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Facilitation and the Organization ofCommunitiesChristopher J. Lortie

Introduction

Species interactions are a cornerstone of ecological research wherein the effects of an individual of one species on another individual,frequently a different species, are studied. Within versus between species interactions are also commonly contrasted as a means to inferrelative importance, but the majority of theory advances, at least at the community level, are associated with interactions betweenindividuals of different species. Interactions can range from positive to negative, and effects are measured at all levels of development,or life history stages, of an organism. Positive interactions have been extensively studied in both population and community ecology.Facilitation, however, is a relatively specific term that has evolved primarily to describe positive plant–plant interactions (see DefiningFacilitation). Facilitation, or positive interactions, is a relatively recent subset of these species interactions in general, including relatedprocesses, such as competition, mutualism, and parasitism. Facilitation is best viewed as the antithesis of the plant competitionliterature, as it shares many of the main attributes, both in terms of scope and approach, and arose as a comparator to this research.Facilitation studies mainly refer to positive plant–plant interactions, as the term was proposed in the plant literature and extensively usedto describe interactions that include a positive effect of one species on another. Mutualism and parasitism research is often plant–insectbased and formally identifies the reciprocal effect in the interaction, that is, (+, +) in mutualism and (+,−) in parasitism, whereasfacilitation studies are generally (+,0) or (+,?), with the second effect often unreported. Interactions that include at least one negativeinteraction are usually described as competition in the plant literature and do not apply the term facilitation (although the frequency ofboth being discussed concomitantly is increasing). Hence, the term facilitation, owing to historical use, describes the subset ofinteractions that are (+,0) and is mostly specific to within plants, although its usage is expanding. The research on facilitation has mostlikely peaked, similar to plant competition studies, in that facilitation has been clearly established as an important process in theformation of plant communities. Additional studies simply demonstrating facilitation are increasing unlikely to be present in the literature.That said, the implications to theory and other, more nuanced aspects of interaction, such as context dependence, shifting balances,and importance of the environment, as they relate to facilitation, are still largely unexplored. In the early 21st century the mostcontentious debates, with respect to facilitation, center on either disagreement concerning what a community is and whether researchshould be conducted at this scale or on how to use environmental gradients (i.e., stress) most effectively. Both of these topics aredescribed herein, with readings also included on Historical Background, Experimental and Analytical Approaches, Evolution, other taxa,and Applications.

General Overviews

Facilitation is a subset of the possible interactions associated with the organization of community, ranging from positive, to neutral, tonegative. Hence, facilitation, in the broadest sense, is often included in many works describing plant communities. There are severalexcellent overviews, both books and peer-reviewed articles, that formally discuss facilitation and that are ideal launching points forfurther reading. Callaway 1995 is the classic and the first review that promoted the term facilitation. A more comprehensive treatise onthe subject by Callaway followed that original paper (Callaway 2007). Although the general focus and theme are implicitly communitybased, this book focuses more directly on facilitation itself, with chapters on direct and indirect mechanisms of facilitation, interactionswith competition, and species specificity. The final chapter is, however, on community organization. A second book on this topic, written

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by a subset of the leaders of the field, including Callaway, and edited by Pugnaire, was published in the following year (Pugnaire 2010).This book is explicitly focused on the community, with chapters on indices, diversity, biodiversity, mycorrhizae, climate change, andstress gradients, and less directly on the specifics of facilitation. Callaway 2007 is the most thorough reader available on plant facilitationand addresses virtually every aspect of its study, whereas the latter text is a broader and more diverse treatment of facilitation, as itrelates to community ecology. Two overviews on facilitation have also been published in the Journal of Ecology and another, in BiologyLetters. The first Journal of Ecology paper (Brooker, et al. 2008) articulates previous research and illuminates future directions whereasthe second (Brooker and Callaway 2009) introduces a special section on a symposium on facilitation held at the University of Aberdeen,Scotland, from 20 to 22 April 2009. The final overview, in Biology Letters (Pakeman, et al. 2009), also discusses this symposium anddescribes the conceptual status of facilitation in the early 21st century, including future directions.

Brooker, Rob W., and Ragan M. Callaway. 2009. Facilitation in the conceptual melting pot. Journal of Ecology 97.6: 1117–1120.

This is a short, synthetic piece that offers a clear overview of the broad significance of facilitation research and its importance to theory.

Brooker, Rob W., Fernando T. Maestre, Ragan M. Callaway, et al. 2008. Facilitation in plant communities: The past, the present,and the future. Journal of Ecology 96.1: 18–34.

This is a highly cited paper for future directions and clearly describes the advances and key developments from the published empiricalwork. The first table provided is an excellent resource for quick identification of readings associated with seminal works. As an excellent,comprehensive starting point that is a single, short read, this is likely the best place to begin for an overview—particularly for futuredirections.

Callaway, Ragan M. 1995. Positive interactions among plants. Botanical Review 61.4: 306–349.

Callaway thoroughly examines all the literature published up to that time on most aspects of facilitation. This paper is a perfect startingpoint for assessing the biology and biological mechanisms associated with positive interactions in plants. As a seminal citation onfacilitation, this publication is extremely useful. Also, the paper is an excellent source for the critical physiological studies that underpinmodern facilitation research. Available online for purchase or by subscription.

Callaway, Ragan M. 2007. Positive interactions and interdependence in plant communities. Dordrecht, The Netherlands:Springer.

This book provides the reader with a comprehensive treatment of direct versus indirect mechanisms of facilitation and examination of theevidence for whether positive effects are species specific. Every aspect of facilitation is covered in detail, and if the reader is interestedin mechanisms, this is the best source for a full understanding of the scope of effects studied in plant facilitation experiments.

Pakeman, Robin J., Francisco I. Pugnaire, Richard Michalet, et al. 2009. Is the cask of facilitation ready for bottling? Asymposium on the connectivity and future directions of positive plant interactions. Biology Letters 5.5: 577–579.

This is a short and accessible essay on the status of facilitation in the early 21st century, in terms of conceptual refinement, evolution,community-level effects, and restoration, and on future directions in general for the field. This is likely the quickest read on the topic,serving as a brief and broad overview. Topical issues are identified and future directions, explained.

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Pugnaire, Francisco I., ed. 2010. Positive plant interactions and community dynamics. Boca Raton, FL: CRC.

