Comparative impacts of aboveground and belowground enemies on an invasive thistle.

Ecol Evol. 2018 Feb; 8(3): 1430–1440. Published online 2017 Dec 27. doi: 10.1002/ece3.3751 PMCID: PMC5792520 PMID: 29435222 Comparative impacts of aboveground and belowground enemies on an invasive thistle Krystal A. Nunes 1 and Peter M. Kotanen 1 Krystal A. Nunes 1 Department of Ecology and Evolutionary Biology, University of Toronto Mississauga, Mississauga, ON, Canada, Find articles by Krystal A. Nunes Peter M. Kotanen 1 Department of Ecology and Evolutionary Biology, University of Toronto Mississauga, Mississauga, ON, Canada, Find articles by Peter M. Kotanen Author information Article notes Copyright and License information Disclaimer 1 Department of Ecology and Evolutionary Biology, University of Toronto Mississauga, Mississauga, ON, Canada, Krystal A. Nunes, Email: . Corresponding author. *Correspondence Krystal A. Nunes, Department of Ecology and Evolutionary Biology, University of Toronto Mississauga, Mississauga, ON, Canada. Email: , Received 2017 Oct 10; Revised 2017 Nov 4; Accepted 2017 Nov 26. Copyright © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Associated DataSupplementary Materials   ECE3-8-1430-s001.docx (1.0M) GUID: EE09597B-BB6B-4AA1-ABE8-83F6AB6CCFFE Data Availability Statement Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.d24pj Abstract Most research examining how herbivores and pathogens affect performance of invasive plants focuses on aboveground interactions. Although important, the role of belowground communities remains poorly understood, and the relative impact of aboveground and belowground interactions is still debated. As well, most studies of belowground interactions have been carried out in controlled environments, so little is known about the role of these interactions under natural conditions or how these relationships may change across a plant's range. Using the invasive plant Cirsium arvense, we performed a reciprocal transplant experiment to test the relative impacts of above‐ and belowground interactions at three sites across a 509‐km latitudinal gradient in its invaded range in Ontario, Canada. At each site, C. arvense seedlings were protected with above‐ and/or belowground exclosures in a factorial design. Plant performance (biomass, height, stem thickness, number of leaves, length of longest leaf, maximum rhizome length) was greatest when both above‐ and belowground exclosures were applied and lowest when no exclosures were applied. When only one type of exclosure was applied, biomass generally improved more with belowground exclosures than with aboveground exclosures. Despite site‐to‐site differences in foliar damage, root damage, and mesofaunal populations, belowground interactions generally had a greater negative impact on performance than aboveground herbivory alone. These results stress the importance of including both aboveground enemy interactions and plant–soil interactions in studies of plant community dynamics and invader performance. Keywords: aboveground interactions, Cirsium arvense, common garden, herbivory, invasive species, plant–herbivore interactions, plant–soil (belowground) interactions, soil mesofauna 1. INTRODUCTION Interactions with natural enemies can potentially have important consequences for the success or failure of invasions by non‐native plants (Elton, 1958; Keane & Crawley, 2002; Torchin & Mitchell, 2004). However, most research investigating the effect of herbivores and pathogens on plant performance focuses on aboveground interactions, despite a growing consensus that belowground interactions may be very important (Dawson, Schrama, & Austin, 2016; van der Putten, Vet, Harvey, & Wackers, 2001), often having a greater impact on plant performance than aboveground damage (Barber, Adler, & Bernardo, 2011). It has been well established that plants heavily attacked by aboveground enemies often show reduced growth and fecundity (e.g., Ang, Kok, Holtzman, & Wolf, 1995; Bacher & Schwab, 2000), but belowground antagonists may also impact plant fitness and survival directly by damaging root tissue (Barber et al., 2011; Maron, 1998; Strong et al., 1995) or indirectly by changing interactions with other organisms (Hol, Raaijmakers, Mons, Meyer, & van Dam, 2016; Soler et al., 2012; Wardle, 2002). For instance, root herbivory can reduce flowering and thus rates of pollinator visitation (Barber et al., 2011), and can alter attack by aboveground herbivores through induction of leaf chemical defenses (Bezemer, Wagenaar, van Dam, & Wackers, 2003). Belowground communities also harbor many plant mutualists, such as mycorrhizal fungi, and indirectly beneficial organisms such as detritivores and decomposers. As a result, net effects of the soil community may be positive, negative, or neutral (Ehrenfeld, Ravit, & Elgersma, 2005). Finally, as aboveground and belowground interactions may act independently or may interact to affect plant performance (Johnson, Mitchell, McNicol, Thompson, & Karley, 2013; Wardle, 2002), understanding their simultaneous effects on a potentially invasive host is a difficult task. A review by Wardle et al. (2004) found that depending on the system, aboveground herbivores can have variable effects on soil organisms through plant–mediated interactions; both positive and negative effects were possible outcomes. Aboveground herbivores may positively impact soil organisms by promoting compensatory growth in the host plant, or by adding nutrients to the soil via frass. Alternatively, negative impacts may occur if defenses are induced in belowground tissues, if host plant productivity is reduced due to low herbivore tolerance, or through selection for unpalatable plants over time. These differing results may be due to the high context dependency of patterns in aboveground–belowground linkages (Johnson et al., 2012). Measurements of relative impacts of aboveground and belowground organisms can depend on the design of the study. In particular, whether a laboratory or field study is conducted can greatly affect results (Heinze, Sitte, Schindhelm, Wright, & Joshi, 2016; Johnson et al., 2012). However, most studies on aboveground–belowground interactions have been carried out in highly controlled environments (Bezemer, Graca, Rousseau, & van der Putten, 2004; Bezemer et al., 2003; Engelkes et al., 2008; Friedli & Bacher, 2001; Gange & Brown, 1989; Kostenko, van de Voorde, Mulder, van der Putten, & Martijn Bezemer, 2012; Masters & Brown, 1992; Moran & Whitman, 1990), and so little is known about these relationships under true field conditions. In one exception, Maron (1998) explored aboveground–belowground interactions in the field by suppressing herbivores on stand (...truncated)