Positive interactions among species (facilitation) enhance biodiversity and ecosystem functioning (Wright et al., 2017, 2021) while buffering communities against environmental change (Bulleri et al., 2018). Facilitation occurs when a foundation species alters the biotic or abiotic environment in a way that enhances the performance, survival, or fitness of beneficiary species (Bronstein, 2009; mechanisms reviewed by Filazzola and Lortie, 2014). Importantly, positive interactions can be species-specific because some foundation species are better facilitators than others, and not all beneficiary species are facilitated equally (Callaway, 1998). The intensity of facilitation also depends upon environmental severity. The stress-gradient hypothesis (SGH) predicts that the frequency (Bertness and Callaway, 1994) and intensity (le Roux and McGeoch, 2010) of positive interactions increase as environmental stress increases. Hundreds of studies have examined the SGH, and meta-analyses have found broad support for its basic predictions (e.g., Lortie and Callaway, 2006; He et al., 2013; Romero et al., 2015; Adams et al., 2022).

Positive interactions can also influence the trajectory of biological invasions by exotic plant species (Cavieres, 2021). Exotic species commonly facilitate each other (Braga et al., 2018), but native species also facilitate plant invasions (Northfield et al., 2018). Native facilitators can promote invasions directly by increasing the local abundance, performance, and fitness of invasive species; or indirectly by increasing the negative impacts of invasive species on neighbors. For instance, Lucero et al. (2021) showed that the invasive annual Bromus tectorum achieved much greater abundance, biomass, and fitness near native shrubs than away from shrubs; and Lortie et al. (2021) showed that invasive annual species had stronger competitive effects on native neighbors when they were facilitated than when they were not. Environmental context can mediate the strength of positive interactions experienced by invasive species (Cavieres et al., 2008; Saccone et al., 2010; Llambi et al., 2018; Filazzola et al., 2020), but we still know very little about the species-specificity of facilitated invasions.

Facilitation by desert shrubs is a useful framework for addressing these issues. Arid and semi-arid ecosystems cover over 40% of the earth’s land surface, comprise 44% of the world’s arable land, support more than 50% of the world’s livestock, and contribute substantially to global biodiversity (Millennium Ecosystem Assessment, 2005; Davies et al., 2021). However, increasing aridity associated with anthropogenic climate change and accelerating biological invasions by exotic plant species are degrading the biodiversity and functioning of desert ecosystems at an alarming rate (DiTomaso et al., 2010; Huang et al., 2016; Phillips et al., 2022). Shrubs can facilitate desert plant communities by creating favorable microsites underneath their canopies that ameliorate environmental extremes (Callaway, 2007; Michalet and Pugnaire, 2016). For instance, shade from shrub canopies can buffer understory plants against solar radiation and heat (Valiente-Benuet and Ezcurra, 1991), and soil nutrients (Schlesinger et al., 1996) and water (Segoli et al., 2012) are often more concentrated under shrub canopies than away from shrubs. Many exotic invaders capitalize on positive interactions in deserts (e.g., Butterfield et al., 2010; Badano et al., 2016; López et al., 2016; Filazzola et al., 2020; Slate et al., 2020), and sometimes to a greater extent than native competitors (Lucero et al., 2019). The SGH predicts that shrub-mediated interactions should be most positive in the most arid environments, but there remains considerable opportunity to test this relationship with multiple invasive species simultaneously (but see Holzapfel and Mahall, 1999; Brooks, 2003; Filazzola et al., 2020). Understanding of the species-specificity of facilitated invasions along aridity gradients—including indirect effects on native competitors—is necessary for explaining, predicting, and ultimately managing the ecological consequences of concomitant exotic plant invasion and environmental change in desert systems.

The objective of this study was to evaluate the potential for native shrubs to directly (by increasing the local abundance of invasive species) and indirectly (by increasing the negative impacts of invasive species on neighbors) facilitate annual plant invasions along an aridity gradient across the Mojave and San Joaquin Deserts, United States. We tested two interrelated hypotheses. First, we tested the hypothesis that the intensity of shrub-invasive annual associations depends upon invasive species identity and relative aridity. Specifically, we predicted that: (i) the intensity of shrub-invasive annual associations varies by species; and (ii) the intensity of shrub-invasive annual associations becomes more positive as relative aridity increases, as predicted by the SGH. Second, we hypothesized that association with native shrubs alters the outcome of biotic interactions (inferred via spatial relationships) between invasive annuals and herbaceous neighbors, including native and exotic species. Specifically, we predicted that abundance relationships between invasive annuals and herbaceous neighbors are more negative (i.e., more competitive) near shrubs than away from shrubs (after Lortie et al., 2021).

