The Prevalence of Ecological Drift in the Heath Vegetation of South America 1, 2 3 3 J

Community assembly in harsh environments: the prevalence of ecological drift in the heath vegetation of South America 1, 2 3 3 J. L. A. SILVA, A. F. SOUZA, J. G. JARDIM, AND B. T. GOTO

1Programa de Po´s-Graduac¸a˜o em Ecologia, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte 59072-970 Brazil 2Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte 59072-970 Brazil 3Departamento de Botaˆnica e Zoologia, Universidade Federal do Rio Grande do Norte, Natal, Rio Grande do Norte 59072-970 Brazil

Citation: Silva, J. L. A., A. F. Souza, J. G. Jardim, and B. T. Goto. 2015. Community assembly in harsh environments: the prevalence of ecological drift in the heath vegetation of South America. Ecosphere 6(7):111. http://dx.doi.org/10.1890/ ES14-00548.1

Abstract. Metacommunity dynamics is marked by a gradient ranging from pure ecological determinism to pure stochasticity. This gradient encompasses compositional turnover that is governed by ecological drift, selection and dispersal. Here we estimate the influences of selection, dispersal limitation acting in concert with drift, drift acting alone and homogenizing dispersal on the structure of tropical restinga heath vegetation growing under stressful conditions in north-eastern South America. We hypothesize that if abiotic heterogeneity is strong enough, it could select distinct sets of colonizing species from neighbor ecosystems, with stress sensitive species occupying refuges created by abiotic heterogeneity and stress tolerators dominating the more exposed areas. In this case selection would occur at both biogeographical and local scales. Under its prevalence, we expect selection to have a major signature in the woody plant community structure in a phylogenetic null model. Alternatively, if abiotic heterogeneity is not strong enough to impose significant selection, the environment would be homogeneously stressful for the majority of species, and would be dominated species selected at biogeographical scale only. Under its prevalence, we expect drift to have a major signature in the phylogenetic null model. We used an analytical framework based on phylogenetic and community structure null models to assess the relative importance of ecological processes. We also aimed to characterize the ecosystem features that impose selection and dispersal limitation. We found that 95.1% of turnover in composition is attributable to drift, 2.4% to homogenizing dispersal, 2.1% to selection, and just 0.40% to dispersal limitation, thus confirming our Neutrality hypothesis. As expected, both soil and topographic variables influenced metacommunity structure. However, contrary to our prediction, light availability and vegetation structure were also important. The predominance of coarse spatial patterns correlated to topographic and soil properties suggests that coarse differences in wind exposure and associated vegetation and soil factors represent the main selective forces acting on the studied vegetation. The dominance of drift in the assembly of restinga heath vegetation is likely to result from homogeneously stressful environmental conditions and also from the ongoing colonization process that is taking place in the restinga by immigrants from species-rich neighboring ecosystems.

Key words: Brazil; dune ecosystems; neutral dynamics; niche; soil nutrients.

Received 29 December 2014; revised 22 February 2015; accepted 4 March 2015; final version received 31 March 2015; published 15 July 2015. Corresponding Editor: D. P. C. Peters. Copyright: Ó 2015 Silva et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. http://creativecommons.org/licenses/by/3.0/ E-mail: [email protected]

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INTRODUCTION sented by Vellend’s (2010) conceptual framework, which proposes that community assembly is A major goal of community ecology is to based on selection, drift, dispersal, and specia- understand the processes that determine local tion. Selection is the result of deterministic fitness species abundances and the resulting community differences among species due to biotic and structure. Recent developments in this area have abiotic factors; dispersal dictates the intensity of been marked by the attempt to disentangle the individual movement among communities; drift relative importance of deterministic niche-assem- represents stochastic changes in species abun- bly and stochastic processes (Cottenie 2005, dance; and speciation may produce differences in Chase and Myers 2011, Vellend et al. 2014). species richness among communities that do not Variation partitioning analyses of community exchange individuals through dispersal (Vellend structure between environmental and spatial 2010). Speciation is expected to have little components based on Redundancy Analysis has influence within a set of communities connected been associated with deterministic and stochastic through dispersal, known as a ‘metacommunity’ processes, respectively (Borcard et al. 1992, 2011). (Leibold et al. 2004). Species composition turn- Based on this approach, Cottenie (2005) found a over in within a metacommunity is therefore gradient in the distribution of different commu- governed by the combined effects of selection, nity types, with communities structured by dispersal and drift (Stegen et al. 2013). environmental processes and communities with In spite of advances in the characterization of an important independent spatial component at selection through null models (e.g., Chase et al. opposite ends of the same spectrum. Hence, the 2011), a methodological framework for the position of a community along this axis would identification of the relative importance of indicate the relative importance of deterministic multiple processes acting together in ecological and stochastic processes in the assembly of its systems has only very recently been proposed species (Cottenie 2005, Chase and Myers 2011, (Stegen et al. 2013), and has remained so far Logue et al. 2011). Given the recognition of such restricted to microbial communities. Here we gradient, researchers have begun to seek the estimate for the first time the influences of mechanisms able to influence the proportion of selection, dispersal limitation acting in concert determinism and stochasticity in ecological com- with drift, drift acting alone and homogenizing munities (Chase and Myers 2011). Different dispersal on the structure of a community of mechanisms seem to act for distinct species macroscopic organisms. We studied the tropical groups at distinct scales (Driscoll and Linden- restinga heath vegetation growing under stress- mayer 2009). Examples are suggestions that ful conditions in northeastern South America. ecological determinism increases with organism Restinga refers to the heath vegetation that size (Farjalla et al. 2012) and age of ecological covers the South American sandy plains mostly succession (Vellend et al. 2007) and decreases along the approximately 7,000 km of the Brazil- with the size of the regional species pool (Chase ian coast, forming vegetation complexes includ- and Myers 2011). Furthermore, ecological deter- ing open scrubland and short and dense forests minism has been proposed to (Brown et al. 2011) on flat terrain or on dune fields (Oliveira-Filho and indeed found to increase with habitat 2009). Plants colonizing these habitats have heterogeneity and the consequent increase in reduced productivity (Pires et al. 2006) due to available niches (Laliberte´ et al. 2009, Legendre et nutrient-poor soils with poor water retention al. 2009, Baldeck et al. 2012, De Ca´ceres et al. (Brancalion et al. 2012), face strong edaphic 2012). gradients and, in northeastern South America, Methodological (Økland 1999, Gilbert and seasonal water shortage. Heath vegetation is very Bennett 2010, Smith and Lundholm 2010) and young in the South American Atlantic coast, interpretational (Vellend et al. 2014) flaws in colonizing sand deposits mainly in the last 7,000 traditional variance partition analyses have, years (Scarano 2002). The restingas present few however, been identified and cast doubt on the endemics, with most of its species also occurring aforementioned findings. An alternative and in neighbor species-rich ecosystems (Scarano theoretically sounder approach has been repre- 2002). Even though many species have physio-

