Trait-mediated indirect effects in a natural tidepool system
We demonstrate an apparent trait-mediated indirect interaction (TMII) of predators on primary producers in a natural community by altering prey behavior over short and long time scales. Small predatory sea stars (Leptasterias spp.) caused herbivorous snails (Tegula funebralis) added to rocky intertidal tidepools to quickly flee into refuge microhabitats outside tidepools within days, and this was associated with a 58% increase in microalgal growth after 2 weeks. Similarly, removing sea stars caused snails to increase use of tidepools for 1–10 months. After adding sea stars to tidepools, snails quickly fled and then consistently increased use of refuges outside tidepools for 10 months. This was associated with average increases of 59% for microalgal growth over 1 month and 254% for macroalgal growth over 8 months inside tidepools. In 63 unmanipulated tidepools, densities of sea stars and snails were negatively correlated. High densities of snails were associated with unpalatable algal species and bare rock, while high densities of sea stars were associated with palatable algal species, suggesting that this apparent TMII may have community-level impacts. Though multiple lines of evidence suggest TMIIs were likely operating in this system, it was not possible to experimentally partition the relative contributions of TMIIs and density-mediated indirect interactions (DMIIs), so further caging experiments are necessary to distinguish their relative strengths. Overall, we suggest that predators can benefit primary producers by changing prey behavior even when predators and prey are unrestrained by cages or mesocosms, embedded in complex communities, and observed over multiple time scales.
For assistance in the field and laboratory, thanks to Sarah Traiger, Olivia Turnross, Aiko Michot, Alex von Boer, Jonathan Demmer, Ryanne Ardisana, Amy Fonarow, Andrew Chen, Preston Malm, and Mimi Gravem. Thanks to Blake Brown, Sarah Hameed, and Erin Satterthwaite for support. Thanks to Drs. Seth Miller, Mark Novak, Susan Williams, Andy Sih, Eric Sanford, Brian Gaylord, Jarrett Byrnes, Ben Dalziel and our anonymous reviewers for providing constructive comments on experimental design and/or the manuscript. This is a contribution of Bodega Marine Laboratory and dedicated to the memory of Dr. Susan Williams, whose many direct and indirect effects are intense, profound, and will be long-lasting.
SG and SM conceived the project idea. SG collected and analyzed the data and was the primary author. SM provided constant guidance and edited the manuscript.
This study was funded by California SeaGrants R/FISH218, R/MPA14 and R/MPA24 awarded to Steven Morgan, National Science Foundation Grants OCE-1334448 and OCE-0927196 awarded to Steven Morgan, National Science Foundation GK-12 Grant 0841297 awarded to Susan Williams, the Conchologists of America, the Mildred E. Mathias Foundation, Henry A. Jastro fellowship, the UC Davis Graduate Group in Ecology, and the Bodega Marine Laboratory Fellowship.
Compliance with ethical standards
Conflict of interest
The authors declare no conflicts of interest.
All procedures performed in studies involving. animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. All collections and manipulations of animals in the study were in compliance with the California Department of Fish and Game collecting permit SC-4688 to Steven Morgan and approved by the University of California Natural Reserve System.
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