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- Supporting Information
Facilitation, that is, the positive effects of one organism on others, is a common interaction among co-occurring plants (Callaway, 2007). Over the last two decades, important progress has been made in the understanding of the mechanisms of facilitation and its context dependence (Brooker et al., 2008). Most facilitative effects consist of the amelioration of abiotically and biotically stressful conditions in ways that benefit other species (Stachowicz, 2001). Facilitative effects can consist of relief from physical stress (Bertness & Hacker, 1994; Callaway, 1994; Bruno, 2000), resource supply which can be either direct (nutrients, Turkington & Harper, 1979; water, Caldwell et al., 1998) or indirect (nutrients, van der Heijden & Horton, 2009; water, Pugnaire et al., 1996a), protection from herbivores (Smit & Ruifrok, 2011; Louthan et al., 2014) or pollinator attraction (Reid & Lortie, 2012). All of these mechanisms of facilitation share a common result in which one species ameliorates the limiting environmental conditions of another species, thereby creating improved or even newly suitable environmental conditions at fine scales in an otherwise less suitable or unsuitable habitat (Bruno et al., 2003; Schöb et al., 2012; McIntire & Fajardo, 2014). Although facilitative processes occur at fine spatial scales, they can have important ecological consequences from local to global scales. Facilitative effects can increase species richness (Pugnaire et al., 1996a; Michalet et al., 2006; Cavieres et al., 2014), conserve phylogenetic diversity (Valiente-Banuet et al., 2006; Butterfield et al., 2013), drive natural selection (Michalet et al., 2011), and improve ecosystem services (Mulder et al., 2001; Li et al., 2007; Badano & Marquet, 2009).
We know a great deal about the mechanisms and context dependence of facilitative effects of benefactors on beneficiaries (Callaway, 2007), but our understanding of how facilitated (beneficiary) species feed back to benefactors is limited. Recent studies have shown that the close co-occurrence of benefactor and beneficiary species can induce a feedback effect of the beneficiary on the benefactor (hereafter called the beneficiary feedback effect (BFE); Supporting Information Fig. S1). BFEs can be positive (Pugnaire et al., 1996b), resulting in a mutualism, but generally the effect has been shown to be negative, that is, resulting in an antagonistic interaction, for example facultative parasitism (McAuliffe, 1984, 1988; Valiente-Banuet et al., 1991; Flores-Martínez et al., 1994; Holzapfel & Mahall, 1999; Michalet et al., 2011; Cranston et al., 2012; Schöb et al., 2014a,b). However, compared with the better known co-occurring negative effects of competitive interactions (Keddy, 2001), we are just beginning to understand the mechanisms underlying reciprocal feedbacks that are associated with positive effects. In particular, from studies in arid environments, we know that direct feedback effects from beneficiaries to benefactors occur, and that they probably involve competition for resources (Valiente-Banuet et al., 1991; Holzapfel & Mahall, 1999; Schöb et al., 2014a). However, we do not know if these BFEs are context-dependent, such as competitive and facilitative interactions in general (Bertness & Callaway, 1994; He et al., 2013) and, if so, whether they are related to the facilitative effect of the benefactor on the beneficiary, whether these effects depend on the composition of the beneficiary community, or if they are modulated by changing environmental conditions. Therefore, a quantitative analysis of the context dependence of feedbacks between benefactors and beneficiaries will contribute substantially to understanding how relationships among these species evolve, are sustained over generations, or wane in intensity over time.
Recent reports indicate that the frequency, intensity and importance of facilitative effects of benefactors on beneficiaries are context-dependent (He et al., 2013; Le Bagousse-Pinguet et al., 2014). For instance, the interaction can change during ontogeny from facilitative at early life history stages of the beneficiary species to competitive at later stages (Miriti, 2006; Sthultz et al., 2007; Armas & Pugnaire, 2009; Soliveres et al., 2010; le Roux et al., 2013). Facilitation can also vary among functional groups of species, with competitive species benefiting more from stress amelioration than stress-tolerant species (Liancourt et al., 2005; Maestre et al., 2009; Forey et al., 2010). Similarly, the facilitative effects may also depend on the tolerance of the particular prevailing stress by the benefactor and the ability of the benefactor to ameliorate this stress (Michalet et al., 2014). For example, for cushion plants it has been shown that the cushion morphology can change along environmental gradients, including changes in the traits involved in facilitation, with significant consequences for the facilitation effect (Michalet et al., 2011; Schöb et al., 2013). Furthermore, facilitative effects are generally more intense in stressful environments, where high levels of stress or disturbance limit plant growth in the absence of biotic habitat amelioration (Bertness & Callaway, 1994; Brooker & Callaghan, 1998; He et al., 2013). In addition, simultaneously co-occurring stress gradients can result in complex changes in plant interaction intensity (Mod et al., 2014).
