Changes in community phylogenetic structure in a North American forest chronosequence ABIGAIL I. PASTORE AND BRENDAN P. SCHERER Department of Biological Science, Florida State University, Tallahassee, Florida 32306 USA Citation: Pastore, A. I., and B. P. Scherer. 2016. Changes in community phylogenetic structure in a North American forest chronosequence. Ecosphere 7(12):e01592. 10.1002/ecs2.1592
Abstract. Several studies of succession in tropical and subtropical climates include phylogenetic analyses of the plant communities; the majority of these studies find a shift from more closely related to less closely related assemblages over succession. It has been suggested that this pattern indicates a shift from abiotic to biotic filters structuring communities over time, but there is considerable debate surrounding this interpretation. Conducting analyses for multiple components of plant assemblages can provide insight into the processes structuring communities. Here, we present community phylogenetic analyses of a deciduous forest chronosequence for three community components: standing vegetation, seed bank, and vegetation regenerated after small-scale disturbance. We constructed a phylogeny from 228 taxa present in the community data of a chronosequence obtained from previously published research. In the standing vegetation, we found a shift from more closely related to less closely related vegetation over the chronosequence. These results are consistent with other studies of chronosequences in tropical forests, lending support to the ubiquity of such shifts in relatedness over succession under different climatic conditions. However, the seed bank and vegetation regenerated after small-scale disturbance showed no consistent pattern with stand age, suggesting recruits are experiencing different forces than surrounding vegetation. These phylogenetic analyses of seed banks and vegetation regenerated after small-scale disturbance over a chronosequence provide additional evidence into the mechanisms driving forest succession. Key words: abiotic filters; biotic filters; community phylogenetics; disturbance; facilitation; succession; temperate forests. Received 22 July 2016; revised 20 September 2016; accepted 23 September 2016. Corresponding Editor: Debra P. C. Peters. Copyright: © 2016 Pastore and Scherer. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. E-mail:
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INTRODUCTION
explanation for this pattern is that the phylogenetic structure in a community is a consequence of the ecological processes occurring in a system, specifically shifts from abiotic to biotic filters structuring community composition over succession. This is based on the assumption that closely related species are expected to be ecologically more similar because they have shared the majority of their evolutionary history (Harvey and Pagel 1991, Prinzing et al. 2001). Consequently, more closely related species should have similar traits that determine abiotic constraints
Several studies of succession in tropical and subtropical forests investigate phylogenetic patterns of the plant communities. The majority of these studies demonstrate a pattern in which the standing vegetation shifts from assemblages that are more closely related than expected given a regional species pool, to assemblages that are less closely related than expected (Letcher 2010, Letcher et al. 2012, Norden et al. 2012, Whitfeld et al. 2012, Muscarella et al. 2015). A common ❖ www.esajournals.org
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evidence for this mechanism. Additionally, one would expect the standing vegetation to become more similar to the seed bank over time as more distantly related lineages from the seed bank are facilitated and become part of the standing vegetation. Comparing the phylogenetic relationships of several community components of plants may help to distinguish between facilitation and filtering hypotheses to explain the shift from more closely related to less closely related communities seen over succession. However, few studies have investigated phylogenetic patterns in different community components, such as the seed bank, and vegetation regenerated after smallscale disturbances of plants over succession, although Norden et al. (2012) found more diverse seedling assemblages likely drive the patterns in standing vegetation. For example, the seed banks and establishing vegetation are heavily influenced by abiotic constrains such as temperature and humidity of microclimates (De Steven 1991, Holl and Lulow 1997, Rey et al. 2002). If similar abiotic processes determine the standing vegetation, it should be similar to the seed bank and establishing vegetation in composition and community phylogenetic patterns. However, if biotic mechanisms are