v www.esajournals.org 2 July 2015 v Volume 6(7) v Article 111 SILVA ET AL. logical features to deal with water shortages, have a major signature in the woody plant high light levels and lack of specialized pollina- community structure. tors seem to constrain the growth and reproduc- We used a combination of phylogenetic and tion of many species (Scarano et al. 2001, Farias et abundance-based null models (Stegen et al. 2013) al. 2006). to test which of the two competing hypotheses Several studies have shown reduced levels of outlined above prevail in the assembly of South both a- and b-diversity among localities that American heath vegetation plant community. experience relatively ‘harsh’ environmental con- Furthermore, we aimed to characterize the ditions, such as higher disturbance or lower ecosystem features that impose selection and productivity (review in Chase 2010). From these dispersal limitation. Since it is a limiting factor in observations, it has been hypothesized that harsh heath forests (Pires et al. 2006, Brady and Weil conditions impose a deterministic filter on 2010, Brancalion et al. 2012), we expect that community assembly if the species pool of the variation in soil nutrients will explain a signifi- harsher environments is a subset of the species cant proportion of community structure, but pool of a more benign environments (Chase 2010, variation in light will not, due to low productiv- Chase and Myers 2011). At smaller scales harsh ity and the consequently relatively low light environments are known to be heterogeneous captured by the short canopies. We also expect systems, with strong temperature, wind, and topography to exert significant influence on humidity gradients produced by rocks, dunes, community structure apart from its influence on and marine effects (Brancalion et al. 2012, Saraiva nutrient variability because of its indirect effects and Souza 2012, Dura´n and Moore 2013, Moe- on solar energy inputs, wind exposure, and slund et al. 2013). While this heterogeneity water availability (Moeslund et al. 2013). imposes clear selective pressure on small and dispersal-limited groups like globose cactus METHODS (Saraiva and Souza 2012), it is unclear what its effects are for the woody vegetation. If abiotic Study area heterogeneity in harsh environments is strong The study was carried out at the Barreira do enough, it could select distinct sets of colonizing Inferno Lauch Center, Parnamirim municipality, species from neighbor ecosystems (Chase and Rio Grande do Norte state, northeastern Brazil Myers 2011), with stress sensitive species (sensu (58540 S, 358100 W; Fig. 1A). The Launch Center Grime and Pierce 2012) occupying refuges belongs to the Brazilian Air Force, and human created by abiotic heterogeneity and stress activities have been restricted to aerospacial tolerators dominating the more exposed areas. research since 1965. The Launch Center’s 19.6- In this case selection would occur at both ha area accompanies the roughly north-south biogeographical and local scales. We will refer coastline along which a set of tall (approximately to this hypothesis as the Selection hypothesis. 80 m high) sand dunes runs parallel to the Under its prevalence, we expect significant shoreline directly inland from the beach. This clustering of ecologically similar species and coastal dune field extends inland for 0.5 to 2.0 segregation of ecologically dissimilar ones, and km, where it is then replaced by a relatively flat selection to have a major signature in the woody sandy plain (approximately 40 m a.s.l.) and by plant community structure. Alternatively, if palaeodunes a few meters high (Muehe 2006). abiotic heterogeneity in harsh environments is Soils are formed by young sediments eroded not strong enough to impose significant selection from the broad and frequently emergent arenitic pressure on community assembly, the environ- bedrock of the Tertiary Barreiras formation ment would be homogeneously stressful for the (SUDENE/DNPEA 1971). They consist of nutri- majority of species, and would be dominated by ent-poor white sand Neosols with patches of red stress tolerators selected at a larger, biogeograph- or yellow Latosols (SUDENE/DNPEA 1971). The ical scale only. We will refer to this hypothesis as climate is tropical with a severe dry season (Aw; the Drift hypothesis. Under its prevalence, we Peel et al. 2007). Trade winds blow from the expect no clustering or segregation of species southeast and may reach 5.1 m s1 (INMET 2014; relative to their ecological similarity, and drift to http://www.inmet.gov.br). Mean annual temper-

