ms-143 - silva, reis, feio, ribeiro filho.indd

South American Journal of Herpetology, 4(3), 2009, 286-294
© 2009 Brazilian Society of Herpetology
Diet of the invasive frog Lithobates catesbeianus (Shaw, 1802)
(anura: ranidae) in Viçosa, Minas Gerais State, Brazil
Emanuel Teixeira da Silva1,3, Evelyze Pinheiro dos Reis2,
Renato Neves Feio1 and Oswaldo Pinto Ribeiro Filho1
Programa de Pós-graduação em Biologia Animal, Departamento de Biologia Animal.
Programa de Pós-graduação em Genética e Melhoramento, Departamento de Biologia Geral,
Universidade Federal de Viçosa, 36571‑000, Viçosa, MG, Brasil.
3
Corresponding author. E‑mail: [email protected]
1
2
Abstract. Based on the stomach content analysis of 113 individuals, the diet of the invasive amphibian Lithobates catesbeianus
(American Bullfrog) was examined in four sites located within the municipality of Viçosa (20°45’S and 42°51’W), state of Minas
Gerais, Brazil, from August 2005 to March 2007. The effects of frog size and sexual maturity on stomach contents were determined.
Prey items were grouped according to their primary habitat, being classified as aquatic, terrestrial and amphibious. In general,
the most frequent prey categories were post-metamorphic Anura, Diplopoda, Hemiptera, Hymenoptera Formicidae and Araneae.
The diet of adults of both sexes was similar, but differed from the diet of young frogs. Terrestrial prey were most abundant
both in number and occurrence. For adult Bullfrogs, amphibious prey were most significant in volume. There was a significant
correlation between prey and predator sizes, as well as a greater consumption of native anurans by larger Bullfrogs. The results
confirmed that Bullfrogs have a generalist feeding habit that can have important negative effects on native amphibian communities
in environments occupied by this invasive species.
Keywords. Feeding habits; biological invasion; American Bullfrog; Lithobates catesbeianus.
Introduction
Native to North America, Lithobates catesbeianus (Shaw, 1802), commonly known as the Bullfrog,
was introduced in several countries for commercial harvest (Moyle, 1973; Bury and Whelan, 1984;
Giovanelli et al., 2008). The Bullfrog is the largest
anuran species in North America. It is mostly aquatic
and is a generalist predator, reflecting prey availability, including cannibalism (Bury and Whelan, 1984).
The feeding habits of L. catesbeianus have been
studied several times and many of these studies described the occurrence of uncommon prey types for
an anuran, such as moles, mice, bats, birds, snakes,
lizards, turtles, small alligators, salamanders and
fish (Korschgen and Moyle, 1955; Cohen and Howard, 1958; Korschgen and Baskett, 1963; Brooks Jr.,
1964; Corse and Metter, 1980; Bury and Whelan,
1984; Silva et al., 2007; Camargo Filho et al., 2008).
The Bullfrog was chosen for commercial exploitation because of its high fecundity, which results in
greater performance in captivity than other frog species (Vizotto, 1984; Fontanelo, 1994). In Brazil, the
first individuals of L. catesbeianus arrived in 1935
(Fontanello, 1994), and since then tadpoles and mature frogs were freely given to producers in order to
stimulate the cultivation of this species. This species easily colonized different ecosystems in Brazil,
which lead to the recommendation of its production
in many Brazilian states (Fontanello, 1994).
It is well known that intentional introductions and
farming escapes due to harvest deficiencies lead to
population establishment in aquatic sites near frog
farms (Hammerson, 1982; Bury and Whelan, 1984).
The occurrence of invasive populations of the Bullfrog have been reported in the south, southeast and
central regions of Brazil (Guix, 1990; Batista, 2002;
Martins et al., 2002; Boelter and Cechin, 2007;
Giovanelli et al., 2008; Kaefer et al., 2007; Reis
et al., 2007; Silva et al., 2007). Given the generalist predatory habits of the Bullfrog, its introduction
into natural environments is a cause for concern and
prompts further investigation. Its ability to prey on
other anurans, as well as competitive effects among
tadpoles (Kupferberg, 1997; Lawler et al., 1999; Kiesecker et al., 2001) and possible pathogen transmission (Hanselmann et al., 2004; Garner et al., 2006;
Barrasso et al., 2009), makes the Bullfrog a possible
agent of amphibian population decline at its introduction sites (Hayes and Jennings, 1986; Kats and Ferrer,
2003; Pearl et al., 2004).