driving patterns in the vegetation, it may become increasingly dissimilar to the seed bank and establishing vegetation. This study takes advantage of a well-documented chronosequence of plant succession in a temperate North American forest (Snyder 1984, Roberts and Vankat 1991, Vankat 1991, Vankat and Carson 1991, Vankat and Snyder 1991). These comprehensive studies described the extant vegetation, seed bank, and vegetation regenerated after tilling in sites from 2 to over 200 yr since a disturbance. Here, we conduct community phylogenetic analyses on this data set to assess the relationships among different community components of vegetation over a chronosequence. We ask: (1) Do temperate forests show the same community phylogenetic patterns as tropical forests? and (2) Do standing vegetation, seed banks, and vegetation regenerated after small-scale disturbance show the same phylogenetic patterns over the chronosequence? This is a unique study of community phylogenetic analyses performed on the seed bank and
and resource use, and thus should compete strongly for resources (Webb 2000, Webb et al. 2002). If so, early in succession, when abiotic constraints determine establishment, more closely related species would be expected to dominate, whereas later in succession, when competition prevents closely related species from coexisting on shared resources, communities would be composed of more distantly related species. However, it has become clear that there are many ways to violate the assumptions of this conceptual framework, and evidence is accumulating to suggest that such violations may be common (Mouquet et al. 2012). For example, if convergent evolution occurs between distant taxa or divergent evolution occurs between closely related taxa, this relationship will break down (Cahill et al. 2008, Losos 2008, CavenderBares et al. 2009). Additionally, the hypothesis that more closely related species are more likely to exclude each other has been criticized because traits that contribute to the fitness of an organism, when similar between species, promote coexistence through equalizing competitive abilities (Grime 2006, Mayfield and Levine 2010). In fact, in a study where species’ niches and average fitness were quantified, species’ average fitnesses were correlated with phylogeny, but species’ niches were not (Godoy et al. 2014). Finally, it may be a false dichotomy that either abiotic filters or biotic filters are the driver of species composition or that they shift in some regular way through succession; it is more likely that both are acting simultaneously to structure communities (Swenson and Weiser 2014). These criticisms leave the consistent pattern in the phylogenetic structure of plant communities over succession unresolved. However, alternative hypotheses have been proposed (Meiners et al. 2015). Preeminent among these is the hypothesis that facilitation among distantly related clades increases phylogenetic diversity et al. 2009). One mechanism for over time (Verdu this phenomenon is through increasing structural heterogeneity over succession (Lasky et al. 2014, Swenson and Weiser 2014). This could create niches for more species and lead to greater functional and phylogenetic diversity in older stands compared to young stands (Flynn et al. 2011). Comparing species diversity to phylogenetic diversity through succession could provide ❖ www.esajournals.org
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vegetation regenerated after small-scale disturbance in a chronosequence performed in temperate climates.
from any of the plots, including the seed bank and regenerated vegetation plots, could have potentially dispersed to any other stand sometime during the current climatic regime and thus constitute the regional pool; no seedless vascular plants were reported. To construct a phylogeny for this regional species pool, gene sequences were obtained from GenBank (Wheeler et al. 2004). Of the 242 species in the regional pool, at least one, if not all, of the RBCL, MATK, and TRNL gene sequences was obtained for 233 of the species sampled or a congener. Sequences for each gene were aligned separately in SATe (Liu et al. 2009) and adjusted by hand by amino acid sequence, and then, all three genes were concatenated into a supermatrix in MacClade (Maddison and Maddison 2000). A time-calibrated tree was created in Geneious 9.1.2 (Kearse et al. 2012). Due to the high variability in the TRNL region across the angiosperms, all analyses were run with and without the TRNL region. The data set’s parameters were set in BEAUti and then analyzed in BEAST 1.8.3 (Drummond et al. 2012) using the CIPRES Online Portal (Miller et al. 2010). The analysis was run for 100,000,000 generations under an uncorrelated relaxed lognormal clock model, with a GTR substitution model, a