Journal of Herpetology, Vol. 43, No. 1, pp. 49–54, 2009
Copyright 2009 Society for the Study of Amphibians and Reptiles
Effects of Density on Metamorphosis of Bullfrogs in a Single Season
STACY E. PROVENZANO
AND
MICHELLE D. BOONE1
212 Pearson Hall, Department of Zoology, Miami University, Oxford, Ohio 45056 USA
ABSTRACT.—Although the number of temporary wetlands used by many amphibian species has declined
nationally, permanent wetlands have increased on the landscape in many regions. Species like Bullfrogs
(Rana catesbeiana) may benefit from permanent wetlands and increase their density on the landscape,
making them more likely to encounter wetlands used by amphibians breeding in temporary ponds.
Although Bullfrogs are typically viewed as inhabitants of permanent wetlands because of their long larval
periods, they are known to use temporary ponds. This study examined how larval density influenced
proportion of Bullfrogs metamorphosing, time to metamorphosis, mass at metamorphosis, and total Bullfrog
survival in mesocosm ponds. Proportion of Bullfrogs metamorphosing and tadpole development were
greatest in mesocosms with low tadpole density with up to 25% of tadpoles reaching metamorphosis. Our
study indicates Bullfrogs can metamorphose in more northern climates within a single season across a range
of densities, and highlights the potential for Bullfrogs to successfully use temporary pond environments.
Amphibians are experiencing worldwide
population declines that appear to be more
severe than declines of mammals or birds
(Houlahan et al., 2000; Semlitsch, 2003; Stuart
et al., 2004). A leading cause for these declines is
habitat destruction and alteration (Stuart et al.,
2004). Although temporary wetlands are declining across North America (Zedler and Kersher,
2005), permanent, human-made water bodies
have increased in some areas (Smith et al., 2002;
Zedler and Kersher, 2005). Because many
human-made ponds are stocked with fish, this
could facilitate species such as Bullfrogs (Rana
catesbeiana) that can coexist with fish (Bury and
Whelan, 1984). Although many amphibian
populations appear to be at risk of extinction,
Bullfrogs are generally not declining (but see
Hecnar and M’Closkey, 1997) and appear to be
expanding their range naturally and through
human introductions (Hayes and Jennings,
1986; Adams et al., 2003; Hanselmann et al.,
2004). Given that Bullfrogs have been associated
with declines of other amphibian species (Hayes
and Jennings, 1986; Lawler et al., 1999; Pearl et
al., 2004), factors that affect their abundance or
density could have serious consequences within
and outside their native range. Increased permanent pond habitat may favor Bullfrogs and
increase their density on the landscape, which
may lead to an increased probability that
Bullfrogs encounter and use temporary pond
environments for larval development. Although
it is generally assumed that Bullfrogs do not use
temporary ponds, they have been found to
breed in temporary ponds (Pechmann et al.,
1
Corresponding Author. E-mail: boonemd@muohio.
edu
1989, 2001; Scott et al., 2002). Therefore, Bullfrogs have the potential to affect temporary
pond communities, and understanding the
flexibility of the larval period of Bullfrogs is of
interest.
Bullfrogs are known to have a large effect on
the structure of amphibian communities. For
instance, the relative abundance of species such
as the Green Frog (Rana clamitans; Collins and
Wilbur, 1979), the Foothill Yellow-Legged Frog
(Rana boylii; Moyle, 1973), and Carpenter Frogs
(Rana virgatipes) and Pine Barrens Treefrogs
(Hyla andersonii; Zampella and Bunnell, 2000)
has been found to be inversely related to
Bullfrog abundance. Bullfrogs compete with
other amphibian species for food resources
(Kupferberg, 1997; Adams, 2000; Boone et al.,
2004) and can prey upon the larvae, juveniles,
and adults of other anurans (Stewart and
Sandison, 1972; Kiesecker and Blaustein, 1997;
Lawler et al., 1999; Pearl et al., 2004). Bullfrogs
can also carry Batrachochytrium dendrobatidis, the
chytrid fungus associated with amphibian
declines, whereas not exhibiting clinical signs
of the disease (Daszak et al., 2004; Hanselmann
et al., 2004). Therefore, addition of Bullfrogs to
temporary pond communities across their range
could have significant consequences.