In the municipality of Viçosa, state of Minas
Gerais, the first Bullfrogs arrived in the early 1980’s
after the construction of the “Ranário Experimental”
(RE; experimental frog farming) at the Universidade
Federal de Viçosa (UFV) campus (Lima, 1994). Since
then, the RE has become a source of tadpoles and immature frogs that have established invasive populations in aquatic sites located in surrounding areas, due
to escapes from the RE. The aim of the present study
Silva, E. T. et al.
was to describe the diet of L. catesbeianus in aquatic
environments on the UFV campus in an attempt to
analyze the effects of frog size, sex and sexual maturity on the prey types consumed.
Material and methods
Study sites
Bullfrog specimens were collected at four sites located on the campus of the Universidade Federal de
Viçosa, in the municipality of Viçosa (20°45’S and
42°07’W), Minas Gerais state, southeastern Brazil.
The municipality of Viçosa lies within the Atlantic
Rainforest domain; the region was originally covered
by semi-deciduous forest. Currently, secondary forest
fragments surrounded by agriculture, pastures, and
eucalyptus plantations make up the landscape (Ribon
et al., 2003; Coelho et al., 2005).
The first sampling site, known as the “Represa do
Belvedere”, consists of a group of small connected
dams surrounded by a secondary forest fragment and
a grassplot. The dams have abundant aquatic vegetation composed of Salvinia sp. and Nympheaceae.
The second site, known as “Estação Experimental
de Fruticultura” is an area designated for the experimental cultivation of fruit trees, with four small dams
originally built to serve as water reservoirs for irrigation. The shoreline herbaceous vegetation is managed
regularly. There are a few aquatic plants, including
Nympheaceae. The third sampling site consists of
two artificial reservoirs located in an area of experimental grain production. The shoreline is dominated
by Poaceae and sparse tree coverage, and there is no
evident aquatic vegetation. The last site is an experimental fish station located near the Ranário Experimental site. It consists of 95 dams of different sizes,
surrounded by regularly cut herbaceous vegetation.
Some of the dams have aquatic vegetation, with the
presence of Eichhornia crassipes and Nympheaceae.
Data collection
Frogs were captured at night (18:30‑22:00 h) from
August 2005 to March 2007. Field activities in sites
1 and 2 were carried out twice per month, and sites 3
and 4 were sampled sporadically, starting in August
2006. Frogs were captured by hand with the help of
nets and an air rifle. The specimens collected were
killed in situ and stored on ice to retard digestion
287
(Boelter and Cechin, 2007). The samples were then
deposited in the herpetological collection at “Museu
de Zoologia João Moojen” (MZUFV). In the laboratory, frogs were weighed to the nearest 1 g, and the
snout-vent length (SVL) and jaw width (JW) were
measured to the nearest 0.05 mm using calipers. The
individuals were grouped in seven size classes based
on the SVL, adapting the classification of Lima et al.
(1998): class 1 (< 50 mm); class 2 (50.05‑70 mm);
class 3 (70.05‑90 mm); class 4 (90.05‑110 mm); class
5 (110.05‑130 mm); class 6 (130.05‑150 mm) and
class 7 (> 150.05 mm).
Frogs were dissected to remove the stomachs
which were preserved in 70% ethanol. The individuals were sexed by gonad analysis and development
of the secondary sexual traits (diameter of tympanic
membrane, throat coloration and swollen thumbs;
Bury and Whelan, 1984). Females (young and mature) were separated based on gonad development
(Costa et al., 1998). Males weighing more than 45 g
were classified as adults (Lima et al., 1998). Three
groups were considered in diet analyses: adult males,
adult females and juveniles.