gamma-plusinvariant-sites site heterogeneity model, and a YULE speciation tree prior. The data sets with and without the TRNL region did not yield quantitatively different result in the downstream analyses; here, we present the results excluding the TRNL region. The output tree file was then annotated using TreeAnnotator (Drummond et al. 2012) and edited for readability using FigTree (Rambaut 2009). Lastly, trees were analyzed in Tracer (Rambaut and Drummond 2013) to assess effective sample size (ESS) values. All ESS values were above 100, with most being well beyond 200. The calibrations used can be seen in Appendix S2. Each calibration is based on fossil evidence reviewed by n et al. (2015). The tree prior was set as a Magallo normal distribution with a range between 314 and 350, corresponding to the split between gymnosperms and angiosperms described in n et al. (2013). For all other calibrations, Magallo the prior was set as the stem age rather than the crown age, due to fact that our data set did not capture the most basal split within the taxon
METHODS Data set Vankat et al. collected a data set from an oldfield chronosequence in southwestern Ohio in 1980 and published it in a series of papers in 1984 and 1992 (Snyder 1984, Roberts and Vankat 1991, Vankat 1991, Vankat and Carson 1991, Vankat and Snyder 1991). Stands of ages 2, 10, 50, 90 and over 200 yr were chosen for similar microenvironments, and stands ranged in size from 1.5 to 60 ha and were within 4.5 km of each other (Vankat and Snyder 1991). The standing vegetation was sampled in a 1-ha area within each stand. First, the herb layer was sampled nine times throughout 1980 using a 10-pin, 1-m-wide point frame at 50 random locations. Second, trees and shrubs were sampled with the point-quarter method (Vankat and Snyder 1991), hereafter referred to as “standing vegetation.” The standing vegetation data were gathered in two 90-yrold stands, for a total of six stands (Snyder 1984), whereas the vegetation regenerated after tilling a 1-m plot, and the seed bank were only sampled in one stand from each of the five ages. The seed bank was sampled at 10 points in each stand using a 12-cm-deep soil core. Samples were transported to a glasshouse and germinated to identify species present in the seed bank (Roberts and Vankat 1991). Additionally, at each point where the seed bank was sampled, soil was turned to a depth of 20–25 cm in 1.5 9 1.5 m plots (only five plots were turned in the oldest stand). Every two weeks, the vegetation regenerated in 1 m2 of the tilled area (consisting of germinating seeds, regrown tubers and roots) was quantified as species percent cover with a 10-pin, 1-m-wide point frame, hereafter referred to as regenerated vegetation (Vankat and Carson 1991).
Phylogenetic analyses A regional species pool by definition consists of all of the species that have the potential to be present in any of the stands via seed dispersal (Ricklefs 1987). For this analysis, it was assumed that all gymnosperm and angiosperm species ❖ www.esajournals.org
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described. The one exception to this was the Brassicaceae, which was set as a crown age calibration. Branch lengths and between-taxa distances were calculated and exported for analyses in R (R Development Core Team 2013). Scripts were written to calculate mean pairwise phylogenetic distance (MPD; the average branch length between each species pair in a community) and net relatedness index (NRI) for each community. Net relatedness index is a measure of how phylogenetically clustered or evenly spaced taxa within a community are compared to a community that is assembled at random from the regional species pool (Webb 2000, Webb et al. 2002). Both MPD and NRI are measures of phylogenetic diversity in a community; NRI corrects for the effects of species richness on phylogenetic diversity. Standard deviation in MPD and NRI associated with phylogenetic uncertainty was calculated by randomly subsampling 1000 trees after burn-in and calculating MPD and NRI for this subset. Net relatedness index and MPD were calculated separately for the standing vegetation, the seed bank, and the regenerated vegetation in each stand. A linear regression was performed on MPD, NRI, and species richness against age of the stand for the standing vegetation, seed bank, and regenerated vegetation, before and after rarefying data using the vegan package in R (Oksanen et al. 2012). Additionally, 95% confidence intervals were found for NRI to determine whether communities were significantly more clustered or even than a randomly assembled community. Differences in the species composition of standing vegetation, seed bank, and regenerated vegetation over the chronosequence were tested with metaMDS in the vegan package and PERMANOVA (Oksanen et al. 2012).
