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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.
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Supplementary resource (1)

Data
October 2007
Gentile Francesco Ficetola · Christophe Coïc · Mathieu Detaint · Matthieu Berroneau · Claude Miaud
... The trade in live bullfrogs at a local pet market in the early 2000s can be expected to have contributed to the observed distribution pattern. A non-continuous spatial distribution of invasive bullfrogs linked to secondary translocations after initial introduction has also been reported in France and Italy (Ficetola et al. 2007a). ...
... the situation here can be expected to progressively evolve into one that can currently be found in France and Italy, where bullfrogs have occupied approximately 2000 km² and 5000 km² since their first introduction in 1968 and the 1930s, respectively (Ficetola et al. 2007a). These enormous occupied areas have also been reported for other invasive amphibian species, such as the African clawed frog in France, which has occupied 2055 km² since its single introduction in the 1980s (Measey et al. 2012;Vimercati et al. 2019). ...
... Nonetheless, our results indicate the presence of three clearly distinct metapopulations in the valley of the Grote Nete. Considering that no bullfrog eDNA was detected in a large number of water bodies in between these metapopulations, and that the buffer sizes on which the constructed AOO's were based had a radius that slightly exceeded the maximal annual bullfrog displacement distance observed, it is likely that multiple anthropogenically-mediated introductions have occurred even within this valley (Ficetola et al. 2007a). In other words, our results seem to contradict the common belief that invasive bullfrogs have spread in a linear fashion all the way from the region where they were first introduced, resulting in one large, interconnected metapopulation. ...
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The American bullfrog (Lithobates catesbeianus [Shaw, 1802]) is one of the hundred most destructive Alien Invasive Species (AIS) worldwide that has invaded more than 40 countries across 4 continents. In Belgium, bullfrogs have occupied a large area in a relatively short period of time despite a decade of intensive management interventions. Acquiring better insights into the distribution, abundance, and spatial spread of this invasive frog species is an important first step towards a successful management strategy. In this study, we sampled 382 permanent water bodies and combined environmental DNA (eDNA)-based analyses using quantitative droplet digital PCR (ddPCR) with assessments of habitat characteristics to generate an overview of the present distribution of bullfrogs in Flanders (Northern Region of Belgium) and the type of water bodies they have invaded. Our results revealed a fragmented distribution pattern covering an area of 364.76 km² that consisted of eight metapopulations located in five different river valleys, suggesting the occurrence of multiple anthropogenically-mediated introductions. Bullfrogs appeared to be firmly established in the valley of the Grote Nete, where invaded waterbodies have been found along 72% of the length of this river, divided into three distinct metapopulations. Unlike refuge sites, bullfrogs were found to be highly selective in their choice of breeding sites, which were characterised by abundant emergent vegetation and sparse tree cover along the shoreline. The division of the vast occupied area into well-defined, accurately delineated metapopulations facilitates the identification of functional management units. Furthermore, the obtained knowledge of the patterns of range expansions and the spatial configuration and associated environmental features of breeding sites can be used to prioritise management interventions in strategically located invasion hubs. Overall, we conclude that eDNA-based monitoring combined with environmental assessments provide important information that can be used to manage widespread aquatic AIS more effectively.
... In Europe, the American bullfrog has been introduced in several regions and it has naturalized populations in France, Germany, Italy, Belgium, and Greece [16]. In the three first countries, the depletion of native amphibian species has been documented [17]. ...
... At the beginning of this century, some specimens were occasionally captured in the Collserola Mountains (Barcelona) and in the Canary Islands, the latter being suspected of introduction through trade [18,19]. However, all of these records reported non-successful introductions, and the study from Ficetola et al. [16] considered this species to be eradicated in the Peninsula. More recently, in 2009, bullfrog tadpoles were detected in Barcelona among aquarium trade from Italy [20] and in the Ebre Delta, where a single specimen was recorded in 2012 [21]. ...
... Therefore, the two specimens found and the positive eDNA results in 2020 would correspond to a new invasion process, or possibly multiple introductions in the two invasion focuses. In other countries, reiterated intentional releases of the American bullfrog have been documented [16,57], and the same pattern could be taking place in the Ebre Delta. European legislation prohibits introductions of the American bullfrog and its commercial farming is completely forbidden in the Iberian Peninsula (Royal Decree 630/2013, 2 August). ...
