PLANT COMPETITION IN A CHANGING WORLD EDITED BY : Judy Simon and Susanne Schmidt PUBLISHED IN : Frontiers in Plant Science 1 June 2017 | Plant C ompetition in a C hanging World Frontiers in Plant Science Frontiers Copyright Statement © Copyright 2007-2017 Frontiers Media SA. All rights reserved. All content included on this site, such as text, graphics, logos, button icons, images, video/audio clips, downloads, data compilations and software, is the property of or is licensed to Frontiers Media SA (“Frontiers”) or its licensees and/or subcontractors. The copyright in the text of individual articles is the property of their respective authors, subject to a license granted to Frontiers. The compilation of articles constituting this e-book, wherever published, as well as the compilation of all other content on this site, is the exclusive property of Frontiers. For the conditions for downloading and copying of e-books from Frontiers’ website, please see the Terms for Website Use. 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ISSN 1664-8714 ISBN 978-2-88945-205-7 DOI 10.3389/978-2-88945-205-7 About Frontiers Frontiers is more than just an open-access publisher of scholarly articles: it is a pioneering approach to the world of academia, radically improving the way scholarly research is managed. The grand vision of Frontiers is a world where all people have an equal opportunity to seek, share and generate knowledge. Frontiers provides immediate and permanent online open access to all its publications, but this alone is not enough to realize our grand goals. Frontiers Journal Series The Frontiers Journal Series is a multi-tier and interdisciplinary set of open-access, online journals, promising a paradigm shift from the current review, selection and dissemination processes in academic publishing. All Frontiers journals are driven by researchers for researchers; therefore, they constitute a service to the scholarly community. 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What are Frontiers Research Topics? Frontiers Research Topics are very popular trademarks of the Frontiers Journals Series: they are collections of at least ten articles, all centered on a particular subject. With their unique mix of varied contributions from Original Research to Review Articles, Frontiers Research Topics unify the most influential researchers, the latest key findings and historical advances in a hot research area! Find out more on how to host your own Frontiers Research Topic or contribute to one as an author by contacting the Frontiers Editorial Office: researchtopics@frontiersin.org 2 June 2017 | Plant C ompetition in a C hanging World Frontiers in Plant Science PLANT COMPETITION IN A CHANGING WORLD Topic Editors: Judy Simon, University of Konstanz, Germany Susanne Schmidt, University of Queensland, Australia Competitiveness describes a key ability important for plants to grow and survive abiotic and biotic stresses. Under optimal, but particularly under non-optimal conditions, plants compete for resources including nutrients, light, water, space, pollinators and other. Competition occurs above- and belowground. In resource-poor habitats, competition is generally considered to be more pronounced than in resource-rich habitats. Although competition occurs between different players within an ecosystem such as between plants and soil microorganisms, our topic focusses on plant-plant interactions and includes inter-specific competition between different species of similar and different life forms and intra-specific competition. Strategies for securing resources via spatial or temporal separation and different resource needs generally reduce competition. Increasingly important is the effect of invasive plants and sub- sequent decline in biodiversity and ecosystem function. Current knowledge and future climate predictions suggest that in some situations competition will be intensified with occurrence of increased abiotic (e.g. water and nutrient limitations) and biotic stresses (e.g. mass outbreak of insects), but competition might also decrease in situations where plant productivity and survival declines (e.g. habitats with degraded soils). Changing interactions, climate change and biological invasions place new challenges on ecosys- tems. Understanding processes and mechanisms that underlie the interactions between plants and environmental factors will aid predictions and intervention. There is much need to develop strategies to secure ecosystem services via primary productivity and to prevent the continued loss of biodiversity. This Research Topic provides an up-to-date account of knowledge on plant-plant interactions with a