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Fig. 1. (A) Geographical situation of the study area in northeastern Brazil. (B) The spatial distribution of the study transects in coastal vegetation areas. Shades of gray correspond to herbaceous (light grey), scrub (medium grey), and forest (dark grey) physiognomies. Numbered ellipses indicate clusters of transects used as small scales. ature is 268C, and mean annual precipitation is was carried through well beyond sampling 1746 mm, concentrated between March and sufficiency in order to assure the sampling of August (INMET 2014). The dry season’s length rare species. Transects were placed perpendicu- (months , 100 mm) experiences considerable larly to pre-existing trails scattered throughout interannual variation (3–9 months) and averages the distinct physiognomies (Fig. 1B). All wood 6.2 months. The vegetation is a mosaic of plants with a diameter at soil level 3.0 cm were herbaceous, scrub and forest restinga (broadleaf numbered and all specimens were collected with semideciduous tropical coastal physiognomies; the exception of lianas. Voucher specimens were Oliveira-Filho 2009). Open herbaceous vegetation deposited at the Rio Grande do Norte Federal occurs mainly along the shore, while forests University Herbarium (UFRN). Three topo- occur mainly on the leeward side of tall dunes graphic attributes were obtained for each plot: and on the valleys between dunes. elevation (the difference in elevation between the highest and lowest plots was 65 m), terrain Data collection convexity (with values from 7.50 to 5.50 m) and Data were collected in 85 5 3 5 m plots slope (with values from 0 to 33.08). The elevation randomly distributed along 17 100-m long of a cell was defined as the mean of the elevation transects (five plots per transect). A rarefaction at the center and four corners of larger 20 3 20 m curve built with the ‘rarefy’ function of the vegan areas surrounding each plot. All values were R package was calculated to assess the complete- measured using Google Earth 7.1.2.2041. Con- ness of the inventory (Appendix: Fig. A1), which vexity was defined as the elevation of the cell’s

v www.esajournals.org 4 July 2015 v Volume 6(7) v Article 111 SILVA ET AL. center minus the mean elevation of the corners Forest. Each species was classified as belonging (Legendre et al. 2009). Slope was measured with to one or more of the above biogeographic a digital clinometer perpendicular to the eleva- regions besides restinga itself by checking its tion contour within each plot midline. geographical occurrence in the Brazilian Flora Several edaphic attributes were collected. checklist (floradobrasil.jbrj.gov.br/2011/index) in Litter depth (with values from 0 to 12.4 cm) March 2014. was measured to the nearest mm at the corners of All statistical analyses were carried out in each plot. Soil compaction (with values from 0.08 RStudio (version 0.98.501; 2012) and the code to to 0.36 mm) was the inverse of penetration depth run the simulations are available as a Supplement. of a 0.5-m long and 0.5-kg aluminum rod We used the analytical framework proposed by released from a height of 1.2 m at the corners Stegen et al. (2013) in order to estimate the relative of each plot (adapted from Morrisey et al. 2003). contributions of selection, drift, dispersal limita- pH, Ca, Mg, Na, K, P, H þ Al, total N, organic tion, and homogenizing dispersal to the commu- matter content, soil conductivity, humidity, and nity assembly of the heath vegetation. Only texture (% clay þ silt) were obtained from three species with five or more individuals were soil-surface samples (0–20 cm depth) collected retained for analyses. The effect of selection was using a soil auger at each plot at haphazard estimated through phylogenetic turnover, which locations and then bulked and subsampled. The is the evolutionary distance separating species organic matter layer was removed before sam- found in one community from species found in a pling. The laboratory methods used for soil second community (Graham and Fine 2008). analyses are detailed in EMBRAPA/CNPS (1997). Phylogenetic signal, whereby habitat preferences Canopy openness was used as a proxy for light of closely related species are more similar to each availability, and was estimated through three other than to the habitat preferences of distant nonoverlapping wide-angle digital photographs relatives, is a requirement for phylogenetic turn- at each plot. The photographs were taken using a over-based evaluation of ecological processes 16-mm lens and a digital still camera (Sony a57, (Cavender-Bares et al. 2009). We tested for Sony Corporation, Japan) during uniformly phylogenetic signal using a phylogenetic tree overcast sky conditions. The camera was leveled produced by Phylomatic 3 (http://phylodiversity. on a tripod at 0.5 m from the soil with the lens net/phylomatic/) using the megatree R20120829. facing straight up. The upper side of the camera Branch lengths were assigned to the initial super- was adjusted for plot side so that the width of the tree using the ‘bladj’ function in Phylocom 4.2 frame of view stretched from one plot side to the with angiosperm nodes aged according to Wik- other. The camera was set at high resolution stro¨m et al. (2001), and single nodes were deleted (resulting in 2448 3 1624 pixels) for all pictures. with the ‘collapse.singles’ function (package Exposure time and aperture were then set ‘phytools’,N¼ 32 species, Appendix: Fig. A2). automatically by the camera. Images were We produced a matrix of phylogenetic distances analyzed with the software Adobe Photoshop with the function ‘cophenetic’ (package ‘picante’). 7.0 (Adobe Systems, San Jose, California, USA) This matrix was then compared to a matrix of following the protocol of Engelbrecht and Herz niche preferences, in which the normalized (2001:211). Undesirable bright spots on leaves, average of each topographic, soil, and light trunks and branches were manually corrected variables weighted by each species abundance before analysis. Throughout this study, we refer (function ‘wascores’;package‘vegan’) was used as to canopy openness, soil and topographic vari- indicative of each species niche (Pei et al. 2011). ables together as environmental variables. We related between-species niche differences to between-species phylogenetic distances using Data analysis Mantel correlograms with permutation-based In order to evaluate the distribution of the significance tests for each of 50 phylogenetic geographic ranges of species found in the studied distance classes. Significance tests were based on area, we used the broad division of Brazilian 999 permutations using the R function ‘mantel. vegetation into Amazon, Caatinga (seasonally correlog’ (package ‘vegan’) with a progressive dry forests), Cerrado (savanna), and Atlantic Bonferroni correction (Legendre and Legendre

