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Contemporary Evolution of Plant Growth Rate Following Experimental Removal of Herbivores. Author(S): Nash E The University of Chicago Contemporary Evolution of Plant Growth Rate Following Experimental Removal of Herbivores. Author(s): Nash E. Turley, Walter C. Odell, Hanno Schaefer, Georg Everwand, Michael J. Crawley, and Marc T. J. Johnson Source: The American Naturalist, Vol. 181, No. S1, A Critical Look at Reciprocity in Ecology and Evolution (May 2013), pp. S21-S34 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/10.1086/668075 . Accessed: 22/04/2013 11:40 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press, The American Society of Naturalists, The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org This content downloaded from 142.150.9.14 on Mon, 22 Apr 2013 11:40:30 AM All use subject to JSTOR Terms and Conditions vol. 181, supplement the american naturalist may 2013 Symposium Contemporary Evolution of Plant Growth Rate Following Experimental Removal of Herbivores Nash E. Turley,1,* Walter C. Odell,2 Hanno Schaefer,3 Georg Everwand,4 Michael J. Crawley,5 and Marc T. J. Johnson1 1. Department of Biology, University of Toronto, 3359 Mississauga Road, Mississauga, Ontario L5L 1C6, Canada.; 2. Department of Plant Biology, North Carolina State University, Raleigh, North Carolina 27695; 3. Biodiversita¨t der Pflanzen, Technische Universita¨t Mu¨nchen, Maximus-von-Imhof Forum 2, 85354 Freising, Germany; 4. Georg-August-University Go¨ttingen, Department of Crop Sciences, Agroecology, Grisebachstrasse 6, 37077 Go¨ttingen, Germany; 5. Department of Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom Online enhancement: appendix. Dryad data: http://dx.doi.org/10.5061/dryad.cp00b. defense traits observed among plants (Fraenkel 1959; Ehr- abstract: Herbivores are credited with driving the evolutionary lich and Raven 1964; Becerra 1997; Agrawal 2007; Walters diversification of plant defensive strategies over macroevolutionary time. For this to be true, herbivores must also cause short-term 2011). Plant defenses are often classified as either resistance evolution within plant populations, but few studies have experi- traits or tolerance traits, where the former reduce herbi- mentally tested this prediction. We addressed this gap using a long- vore damage and the latter limit the negative fitness con- term manipulative field experiment where exclosures protected 22 sequences of damage (Karban and Baldwin 1997; Strauss plant populations from natural rabbit herbivory for !1to26years. and Agrawal 1999). For herbivores to drive the evolution We collected seeds of Rumex acetosa L. (Polygonaceae) from our of plant defenses over macroevolutionary timescales, they plots and grew them in a common greenhouse environment to quan- must also drive the evolution of defenses over micro- tify evolved differences among populations in individual plant growth rate, tolerance to herbivory, competitive ability, and the concentra- evolutionary timescales (one to hundreds of generations). tion of secondary metabolites (tannins and oxalate) implicated in Numerous studies show that the ingredients necessary for defense against herbivores. In 26 years without rabbit herbivory, plant this short-term adaptive evolution are ubiquitous: plants growth rate decreased linearly by 30%. We argue that plant growth contain heritable variation for both resistance and toler- rate has evolved as a defense against intense rabbit herbivory. In ance (Berenbaum et al. 1986; Maddox and Root 1987; contrast, we found no change in tolerance to herbivory or concen- Nu´n˜ez-Farfa´n et al. 2007), and herbivores impose selection trations of secondary metabolites. We also found no change in com- petitive ability, suggesting that contemporary evolution may not feed on these traits (Rausher and Simms 1989; Marquis 1992; back to alter ecological interactions within this plant community. Stinchcombe et al. 2002; Agrawal 2005). Despite these im- Our results combined with those of other studies show that the portant results, few studies have explicitly linked the pres- evolution of gross morphological traits such as growth rate in re- ence or absence of herbivores to actual evolutionary re- sponse to herbivory may be common, which calls into question sponses within plant populations, and these studies are assumptions about some of the most popular theories of plant typically observational (Zangerl and Berenbaum 2005; defense. Stenberg et al. 2006). Thus, our understanding of which Keywords: community