Although Bullfrogs inhabit a variety of
wetlands, they are typically found in permanent
ponds (Bury and Whelan, 1984; Wellborn et al.,
1996) because their larvae often overwinter as
tadpoles (Bury and Whelan, 1984; Hecnar and
M’Closkey, 1997; Govindarajulu et al., 2006).
However, Bullfrog tadpoles are also known to
metamorphose in less than one year (Viparina
and Just, 1975; Cecil and Just, 1979; Pechmann et
al., 1989) with their larval periods ranging from
50
S. E. PROVENZANO AND M. D. BOONE
four months in Louisiana to three years in New
York (Wills et al., 1956; Bury and Whelan, 1984).
However, metamorphosis in a single season is
generally believed to be probable only in
warmer climates like the southern United
States.
The long larval period of Bullfrogs can allow
them to reach large size at metamorphosis
(Wilbur and Collins, 1973) and is a balance
between mortality risks and potential growth in
aquatic and terrestrial habitats (Werner, 1986).
Because large size at metamorphosis is positively associated with fitness in amphibians
(Semlitsch et al., 1988; Morey and Reznick, 2001;
Altwegg and Reyer, 2003), larval periods exceeding one year may be more favorable and
select against early metamorphosis. However,
conditions that favor rapid growth may encourage metamorphosis without overwintering
(Collins, 1979). Low-density conditions (Wilbur,
1977; Scott, 1994; Semlitsch et al., 1996) and
higher environmental temperatures (Dodd and
Dodd, 1976; Crawshaw et al., 1992; Duellman
and Trueb, 1994) can both promote more rapid
development and may also provide conditions
that yield greater food resources. All of these
factors could potentially lead to single-season
metamorphosis for Bullfrogs.
We examined the potential for single-season
metamorphosis of Bullfrogs reared at varying
densities in drying pond mesocosms to explore
the ability of Bullfrog tadpoles to successfully
use temporary wetlands (drying every one to
two years). We tested the hypothesis that larval
density of Bullfrogs would influence rates of
metamorphosis in a single season. This is the
first study to experimentally examine factors
that influence the rates of single season metamorphosis.
MATERIALS AND METHODS
This experiment was conducted outdoors at
the Ecology Research Center (ERC) of Miami
University in Oxford, Ohio (39u319N, 84u459W).
The average number of frost-free days in nearby
Dayton, Ohio, is 239 (NCDC, 2007), which is less
than other areas where Bullfrogs have been
found to have short larval periods (343 average
frost-free days in Baton Rouge, Louisana, 272
average frost-free days in Lexington, Kentucky;
NCDC, 2007). We collected Bullfrog eggs from
two different clutches at a permanent, fishless
supply pond located at the ERC on 26 May 2006,
which represents some of the earliest Bullfrog
egg masses laid in our area that season (Bury
and Whelan, 1984). The eggs were taken to the
laboratory until hatching. Eggs and tadpoles
were held at room temperature (21–22uC); after
absorption of their yolk sac, they were fed
TetraMinH Fish Flakes ad libitum until we
added tadpoles to mesocosms. The clutches
were mixed to homogenize genetic differences
before addition to mesocosms.
Sixteen mesocosm ponds (1.85 m in diameter;
1,480-liter volume) were set up outdoors at the
ERC and filled with 1,000 liters of tap water on
23 May. To each mesocosm, we added 1 kg of
leaf litter and inoculated each with a total of
three liters of plankton suspension from natural
ponds on 25, 26, 29 May and 1 June. The
mesocosms were covered with mesh lids made
of window screen to deter predators and anuran
colonists.
