Trait-mediated indirect effects in a natural tidepool system

Background/Question/Methods

In classic trophic cascades, predators eat prey and indirectly benefit primary producers. However, predators can also benefit primary producers by causing prey to graze less or use refuges, termed a trait-mediated indirect interaction (TMII). Though many studies have demonstrated the importance of TMIIs, most lack realism and may inaccurately estimate TMII strength because they separate focal species from the surrounding community, span short time periods, or artificially constrain organisms by using mesocosms or cages. We examined a tri-trophic TMII where small predatory seastars (Leptasterias sp.) eat herbivorous snails (Chlorostoma funebralis), which eat both microalgae and macroalgae in rocky intertidal tidepools in northern California. TMIIs are likely the primary mechanism of the cascade because predation by seastars is low: waterborne seastar cues quickly scare many more snails than can be eaten, snail avoidance responses are long lasting, and larger snails cannot be eaten. We first determined if seastar and snail densities were associated with algal community structure in 63 tidepools. We then manipulated seastar and snail presence without caging in 37 tidepools over 10 months to test if seastars cause snails to shift habitats over multiple time scales (days to months) and exert TMIIs on naturally growing microalgae and macroalgae.

Results/Conclusions

We provide one of the first studies to demonstrate TMIIs in a natural community without impeding the movements or behaviors of organisms. Seastars caused snails to quickly flee tidepools and caused immigrating snails to select refuge habitats outside tidepools. Snails continued to avoid seastars for at least 10 months, and this resulted in positive TMIIs on naturally growing microalgae over 1 month and macroalgae over 8 months. Densities of Leptasterias and Chlorostoma were also negatively associated in 63 unmanipulated tidepools, and the two species were associated with differing algal communities even after statistically considering other key abiotic and biotic factors. The strongest TMIIs occurred when experiments mimicked a natural predator invasion, whereas the weakest TMIIs but strongest behavioral responses occurred when prey were added to tidepools containing seastars, highlighting the importance of using realistic predator-prey encounters when studying TMIIs. Overall, our results suggest that Leptasterias may have effects on algal community structure by changing Chlorostoma herbivory. We show that TMIIs occur over long time periods even in natural, complex communities where the movements and behaviors of all species are unconstrained.