Age and body size in four introduced populations of the American bullfrog, Lithobates catesbeianus (Ranidae)

Abstract

The American bullfrog, native to the eastern half of North America including southern Quebec, is considered one of the most invasive species in the world. It has been introduced in America, Asia and Europe, mainly for food purposes. A study on the age and body size of this species was carried out on individuals obtained from four introduced populations (one from Western Canada and three from France), using the skeletochronological method. Adults did not differ between sexes in mean body size or mean age, with the exception of one population in France where males were younger than females. Several differences in the mean age and body size were observed, with the individuals from the population in Canada exhibiting the highest values for both sexes. The scarcity of studies in the native range prevents the comparison of introduced versus native populations, and we focus on comparisons between introduced populations.

Full text

Full Terms & Conditions of access and use can be found at
http://www.tandfonline.com/action/journalInformation?journalCode=tizo20
Download by: [80.117.88.47] Date: 05 December 2016, At: 13:28
Italian Journal of Zoology
ISSN: 1125-0003 (Print) 1748-5851 (Online) Journal homepage: http://www.tandfonline.com/loi/tizo20
Age and body size in four introduced populations
of the American bullfrog, Lithobates catesbeianus
(Ranidae)
G. Tessa, C. Delforno, P. Govindarajulu, N. Tissot, C. Miaud & F. Andreone
To cite this article: G. Tessa, C. Delforno, P. Govindarajulu, N. Tissot, C. Miaud & F. Andreone
(2016): Age and body size in four introduced populations of the American bullfrog, Lithobates
catesbeianus (Ranidae), Italian Journal of Zoology, DOI: 10.1080/11250003.2016.1259360
To link to this article: http://dx.doi.org/10.1080/11250003.2016.1259360
Published online: 05 Dec 2016.
Submit your article to this journal
View related articles
View Crossmark data

Age and body size in four introduced populations of the American
bullfrog, Lithobates catesbeianus (Ranidae)
G. TESSA
1
*, C. DELFORNO
1
, P. GOVINDARAJULU
2
, N. TISSOT
3
, C. MIAUD
3,4
,&
F. ANDREONE
1
1
Museo Regionale di Scienze Naturali, Italy,
2
Department of Biology, University of Victoria, Canada,
3
Laboratoire d’Ecologie
Alpine, Université Savoie-Mont Blanc, France, and
4
Laboratoire d’Ecologie et Biogéographie des Vertébrés, Centre d’Ecologie
Fonctionnelle et Evolutive, France
(Received 21 September 2016; accepted 3 November 2016)
Abstract
The American bullfrog, native to the eastern half of North America including southern Quebec, is considered one of the
most invasive species in the world. It has been introduced in America, Asia and Europe, mainly for food purposes. A study
on the age and body size of this species was carried out on individuals obtained from four introduced populations (one from
Western Canada and three from France), using the skeletochronological method. Adults did not differ between sexes in
mean body size or mean age, with the exception of one population in France where males were younger than females.
Several differences in the mean age and body size were observed, with the individuals from the population in Canada
exhibiting the highest values for both sexes. The scarcity of studies in the native range prevents the comparison of introduced
versus native populations, and we focus on comparisons between introduced populations.
Keywords: Invasive species, Lithobates catesbeianus, skeletochronology, France, Canada
Introduction
Invasive alien species (IAS) are among the most impor-
tant threats to biodiversity, being one of the main causes
of species decline and extinction at the global scale
(Vitousek et al. 1997). IAS are usually the result of
accidental or deliberate introductions into natural envir-
onments where they were absent, with the subsequent
risk of acclimatisation and potentially negative conse-
quences for their new environment. Dedicated regula-
tions have been established to protect native biodiversity
and ecosystems, as well as to mitigate the impacts that
these species can have, with actions aimed at preven-
tion, detection, eradication (when possible) and man-
agement (Vitousek et al. 1997; Simberloff et al. 2013).