A collection of essays focused on facilitation and the plant community. This is not so much a book about the biology of facilitations asone on the derived or advanced aspects of facilitation, in that it addresses implications at the community level. This source is anexcellent community ecology book mainly focused on positive plant interactions, with less detail than Callaway 2007 but with more focuson the community. A logical pipeline for the reader would be to begin with Callaway 2007, for an understanding of the mechanisms, andthen move on to this book for community-level implications.

Journals

The number of publications on plant facilitation increased exponentially in peer-reviewed ecology and evolution journals between 1993and the early 21st century (Institute for Scientific Information Web of Science search for plant facilitation, line of best fit, r2 = 0.85, p =0.0001). The range of values begins at 7 publications per year and increases to more than 100 per year, for a total of approximately1,000 publications. There have been more than 20,000 citations to these papers (excluding self-citations), which is a rate of 20 citationsper publication. For a detailed contrast of the relative success of these journal articles to a related field, for example, plant competitionstudies, see Lortie and Callaway 2009 (cited under Historical Background). A total of 130 authors have published on this topic, fromforty-four different countries, including every major ecology and evolution journal, with at least five papers, but often more; many journalshave published several papers. A total of seventy-three journals have published on the topic, with the following six accounting for morethan 50 percent of the papers: Journal of Ecology, Journal of Vegetation Science, Plant Ecology, Oecologia, and Oikos in descendingorder. Three journals, however, account for approximately 50 percent of the total citations to plant facilitation: Ecology, Journal ofEcology, and Ecological Monographs, with Trends in Ecology and Evolution close behind, with more than 1,500 citations. Each journalgenerally has representative articles exploring both conceptual and empirical aspects of facilitation and community organization (but seeFoundational Works for the best journal articles). Some journals focus more on the theoretical implications, for example, Ecology Letters,whereas others primarily provide clear demonstration of empirical importance, for example, Journal of Ecology.

Ecology. 1920–.

Published by the Ecological Society of America, this journal offers articles on basic and applied ecology.

Ecology Letters. 1998–.

A broad ecology journal for all taxa that promotes novelty.

Journal of Ecology. 1913–.

An international journal published by the British Ecological Society covering all aspects of plant ecology. The top journal for plantecology research.

Journal of Vegetation Science. 1990–.

An international journal published by the International Association for Vegetation Science that includes original studies, notes, andreviews for vegetation and plant community ecology.

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Oecologia, 1968–.

This is a broad ecological journal covering all aspects of interactions but is particularly well known for plant–animal interactions.

Oikos. 1949–.

Also a broad ecological journal encompassing all aspects of ecology, published by the Nordic Ecological Society. Best known for shortcommunications and novel synthesis in ecology.

Plant Ecology. 1949–.

Formerly Vegetatio (1949–1996). Journal specific to plant ecology, publishing all aspects of study.

Defining Facilitation

Broadly speaking, facilitation is the positive effect of one plant species on another. These studies commonly document increasedsurvival or growth of one species, when associated with another species, that in some way ameliorates the local microhabitat, making itsconditions more favorable. For instance, provision of shade, which can increase available moisture, is a common mechanism in arid andsemiarid systems. Facilitation is thus best defined as positive interactions between two different species of plants; one individualbenefits, and the cost is either not present or not documented for the other. As explained in the Introduction, the effects described byfacilitative interactions commonly refer to (+,0) or (+, ?). The interaction must be positive for at least one of the individuals, with survival,growth, or fitness benefits. Direct reproductive or fitness benefits are, of course, desirable as a response and should be measured, butmany studies do not do so. If a negative interaction is reported, the study is generally reported as a study on competition, at leasthistorically; however, in the early 21st century, papers include discussion of both positive and negative effects. There is some debate asto whether intraspecific interactions between individual plants can be considered facilitation; these interactions are usually accepted assuch but are simply less studied than interactions between different species within this field. The clearest definition of facilitation can befound in Callaway 1995. Facilitation is generally specific to plant-plant interactions (primarily terrestrial), although marine ecologists usethe term (Bulleri 2009), and it is related to mutualism, but facilitation is better viewed as specific to interactions and not to evolution orcoevolution per se (Bronstein 2009). Parasitic plants can also be facilitators but are not often referred to as such in the literature (Watson2009). There is also a facilitation model for succession, but early-21st-century studies using the term facilitation are largely unrelated(i.e., the 1,000 publications described in Journals do not refer to succession, but for clarification on this, see Verdú, et al. 2009). Hence,facilitation has come to serve as a direct term, in concert with plant competition, a simple description of one individual benefiting fromanother, predominantly applied to interaction studies within community ecology.

Bronstein, Judith L. 2009. The evolution of facilitation and mutualism. Journal of Ecology 97.6: 1160–1170.

Excellent explanation of the conceptual differences between facilitation and mutualism. The similarities, differences, future directions,and general implications of considering the two concepts jointly are described.

Bulleri, Fabio. 2009. Facilitation research in marine systems: State of the art, emerging patterns and insights for futuredevelopments. Journal of Ecology 97.6: 1121–1130.

Clearly establishes how facilitation is studied in marine ecology and how the term is not always uniformly applied even though the

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concept and studies are similar to terrestrial ecology. The differences in the application of the related terminology are discussed, andnumerous studies that clearly test facilitation but do not report as such are highlighted.

Callaway, Ragan M. 1995. Positive interactions among plants. Botanical Review 61.4: 306–349.

Specific and clear definition that among several others at this time launched the widespread use of the term. Importantly, this referenceserves as the best initial starting point for a survey of the general mechanistic categories that facilitation studies examine. Availableonline for purchase or by subscription.

Verdú, Miguel, Pedro J. Rey, Julio M. Alcántara, Gemma Siles, and Alfonso Valiente-Banuet. 2009. Phylogenetic signatures offacilitation and competition in successional communities. Journal of Ecology 97.6: 1171–1180.

Reviews and relates facilitation to success and serves as an excellent explanation of the opposite of what one might assume—howsuccession might be used to study facilitation, and not the converse.

Watson, David M. 2009.Parasitic plants as facilitators: More Dryad than Dracula? Journal of Ecology 97.6: 1151–1159.