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1998) and no distance class cutoff. We found weak coupled with drift should lead to greater than but significant phylogenetic signal across short expected turnover whereas homogenizing dis- phylogenetic distances for five soil variables persal should lead to less than expected turnover (Appendix:Fig.A3).Wethenproceededto (Stegen et al. 2013). Species turnover was estimate phylogenetic turnover using the (abun- estimated using the null model approach pro- dance-weighted) b-mean-nearest taxon distance posed by Chase et al. (2011), which employs the (bMNTD) (Webb et al. 2011). bMNTD quantifies re-scaled Raup-Crick (RC) probability metric the phylogenetic distance between each species in ranging from 1 to 1 to indicate whether local one community and its closest relative in a second communities are more dissimilar (approaching community, and was obtained using the function 1), as dissimilar (approaching 0), or less dissim- ‘comdistnt’ (abundance.weighted ¼ TRUE; pack- ilar (approaching 1), than expected by random age ‘picante’). bMNTD was used to estimate the chance. Local communities were assembled effect of selection on community assembly probabilistically, where the probability of observ- through a null model approach. The degree to ing an individual of a given species was related which bMNTD deviates from a null model to the number of plots occupied by the species. expectation measures the degree to which com- Observed species richness was maintained for munity composition is limited by selection on each community (plot). For a given pair of species ecological niches (Stegen et al. 2013). We communities, each was probabilistically assem- used a null model that randomized species names bled 999 times. The fraction of all pairwise and abundances across the tips of the phylogeny comparisons with (jbNTIj , 2 and RC , 0.95 and recalculated bMNTD. A null distribution of was taken as an estimate for the influence of bMNTD values was obtained repeating this homogenizing dispersal. The fraction of all procedure 999 times. The difference between pairwise comparisons with jbNTIj , 2 and jRCj observed bMNTD and the mean of the null , 0.95 estimates the influence of drift acting distribution was measured in s.d. units of the null alone (Stegen et al. 2013). distribution and was referred to as the b-nearest In order to identify environmental factors that taxon index (bNTI). bNTI values ,2or. þ2 impose selection and dispersal limitation to the indicated significantly less than or greater than heath vegetation metacommunity, we described expected phylogenetic turnover, respectively, and spatial and environmental relationships among both cases would indicate the effect of selection local communities by combining spatial eigen- (Stegen et al. 2013). Lower than expected bNTI vector analysis with measured abiotic variables. indicated that the environmental filter assembled We modeled the spatial variation among com- communities of closely related species, while munities with the principal coordinates of neigh- greater than expected bNTI indicated that diver- boring matrices (PCNM; Borcard and Legendre gent environmental conditions assembled com- 2002). PCNM eigenfunctions represent a spectral munities composed of ecologically distinct set of decomposition of the spatial relationships among species. These expectations assume minimum the grid cells and describe all spatial scales that organismal exchange among local communities can be accommodated in the sampling design. through evolutionary time so that individual See Borcard and Legendre (2002) and Borcard et communities (in this case individual plots) do al. (2011) for further details on this technique. not evolve evolutionarily distinct assemblages in Due to the irregularity of our sampling design, situ (Stegen et al. 2013). The proportion of we added 15 supplementary points to our spatial pairwise plot comparisons with jbNTIj . 2was data to reduce the threshold distance, computed attributed to selection. Pairwise comparisons with the PCNM variables, and removed the supple- jbNTIj , 2 should thus be governed by drift mentary points from the PCNM matrix. This acting alone, dispersal limitation acting alongside ensures that the finest scales are better modeled drift or homogenizing dispersal. (Borcard and Legendre 2002). The largest dis- To disentangle these influences, we quantified tance in a minimum spanning tree linking all species turnover for pairwise community com- plots was computed and used as the truncation parisons that were not governed by selection value. Forward selection was applied to the (jbNTIj , 2). Within this set, dispersal limitation matrix containing all positive PCNMs in order

