The fine line between mutualism and parasitism: complex effects in a cleaning symbiosis demonstrated by multiple field experiments
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Ecological theory and observational evidence suggest that symbiotic interactions such as cleaning symbioses can shift from mutualism to parasitism. However, field experimental evidence documenting these shifts has never been reported for a cleaning symbiosis. Here, we demonstrate shifts in a freshwater cleaning symbiosis in a system involving crayfish and branchiobdellid annelids. Branchiobdellids have been shown to benefit their hosts under some conditions by cleaning material from host crayfish’s gill filaments. The system is uniquely suited as an experimental model for symbiosis due to ease of manipulation and ubiquity of the organisms. In three field experiments, we manipulated densities of worms on host crayfish and measured host growth in field enclosures. In all cases, the experiments revealed shifts from mutualism to parasitism: host crayfish growth was highest at intermediate densities of branchiobdellid symbionts, while high symbiont densities led to growth that was lower or not significantly different from 0-worm controls. Growth responses were consistent even though the three experiments involved different crayfish and worm species and were performed at different locations. Results also closely conformed to a previous laboratory experiment using the same system. The mechanism for these shifts appears to be that branchiobdellids switched from cleaning host gills at intermediate densities of worms to consuming host gill tissue at high densities. These outcomes clearly demonstrate shifts along a symbiosis continuum with the maximum benefits to the host at intermediate symbiont densities. At high symbiont densities, benefits to the host disappear, and there is some evidence for a weak parasitism. These are the first field experimental results to demonstrate such shifts in a cleaning symbiosis.
KeywordsSymbiosis Mutualism Parasitism Context dependence Cleaning behavior
We are grateful to Katie Greene, Brett Tornwall, Laura Ammons, Josh Lomonaco, David Young, Adam Speake, Ryan Hassler, Travis Knott, Chelsae Weithman, Patty Whitener, John Brunt, Jon Boroughs, Tim Torongeau, Matt Sanderson, and Brandon Carpenter for help with the experiments. We thank everyone at Boone Ironworks for help in designing and building the cages. Funding for this research was provided by the National Science Foundation (DEB-0949823 to R.P.C. and DEB-0949780 to B.L.B.), a Research Development Award to R.P.C. from the Graduate School at Appalachian State University, and by funds from Clemson University’s University Research Grant Committee to B.L.B. Discussions with Jeff Butts and comments on previous versions on the manuscript by Robert Baldwin, Mathew Turnbull, Julie Ryan and two anonymous reviewers were helpful and greatly appreciated.
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