Clarification of parasitism conceptually, as to how it relates to the body of facilitation literature.

Historical Background

Competition was the main and virtually exclusive focus of plant interaction studies for more than a hundred years. Facilitation is arelatively recent development in this literature, present only since the 1990s. Plant community theory was not necessarily resistant to thestudy of facilitation but focused more predominantly on the study of competition, because it is more intuitively linked to individual benefitand to evolution; for example, the competitive dominant could have higher fitness, thereby providing the means for selection to promoteincreased competitiveness. Clements’s concept of community was critical to the paradigm shift that began in the late 1980s but thatreally accelerated in the mid-1990s. The concept of community as integrated with species that are linked in some way was critical to thesuccess of facilitation studies, and most facilitation researchers adopted this view of community. This is in direct contrast to theindividualistic concept of communities, as developed by Gleason 1926, that held favor almost exclusively in plant community ecologyand that led to a one-sided focus on negative interactions, or competition, for nearly the hundred-plus years described. The return ofmore community-level thinking to plant ecology was instrumental in the placing of facilitation studies on a par with competition studies interms of citations within a ten-year period (i.e., by 2009; see Lortie and Callaway 2009). Facilitation, as it relates to community ecology,can thus be traced to at least two sources: the superorganism concept proposed by Clements 1916 and the more recent Hunter andAarssen 1988. The latter work is mainly viewed as the first contemporary paper on plant facilitation, wherein it was restated that twoplants could be competing or facilitating simultaneously. Most plant ecologists at the time, of course, recognized this, but it was this workthat essentially began a subtle shift in the study of plant–plant interactions, as they relate to communities. Callaway 1995 provided areview of facilitation that, given its clarity and comprehensive nature, further accelerated the progress of the field. In the early 1990s thefield began accumulating clear empirical evidence for facilitation, but after the Callaway review the publication rate dramaticallyincreased. A final driver further promoted study in this field: the short concept paper, Bertness and Callaway 1994, which proposed thatstress gradients are a useful means of disentangling the relative frequency of positive versus negative interactions within communities.As discussed in Foundational Works, empirical studies documenting nurse plant effects offered a firm platform and the bulk of thehistorical field research for Hunter and Aarssen 1988 and Callaway 1995.

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Bertness, Mark D., and Ragan Callaway. 1994. Positive interactions in communities. Trends in Ecology and Evolution 9.5: 191–193.

The stress gradient hypothesis is proposed, which, although often misunderstood and sometimes debated, became the hypothesissynonymous with the study of facilitation, in many respects. Available online for purchase or by subscription.

Callaway, Ragan M. 1995. Positive interactions among plants. Botanical Review 61.4: 306–349.

Seminal review of the topic, with a clear set of explanations of mechanisms and numerous examples of facilitation in a wide range ofecosystems. Available online for purchase or by subscription.

Clements, Frederic E. 1916. Plant succession: An analysis of the development of vegetation. Washington, DC: CarnegieInstitution of Washington.

The classic paper that was instrumental in the paradigm shift in the definition of community, allowing for the study of facilitation inaddition to competition.

Gleason, H. A. 1926. The individualistic concept of the plant association. Bulletin of the Torrey Botanical Club 53.1: 7–26.

The classic paper that served to promote more individual-based competition studies in plant community ecology for close to a hundredyears.

Hunter, A. F., and L. W. Aarssen. 1988. Plants helping plants. BioScience 38.1: 34–40.

The first modern paper on plant facilitation; restates the evident truth that facilitation and competition are two sides of the same coin.Also contains the novel argument, which has also not been explored at length, that even between two individuals the interactions canvary from positive to negative as one moves from above- to belowground estimates of effects. Available online for purchase or bysubscription.

Lortie, Christopher J., and Ragan M. Callaway. 2009. David and Goliath: Comparative use of facilitation and competitionstudies in the plant ecology literature. Web Ecology 9: 54–57.

A scientometric contrast of the relative success of facilitation studies versus competition studies, controlling for length of time publishedin the literature. Citations and number of publications are compared, as they contribute to most general categories of ecology.

FOUNDATIONAL WORKS

This is a relatively new field, given its specificity (i.e., positive interactions between plants, as they relate to gradients, competition, orcommunity), but positive plant interactions have likely been studied from an agricultural perspective since humans developed the meansto cultivate crop species in mixtures. All foundation studies of facilitation, as it is conceived in the early 21st century, began in arid andsemiarid systems, with the study of shrub nurse plants. A nurse plant is an individual that facilitates other plant species under its canopy,and the arid/semiarid is a model system, as stress is so pronounced, and shrubs are the dominant life-form. Hence, nurse plant effectsdescribe the amelioration produced by the limiting of factors in the environment by a larger, canopy-forming species, such as a tree orshrub, for other, smaller plant species, such as annuals. The mechanism most commonly described is reduced temperatures in arid and

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semiarid systems, which increase available soil moisture for other plant species. The first study to demonstrate this was Niering, et al.1963, which showed that more species grew under saguaro than in more open microhabitats without a canopy. Another classic study inturn showed that the saguaro also benefit from a canopy, but only as young seedlings. In the early 21st century there are at least 300such studies published, demonstrating the positive effect of a shrub species on other plant life-forms, including herbs, forbs, andgrasses, via amelioration of the local environment. Few studies examine other life-forms, although cacti have been shown to befacilitated by shrubs (Turner, et al. 1969), as have trees (Gómez-Aparicio 2009). A second stream of research also serves as anunderpinning to facilitation and, interestingly, took place in the intertidal and in salt marshes. The intertidal work is the best atdemonstrating facilitation but also shifts in strength and sign from positive to negative, depending on the position on gradients. The saltmarsh studies clearly illustrate the importance of physical stress; Bertness 1991, Bertness 1989, Bertness and Hacker 1994, Bertnessand Shumway 1993, and Bertness and Yeh 1994 were the pioneering studies in this area. Lortie, et al. 2004 is a foundational conceptpaper that helped establish the framework for facilitation as an important driver of community organization, given the evidence for thegeneral prevalence of facilitation in plant communities.

Bertness, Mark D. 1989. Intraspecific competition and facilitation in a northern acorn barnacle population. Ecology 70.1: 257–268.