v www.esajournals.org 6 July 2015 v Volume 6(7) v Article 111 SILVA ET AL. to select the PCNM eigenfunctions that were Overall vegetation significantly related to the compositional data. A total of 55 species, 39 genera, and 27 families We evaluated the importance of abiotic vari- were found among the 918 individuals sampled ables and spatial eigenvectors to the abundance (Appendix: Table A3). Only four species had of species through a Redundancy Analysis abundances higher than 5% of the total abun- (RDA) (Borcard et al. 2011). To combine all dance, and the seven most abundant species variables and minimize co-variation, we com- represented 50.1% of all stems, characterizing a bined 22 measured biotic and abiotic variables community dominated by rare species (Appen- with spatial eigenvectors using principal compo- dix: Fig. A4). Geographical range could be nents analysis (PCA, see Appendix text for determined for 45 (80.3%) species. Only two further details). The resulting PCA axes (Appen- species (4.4%; Eugenia azeda and Padrosia resting- dix: Table A1) were used as independent ae) were restricted to restinga coastal vegetation. variables in a model-selection procedure with a Only eight (17.8%) of the species were restricted matrix of Hellinger-transformed species abun- to a single vegetation domain, 12 species oc- dances (Legendre and Gallagher 2001) as the curred in two (26.7%) domains, 10 species in dependent variable. Variables were log- or arc three (22.2%), and 14 species (31.1%) occurred in sin-transformed when necessary. Only variables all four vegetation domains (Appendix: Figs. A5 significantly related to the species abundance and A6). matrix through forward selection (function Quantitative process estimates and ‘forward.sel’; package ‘packfor’) were retained environmental relationships for further analysis (Borcard et al. 2011). The We found that 95.1% of turnover in community proportion of variation explained by a set of composition is attributable to drift, 2.4% to variables is given as the adjusted R2 of the homogenizing dispersal, 2.1% to selection, and explanatory variable set in the RDA, which is an just 0.40% to dispersal limitation. The RDA on unbiased estimator that corrects for the number species abundances indicated that environmental of variables in the set (Peres-Neto et al. 2006). and spatial variables together—as represented by the PCA axes—explained a limited amount of RESULTS composition variation (adjusted R2 ¼ 18.7%). The The environmental setting forward selection procedure retained seven of the 36 positive original PCNM eigenfunctions for Environmental variables portrayed loose, salty, modeling species composition. Most (5) of these acidic and low-fertility soils in the studied area were among the first 12 of the 36 PCNM covered by leaf litter with patchy distribution functions, thus representing broad-scale varia- (Appendix: Table A2). Canopies were rather tion, while the remaining eigenfunctions repre- % open,withanaverageof37 visible sky. sented medium scales (PCNMs 17 and 19). Elevation, slope, and to a lesser degree sodium, Despite the reduced influence of selection on soil compaction, and leaf litter, were spatially community turnover, seven PCA axes were auto-correlated at short distances (Fig. 2). These significantly related to species abundance varia- variables thus formed patches of a few hundred tion according to the forward selection procedure meters that were variably aggregated or segre- (Appendix: Table A1). The strongest loadings on gated at different scales. Pairwise correlations these axes were slope, silt/clay content, canopy (not shown) indicated that canopy openness was openness, basal area, soil density, soil H þ Al higher at lower elevations, depicting the presence content, and elevation (Appendix: Table A1). Tree of denser arboreal vegetation on the (leeward) density, aluminum and potassium contents, and slopes of tall dunes, with relatively richer and soil humidity were of practical significance more acidic soils covered by deeper leaf litter, in (loading 0.50; Hair et al. 1998) to the first opposition to the sparsely vegetated inland three axes. No measured environmental variables scrub. Steep dune slopes were also correlated significantly loaded on PC5, PC6, PC7, and PC9, with higher levels of sodium, magnesium, although K and convexity were of practical aluminum, and cation exchange capacity. significance on PC5 and PC6, respectively.

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Fig. 2. Topographic, canopy openness and soil variables and their relationship with distance in the study area. Each map shows the location of 79 sample plots scattered across the study area, with larger circles denoting higher values of each variable. Scale: side of each map ¼ 3 km. Graphs are spatial correlograms showing Moran’sI by distance (m). Filled circles indicate significance (tested by normal approximation).

DISCUSSION neutral communities, dominated by drift. This result confirms our Drift hypothesis, according to Community assembly processes which abiotic heterogeneity in harsh environ- We found that the heath vegetation on dune ments is not strong enough to impose significant fields and sand plains in northeastern South selection pressure, producing a homogeneous America can be regarded as predominantly stressful environment for the majority of species.

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Such environment would be thus dominated by abundant heath vegetation species and no clear stress tolerators selected at a larger, biogeograph- pattern relating performance to local dominance ical scale only. Our results showed that, with or geographic distribution patterns. very few exceptions, species in the northeastern It is worth noting that the dominance of drift in South American heath vegetation are a subset of the assembly of restinga heath vegetation is likely the neighboring biomes of the Atlantic Forest, to result from not only homogeneously stressful Cerrado (savanna), Caatinga (dry forest) and environmental conditions but also from the Amazonia, as suggested by Scarano (2002). The ongoing colonization process that is taking place paucity of species endemic to the heath vegeta- in the restinga by immigrants from species-rich tion, coupled with its reduced species richness neighboring ecosystems (Scarano 2002). Chave relative to surrounding biomes (Scarano 2002) (2004) argued that stochasticity would emerge if indicate that selection occur at large spatial rare species were only occasional in the meta- scales. Thus a deterministic filter based on community, with their presence not being indic- selection to tolerate poor soils and drought ative of a strong match between the individuals’ imposed by sandy soils, seasonal rainfall, and requirements and environmental factors. This strong and persistent winds, is expected to argument seems particularly suited to the heath operate along the South American Atlantic vegetation, with its ongoing colonization process coastal plains. This agrees with the empirically by immigrants from species-rich neighboring based suggestion that the restinga heath vegeta- ecosystems. Many of these recent colonists seem tion to be an edaphically controlled environment maladapted to the harsh conditions of the at large scales (Oliveira et al. 2014). restingas (Scarano et al. 2001, 2005, Farias et al. Scarano (2002) hypothesized that plant coloni- 2006). We thus hypothesize that drift is a zation of habitats marginal to the Atlantic rain dominant process in habitats with ongoing forests was largely related to terrestrial nurse colonization has been found in frequently dis- plants that originally, in the rainforest habitat, turbed habitats (Vandermeer et al. 2004, Keppel were canopy plants such as epiphytes or hemi- et al. 2010). We expect that their presence there is epiphytes. Adaptations to water and nutrient likely to represent more of a transient phenom- restrictions, typical of life in the canopy, would enon than viable populations (i.e., an average have granted success to such plants upon population growth rate ,1.0). migration to sandy substrates in neighboring The apparently limited impact of dispersal areas, where they have been shown to facilitate limitation in our metacommunity system has also colonization by a number of other rainforest been found in Danish coastal-dune metacom- species (Scarano 2002). Our results suggest that munities (Brunbjerg et al. 2012) and may reflect selection to tolerate harsh conditions, like repeat- high habitat continuity and efficient dispersal by ed resprouting in face of chronic disturbance animals and strong winds. Accordingly, the (e.g., Cirne and Scarano 2001) and elevated leaf limited impact of homogenizing dispersal sug- longevity (Grime and Pierce 2012), has also been gests that dispersal is not frequently so high as to imposed upon woody species colonizing the impose mass effects on community structure, heath vegetation. While the well-known hetero- and that the spatial patterns detected through geneity of harsh environments imposes clear PCNM eigenfunctions likely reflect the spatial selective pressure on small and dispersal-limited autocorrelation created by local dispersal in groups like globose cactus (Saraiva and Souza neutral communities (Bell 2001) and not source- 2012), this did not apply for the woody vegeta- sink dynamics (Ng et al. 2009). tion. The prevalence of drift dynamics among woody species implies ecological equivalence Environmental relationships and neutral stochasticity, what means that the In spite of the reduced effect of selection on the individual demographic events which cause assembly of the heath vegetation, several envi- population fluctuations occur at random with ronmental variables showed to subtly affect respect to species identities (Vellend et al. 2014). community structure. Furthermore, two PCA Indeed, Scarano et al. (2005) found wide varia- axes (PC7 and PC9) were selected by the forward tion of ecophysiological performance among procedure despite not having any environmental

