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Asian Herpetological Research 2015, 6(1): 34–44
DOI: 10.16373/j.cnki.ahr.140044
1. Introduction
Biological invasion is a major cause of biotic homo
-
genization, which is often mentioned as the process of
the replacement of native species by widespread exotic
species (Olden and Rooney, 2006). Amphibians stand
out among the casualties of such homogenization and
are now considered the most threatened vertebrate
Diet and Prey Selection of the Invasive American Bullfrog
(Lithobates catesbeianus) in Southwestern China
Xuan LIU
1
, Yu LUO
2
, Jiaxin CHEN
3
, Yisong GUO
4
, Changming BAI
1
,
5
and Yiming LI
1*
*
Corresponding author: Prof. Yiming LI, from Institute of Zoology,
Chinese Academy of Sciences, Beijing, China, with his research
focusing on conservation biology and ecology of amphibians, and
macroecology of vertebrates.
E-mail: liym@ioz.ac.cn
Received: 12 August 2014 Accepted: 7 December 2014
Abstract Invasive predators have been widely regarded as one of the principle drivers of the global decline of
amphibians, which are among the most threatened vertebrate taxon on Earth. The American bullfrog (Lithobates
catesbeianus) is identied as one of the most successful vertebrate invaders and has caused the decline or extinction of
some native amphibians in many regions and countries including China. Based on eld surveys and stomach content
analyses, we examined the diet composition of the invasive bullfrog for the rst time in two invaded populations in
Yunnan Province, southwestern China, a region of global conservation priority, during the breeding season from 2008
to 2014. Additionally, we conducted the first quantitative study on the prey selection of this global invader among
their invaded ranges after controlling for the local anuran assemblage and other aquatic preys in the environment. Our
results showed that the range of food items in the stomachs of bullfrogs spanned more than 30 species belonging to ten
taxonomic classes. Both of post-metamorphosis individuals and juveniles preyed upon native frogs, independent of the
bullfrog’s body size and mouth width. Importantly, Jacobs’ selection index showed a bullfrog preference for the Yunnan
pond frog (Babina pleuraden), one native endemic anuran with population decline, in terms of both food volume and
occurrence. We therefore provided direct evidence on the predation impact of the invasive bullfrog on an endemic
anuran and urged further efforts to prevent the dispersal of this invader into more fragile habitats to reduce their negative
impacts on native amphibians.
group on the planet (Stuart et al., 2004), and invasive
predators are widely known as a pernicious driver of
global amphibian decline (Kats and Ferrer, 2003). Among
them, the American bullfrog (Lithobates catesbeianus;
hereafter referred to as the bullfrog) has long been
of conservation concern due to its wide non-native
distribution over 50 countries and regions (Ficetola
et al., 2007; Kraus, 2009), rapid adaptability to novel
environments (Li et al., 2014; Liu et al., 2010), rapid
population growth rate (Govindarajulu et al., 2005), and
high range of expansion (Austin et al., 2003; Liu et al.,
2014). The bullfrog is also an important vector of the
chytrid fungus (Batrachochytrium dendrobatidis), an
Keywords Amphibian decline, American bullfrog, diet preferences, invasive species, Babina pleuraden, predation
1
Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences,
1 Beichen West Road, Chaoyang District, Beijing 100101, China
2
School of Life Science, Guizhou Normal University, Guiyang 550001, China
3
School of Life Science, South China Normal University, Guangzhou 510631, China
4
Department of Ecology, Chemistry and Environmental Engineering, Yunyang Teachers’ College, Danjiangkou 442000,
China
5
Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, Yellow Sea Fisheries
Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266071, China
ORIGINAL ARTICLE
Xuan LIU et al. Diet Preference of Invasive BullfrogsNo. 1 35
emerging disease implicated in the global amphibians
decline (Garner et al., 2006; Liu et al., 2013b). Except
for the disease transmission, this species can have direct
negative effects on native fauna through competition
(Kiesecker et al., 2001; Kupferberg, 1997), breeding
interference (D’Amore et al., 2006; Pearl et al., 2005),
but most commonly its unspecialized predation on natives
(Jancowski and Orchard, 2013). Many efforts have
been made to explore the bullfrog predation on native
communities around the world, with results showing that
bullfrogs can predate a large number of prey species,
including insects, crustaceans, and large vertebrates such
as fishes, birds, reptiles, and amphibians (e.g., Hirai,
2004; Hothem et al., 2009; Krupa, 2002; Lopez-Flores
and Vilella, 2003; Silva et al., 2011; Werner et al., 1995;
Wu et al., 2005). However, these studies mainly focused
on diet compositions through analyses on stomach
contents, or examined prey selection of bullfrogs only
on native anuran assemblage (Boelter et al., 2012; Pearl
et al., 2004; Wang et al., 2005), and to the best of our
knowledge, their predation preferences after controlling
for the environmental anuran and other aquatic prey
availability are unfortunately unknown. Indeed,
quantifying the predation preference of introduced
bullfrogs is important for estimating their predatory
impacts on native amphibians and for understanding
the mechanism of native biotic homogenization by this
invader.