In any case, there is a fundamental lack of basic biolo-
gical information on many species, especially on natur-
alised populations, which are the basis for proper
conservation measures (Wilcove et al. 1998).
The American bullfrog, Lithobates catesbeianus
(Shaw, 1802), native to the United States, is
considered one of the 100 worst invasive species of
the world and is nowadays present in 32 countries
(Lowe et al. 2000). It was ascertained that this large
frog can threaten native amphibians through different
actions, among which are direct predation (Werner
et al. 1995;Jankowski&Orchard2013), habitat com-
petition (Snow & Witmer 2011), sexual interference
(Pearl et al. 2005), and transmission of pathogens
including emerging infectious diseases such as rana-
virus (Sharifian-Fard et al. 2011) and chytrid fungus
Batrachochytrium dendrobatidis (Daszak et al. 2004;
Garner et al. 2006; Jankowski & Orchard 2013;
Miaud et al. 2016). This bullfrog was introduced in
many parts of North America (including the
Hawaiian Islands) and in many other areas, such as
the Caribbean region, South America, Asia and
Europe (Ficetola et al. 2007a; Snow & Witmer
2010;Bothetal.2011; Vannini et al. 2015), mainly
with the purpose of frog farming. The actual distribu-
tion is the effect of multiple introductions from North
America, secondary translocations within European
*Correspondence: G. Tessa, Museo Regionale di Scienze Naturali, Via G. Giolitti, 36, I-10123, Torino, Italy. Tel:+39 3381948583. Fax:+39 0114325914.
Email: tessagiu@libero.it
Italian Journal of Zoology, 2016, 1–6
http://dx.doi.org/10.1080/11250003.2016.1259360
© 2016 Unione Zoologica Italiana

countries, and natural expansion. In Europe at least
25 different introductions of L. catesbeianus have been
reported, in Belgium, France, Germany, Greece,
Holland, Italy, Spain and the United Kingdom, but
acclimatised populations are nowadays confirmed
only in Belgium, France, Germany, Greece and Italy
(Ficetola et al. 2007a and references therein).
Moreover, predictions of the species’distribution evi-
denced higher risk areas that may soon be invaded
(Ficetola et al. 2007b).
Several life-history traits of L. catesbeianus have
been analysed in its habitat of origin (e.g. Durham
& Bennett 1963; Schroeder & Baskett 1968; Shirose
et al. 1993). Life-history traits in countries where it
was introduced remain largely understudied.
Govindarajulu et al. (2006) recorded tadpole and
adult growth in introduced populations in British
Coumbia, but found that the seasonal pattern and
growth rate of introduced bullfrogs were similar to
those of lower latitude native populations in
Kentucky and Missouri.
In the present note, we evaluated age and body
size of bullfrog individuals in four introduced popu-
lations (one from Western Canada, on Vancouver
Island in British Columbia (CAN), and three from
France (Gironde Gabauds –GG; Loir et Cher –LC;
Perigord Limousin –PL); see Table I). The age of
individuals was assessed using the skeletochronolo-
gical method (Castanet et al. 1993).
Materials and methods
Overall we provided data for 93 juveniles, 140 males
and 68 females of Lithobates catesbeianus. Bullfrogs
were captured with nets or traps, measured (snout-
vent length (SVL) and weight) and sexed on the
basis of the presence of the larger eardrum and the
yellowish throat in males, and sacrificed by immer-
sion in overdose of MS222 Sandoz or phenoxyetha-
nol within eradication projects. The third toe of the
hind foot was cut off and preserved in ethanol 75%
for skeletochronological analysis. Phalanges were
decalcified in 5% nitric acid for about 1 h, cross-
sectioned at 14 μm with a cryostat and stained with
Ehrlich’s haematoxylin for about 4 h. Sections were
then observed for lines of arrested growth (LAGs)
count under a light microscope by two different
researchers, and images were captured with a camera
interfaced with a personal computer. Age at sexual
maturity was estimated using the criterion of LAGs
rapprochement as proposed by Kleineberg and
Smirina (1969). Age at sexual maturity assessment
was used to discern between adults and juveniles and
to correct the life stage determination in the field.