vegetation, whereas the MPD of seed banks and regenerated vegetation was not correlated with the age of the stand (Fig. 1C, E). Net relatedness index is a measure of how far any community differs in MPD from the null expectation of random communities assembled from the regional pool. No assemblage of standing vegetation, seed bank, or regenerated vegetation was outside of the 95% confidence interval of the null expectation; thus, none were significantly clustered or even in their distribution of relatedness among taxa. Net relatedness index of the standing vegetation in a stand was significantly positively correlated with the age of the stand (Fig. 1B; R2 = 0.799, P = 0.016). The NRI of seed banks and regenerated vegetation of each stand was not correlated with the age of the stand (Fig. 1D). Species richness of the standing vegetation and regenerated vegetation was not correlated with the age of the stand, whereas we find weak support for a negative relationship between the species richness of the seed bank and the age of the stand (Fig. 2; R2 = 0.753, P = 0.056); rarefied data had no significant relationships with stand age. Analyses for the standing vegetation were rerun excluding Juniperus virgiana, which was present in the 50-yr-old stand; this was the only gymnosperm occurrence in all plots. Consequently, MPD and NRI had weaker relationships with the age of the stand (R2 = 0.715, P = 0.034; and R2 = 0.604, P = 0.069, respectively). MetaMDS on two axes had a stress of 0.0738. PERMANOVA revealed significant influences of community type (standing vegetation, seed bank, regenerated vegetation; Fig. 3A; P = 0.014) and stand age (Fig. 3B; P = 0.001) on the composition of the sample, with weak support for a positive interaction between the two factors (P = 0.097).
RESULTS
DISCUSSION
The tree reconstruction (Appendix S1) conforms to the Entrez Taxonomy (Maglott et al. 2005) structure on GenBank with few exceptions. Mean phylogenetic distance, a measure of the relatedness of species within a stand, was significantly positively correlated with the age of the stand (Fig. 1A; R2 = 0.790, P = 0.018) for standing
This study of a North American temperate forest demonstrates a shift in the phylogenetic structure of the standing vegetation from more closely related to less closely related communities over succession. The community phylogenetic patterns of temperate forest succession demonstrated here are consistent with those
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Fig. 1. Phylogenetic diversity of species present in the standing vegetation, seed bank, and vegetation regenerated after a small-scale disturbance over the chronosequence, as measured by mean phylogenetic distance (MPD) (A, B, C) and net relatedness index (NRI) (D, E, F). Solid lines indicate linear regressions with P < 0.05. No values of NRI were significantly more clustered (positive) or even (negative) than a random community assemblage. Gray lines indicate the average value for the regional species pool for MPD and NRI. Error bars are the standard deviation associated with phylogenetic uncertainty.
presented in tropical forests. However, the seed bank and vegetation regenerated after tilling of 1 m2 did not show changes in phylogenetic structure associated with the age of the vegetation stand. Two main hypotheses have been made for such a pattern in the standing vegetation: (1) forces structuring standing vegetation shift from abiotic (such as temperature and humidity) to biotic (such as competition) over succession (Weiher et al. 2011), and (2) facilitation between distantly related species increases with stand age et al. 2009). The results presented here (Verdu are most consistent with shifts in the relative strength of abiotic and biotic stressors over succession due to patterns observed in phylogenetic analyses of the community components, species diversity, and species ordination. Novel evidence for this hypothesis comes from the seed bank and regenerated vegetation, which are less
Fig. 2. Species richness of the standing vegetation, seed bank, and vegetation regenerated after smallscale disturbance in each stand. Dashed lines indicate linear regressions with P < 0.10.
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regenerating after disturbance would become more phylogenetically diverse as this mirrors the pool of species entering the standing vegetation. Additionally, if facilitation of distantly related taxa is the mechanism generating more phylogenetic diversity in the standing vegetation, then there would be a simultaneous increase in the species richness with increasing phylogenetic diversity of the extant vegetation as a consequence of the retention of early successional species with the addition of the distantly related facilitated taxa. This is not consistent with this study as richness peaks in the 50-yr-old stand (Fig. 2), but phylogenetic diversity is highest in the 200-yr-old stand. Furthermore, the hypothesis of facilitation of distantly related taxa is not supported by these data as the seed bank (the pool of possible recruits into the extant vegetation) and the standing vegetation are not becoming more similar over time; instead, we find weak support that they are becoming more dissimilar (Fig. 3). In general, the major limitation of this study is low sample size of stands of vegetation. Although interesting patterns emerge from this study in the seed bank and vegetation regenerated after smallscale disturbance, a more comprehensive study would be necessary to draw conclusions about differences in phylogenetic patterns between these assemblages and the standing vegetation. However, an interesting anomaly of the seed bank itself is that although one might expect the seed bank to be similar to early successional species (Decocq et al. 2004), this was only true in younger stands (Fig. 3). The consequences of differential dispersal abilities could be an interesting avenue for understanding these patterns. Additionally, time is having an effect on the assemblages, suggesting some similar underlying processes may be governing these community components (Fig. 3). As phylogenetic approaches to studying communities have increased in frequency, it has become clear that there are more problems with interpreting these patterns than initially suggested (reviewed in Mouquet et al. 2012). However, when ecologists see patterns repeated consistently in communities, we must ask: What is generating these patterns? Most studies of phylogenetic diversity over succession have been performed in tropical forest regimes, which may be experiencing fundamentality different processes
Fig. 3. NMDS plots of the vegetation, seed bank, and vegetation regenerated after small-scale disturbance (v, s, and r, respectively) in stands of different ages (2, 10, 50, 90, and 200 yr). (A) Convex polygons of community type. (B) Convex polygons of different aged communities.