The bullfrog was first introduced into China for
aquaculture in the 1960s, and it then expanded across
the country in the 1980s (Liu et al., 2010). Currently, the
bullfrog has successfully established feral populations
in many provinces from eastern to western China (Li
and Xie, 2004; Li et al., 2006; Liu and Li, 2009). In the
Zhoushan Archipelago of China, the density of post-
metamorphosis bullfrogs showed a negative relationship
with the native frog density and species richness (Li et al.,
2011). The bullfrog has also successfully invaded the
southwestern China Plateau (Liu and Li, 2009; Liu et al.,
2013a; Liu et al., 2012), an area that is a global
biodiversity conservation hotspot (Myers et al., 2000)
and is among the areas with the largest number of
endemic amphibian species in China (Xie et al., 2007).
However, direct evidence for bullfrog predation on
endemic amphibians is still lacking. The bullfrog also
exhibits geographical variations in body size and sexual
size dimorphism in response to different elevations (Liu
et al., 2010), thus providing opportunities to investigate
geographical variations in their diet habits and to evaluate
differences in their predation impacts on native fauna.
There are three main objectives in the present study: (1)
to describe the bullfrog diet composition in two invaded
communities in Yunnan Province, southwestern China;
(2) to investigate variations in the bullfrog diet among
individuals of different body size, sex, and populations;
and (3) to explore the bullfrog’s feeding preference on
native aquatic communities and to evaluate the degree of
the predation impact on endemic amphibians.
2. Materials and Methods
2.1 Study area Our study was conducted in Yunnan
Province situated in the plateau region of southwestern
China, where there is a complex climate including
tropical, subtropical, temperate, and boreal climates
(Yang et al., 1991). We focused on intensive samplings at
two sites, one with a low altitude (Shiping at an elevation
of 1500 m, 23°42' N 102°28' E) and one with a high
altitude (Caohai, Lugu Lake at an elevation of 2,692 m,
27°42' N 100°51' E), on the border between Ninglang
County of Yunnan Province and Yanyuan County of
Sichuan Province (Figure 1). The bullfrog has established
feral populations in these two sites, which descended
from a single source population introduced from Cuba in
the 1980s (Liu et al., 2010). The Shiping site is located at
Yilong Lake, which is a large freshwater lake in Yunnan
Province. Caohai is a grassy plateau wetland that is part
of Lugu Lake, the largest lake in Yunnan Province, a
natural lake in the Hengduan Mountain System and set in
the subalpine zone in the southern Hengduan Mountains
as a pine-covered eco-region. Except for the bullfrog,
historical literatures also recorded the distribution of
Figure 1 Map of the study area showing the bullfrog sampling sites
in Yunnan province, southwestern China (A: Caohai Population, B:
Shiping Population).
Asian Herpetological Research
Vol. 636
several other native amphibian species including the
Yunnan Pond Frog (Babina pleuraden), the Large-
webbed Bell Toad (Bombina maxima), the Yunnan
Odorous Frog (Odorrana andersonii) and the Vocal-
Sacless Spiny Frog (Paa liui) in the study area (Fei et
al., 1999; Yang et al., 1991). However, we did not detect
the occurrence of O. andersonii and P. liui but only B.
pleuraden and B. maxima during our field surveys in
recent years (Liu and Li, 2009; Liu et al., 2013a; Liu
et al., 2012).
2.2 Bullfrog diet habits We sampled both adult and
juvenile bullfrogs during the breeding season from the
year 2008 to 2014 by hand, dip-netting, and electroshing
with the aid of an electronic torch at night (19:00–23:00).
The bullfrogs were captured along line transects that were
2 m wide (with 1 m in the water and the other half on the
bank) and 20 m long along the accessible shorelines. All
captured frogs were taken indoors for further analysis.