As with facilitative effects, BFEs may be context-dependent, but to our knowledge this has hardly been explored. BFEs vary with changes in species richness of the beneficiary community, indicating that the feedback effect is dependent on the number and identity of the species that cause the BFE (Schöb et al., 2014b). This may be attributable to diversity effects such as niche partitioning, facilitation or sampling effects in which taxonomically and phylogenetically more diverse beneficiary species assemblages have stronger effects (Flynn et al., 2011). Furthermore, it may depend on limiting niche similarity effects, in which interactions of species sharing more similar niches with the benefactor are more competitive (MacArthur & Levins, 1967; Adler et al., 2012). These ideas have not been directly addressed, even though the corresponding phylogenetic pattern, that is, a higher phylogenetic distance between beneficiaries and benefactors than expected by chance, has been described (Castillo et al., 2010; Valiente-Banuet & Verdú, 2013). Furthermore, we know that, when two interacting species compete for the same resource, the effect of one species on the other is directly linked to the feedback effect of the latter species on the former (Keddy, 2001). If there was a similar direct link between the facilitative effect and the feedback effect between a benefactor and a beneficiary, the intensity of the BFE would increase with increasing intensity of the facilitative effect. Surprisingly, and to our knowledge only very recently, has this facilitation–BFE link started to be explored (Schöb et al., 2014a) and, despite a wealth of understanding of how competitive and facilitative interactions change with environmental conditions (Grime, 1977; Bertness & Callaway, 1994), we are not aware of any study assessing the response of BFE to environmental severity gradients.
The limited understanding of the context dependence of BFEs calls for large-scale studies where we can relate properties of the beneficiary community and variability in environmental conditions to BFE. To this end, we re-analysed a global data set on alpine cushion plants (Butterfield et al., 2013; Cavieres et al., 2014; Schöb et al., 2014b). This data set was used previously to assess the impact of cushion plants on phylogenetic and taxonomic diversity and community composition along global-scale environmental gradients (Butterfield et al., 2013; Cavieres et al., 2014), and to assess the fitness consequences of the benefactor cushions acting as facilitators (Schöb et al., 2014b). Whereas the former studies demonstrated the context dependence of facilitative effects, the latter study showed that cushion plants experience reduced flowering and reproductive output with increasing abundance of beneficiaries, indicating a predominating negative BFE in cushions. Here, we combined aspects of all three studies by investigating the context dependence of the BFEs. In other words, we determined the sign and strength of BFEs on alpine cushion plants based on flower density of cushions and assessed the dependence of BFEs on beneficiary community composition, the strength of the facilitative effects of cushions, and local-scale biotic and climatic habitat conditions using structural equation modelling. We hypothesized that the strength and direction of BFEs would be related to the composition of the beneficiary community. We expected that those beneficiary communities consisting of species more closely related to their benefactor cushion species would have stronger negative feedback effects than communities of species distantly related to their benefactor. We further hypothesized a relationship between facilitation intensity and BFE. On the one hand, we expected that stronger facilitation (e.g. larger plants) would directly increase negative BFEs. On the other hand, we expected that the intensity of facilitation would indirectly modulate the BFE if it affects the diversity and composition of the beneficiary community. Finally, we hypothesized a relationship between the local-scale environmental conditions and BFE. We expected that more favourable local-scale environmental conditions would directly reduce facilitation and increase beneficiary community diversity, and therefore indirectly modulate the BFE.
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Overall, the feedback effect of beneficiary species (BFE) on their cushion benefactor was mostly negative, although this was highly context-dependent. This was shown by both the manipulative and descriptive approaches as the BFE varied among sites and ranged from significantly negative to significantly positive. In other words, the feedback effect on benefactors ranged from a cost to a benefit, depending on the environmental context. Our results provided support for our first hypothesis suggesting that the diversity of the beneficiary community alters feedback effects (see also Michalet et al., 2011; Schöb et al., 2014b). However, our results also indicate that higher phylogenetic diversity per se makes the BFE on cushion benefactors less negative, whereas higher species richness per se makes BFEs more negative. In contrast to our expectations, the phylogenetic similarity of the beneficiary community to the cushion did not affect the BFE of cushion benefactors in either manipulative or descriptive approaches. As hypothesized, the intensity of the facilitative effect of the benefactors was an additional driver of the BFE, even though in the manipulative approach this link was only indirect and weak. The descriptive approach suggests that stronger facilitation intensity corresponded with a more negative BFE, indicating the presence of a direct link between facilitation intensity and the corresponding BFE.