focus on identifying the mechanisms underpinning competitive ability. The Research Topic aims to showcase knowledge that links ecological relevance with physiological processes to better understanding plant and ecosystem function. Citation: Simon, J., Schmidt, S., eds. (2017). Plant Competition in a Changing World. Lausanne: Frontiers Media. doi: 10.3389/978-2-88945-205-7 3 June 2017 | Plant C ompetition in a C hanging World Frontiers in Plant Science Table of Contents 05 Editorial: Plant Competition in a Changing World Judy Simon and Susanne Schmidt Section 1: Facilitation 08 Facilitation among plants in alpine environments in the face of climate change Fabien Anthelme, Lohengrin A. Cavieres and Olivier Dangles 23 Species coexistence in a changing world Fernando Valladares, Cristina C. Bastias, Oscar Godoy, Elena Granda and Adrián Escudero Section 2: Competition 39 Abiotic and biotic controls on local spatial distribution and performance of Boechera stricta Kusum J. Naithani, Brent E. Ewers, Jonathan D. Adelman and David H. Siemens 50 Stimulating seedling growth in early stages of secondary forest succession: a modeling approach to guide tree liberation Marijke van Kuijk, Niels P . R. Anten, Roelof J. Oomen and Feike Schieving 63 Across a macro-ecological gradient forest competition is strongest at the most productive sites Lynda D. Prior and David M. J. S. Bowman 75 Diverse urban plantings managed with sufficient resource availability can increase plant productivity and arthropod diversity Jonathon N. Muller, Susan Loh, Ligia Braggion, Stephen Cameron and Jennifer L. Firn 85 Competition for nitrogen between Fagus sylvatica and Acer pseudoplatanus seedlings depends on soil nitrogen availability Xiuyuan Li, Heinz Rennenberg and Judy Simon 96 Metabolomics differentiation of canola genotypes: toward an understanding of canola allelochemicals M. Asaduzzaman, James E. Pratley, Min An, David J. Luckett and Deirdre Lemerle Section 3: Plant invasions 105 Resource competition in plant invasions: emerging patterns and research needs Margherita Gioria and Bruce A. Osborne 126 Overcoming barriers to seedling regeneration during forest restoration on tropical pasture land and the potential value of woody weeds Amelia T. Elgar, Kylie Freebody, Catherine L. Pohlman, Luke P . Shoo and Carla P . Catterall 4 June 2017 | Plant C ompetition in a C hanging World Frontiers in Plant Science 136 Resource-use efficiency explains grassy weed invasion in a low-resource savanna in north Australia Emilie Ens, Lindsay B. Hutley, Natalie A. Rossiter-Rachor, Michael M. Douglas and Samantha A. Setterfield 146 Herbaceous plant species invading natural areas tend to have stronger adaptive root foraging than other naturalized species Lidewij H. Keser, Eric J. W. Visser, Wayne Dawson, Yao-Bin Song, Fei-Hai Yu, Markus Fischer, Ming Dong and Mark van Kleunen EDITORIAL published: 26 April 2017 doi: 10.3389/fpls.2017.00651 Frontiers in Plant Science | www.frontiersin.org April 2017 | Volume 8 | Article 651 | Edited and reviewed by: Francisco I. Pugnaire, Consejo Superior de Investigaciones Científicas (CSIC), Spain *Correspondence: Judy Simon judy.simon@uni-konstanz.de Specialty section: This article was submitted to Functional Plant Ecology, a section of the journal Frontiers in Plant Science Received: 07 March 2017 Accepted: 10 April 2017 Published: 26 April 2017 Citation: Simon J and Schmidt S (2017) Editorial: Plant Competition in a Changing World. Front. Plant Sci. 8:651. doi: 10.3389/fpls.2017.00651 Editorial: Plant Competition in a Changing World Judy Simon 1 * and Susanne Schmidt 2 1 Ecology Group, Department of Biology, University of Konstanz, Konstanz, Germany, 2 Plant Nutrition and Ecophysiology, School of Agriculture and Food Sciences, University of Queensland, Brisbane, QLD, Australia Keywords: competition, climate change, invasion, conservation, allelochemicals, global warming, facilitation, plant–plant interactions Editorial on the Research Topic Plant Competition in a Changing World Climate change and biological invasions place new challenges on plants, their development, fitness, and competitiveness. To develop and evaluate strategies for sustainable ecosystem management and to respond to biodiversity loss, we need mechanistic understanding of the changes that are occurring in plant communities. Underlying drivers of change are plant–plant interactions which include competition, facilitation, and avoidance of competition, and their regulation by environmental factors (Trinder et al., 2013). The studies highlighted in this ebook examine plant competition in range of communities that span from forests to meadow and crop systems across