We measured snout to vent length (SVL; to the nearest
0.02 mm) and mouth width with a vernier caliper and
body mass (to the nearest 0.1 g) with an electronic
balance of each live specimens. We identified the sex
and ontogenetic stage of each specimen according to
the development of secondary sexual characters. Males
were identied based on the presence of nuptial pads and
yellow pigments on the throat and chest. Frogs lacking
male characteristics were classied as females and those
with SVL lower than the minimum size of male bullfrog
were considered as juveniles (Wang et al., 2007; Wu
et al., 2005). We performed a ventral incision on the
alimentary canal of each anaesthetized specimen with
ethyl acetate, and the stomach contents were immediately
removed to a Petri dish and preserved in 70% alcohol
(Jancowski and Orchard, 2013; Leivas et al., 2012; Silva
et al., 2011). The contents of each stomach were identied
to the lowest possible taxon (usually family) with the
aid of a magnier (8 ×), and the length and width (to the
nearest 0.02 mm) and body mass (to the nearest 0.1 g) of
each prey item were measured.
2.3 Prey selection To quantify the feeding preference
of the bullfrog on native amphibians, we studied bullfrog
prey selection focused on aquatic vertebrates including
amphibians and fishes in the Caohai population. These
prey types were studied because they comprised the
major aquatic vertebrate prey based on our stomach
content analyses in Caohai (Table 1). In the case of native
anurans, we included the B. pleuraden and the B. maxima,
which were the two dominant amphibian endemic species
in Caohai based on the field survey (Liu and Li, 2009).
We treated tadpoles and juveniles together for the data
analyses. For fishes, we focused on the Cypriniformes
species that appeared in the bullfrog diet. The Caohai
population was chosen for the prey selection study
because the aquatic habitat at this site was accessible
to the investigators, and thus tadpoles, fishes, frogs
and toads could be collected by nets and electrofishing.
The frogs and toads were sampled along a total of 11
line transects where the bullfrogs were captured. Fish
and tadpole sampling was conducted using nets located
parallel to the land transects, and the sampling of each
individual per amphibians and freshwater species was
conducted simultaneously by two researchers during
1 hour (Blanco-Garrido et al., 2008). The availability/
abundance of each prey species was calculated by both
the number (individuals/m) and biomass (g/m), and
then we calculated the proportion of each prey species
in the environment for further Jacobs’ selection index
estimation.
2.4 Data analyses We quantied the prey composition
of each stomach by estimating the number of prey
individuals, the composition of prey species, prey
biomass, and prey volume which was approximated
as an ellipsoid using the formula: Volume =
4/3π(length/2)×(Width/2)
2
(Magnusson et al., 2003).
Those accidental fragments of plants and minerals were
not included in the further data analyses. We determined
the relative frequency of the number of individuals,
biomass and volume of each prey category in the total
stomach content of bullfrogs. Considering that there
was a strong positive correlation between the body size
and mouth width of the bullfrog (Pearson correlation r
= 0.937, P < 0.001), we performed Pearson correlation
analyses and only reported the results involving number
of prey individuals, biomass, volume and body size of
the bullfrogs (ln-transformed). We conducted Kruskal-
Wallis test to explore the difference in prey composition
among males, females and juveniles. We used ANCOVA
to evaluate variations in prey composition, biomass and
volume between two populations after controlling for the
effects of bullfrog body size which might influence the
results.
To quantify the bullfrogs’ feeding preference or
avoidance, we used Jacobs’ selection index, calculated
as: D = (r – p)/(r + p – 2rp); where r is the proportion
of a prey category in the diet and p is the proportion of
the prey category in the environment (Hayward et al.,
2006; Jacobs, 1974). The index has a range from –1 to
+1, with –1 being maximum avoidance, 0 indicating
random selection and +1 indicating maximum preference.
Xuan LIU et al. Diet Preference of Invasive BullfrogsNo. 1 37
We used this selection index because it was suggested
independently of prey sizes and the relative abundances
of prey items in the environment (Jacobs, 1974).
The Jacobs’ index was calculated both at the level of
individuals and biomass for each prey category in each of
the 11 sampling transects. We firstly examined whether
bullfrogs predated each prey category randomly against
the null hypothesis of a mean Jacobs’ index equal to
zero using t-tests. We then explored difference in mean
Jacobs’ indexes among prey species using Kruskal-Wallis
test, and performed Mann-Whitney U tests for multiple
comparisons. All analyses were performed in R (Version
2.15.1, R Development Core Team, 2012).
3. Results
3.1 Diet compositions of bullfrogs A total of 214
bullfrogs (Shiping: n = 101
;
40 males, 37 females, 24
juveniles; Caohai: n = 113; 47 males, 45 females, 21
juveniles) were sampled, and a proportion of 18.2%
(39 individuals) were found with empty stomachs.