The stomach content was analyzed with the help
of a stereomicroscope. Food items were determined
to the lowest possible taxonomic level. The plant
remains found were considered to be accidently ingested. Prey items were grouped according to their
primary habitat, being classified as aquatic, terrestrial
and amphibious. The length and maximum width of
each intact prey item was measured with calipers (to
the nearest 0.05 mm) (Wu et al., 2005). Individual
prey volume (mm3) was calculated using the formula
for an ellipsoid (Magnusson et al., 2003):
Prey volume = 4/3 π (lenght/2) (width/2)2
The total volume (cm3) of prey categories was
estimated by water displacement (Magnusson et al.,
2003). This method was used because of the presence
of fragmented prey items that could be identified but
not measured, and could be grouped to estimate the
total volume of each prey sample.
Data analysis
Frogs with empty stomachs or with only plant remains were not considered in the analysis. The frequency of prey occurrence per Bullfrog (FO = 100
x number of stomachs containing the prey category
t divided by the total number of stomachs), relative
Diet of Lithobates catesbeianus
288
Table 1. Snout-vent length (SVL), prey length (all these in mm), and prey volume (mm3) of Lithobates catesbeianus collected in Viçosa,
Minas Gerais State, Brazil (N = 113), presented as mean ± one standard deviation. Nf = number of frogs; Np = number of prey measured.
Adult males
(Nf = 46; Np = 85)
Adult females
(Nf = 33; Np = 65)
Juveniles
(Nf = 34; Np = 68)
Size class 1
(Nf = 11; Np = 24)
Size class 2
(Nf = 16; Np = 36)
Size class 3
(Nf = 9; Np = 34)
Size class 4
(Nf = 4; Np = 2)
Size class 5
(Nf = 11; Np = 10)
Size class 6
(Nf = 44; Np = 68)
Size class 7
(Nf = 18; Np = 44)
SVL
71.45‑175.75
(136.65 ± 19.79)
88.65‑187.25
(144.27 ± 20.05)
35.90‑99.80
(59.37 ± 13.71)
35.90‑49.60
(44.70 ± 4.71)
51.50‑69.30
(61.36 ± 6.09)
70.70‑88.65
(76.98 ± 6.71)
99.65‑108.60
(103.10 ± 4.27)
111.05‑129.90
(118.85 ± 6.12)
130.25‑149.90
(141.22 ± 5.07)
152.20‑187.25
(162.34 ± 10.28)
abundance of prey in Bullfrog stomachs (NF = 100
x total number of individuals of the prey category t
divided by the total number of all individuals consumed), and relative volumetric abundance of prey
in Bullfrog stomachs (VF = 100 x total volume of
individuals of the prey category t divided by the total
volume of all prey categories in all stomachs) were
calculated for each prey category.
The diet overlap among the three Bullfrog groups
(adult males, adult females and juveniles) was calculated using the index of Pianka (1973). Diet overlap
between predator group j and group k was calculated
as
Ojk = Okj = [S (pij x pik)] / (S pij2 x pik2) 0.5
Where pij and pik are the relative abundance (NF)
of the category i used as prey by the groups j and k
paired in each treatment, and Ojk = Okj means that the
effect of group j on group k is equal to the effect of
group k on group j.
An analysis of variance (ANOVA) was used to examine differences between Bullfrog groups in terms
of the number of ingested prey items and SVL. Prey
length and volume were also compared among adult
males, females and juveniles by using ANOVA. If
one of these differences was significant, a Tukey’s
test was used to make a side-by-side comparison of
the corresponding variable among Bullfrog groups.