alpine, temperate, and tropical climates. Facilitation , positive interactions between plant species, is a key driver of plant community dynamics and structure, but comparatively few studies have examined how facilitation is modulated in response to climate change (Brooker, 2006; Brooker et al., 2007; Lavergne et al., 2010). In their review, Anthelme et al. discuss four aspects of facilitative effects in alpine systems in response to climate change: (1) a reduction of facilitative effects in alpine plant presence in response to declining cold-temperature stress due to warming in established alpine systems, (2) an increase in facilitative effects as a response to migration to colder environments with higher elevation, (3) changing patterns of facilitation along latitudinal gradients, and (4) the potential of nurse plants to buffer changes in microhabitats. Anthelme et al. present different migration scenarios that include various types of facilitation in response to increasing temperature. Valladares et al. review the consequences of facilitation and competition in context of global change, encompassing climate change, and biological invasions, with a focus on phylogenetic relatedness, functional traits, and phenotypic plasticity. Valladares et al. summarize the direct and indirect drivers of species richness in different ecosystems, such as temperate and tropical forests, grasslands, and alpine systems. The authors argue that studying pauci-specific communities will provide the necessary understanding on species interactions in more complex systems. The reviews by Valladares et al. and Anthelme et al. conclude that although there is no doubt that climate change impacts on plant communities directly (e.g., via increasing temperatures) and indirectly (e.g., via changes in the interactions between species), further empirical knowledge is needed to advance understanding of the underlying mechanisms of plant–plant interactions in different plant communities, climate, and resource settings. For example, studies on alpine systems are biased toward certain regions, especially Europe, with other regions overlooked. The authors recommend examining systems in which single species and their intra-specific functional variability are important to expand from the current focus on species-rich systems such as tropical rainforests. 5 Simon and Schmidt Plant Competition in a Changing World The other key driver discussed here is competition , especially in resource-poor habitats where plant growth and reproduction is challenging and/or further impaired with global change. A plant’s ability to occupy space influences its ability to access resources such as light, water, and nutrients. Studying the relative influence of topography, environment, and spatial distance of rockcress ( Boechera stricta ) to other individuals, either intra- or inter-specific, Naithani et al. found that this species’ performance in a meadow community is predominantly influenced by intra- specific competition and insect herbivory. In contrast, its spatial distribution in the meadow community is limited by dispersal and microhabitat preference. At the other end of the plant size spectrum and focusing on competition for light, van Kuij et al. present a 3D-model, validated with field data, for calculating photosynthesis rates for individual trees in forests. Such model has potential to assist forest management strategies, such as aiding the potential effect of accelerated succession to generate resilient forests/plantations. Prior and Bowman investigated the interaction between tree growth and microhabitat across a macro-ecological gradient. They present new evidence from an extensive dataset of eucalypt tree growth collected across temperate and sub-tropical mesic Australia that in cooler habitats with sufficient water availability, light is the most limiting resource which results in increased competition, whereas in hot and dry habitats where water is the limiting factor, light is no longer driving competition. The study by Muller et al. on species interactions in urban plantings at three buildings in subtropical Australia, expands on the relationships of light and water, and demonstrates that plant productivity and arthropod diversity increase in situations with abundant availability of resources. This study provides evidence that ecological principles are transferrable from natural systems to human-made urban systems. Expanding on plant–plant competition from light and water, the study by Li et al. examines nitrogen as a main macronutrient that limits plant growth in many plant communities, and demonstrate that competition is reduced in two co-occurring tree