We recovered 34 prey items in the two populations
with 27 prey items found in the Shiping population
and 16 prey items in the Caohai population. When
combining all insect items together, the stomach
content analysis showed that insects were the most
commonly observed food (proportion of occurrence:
Prey categories % SV % Ocu % Bio
Population
a
Sex
b
Shiping Caohai ♀ ♂ Juveniles
Invertebrates
Arachnoida
Araneida 0.73 3.78 1.61 1.52 — 0.41 0.14 6.13
Clitellata
Haplotaxida
Haplotaxidae 0.09 0.31 0.08 — 0.17 — 0.22 —
Crustacea
Decapoda
Cambaridae 15.95 3.14 7.54 33.42 — 19.60 14.19 0.21
Palaemonidae 4.97 11.01 6.70 10.41 — 1.05 9.35 8.75
Potamidae 7.85 3.14 9.94 16.46 — 10.29 6.17 —
sp. 0.27 0.63 0.20 0.58 — — 0.20 2.60
Isopoda
Armadillidiidae 0.09 0.63 0.10 0.06 0.11 — 0.07 0.76
Gastropoda
Mesogastropoda
Viviparidae 3.80 6.29 4.03 — 7.27 5.25 2.29 1.83
Gastropoda
Stylommatophore
Bradybaenidae 2.84 8.49 3.07 6.00 — 0.93 2.93 15.76
Insecta
Blattodea
Blattidae 0.13 0.31 0.12 0.27 — — 0.32 —
sp. 0.08 0.63 0.10 0.16 — — — 1.02
Coleoptera
Carabidae 0.01 0.63 0.02 0.03 — — 0.04 —
Cerambycidae 0.67 2.20 0.65 0.91 0.44 0.86 0.54 —
Table 1 Bullfrog diet described as relative frequency of occurrence (% Ocu), percentage of biomass (% Bio) and volume (% SV) in two
invaded populations in Yunnan province, southwestern China.
Asian Herpetological Research
Vol. 638
Prey categories % SV % Ocu % Bio
Population
a
Sex
b
Shiping Caohai ♀ ♂ Juveniles
Coccinellidae 0.01 0.31 0.005 — 0.02 0.02 — —
Scarabeidae 0.86 0.31 2.47 1.81 — 0.64 — 7.05
sp. 2.61 7.23 1.82 2.53 2.68 2.88 2.54 1.15
Diptera
Muscidae 0.12 1.57 0.14 — 0.23 — 0.04 1.43
sp. 0.13 0.94 0.12 0.08 0.19 — 0.34 —
Hemiptera
Belostomatidae 5.34 11.01 3.52 5.42 5.35 2.29 3.59 14.80
sp. 0.14 0.94 0.21 0.29 — 0.25 0.01 0.04
Homoptera
Cicadellidae 0.31 0.31 0.33 0.64 — — 0.76 —
Hymenoptera
sp. 0.15 1.57 0.08 — 0.28 0.04 0.31 —
Lepidoptera
Pieridae 0.08 0.31 0.16 0.17 — 0.16 — —
Odonata
sp. 0.86 1.89 1.21 — 1.64 0.38 1.63 —
Orthoptera
Gryllidae 0.63 4.09 0.93 0.80 0.47 0.16 1.07 1.51
Gryllotalpidae 0.19 0.63 0.43 0.39 — 0.36 — —
Lamellibranchia
Unionoida
Unionidae 0.03 0.31 0.06 0.06 — — 0.07 —
Unidentied 0.65 1.57 0.41 0.47 0.81 1.68 2.36 5.67
Larvas 1.69 0.94 0.93 3.54 — 0.60 3.42 —
Vertebrate
Pisces
Cypriniformes 11.49 12.58 9.4 9.42 12.89 9.74 13.35 13.78
Reptilia
Squamata
Colubridae (Dinodon rufozonatum) 0.16 0.31 2.77 0.33 — 0.30 — —
Amphibia
Anura
Ranidae
Babina pleuraden 16.14 6.60 20.18 — 30.90 13.18 21.12 10.42
Lithobates catesbeianus 19.99 3.14 19.78 2.02 36.42 28.52 12.69 —
sp. 0.59 0.94 0.50 1.24 — 0.08 — 7.10
Unidentied at the Class level 0.28 1.26 0.36 0.96 0.12 0.35 0.25 —
sp. indicates the unidentied species at the possible lowest level within the taxon;
a: diet volumetric percentage for two bullfrogs sampling population, respectively;
b: diet volumetric percentage for two sex and juveniles, respectively.