Invasive annuals formed species-specific associations with native shrubs (Figure 1 and Supplementary Table 2). Across sites, mean RIIs for B. rubens, B. tectorum, B. diandrus, H. murinum, and B. tournefortii ranged from 0.829 (0.043 SE; P < 0.001) to 1.000, indicating that each of these invasive species formed remarkably intense positive associations with native shrubs across our study area. In contrast, mean RII across sites for invasive annual grass Schismus spp. was −0.435 (0.195 SE; P = 0.032), indicating a negative association with shrubs across our study area. Mean RII across sites for E. cicutarium was −0.374 (0.147 SE; P = 0.061), indicating no strong associations with shrubs. Interestingly, at the site level, RIIs for B. rubens, B. tectorum, B. diandrus, H. murinum, and B. tournefortii were always positive and never fell below 0.545 (0.059 SE; P < 0.001), suggesting consistent positive associations with native shrubs at each site. At the site level, RIIs for Schismus spp. and E. cicutarium varied from −1.000 to 0.645 (1.06 SE), suggesting that their associations with shrubs were not only negative net neutral or, but also highly variable. Across sites, mean RIIs for native abundance and native species richness (all native species combined) were −0.358 (0.153 SE; P = 0.024) and −0.321 (0.132 SE; P = 0.020), respectively, suggesting that the native annual community was negatively associated with shrubs across our study area. Across sites, mean RIIs for exotic species richness (all exotic species combined) and total species richness (all species combined) were 0.014 (0.046 SE; P = 0.740) and −0.121 (0.074 SE; P = 0.101), respectively, suggesting no meaningful effect of shrubs on the species richness of the exotic or total annual community across our study area.

The intensity of shrub-annual associations was not influenced by aridity (i.e., A_dM) or shrub size (Table 1). As aridity and shrub size increased, RIIs for all vegetation measures remained constant. Thus, we found no support for the SGH. In addition, we found no evidence for aridity × shrub size interactions (Table 1).

Native shrubs altered abundance relationships between the invasive annual B. rubens and the native annual community (Figure 2 and Table 2). In shrub microsites, increasing B. rubens abundance corresponded to decreasing native abundance and native species richness, suggesting competitive interactions between B. rubens and native annuals under shrubs. In contrast, in open microsites, we found no significant relationships between B. rubens abundance and native abundance or native species richness, suggesting relatively weak interactions in the open. Increasing exotic abundance (all exotic species combined) corresponded to decreasing native abundance and native species richness in shrub microsites, but again, not in open microsites (Figure 3). These negative relationships under shrubs were apparently driven primarily by B. rubens, because removing B. rubens from the exotic abundance data eliminated all significant exotic-native relationships (Figure 4).

Shrubs also altered abundance relationships between B. rubens and the broader exotic annual community (all exotic species combined except for B. rubens) (Supplementary Figure 2 and Supplementary Table 3). In shrub microsites, increasing B. rubens abundance was negatively related to exotic abundance but had no relationship to exotic species richness. In open microsites, increasing B. rubens abundance had no relationship to exotic abundance but was positively related to exotic species richness.

Our study enriches our understanding of the species-specificity of facilitated invasions. We have long known that not all species are facilitated equally (Callaway, 1998). However, few studies have evaluated the potential for positive interactions to affect multiple invasive species simultaneously along aridity gradients. We found that spatial association with native shrubs consistently increased the abundance of some invasive annual species (B. rubens, B. tectorum, B. diandrus, H. murinum, and B. tournefortii), decreased the abundance of other invasive annuals (Schismus spp.), and had no consistent effects on another invasive annual (E. cicutarium). These findings support our hypothesis that the intensity of shrub-invasive annual associations depends strongly upon invasive species identity. Interestingly, the direction and intensity of these associations were unaffected by shrub size or relative aridity across our observed gradient. Thus, we found no support for the hypothesis that the intensity of shrub-invasive annual associations depends upon relative aridity. Additionally, we found correlative evidence (via abundance relationships) that native shrubs exacerbated the negative impacts of B. rubens on neighboring annuals. This supports the hypothesis that spatial association with native shrubs can alter the outcome of biotic interactions between invasive annuals and herbaceous neighbors. Taken together, our main findings suggest that native shrubs have considerable potential to facilitate exotic plant invasions across a broad spatial scale, but this potential may depend more upon invader identity than environmental severity. This accords with studies showing that species-specific factors can be more important than environmental conditions as drivers of nurse plant effects in drylands (Soliveres et al., 2012; Filazzola et al., 2020).