species, beech and sycamore maple, that have a preference for organic and inorganic nitrogen forms, respectively. Another mechanism to avoid competition is allelopathy, the release of plant-growth inhibiting or toxic substances into the rhizosphere. Asaduzzaman et al. identified potentially allelopathic compounds in a laboratory bioassay investigating root and shoot tissue of different canola cultivars when growing in competition with weeds. The authors suggest that an allelopathic effect depends not only on the synthesis of certain compounds, but also on their active exudation into the rhizosphere and this seems to be dependent on intrinsic genotypic factors. Plant invasions and their contribution to the competition for resources in native plant communities were reviewed by Gioria and Osborne. The authors discuss how “winning” the competition depends on factors that include resource distribution and stage of the invasion process, and that raise conceptual and methodological issues for future studies on competition in plant invasions. Considering environmental, such as competition for nutrients, water, light, and space, as well as biotic constraints, they find “windows of opportunity” during which competition is reduced. Furthermore, Gioria and Osborne show seasonal shifts between environmental or biotic constraints as key drivers of competition. Plant invasions and their role in plant–plant competition for resources has also been the focus of several original research articles here. Elgar et al. showed facilitation can provide a measure to overcome competition between native woody plants and invasive grasses in rainforest reforestation on former agricultural land. Ens et al. used leaf-scale ecophysiological and stand-scale growth traits between an invasive and a native grass and present evidence that the higher photosynthetic nitrogen use-efficiency of the invasive grass selects for improved nitrogen acquisition from soil in nitrogen-poor ecosystem. Exploring the foraging responses and performance of herbaceous invaders to nitrogen- rich patches, Keser et al. suggest that strong plasticity of root- foraging responses is adaptive and appears to contribute to invasiveness. Overall, plant–plant competition and facilitation present a framework for understanding changes in plant communities. Such interactions are likely to become more prevalent where plants have to increasingly secure resources in response to climate change. Current knowledge together with climate predictions indicate that in some habitats competition will intensify with increased abiotic stress (e.g., water and nutrient limitations). Adding biotic stresses, such as plant invasions, will further impact on native plant communities with outcomes including declining biodiversity and ecosystem function. To date, different empirical approaches have mainly been used separately; however, using them in combination would increase resolution (Valladares et al.). Including multiple potential drivers of plant interactions in combinations in future studies, would aid in developing and evaluating strategies for sustainable ecosystem management to secure ecosystem services for modern society. AUTHOR CONTRIBUTIONS JS wrote the first draft of the editorial, both JS and SS then jointly edited the final version. ACKNOWLEDGMENTS We would like to thank the authors, reviewers, and the Frontiers Editorial Office for their support in creating this special topic. REFERENCES Brooker, R. W. (2006). Plant-plant interactions and environmental change. New Phytol. 171, 271–284. doi: 10.1111/j.1469-8137.2006.01752.x Brooker, R. W., Travis, J. M., Clark, E. J., and Dythjam, C. (2007). Modelling species’ range shifts in a changing climate: the impacts of biotic interactions, dispersal distance and the rate of climate change. J. Theor. Biol. 245, 59–65. doi: 10.1016/j.jtbi.2006.09.033 Lavergne, S., Mouquet, N., Thuilller, W., and Ronce, O. (2010). Biodiversity and climate change: integrating evolutionary and ecological responses of species and communities. Ann. Rev. Ecol. Evol. Syst. 41, 321–350. doi: 10.1146/annurev-ecolsys-102209-144628 Frontiers in Plant Science | www.frontiersin.org April 2017 | Volume 8 | Article 651 | 6 Simon and Schmidt Plant Competition in a Changing World Trinder, C. J., Brooker, R. W., and Robinson, D. (2013). Plant ecology’s guilty little secret: understanding the dynamics of plant competition. Funct. Ecol. 27, 918–929. doi: 10.1111/1365-2435.12078 Conflict of Interest Statement: 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. Copyright © 2017 Simon and Schmidt. