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Environmental Stress, Facilitation, Competition, and Coexistence Ecology, 94(12), 2013, pp. 2719–2731 Ó 2013 by the Ecological Society of America Environmental stress, facilitation, competition, and coexistence 1,3 1,2 SIMON P. HART AND DUSTIN J. MARSHALL 1School of Biological Sciences, University of Queensland, Queensland 4072 Australia 2School of Biological Sciences, Monash University, Clayton, Victoria 3800 Australia Abstract. The major theories regarding the combined influence of the environment and species interactions on population and community dynamics appear to conflict. Stress/ disturbance gradient models of community organization, such as the stress gradient hypothesis, emphasize a diminished role for competition in harsh environments whereas modern coexistence theory does not. Confusion about the role of species interactions in harsh environments is perpetuated by a disconnect between population dynamics theory and data. We linked theory and data using response surface experiments done in the field to parameterize mathematical, population-dynamic competition models. We replicated our experiment across two environments that spanned a common and important environmental stress gradient for determining community structure in benthic marine systems. We generated quantitative estimates of the effects of environmental stress on population growth rates and the direction and strength of intra- and interspecific interactions within each environment. Our approach directly addressed a perpetual blind spot in this field by showing how the effects of competition can be intensified in stressful environments even though the apparent strength of competition remains unchanged. Furthermore, we showed how simultaneous, reciprocal competitive and facilitative effects can stabilize population dynamics in multispecies communities in stressful environments. Key words: Bugula neritina; competition; competition coefficients; environmental stress; facilitation; filter-feeding bryozoans; marine invertebrates; multispecies communities; Ricker model; stress gradient hypothesis; Watersipora subtorquata. INTRODUCTION es with increasing environmental stress (Bruno et al. Because environmental variation is ubiquitous, un- 2003, Callaway 2007, Maestre et al. 2009). Empirical derstanding how changes in the environment influence support has been generated through estimates of the species interactions is crucial for predicting population strength of interspecific interactions between individuals and community dynamics. Many classic (e.g., Connell or surveys of community-wide patterns in the frequency 1978, Grime 1979, Huston 1979) and modern (e.g., of positive and negative interactions along environmen- derivatives of the Menge and Sutherland [1987] stress tal gradients (Callaway 2007, Maestre et al. 2009). This gradient hypothesis; Callaway 2007) theories of com- work has been useful for identifying common patterns in munity dynamics continue to emphasize a diminished the strength and direction (positive vs. negative) of role for competition in harsh environments, but modern species interactions among disparate communities, and species coexistence theory does not (Chesson and Huntly for highlighting the role of facilitation in community 1997, Chase et al. 2002, Violle et al. 2010, Fox 2012). dynamics (Stachowicz 2001, Bruno et al. 2003). How- Understanding how these theories can mutually inform ever, these conceptual theories and the empirical each other is therefore an important goal. methods used to support them are rarely suited to Stress gradient models (commonly called ‘‘stress understanding the consequences of changes in the gradient hypotheses,’’ SGH) of community organization strength and direction of species interactions for the have been important for simplifying the enormous regulation of populations, and therefore for species context dependency of species interactions across coexistence (Freckleton et al. 2009, Siepielski and environmental gradients (Menge and Sutherland 1987, McPeek 2010). For example, stress gradient hypotheses Bertness and Callaway 1994, Angelini et al. 2011). These are often framed in terms of the commonness of theories specifically predict that the frequency and/or particular types of interactions (Maestre et al. 2009), strength of competition declines and facilitation increas- but the commonness of an interaction type across an entire community provides little information on the Manuscript received 17 May 2012; revised 30 April 2013; density-dependent regulation of populations within accepted 11 June 2013. Corresponding Editor: L. Stone. those communities. Furthermore, intraspecific compet- 3 Present address: Institute for Integrative Biology, ETH itive effects are rarely estimated in these studies even Zu¨rich (Swiss Federal Institute of