Data on body size (SVL), longevity and age at
sexual maturity were compared between sexes and
populations with Mann–Whitney test and Kruskal–
Wallis test with Mann–Whitney pairwise post-hoc
comparison. The relation between size and age was
assessed with Spearman correlation. Age and SVL
were significantly correlated (see results) so we rea-
nalysed the effect of population, sex and their inter-
action on SVL using a non parametric two-way
analysis of covariance (ANCOVA) with age con-
trolled for as a covariate.
Results
Skeletochronology was performed successfully in all
of the analysed samples (Table II;Figure 1). From a
histological point of view, the reading of the sections
showed a wide homogeneity of the characteristics in
all populations, with LAGs clearly visible.
The presence of double and false LAGs was rare
in French populations (respectively, 4.6% and 7.0%
in GG; 10.1% and 7.2% in PL; 6.5% and 7.2% in
LC). In the French populations the first LAG is
resorbed in only 2.3% of individuals in GG, 3.4%
in PL and 1.4% in LC. Double and false LAGs and
resorption phenomena were not detected in the
Canadian population.
Taking into account adults, there were no differ-
ences in body size between males and females (GG:
z=−0.74; P = 0.45; PL: z = −1.09; P = 0.35; LC:
z=−0.56; P = 0.79; CAN: z = −0.23; P = 0.97), and
only in the LC population was the age different
between the sexes, with males turning out to be
younger than females (z = −2.20; P = 0.02), while
the other populations did not show any significant
difference (GG: z = −0.59; P = 0.73; PL: z = −0.62;
P = 0.69; CAN: z = −0.43; P = 0.66). Furthermore,
there were no differences between the sexes in the
Table I. Origin of the studied populations, with information about number of individuals (males = M, females = F and juveniles = J) and
data on capture and introduction.
Population Country Locality Number of individuals Date Introduction data
GG France Gironde Gabauts 4 M, 12 F, 17 J 2006–2007 1968
LC France Loir et Cher 82 M, 35 F, 22 J 2006–2007 2000
PL France Perigord Limousin 29 M, 12 F, 28 J 2006–2007 1990
CAN Canada Vancouver Island (British Columbia) 15 M, 9 F, 26 J 1999 1930
2G. Tessa et al.

age at sexual maturity in all of the populations (LC:
z=−1.29; P = 0.27; GG: z = −1.02; P = 0.34; PL:
z=−0.33; P = 0.80; CAN: z = −1.84; P = 0.13).
Kruskal–Wallis test (H = 42.12; df = 3; P < 0.01)
showed that populations varied in body size. PL and
LC populations have a significantly lower body size
than GG and CAN, with LC showing the lowest
values (Mann–Whitney pairwise comparisons:
P < 0.01). Populations differed also in age
(H = 23.45; df = 3; P < 0.01): in males, LC showed
again the lowest value, highly different from CAN
and GG (Mann–Whitney pairwise comparisons:
P < 0.01), while differences from PL were smaller
and marginally significant (Mann–Whitney pairwise
comparisons: P = 0.04). Females, on the contrary,
didn’t show differences (H = 2.087; df = 3;
P = 0.19). CAN shows the highest mean age values
for both sexes (Table II). Sexual maturity is reached
later in the Canadian population than in the French
ones (H = 11.336; df = 3; P < 0.01; Mann–Whitney
pairwise comparisons: P = 0.03). The correlation
between age and body size was positive in all sexes
and populations (GG: males: r = 0.77, P < 0.01,
females: r = 0.92, P < 0.01; LC: males: r = 0.75,
P < 0.001, females: r = 0.99, P < 0.01; PL: males:
r = 0.72, P < 0.01, females: r = 0.71, P = 0.02;
CAN: males: r = 0.73, P < 0.01, females: r = 0.72,
P = 0.04). Comparing the same sex between the
Table II. Structure of the studied populations with data on mean, standard deviation (SD) and range of age; age at sexual maturity; and
body size, snout-vent length (SVL).