Exemplar of classic facilitation studies; includes the concept of a shifting interplay on gradients. Intertidal studies very clearly examinefacilitation and offer model systems that have been emulated in plant ecology. Available online for purchase or by subscription.

Bertness, Mark D. 1991. Interspecific interactions among high marsh perennials in a New England salt marsh. Ecology 72.1:125–137.

Exemplar of classic facilitation studies; includes the concept of a shifting interplay on gradients, but in terrestrial salt marshes. Studiessuch as this one launched a very substantial set of publications by others. Available online for purchase or by subscription.

Bertness, Mark D., and Sally D. Hacker. 1994. Physical stress and positive associations among marsh plants. AmericanNaturalist 144.3: 363–372.

An excellent paper that begins to examine importance of stress on plant interactions. Available online for purchase or by subscription.

Bertness, Mark D., and Scott W. Shumway. 1993. Competition and facilitation in marsh plants. American Naturalist 142.4: 718–724.

Another example of the shifting interplay between facilitation and competition.

Bertness, Mark D., and Su Ming Yeh. 1994. Cooperative and competitive interactions in the recruitment of marsh elders.Ecology 75.8: 2416–2429.

A fine example in the same genre of shifting interplay between positive and negative interactions. Available online for purchase or bysubscription.

Gómez-Aparicio, Lorena. 2009. The role of plant interactions in the restoration of degraded ecosystems: A meta-analysisacross life-forms and ecosystems. Journal of Ecology 97.6: 1202–1214.

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This study is one of the few examples showing that tree seedlings are also facilitated by shrubs and clearly links these findings torestoration, which is uncommon. The statistics are also very elegant, and the restoration implications, very useful for management.

Lortie, Christopher J., Rob W. Brooker, Phillipe Choler, et al. 2004. Rethinking plant community theory. Oikos 107.2: 433–438.

One of the first conceptual papers examining the implications of facilitation in defining a community. Available online for purchase or bysubscription.

Niering, W. A., R. H. Whittaker, and C. H. Lowe. 1963. The saguaro: A population in relation to environment. Science 142.3588:15–23.

One of the first nurse plant papers, which were critical early evidence for facilitation. Available online for purchase or by subscription.

Turner, Raymond M., Stanley M. Alcorn, and George Olin. 1969. Mortality of transplanted saguaro seedlings. Ecology 50.5:835–844.

One of the first studies showing that other life-forms, when seedlings, can enjoy facilitation from a canopy-forming species in addition tosmall, herbaceous plant species. Available online for purchase or by subscription.

CONTEMPORARY VIEWS

Similar to plant competition studies, facilitation studies have crossed a threshold in terms of volume of studies published, that is, proof ofconcept has been effectively established. Plant facilitation is frequent, sometimes intense, varies with stress, and is often important.Several works have helped establish the major contemporary views of facilitation, and it is improbable that a paper, without a novel twistor link to shifting interactions, evolution, genetics or phylogenetics, trophic consequences, and so on, would be publishable in a topecological journal. (Similar to the evolution of competition studies, first demonstrate concept, then importance, then links to othercommunity-level processes.) Contemporary views include the following. The frequency of including environmental gradients willnecessarily increase (extensions to the stress gradient hypothesis), and this is critical to better understanding the effects of a changingclimate on plant communities (Brooker and Kikidze 2008). The difference between the intensity of an interaction (i.e., the strength of theeffect or effect size measure) and the importance of an interaction—in a more broad sense, calculated as the impact—is now clearlydistinguished in most top publications in this field (Brooker, et al. 2005, Brooker, et al. 2008). To facilitate synthesis, most facilitationstudies report means and conventional statistics but also present the relative interaction intensity (rii), which is an effect size metricproposed by Armas, et al. 2004 that allows easy cross- comparison between response variables, species, or different studies. It has alsobecome accepted that facilitation can shape evolution; for an excellent review on facilitation and evolution, see Thorpe, et al. 2011.Extensions of this thinking have led to more speculative papers, such as group selection and facilitation (McIntire and Fajardo 2011),that would not have been accepted by the peer review community even several years ago. Finally, phylogenetics has also become apart of the contemporary thinking, with respect to facilitation as a means of contrasting nurse versus beneficiary species. For excellentexamples on early-21st-century thinking on this topic, see any of the more recent papers by Valiente-Banuet (Valiente-Banuet, et al.2006 and Valiente-Banuet and Verdú 2007 are good starting points on phylogenetics and facilitation). The field is, of course, stillmaturing; many of the lessons learned in plant competition are being applied more quickly to the newer field of facilitation, and,importantly, the implications of these and other views are being cast in the light of climate change, invasion, and disturbance.

Armas, Cristina, Ramón Ordiales, and Francisco I. Pugnaire. 2004. Measuring plant interactions: A new comparative index.Ecology 85.10:2682–2686.

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This paper develops the effect size metric, which has been widely adopted by most facilitation studies in reporting results. The primaryadvantage of this metric is that it is bounded and symmetric around 0. Available online for purchase or by subscription.

Brooker, Rob W., and Zaal Kikvidze. 2008. Importance: An overlooked concept in plant interaction research. Journal of Ecology96.4: 703–708.

The relevance of intensity versus importance is explained in depth. This paper illustrates the value in ascertaining impact versuspresence of an interaction in a given context.

Brooker, Rob, Zaal Kikvidze, Francisco I. Pugnaire, et al. 2005. The importance of importance. Oikos 109.1: 63–70.

This is the original proposition of the relative difference between importance and intensity in modern facilitation studies, which has tosome extent resolved the debate concerning the importance of facilitation despite its sometimes being weak in intensity. Available onlinefor purchase or by subscription.

Brooker, Rob W., Fernando T. Maestre, Ragan M. Callaway, et al. 2008. Facilitation in plant communities: The past, the present,and the future. Journal of Ecology 96.1: 18–34.

An excellent and balanced summation of past and future research directions in this field. This is the best single reader for a list of futuredirections of research involving facilitation.

McIntire, Eliot J. B., and Alex Fajardo. 2011. Facilitation within species: A possible origin of group-selected superorganisms.American Naturalist 178.1: 88–97.

An example of the extensions derived from the study of facilitation. Available online for purchase or by subscription.