(Continued Table 1)
Xuan LIU et al. Diet Preference of Invasive BullfrogsNo. 1 39
37.4%), with the highest prey species diversity (19
species) (Table 1). The other relatively frequent
categories included Cypriniformes fishes (12.6%),
Palaemonidae crustaceans (11.0%), and Ranidae
(10.7%) (Table 1). Cannibalism of bullfrogs (juveniles
and tadpoles) and B. pleuraden made up approximately
19.9% and 16.1% in terms of volume, respectively,
followed by Cambaridae (crayfish; Procambarus
clarkii) (15.9%). In terms of biomass, B. pleuraden and
bullfrog cannibalism represented 20.2% and 19.8%,
respectively, followed by Potamidae crabs (9.9%) and
Cypriniformes fishes (9.4%) (Table 1). Other prey
categories had relatively minor importance (Table 1).
3.2 Comparison among different bullfrog groups
(adult males, females and juveniles) Although there
was a weak positive relationship between bullfrog body
size and prey biomass (Pearson correlation coefficient
r = 0.188, P = 0.045) (Figure 2), we did not find
significant relationships between bullfrog body size
and prey volume (r = 0.093, P = 0.325), number of
prey individuals (r = –0.054, P = 0.564), or number of
prey species (r = 0.000, P = 0.998). The bullfrogs that
consumed native frogs and those that did not use native
frogs as prey did not differ in body size (Mann-Whitney
U-test, z = –1.117, P = 0.264), weight (z = –1.469, P =
0.142), or mouth width (z = –1.284, P = 0.199). Finally,
there was no difference in prey biomass (Kruskal-Wallis
test, χ
2
= 4.57, d.f. = 2, P = 0.102), volume (χ
2
= 5.58, d.f.
= 2, P = 0.061), number of prey individuals (χ
2
= 3.82,
d.f. = 2, P = 0.148), or number of prey species (χ
2
= 3.20,
d.f. = 2, P = 0.202) among males, females, and juveniles.
However, there were differences in diet composition
among the bullfrog groups (Table 1). Although insects
were the most frequent prey for females (37.4%), males
(38.2%), and juveniles (42.0%), the adult bullfrogs
consumed a large proportion of vertebrates, especially
amphibians; Ranidae were the second most frequent
(18.7%) and most abundant prey in terms of volume
(41.8%) and biomass (44.9%) for female bullfrogs.
Within Ranidae, B. pleuraden (10.9%) was predated
more than bullfrog cannibalism (7.7%) by females, but
bullfrog cannibalism represented a higher proportion with
regard to biomass (27.2%) and volume (28.5%) than that
of B. pleuraden (17.8% for biomass, 13.2% for volume).
Ranidae also accounted for a large proportion of the food
biomass (36.5%) and volume (33.8%) of males, followed
by crustaceans (occurrence: 17.3%, volume: 30.0%,
biomass: 29.7%) and shes (occurrence: 13.9%, volume:
13.3%, biomass: 11.2%). In contrast to the females, the
males predated more frequently on B. pleuraden (6.9%),
with a greater biomass (23.6%) and volume (21.1%)
than those of bullfrog cannibalism (1.7% for occurrence,
12.9% for biomass, and 12.7% for volume). Following
insects, the major diet category for juvenile bullfrogs
was snail (occurrence: 38.0%, volume: 17.6%, biomass:
23.9%). We also detected other vertebrate prey including
one Cypriniformes fish, one B. pleuraden, and another
unidentied frog in the stomachs of juveniles.
3.3 Variations between two populations There were
variations in the bullfrog prey compositions between
two populations. Overall, ten items were shared by
both frog populations, whereas only six items appeared
exclusively in the Caohai population and only 18 items
occurred exclusively in the Shiping population (Table 1).
For the Shiping population, the craysh P. clarkii was a
very frequent food, accounting for more than 30% of the
total volume and more than 25% of the total biomass.
Palaemonidae crustaceans were another dominant food,
with more than 20% of the individual occurrences. We
recorded one red-banded snake (Dinodon rufozonatum)
in the stomach of a female bullfrog in Shiping, but the
bullfrogs there rarely predated on amphibians (one
bullfrog tadpole and two unidentied frogs). In contrast,
we detected more amphibian prey items in the Caohai
bullfrogs, with bullfrog cannibalism representing over
36% and B. pleuraden over 30% of the total volume, and
over 37% and 40% of the total biomass, respectively. The
B. pleuraden had a high frequency of occurrence, present
in more than 15% of the total bullfrogs. Cypriniformes
fishes were also important prey (12.9% of volumes,
10.3% of biomass, and 21.9% of prey individuals).