Population Sex
SVL Age Sexual maturity
mean ± SD (range) mean ± SD (range) mean ± SD (range)
GG Juveniles (17) 68.35 ± 25.94 (30–110) 0.70 ± 0.68 (0–2) n.d.
Males (14) 147.78 ± 10.75 (127–165) 3.86 ± 0.76 (2–5) 2.35 ± 0.49 (2–3)
Females (12) 140.33 ± 26.51 (100–175) 3.66 ± 1.15 (2–5) 2.16 ± 0.38 (2–3)
PL Juveniles (28) 74.17 ± 12.06 (54–97) 2.21 ± 0.95 (0–3) n.d.
Males (29) 132.21 ± 19.65 (104–165) 3.65 ± 1.63 (2–7) 2.24 ± 0.43 (2–3)
Females (12) 124.41 ± 21.79 (89–165) 3.91 ± 1.16 (2–6) 2.16 ± 0.38 (2–3)
LC Juveniles (22) 65.85 ± 11.95 (48–80) 0.57 ± 0.5 (0–1) n.d.
Males (82) 114.20 ± 19.24 (75–165) 2.75 ± 0.89 (2–6) 2.18 ± 0.38 (2–3)
Females (35) 112.80 ± 18.73 (77–145) 3.25 ± 1.14 (2–5) 2.25 ± 0.44 (2–3)
CAN Juveniles (26) 89.30 ± 12.90 (67–114) 0.57 ± 0.5 (0–1) n.d.
Males (15) 146.00 ± 16.9 (116–172) 4.33 ± 1.34 (3–8) 2.61 ± 0.65 (2–4)
Females (9) 147.00 ± 18.5 (115–170) 4.33 ± 1.93 (3–9) 3.14 ± 0.37 (3–4)
Figure 1. Phalanx section of Lithobates catesbeianus: Adult female showing five lines of arrested growth (LAGs) (arrows).
Age in introduced American bullfrog 3

populations, we also found that males and females of
L. catesbeianus showed different size at the same age
depending on the populations (non-parametric
ANCOVA: males, F = 11.17; df = 3; P < 0.01;
females, F = 25.88; df = 3; P < 0.01).
Discussion
The life-history traits of organisms which are intro-
duced outside their native range can diverge from
those of native populations, due to release from e.g.
predators, competitors and parasites. The differ-
ences can also result from pre-existing differences
in the native source populations, and during accli-
matisation by genetic drift and local adaptation
(Ficetola et al. 2008). For example, at least six inde-
pendent bullfrog introductions from the native range
occurred in Europe, with displaced individuals ori-
ginating from different part of the North America
native range (Ficetola et al. 2008). Life-history trait
comparisons between introduced and native popula-
tions allow testing predictions such as larger body
size in introduced populations (Govindarajulu et al.
2006). Due to large inter-individual variability in
growth trajectories, the knowledge of age is essential
for body size comparison: a mean larger size in one
population may only result from a mean higher age
(i.e. greater opportunity for growth). Unfortunately,
age structure estimation (established with skeleto-
chronology) in native populations is scarce: Spear
et al. (2009) provided this information in six popula-
tions investigated in the same region (Yamaska drai-
nage basin in South Quebec). We limit this
discussion to the expression of differences among
introduced populations.
Individuals of the four introduced populations ori-
ginated from sites with temperate climatic environ-
ment (Vancouver Island for the Canada population,
sites in Centre and South-west France for the France
populations; see Table I). The climate seasonality of
these regions favours the formation of LAGs during
the latency period, i.e. winter. Populations from
France and Canada showed a quite homogeneous
age structure of the individuals, with an abundant
presence of juveniles, and a high percentage of
males, due to their intense activity during the breed-
ing season, the period when they were collected.