Our main findings corroborate that desert shrubs can facilitate heterospecific neighbors, including invasive annuals. Positive effects of desert shrubs on annual species include increased abundance, performance, and population growth (Callaway, 2007; Griffith, 2010). Desert shrubs and their interactions can bolster the biodiversity (Bashirzadeh et al., 2022) and functioning (Khosravi Mashizi and Sharafatmandrad, 2019) of desert ecosystems (but see Báez and Collins, 2008), but desert shrubs do not facilitate all taxa equally (Filazzola et al., 2020). In this context, our findings coincide nicely with the literature review of Abella and Smith (2013), who found that across the Mojave Desert, exotic annuals were generally more abundant near native perennials than in interspaces, suggesting overall facilitation of exotic annuals by native perennials. In particular, they found that B. rubens formed stronger positive associations with native perennials than Schismus spp. or E. cicutarium. Our findings also coincide with reports that exotic annuals respond more strongly to positive interactions than native annuals at the provenance level. In a southern California rangeland, Lucero et al. (2019) found that exotic annuals as a group were facilitated over 2.75 times stronger in abundance than native annuals, and across the Mojave and San Joaquin Deserts, Lucero et al. (2020) found that positive associations were intense and important for invasive B. rubens but not the native annual community. By promoting plant invasions (Lortie et al., 2021), intense facilitation of invasive species can indirectly erode biodiversity and ecosystem functioning (Northfield et al., 2018). Thus, any community-level benefits of shrub facilitation may backfire when invasive species are strongly facilitated. Our work extends this literature to multiple invasive taxa interacting with native shrubs across a broad geographical scale that spans substantial environmental variability.

Our study highlights the precocious ability of invasive Bromus species to capitalize on native facilitators. Native shrubs, trees, and grasses across the Great Basin, Mojave, San Joaquin, and Colorado Plateau Deserts can increase the abundance, biomass, fitness, and population growth of B. tectorum (Belnap and Sherrod, 2008; Griffith, 2010; Kane et al., 2011; Lucero et al., 2021). Across the Mojave and San Joaquin Deserts, native perennials often strongly facilitate B. rubens (reviewed by Abella and Smith, 2013). In central California, invasive B. diandrus and B. mollis can be facilitated by native Quercus douglasii (Callaway et al., 1991). In this study, each invasive Bromus species we encountered (B. rubens, B. tectorum, B. diandrus) formed intense positive associations with native shrubs, regardless of environmental context. Taken together, this literature suggests that invasive Bromus species are broadly facilitated by native plants from a variety of functional groups and environments. We suggest that disrupting positive interactions from native facilitators may be a useful strategy for controlling Bromus invasions across western North America. For instance, herbicide applications to reduce invasive Bromus densities could be most cost-effective when focused under shrub canopies. Importantly, we acknowledge that invasive Bromus species do not necessarily need native facilitators to establish (Holzapfel and Mahall, 1999; Brooks and Berry, 2006; Lucero et al., 2021) or spread (Reid et al., 2006). Rather, our findings suggest that native shrubs can aggravate Bromus invasions by increasing their local densities and impacts.

Biotic interactions do not always become more positive as aridity increases. Meta-analyses across taxa and biomes have returned broad support for the prediction derived from the SGH that positive interactions become more important as environmental severity increases (Bertness and Callaway, 1994; Lortie and Callaway, 2006; He et al., 2013; Romero et al., 2015; Adams et al., 2022). However, with respect to aridity gradients in drylands, and especially with exotic species, support for the SGH has varied (Butterfield et al., 2016; Bashirzadeh et al., 2022). For instance, Lucero et al. (2021) showed that invasive B. tectorum formed strong positive associations with native shrubs along a substantial aridity gradient across the Great Basin, Mojave, and San Joaquin Deserts, but relative aridity did not predict the intensity of these associations. Similarly, our analyses found no support for the SGH for any vegetation measure along our aridity gradient. It is possible that our gradient was too shallow to detect significant aridity-RII relationships, but our findings over a single growing season coincide with similar studies across much steeper aridity gradients (Lucero et al., 2021). We hypothesize that the intensity of shrub-invasive annual associations may not closely track aridity if invasive annuals are less limited by water than other resources, such as nutrients (Rao and Allen, 2010; Suazo et al., 2012; Bansal et al., 2014; Gill et al., 2018; see discussion below). In this context, an exciting next step would be to experimentally evaluate shrub facilitation of invasive species along multiple, interacting stress gradients.