Technology), Universita¨t- strasse 16, 8092 Zu¨rich, Switzerland. though it is the ratio of the strength of population-level E-mail: [email protected] intra- to interspecific effects that determines the outcome 2719 2720 SIMON P. HART AND DUSTIN J. MARSHALL Ecology, Vol. 94, No. 12 of species interactions (Macarthur and Levins 1967, species interactions is a challenge that is rarely met Chesson 2000). empirically (Chesson and Huntly 1997, Freckleton et al. Modern coexistence theory, in contrast, tends to 2009, Siepielski and McPeek 2010). explain community structure as a consequence of the Approaches that allow formal links between mathe- influence of the environment on interspecific interac- matical population demographic theory and data are tions, but also on density-independent processes and ideally suited for quantifying the strength and direction intraspecific interactions (Chesson 2000, Snyder 2008, of species interactions and for determining how these Levine and HilleRisLambers 2009). These mathematical changes affect population dynamics (Inouye 2001, theories demonstrate that environmental gradients, Levine and HilleRisLambers 2009). However, such including stress and disturbance gradients, can promote approaches are rarely replicated across stress gradients. coexistence (Caceres 1997, Bolker and Pacala 1999, Using a classic model system for studying competition— Chesson 2003, Adler et al. 2006, Snyder 2008). benthic marine invertebrates—we replicate a powerful Furthermore, modern coexistence theory does not but rarely used experimental design in the field in two preclude changes in the strength, direction, or frequency strongly contrasting environments that span an impor- of particular types of interspecific interactions in tant natural stress gradient in marine systems. Using our different environments such as those suggested by stress experimental field data, we parameterize a mathematical gradient hypotheses (e.g., Sears and Chesson 2007). model of competitive population dynamics to provide However, coexistence theory provides no a priori quantitative estimates of the direct effects of environ- predictions about the outcome of those interactions mental conditions on density-independent rates of (Chase et al. 2002). In particular, the strength of an increase, and the indirect effects of the environment on interaction cannot be used to determine the importance population dynamics via changes in the direction and of an interaction for population regulation (Freckleton strength of both intra- and interspecific interaction et al. 2009). This is because the direct density- coefficients. We test the predictions of stress gradient independent effects of a harsh environment can make models by evaluating how the strength and direction of a population less tolerant of competition, which means species interactions vary depending on environmental that competitive exclusion can occur more readily in harshness, and we show that the consequences of these harsh environments even though the intensity of changes for competitive population dynamics are not competition may be weaker (Chesson and Huntly straightforward. 1997). Ultimately, coexistence depends on how the MATERIALS AND METHODS environment affects the relative strengths of both intra- and interspecific interactions, and the direct Assemblage, study species, and the environment density-independent effects of the environment on a We studied population dynamics in diverse, subtidal, species’ tolerance to competition (Chesson 2000). sessile marine invertebrate assemblages in which strong Importantly, independent changes in each of these interactions, both competitive and facilitative, are a variables depend strongly on species-specific responses distinctive feature (Buss 1990, Stachowicz and Byrnes to the environment (Angert et al. 2009), an area recently 2006). We were explicitly interested in interactions identified as being crucial for improving stress gradient among early-successional invasive species before they models of community organization (Maestre et al. were largely outcompeted by later-successional domi- 2009). nants (typically after four to six weeks). Therefore, we The foci and underlying motivations behind stress studied competition between two filter-feeding bryozo- gradient hypotheses (e.g., Callaway 2007) and modern, ans: an encrusting species, Watersipora subtorquata, and population dynamic coexistence theories (e.g., Chesson an arborescent species, Bugula neritina. Both species are 2000) are therefore different, but their predictions are invasive and widespread globally and often dominate not necessarily mutually exclusive. Where possible, the recruitment of recently exposed substrata at our field conclusions of these theories might mutually inform site, such that there is strong potential
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