The studied populations did not show a significant
sexual dimorphism in size or a difference in sexual
maturity, as observed in native populations (Shirose
et al. 1993). Males have a very aggressive territorial
behaviour that favours selection for larger size (Shine
1979). Females are known to invest energy resources
into body growth, permitting a higher number of
eggs and thus increasing fecundity (Woolbright
1983). The lack of sexual dimorphism in the studied
populations could result from these independent
selective forces.
Life-history trait differences among introduced
populations can result from several non exclusive
causes, such as: (1) the introduced individuals can
originate from geographically distinct sites in the
native range, exhibiting life-history trait variation.
Variation in age and size along environmental gradi-
ents is very well documented in amphibians, with
e.g. larger body size and delayed age at maturity in
high latitudes and altitudes (Miaud et al. 1999;
Miaud & Guillaume 2005); (2) the environmental
conditions at the introduction sites can vary (e.g.
longer activity period, higher productivity, etc.)
allowing the expression of wide phenotypic plasticity
in life-history traits; (3) bullfrogs in introduced sites
are exposed to selective forces shaping life-history
traits (e.g. local adaptation), leading to specific life-
history trait characteristcs through the process of
naturalisation. The four populations slightly differ
in body size and age. The Canadian population
shows the highest mean values of body size and age
(other than sexual maturity). The introduced
Gironde (France) population originated from the
western part of the bullfrog native range (Ficetola
et al. 2008), and the Perigord Limousin introduced
population results from a secondary translocation of
individuals from successfully established populations
in Gironde. On the other hand, the origin of the
Vancouver Island and Loir et Cher introduced popu-
lations are unknown. It is thus not yet possible to
assign observed inter-populational differences to dif-
ferences in native populations. The mean highest
body size and age observed in the Vancouver Island
population could result from harsher climatic condi-
tions: bullfrogs emerged from hibernation in late
April and early May on Vancouver Island
(Govindarajulu et al. 2006), while this occurred in
March–April in France. A longer activity period can
lead to smaller body size, and younger age (mean
and at maturity) in anurans (Cvetkovićet al. 2008).
Finally, the populations also vary in their introduc-
tion history: bullfrogs were introduced since the
1930s in British Columbia, i.e. 40 years before the
earliest introduction in France (Table II). Taking
into account a generation time of 6 years (Ficetola
et al. 2008), the number of generations since intro-
duction is thus about 12 in the Canadian population
and six in the Gironde population. How the
observed life-history trait differences result in evolu-
tionary processes such as local adaptation remains to
be tested.
The risks and effects associated with such intro-
ductions are significant, especially for species with
4G. Tessa et al.

high potential expansion that increases their distribu-
tion range: introducted in 1968 at one site, fewer
than six females were able to generate a population
reaching about 1800 km
2
in the year 2000 (Ficetola
et al. 2008). However, preventive plans for the con-
trol of bullfrogs coordinated at the scale of e.g.
Europe do not currently exist. Several management
plans have been proposed and implemented in
France, the United Kingdom and Belgium, but the
current lack of basic biological information to under-
stand the success or failure of introduction limits the
definition of testable managing actions.
Acknowledgements
The authors thank the Alpine Ecology Laboratory of
the University of Savoy Mont Blanc (France), for
help in sample preparation and in analysing the stu-
died samples. We would also like to thank the people
involved in sample collection and especially Bradley
Anholt for the British Columbia (Canada) popula-
tion, and Christophe Coïc and Mathieu Berroneau
(Gironde), Dominique Beguin and Gabriel Michelin
(Loir et Cher) for the France populations. The study
was conducted during the master’s thesis of CD.
The samples were collected under a Wildlife Act
Permit from British Columbia Ministry of
Environment and French Ministry of Environment
(DREAL Loir et Cher, Gironde, and Dordogne)
with Animal Care Committee approval of the
University of Victoria ad of the University of
Savoie. We would like to thank G.F. Ficetola and
the anonymous referee for their helpful comments.