Individual prey length
2.35‑97.60
(30.11 ± 25.65)
1.25‑83.40
(24.42 ± 19.95)
0.80‑30.85
(9.58 ± 7.19)
2.05‑30.85
(8.42 ± 7.51)
0.80‑28.95
(10.13 ± 7.05)
2.80‑72.95
(14.48 ± 12.73)
26.05‑97.60
(61.83 ± 50.59)
8.10‑34‑35
(17.40 ± 9.10)
1.55‑96.90
(29.48 ± 21.68)
1.25‑95.60
(32.68 ± 28.06)
Individual prey volume
1.69‑17193.80
(1810.94 ± 3532.26)
0.32‑26625.37
(1696.81 ± 3979.04)
0.49‑1917.49
(103.55 ± 278.29)
0.49‑1125.66
(94.01 ± 247.69)
0.68‑1917.49
(118.54 ± 325.67)
1.62‑1627.78
(198.72 ± 390.87)
397.53‑2538.67
(1468.10 ± 1514.01)
14.08‑2116.24
(555.05 ± 714.34)
0.52‑17193.80
(2461.97 ± 4160.17)
0.32‑26625.37
(1865.52 ± 4263.98)
The average prey length and volume, as well as the
length and volume of the largest prey items obtained
from each stomach were compared to the SVL with
the Pearson Correlation test. Only the specimens that
had at least one prey that could be measured were
considered in this analysis.
Results
Bullfrog body size (SVL) varied from 35.9 to
187.2 mm (113.9 ± 42.6 mm), and was highly correlated to JW (rs = 0.982; p < 0.05). Adult males and females had no significant differences in size, but were
significantly larger than juveniles (F = 232.4; df = 2;
P < 0.05; Q[0.05, 110] = 3.364; Table 1).
A total of 129 specimens of L. catesbeianus were
collected and 11 of them (8.5%) had empty stomachs. Plant remains were found in the stomachs of
81 individuals (62.8%), of which five (3.9%) proved
to have nothing but plant remains present. After the
exclusion of those individuals with empty stomachs
or with stomachs containing only plant remains, information on diet composition was obtained from 113
specimens (46 adult males, 33 adult females and 34
juveniles). Of the 129 collected frogs, 107 (82.9%)
had at least one identifiable prey, and the other six
specimens (4.6%) had only arthropod fragments or
non-identifiable remains in their stomachs.
Silva, E. T. et al.
289
Table 2. Diet composition of Lithobates catesbeianus in Viçosa, Minas Gerais State, Brazil (N = 113); NF = numeric frequency; FO = frequency of occurrence; VF = volumetric frequency.
Prey categories
Annelida
Hirudinea
Oligochaeta
Mollusca
Gastropoda
Pulmonata
Prosobranchia
Arthropoda
Diplopoda
Juliformes
Polydesmida
Arachnida
Araneae
Acarina
Opiliones
Crustacea
Decapoda
Ostracoda
Insecta
Ephemeroptera (adults)
Ephemeroptera (naiads)
Isoptera
Odonata (adults)
Odonata (naiads)
Orthoptera
Hemiptera
Coleoptera
Hymenoptera
Formicidae
Others
Lepidoptera (adults)
Lepidoptera (larvae)
Diptera
Chordata
Amphibia
Anura
Tadpoles
Post‑metamorphic
Terrestrial prey
Aquatic prey
Amphibious prey
Arthropod remains
Undetermined remains
Adult males (N = 46)
NF
FO
VF
Adult females (N = 33)
NF
FO
VF
NF
1.57
0.79
2.17
2.17
<0.01
0.20
1.11
—
3.03
—
0.01
—
—
2.17
—
5.88
—
3.03
3.94
2.36
0.79
8.70
4.35
2.17
0.85
0.48
0.34
6.67
3.33
1.11
15.15
9.09
3.03
3.51
2.51
0.91
2.17
1.09
1.09
5.88
2.94
2.94
13.44
12.71
0.73
16.54
13.39
3.15
11.02
10.24
—
0.79
0.79
0.79
—
43.31
—
—
0.79
4.72
0.79
0.79
8.66
7.87
7.09
6.30
0.79
