breeding habitat. As such, pond-breeding species are often alleged to form metapopulations. Amphibian species worldwide appear to be suffering population level declines caused, at least in part, by the degradation and fragmentation of habitat and the intervening areas between habitat patches. If the simplification of amphibians occupying metapopulations is accurate, then a regionally based conservation strategy, informed by metapopulation theory, is a powerful tool to estimate the isolation and extinction risk of ponds or populations. However, to date no attempt to assess the class-wide generalization of amphibian populations as metapopulations has been made. We reviewed the literature on amphibians as metapopulations (53 journal articles or theses) and amphibian dispersal (166 journal articles or theses for 53 anuran species and 37 salamander species) to evaluate whether the conditions for metapopulation structure had been tested, whether pond isolation was based only on the assumption of limited dispersal, and whether amphibian dispersal was uniformly limited. We found that in the majority of cases (74%) the assumptions of the metapopulation paradigm were not tested. Breeding patch isolation via limited dispersal and/or strong site fidelity was the most frequently implicated or tested metapopulation condition, however we found strong evidence that amphibian dispersal is not as uniformly limited as is often thought. The frequency distribution of maximum movements for anurans and salamanders was well described by an inverse power law. This relationship predicts that distances beneath 11–13 and 8–9 km, respectively, are in a range that they may receive one emigrating individual. Populations isolated by distances approaching this range are perhaps more likely to exhibit metapopulation structure than less isolated populations. Those studies that covered larger areas also tended to report longer maximum movement distances – a pattern with implications for the design of mark-recapture studies. Caution should be exercised in the application of the metapopulation approach to amphibian population conservation. Some amphibian populations are structured as metapopulations – but not all.
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Community ecology theory can be used to understand biological invasions by applying recent niche concepts to alien species and the communities that they invade. These ideas lead to the concept of ‘niche opportunity’, which defines conditions that promote invasions in terms of resources, natural enemies, the physical environment, interactions between these factors, and the manner in which they vary in time and space. Niche opportunities vary naturally between communities but might be greatly increased by disruption of communities, especially if the original community members are less well adapted to the new conditions. Recent niche theory clarifies the prediction that low niche opportunities (invasion resistance) result from high species diversity. Conflicting empirical patterns of invasion resistance are potentially explained by covarying external factors. These various ideas derived from community ecology provide a predictive framework for invasion ecology.