References
Both C, Lingnau R, Santos-Jr A, Madalozzo B, Lima LP, Grant
T. 2011. Widespread occurrence of the American bullfrog,
Lithobates catesbeianus (Shaw, 1802) (Anura: Ranidae), in
Brazil. South American Journal of Herpetology 6:127–134.
DOI: 10.2994/057.006.0203.
Castanet J, Francillon-Vieillot H, Meunier FJ, De Riqles A. 1993.
Bone and individual aging. In: Hall BK, editor. Bone: Bone
growth. Boca Raton, FL: CRC Press. pp. 245–283.
CvetkovićD, Tomasevic N, Ficetola GF, Crnobrnja-IsailovićJ,
Miaud C. 2008. Bergmann’s rule in amphibians: Combining
demographic and ecological parameters to explain body size
variation among populations in the common toad Bufo bufo.
Journal of Zoological Systematics and Evolutionary Reasearch
47:171–180. DOI: 10.1111/j.1439-0469.2008.00504.x.
Daszak P, Strieby A, Cunningham AA, Longcare JE, Brown CC,
Porter D. 2004. Experimental evidence that the bullfrog (Rana
catesbeiana) is a potential carrier of chytridiomycosis, an emer-
ging fungal disease of amphibians. The Herpetological Jounal
14:201–207.
Durham L, Bennett GW. 1963. Age, growth, and homing in the
bullfrog. The Journal of Wildlife Management 27:107–123.
DOI: 10.2307/3797785.
Ficetola GF, Bonin A, Miaud C. 2008. Population genetics
reveals origin and number of founders in a biological invasion.
Molecular Ecology 17:773–782. DOI: 10.1111/j.1365-
294X.2007.03622.x.
Ficetola GF, Coic C, Detaint M, Berroneau M, Lorvelec O,
Miaud C. 2007a. Pattern of distribution of the American bull-
frog Rana catesbeiana in Europe. Biological Invasions 9:767–
772. DOI: 10.1007/s10530-006-9080-y.
Ficetola GF, Thuiller W, Miaud C. 2007b. Prediction and valida-
tion of the potential global distribution of a problematic alien
invasive species the American bullfrog. Diversity and
Distributions 13:476–485. DOI: 10.1111/j.1472-
4642.2007.00377.x.
Garner TWJ, Perkins MW, Govindarajulu P, Seglie D, Walker S,
Cunningham AA, Fisher MC. 2006. The emerging amphibian
pathogen Batrachochytrium dendrobatidis globally infects intro-
duced populations of the North American bullfrog, Rana cates-
beiana. Biology Letters 2:455–459. DOI: 10.1098/
rsbl.2006.0494.
Govindarajulu P, Price WMS, Anholt BR. 2006. Introduced
Bullfrogs (Rana catesbeiana) in Western Canada: Has their
ecology diverged? Journal of Herpetology 40:249–260. DOI:
10.1670/68-05A.1.
Jankowski K, Orchard SA. 2013. Stomach contents from invasive
American Bullfrogs Rana catebeiana (= Lithobates catesbeianus)
on southern Vancouver Island, British Columbia, Canada.
NeoBiota 16:17–27. DOI: 10.3897/neobiota.16.3806.
Kleineberg SE, Smirina EM. 1969. A contribution to the method
of age determination in amphibians. Zoologicheskiy Zhurnal
48:1090–1094.
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. Aliens 12:1–12.
Miaud C, Dejean T, Savard K, Millery A, Valentini A, Garner
TWJ. 2016. Invasive North American bullfrogs transmit lethal
fungus Batrachochytrium dendrobatidis infections to native
amphibian host species. Biological Invasions. In press. DOI:
10.1007/s10530-016-1161-y.
Miaud C, Guillaume O. 2005. Variation in age, body size and
growth among surface and cave-dwelling populations of the
Pyrenean Newt, Euproctus asper (Amphibia; Urodela).
