ET&C Spotlight—Consider the Litter: Amphibian Toxicity and the Effect of Natural Organic Matter
Brian Church, Windward Environmental LLC
Two articles recently published in Environmental Toxicology and Chemistry present results from two investigations with amphibians and leaf litter, a particularly important component of natural aquatic systems. The effect that leaf litter can have on a community is well understood, as it comprises a major source of nutrients in the freshwater environment. But litter is not as simple as that, clearly, as it now appears that the composition of riparian vegetation can both cause and mitigate toxicity in frog species.
Is all litter created equal? Obviously not, according to Earl et al. (2012), who studied the direct impact of different tree and grass litter on the survival and development two chorus frog (Pseudacris maculata and Pseudacris crucifer) tadpoles. Dried leaf litter from non-native white pine, native and dominant red oak, and prairie cordgrass were finely ground and added to purified water to steep like tea, similar to what occurs in a natural setting as the chemicals inside dead leaves slowly leach into lakes and streams. This leachate often contains essential nutrients, but it can also contain toxic phytochemicals. These chemicals (e.g., tannins, monoterpenes) act as natural pest deterrents in the source plant (Roth and Lindroth, 1994 as cited in Earl et al., 2012) and have been observed to cause gill damage in fish and reduced dietary protein availability (Temmink et al. 1989; Larcher 2001 both cited in Earl et al. 2012).
In toxicity tests that used the leaf litter leachate, the authors found that the non-native white pine extract was much more acutely toxic than those from the other plants, and all tadpoles died within 3 days of exposure. White pine is known to contain higher concentrations of monterpenes, which the authors suspect may be causing increased toxicity. Red oak, which is naturally high in tannins, caused a similar decline in time to death. Of the few tadpoles that survived in the red oak test, none was able to metamorphose by the end of the 60 days.
The grass extract was not different than the control in respect to the aforementioned endpoints (i.e., nearly all survived to metamorphosis and at the same time), but was found to have a positive effect on tadpole mass at metamorphosis and body condition, each expected to result in a better chance of survival as a juvenile.
Enticed by their findings of the relative toxicity of white pine extract to chorus frogs, the authors followed up with a second test, using only the white pine extract but with tadpoles of two other species: Hyla versicolor and Bufo americanus. Both tadpole species died within 4 hours of being exposed to white pine extract, whereas all survived in the control. The confounding implication that naturally occurring leaf litter may cause toxicity, an effect that would have previously gone unnoticed, could have toxicologists fixing their gaze upward on the riparian canopy instead into the water.
Now that you are scared of toxic leaf litter, consider the results presented by Boone and Sullivan (2012) that indicated quite the opposite, at least in a way. They studied the effect of leaf litter mass inputs on the toxicity of carbaryl, a carbamate insecticide, to green frog (Rana clamitans) tadpoles. In previous studies, many insecticides have been shown to have a direct negative impact on amphibians (i.e., behavioral, sublethal, and acute toxicity) (Relyea 2005; Boone 2008; Relyea 2009 all as cited in Boone and Sullivan 2012). However, this is contrary to the expected result, as hypothesized by the authors.
The study utilized mesocosm test ponds that allowed for community-level responses to controlled environmental changes. This was integral to testing the authors’ somewhat counterintuitive hypothesis, that altering the mass of leaf litter, in the presence of co-varying carbaryl, would actually have a positive effect on tadpole growth and survival. That is to say that as leaf litter and carbaryl increase, toxicity will decrease! This hypothesis is based on the assumption that a “trophic cascade” will occur in the presence of high nutrients that leach from the leaf litter, and concentrations of carbaryl that are toxic to some species. The principle is simple enough: removal of a top predator alters the abundance of species occupying other levels within a food web. For example, if a predator of grazing species is removed from a system, then grazers increase in abundance (for a time) and primary producers likely decrease.
As hypothesized, it was observed in multiple experimental ponds that significant increases in tadpole development and survival occurred where there was more leaf litter and higher concentrations of carbaryl. Furthermore, the two factors were not always interactive; treatments with 1.75 mg carbaryl/L significantly increased survival and development compared to control treatments with no carbaryl. This indicates that carbaryl has a positive direct effect on R. clamitans when measuring the observed endpoints. But that is no reason to pour carbaryl in ponds. On the contrary, the authors make it clear that the effective increase in frog survival and development is an effect of indirect toxicity within the system that maybe altering the abundance of food for the tadpoles; the positive effect ceases to occur when nutrients decrease. In fact, there was no response or a negative response to carbaryl exposure when leaf litter mass was very low.
The positive effect of carbaryl in a natural system may not be long-lasting. As time progressed in the study (from one week to 35 days), environmental conditions worsened, such that dissolved oxygen (DO) decreased and the periphyton community decreased slightly in relative abundance. A rapid decrease in DO was also observed by Earl et al. (2012) after adding leaf leachate and is likely a result of increased biological and chemical oxygen demands in nutrient-enriched systems. The small decline in the periphyton community could be a result of many factors, one being the increased rate of consumption by larger tadpoles. The change may also be a result of fluctuating temperature, decreasing pH, increased nutrient load from leaf litter (evidenced by the current study as dissolved organic carbon), and/or chemical toxicity, either due to phytochemicals (as indicated by Earl et al. 2012) or the insecticide, carbaryl.
It is important to note that the expected trophic cascade described above was not clearly deducible from the results. Periphyton relative abundance changed only slightly and it was not clear what alterations within the mesocosm food web contributed to the increased survival, growth, and development in R. clamitans. Green frogs are constant and opportunistic feeders (Jenssen 1967), such that they may have been feeding on organisms other than the periphyton.
Both studies taken together do not give us a clear picture of effects of leaf litter on an aquatic ecosystem. The type of vegetation can cause acute toxicity, and the mass of vegetation that becomes litter can mitigate toxicity. In either case, leaf litter deserves greater focus, as it is not quite the innocuous ingredient we once took it to be.
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