v www.esajournals.org 9 July 2015 v Volume 6(7) v Article 111 SILVA ET AL. variable correlated with them. These axes can within them, although sample size precludes us thus be regarded as unmeasured, spatially to test this hypothesis, since ecological determin- structured environmental variable that imposes ism increases with habitat heterogeneity while selection or dispersal limitation (Stegen et al. neutrality should prevail in smaller or more 2013). As expected, both soil and topographic homogeneous habitats (Laliberte´ et al. 2009, variables influenced metacommunity structure. Legendre et al. 2009, Brown et al. 2011, Baldeck However, contrary to our prediction, light et al. 2012, De Caćeres et al. 2012). availability and vegetation structure were also Contrary to most recent studies on community important. Despite the importance of soil nutri- structure determinants in terrestrial plant eco- ents and properties to the variation in tropical systems (Legendre et al. 2009, Baldeck et al. 2012, tree community composition (Baldeck et al. 2012, De Caćeres et al. 2012, Lin et al. 2013), we were Lin et al. 2013), soil factors are not only limiting able to include vegetation cover among explan- (Pires et al. 2006, Brancalion et al. 2012), but also atory variables through canopy openness. Our too homogeneously distributed to impose selec- results showed that it was influential on com- tion on heath vegetation species. A pattern found munity structure, suggesting some role for light in other dune systems and that might also apply partitioning among species colonizing the heath in the heath vegetation we studied is the vegetation, probably reflecting the contrast be- compositional gradient between east- and west- tween the sun-bathed scrub and the leeward facing slopes. Microtopography is known to dune forests, as well as between colonizing affect solar energy inputs, wind exposure, and species originating from open biomes like the water availability (Moeslund et al. 2013), and is Cerrado savannas and the Caatinga dry forests likely responsible for west-facing slopes to be versus forested biomes like the Atlantic forests moister and be covered by forest patches while and the Amazon. east-facing slopes present shorter and open vegetation. The predominance of coarse scales ACKNOWLEDGMENTS in the PCNM eigenfunctions correlated to topographic and soil properties in the PCA suggests Financial support was provided by Fundaçaõde Apoio a` Pesquisa do Estado do Rio Grande do Norte that coarse differences in wind exposure and (FAPERN) through the grant Edital N8005/2011— associated vegetation and soil factors represent Programa Primeiros Projetos IV, and by CAPES the main selective forces acting on the studied through a scholarship to J. L. A. Silva. We thank the heath vegetation. Brazilian Air Force, Aviator Cel. Luiz Guilherme S. Studies carried out in tropical and subtropical Medeiros, and Glauberto Leilson for facilitation of regions have exposed the importance of topog- access to the Barreira do Inferno Launch Center. We raphy in tree community structure (Legendre et are thankful to Amarilys D. Bezerra, A´ tila D.E. Melo, al. 2009, Baldeck et al. 2012, De Caćeres et al. Ange´lica A. Souza, Augusto Ce´sar da Silva, and ç 2012, Lin et al. 2013). This importance is milder, Morvan Fran a for invaluable help in the field. James C. Stegen provided the code for bMNTD/bNTI null however, in flatter (Baldeck et al. 2012, De model and helped with data preparation. Amom Caćeres et al. 2012), more homogeneous (Brown Mendes greatly helped with R code implementation. et al. 2011) habitats. Our results confirm that in A. F. Souza is thankful to TMVS for her patience and relatively flat areas such as the one we studied, support during the writing of this manuscript. where relief is dominated by approximately 40 Comments by Gabriel C. Costa, Gislene M.S. Ganade, m-high dune fields parallel to the sea and Karl Cottenie, Luiz A. Cestaro, and two anonymous smoothly undulated terrain inland, heterogeneity referees greatly helped to improve an earlier version of produces only mild signs in heath vegetation this manuscript. structure. The windward scrub occurring on the foredunes and the leeward forests probably LITERATURE CITED represent the harshest and the mildest commu- Baldeck, C. A., et al. 2012. Soil resources and nities in heath vegetation, respectively, with the topography shape local tree community structure dominant scrub representing intermediate stress in tropical forests. Proceedings of the Royal Society. levels. Selection and dispersal limitation are more doi: 10.1098/rspb.2012.2532 likely to occur among these loose units than Bell, G. 2001. Neutral macroecology. Science 293:2413–

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Phylocom: software for the analysis of phylogenet- Wikstro¨m, N., V. Savolainen, and M. W. Chase. 2001. ic community structure and character evolution Evolution of the angiosperms: calibrating the (with phylomatic and ecoevolve). User’s manual version 4.2. http://www.phylodiversity.net/ family tree. Proceedings of the Royal Society phylocom/ 268:2211–2220.

