Putative linkages between below- and aboveground mutualisms during alien plant invasions

Putative linkages between below- and aboveground mutualisms during alien plant invasions Susana Rodrı́guez-Echeverrı́a 1* and Anna Traveset2 1 2 CFE-Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, 3000-456 Coimbra, Portugal. Mediterranean Institute of Advanced Studies (CSIC-UIB), C/Miquel Marqués 21, E07190 Esporles, Mallorca, Spain. Received: 1 August 2014; Accepted: 20 May 2015; Published: 1 June 2015 Associate Editor: Inderjit Citation: Rodrı́guez-Echeverrı́a S, Traveset A. 2015. Putative linkages between below- and aboveground mutualisms during alien plant invasions. AoB PLANTS 7: plv062; doi:10.1093/aobpla/plv062 Abstract. Evidence of the fundamental role of below – aboveground links in controlling ecosystem processes is mostly based on studies done with soil herbivores or mutualists and aboveground herbivores. Much less is known about the links between belowground and aboveground mutualisms, which have been studied separately for decades. It has not been until recently that these mutualisms—mycorrhizas and legume – rhizobia on one hand, and pollinators and seed dispersers on the other hand—have been found to influence each other, with potential ecological and evolutionary consequences. Here we review the mechanisms that may link these two-level mutualisms, mostly reported for native plant species, and make predictions about their relevance during alien plant invasions. We propose that alien plants establishing effective mutualisms with belowground microbes might improve their reproductive success through positive interactions between those mutualists and pollinators and seed dispersers. On the other hand, changes in the abundance and diversity of soil mutualists induced by invasion can also interfere with below– aboveground links for native plant species. We conclude that further research on this topic is needed in the field of invasion ecology as it can provide interesting clues on synergistic interactions and invasional meltdowns during alien plant invasions. Keywords: Community dynamics; invasion; mutualism; mycorrhiza; pollination; rhizobia; seed dispersal; symbiosis. Introduction Interactions and feedbacks between belowground and aboveground subsystems play a fundamental role in regulating community structure and ecosystem functioning (e.g. Bever et al. 1997, 2010, 2012; Wardle et al. 2004; Kulmatiski et al. 2008; Bardgett and Wardle 2010; Bezemer et al. 2013; Fukami and Nakajima 2013; Kardol et al. 2013; Van der Putten et al. 2013; Bardgett and van der Putten 2014). However, studies examining below – aboveground interactions have focussed mainly on belowand aboveground herbivores (e.g. Moran and Whitham 1990; Bezemer and van Dam 2005; Ruijven et al. 2005; Mckenzie et al. 2013; de la Peña and Bonte 2014) or, to a lesser extent, on belowground mutualists and aboveground herbivores (e.g. Gehring and Whitham 1994, 2002; Gange et al. 2002; Kempel et al. 2009; Koricheva Invited Review SPECIAL ISSUE: The Role of Below-Ground Processes in Mediating Plant Invasions * Corresponding author’s e-mail address: Published by Oxford University Press on behalf of the Annals of Botany Company. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015 1 Rodrı́guez-Echeverrı́a and Traveset — Mutualisms during plant invasions Below- and Aboveground Plant Mutualisms Regarding mutualistic soil microorganisms, we will focus on mycorrhizas (associations between soil fungi and roots of vascular plants) and rhizobia (a- or b-Proteobacteria engaged in symbiosis with legumes). Mycorrhizas occur in more than 90 % of the examined plant families (Brundrett 2009), and at least in a third of the world’s most widespread invasive woody species (Traveset and 2 AoB PLANTS www.aobplants.oxfordjournals.org Richardson 2014). The two main types of mycorrhizas are arbuscular mycorrhizas, occurring in 80 % of plant families, from grasslands to tropical forests; and ectomycorrhizas, dominating woodlands and forests in boreal, Mediterranean and temperate areas (Brundrett 2009; Barea et al. 2011). The legume – rhizobia symbiosis, on the other hand, is prevalent in most terrestrial ecosystems, occurring in 80 % of legumes, and is responsible for over 90 % of the biologically fixed nitrogen entering into terrestrial ecosystems worldwide (Sprent 2001). Both types of belowground mutualisms are crucial for the uptake of nutrients and water by plants, and, as such, can play an important role in determining the structure and dynamic of terrestrial ecosystems (e.g. Wall and Moore 1999; van der Heijden 2002; van der Heijden et al. 2006; Klironomos et al. 2011). However, the degree of dependency on soil mutualisms varies for different plant species and the net benefit for the plant can also change depending on the plant species, mycorrhizal type and biotic conditions (Johnson et al. 1997; Pringle et al. 2009b; Hoeksema et al. 2010; Thrall et al. 2011). Nonetheless, most of these studies have been done using inoculation experiments in the greenhouse and this could not reflect the real outcome of these mutualisms in the field (Hoeksema et al. 2010). Aboveground, we will be centred on the most conspicuous mutualisms involving plants, viz. pollination and seed dispersal. These mutualisms are directly associated with the reproduction of plant species and, thus, with their ability to establish self-replacing populations. Therefore, these two types of mutualisms are crucial to understand the spatial structure and demographic processes of populations and communities (Bond 1994). Although wind pollination is common among monocots, biotic pollination is an essential ecosystem service as .90 % of flowering plants are pollinated by animals (Ollerton et al. 2011) and 75 % of the world’s main food crops are obligate out-crossers (Klein et al. 2007). Animals also disperse up to 90 and 60 % of plant species in tropical and temperate regions, respectively (Farwig and Berens 2012), and their service provides a way to escape from competing siblings and natural enemies around parent plants at the same time that facilitates the colonization of vacant recruitment sites. Moreover, such service helps in maintaining genetic diversity and drives adaptation of plants to changing environments (Traveset et al. 2013). Most flowering and fleshy-fruited plants rely on generalist pollinators/ dispersers, i.e. animals that pollinate/disperse a wide range of plants (Ollerton et al. 2011; Farwig and Berens 2012; Traveset et al. 2013). This indeed facilitates the integration of alien plants and alien pollinators/dispersers into the native pollination/disperser networks (Stouffer et al. 2014; Traveset and Richardso (...truncated)