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Simple Summary The introduction of alien species is one of the major causes of biodiversity loss. The American bullfrog (Lithobates catesbeianus) is considered to be one of the most harmful invasive species which overall threatens native amphibians. The detection of an invasive species in the first stage of its arrival is critical to control its colonization and to avoid its establishment. This early detection requires tools with high sensitivity. Methods based on the analysis of free environmental DNA (eDNA) are promising. The present article develops an eDNA assay to monitor the early process of invasion of the American bullfrog in the Ebre Delta (Spain), in a scenario where the presence of bullfrog specimens is really low and scarcely detected by traditional methods. In 2018, the first bullfrog tadpoles were found for the first time in the Ebre Delta. Two years after, despite the species not being well established, our eDNA assay detected the presence of bullfrogs in several locations. This methodology proved to yield a higher sensitivity with a lower sampling effort than traditional methods. Based on our experience, we also provided solutions to face challenges associated with the use of eDNA. Developing a rapid and low-cost-effective protocol to use in the early stages of an invasion (as occurred with the American bullfrog in the Iberian Peninsula) is essential to facilitate the detection, control, and eradication of an invasive species in the early stages of the invasion process. Abstract The American bullfrog (Lithobates catesbeianus) is considered to be one of the most harmful invasive species. In the Iberian Peninsula, this species had been cited occasionally until the year 2018, when L. catesbeianus appeared in the Ebre Delta, and, for the first time, it started breeding in a territory of the Peninsula. Using environmental DNA (eDNA) analysis and visual surveys, the American bullfrog invasion in the Ebre Delta was monitored across two consecutive years (2019–2020). No specimens were observed in 2019, and results for the eDNA survey also failed to detect this species in the Delta. In 2020, two individuals were captured and, under the most conservative criteria to constrain the number of positive detections, eDNA analyses detected the presence of the American bullfrog in at least five locations. Performing an eDNA assay yielded a higher sensitivity with a lower sampling effort than traditional methods. Although the American bullfrog does not appear to still be well-established in the Ebre Delta, only a few bullfrog individuals could be enough for their establishment in suitable habitats. In this context, eDNA assays are essential tools to facilitate the detection, control, and eradication of this species in the first stage of the invasion process.
... Free-ranging bullfrog populations are present in six countries in Europe; Belgium, France, Germany, Greece, Spain and Italy (Ficetola et al. 2007). They form regionally a threat to native biodiversity through predation, habitat and food competition (Batista 2002;Cross 2002;Wang and Li 2009) and as a vector of the Chytrid-fungus (Batrachochytrium dendrobatidis Loncore, 1999) (Blaustein and Kiesecker 2002;Hanselmann et al. 2004;Pasmans and Martel 2012). ...
... These measures only, however, are not effective to stop the further expansion of the species. Eradications in Europe have only been successful in an early stage of invasion (Banks et al. 2000;Devisscher et al. 2012;Ficetola, et al. 2007;Theismeier et al. 1994). New control methods for well-established populations are urgently needed to stop the further dispersion of this invasive species in Europe. ...
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Chemical sterilisation is a way to control populations of invasive exotic species. To investigate the potential to control populations of invasive American bullfrog (Lithobates catesbeianus), 26 adult male individuals were caught and injected with a dose of 0, 12.5, 25, 50, 100 mg/kg bisazir in order to induce DNA fragmentation in sperm cells and subsequent induce sterility. The results indicate that injecting 50 mg/kg bisazir causes significant fragmentation in the sperm of Lithobates catesbeianus. Before using chemicals in situ their potential risk for the environment should be documented. As a first step the inherent ecotoxic properties of bisazir were evaluated in both acute and chronic aquatic tests: microtox (Aliivibrio fischeri), microalga (Raphidocelis subcapitata), duckweed (Lemna minor), waterflea (Daphnia magna). The no effect concentration (NOEC) was 1 mg/l for Daphnia reproduction. Based on these results the predicted no effect concentration (PNEC) value was 20 µg/l. These results show the inherent ecotoxic properties of the compound and raise questions on the safe applicability in aquatic habitats.
... The invasive cane toad (Rhinella marinus) in Australia (Lever, 2001) exploits roads to achieve rapid range expansion (Seabrook and Dettmann, 1996;Brown et al., 2006). Widespread distribution may also arise from repeated introductions, as well as by post-introduction translocation; the discontinuous distribution of the invasive alien North American bullfrog (Lithobates catesbeianus) in southwest France was likely facilitated through translocations by humans (Ficetola et al., 2007). ...