After controlling for the bullfrog body size, we found
Figure 2 Total diet biomass as a function of bullfrog body size
(SVL).
0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
4.24.4 4.64.8 5.0 5.25.4
Ln SVL of Bullfrog (mm)
Ln Mean Prey Biomass (g)
Asian Herpetological Research
Vol. 640
that there were no signicant differences in prey biomass
(ANCOVA; F = 0.22, d.f. = 1, P = 0.644) or volumes (F
= 0.03, d.f. = 1, P = 0.856) between the two populations.
However, the bullfrogs in the Shiping population
consumed more prey individuals (F = 6.69, d.f. = 1, P =
0.011), and tended to have more prey species (F = 3.82,
d.f. = 1, P = 0.053).
3.4 Prey selection by bullfrogs The abundance of the
two native amphibian species in the environment was 0.16
± 0.014 individuals/m (mean ± S.E.) and 1.29 ± 0.032
g/m for the B. pleuraden, and 0.07 ± 0.012 individuals/
m and 1.98 ± 0.310 g/m for the B. maxima. Concerning
prey individuals, B. pleuraden and Cypriniformes shes
were the preferred bullfrog prey items, whereas bullfrog
cannibalism were avoided (Figure 3). Nevertheless,
there was no difference between the two preferred items
(Mann-Whitney U-test, z = –0.53, P = 0.599). In contrast,
regarding prey biomass, B. pleuraden and bullfrog were
preferred, and Cypriniformes shes were avoided (Figure
3). We did not nd a signicant difference in preference
between B. pleuraden and bullfrog cannibalism (z =
–1.38, P = 0.171). Specically, B. maxima was captured
in transects but was absent in the bullfrogs’ stomachs, and
thus the Jacobs’ index (= –1) showed a total avoidance of
this toad by the bullfrogs (Figure 3).
4. Discussion
This study is the first report of the invasive American
bullfrog’s diet in Yunnan Province, southwestern
China, and to the best of our knowledge, provides the
first quantitative study of bullfrog prey selection in the
context of the local anuran assemblage and other aquatic
preys among their invaded ranges. Insects were the most
frequent prey category, with the richest species diversity,
which is consistent with previous studies both in their
invaded ranges, such as in Argentina (Barrasso et al.,
2009), Canada (Govindarajulu et al., 2006; Jancowski
and Orchard, 2013), Germany (Laufer, 2004), the
western USA (e.g., Hothem et al., 2009; Krupa, 2002),
and Venezuela (Diaz de Pascual and Guerrero, 2008),
and their native ranges (e.g., Werner et al., 1995). This
was not surprising, as insects have a relatively large
abundance and availability in the environment, and are
usually the most frequently consumed prey item of frogs
(Yousaf et al., 2010). We also confirmed that crayfish
is an important prey of the bullfrog, as previously
found in the Zhoushan Archipelago, China (Wu et al.,
2005), Tokyo, Japan (Hirai, 2004), and California, USA
(Carpenter et al., 2002; Clarkson and deVos, 1986), and
their native ranges including Kentucky (Bush, 1959),
Eastern Texas (Penn, 1950), Oklahoma (McCoy, 1967;
Tyler and Hoestenbach, 1979), Arkansas (McKamie
and Heidt, 1947), Ohio (Bruggers, 1973), and Missouri
(Korschgen and Baskett, 1963; Korschgen and Moyle,
1955). One interesting nding in our study was that the
red-swamp craysh was one major prey of the bullfrogs
in Shiping, where this craysh has invaded (Liu and Li,
2009). However, with the absence of craysh in Caohai,
anurans comprised a large proportion of the total prey
volume. Positive interactions among invaders (termed
“invasional meltdown”) are considered a phenomenon
that exacerbates the impacts of different invaders on
native species (Simberloff and Von Holle, 1999). For
example, in Oregon, USA, the invasion of bullfrogs was
found to be facilitated by co-evolved non-native fishes
(Adams et al., 2003). However, our findings indicated
that one invader (e.g., bullfrog) might be able to reduce
the negative effect of another (e.g., crayfish) on native
species, especially when one was the favorite prey of
the other. However, this conclusion should be made with
caution, as the craysh is also known as an alien predator
of amphibians (Kats and Ferrer, 2003; Wu et al. 2008).