2.36
8.66
0.79
23.91
21.74
2.17
23.91
21.74
—
2.17
2.17
2.17
—
67.39
—
—
2.17
10.87
2.17
2.17
13.04
21.74
17.39
15.22
2.17
4.35
17.39
2.17
26.72
26.58
0.15
0.90
0.80
—
0.10
4.18
4.18
—
11.49
—
—
<0.01
1.55
0.22
0.29
2.16
3.62
0.39
0.33
0.06
1.24
3.73
0.05
12.22
11.11
1.11
13.33
13.33
—
—
1.11
—
1.11
46.67
3.33
—
1.11
4.44
1.11
1.11
13.33
6.67
10.00
7.78
2.22
2.22
3.33
—
21.21
21.21
3.03
24.24
24.24
—
—
3.03
—
3.03
51.52
3.03
—
3.03
9.09
3.03
3.03
24.24
12.12
18.18
12.12
6.06
6.06
9.09
—
11.38
10.98
0.40
2.99
2.99
—
—
<0.01
—
<0.01
21.51
0.28
—
<0.01
0.21
0.06
0.17
16.32
1.53
0.96
0.33
0.63
1.41
0.85
—
3.26
1.09
2.17
10.87
9.78
1.09
—
—
—
—
77.17
—
1.09
—
7.61
1.09
10.87
10.87
6.52
30.43
26.09
4.30
1.09
—
7.61
8.82
2.94
5.88
26.47
23.53
2.94
—
—
—
—
79.41
—
2.94
—
20.59
2.94
17.65
20.59
17.65
47.06
44.12
11.76
2.94
—
14.71
2.42
<0.01
2.42
2.66
1.94
0.73
—
—
—
—
60.53
—
<0.01
—
18.77
4.12
19.85
4.84
2.54
8.35
4.00
5.14
<0.01
—
2.06
22.05
22.05
3.15
18.90
59.06
18.90
21.26
—
—
34.78
34.78
6.52
28.26
86.96
28.26
30.43
21.74
15.22
50.97
50.97
4.51
46.46
39.14
11.38
46.55
1.44
1.55
18.89
18.89
4.44
14.44
58.89
25.56
15.56
—
—
36.36
36.36
12.12
27.27
63.64
39.39
33.33
21.21
9.09
58.09
58.09
13.76
44.34
20.98
32.43
44.34
1.67
0.59
4.35
4.35
1.09
3.26
82.61
13.04
4.35
—
—
11.76
11.76
2.94
8.82
79.41
26.47
3.26
20.59
11.76
10.65
10.65
0.73
9.93
69.37
13.44
9.93
3.03
0.97
A total of 309 prey items were identified (127 in
adult males, 90 in adult females and 92 in juveniles;
Table 2). The number of prey items per individual was
similar among Bullfrog groups (range, average ± SD;
adult males: 1‑9; 2.98 ± 2.20; adult females: 1‑13;
3.13 ± 2.42; juveniles: 1‑10; 2.94 ± 2.06; F = 0.066;
df = 2; P > 0.05).
Juveniles (N = 34)
FO
VF
The most frequent prey categories of adult males
were post-metamorphic Anura and Diplopoda (Table 2). Post-metamorphic Anura were found to be
most common in adult females, along with Araneae,
Hemiptera, and Diplopoda. For juveniles, Hymenoptera Formicidae, Orthoptera, Hemiptera, Odonata,
and Araneae were the most frequent prey categories.
Diet of Lithobates catesbeianus
290
Table 3. Correlation (Pearson) among SVL of Lithobates catesbeianus (N = 87) and prey length and volume, from Viçosa,
Minas Gerais State, Brazil.
Variables
Mean prey length
Largest prey length
Mean prey volume
Largest prey volume
rs
0.4805
0.4916
0.3348
0.3331
T
5.0519
5.2049
3.2752
3.2566
p
0.0001
0.0001
0.0005
0.0006
A total of 49 anurans were consumed by Bullfrogs,
being 40 post-metamorphic and nine tadpoles, one
of them a L. catesbeianus tadpole. The post-metamorphic anurans identified were the native hylids
Dendropsophus minutus (N = 2), D. elegans (N = 3),
Scinax crospedospilus (N = 1), S. eurydice (N = 9),
Hypsiboas faber (N = 2), and the bufonid Rhinella
pombali (N = 1), besides 22 undetermined individuals. The post-metamorphic anurans (N = 15) ranged
from 12.7 to 56.1 mm in length (average ± SD:
37.3 ± 11.8 mm) and 216.8 to 17,193.8 mm3 in volume (6848.4 ± 5793.1 mm3).