Thorpe, Andrea S., Erik T. Aschehoug, Daniel Z. Atwater, and Ragan M. Callaway. 2011. Interactions among plants andevolution. Journal of Ecology 99.3: 729–740.

A clear review of how facilitation relates to evolution.

Valiente-Banuet, Alfonso, Adolfo Vital Rumebe, Miguel Verdú, and Ragan M. Callaway. 2006. Modern Quaternary plant lineagespromote diversity through facilitation of ancient Tertiary lineages. Proceedings of the National Academy of Sciences 103.45:16812–16817.

The first example of facilitation over evolutionary time scales and the first application of phylogenetics to contrast nurse versusbeneficiary species.

Valiente-Banuet, Alfonso, and Miguel Verdú. 2007. Facilitation can increase the phylogenetic diversity of plant communities.Ecology Letters 10.11: 1029–1036.

Another excellent example of the application of phylogenetics to facilitation in community ecology and the subsequent implications thatscale, either through time or to larger scales. Available online for purchase or by subscription.

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Ecological Theory

The implications for 21st-century theory are succinctly and accurately described in a comprehensive review by Brooker, et al. 2008. Thefirst table in this paper lists seminal works that link to the dominant theories in ecology and evolution. As one might expect, facilitation,although a relatively new subdiscipline, has passed a critical threshold in both volume and individual complexity within studies so as tomake worthwhile contributions to theory development. In the early 21st century every major aspect of community theory has been linkedto facilitation, but there are still few papers within each area. As a highlight and starting point that began the search for linkages totheory, Bruno, et al. 2003 was the first paper to challenge ecologists to integrate findings from facilitation research into dominanttheories. This is a great first paper to read in beginning a study on facilitation and theory. Initially, of course, there was some resistanceto the inclusion of facilitation into mainstream theory, and this debate is well summarized in a report in Science by Shouse (Shouse2003). We have, however, generally moved past this and generated new debates. A second great paper, and perhaps the best exampleof how facilitation can reshape theory, is Michalet, et al. 2006, wherein facilitation is applied to the intermediate disturbance hypothesis,a keystone theory in ecology and in all ecology textbooks. This paper shows that the patterns of diversity are better explained with theaddition of facilitation. Perhaps the next best point for reading to appreciate contributions to theory would be Michalet and Touzard 2010.The niche is a dominant theory in ecology, and links to understanding how facilitation reshapes our use of the niche are well explained;with this understanding one can easily envisage how facilitation relates to climate change, diversity, and so on. Finally, with theincreasing application of meta-analyses and systematic reviews in ecology and evolution, and with the volume of papers being sufficient,we can expect to see more synthesis of sets of facilitation studies. Hence, a good reader on how to apply synthesis to facilitation studieseffectively, given that some aspects of these studies are unique (i.e., are mainly gradient based, often assume stress, and often usenurses), can be found in Lortie and Callaway 2006. More synthesis and direct examinations of the implications of facilitation will andmust necessarily occur, so it is instructive to examine some of these first attempts and underpinnings.

Brooker, Rob W., Fernando T. Maestre, Ragan M. Callaway, et al. 2008. Facilitation in plant communities: The past, the present,and the future. Journal of Ecology 96.1: 18–34.

A clear summary of empirical studies, as they relate to theory.

Bruno, John F., John J. Stachowicz, and Mark D. Bertness. 2003. Inclusion of facilitation into ecological theory. Trends inEcology and Evolution 18.3: 119–125.

The first paper to challenge ecologists to revise theories in light of facilitation. Most major theories of ecology and evolution arereinterpreted in these terms. Available online for purchase or by subscription.

Lortie, Christopher J., and Ragan M. Callaway. 2006. Re-analysis of meta-analysis: Support for the stress-gradient hypothesis.Journal of Ecology 94.1: 7–16.

A critique and summary of how to apply synthesis to facilitation studies. This is a good primer for beginners to meta-analysis in ecologyand evolution, although the literature has rapidly evolved with respect to meta-analyses. Hence, it is primarily useful for those interestedin examining gradient or facilitation studies broadly in community ecology.

Michalet, Richard, Robin W. Brooker, Lohengrin A. Cavieres, et al. 2006. Do biotic interactions shape both sides of the

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humped-back model of species richness in plant communities? Ecology Letters 9.7: 767–773.

The first highly novel application of facilitation to mainstream theory, namely, the intermediate disturbance hypothesis. This paper positsthat facilitation likely modifies the shape of this curve to extend species into more disturbed habitats than they would likely be able totolerate, thereby increasing diversity. Available online for purchase or by subscription.

Michalet, Richard, and Blaise Touzard. 2010. Biotic interactions, biodiversity, and community productivity. In Positive plantinteractions and community dynamics. Edited by Francisco I. Pugnaire, 59–78. Boca Raton, FL: CRC.

An excellent chapter explaining how facilitation relates to niche, disturbance, and productivity.

Shouse, Ben. 2003. Conflict over cooperation. Science 299.5507: 644–646.

A summary of the initial resistance to include facilitation in mainstream theory. Available online for purchase or by subscription.