Therefore, the interactions of different invaders on native
species might be very complex, which requires further
investigations with the aid of mesocosms experiments.
Figure 3 Jacobs’ selection index applied to individuals and biomass
consumed for each aquatic prey species by bullfrogs in the Caohai
population.
-1.2
-1.0
-0.8
-0.6
-0.4
-0.2
0
0.2
0.4
0.6
Individuals
-1.2
-1.0
-0.8
-0.6
-0.4
-0.2
0
0.2
0.4
0.6
Biomass
Cypriniformes sp. B. maxima B. pleuraden L. catesbeianus
Mean value of Jacobs’ selection index (± S. E.)
Xuan LIU et al. Diet Preference of Invasive BullfrogsNo. 1 41
Alternatively, as we did not conduct prey selection studies
on the Shiping population due to difficulty in aquatic
organism sampling, the high proportion of crayfish in
the bullfrogs’ stomachs might merely be due to the high
availability of the craysh in the environment.
We found that the invasive bullfrogs predated on some
vertebrates, particularly the amphibians in our study area.
The consumption of native anurans by bullfrogs has been
widely recorded in the Zhoushan Archipelago of China
(Wang et al., 2007; Wu et al., 2005), and other regions
of the world (see review of Bury and Whelan, 1985).
Collectively, we provide the first evidence of bullfrog
predation on endemic species in China. Predation on
endemics means a more severe impact of this invader on
native amphibians because these endemic species are only
distributed in China and their extinctions will result in
irretrievable loss to the local biodiversity. The predation
preference of the bullfrog on B. pleuraden suggests that
it might be one potential mechanism behind the declining
population trend of this endemic species (Yang and Lu,
2004). Our findings also indirectly demonstrate that a
previous postulation might be true: that bullfrogs were
hypothesized as a major factor causing the decline and
even extinction of two endemic amphibian species,
Cynops wolterstorf in Dian Lake, Yunnan Province (He,
1998), and Paa liui in Lugu Lake (Li and Xie, 2004).
Indeed, our field surveys since 2008 did not record
the presence of P. liui in Caohai. We argue that future
studies could be undertaken by investigating stomach
contents of preserved museum specimens of bullfrogs
to explore its predation history on these endemics.
Although the bullfrog is generally recognized as an
opportunistic generalist predator, it has been suggested
that ranids are preferred by bullfrogs compared with
other anurans (see review in Werner et al., 1995). Our
feeding preference study quantitatively verified that the
Yunnan pond frog, B. pleuraden, was selected by the
bullfrog in terms of both the number of individuals and
the biomass, whereas another endemic toad, B. maxima,
was completely avoided by the bullfrog although several
previous studies have recorded the predation of toad
species by the bullfrog (e.g., Reis et al., 2007; Silva et al.,
2011; Wang et al., 2006; Wang et al., 2007; Wu et al.,
2005). However, this was consistent with another bullfrog
predation selection study which found that toad was
completely avoided among anuran preys by the bullfrog
in southern Brazil (Boelter et al., 2012). Previous studies
have suggested that the habitat use of native frogs could
inuence their predation by bullfrogs (Silva et al., 2011);
therefore, one mechanism involved might be related to
the difference in habitat use between the toad and bullfrog
(Fei et al., 1999). For example, although they could
both inhibit in the permanent still waters, the B. maxima
could also use those slow streams (Fei et al., 1999),
where the bullfrogs rarely select (Wang and Li, 2009).
Another potential explanation might be that toads are less
palatable than are frogs to the bullfrog due to their dermal
toxins (Ahola et al., 2006; Pearl and Hayes, 2002).
Finally, the finding might also simply reflect the low
abundance of this toad in the habitat observed in the eld
survey (Liu and Li, 2009). Theoretically, the body size of
predators could inuence their predation on native frogs
(Wang et al., 2007; Silva et al., 2009; Silva et al., 2011).
However, we did not nd effects of body size, weight, or
mouth width on the predation of natives, indicating that
smaller bullfrogs might not have less predation impacts
on native frogs. Therefore, conservation attentions should
be given irrespective of bullfrog body size.
We recorded a high prevalence of the cannibalism in
both populations of the bullfrogs. Cannibalism in bullfrog
was previously reported both in their native ranges
(Korschgen and Moyle, 1955) and in areas where they
have invaded (e.g., Barrasso et al., 2009; Diaz de Pascual
and Guerrero, 2008; Govindarajulu et al., 2006; Silva
et al., 2009). However, our feeding preference analysis
showed that the bullfrog preferred the juvenile bullfrogs
and tadpoles in terms of biomass but tended to avoid them
in terms of the number of individuals, indicating that the
cannibalism of bullfrogs might be not due to a selection
process and merely may be due to the high energy that
bullfrog tadpoles provide.