Terrestrial prey items were the most frequent
in number, especially in the stomachs of juveniles
(82.6%; Table 2). Regarding total volume, terrestrial
prey were most frequent only for juveniles (69.37%),
while amphibious prey were most frequent in adult
Bullfrogs (males: 46.5%; females: 44.3% of the diet).
Diet overlap was higher between adult males and females (0.944; 83.3%) than between adults and juveniles (adult females 0.671, 61.6%; adult males 0.554,
55.9%). Adults of both sexes showed no significant
differences in relation to prey size, but consumed
larger prey than juveniles [prey length: F = 21.01;
df = 2; P < 0,05; Q (0.05, 215) = 3.310; prey volume:
Figure 1. Diet composition of the size classes of Lithobates catesbeianus collected in Viçosa, Minas Gerais State, Brazil (N = 109)
according to the numeric frequency (NF). The group “Others”
refers to Annelida, Gastropoda and Crustacea.
F = 6.715; df = 2; P < 0,05; Q (0.05, 215) = 3.310]. The
length and volume of the largest prey items, as well as
the average prey length and volume, were positively
correlated to the SVL of frogs (Table 3). Because of
the small number of individuals collected (N = 4),
size class 4 was not considered in the analyses. Insects were the most abundant prey group in the diet of
all size classes, although a progressive reduction was
observed in consumption of insects from class 3 to
class 7 (Figure 1). On the other hand, the presence of
Diplopoda and Amphibia tended to increase ontogenetically, and Amphibia was not consumed by class 1.
Discussion
Amphibians are generally considered opportunistic predators. Their diets often reflect the availability
of prey in their habitats, and they ingest any prey of
appropriate size (Korschgen and Baskett, 1963; Duellman and Trueb, 1994; Stebbins and Cohen, 1995).
Compared to other frogs, L. catesbeianus seems to be
an extremely opportunistic predator (Korschgen and
Moyle, 1955; Cohen and Howard, 1958; Korschgen
and Baskett, 1963; Brooks Jr., 1964; Corse and Metter, 1980; Bury and Whelan, 1984; Silva et al., 2007;
Camargo Filho et al., 2008) and the results herein
on the diet of invasive populations corroborate this
suggestion.
Insects were the most diverse and abundant prey
group in the diet of L. catesbeianus, as observed by
Korschgen and Moyle (1955), Korschgen and Baskett (1963) and Corse and Metter (1980), probably
because of their high availability, although this was
not evaluated in this study. Amphibia and Diplopoda
also represented a considerable portion of total prey
volume (53.9% and 19.9%, respectively). Our results
were similar to those obtained in a similar study by
Boelter and Cechin (2007) in areas where the species was introduced in the state of Rio Grande do Sul,
southern Brazil.
Plant ingestion by Bullfrogs was considered accidental by several authors (Korschgen and Moyle,
1955; Korschgen and Baskett, 1963; Corse and Metter, 1980; Wu et al., 2005). In area 1, 30.2% of the
frogs with plant in their stomachs (N = 43) showed
remains of Salvinia sp., a common aquatic pteridophyte in local dams. Potential prey of L. catesbeianus,
such as spiders, moths, and treefrogs were observed
on this floating vegetation in several occasions during
fieldwork, and were also found in Bullfrog stomachs
together with Salvinia sp. remains. Thus, Salvinia sp.
Silva, E. T. et al.
may have been ingested accidentally when the Bullfrogs were ingesting arthropods and anurans. Korschgen and Baskett (1963) suggest that the presence of
plant remains in Bullfrog stomachs is a result of its
proximity to the prey at the moment of capture or due
to its movement on the water’s surface.
