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

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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.
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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
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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 dEcologie
Alpine, Université Savoie-Mont Blanc, France, and
4
Laboratoire dEcologie et Biogéographie des Vertébrés, Centre dEcologie
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 (Sharian-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, 16
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 conrmed
only in Belgium, France, Germany, Greece and Italy
(Ficetola et al. 2007a and references therein).
Moreover, predictions of the speciesdistribution 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 sacriced 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
decalcied in 5% nitric acid for about 1 h, cross-
sectioned at 14 μm with a cryostat and stained with
Ehrlichs 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 eld.
Data on body size (SVL), longevity and age at
sexual maturity were compared between sexes and
populations with MannWhitney test and Kruskal
Wallis test with MannWhitney pairwise post-hoc
comparison. The relation between size and age was
assessed with Spearman correlation. Age and SVL
were signicantly 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 rst 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 signicant
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 20062007 1968
LC France Loir et Cher 82 M, 35 F, 22 J 20062007 2000
PL France Perigord Limousin 29 M, 12 F, 28 J 20062007 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).
KruskalWallis test (H = 42.12; df = 3; P < 0.01)
showed that populations varied in body size. PL and
LC populations have a signicantly lower body size
than GG and CAN, with LC showing the lowest
values (MannWhitney 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 (MannWhitney pairwise comparisons:
P < 0.01), while differences from PL were smaller
and marginally signicant (MannWhitney pairwise
comparisons: P = 0.04). Females, on the contrary,
didnt 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; MannWhitney
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 (30110) 0.70 ± 0.68 (02) n.d.
Males (14) 147.78 ± 10.75 (127165) 3.86 ± 0.76 (25) 2.35 ± 0.49 (23)
Females (12) 140.33 ± 26.51 (100175) 3.66 ± 1.15 (25) 2.16 ± 0.38 (23)
PL Juveniles (28) 74.17 ± 12.06 (5497) 2.21 ± 0.95 (03) n.d.
Males (29) 132.21 ± 19.65 (104165) 3.65 ± 1.63 (27) 2.24 ± 0.43 (23)
Females (12) 124.41 ± 21.79 (89165) 3.91 ± 1.16 (26) 2.16 ± 0.38 (23)
LC Juveniles (22) 65.85 ± 11.95 (4880) 0.57 ± 0.5 (01) n.d.
Males (82) 114.20 ± 19.24 (75165) 2.75 ± 0.89 (26) 2.18 ± 0.38 (23)
Females (35) 112.80 ± 18.73 (77145) 3.25 ± 1.14 (25) 2.25 ± 0.44 (23)
CAN Juveniles (26) 89.30 ± 12.90 (67114) 0.57 ± 0.5 (01) n.d.
Males (15) 146.00 ± 16.9 (116172) 4.33 ± 1.34 (38) 2.61 ± 0.65 (24)
Females (9) 147.00 ± 18.5 (115170) 4.33 ± 1.93 (39) 3.14 ± 0.37 (34)
Figure 1. Phalanx section of Lithobates catesbeianus: Adult female showing ve 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 signicant
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 specic 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
MarchApril 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 signicant, 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
denition 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 masters 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.
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... 22,23 Gonadal maturation in female bullfrogs begins at one year of age, but do not reach full maturity until year two. 24 This could explain the lack of differences in weight and body condition between male and female juvenile bullfrogs. Also, juvenile amphibians use nutrients mainly for body growth, and a redistribution of these resources towards the gonads occur as they mature sexually to favor reproduction. ...
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