All of these community-level patterns and processes of beneficiary diversity and facilitation were modulated by the environmental conditions of sites, such as the available species pool, site productivity and climatic conditions. Overall metrics of better growth conditions at a site (i.e. larger species pool, higher site productivity and higher summer precipitation) indirectly induced more negative BFEs but direct positive effects of these conditions on the BFE overrode the indirect negative effects. This resulted in overall less negative or more positive feedback effects of beneficiaries on benefactors in generally less stressful or more productive abiotic and biotic conditions. Consequently, similar to competitive or facilitative effects (Michalet et al., 2014), BFEs are dependent on a variety of conditions ranging from the characteristics of the interacting beneficiary community to environmental conditions at the site where the interaction takes place.
The impact of beneficiary community composition on BFE
The impact of the beneficiary community on benefactor cushions is probably related to the sign and strength of the direct plant–plant interactions, such as resource-related competition, facilitation and niche complementarity effects. By controlling for covariation between species richness and phylogenetic diversity of the beneficiary community we demonstrated that some of the variance in the BFE was uniquely explained by either species richness or phylogenetic diversity. Based on this, the interplay between the positive effect of phylogenetic diversity and the negative effect of species richness on BFE suggests that a species-rich community of closely related species imposed significant costs in terms of reduced flower production by the benefactor cushion. By contrast, more phylogenetically diverse but species-poor assemblages reduced this cost because of reverse facilitation effects of beneficiaries on the benefactor, or via increased niche complementarity. These diversity effects of beneficiaries on benefactors might shift at other stages of reproduction (e.g. fruiting), though Schöb et al. (2014a,b) showed that the significant reduction in flower production attributable to BFEs is unlikely to be compensated for by BFEs on later stages of reproduction, and therefore flower production serves as a good indicator of the final reproductive output of cushion plants.
The unique phylogenetic diversity component may indicate niche complementarity or sampling effects that may positively feed back to the benefactor. Such a relationship between phylogenetic diversity and niche complementary has been demonstrated in experimental grassland communities, where high phylogenetic diversity increased community-level productivity (Flynn et al., 2011). They also showed that phylogenetic diversity was at least partially related to functional diversity, as proposed by the phylogenetic niche conservatism hypothesis (Ackerly, 2003). Therefore, a more phylogenetically diverse beneficiary community probably provides more trait variation and therefore increases the probability of harbouring species with facilitative effects (e.g. legumes). By contrast, a phylogenetically clumped but species-rich beneficiary community probably has a reduced potential for these positive feedback effects because of a high probability of occurrence of species sharing similar traits and strategies for resource uptake. This could cause strong negative effects on the benefactor if this group of closely related beneficiary species shared much of the niche occupied by the benefactor cushion (MacArthur & Levins, 1967). However, the nonsignificant relationship between the phylogenetic distance of the beneficiary community to the benefactor cushion, on the one hand, and the strength of the beneficiary feedback effect, on the other hand, shows that this phylogenetic signal of limiting niche similarity was not evident in our studied ecosystem. The negative species richness effect may result, therefore, from the overall negative impact (e.g. competition for resources) of a specific phylogenetic group of common beneficiary species that are not particularly close relatives of the cushion benefactor, for example grasses. However, further research is needed to explore the feedback effects of specific functional groups of beneficiary species.
The impact of facilitation on BFE
The indirect effects of facilitation on the BFE through cushion effects on species richness and phylogenetic diversity were weak. This may seem surprising given that a number of studies have shown increased diversity of species within cushions compared with open areas (e.g. Cavieres et al., 2002; Michalet et al., 2011; Schöb et al., 2012). However, previously published studies from this global initiative on facilitation by alpine cushion plants detected positive effects of cushions on site-level phylogenetic diversity and species richness (Butterfield et al., 2013; Cavieres et al., 2014), where the higher plant diversity of sites with cushions was mainly attributable to different species inhabiting the cushion and open microhabitats, respectively, rather than a higher diversity within the cushion microhabitat (Butterfield et al., 2013). This could explain the lack of a significant relationship between facilitation and beneficiary community diversity within cushions in our global experimental design.