genetics, eco-evolutionary interactions, her- plant traits will evolve due to the direct or indirect con- bivory, plant competition, plant defenses, Rumex acetosa. sequences of herbivory are limited. This represents a large gap in our understanding of the evolutionary ecology of plant-herbivore interactions (Agrawal 2011; Johnson Introduction 2011). Herbivores have fed on plants for more than 400 million Several observational studies provide strong evidence years (Labandeira 2007), and these interactions are be- that natural selection imposed by the presence or absence lieved to have driven the diversification of the myriad of herbivores drives the microevolution of plant defensive traits. Both Stenberg et al. (2006) and Zangerl and Ber- * Corresponding author; e-mail: [email protected]. enbaum (2005) found a positive correlation between her- Am. Nat. 2013. Vol. 181, pp. S21–S34. ᭧ 2013 by The University of Chicago. bivory pressure and the level of plant defenses among plant 0003-0147/2013/181S1-53415$15.00. All rights reserved. populations, suggesting that the absence of herbivores DOI: 10.1086/668075 drives the evolution of decreased defenses and the presence This content downloaded from 142.150.9.14 on Mon, 22 Apr 2013 11:40:30 AM All use subject to JSTOR Terms and Conditions S22 The American Naturalist of herbivores drives the evolution of increased defenses. gland are an excellent setting to test the evolutionary im- Lennartsson (1997) found similar results with respect to pacts of herbivores. In this system, rabbits crop plants tolerance to herbivory. The results from these observa- closely to the ground, which prevents flowering and causes tional studies are consistent with the prediction that the individual plants to be much smaller than when rabbits presence and absence of herbivores can impose natural are absent (fig. 1). On average, grazing directly reduces selection on plant defense traits that cause evolutionary average plant height in communities by 56% p p change over tens to hundreds of years. However, these (ungrazed mean18 cm, grazed mean 8 cm) and standing p results are not sufficient to conclusively implicate a role aboveground biomass by 25% (ungrazed mean 80 g, p 2 of herbivores in driving evolution as recent theory shows grazed mean 60 g dry weight per 0.125 m ; M. J. Crawley, that such correlations based on observational data can unpublished data). Excluding rabbit herbivores also has result from multiple evolutionary processes, including cascading effects on net primary productivity (measured those that do not involve selection from biotic agents as total aboveground biomass produced in a growing sea- (Nuismer et al. 2010). son) and nutrient availability in soil, which increase by Herbivores can drive the evolution of plant traits ∼60% and ∼180%, respectively, following 14 years of rab- through the direct effects of consumption and through bit exclusion (Olofsson et al. 2007). Furthermore, rabbits any indirect effects of herbivory that modify the abiotic alter the composition of plant communities over time due or biotic environment (Miller and Travis 1996; Agrawal et to the direct effects of grazing and indirect effects mediated al. 2006). This is especially true for interactions between through competitors (Farrow 1917; Watt 1962; Crawley plants and grazing vertebrate herbivores, which have large 1990). Specifically, some species (e.g., Holcus lanatus, Se- impacts on plant community structure and are in many necio jacobaea, and Trifolium repens) increase in relative ways fundamentally different from those involving ar- abundance and other species (e.g., Achillea millefolium, thropods (McNaughton 1984; Pollard 1992; Edwards and Vicia sativa, and Festuca rubra) decrease in relative abun- Crawley 1999). Grazing can impose selection directly on dance in the presence of rabbit grazing (Crawley 2005). traits, such as plant palatability, morphology, and growth Experimental evidence suggests that increasing species are rate (McNaughton 1984), but also indirectly, for example, faster growing and more tolerant to repeated damage than by influencing nutrient availability or by altering com- decreasing species (Del-Val and Crawley 2005a). A third petitive hierarchies among plant species (Crawley 1983; class of species (e.g., Rumex acetosa, Stellaria graminea, Agrawal et al. 2006). Thus, predicting what traits will and Veronica chamaedrys) does not significantly change in evolve in response to the presence or absence of herbivores
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