Experimental and Analytical Approaches

The sets of experiments and approaches (or toolbox) available to the ecologist studying facilitation are not as extensive as the onesassociated with plant competition. Plant competition can be studied through increasing resources, changing density, doing additions orremovals, monitoring target species, or introducing phytometer species (i.e., species as a biotic measure of the effect of the communityor environment). Gibson, et al. 1999 is an excellent first-read paper, summarizing effective designs to test for competition, but there aremany others. In contrast, facilitation studies usually have a more limited palette of approaches, although this is rapidly changing.Kikvidze and Armas 2010 details the experimental designs and explains the most common effective size metric adopted by facilitationstudies in the early 21st century for estimating the sign and magnitude of facilitation. In brief, more than 40 percent of facilitation studiesuse nurse plant species, and the majority of these studies are mensurative, using surveys under shrubs (or associated with the nurse insome way), relative to open sides, without the nurse or a dominant canopy. Two systematic reviews accurately summarize theimportance of nurse plants and explain the general approach (Flores and Jurado 2003, Arredondo-Núñez, et al. 2009). The mostcommon metric, relative interaction intensity (Armas, et al. 2004), calculates the relative difference in the benefit of cushion to the open,or noncanopy, site (or without neighbors) and is predicated upon the assumption that either treatments or surveys are conducted in pairs(cushion versus open). The importance versus the intensity of the interaction is also sometimes calculated, and the means to do so isprovided in Brooker, et al. 2005. Unfortunately, the method requires that a phytometer species be included in the experimental designand at this point has not been widely adopted. Another alternative methodology is neighbor removal; the best and most cited examplewas published in Nature, in 2002 (Callaway, et al. 2002). This study is highly cited because of strengths in its design, including thefollowing: neighbor removal via aboveground clipping of all plants within 10 centimeters of a target, selection of three to ten targetspecies at each site, and replication at a high and low elevation at each location. This design was then replicated cross-continentally ateleven locations. Unlike most plant competition removal studies, the neighborhood is removed instead of a dominant competitor, and theresponse of the target species left intact, with and without neighbors, is compared. Importantly, removing all nearby plants that caneither act as competitors or facilitators concurrently with the two elevations (low and high) permits a test for a potential shift ininteractions from negative to positive sensu the stress gradient hypothesis, with lower elevations being less limited and morecompetitive. Finally, the general suite of methodologies used in plant competition studies could be applied to the study of facilitation.More recently, density as a tool to test for facilitation has been explored in simulation models (Xiao, et al. 2009) and in the field(Wyszomirski and Weiner 2009).

Armas, Cristina, Ramón Ordiales, and Francisco I. Pugnaire. 2004. Measuring plant interactions: A new comparative index.

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Ecology 85.10:2682–2686.

This paper develops the most common effect size metric used in facilitation studies. The metric is a simple ratio, but the paper alsoprovides an assessment of its relative merits to other metrics in the early 21st century. Available online for purchase or by subscription.

Arredondo-Núñez, A., E. I. Badano, and R. O. Bustamante. 2009. How beneficial are nurse plants? A meta-analysis of theeffects of cushion plants on high-Andean plant communities. Community Ecology 10.1: 1–6.

A meta-analysis of cushion plants (nurse species) and its efficacy as a facilitator and generalist in the alpine. This is a useful paper inthat it very effectively applies meta-analytical statistics and clearly demonstrates the capacity for other life-forms, in addition to shrubs, toact as benefactors.

Brooker, Rob W., Zaal Kikvidze, Francisco I. Pugnaire, et al. 2005. The importance of importance. Oikos 109.1: 63–70.

Develops a metric to disentangle importance from intensity, as intensity can sometimes be low, but importance, high. Available online forpurchase or by subscription.

Callaway, Ragan M., R. W. Brooker, Philippe Choler, et al. 2002. Positive interactions among alpine plants increase with stress.Nature 417:844–848.

The most-cited empirical study demonstrating facilitation on gradients uses neighbor removal to explore facilitation and competition. Thestudy is cross-continental and includes many different species and two elevations at each species location.

Flores, Joel, and Enrique Jurado. 2003. Are nurse–protégé interactions more common among plants from arid environments?Journal of Vegetation Science 14.6: 911–916.

A clear, systematic review of the frequency of facilitation by nurse plants. Available online for purchase or by subscription.

Gibson, David J., John Connolly, David C. Hartnett, and Jeffrey D. Weidenhamer. 1999. Designs for greenhouse studies ofinteractions between plants. Journal of Ecology 87.1: 1–16.

A classic paper explaining effective designs for testing competition between plants. This is likely one of the most useful starting points forreading about effective experimental design when examining the interactions in plants. Available online for purchase or by subscription.

Kikvidze, Zaal, and Cristina Armas. 2010. Plant interaction indices based on experimental plant performance data. In Positiveplant interactions and community dynamics. Edited by Francisco I. Pugnaire, 17–37. Boca Raton, FL: CRC.

A clear chapter explaining the study of interactions (competition and facilitation) from methodology and statistical estimate perspectives.

Wyszomirski, Tomasz., and Jacob Weiner. 2009. Variation in local density results in a positive correlation between plantneighbor sizes. American Naturalist 173.5: 705–708.

An exemplar of the relative importance of considering positive interactions when changing density in populations or communities.

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Xiao, Sa, Richard Michalet, Gang Wang, and Shu-Yan Chen. 2009. The interplay between species’ positive and negativeinteractions shapes the community biomass–species richness relationship. Oikos 118.9: 1343–1348.

A simulation model examining whether increasing disturbance can increase diversity (and includes consideration of density, to a limitedextent). Available online for purchase or by subscription.

Gradients

The stress gradient hypothesis is a major hypothesis commonly tested in facilitation studies. Bertness and Callaway 1994 first proposedit. Many studies have tested this hypothesis subsequent to its proposal, yet there remains some confusion regarding its specificapplication. The frequency of positive interactions was predicted to increase with increasing abiotic stress or consumer pressure—meaning only that facilitation is more likely to be found at these ends of a relative continuum. Clearly, more than one point in anenvironment must be measured to constitute a gradient, and although it is common to measure only the extremes in a given study, suchas high and low stress sites, failure to detect facilitation is difficult to interpret with only two points. The interpretation that the stressgradient hypothesis is supported using only one point is also common and largely incorrect. Detecting facilitation in a stressfulenvironment is certainly support for the argument that facilitation is an important process to consider in the study of species interactionsbut not necessarily that it increases in frequency with stress. By way of example, Maestre, et al. 2005 is a meta-analysis of all studies inarid and semiarid environments testing this hypothesis and is excellent beginning reading on the use of gradients in studying facilitation.In sum, the study and identification of a positive interaction between different species of plants are support for facilitation but notnecessarily for the stress gradient hypothesis. A gradient, or directional variation, in a suite of abiotic factors, or consumer pressure,must be identified, and for this specific hypothesis to be examined effectively, experiments must include contrasts of the frequency ofpositive versus negative interactions. A more recent book chapter on the subject examines the use of gradients in general, focuses onfacilitation, and provides formal definitions of all relevant terms (Lortie 2010). Probably the most critical refinement to the theory isMichalet 2007, wherein more effective experimental tests are needed for this hypothesis. It is uncommon for studies of facilitation to usegradients and not refer to this hypothesis. However, most gradients in this body of literature use only the two endpoints of anenvironmental gradient and not more. This must change and is changing with the advent of larger, regional-level experiments incommunity ecology. As a final note, the concept of stress is often assumed and not frequently well defined. This has been debated, witha critique of the concept (Körner 2003) and a rebuttal (Lortie, et al. 2004). There is little evidence that this debate reshaped or improvedthe use of stress in community ecology, but gradients in this field are being more accurately measured, which will de facto resolve theissue.