influenced by competition and more influenced by abiotic stressors such as temperature and humidity (De Steven 1991, Holl and Lulow 1997, Rey et al. 2002). Seed bank and regenerated vegetation relatedness were constant over succession suggesting that there was no predictable change in the regulators of these species pools over succession. On the other hand, if facilitation were driving phylogenetic patterns in the standing vegetation, one would predict that the vegetation ❖ www.esajournals.org
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structuring communities as a consequence of geography and latitudinal diversity gradients. As such, this study, performed in a temperate climate, represents increasing support for the ubiquity of shifts from more closely related to less closely related assemblages over the succession of forests. Additionally, phylogenetic patterns in seed banks and regenerated vegetation have rarely been documented, and offer alternate evidence for mechanisms acting on successional forests. The patterns observed here are consistent with those that would be observed if successional forests are structured by shifts in the relative strength of abiotic and biotic species filters. In light of the challenges associated with interpreting these patterns, it is essential to link plant traits with phylogenetic patterns as well as experimental manipulations to delve into these mechanisms more deeply (Bernard-Verdier et al. 2013, Mason and Pavoine 2013).
De Steven, D. 1991. Experiments on mechanisms of tree establishment in old-field succession: seedling survival and growth. Ecology 72:1076–1088. Decocq, G., B. Valentin, B. Toussaint, F. Hendoux, R. Saguez, and J. Bardat. 2004. Soil seed bank composition and diversity in a managed temperate deciduous forest. Biodiversity and Conservation 13:2485–2509. Drummond, A. J., M. A. Suchard, D. Xie, and A. Rambaut. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29:1969–1973. Flynn, D. F. B., N. Mirotchnick, M. Jain, M. I. Palmer, and S. Naeem. 2011. Functional and phylogenetic diversity as predictors of biodiversity–ecosystem– function relationships. Ecology 92:1573–1581. Godoy, O., N. J. B. Kraft, and J. M. Levine. 2014. Phylogenetic relatedness and the determinants of competitive outcomes. Ecology Letters 17: 836–844. Grime, J. P. 2006. Trait convergence and trait divergence in herbaceous plant communities: mechanisms and consequences. Journal of Vegetation Science 17:255–260. Harvey, P. H., and M. D. Pagel. 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford, UK. Holl, K. D., and M. E. Lulow. 1997. Effects of species, habitat, and distance from edge on post-dispersal seed predation in a tropical rainforest. Biotropica 29:459–468. Kearse, M., et al. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. Lasky, J. R., M. Uriarte, V. K. Boukili, D. L. Erickson, W. John Kress, and R. L. Chazdon. 2014. The relationship between tree biodiversity and biomass dynamics changes with tropical forest succession. Ecology Letters 17:1158–1167. Letcher, S. G. 2010. Phylogenetic structure of angiosperm communities during tropical forest succession. Proceedings of the Royal Society of London, Series B: Biological Sciences 277:97–104. Letcher, S. G., R. L. Chazdon, A. C. S. Andrade, F. Bongers, M. van Breugel, B. Finegan, S. G. Laurance, R. C. G. Mesquita, M. Martınez-Ramos, and G. B. Williamson. 2012. Phylogenetic community structure during succession: evidence from three Neotropical forest sites. Perspectives in Plant Ecology, Evolution and Systematics 14:79–87. Liu, K., S. Raghavan, S. Nelesen, C. R. Linder, and T. Warnow. 2009. Rapid and accurate large-scale coestimation of sequence alignments and phylogenetic trees. Science 324:1561–1564.