Herpetologica 61:241–249. DOI: 10.1655/04-29.1.
Miaud C, Guyétant R, Elmberg J. 1999. Variations in life-history
traits in the common frog Rana temporaria (Amphibia, Anura):
A literature review and new data from the French Alps. Journal
of Zoology 249:61–73. DOI: 10.1111/j.1469-7998.1999.
tb01060.x.
Pearl CA, Hayes MP, Haycock R, Engler JD, Bowerman J. 2005.
Observations of interspecific amplexus between Western North
American Ranid frogs and the introduced American Bullfrog
(Rana catesbeiana) and an hypothesis concerning breeding
interference. The American Midland Naturalist 154:126–134.
DOI: 10.1674/0003-0031(2005)154[0126:OOIABW]2.0.
CO;2.
Schroeder EE, Baskett TS. 1968. Age estimation, growth rates,
and population structure in Missouri bullfrogs. Copeia
1968:583–592. DOI: 10.2307/1442029.
Sharifian-Fard M, Pasmans F, Adriaensen C, Devisscher S,
Adriaens T, Louette G, Martel A. 2011. Ranavirosis in inva-
sive Bullfrogs, Belgium. Emerging Infectious Diseases
17:2371–2372. DOI: 10.3201/eid1712.110236.
Shine R. 1979. Sexual selection and sexual dimorphism in the
amphibia. Copeia 1979:297–306. DOI: 10.2307/1443418.
Shirose L, Brooks RJ, Barta JR, Desser SS. 1993. Intersexual
differences in growth, mortality and size at maturity in
Age in introduced American bullfrog 5

bullfrogs (Rana catesbeiana). Canadian Journal of Zoology
71:2363–2369. DOI: 10.1139/z93-332.
Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson
J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pyšek P,
Sousa R, Tabacchi E, Vilà M. 2013. Impacts of biological inva-
sions - what’s what and the way forward. Trends in Ecology and
Evolution 28:58–66. DOI: 10.1016/j.tree.2012.07.013.
Snow NP, Witmer G. 2010. American Bullfrogs as invasive spe-
cies: A review of the introduction, subsequent problems, man-
agement options, and future directions. Proceedings of the
Vertebrate Pest Conference 24:86–89.
Snow NP, Witmer GW. 2011.Afield evaluation of a trap for
invasive American bullfrogs. Pacific Conservation Biology
17:285–291.
Spear PA, Boily MB, Giroux I, DeBlois C, Leclair MH, Levasseur
M, Leclair R. 2009. Study design, water quality, morphometrics
and age of the bullfrog, Rana catesbeiana,insubwatershedsof
the Yamaska River drainage basin, Québec, Canada. Aquatic
Toxicology 91:110–117. DOI: 10.1016/j.aquatox.2008.09.011.
Vannini A, Bruni G, Cantini M, Tricarico E, Inghilesi AF. 2015.
Updating the distribution of the American bullfrog Lithobates
catesbeianus (Anura: Ranidae) in Tuscany (Central Italy), with a
note on predatory interactions with red swamp crayfish
Procambarus clarkii (Decapoda: Cambaridae). Italian Journal of
Zoology 82:416–424. DOI: 10.1080/11250003.2015.1020348.
Vitousek PM, D’Antonio CM, Loope LL, Rejmánek M, Westbrooks
R. 1997. Introduced species: A significant component of human
caused global change. New Zealand Journal of Ecology 21:116.
Werner EE, Wellborn GA, McPeek MA. 1995. Diet composition
in postmetamorphic bullfrogs and green frogs: Implications for
interspecific predation and competition. Journal of
Herpetology 29:600–607. DOI: 10.2307/1564744.
Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E. 1998.
Quantifying threats to imperiled species in the United States.
BioScience 48:607–615. DOI: 10.2307/1313420.
Woolbright LL. 1983. Sexual selection and size dimorphism in
anuran amphibia. The American Naturalist 121:110–119.
DOI: 10.1086/284042.
6G. Tessa et al.