Relyea, RA. 2003. Predator cues and pesticides: a double dose of danger for amphibians. Ecological Applications 13 (6): 1515-1521.
Amphibian populations around the world have been in decline for at least the past fifteen years. Several theories have been advanced to explain the losses, including a spreading fungal disease, increased UV exposure, habitat loss, predation by introduced species and chemical contamination.
In this study, Relyea shows that even low, environmentally-relevant levels of a pesticide can cause high levels of tadpole mortality, and that mortality rates can be much higher when the tadpoles are stressed simultaneously by proximity to a natural predator. In one of the 6 species he studied, predator cues made tadpoles up to 46 times more likely to die when exposed to carbaryl.
Relyea's findings are important not just for the insights they provide into factors affecting amphibian populations. None of the current toxicity testing protocols used by the Environmental Protection Agency consider interactions among simultaneous stress factors. His results thus draw into question the validity of toxicity testing used to develop health standards when the experiments focus on one stress at a time.
What did Relyea do?
Relyea collected 6 species of tadpoles as newly oviposited eggs and hatched them in the absence of predators. He then exposed populations of 10 tadpoles each to varying concentrations of Sevin, a commercial form of the pesticide carbaryl, using levels relevant to those found in the environment.
Half of the populations at each exposure level were in the presence of a caged red-spotted newt, a predator shared by all of the species tested. The newt could not reach the tadpoles because it was held within a screened cage within the tadpoles' container. The newt was fed tadpoles of the same species as in the current experiment to generate olfactory cues of its presence.
Each of the 12 treatment combinations was replicated four times. The exposure lasted 16 days, a relatively long time for experiments of this type.Relyea also measured levels of ammonia (due to waste) and oxygen (due to respiration) to determine whether abiotic conditions were affected by the presence of a predator.
What did he find?
The highest concentration of carbaryl caused high mortality rates in all species studied.
This can be seen in the graphs to the left (two species shown); the highest concentrations are in the uppermost panels. The graphs plot tadpole survival over the 16 days of each experiment. The green plot shows survival of tadpoles absent the predator, whereas the black plot is for tadpoles with a predator nearby.
In the mid-range concentrations (most evident at 1.6 mg/L), survival when the predator was absent was quite high, but with the predator present it was quite low. In fact for bullfrogs, by the 16th day survival with the newt present was 46-times lower than when it was absent.
For two of the other species (Leopard Frogs and American Toads; not shown) even low levels of carbaryl killed most of the tadpoles. Neither Wood Frogs nor Grey Tree Frogs showed an interaction between pesticide and predator effects.
Relyea observed some changes in abiotic factors related to the presence of the predator. Specifically, he reported a significant reduction in dissolved oxygen levels for toads and leopard frogs as well as a 14% reduction in ammonia for toads. Relyea notes that these changes are unlikely to have contributed to tadpole mortality as conditions were still well within ranges observed naturally.
What does it mean?
These experiment demonstrate that predatory stress dramatically increases the lethality of carbaryl in three of six amphibian species tested.
Carbaryl levels have been found in natural field conditions up to 4.8 mg/L, above levels at which the carbaryl-predator risk interaction induced high mortality rates in these experiments. In fact carbaryl is one of the most widely used pesticides, applied to over 100 crop species, in forests, rangelands and the ocean, as well as used in tens of millions of homes and gardens in the US. These results thus suggest that this pesticide could be contributing significantly to amphibian declines in many areas. Because carbaryl's mechanism of action (inhibition of acetylcholine esterase) is shared with a wide range of carbamate and organophosphate pesticides, the synergistic interaction between the carbaryl and predator-induced stress may be relevant to other pesticides as well.
According to Relyea: “When we include some of the natural ecology, even low concentrations of a pesticide can be highly lethal to amphibians… Ignoring the relevant ecology can cause incorrect estimates of a pesticides’ lethality in nature, yet it is the lethality of pesticides under natural conditions that is of utmost interest. The accumulating evidence suggests that pesticides in nature could be playing a role in the decline of amphibians.”
Relyea's results also indicate that in tests to establish health standards for pesticide exposures, more attention must be paid to interactions among stress factors. The highly controlled environment in which toxicological experiments are normally conducted may be leading to gross underestimates of the true impacts of exposure, as it is experienced in the real world.