ACKNOWLEDGMENTS We would like to thank Scott Steppan for instigating and advising this project in his excellent macroevolution class. We especially thank John Vankat for help locating data and for coordinating the collection of the data set nearly 40 yr ago. Many thanks go to Thomas Miller for insightful discussions. We would also like to thank Jonathan Davies, Nathan Kraft, two anonymous reviewers, and the FSU ecology reading group for providing comments on earlier versions of this manuscript. Additionally, we would like to thank Thomas Miller and the FSU Department of Biological Science for funding.
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Losos, J. B. 2008. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecology Letters 11:995–1003. Maddison, W. P., and D. R. Maddison. 2000. MacClade 4: analysis of phylogeny and character evolution. Version 4.0. Sinauer, Sunderland, Massachusetts, USA. n, S., S. Go mez-Acevedo, L. L. Sanchez-Reyes, Magallo and T. Hernandez-Hernandez. 2015. A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytologist 207:437–453. n, S., K. W. Hilu, and D. Quandt. 2013. Land Magallo plant evolutionary timeline: gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates. American Journal of Botany 100:556–573. Maglott, D., J. Ostell, K. D. Pruitt, and T. Tatusova. 2005. Entrez gene: gene-centered information at NCBI. Nucleic Acids Research 33:D54–D58. Mason, N. W. H., and S. Pavoine. 2013. Does trait conservatism guarantee that indicators of phylogenetic community structure will reveal niche-based assembly processes along stress gradients? Journal of Vegetation Science 24:820–833. Mayfield, M. M., and J. M. Levine. 2010. Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecology Letters 13:1085–1093. Meiners, S. J., M. W. Cadotte, J. D. Fridley, S. T. A. Pickett, and L. R. Walker. 2015. Is successional research nearing its climax? New approaches for understanding dynamic communities. Functional Ecology 29:154–164. Miller, M. A., W. Pfeiffer, and T. Schwartz. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop, GCE 2010. IEEE, Piscataway, New Jersey, USA. Mouquet, N., et al. 2012. Ecophylogenetics: advances and perspectives. Biological Reviews 87:769–785. Muscarella, R., M. Uriarte, T. M. Aide, D. L. Erickson, J. Forero-Monta~ na, W. J. Kress, N. G. Swenson, and J. K. Zimmerman. 2015. Functional convergence and phylogenetic divergence during secondary succession of subtropical wet forests in Puerto Rico. Journal of Vegetation Science 27:283–294. Norden, N., S. G. Letcher, V. Boukili, N. G. Swenson, and R. Chazdon. 2012. Demographic drivers of successional changes in phylogenetic structure across life-history stages in plant communities. Ecology 93:70–82. Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H.
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PASTORE AND SCHERER assembly theory. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 366:2403–2413. Wheeler, D. L., et al. 2004. Database resources of the National Center for Biotechnology Information: update. Nucleic Acids Research 32:D35–D40. Whitfeld, T. J. S., W. J. Kress, D. L. Erickson, and G. D. Weiblen. 2012. Change in community phylogenetic structure during tropical forest succession: evidence from New Guinea. Ecography 35:821–830.
Webb, C. O. 2000. Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. American Naturalist 156:145–155. Webb, C. O., D. D. Ackerly, M. A. McPeek, and M. J. Donoghue. 2002. Phylogenies and community ecology. Annual Review of Ecology and Systematics 33:475–505. Weiher, E., D. Freund, T. Bunton, A. Stefanski, T. Lee, and S. Bentivenga. 2011. Advances, challenges and a developing synthesis of ecological community
SUPPORTING INFORMATION Additional Supporting Information may be found online at: http://onlinelibrary.wiley.com/doi/10.1002/ ecs2.1592/full
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