Facilitation in communities: underlying mechanisms, community and ecosystem implications

Facilitation (positive interactions among organisms) in communities has been the subject of increasing interest for community ecologists since the mid-nineties (Fig. 1), although this is a pioneer core concept in community theory, proposed a 100 years before this issue by Clements (1916), as the main driving biotic mechanism of plant community succession. However, it was neglected by most community ecologists for decades due to the overwhelming popularity at that time of the individualistic (Gleason 1926; Whittaker 1956) and competition theories (Grime 1974; Tilman 1982). Until the mid-nineties, competition was by far the most studied biotic interaction, in particular by plant community ecologists (see Fig. 1: more than 90% of the biotic interactions studies published at that time concerned only competition). However, due to the increasing evidence of facilitation in experiments conducted in severe conditions from marine intertidal and terrestrial environments, Bertness & Callaway (1994) proposed a conceptual model where competition switches to facilitation with increasing environmental severity. Since then, and during the following two decades, the interest in facilitation has never ceased to increase (see Fig. 1: currently only 76% of the biotic interactions studies concerns only competition). During the first half of this period of emergence of facilitation as an important research area, a number of conceptual studies evidenced the multiple community and ecosystem implications of facilitation (Callaway 1995, 1997, 1998; Pugnaire, Haase & Puigdef abregas 1996; Callaway & Walker 1997; Hacker & Gaines 1997; Holmgren, Scheffer & Huston 1997; Brooker & Callaghan 1998; Stachowicz 2001; Bruno, Stachowicz & Bertness 2003; Lortie et al. 2004; Armas & Pugnaire 2005; Brooker 2006; Padilla & Pugnaire 2006), and many empirical studies focused on the experimental test of the pioneer model of Bertness & Callaway (1994) (e.g. Pugnaire & Luque 2001; Callaway et al. 2002; but see Callaway 2007 and Brooker et al. 2008 for reviews). Facilitation became during this period a well-established phenomenon. However, a strong controversy questioned in 2005 the importance of facilitation in dry environments and, thus, the validity of the Stress Gradient Hypothesis (Maestre, Valladares & Reynolds 2005; Michalet 2006, 2007; Maestre et al. 2009; but see Lortie & Callaway 2006; Armas, Rodr ıguez-Echeverr ıa & Pugnaire 2011). This controversy was followed by the publication of other alternative models to the SGH, proposing a collapse of facilitation in extremely stressful conditions (Michalet et al. 2006, 2014a; Xiao et al. 2009; Holmgren & Scheffer 2010; Verwijmeren et al. 2013; Le Bagousse-Pinguet et al. 2014a). At this time of important conceptual refinement, a European Science Foundation meeting was held in Arcachon (France) in 2006, the conclusions of which were collected in a highly cited publication (Brooker et al. 2008; see Fig. 1). Brooker et al. (2008) also highlighted several key issues for developing future facilitation studies which were the main basis of a BES symposium organized in 2009 in Aberdeen and the subsequent special issue in the Journal of Ecology (Brooker & Callaway 2009; see Fig. 1). The main goal of the BES symposium and special issue was to open facilitation research to new directions, and to actively develop conceptual links with other research fields from which research on facilitation would profit, such as evolutionary ecology, restoration ecology and marine sciences. Since then, the field has moved incredibly fast (Fig. 1). There have been many important and novel recent advances, such as the assessment of the evolutionary consequences of facilitation (e.g. Michalet et al. 2011; Thorpe et al. 2011; Butterfield et al. 2013), the feedback effects between facilitator and facilitated species (e.g. Sch€ ob et al. 2014a,b,c), the functional consequences of facilitation (e.g. Sch€ ob, Butterfield & Pugnaire 2012; Butterfield & Callaway 2013; Sch€ ob et al. 2013) or the interactions with below-ground organisms (e.g. Hortal et al. 2013; Rodr ıguez-Echeverr ıa et al. 2013). Several meta-analyses and theoretical studies have further analysed the relevance of the SGH with contrasting results or conclusions (He, Bertness & Altieri 2013; He & Bertness 2014; Michalet et al. 2014a,b; Soliveres & Maestre 2014; Soliveres, Smit & Maestre 2015; and see Armas, Rodr ıguez-Echeverr ıa & Pugnaire 2011; Pugnaire et al. 2015). However, as *Correspondence author. E-mail: r.michalet@ecologie.ubordeaux1. fr