Our findings indicate that desert shrubs can alter biotic interactions between invasive plants and their neighbors. Invasive species in deserts can inhibit native species in both shrub and open microsites (Brooks, 2000; Bishop et al., 2019), and many studies have investigated the potential for environmental factors to shift competitive outcomes (Hart and Marshall, 2013). Our study reinforces this literature by highlighting the potential for native shrubs to indirectly facilitate plant invasions by increasing the competitive impacts of invasive species (Lortie et al., 2021). We hypothesize that negative B. rubens-herbaceous neighbor relationships (evidence for competition) arose near but not away from shrubs due to relatively fertile soils near shrubs (Schlesinger et al., 1996) that ameliorated nutrient limitation and favored the performance of B. rubens over neighbors. Across the literature, nutrient enrichment almost always promotes the local dominance of invasive species (Brooks, 2003; Levine et al., 2004; Davis and Pelsor, 2008; Besaw et al., 2011). Of course, we do not discount the possibility that enhanced soil water near shrubs relative to open areas (Segoli et al., 2012) also bolstered the competitive impacts of B. rubens because water and nutrient availability act synergistically to affect plant performance (Rao and Allen, 2010; Suazo et al., 2012; Plett et al., 2020). These possibilities underscore the need to experimentally manipulate shrub-invasive annual interactions along mixed water and nutrient gradients. Importantly, this pattern arose only for B. rubens, suggesting that the risk of facilitated invasion (both directly via increased abundance and indirectly via increased impacts) is particularly high for this species across our study area. All of the invasive species we examined can negatively impact natives, but in our system, B. rubens appears to be the invader most responsible for displacing native annuals under shrubs, though experimentation is needed to confirm this.

This observational study did not test for mechanisms of species-specific facilitation, but the functional traits of our focal species may provide some clues (Funk et al., 2017). Facilitation in plant communities can arise via a number of pathways, including abiotic stress amelioration, herbivore protection, pollinator attraction, substrate modification, seed trapping, soil moisture retention, and soil nutrient enhancement (Flores and Jurado, 2003; Filazzola and Lortie, 2014). Not all shrub species are equal facilitators because not all shrub species have equal traits (McAuliffe, 1988). For instance, Larrea tridentata, the dominant shrub species across our Mojave Desert sites, can be a relatively poor facilitator compared to other shrub species due to strong competitive effects and allelopathy (reviewed by Callaway, 2007), though we found limited evidence for this. A key mechanism that determines whether shrub-neighbor interactions are positive or negative is the match between what the shrub offers and what the beneficiary species requires (Paterno et al., 2016). Importantly, the offerings and requirements of species depend upon their functional traits (Funk et al., 2017). Thus, species-specific patterns of shrub-annual associations in our study likely reflect the unique functional traits of our focal species. In this context, our three most commonly encountered invasive annual species—B. rubens, Schismus spp., and E. cicutarium—have distinct physiological characteristics. Relative to other Mojave Desert species, B. rubens uses water very rapidly, has high N uptake, and high net assimilation; Schismus spp. has thin leaves, low leaf mass per area, and low leaf N content; and E. cicutarium may be less physiologically specialized than B. rubens or Schismus spp. (DeFalco et al., 2003; Steers et al., 2011). These trait sets suggest that B. rubens can rapidly capitalize on water and nutrient additions, Schismus spp. has relatively low N requirements, and E. cicutarium may have less specialized physiological requirements than B. rubens or Schismus spp. (DeFalco et al., 2003; Steers et al., 2011). These functional trait syndromes coincide nicely with our species-specific findings: B. rubens associated strongly and consistently with shrubs, perhaps due to its ability to rapidly capitalize on shrub-mediated resource additions; Schismus spp. consistently formed negative associations with shrubs, perhaps due to its relatively low requirements for shrub-mediated nutrient additions; and E. cicutarium varied in its spatial association with shrubs, perhaps due to its intermediate or facultative requirements for shrub-mediated resources. These possibilities present exciting avenues for future experimentation.

We found a pattern consistent with invasional meltdown in open microsites. Invasional meltdown, or positive interactions among exotic species (Simberloff and Von Holle, 1999), can accelerate the transformation of communities by exotic invaders (Braga et al., 2018). In this context, we found positive relationships between B. rubens abundance and exotic species richness in open microsites across the study area. This finding closely coincides with that of Lucero et al. (2021), which reported a positive relationship between B. tectorum abundance and exotic species richness in open microsites across the Great Basin Desert. Because our findings were based on abundance relationships, it is unclear if B. rubens directly facilitated exotic species richness, or if B. rubens and the broader exotic community capitalized on similar advantageous microsites away from shrubs. Experimentation is necessary to disentangle these possibilities and explain why these patterns emerged in open, not shrub, microsites. Again, we emphasize that we only detected this pattern for B. rubens.

Along an aridity gradient across the Mojave and San Joaquin Deserts, invasive annual species formed highly species-specific associations with native shrubs that varied from positive to negative. Interestingly, the direction and intensity of these associations were unaffected by shrub size or relative aridity, and we found correlative evidence that native shrubs exacerbated the negative impacts of B. rubens (but no other invader) on neighboring annuals. We conclude that native shrubs have considerable potential to increase the abundance and impacts of invasive plant species across broad spatial scales, but this potential may depend more upon invader identity than environmental severity.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

JL, CL, RC, and AF conceived the idea. JL collected the data, analyzed the data, and wrote the manuscript. RC, CL, and AF contributed to editorial input. All authors contributed substantially to the development of this manuscript.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.