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The alpine newt Ichthyosaura alpestris has achieved a widespread distribution as a non-native (alien) species in Britain since its initial introduction over a century ago, but the patterns of its release and subsequent dispersal have never yet been collectively analysed. We employed a multi-disciplinary combination of methods, using geographic profiling to estimate the likely number and locations of introductions, and mitochondrial DNA polymorphisms to investigate the likely geographic source of primary introductions, including the potential role of the pet trade. In parallel we used population genetic analysis and coalescence-based modelling to infer the demographics and directionality of dispersal from founding populations. Our results show that alpine newts have been released at multiple sites. We found a close resemblance between patterns of mtDNA haplotypes in the pet trade and those of established alpine newt populations, suggesting a relationship between trade, releases, and dispersal. Results from demographic modelling using Approximate Bayesian Computation are also consistent with multiple independent introductions with limited local dispersal, and additionally suggest that releases may occur from intermediate sources, such as captive populations. Our results support the hypothesis that deliberate human activity is largely responsible for both introductions of alpine newts into the UK and their wider dispersal post-introduction. The likely involvement of the international pet trade highlights the risk that ongoing releases of I. alpestris may expose native species to pathogens, whether pre-existing or novel.
... The bullfrog is an amphibian species endemic to North America, distributed from southern Canada to the eastern United States and northern Mexico (Ficetola et al., 2007). The first records of aquaculture farms for bullfrogs (Lithobates catesbeianus) production in the Americas date back to the late 19 th century, on farms with closed ponds and low productive yields (Orchard & Stéfani, 2022). ...
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In Mexico, intensive production of bullfrogs is one of the most important aquaculture activities, due to growing demand for their meat. Frogs can be hosts for several parasites that negatively affect their development and health. The objective of this study was to identify the presence of intestinal parasites in bullfrogs in aquaculture production units. Eighteen bullfrogs aquaculture production units were selected, and 20 animals (n=360) from each farm. Fecal samples were obtained by mucosal scraping and processed using the concentration method. The overall prevalence of intestinal parasites was 70.5%, and all farms had frogs infected by some species of parasite. Two species of parasites were identified: Eimeria sp. and Strongyloides sp. Significant differences were found regarding parasite prevalence between males and females (73.8% vs 58.8%) and regarding tibia length (5.5 vs 6.1 cm) and weight (168 vs 187 g) between parasitized and non-parasitized frogs. In conclusion, the present study showed a high prevalence of intestinal parasites, and morphometric alterations (weight, snout-cloaca length, radio-ulna length, tibia length and distance between parotid glands) were identified in the parasitized animals. These results provided useful information that will enable establishment of adequate control measures to help minimize the adverse effects of these parasites.
... In Europe, the American bullfrog has been introduced in several regions and it has naturalized populations in France, Germany, Italy, Belgium and Greece (Ficetola et al. 2007a). In the three rst countries, depletion of native amphibian species has been documented (Kraus 2009). ...
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The American bullfrog ( Lithobates catesbeianus ) is considered one of the most harmful invasive species. In the Iberian Peninsula, this species had been cited occasionally until the year 2018, when L. catesbeianus appeared in the Ebre Delta, and for the first time, it seemed to breed in a territory of the Peninsula. We used the methodology based on environmental DNA analysis (eDNA), to monitor the American bullfrog invasion in the Ebre Delta along two consecutive years (22019 − 2020). No specimens were observed in 2019, and results for the eDNA survey also failed to detect this species in the Delta. In 2020, two individuals were captured and eDNA analyses detected the presence of the American bullfrog in several locations. Under the most conservative criteria to constrain the number of positive detections, American bullfrog presence was confirmed in at least five locations. Based on our experience, we also aimed to explain how to face the potential errors and challenges of the eDNA method. Our eDNA assay yielded a higher sensitivity with lower sampling effort than traditional methods. Findings of this study suggest that attempts of American bullfrog introduction could be taking place in Ebre Delta. Despite the species does not appear to be well established yet, very few bullfrog individuals could be enough for the establishment of this species in suitable habitats. In this context, eDNA assays are essential tools to facilitate detection, control and eradication of this species at the first stage of the invasion process.
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Olfaction is a crucial capability for most vertebrates and is realized through olfactory receptors in the nasal cavity. The enormous diversity of olfactory receptors has been created by gene duplication, following a birth-and-death model of evolution. The olfactory receptor genes of the amphibians have received relatively little attention up to now, although recent studies have increased the number of species for which data are available. This study analyzed the diversity and chromosomal distribution of the OR genes of three anuran species (Engystomops pustulosus, Bufo bufo and Hymenochirus boettgeri). The OR genes were identified through searches for homologies, and sequence filtering and alignment using bioinformatic tools and scripts. A high diversity of OR genes was found in all three species, ranging from 917 in B. bufo to 1194 in H. boettgeri, and a total of 2076 OR genes in E. pustulosus. Six OR groups were recognized using an evolutionary gene tree analysis. While E. pustulosus has one of the highest numbers of genes of the gamma group (which detect airborne odorants) yet recorded in an anuran, B. bufo presented the smallest number of pseudogene sequences ever identified, with no pseudogenes in either the beta or epsilon groups. Although H. boettgeri shares many morphological adaptations for an aquatic lifestyle with Xenopus, and presented a similar number of genes related to the detection of water-soluble odorants, it had comparatively far fewer genes related to the detection of airborne odorants. This study is the first to describe the complete OR repertoire of the three study species and represents an important contribution to the understanding of the evolution and function of the sense of smell in vertebrates.