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Frontiers in Plant Science | www.frontiersin.org April 2017 | Volume 8 | Article 651 | 7 REVIEW ARTICLE published: 12 August 2014 doi: 10.3389/fpls.2014.00387 Facilitation among plants in alpine environments in the face of climate change Fabien Anthelme 1,2 *, Lohengrin A. Cavieres 3,4 and Olivier Dangles 5,6 1 Institut de Recherche Pour le Développement, UMR AMAP , Montpellier, France 2 Instituto de Ecología, Universidad Mayor San Andrés, La Paz, Bolivia 3 Departamento de Botánica, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile 4 Instituto de Ecología y Biodiversidad, Santiago, Chile 5 Institut de Recherche pour le Développement, UR 072, Laboratoire Evolution, Génomes et Spéciation, UPR 9034, Centre National de la Recherche Scientifique, Gif-sur-Yvette, France 6 Université Paris-Sud 11, Orsay, France Edited by: Judy Simon, University of Konstanz, Germany Reviewed by: Graciela Mónica Rusch, Norwegian Institute for Nature Research, Norway Wayne Dawson, University of Konstanz, Germany *Correspondence: Fabien Anthelme, Institut de Recherche Pour le Développement (IRD), UMR AMAP , Boulevard de la Lironde, TA A-51/PS2, 34398 Montpellier Cedex 5, France e-mail: fabien.anthelme@ird.fr While there is a large consensus that plant–plant interactions are a crucial component of the response of plant communities to the effects of climate change, available data remain scarce, particularly in alpine systems. This represents an important obstacle to making consistent predictions about the future of plant communities. Here, we review current knowledge on the effects of climate change on facilitation among alpine plant communities and propose directions for future research. In established alpine communities, while warming seemingly generates a net facilitation release, earlier snowmelt may increase facilitation. Some nurse plants are able to buffer microenvironmental changes in the long term and may ensure the persistence of other alpine plants through local migration events. For communities migrating to higher elevations, facilitation should play an important role in their reorganization because of the harsher environmental conditions. In particular, the absence of efficient nurse plants might slow down upward migration, possibly generating chains of extinction. Facilitation–climate change relationships are expected to shift along latitudinal gradients because (1) the magnitude of warming is predicted to vary along these gradients, and (2) alpine environments are significantly different at low vs. high latitudes. Data on these expected patterns are preliminary and thus need to be tested with further studies on facilitation among plants in alpine environments that have thus far not been considered. From a methodological standpoint, future studies will benefit from the spatial representation of the microclimatic environment of plants to predict their response to climate change. Moreover, the acquisition of long-term data on the dynamics of plant–plant interactions, either through permanent plots or chronosequences of glacial recession, may represent powerful approaches to clarify the relationship between plant interactions and climate change. Keywords: competition, cushion plants, early snowmelt, facilitation, latitudinal gradient, nurse plant, stress- gradient hypothesis, global warming INTRODUCTION Empirical studies and reviews in the last decade leave no doubt that the multiple effects of current and predicted cli- mate change will affect plant communities not only directly, e.g., via “thermophilization,” but also indirectly, through changes in interactions among species (Lortie et al., 2004; Brooker, 2006; Poloczanska et al., 2008; Gilman et al., 2010; Adler et al., 2012; Gottfried et al., 2012; Grassein et al., 2014). To date, however, non-trophic interactions are still poorly considered in predic- tive models of plant community responses to climate change (Lavergne et al., 2010; Walther, 2010; Bellard et al., 2012; but see Sutherst et al., 2007). Most efforts aiming at including interactions in predictions of the impact of climate change on plant communities have been based on negative interactions (hereafter termed “competition”; Brooker, 2006; Araújo and Luoto, 2007; Tylianakis et al., 2008; Meier et al., 2012). In comparison, the role of non-trophic posi- tive interactions among species (hereafter termed “facilitation”) in driving the structure and dynamics of plant communities under rapid climate change has rarely been tested, even though conceptual models and reviews predict that this type of interac- tion might be pivotal, especially in harsh environments (Brooker, 2006; Brooker et al., 2007; Lavergne et al., 2010). Improving our knowledge on facilitation