Bertness, Mark D., and Ragan Callaway. 1994. Positive interactions in communities. Trends in Ecology and Evolution 9.5: 191–193.

The stress gradient hypothesis is proposed, which is often tested in facilitation studies. Available online for purchase or by subscription.

Körner, C. 2003. Limitation and stress—always or never? Journal of Vegetation Science 14.2: 141–143.

The use of the term stress is criticized in community ecology and facilitation studies. Available online for purchase or by subscription.

Lortie, Christopher J. 2010. Synthetic analysis of the stress–gradient hypothesis. In Positive plant interactions and communitydynamics. Edited by Francisco I. Pugnaire, 125–147. Boca Raton, FL: CRC.

The use of gradients is explained and defined, as they relate to the study of facilitation.

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Lortie, Christopher J., Rob W. Brooker, Zaal Kikvidze, and Ragan M. Callaway. 2004. The value of stress and limitation in animperfect world: A reply to Körner. Journal of Vegetation Science 15.4: 577–580.

A rebuttal of Körner 2003. Available online for purchase or by subscription.

Maestre, Fernando T., Fernando Valladares, and James F. Reynolds. 2005. Is the change of plant–plant interactions with abioticstress predictable? A meta-analysis of field results in arid environments. Journal of Ecology 93.4: 748–757.

The first and, in the early 21st century, only meta-analysis of the stress gradient hypothesis. The hypothesis is not supported based onthese analyses, yet facilitation is common in these ecosystems.

Michalet, Richard. 2007. Highlighting the multiple drivers of change in interactions along stress gradients. New Phytologist173.1: 3–6.

A refinement of the stress gradient hypothesis, with clear recommendations on how to improve future experiments.

Community Structure

In the early 21st century, most aspects of community structure, as they are impacted by facilitation, have been explored. Diversity is wellexplained in the book chapter Cavieres and Badano 2010 and in several papers (Butterfield 2009, Cavieres and Badano 2009).Productivity has been examined in the book chapter Michalet and Touzard 2010 and also directly in the more recent paper Brooker2006. Community assembly, however, has only been explored indirectly, through a review of the importance of multitrophic facilitation,van der Putten 2009, and through studies of indirect interactions, such as the classic paper Tielborger and Kadmon 2000. Studyingfacilitation and interactions at the local scale to assess community structure has been criticized (Ricklefs 2008), but a more balancedview of both regional and local studies likely generates the best set of facilitation studies examining factors that influence structure(Brooker, et al. 2009).

Brooker, Rob W. 2006. Plant–plant interactions and environmental change. New Phytologist 171.2: 271–284.

Facilitation, productivity, and stress are all linked to climate change and community structure.

Brooker, Rob W., Ragan M. Callaway, Lohengrin A. Cavieres, et al. 2009. Don’t diss integration: A comment on Ricklefs’sdisintegrating communities. American Naturalist 174.6: 919–927.

An analysis of the concerns expressed in Ricklef 2008 over the use of local interactions to study community structure. Available onlinefor purchase or by subscription.

Butterfield, B. J. 2009. Effects of facilitation on community stability and dynamics: Synthesis and future directions. Journal ofEcology 97.6: 1192–1201.

Diversity and facilitation are linked to examine stability and dynamics in communities.

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Cavieres, Lohengrin A., and Ernesto I. Badano. 2009. Do facilitative interactions increase species richness at the entirecommunity level? Journal of Ecology 97.6: 1181–1191.

The impacts of facilitation on species diversity, one of the most important measures of community structure in the research climate, arereviewed.

Cavieres, Lohengrin A., and Ernesto I. Badano. 2010. Consequences of facilitation on species diversity in terrestrial plantcommunities. In Positive plant interactions and community dynamics. Edited by Francisco I. Pugnaire, 39–58. Boca Raton, FL:CRC.

Similar to Cavieres and Badano 2009, this chapter examines the role of facilitation in shaping diversity of plant communities.

Michalet, Richard, and Blaise Touzard. 2010. Biotic interactions, biodiversity, and community productivity. In Positive plantinteractions and community dynamics. Edited by Francisco I. Pugnaire, 59–78. Boca Raton, FL: CRC.

The importance of facilitation to productivity is explicitly discussed in this chapter, both conceptually and through review of studies.

Ricklefs, Robert E. 2008. Disintegration of the ecological community. American Naturalist 172.6: 741–750.

This paper expresses significant concerns over the use of local interactions, whether competition or facilitation, in understanding factorsthat determine plant community structure.

Tielbörger, Katja, and Ronen Kadmon. 2000. Indirect effects in a desert plant community: Is competition among annuals moreintense under shrub canopies? Plant Ecology 150.1–2: 53–63.

A classic paper testing for indirect interactions caused by overarching facilitation by a nurse plant. Few studies examine indirectinteractions, and this is a perfect model for how this can be done.

van der Putten, Wim H. 2009. A multitrophic perspective on functioning and evolution of facilitation in plant communities.Journal of Ecology 97.6: 1131–1138.

A review of the importance of considering more than one trophic level in more fully appreciating the consequences of facilitation oncommunity structure.

Evolution

An increasing number of papers have explored the linkages between facilitation and evolution. One of the first (Scheffer and van Nes2006) examined whether indirect facilitation can promote the evolution of niche overlap, whereas Valiente-Banuet, et al. 2006 firstdemonstrated facilitation over evolutionary time scales in a study using phylogenetics and traits. Bronstein 2009 provides a delightfultreatment of the relationship of facilitation to mutualism and clarifies the confusion around terminology, and Verdú, et al. 2009 similarlyrelates facilitation to success and community change over time. The best single reader, however, is a comprehensive essay review

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providing an overview of both the history and research lines of facilitation and evolution (Thorpe, et al. 2011).

Bronstein, Judith L. 2009. The evolution of facilitation and mutualism. Journal of Ecology 97.6: 1160–1170.

Clear explanation of how facilitation and mutualism relate and under what conditions you would use each.