SUPPLEMENTAL MATERIAL

APPENDIX prior to analysis. Only principal components with eigenvalues 1.0 were retained for analysis Principal components analysis of environmental factors and spatial eigenvectors (Hair et al. 1998). Significance of component To combine all variables and minimize co- loadings was obtained from Hair et al. (1998) variation, we combined 21 measured biotic and based on sample size needed to attain signifi- abiotic variables with spatial eigenvectors using cance based on a 0.05 significance level, a power principal components analysis (PCA). The PCA level of 80% and standard errors assumed to be was based on a correlation matrix using function twice those of conventional correlation coeffi- ‘principal’ of the package Psych 1.3.2 in the RStudio 0.97.320 software. When needed, traits cients. Following Hair et al. (1998), we regarded and vital rates were log-transformed to achieve loadings 0.62 as of statistical significance and normality and all variables were standardized 0.50 as of practical significance.

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Table A1. Loadings of measured environmental variables and PCNM spatial eigenvectors on PCA axes for 79 heath vegetation plots in northeastern Brazil.

Principal component Variable PC2 PC1 PC3 PC5 PC6 PC7 PC9 PC4 PC8 Axis features (%) 12.0 21.0 10.0 7.0 6.0 5.0 4.0 8.0 4.0 Axis features (eigenvalue) 3.3 6.0 2.9 2.0 1.6 1.5 1.1 2.1 1.1 RDA forward (%) 4.7 4.8 2.5 2.4 1.8 1.3 0.8 NS NS RDA forward (P) 0.001 0.001 0.001 0.001 0.001 0.006 0.027 NS NS Basal area 0.08 0.72 0.22 0.25 0.20 0.02 0.01 0.08 0.02 Tree density 0.37 0.61 0.23 0.02 0.22 0.21 0.02 0.24 0.01 Slope 0.62 0.55 0.24 0.27 0.02 0.06 0.02 0.14 0.02 Convexity 0.28 0.19 0.08 0.24 0.50 0.43 0.16 0.10 0.04 Elevation 0.24 0.49 0.63 0.14 0.01 0.04 0.05 0.26 0.11 Soil compaction 0.40 0.28 0.19 0.25 0.18 0.02 0.45 0.37 0.03 pH 0.34 0.01 0.70 0.21 0.02 0.08 0.13 0.43 0.06 Ca 0.48 0.31 0.32 0.06 0.05 0.41 0.04 0.25 0.14 Mg 0.07 0.44 0.21 0.00 0.14 0.36 0.25 0.44 0.24 Al 0.51 0.08 0.53 0.04 0.06 0.00 0.18 0.30 0.20 Na 0.47 0.47 0.06 0.48 0.01 0.12 0.05 0.41 0.06 K 0.19 0.17 0.16 0.56 0.32 0.29 0.04 0.48 0.06 P 0.14 0.56 0.38 0.22 0.16 0.18 0.16 0.34 0.01 HþAl Ccomplex 0.19 0.64 0.37 0.14 0.11 0.20 0.22 0.31 0.04 N 0.01 0.70 0.08 0.39 0.01 0.30 0.04 0.25 0.11 Soil conductivity 0.11 0.60 0.37 0.24 0.23 0.06 0.11 0.41 0.06 Soil density 0.25 0.76 0.07 0.21 0.26 0.10 0.01 0.18 0.10 Soil humidity 0.59 0.43 0.08 0.38 0.03 0.09 0.05 0.07 0.11 Organic matter 0.33 0.67 0.06 0.04 0.09 0.08 0.06 0.31 0.22 Soil texture 0.76 0.12 0.14 0.29 0.30 0.09 0.00 0.10 0.02 Canopy openness 0.16 0.79 0.14 0.05 0.07 0.26 0.05 0.15 0.04 PCNM1 0.37 0.51 0.46 0.30 0.23 0.08 0.06 0.08 0.02 PCNM2 0.54 0.15 0.16 0.60 0.07 0.17 0.05 0.14 0.01 PCNM3 0.07 0.49 0.28 0.03 0.45 0.47 0.13 0.22 0.02 PCNM8 0.24 0.19 0.49 0.10 0.58 0.01 0.30 0.20 0.05 PCNM10 0.11 0.03 0.08 0.09 0.37 0.45 0.49 0.15 0.33 PCNM17 0.00 0.03 0.49 0.04 0.40 0.23 0.43 0.34 0.07 PCNM19 0.19 0.04 0.10 0.07 0.13 0.17 0.20 0.03 0.86 Notes: Percentage of the variance explained [Axis features (%)] and eigenvalues [Axis features (eigenvalue)] of PCA axes, as well as percentage of variance explained [RDA forward (%)] and P values [RDA forward (P)] of forward selection results are shown. Axes are shown in the order of inclusion by the forward procedure. Values in boldface and underlined are of statistical (0.62) and practical (0.5) significance, respectively (Hair et al. 1998). NS means nonsignificant.