We also recorded a native red-banded snake predated
by a bullfrog in the Shiping population. This was not
surprising as previous studies have reported that the
bullfrogs can prey upon reptiles, such as turtles and snakes
(e.g., Clarkson and deVos, 1986; McKamie and Heidt,
1947). Nevertheless, it was interesting that previous
studies found that bullfrogs in the Zhoushan Archipelago
were the favorite prey of the red-banded snake (Li et al.,
2011), and the water snake (Liophis miliaris) was also
observed preying on juveniles of the bullfrogs in south-
eastern Brazil (Silva and Filho, 2009). Although we only
recorded a single incidence of predation of the snake by
the bullfrog, our results at least suggest that the reciprocal
predation might exist between the two species, as they are
naïve to each other. The nal output might be dependent
on the comparison with regard to relative body size and
other predation ability characteristics between the bullfrog
and the snake, which warrants further investigations.
Although previous studies suggested that larger
Asian Herpetological Research
Vol. 642
bullfrogs of both sexes predated more prey individuals
and a greater biomass than smaller bullfrogs (Wu et al.,
2005), we found that the occurrence, biomass and volume
of diet items were generally independent of bullfrog size
or mouth width, despite a weak positive relationship
between the bullfrog body size and prey biomass in our
study populations. An alternative explanation might be
due to the smaller range in SVL of bullfrogs than that of
the previous study (Wu et al., 2005). However, we found
that there were differences in diet composition among
males, females, and juveniles. One potential explanation
is due to size-related ontogenetic diet variation between
adults and juveniles (Blackburn and Moreau, 2006), or
sex-dependent variations in prey compositions (Quiroga
et al., 2009). Despite that the Caohai (higher elevation)
population of bullfrogs exhibited a smaller body size (Liu
et al., 2010), we did not observe any signicant difference
in prey volume or biomass between the two populations.
Nevertheless, we detected a difference in diet composition
between two sampling sites. This might be inuenced by
the difference in prey availability between the two sites,
which needs future investigations.
We acknowledged that we only found one endemic
species and did not detect more native amphibian species
in the bullfrog’s diet. Nevertheless, this does not mean
that the predation impact of the American bullfrog on
native anurans might be limited. For the two frog species
(O. andersonii and P. liui) not detected but occurred
historically, the bullfrog may have predated them to
extinction since invasion and thus they might have
experienced a “ghost of predation past”. Alternatively,
it is known that stomach content analyses are always
inuenced by the degree of digestion, which can make it
difcult to identify all their consumed species, especially
for vertebrates (Hothem et al., 2009). This might also be
another potential reason on why we did not nd a strong
positive relationship of bullfrog size with prey measures.
We recommend that further, more intensive samplings
across more invaded populations be performed in order to
assess the consumption of other native anuran species by
bullfrogs. Furthermore, in addition to the direct predation
impacts, we also detected the amphibian chytrid fungus B.
dendrobatidis both in the eld and in museum historical
bullfrog specimens from our study area (Bai et al., 2012;
Zhu et al., 2014a). Furthermore, a new chytrid species,
Batrachochytrium salamandrivorans, isolated from
infected Salamandra salamandra in the Netherlands,
has been identified to cause rapid mortality in infected
re salamanders (Martel et al., 2013). Although a recent
study tested negative for B. salamandrivorans in the
bullfrog samples from Yunnan Province (Zhu et al.,
2014b), it is known as a potential disease-tolerant carrier
for chytrid fungi (Garner et al., 2006; Liu et al., 2013b).
Thus we urge the development of effective conservation
and monitoring strategies to prevent the further spread of
this notorious invader to more habitats and eliminate their
negative impacts on native communities.
Acknowledgements We thank the anonymous villagers
in Zhawoluo, Caohai, Lugu Lake for assisting with our
field work. We also thank two anonymous reviewers
for constructive comments that have greatly improved
this manuscript. This research was supported by grants
from National Natural Science Foundation of China
(31200416 and 31370545). The collection and handling
of amphibians were conducted by the Animal Care and
Use Committee of Institute of Zoology, Chinese Academy
of Sciences (Project No. 2008/73). All staff, fellows and
students received appropriate training before performing
animal studies.
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