In contrast to the weak indirect effects of facilitation, we found quite strong direct effects of facilitation on the BFE in the descriptive approach: stronger facilitation resulted in more negative BFEs. This suggests that there is indeed a direct link between the facilitative effect of the cushion benefactor and the feedback effect from the beneficiary. From studies in dry environments we know that one of the mechanisms of facilitation by cushions is increasing soil moisture and therefore improving water availability in cushions (Cavieres et al., 2006; Schöb et al., 2012, 2014a). Similarly, the negative feedback effect of beneficiary species on cushions was related to the competitive water uptake of species growing within cushions, thereby deteriorating the water status of the cushion (Schöb et al., 2014a). Consequently, the link between facilitation and its feedback effect may occur if the two components of the bidirectional interaction function through the same resource, similar to competition (Keddy, 2001). However, many facilitative effects may not be mechanistically related to the BFE and this may in turn be responsible for the relatively weak direct effect of facilitation on the BFE in our study. Many facilitative effects include shelter from herbivory or other attenuation of physical disturbances (e.g. stabilization of substrate or protection from strong winds) that are difficult to link to a similar mechanism of feedback effect of beneficiary species on the benefactor.
The impact of environmental conditions on BFE
Factors that function at the scale of regions such as climate, productivity, and species pool modulated both facilitation intensity and the diversity of the cushion-associated plant assemblage, and thus had indirect effects on BFEs. The species pool in open areas was strongly related to both facilitation intensity and beneficiary community diversity, where sites with larger species pools corresponded to weaker intensity of facilitation by cushions and higher species richness and phylogenetic diversity of the beneficiary community. Similarly, higher site-level productivity was also associated with higher beneficiary community diversity. These relationships correspond well with previous research showing reduced facilitation intensity in species-rich alpine communities, such as in tropical mountains (Anthelme et al., 2012), and reduced facilitation intensity together with species-rich communities in sites with high productivity and large species pools (Cavieres et al., 2014). These effects of local productivity and species pool on the species and phylogenetic diversity of the beneficiary community and facilitation increased negative BFEs and therefore the cost of facilitation.
The negative indirect effects of the local biotic and abiotic conditions on the BFE were, however, overcompensated by their positive direct effects on the BFE. In particular, more summer precipitation, higher productivity, and larger species pools corresponded to less negative or even positive BFEs. This suggests that the cushions of milder sites experienced a reduced cost simply as a result of the better growing conditions. This resembles some aspects of interactions of parasitic plants with their hosts, in which increasing ecosystem productivity correlates with reduced parasite impact on the host (Fibich et al., 2010). We suggest that improved growth conditions via increased resource supply or decreased abiotic stress allow benefactors to better tolerate beneficiaries, that is, the feedback effect becomes less important for the benefactor (sensu Kikvidze et al., 2011).
A global data set on alpine cushion plants has previously shown the important positive effects of cushion plants for alpine biodiversity (Butterfield et al., 2013; Cavieres et al., 2014). As a consequence of this facilitation effect, cushions were shown to suffer from reduced fitness for being cooperative (Schöb et al., 2014b). Here we confirm that the community-level feedback effects of beneficiaries on benefactors were mostly negative, but were strongly context-dependent. The BFEs depended on the diversity and composition of the beneficiary community. Most clearly, more species-rich beneficiary communities increase negative feedback effects on cushion fitness. Apart from these community-level properties that directly affect the intensity of plant–plant interactions between beneficiaries and benefactors, local-scale environmental conditions also modulate these direct effects of beneficiaries. Under more benign environmental conditions, negative BFEs caused by the beneficiary community appear to be less important for the benefactor than under stressful conditions. Interestingly, this impact of the environmental conditions on the intensity of BFEs was of the same order of magnitude as (if the BFE is based on beneficiary cover) or even stronger than (if the BFE is based on the number of beneficiary individuals) the direct impact of the beneficiary community composition on the BFE (Table 1). This suggests a resource-driven nature of BFEs in which the intensity of competitive effects of the beneficiary community depends on their composition, and where these competitive effects are particularly important for the benefactor under resource-poor conditions. Our results therefore demonstrate strong context dependence of the feedback effects of beneficiary species on the nurse, similar to the two decades of work that have shown the effects of nurse plants on beneficiaries being highly context-dependent (Bertness & Callaway, 1994; He et al., 2013). The sort of conditionality we demonstrate here for the generally negative beneficiary feedback effects, if played out over multiple years at a single site, suggests that the BFE is unlikely to be strong enough to have dramatically altered the evolutionary trajectory of the benefactors in this case, perhaps explaining why species with cushion growth forms continue to provide exceptional examples of convergent evolution despite attracting large numbers of other species to reside upon them and embed in them.