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Table A2. Mean and standard deviation of edaphic, Table A3. Woody species and their abundances found topographic and structural variables. at Barreira do Inferno Launch Center restinga, northeastern Brazil. Variable Mean and SD pH 5.64 6 0.49 Family Species Abundance 3 6 Ca (cmolc/dm ) 0.38 0.21 Myrtaceae Myrcia ramuliflora 133 3 6 Mg (cmolc/dm ) 0.33 0.24 Celastraceae Maytenus erythroxyla 95 3 6 Al (cmolc/dm ) 0.01 0.01 Malpighiaceae Byrsonima gardnerana 67 3 6 Na (cmolc/dm ) 0.13 0.08 Polygonaceae Coccoloba ramosissima 43 3 6 K (cmolc/dm ) 0.09 0.06 Rubiaceae Guettarda platypoda 39 3 6 P (cmolc/dm ) 16.59 14.36 Myrtaceae Eugenia azeda 37 3 6 HþAl (cmolc/dm ) 3.53 2.04 Sapotaceae Padrosia restingae 35 3 6 SB (cmolc/dm ) 0.93 0.39 Nyctaginaceae Guapira sp. 29 3 6 CEC (cmolc/dm ) 4.48 2.21 Chrysobalanaceae Hirtella ciliata 29 3 6 Total N (cmolc/dm ) 0.67 0.45 Fabaceae Chamaecrista ensiformis 28 6 Litter (cm) 3.30 2.51 Ochnaceae Ouratea salicifolia 25 % 6 Soil umidity ( ) 4.07 2.32 Myrtaceae Eugenia ligustrina 23 1 6 Soil conductivity (dS m ) 0.03 0.14 Apocynaceae Hancornia speciosa 23 3 6 Soil density (kg dm ) 1.34 0.08 Cactaceae Pilocereus catingicola 21 1 6 Organic matter (g kg ) 23.80 12.38 Sapotaceae Manilkara salzmannii 20 1 6 Soil texture (g kg ) 40.88 22.38 Celastraceae Maytenus distichophylla 20 1 6 Soil compaction (cm ) 0.14 0.05 Nyctaginaceae Guapira pernambucensis 18 8 6 Slope ( ) 9.38 8.97 Schoepfiaceae Schoepfia brasiliensis 18 6 Elevation (m) 43.20 16.11 Myrtaceae Eugenia umbelliflora 17 6 Terrain convexity (m) 0.41 1.82 Bignoniaceae Tabebuia roseoalba 17 % 6 Canopy openness ( ) 0.37 0.83 Myrtaceae Myrcia guianensis 14 Note: CEC ¼ Cation Exchange Capacity. SB ¼ Sum of Bases. Fabaceae Calliandra parvifolia 12 Erythroxylaceae Erythroxylum passerinum 12 Polygonaceae Coccoloba laevis 10 Myrtaceae Eugenia luschnathiana 10 Myrtaceae Eugenia punicifolia 9 Chrysobalanaceae Licania parvifolia 9 Anacardeaceae Anacardium occidentale 8 Polygonaceae Coccoloba ro´sea 8 Myrtaceae Psidium oligospermum 8 Myrtaceae Myrciaria tenella 7 Myrtaceae Myrciaria floribunda 7 Rhamnaceae Ziziphus joazeiro 7 Nyctaginaceae Guapira tomentosa 6 Lecythidaceae Lecythis pisonis 6 Myrtaceae Eugenia sp. 5 Logoniaceae Strychnos parvifolia 5 Lamiaceae Vitex rufescens 4 Capparaceae Cynophalla flexuosa 4 Myrtaceae Campomanesia sp. 3 Chrysobalanaceae Chrysobalanus icaco 3 Myrtaceae Eugenia candolleana 3 Ochnaceae Ouratea hexasperma 3 Peraceae Pera ferruginea 3 Sapindaceae Allophylus puberulus 2 Malpighiaceae Byrsonima verbascifolia 2 Rubiaceae Cordiera myrciifolia 2 Malvaceae Luehea divaricata 2 Rubiaceae Alseis pickelli 1 Fabaceae Hymenaea courbaril 1 Acanthaceae Thyrsacanthus ramosissimus 1 Rubiaceae Tocoyena formosa 1 Rubiaceae Tocoyena sellowiana 1 Olacaceae Ximenia americana 1 Fabaceae Zollernia ilicifolia 1

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Fig. A1. Individual-based rarefaction curve for the restinga coastal vegetation at the Barreira do Inferno Launch Center, northeastern Brazil. Dashed lines indicate standard errors based on jackknife randomi- zations.

Fig. A2. Phylogenetic tree of native woody species in heath vegetation at Parnamirim, northeastern Brazil.

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Fig. A3. Phylogenetic Mantel correlogram showing significant phylogenetic signal across short phylogenetic distances. Solid and open symbols denote significant (P , 0.10) and nonsignificant Bonferroni-corrected correlations, respectively, relating between-species niche differences to between-species phylogenetic distances across a given phylogenetic distance. Asterisks indicate significance at P , 0.05. Significantly positive or negative correlations indicate that ecological niche distance between species increase or decrease with their phylogenetic distance across the phylogenetic distance class being evaluated, respectively.

Fig. A5. Percentage of studied species occurring in one, two, three, or four of the major vegetation domains in Brazil. Fig. A4. A rank-abundance diagram of 55 species of woody plants at the Barreira do Inferno Launch Center coastal vegetation, northeastern Brazil. The dotted line indicates the limit of 5% of overall abundance.

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Fig. A6. Percentage of studied species across major vegetation domains in Brazil.

SUPPLEMENT

R code for conducting the statistical analysis described in the main text (Ecological Archives, http:// dx.doi.org/10.1890/ES14-00548.1.sm).

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