We added Bullfrog tadpoles to the mesocosms on 1 June (experimental day 0). The
density of animals per mesocosm was the
manipulated variable in this study. Mesocosms
were stocked with 10, 20, 40, or 80 tadpoles
(10T, 20T, 40T, and 80T hereafter) with four
replicates per treatment. Periphyton was sampled on days 14, 28, 42, 56, 84, and 112 to
determine how algal food resources were
affected by Bullfrog density. A 1.75 3 3 cm
section of each mesocosm was scraped for
periphyton below the surface of the water on
the west side of each pond. Periphyton was
placed on a glass filter and into a solution of
buffered acetone; after 24 h of refrigeration,
chlorophyll abundance of periphyton samples
was measured by fluorometry.
The water level for all of the mesocosms was
lowered to simulate the effect of a temporary
pond and to increase the likelihood of metamorphosis, if it was possible. We followed the
drying regime of a natural pond by decreasing
water depth in all ponds in increasing increments from 2–5 cm over time (as in Semlitsch,
1987; pond depth was reduced on days 71 [to
31.5 cm], 78 [to 26 cm], 85 [to 22 cm], 92 [to
17 cm], and 128 [to 12 cm]). The water level was
maintained by bailing with a bucket.
We checked the mesocosms every two days
for metamorphs, defined as the emergence of at
least one forelimb (Gosner stage 42; Gosner,
1960). These animals were caught with a net and
taken to the lab until tail resorption was
complete (#9 days, but usually 2–3 days). After
tail resorption, time to metamorphosis and mass
at metamorphosis were recorded. The mesocosms were drained on day 127 (6 October)
when weather turned cold and we were not
finding any more metamorphs. We recorded the
mass and Gosner developmental stage (Gosner,
1960) of all remaining tadpoles.
Statistical Analysis.—Pond means served as
the experimental units in all analyses. Because
individuals lose mass during metamorphic
transformation and because different endpoints
are measured for tadpoles (e.g., developmental
METAMORPHOSIS OF BULLFROGS
stage) and metamorphs (e.g., time to metamorphosis), we conducted separate analyses for
tadpoles and metamorphs. Multivariate analysis of variance (MANOVA) was used to
determine the effects of Bullfrog density on
the development and mass of tadpoles. A
separate MANOVA was used to examine effects
of Bullfrog density on mass at metamorphosis
and time to metamorphosis for Bullfrogs that
underwent metamorphosis during the study.
Analyses of variance (ANOVA) were used to
test for effects of density on proportion metamorphosing (total number of metamorphs/
number of tadpoles initially added to the pond),
absolute number of tadpoles that metamorphosed (total number of metamorphs collected
from the pond), and total survival (total number
of metamorphs plus tadpoles collected by the
end of the study/number of tadpoles initially
added to the pond). The effects of Bullfrog
density on periphyton levels were analyzed
with a repeated-measure ANOVA. We used
Scheffe’s multiple comparison tests to determine the differences within treatments (P #
0.05). To normalize data, proportion metamorphosing and total survival were angularly
transformed, time to metamorphosis and mass
of tadpoles and metamorphs were log-transformed, and tadpole stage was rank transformed.
Two mesocosms had no surviving tadpoles or
metamorphs because of an outbreak of bluegreen algae, which can be toxic (Bold and
Wynn, 1985), or because of the presence of
predatory dragonfly larvae (Werner and
McPeek, 1994), both of which were observed
in these mesocosms (one 20T and one 40T
mesocosm). Therefore, these mesocosms were
excluded from statistical analysis.