Scheffer, Marten, and Egbert H. van Nes. 2006. Self-organized similarity, the evolutionary emergence of groups of similarspecies. Proceedings of the National Academy of Sciences 103.16: 6230–6235.

The importance of indirect facilitation is linked to niche evolution.

Thorpe, Andrea S., Erik T. Aschehoug, Daniel Z. Atwater, and Ragan M. Callaway. 2011. Interactions among plants andevolution. Journal of Ecology 99.3: 729–740.

A perfect first reader for an overview and future directions of facilitation and evolution. Available online for purchase or by subscription.

Valiente-Banuet, Alfonso, Adolfo Vital Rumebe, Miguel Verdú, and Ragan M. Callaway. 2006. Modern Quaternary plant lineagespromote diversity through facilitation of ancient Tertiary lineages. Proceedings of the National Academy of Sciences 103.45:16812–16817.

The first in a series of paper examining whether facilitation occurs over evolutionary time scales (it does).

Verdú, Miguel, Pedro J. Rey, Julio M. Alcántara, Gemma Siles, and Alfonso Valiente-Banuet. 2009. Phylogenetic signatures offacilitation and competition in successional communities. Journal of Ecology 97.6: 1171–1180.

Changes in communities over longer time scales (but not necessarily evolutionary) are examined, and succession is used as a means oftesting for facilitation.

Applications

Facilitation research, as it relates to community structure, has significant potential to speak to several applied issues facing the planet:climate change, invasive species, and restoration ecology. The topic of climate change and the framework that facilitation studies willimpose is developed in Brooker 2010, but there are few studies formally linking the two. The same applies to invasion into plantcommunities and facilitation, with limited studies in the early 21st century, but the literature is well reviewed in chapter 6 of Callaway2007 and in Bulleri, et al. 2008. Finally, restoration ecology is likely the issue most directly related to facilitation and is explained in thesection Restoration Ecology.

Brooker, Rob W. 2010. Plant communities, plant–plant interactions, and climate change. In Positive plant interactions andcommunity dynamics. Edited by Francisco I. Pugnaire, 99–124. Boca Raton, FL: CRC.

A review of climate change theory and facilitation is provided in this book chapter.

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Bulleri, Fabio, John F. Bruno, and Lisandro Benedetti-Cecchi. 2008. Beyond competition: Incorporating positive interactionsbetween species to predict ecosystem invisibility. PloS Biology 6.6: 1136–1140.

The best paper to frame facilitation conceptually in invasion theory.

Callaway, Ragan M. 2007. Positive interactions and community organization. In Positive interactions and interdependence inplant communities. By Ragan M. Calloway, 295–333. Dordrecht, The Netherlands: Springer.

The research on invasion and facilitation is reviewed, along with a brief description of how facilitation can relate to invasion conceptually(pp. 315–318).

RESTORATION ECOLOGY

Restoration is likely the most direct use of pure facilitation studies for management and effecting change, as they relate to human-induced modifications in community structure. The first study to link nurse plant species directly to restoration, both conceptually andempirically, was Maestre, et al. 2001, which showed, in a novel twist, that grasses can facilitate shrubs (it is generally assumed thatgrasses act solely as competitors in interactions with other plants, whereas shrubs mostly act as benefactor species, not beneficiaries).Arid, semiarid, and Mediterranean systems are highly amenable in general to the use of facilitation through nurse plants to maintainplant diversity in a changing and warming climate (Castro, et al. 2004, Padilla and Pugnaire 2006). Facilitation also has a role in forestsystems, with the trees as the beneficiary species (not the nurse itself), and this has been both demonstrated specifically by Gómez-Aparicio, et al. 2004 and formally reviewed by meta-analysis, including all relevant studies as well as direct tests of the method (Gómez-Aparicio 2009). There is no reason to expect that restoration plans will not now include nurse plants or studies that documentnonrandom patterns of associations of species with other plant species, such as enjoyment by the mangrove species of reduced stressfrom microhabitats generated by more salt-tolerant species (Milbrandt and Tinsley 2006).

Castro, Jorge, Regino Zamora, José A. Hódar, José M. Gómez, and Lorena Gómez-Aparicio. 2004. Benefits of using shrubs asnurse plants for reforestation in Mediterranean mountains: A 4-year study. Restoration Ecology 12.3: 352–358.

Shrubs are shown as a means of reforesting degraded steppe systems. Available online for purchase or by subscription.

Gómez-Aparicio, Lorena. 2009. The role of plant interactions in the restoration of degraded ecosystems: A meta-analysisacross life-forms and ecosystems. Journal of Ecology 97.6: 1202–1214.

A systematic review of the literature that supports using facilitation to reforest appropriately impacted ecosystems.

Gómez-Aparicio, Lorena, Regino Zamora, José M. Gomez, José A. Hódar, Jorge Castro, and Elena Baraza. 2004. Applying plantfacilitation to forest restoration: A meta-analysis of the use of shrubs as nurse plants. Ecological Applications 14.4: 1128–1138.

One of the best examples of facilitation’s contradicting the incorrect dogma that trees and shrubs must compete. The implication is thatfacilitation should be considered in most restoration efforts.

Maestre, Fernando T., Susana Bautista, Jordi Cortina, and Juan Bellot. 2001. Potential for using facilitation by grasses to

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establish shrubs on a semiarid degraded steppe. Ecological Applications 11.6: 1641–1655.

An empirical study that concludes that dominant grasses can also serve as nurse plants for shrubs, which is surprising. Available onlinefor purchase or by subscription.

Milbrandt, E. C., and M. N. Tinsley. 2006. The role of saltwort (Batis maritima L.) in regeneration of degraded mangrove forests.Hydrobiologia 568.1: 369–377.

An example of an associational study that has restoration implications, given that mangrove populations are declining.

Padilla, Francisco M., and Francisco I. Pugnaire. 2006. The role of nurse plants in the restoration of degraded environments.Frontiers in Ecology and the Environment 4.4: 196–202.

Facilitation is proposed as a natural mimic for habitat amelioration, similar to bioremediation studies associated with pollution but insteadapplied to plant–plant interactions and communities. Available online for purchase or by subscription.

LAST MODIFIED: 05/23/2012

DOI: 10.1093/OBO/9780199830060-0048

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