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q 2003 by the Ecological Society of America
Abstract. Amphibians are declining globally, and biologists have struggled to identify
the causes. Pesticides may play a role in these declines, but pesticide concentrations in
nature often are low and considered sublethal. Past research has found that the globally
common pesticide carbaryl can become more lethal under different environmental conditions including differences in temperature and competition. A recent study has found that
predatory stress, a situation common for most amphibians, can make carbaryl 24 times
more deadly to gray tree frogs (Hyla versicolor). To determine whether this is a general
phenomenon in amphibians, I examined how carbaryl affected the survival of six amphibian
species in the presence and absence of predatory stress. Higher concentrations of carbaryl
caused higher mortality. In two of the six species, carbaryl became even more lethal when
combined with predatory stress (up to 46 times more lethal). This suggests that apparently
safe concentrations of carbaryl (and perhaps other pesticides with similar modes of action)
can become more deadly to some amphibian species when combined with predator cues.
Key words: amphibian decline; Bufo americanus; Hyla versicolor; pesticide concentrations;
phenotypic plasticity; predation; Rana catesbeiana; Rana clamitans; Rana pipiens; Rana sylvatica;
synergy.
experimental context. For example, the insecticide carbaryl (1-naphthyl N-methylcarbamate, commercial
name: Sevin; Rhone-Poulenc, Research Triangle Park,
North Carolina, USA) can become more lethal to aquatic animals under warmer temperatures (Lohner and
Fisher 1990, Boone and Bridges 1999; but see Bridges
and Boone [2003]) and more or less lethal when combined with competitive interactions from other species
(Boone and Semlitsch 2001, 2002). A recent study
found that carbaryl also becomes more lethal to gray
tree frog tadpoles (Hyla versicolor) when combined
with the chemical cues emitted by predators (Relyea
and Mills 2001). This discovery was important because
most habitats contain predators, so most amphibians
that experience pesticides will simultaneously experience predatory stress (Kats and Dill 1998, Relyea and
Werner 1999, Relyea 2001). However, the combination
of carbaryl and predatory stress has only been examined in one species. In this study, I took a more broadly
comparative approach and tested for the synergistic
effects between carbaryl and predatory stress using six
species of amphibians from three taxonomic families
(wood frogs, Rana sylvatica; leopard frogs, R. pipiens;
green frogs, R. clamitans; bullfrogs, R. catesbeiana;
American toads, Bufo americanus; and gray tree frogs).
While these species are not experiencing declines in
the eastern United States, they do span a wide geographic and taxonomic range and therefore can serve
to assess the general lethality of carbaryl and the prevalence of synergistic interactions with predatory stress.
METHODS
To examine the interactive effects of predator cues
and carbaryl, I reared six species of tadpoles in separate
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INTRODUCTION
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Ecological Applications
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TABLE 1. ANOVA results (P values) from the analyses of how six species of larval amphibians (in six separate experiments)
survived under six concentrations of the pesticide carbaryl crossed with the presence or absence of predator cues over
time in studies conducted at the University of Pittsburghs Pymatuning Laboratory of Ecology.
Species
Wood
frogs
Leopard
frogs
American
toads
Gray tree
frogs
Green
frogs
Bullfrogs
Block
Carbaryl
Predator
Predator 3 carbaryl
Time
Time 3 block
Time 3 carbaryl
Time 3 predator
Time 3 carbaryl 3 predator
0.040
,0.001
,0.001
0.464
1.000
0.090
,0.001
0.224
,0.001
0.263
,0.001
0.812
0.146
1.000
0.688
,0.001
0.706
,0.001
0.202
,0.001
0.009
0.938
1.000
0.091
,0.001
0.036
0.204
0.900
,0.001
0.748
0.564
1.000
0.194
,0.001
0.171
0.826
0.487
,0.001
,0.001
,0.001
1.000
0.943
,0.001
0.157
,0.001
0.325
,0.001
,0.001
0.005
1.000
0.196
,0.001
,0.001
,0.001
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L. Mortality was always .50% with predator cues present; thus the LC50 value with predator cues was not
estimated.
In leopard frogs, there were significant effects of
carbaryl and a significant time-by-carbaryl interaction
(Table 1, Fig. 1). The highest concentrations of carbaryl
(6.53.2 mg/L) killed 100% and 90% of the animals,
respectively. At 1.6 mg/L survival improved to 89%,
but this was still lower than the control (P 5 0.001).
At lower concentrations of carbaryl (0.30.03 mg/L),
leopard frog mortality was low and not different from
the control (P . 0.08). There also was a time-by-carbarylby-predator interaction; predator cues improved survival
at 6.5 mg/L of carbaryl midway through the experiment,
but they had no effect at the other concentrations. This
favorable synergy at 6.5 mg/L rapidly declined over time
as all of the animals eventually died. The LC50 value
across predator treatments was 2.2 mg/L.
In toads, there were significant effects of carbaryl
and predators as well as a time-by-carbaryl and a timeby-predator interaction (Table 1, Fig. 1). At the highest
carbaryl concentration (6.5 mg/L), 95% of the toads
died after 16 d. Midway through the experiment at this
concentration, however, it was clear that predator cues
Communications
FIG. 1. The survival of six tadpole species after being exposed to a factorial combination of predator cues (absent, open
symbols; present, closed symbols) crossed with four concentrations of the pesticide carbaryl. For space consideration, the
lowest concentrations of carbaryl are not shown (0.03 mg/L) because this concentrations had little effect on the survival in
any of the species. Data are means 6 1 SE.
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