RESULTS
We collected a total of 18 metamorphs
(Fig. 1). Proportion metamorphosing was significantly different among Bullfrog density
treatments (F3,10 5 7.32, P , 0.01) with more
metamorphs emerging from lower than higher
density mesocosms (Fig. 1). However, the absolute number of tadpoles metamorphosing was
not significantly different (F3,10 5 2.30, P 5 0.14;
10T: 2.50 6 0.65; 20T: 1.67 6 0.75; 40T: 0.67 6
0.75; 80T: 0.25 6 0.65 metamorphs; Mean 6 1
SE, throughout) although more on average
metamorphosed from low-density ponds. Total
survival (including both tadpoles and metamorphs) did not differ among density treatments (F3,10 5 1.91, P 5 0.19), but on average,
survival was lowest at the greatest density (10T:
0.525 6 0.100; 20T: 0.650 6 0.116; 40T: 0.700 6
0.116; 80T: 0.366 6 0.100). The multivariate
51
FIG. 1. Proportion of Bullfrogs metamorphosing in
mesocosms across tadpole stocking densities (10, 20,
40, and 80 tadpoles per mesocosm). Error bars
represent 61 SE. Differing letters indicate significant
differences (P # 0.05) among treatments according to
Scheffe’s multiple comparison tests.
response for mass at metamorphosis and time to
metamorphosis was not significant among
Bullfrog densities (Wilks’ l 5 0.19, F6,4 5 0.86,
P 5 0.59; mass: F3,3 5 1.18, P 5 0.45; 10T: 2.067
6 0.254; 20T: 2.079 6 0.507; 40T: 1.363 6 0.507;
80T: 1.369 6 0.507 g; time: F3,3 5 2.16, P 5 0.27;
10T: 100.7 6 3.6; 20T: 102.9 6 0.5.1; 40T: 90.0 6
7.2; 80T: 93.0 6 7.2 days).
The multivariate response of mass and
developmental stage of the tadpoles was significantly affected by Bullfrog density (Wilks’ l 5
0.14, F6,16 5 4.56, P , 0.01; Fig. 2). Tadpoles had
a significantly greater mass (F3,9 5 5.34, P 5
0.02) and were significantly more developed
FIG. 2. Tadpole mass and Gosner developmental
stage among densities (10, 20, 40, and 80 tadpoles per
mesocosm) at the end of the study. Error bars
represent 61 SE. P-value represents effect of Bullfrog
density on the multivariate response of mass and
developmental stage, followed by univariate effects.
Differing letters indicate significant differences among
treatments according to Scheffe’s multiple comparison
tests.
52
S. E. PROVENZANO AND M. D. BOONE
FIG. 3. Periphyton abundance (mg/liter) in mesocosms with varying Bullfrog tadpole densities (10, 20,
40, and 80 tadpoles per mesocosm). * indicate
significant differences (P # 0.05) within treatments
at a given sampling date.
(F3,9 5 15.48, P , 0.01) when density was 10 or
20 tadpoles/mesocosm.
Periphyton abundance varied significantly
over time (Wilks’ l 5 0.13, F5,6 5 8.22, P 5
0.01) and varied marginally with Bullfrog
density over time (Wilks’ l 5 0.06, F15,17 5
2.05, P 5 0.08). Generally, although food
resources remained low in high-density mesocosms throughout the study, lower-density
mesocosms had greater amounts of periphyton
(Fig. 3). The level of periphyton in the mesocosms decreased with increasing density, particularly at experimental day 56 (F3,10 5 3.30, P
5 0.06) and day 112 (F3,10 5 10.57, P , 0.01;
Fig. 3).
DISCUSSION
Bullfrogs generally have larval periods exceeding one year, particularly in northern
climates. However, our study indicates that
Bullfrogs can reach metamorphosis across a
range of densities in a single season from
clutches laid early in the breeding season, which
suggests selection could potentially favor use of
temporary wetlands. Metamorphosis of Bullfrogs within a single season was observed in all
density treatments but was most prominent in
the lowest density treatment with an average of
25% of individuals reaching metamorphosis.