among plants under a changing climate is therefore urgently required as part of assessing the impacts of climate change on plant communities and ecosystems. The stress-gradient hypothesis (SGH) is one of the most important conceptual advances made over the past two decades with respect to plant–plant interactions along environmental gra- dients. In its current definition, the SGH predicts that positive www.frontiersin.org August 2014 | Volume 5 | Article 387 | 8 Anthelme et al. Facilitation in the face of climate change interactions among plants (and also among animals: Kawai and Tokeshi, 2007; Dangles et al., 2013) will increase with stress and disturbance, at least up to a certain threshold (Bertness and Callaway, 1994; Brooker and Callaghan, 1998; Michalet et al., 2006; Maestre et al., 2009; He et al., 2013; He and Bertness, 2014). Therefore, a central goal in predicting the response of plant com- munities in a world affected by climate change is to determine to what extent future environments will modify the levels of distur- bance and/or stress experienced by plants ( sensu Grime, 1977). The direct effects of climate change on plants include warmer temperatures, changes in water availability, and a higher occur- rence of extreme events such as drought or heat waves (IPCC, 2013). While limitations related to temperature and water may represent stressors for plants, extreme events are related more to disturbance. Importantly, the effect of a given stress or dis- turbance level on plants is likely to be site- and species-specific. For example, in dry, warm environments such as the Sahara, warming will certainly increase the environmental stress on plants by increasing evapotranspiration (e.g., Johnson et al., 2012), hence decreasing the water availability (McCluney et al., 2012). Conversely, warming in alpine environments is expected to reduce the stress experienced by plants, thus potentially increasing plant productivity (e.g., Cavieres and Sierra-Almeida, 2012). However, the sum of different stresses or disturbances along environmen- tal gradients will not necessarily generate more facilitation, as demonstrated by the possible existence of non-additive models of interactions (Malkinson and Tielbörger, 2010). Alpine regions represent an important model for examining the effects of climate change on plant–plant interactions for sev- eral reasons. First, alpine ecosystems are relatively homogenous in terms of climatic conditions, and they are found on all conti- nents at almost all latitudes, from 0 to 6000 m a.s.l. (Körner, 2003; Nagy and Grabherr, 2009). Alpine plant communities have been widely used by ecologists over the last two decades to infer pat- terns and mechanisms of plant–plant interactions, in particular because mountain environments provide abrupt stress variations along elevation gradients (Körner, 2007). Studies conducted in these environments have provided major contributions to the def- inition and further refinements of the SGH (Choler et al., 2001; Callaway et al., 2002; Maestre et al., 2009; He et al., 2013). In most alpine environments, greater facilitation is observed at higher ele- vation, i.e., in more stressful conditions—readers are referred to the specific cases in dry alpine environments reported by Cavieres et al. (2006) and Michalet et al. (2014) where two opposing stress gradients were found. Accordingly, these environments constitute a sound model for inferring the effects of climate change on the outcomes of plant–plant interactions. In this paper, we provide an overview of the extent to which facilitation among plants will interact with the effects of cli- mate change in the organization of alpine plant communities in future decades. We provide a review of current knowledge, and suggest directions for future research. In particular, we focus our contribution on the following four issues and associated hypotheses: (1) Facilitation in established alpine communities . Our underlying hypothesis is that decreasing abiotic stress through warming reduces the frequency of facilitative effects among plants that are already established in alpine ecosystems. (2) Facilitation in alpine communities migrating to higher eleva- tions . We hypothesize that alpine plants migrating to higher elevations as a response to the effects of warming will inter- act more positively because of the harsher environmental conditions in the newly settled areas (primary succession). (3) Facilitation along latitudinal gradients. We hypothesize that the outcomes of plant–plant interactions will change along large latitudinal gradients, together with the magnitude of climate change and characteristics of the