Ontogenetic shifts in frog diet are often related
to size differences among predators (Duellman and
Trueb, 1994). Larger individuals can continue feeding
on the same types of prey used by the smaller frogs,
while also including larger prey in their diets (Stebbins and Cohen, 1995) which can explain the differences in diet composition observed between adults
and juveniles of L. catesbeianus. This trend became
evident also by the positive correlation between prey
size (length and volume) and frog SVL, as observed
for Leptodactylus ocellatus by França et al. (2004)
and Maneyro et al. (2004). Consumption of Diptera,
Odonata, Orthoptera, and Hymenoptera was more
frequent in juveniles, and the consumption of Hymenoptera Formicidae stands out as the greatest difference between adult and juvenile frogs. The opposite
was true for the consumption of post-metamorphic
anurans and diplopods, which were more frequent
in the adult diet, a factor most likely due to the fact
that most of these prey items are too large for juvenile
frogs. This may also contibute to the low diet overlap
between adults and juveniles. Our comparison of the
diet among size classes (Figure 1) may reflect differences between adults and juveniles, since classes 1
and 2 were composed only of juveniles, class 3 was
composed mostly of juveniles, and classes 5‑7 were
composed only of adults. Similar results were obtained by Govindarajulu et al. (2006) for Bullfrogs
introduced in Canada.
A high similarity and overlap between the diet
of male and female Bullfrogs were also reported by
Brooks Jr. (1964), Werner et al. (1995), and Boelter
and Cechin (2007). Spatial distribution of Bullfrogs
in sampling sites may explain this similarity. Most
adult males and females were collected at the same
place, on the edge of water bodies, which is related
to the reproductive behavior of this species (see Bury
and Whelan, 1984). Similarity in body size and jaw
width may also contribute to the higher diet overlap
between adult males and females than between adults
and juveniles.
A peculiarity in this study was the high consumption of diplopods. These animals have chemical defenses, such as phenolic and quinone compounds,
produced by repugnant glands (Ruppert and Barnes,
1996). Although Stebbins and Cohen (1995) report
291
palatability as a factor that affects prey selection by
amphibians, our results and those of other authors
(Korschgen and Baskett, 1963; Brooks Jr., 1964),
suggest that L. catesbeianus can tolerate these repugnant compounds.
The occurrence of a bufonid (Rhinella pombali)
among the stomach contents, as well as the observation of a Bullfrog preying upon a toad of the same
species (Reis et al., 2007), also indicates tolerance
to bufonid chemical defenses. Korschgen and Moyle
(1955) also found a bufonid in a stomach of L. catesbeianus, and questioned if the occurrence of only one
individual would not indicate a low acceptance of this
amphibian group as prey. Bury and Whelan (1984),
in their review on L. catesbeianus ecology, cite instances of predation on bufonids and the immobilization effect on Bullfrogs by the secretion of bufonid
poison glands. Bufonids were also reported as prey
for other frog species, including Rana pretiosa (Pearl
and Hayes, 2002), Leptodactylus ocellatus (Gallardo,
1958; França et al., 2004), L. labyrinthicus (Cardoso
and Sazima, 1977) and Ceratophrys ornata (Braun
et al., 1980).
Terrestrial prey items were numerically dominant
and most frequent in the stomachs, although other
studies have indicated a high importance of aquatic
prey items in the diet of L. catesbeianus (Werner et al.,
1995; Hirai, 2004; Wu et al., 2005). The low frequency of prey with amphibious habits in the stomachs of
juveniles is a consequence of the low consumption of
post-metamorphic anurans, probably because of size
constraints (see results). On the other hand, the consumption of anurans also explains the greater volumetric contribution of amphibious prey in adult Bullfrogs. The results of Hirai (2004), in Kyoto, Japan,
could have been influenced by the high abundance
of the crayfish (Procambarus clarkii) detected in the
habitat studied, which resulted in a high frequency of
this crustacean in the diet of L. catesbeianus.
Our study confirms that the American Bullfrog
has a generalist feeding habit, which together with
its capacity to occupy modified environments (Barrasso et al., 2009), appears to favor the establishment
of invasive populations in Brazil. The use of native
anurans as a food source was high among adult Bullfrogs, which suggests the possible occurrence of a
negative effect on native anuran populations in sites
occupied by this invasive species. Observations in
the western United States suggest a direct correlation
between Bullfrog dispersal and decrease of native
ranids, and predation is cited as a possible cause of
this decline (Moyle, 1973; Hammerson, 1982; Hayes
Diet of Lithobates catesbeianus
292
and Jennings, 1986; Kats and Ferrer, 2003; Pearl
et al., 2004). Nevertheless, stating that predation is
the cause of population decline based only on stomach content analysis, without data on the size of prey
populations, may not be safe (Hayes and Jennings,
1986). In fact, the high presence of native anurans in
the diet of the Bullfrog, as reported here, can also indicate some level of co-existence, since the invasion
in Viçosa has lasted about 30 years. Unfortunately,
data on the size of native anuran populations are lacking for the sites studied, as well as on their fluctuation
since the Bullfrog introduction, which does not allow
us to draw further conclusions.