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This datasheet on Rana catesbeiana covers Identity, Overview, Associated Diseases, Pests or Pathogens, Distribution, Dispersal, Diagnosis, Biology & Ecology, Environmental Requirements, Natural Enemies, Impacts, Uses, Prevention/Control, Management, Genetics and Breeding, Economics, Further Information.
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Invasive non-native predators negatively affect native species; however, some native species can survive the predation pressures of invasive species by using pre-existing antipredator strategies or evolving defenses against invasive predators. The American bullfrog Lithobates catesbeianus (Anura: Ranidae) has been intentionally introduced to many countries and regions, and has impacted native animals through direct predation. Bombardier beetles (Coleoptera: Carabidae: Brachininae: Brachinini) discharge chemicals at a temperature of approximately 100 °C from the tip of the abdomen when they are attacked by predators. This “bombing” can successfully repel predators. However, adults of a native bombardier beetle Pheropsophus ( Stenaptinus ) occipitalis jessoensis have been reportedly found in the gut contents of the introduced bullfrog L. catesbeianus in Japan. These records suggest that the invasive bullfrog L. catesbeianus attacks the native bombardier beetle P . occipitalis jessoensis under field conditions in Japan; however, the effectiveness of the bombing defense against invasive bullfrogs is unclear. To test the effectiveness of the bombing defense against bullfrogs, we investigated the behavioral responses of L. catesbeianus juveniles to P . occipitalis jessoensis adults under laboratory conditions. Contrary to previous gut content results, almost all the bullfrogs (96.3%) rejected bombardier beetles before swallowing them; 88.9% rejected the beetles after being bombed, and 7.4% stopped attacking the beetles before being bombed. Only 3.7% successfully swallowed and digested the beetle. All of the beetles collected from non-bullfrog-invaded sites could deter bullfrogs, suggesting that the pre-existing defenses of bombardier beetles played an essential role in repelling bullfrogs. When treated beetles that were unable to discharge hot chemicals were provided, 77.8% of bullfrogs successfully swallowed and digested the treated beetles. These results indicate that bombing is important for the successful defense of P . occipitalis jessoensis against invasive bullfrogs. Although invasive bullfrogs have reportedly impacted native insect species, P . occipitalis jessoensis has an existing defense mechanism strong enough to repel the invasive predators.
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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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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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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? Location Europe. Methods Distributions of species are modelled with four species–climate envelope techniques (artificial neural networks, generalized linear models, generalized additive models, and classification tree analyses) and distributions are projected into the future using five climate‐change scenarios for 2050. Future projections are made considering two extreme assumptions: species have unlimited dispersal ability and species have no dispersal ability. A novel hybrid approach for combining ensembles of forecasts is then used to group linearly covarying projections into clusters with reduced inter‐model variability. Results We show that a great proportion of amphibian and reptile species are projected to expand distributions if dispersal is unlimited. This is because warming in the cooler northern ranges of species creates new opportunities for colonization. If species are unable to disperse, then most species are projected to lose range. Loss of suitable climate space for species is projected to occur mainly in the south‐west of Europe, including the Iberian Peninsula, whilst species in the south‐east are projected to gain suitable climate. This is because dry conditions in the south‐west are projected to increase, approaching the levels found in North Africa, where few amphibian species are able to persist. Main conclusions The impact of increasing temperatures on amphibian and reptile species may be less deleterious than previously postulated; indeed, climate cooling would be more deleterious for the persistence of amphibian and reptile species than warming. The ability of species to cope with climate warming may, however, be offset by projected decreases in the availability of water. This should be particularly true for amphibians. Limited dispersal ability may further increase the vulnerability of amphibians and reptiles to changes in climate.
Book
This book describes how the various alien reptiles and amphibians now living in the wild throughout the world were first introduced, how they subsequently became naturalized, their present distribution and status in those countries to which they were introduced, and their ecological and socio-economic impact (if any) on the native biota and local economies. Many species have had a more or less neutral impact, being neither beneficial nor harmful. However, several have had a positive ecological or socio-economic impact, while some such as the cane toad, have had an extremely destructive effect.The criteria for inclusion of a species are that it should have been imported from its natural range to a new country by human agency (either accidentally or deliberately) and that it should currently be established in the wild in self-maintaining and self-perpetuating populations unsupported by, and independent of, mankind.
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