alpine environment. (4) Facilitation and the long-term buffering effect of alpine nurse plants . Our hypothesis here is that the persistent buffering effects on microenvironmental conditions by some alpine nurse plants may offer long-term biotic refuges for other alpine plants. FACILITATION IN ESTABLISHED ALPINE COMMUNITIES: A BIBLIOGRAPHIC REVIEW On 3 April 2014 we conducted a search of the peer-reviewed liter- ature via Web of Science using the following terms: “plants” AND (“alpine” OR “arctic”) AND “climate change” AND (“facilitation” OR “positive interaction”). We obtained a total of 80 references. We then extended this selection by reviewing the relevant litera- ture cited in each of these 80 papers and obtained a second list of 96 references. Later, we reduced this list by retaining only those references that (1) provided explicit data on both climate change and facilitation among plants, and (2) considered facilitation above the treeline (thus excluding forests, but taking into account small and dwarf shrubs). Studies along elevational gradients were only considered if they focussed explicitly on climate change effects. Studies that explicitly documented plant–lichen interac- tions in the face of climate change were also included. This search resulted in a shortlist of only 17 papers, published between 1997 and 2014 ( Table 1 ). To analyse the data, we considered five param- eters: the geographical location of studies; the type of climate change effect (warming, snowmelt timing, water availability); the methodology (experimental, observational, modeling); the num- ber of interacting plants (we assumed that studies involving up to four beneficiary species were “species-pair” studies, in contrast to studies at the community level); and the net interaction out- come (more or less facilitation, neutral, or complex effects with no clear trend). We also took into account the effects of three covariables: nutrients, land abandonment, and wind speed. This quantitative method was not used for Sections Facilitation and the Upward Migration of Alpine Species, Facilitation and Climate Change Along Latitudinal Gradients, and Long-term Facilitative Effects by Nurse plants because of the scarcity of available literature. VARIOUS CLIMATE CHANGES EFFECTS, VARIOUS INTERACTION OUTCOMES The majority of studies (88%; Table 1 ) used temperature warm- ing as a proxy for climate change. Indeed, it is one of the most—if not the most—predictable effects of climate change on alpine environments, either in terms of maximum, minimum, Frontiers in Plant Science | Functional Plant Ecology August 2014 | Volume 5 | Article 387 | 9 Anthelme et al. Facilitation in the face of climate change Table 1 | Review of studies examining facilitation among plants in established alpine communities in the face of climate change. References Country/ Environment Effect Covariable Protocol Climate Interaction Neighbor Target Net State change proxy species interaction Almeida et al., 2013 Ecuador Tropical alpine Warming Observational Elevation gradient Species pairs Azorella aretioides Lasiocephalus ovatus Facilitation decrease Brooker et al., 2007 Global Global Warming Modeling Spatial model Community scale Mutualists and competitors Mutualists and competitors Complex Cavieres and Sierra-Almeida, 2012 Chile Dry alpine Warming Experimental OTC Species pairs Azorella madreporica Hordeum comosum Facilitation decrease Cornelissen et al., 2001 Global Arctic Warming Nutrient Experimental/ Observational Various Community scale Vascular plants Lichens Facilitation decrease Crabtree and Ellis, 2010 Scotland Alpine Warming Wind Observational Elevation gradient Community scale Vegetation structure 11 lichen species Complex Dormann et al., 2004 Norway Arctic Warming Nutrient Experimental OTC Species pairs Luzula confusa , Salix polaris Luzula confusa , Salix polaris Facilitation decrease Hobbie et al., 1999 USA/Alaska Arctic Warming Experimental OTC Community scale Seven species Community Neutral Hülber et al., 2011 Austria Subalpine Snowmelt timing Observational Snowbed- grassland ecotone Species pairs Snowbed community Four snowbed species Complex Klanderud and Totland, 2005 Norway Alpine Warming Nutrient Experimental OTC Species pairs Vegetation structure Thalictrum alpinum, Carex vaginata Complex Klanderud and Totland, 2007 Norway Alpine Warming Experimental OTC Community scale Dryas octopetala Seeds of 27 alpine species Facilitation decrease Klanderud, 2005 Norway Alpine Warming Nutrient Experimental OTC Species pairs Dryas octopetala Thalictrum alpinum, Carex vaginata Facilitation decrease Michalet et al., 2014 Global Alpine Warming, water Observational Elevation