On the other hand, competition for food resources
among adults of invasive Bullfrogs and ecologically
similar species is also suggested as a possible negative
interaction (Hayes and Jennings, 1986; Werner et al.
1995; Barrasso et al., 2009). Some species of South
American leptodactylids, such as Leptodactylus ocellatus, which is common in lentic water bodies and
has a generalist diet, could be affected by this competition, as proposed by Barrasso et al. (2009). Local
extinction of leptodactylids was reported by Batista
(2002) in a locality of the Brazilian State of Goiás,
following Bullfrog introduction. In Viçosa, Lima and
Verani (1988) estimated a population around 200 individuals of L. ocellatus at the second site sampled
in the present study, based on data collected between
January 1978 and January 1979, before the introduction of Bullfrogs. During the fieldwork of the present
study few individuals of this species were observed
in that site, and their encounter was not frequent, suggesting a possible population decrease since those
times. The possibility of negative interactions with
Bullfrogs cannot be discarded, although other factors
can be involved in this apparent decline. Guix (1990)
reported that L. ocellatus was frequent in a locality of
São Paulo State, in spite of the presence of invasive
Bullfrogs. Thus, the possible relationship between the
spread of the Bullfrog and native amphibian population declines in Brazil is a question that remains
unclear.
Resumo
A dieta do anfíbio invasor Lithobates catesbeianus
(rã-touro americana) foi examinada em quatro
locais em Viçosa (20°45’S e 42°51’W), Estado de
Minas Gerais, Brasil, através da análise do conteúdo
estomacal de 113 exemplares coletados entre agosto
de 2005 e março de 2007. Os efeitos do tamanho e
maturidade sexual das rãs foram determinados. As
presas foram classificadas em três grupos de acordo
com seu principal habitat: aquáticas, terrestres e
anfíbias. As categorias de presas mais freqüentes na
dieta foram Anura (pós-metamórficos), Diplopoda,
Hemiptera, Hymenoptera Formicidae e Araneae.
As dietas de adultos de ambos os sexos foram
semelhantes, diferindo em maior grau da dieta de
indivíduos jovens. Presas terrestres foram mais
abundantes em número e ocorrência e, para os adultos,
presas de hábitos anfíbios foram mais representativas
em volume. A dieta variou de acordo com o tamanho
dos indivíduos, havendo relação positiva entre o
tamanho das rãs e o tamanho das presas ingeridas, e
maior consumo de anfíbios anuros pelas rãs maiores.
Estes resultados confirmam que a rã-touro possui
hábito alimentar generalista, podendo ter algum
efeito negativo importante sobre as comunidades de
anfíbios nativos nos locais ocupados por esta espécie.
Acknowledgements
We are grateful to the colleagues of the Museu de Zoologia
João Moojen for their assistance in field work; to Patrícia S.
Santos for her comments and suggestions during the development
of this work; to Jorge A. Dergam and Rubem A. Boelter for their
help in obtaining references; to Paulo R. Cecon for his help with
the statistical analyses; to João Vitor G. Lacerda and Ansley
Ditmore for the English revision; to Departamento de Biologia
Animal for logistic support; to IBAMA for the collection permits
(036/05 and 233/06). Marcio Martins and two anonymous
reviewers also made useful comments on the final version of
this paper. ETS would also like to thank the Conselho Nacional
de Desenvolvimento Científico e Tecnológico (CNPq) for the
fellowship during part of this study (PIBIC/UFV).
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Submitted 21 July 2009
Accepted 12 November 2009