Generally, there was a greater amount of
periphyton in low-density than high-density
treatments; thus, food per individual was
greater in low-density mesocosms, allowing
some tadpoles to reach the minimum size of
metamorphosis (Wilbur and Collins, 1973;
Collins, 1979; Morey and Reznick, 2000). Interestingly, there were some individuals that
reached metamorphosis across all densities,
suggesting that a few individuals may reach
metamorphosis regardless of larval density (at
least within the range used in the present
experiment). Although studies have shown
body size decreases as population density
increases, a small number of individuals in
high-density conditions can reach the range of
body sizes found in low-density populations
(Wilbur and Collins, 1973; Wilbur, 1987). Therefore, some Bullfrogs may be able to metamorphose in a single season in both high and low
density environments, as seen in our study.
The ability to metamorphose in one season
indicates that it is possible for early hatching
Bullfrogs to metamorphose from temporary
ponds even in a northern climate like Ohio,
which may produce sustainable populations
assuming metamorphs can survive terrestrial
overwintering. Green Frogs that metamorphosed in a single season have been found to
have on average 48% survival when reared in
terrestrial enclosures (Boone, 2005), suggesting
that single-season Bullfrog metamorphosis
could maintain a population at temporary
ponds, especially given that less than 1%
survival from hatching to reproductive maturity
is needed to maintain Bullfrog populations
(Cecil and Just, 1979). Although Bullfrogs are
associated with permanent ponds (Paton and
Crouch, 2002; Babbitt et al., 2003), they are also
found in temporary ponds (Pechmann et al.,
1989, 2001; Scott et al. 2002). Longer-term
studies at temporary ponds show that Bullfrogs
will breed there yearly even if juvenile recruitment is low (Pechmann et al., 1989, 2001).
Movement and molecular data suggest Bullfrogs are highly mobile (Raney, 1940; Ingram
and Raney, 1943; Austin et al., 2004), suggesting
they can disperse across a landscape and use
wetlands that they encounter. Willis et al. (1956)
found 8% of adult Bullfrogs moved between
ponds and that recently metamorphosed frogs
may be important in dispersal to new ponds, as
at least 20 metamorphs arrived in a recently
filled pond in one week. Bullfrogs are also
frequently found in newly constructed wetlands
such as golf course ponds (Paton and Egan,
2002), suggesting high dispersal rates. With an
increase in permanent ponds on the landscape
caused by human landscape alteration (Smith et
al., 2002), Bullfrogs have an increased number
of permanent ponds to occupy, which could
lead to an increased number of Bullfrog
populations and an increased number of individual Bullfrogs on a landscape. As a result,
Bullfrogs may encounter and use temporary
ponds for larval development more frequently
than they may have in the past. Late-breeding
endemic species of temporary pond communities may be negatively affected by the presence
METAMORPHOSIS OF BULLFROGS
of Bullfrogs through competition, predation, or
spread of disease even if only one pair breeds at
the site. Indeed, even if Bullfrogs could not
metamorphose in a single season, they could
potentially alter community dynamics through
competition for food resources (Kupferberg,
1997; Adams, 2000; Kiesecker et al., 2001; Boone
et al., 2004).
Bullfrogs are often assumed to have larval
periods exceeding one year, but our study
illustrates the potential for some percent of
Bullfrogs that hatch early in the breeding season
to complete larval development in a singleseason. This flexibility suggests that Bullfrogs
can respond to conditions that indicate pond
drying and that they could successfully use
aquatic habitats that are temporary across large
portions of their range across a range of larval
densities. Because Bullfrogs have been implicated in amphibian population declines, understanding variation in their life history is
important, and our study suggests they could
successfully use temporary pond communities,
which could allow them to affect amphibian
populations in these habitats.
Acknowledgments.—We thank M. Kohrman, R.
Kolb, J. Purrenhage, E. Sams, R. Nowak, L.
Aschemeier, R. Spurling, N. Sullivan, and the
ERC staff for assistance in the field. This
research was supported by Miami University’s
Field Workshop and Committee on Faculty
Research Grant. This research was conducted
under Miami University IACUC Protocol issued
to MDB.
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Accepted: 25 May 2008.