gradient Community scale Various Various Complex Olsen and Klanderud, 2014 Norway Alpine Warming Experimental OTC Community scale Dryas octopetala Seeds of 27 alpine species Facilitation decrease Pajunen et al., 2011 Finland, Russia Arctic Warming Observational Shrub abundance Community scale Shrubs Plant community (functional groups) Complex Shevtsova et al., 1997 Finland Subarctic Warming, water Experimental OTC, water addition Species pairs Empetrum nigrum, Vaccinium vitis-idae Empetrum nigrum, Vaccinium vitis-idae Complex (Continued) www.frontiersin.org August 2014 | Volume 5 | Article 387 | 10 Anthelme et al. Facilitation in the face of climate change Table 1 | Continued References Country/ Environment Effect Covariable Protocol Climate Interaction Neighbor Target Net State change proxy species interaction Vittoz et al., 2009 Switzerland Subalpine Warming Land aban- donment Observational Permanent plots Community scale Community Community Facilitation decrease Wipf et al., 2006 USA/Alaska Subarctic Snowmelt timing Experimental Snow manipulation Species pairs Empetrum nigrum, Vaccinium vitis-idae Empetrum nigrum, Vaccinium vitis-idae Facilitation increase or average values (IPCC, 2013). In the majority of these stud- ies (53% of the warming studies), warming decreased the net effects of facilitation among alpine plants, and they never gen- erated an increase in facilitation. In alpine environments, cold temperatures—especially low extremes—are one of the main physical stresses experienced by plants, despite the fact they are generally well adapted to such conditions (Körner, 2003). The buffering of extreme temperature has been shown to be one of the main mechanisms by which nurse plants facilitate other species in alpine regions (Nyakatya and McGeoch, 2008; Badano and Marquet, 2009), supporting the hypothesis that facilitation in alpine environments is primarily generated by stresses that are not directly related to resource availability (Maestre et al., 2009). Therefore, the reduction of temperature stress alongside global warming is expected to reduce the positive effects of alpine nurse plants, lowering net facilitation among plants in established com- munities, as predicted by the SGH. Facilitation release is thought to be related to (1) higher abundance/cover of competing species (Cornelissen et al., 2001; Vittoz et al., 2009), and (2) a higher growth rate at the individual scale (taller individuals; Klanderud, 2008; Pajunen et al., 2011). However, the causal relationship between warming and reduced net facilitation among alpine plants is not clear-cut. In one study, reduced facilitation appeared to partly result from land abandonment, which affected plant cover dynamics (Vittoz et al., 2009); whereas, in another study, net facilitation release was pos- sibly compensated by a reduction in wind speed (Crabtree and Ellis, 2010). Five other studies have revealed complex interac- tion patterns related to (1) site-specific effects (dry vs. temperate; Michalet et al., 2014), (2) species-specific effects (Shevtsova et al., 1997; Klanderud and Totland, 2005; Brooker et al., 2007; Pajunen et al., 2011), and (3) variation in the performance variable used (Klanderud and Totland, 2005). Taken together, these studies sug- gest uncertainty remains in terms of to what extent warming will reduce the importance of facilitation in the organization of estab- lished alpine plant communities. Facilitation release may be more obvious when taking into account interactions between estab- lished alpine species and species migrating from lower vegetation belts, as supported extensively in the literature (e.g., Grabherr et al., 1994; Pauli et al., 2012; Olsen and Klanderud, 2014). Greater nutrient availability, in particular through nitrogen deposition, is expected to be another covariable of climate change in alpine regions (Bobbink et al., 1998; Hu et al., 2014) with well-known positive effects on plant productivity (Alatalo and Little, 2014; McDonnell et al., 2014). Interestingly, four stud- ies (Cornelissen et al., 2001; Dormann et al., 2004; Klanderud, 2005; Klanderud and Totland, 2005) found that climate change may interact with changes in nutrient levels, leading to reduced net facilitation among plants ( Figure 1 ). Therefore, it is pos- sible that nutrient enrichment related to nitrogen deposition may be a “hidden” driver of facilitation release in alpine com- munities also experiencing climate change. This hypothesis is coherent with recent data pointing toward a positive relation- ship between facilitation and nutrient stress in alpine regions (Yang et al., 2010; Anthelme et al., 2012). These results, sup- ported by a