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Ecology, 93(8) Supplement, 2012, pp. S70–S82 Ó 2012 by the Ecological Society of America Demographic drivers of successional changes in phylogenetic structure across life-history stages in plant communities NATALIA NORDEN,1,2,5 SUSAN G. LETCHER,3 VANESSA BOUKILI,2 NATHAN G. SWENSON,4 1 AND ROBIN CHAZDON2 Departamento de Ciencias Biológicas, Universidad de los Andes, Carrera 1 número 18A-10, Bogotá, D.C., Colombia Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut 06269-3043 USA 3 Organization for Tropical Studies, Apartado Postal 676 2050, San Pedro de Montes de Oca, Costa Rica 4 Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824 USA 2 Abstract. To gain insight into the ecological processes driving community reassembly in disturbed ecosystems, we assessed the phylogenetic dispersion of early- and late-successional tree species occurring in lowland forests of northeastern Costa Rica. Early-successional species were more closely related than expected by chance, whereas late-successional species tended to be less closely related than expected by chance. Then, we evaluated temporal changes in the phylogenetic structure of seedling and tree assemblages in four 1-ha plots of secondary forests in this region. We found an increase in the phylogenetic evenness among tree individuals over time in all secondary tree assemblages, indicating that relatedness among tree individuals decreases as succession unfolds. This pattern was jointly promoted by recruitment and mortality processes, suggesting that increasing evenness was caused by the replacement of individuals of early-successional species from closely related lineages by late-successional species belonging to a wider diversity of lineages. Based on species occurrence, however, tree community reassembly did not show any significant phylogenetic trend over time. These results suggest that shifts in species abundance over succession have a greater impact on the phylogenetic structure of the community than the turnover of species. Seedling assemblages showed higher phylogenetic evenness than tree assemblages, suggesting that propagule colonization is an important process driving phylogenetic changes in species composition throughout succession. Overall, our findings showed that the phylogenetic structure of these successional communities varies at two temporal scales. At short timescales, decreased dominance by early-successional species over succession leads to increased evenness among tree individuals. At longer timescales, colonization processes result in increased phylogenetic evenness in seedling communities compared to tree communities, forecasting increasing phylogenetic evenness among adult individuals at late-successional stages. Key words: community assembly; Costa Rica; life-history stages of plants; mortality; phylogenetic structure; recruitment; succession; vegetation dynamics. INTRODUCTION Disturbed ecosystems are increasing in extent across the landscape, to the degree that successional forest cover exceeds mature forest cover in many regions (ITTO 2002, FAO 2005). Despite the growing role of these successional communities in the conservation of biodiversity, climate change mitigation, and many ecosystem services (Chazdon et al. 2009), recent theoretical developments in plant ecology have focused on species-rich, mature plant communities, rather than on less diverse secondary forests (Webb 2000, Hubbell 2001, Muller-Landau et al. 2006, Jabot and Chave 2009, Manuscript received 13 November 2010; revised 22 March 2011; accepted 4 April 2011. Corresponding Editor: J. Cavender-Bares. For reprints of this Special Issue, see footnote 1, p. S1. 5 Present address: Departamento de Ecologı́a y Territorio, Pontificia Universidad Javeriana, Transversal 4 number 4200, Bogotá, D.C., Colombia. E-mail: [email protected] Kraft and Ackerley 2010, Swenson et al. 2012). Secondary forests, however, provide an ideal laboratory for testing ecological theories, as they reflect community assembly in action. So far, successional models have been based on the premise that species turnover through time is dictated by differences in growth rates and life span (Finegan 1996, Rees et al. 2001). These attributes define species’ ecological syndromes (Westoby et al. 2002) and underpin most explanations of temporal changes in the community during secondary succession (Rees et al. 2001). Yet, these theoretical approaches do not consider the phylogenetic background of cooccurring species. Linking observed patterns of community structure to processes occurring over evolutionary timescales offers a compelling framework for the development of a synthetic ecological theory (Webb et al. 2002, Cavender-Bares et al. 2009, Vamosi et al. 2009). Moreover, it provides valuable information for the assessment of species conservation status and anthropogenic impacts (Warwick and Clarke 1998, Helmus et al. 2010). S70 August 2012 PHYLOGENETIC STRUCTURE OVER SUCCESSION Recent studies have shown that disturbed ecosystems contain more closely related species than non-perturbed ones (Verdú and Pausas 2007, Knapp et al. 2008, Helmus et al. 2010, Cavender-Bares and Reich 2012), suggesting that species’ response to disturbance has a phylogenetic component. If so, the phylogenetic relatedness exhibited by early-successional species should translate into a temporal change in the phylogenetic structure of the community as succession unfolds. Yet uncertainty persists regarding this issue, since the few studies evaluating the effect of disturbance on the relatedness of co-occurring species are limited to the comparison of perturbed and non-perturbed communities (Verdú and Pausas 2007, Knapp et al. 2008, Helmus et al. 2010). These single-time investigations represent a snapshot of species composition in time and space, ignoring the fact that succession is a continuous and dynamic process. Integrating a temporal dimension into studies of phylogenetic community structure should add critical elements to disentangle the different mechanisms driving community reassembly after disturbance. In the most comprehensive study addressing this issue, Letcher (2010) evaluated changes in the phylogenetic structure of successional tropical forests in a replicated chronosequence of 30 sites in northeastern Costa Rica. By dividing tree plots into five stand age categories, she found increased phylogenetic evenness (i.e., overdispersion sensu Webb et al. 2002) over succession. Further, Letcher (2010) found that small stems were less closely related than large stems, suggesting that the increased phylogenetic evenness observed over succession was related to the recruitment of late-successional species. These findings concur with previous studies (Verdú and Pausas 2007, Knapp et al. 2008, Helmus et al. 2010), and suggest that communities at the onset of succession are mainly comprised of closely related species, whereas late stages of succession contain species belonging to a wide array of lineages. Indeed, pioneer species in the neotropics typically belong to the genus Cecropia (Urticaceae) or to the family Malvaceae sensu lato (both groups belonging to the Rosid clade). Contrastingly, since the most common environmental condition in tropical forests’ understory is shade, functional convergence on traits giving adaptive value for regeneration under low light availability (Hubbell 2005) would lead to phylogenetic evenness among late-successional species. So far, the degree of relatedness among early- or late-successional species has never been evaluated quantitatively, partly because classifying species into these ecological syndromes is a challenging task (Wright et al. 2003). In this study, we assessed the phylogenetic relatedness of early- and late-successional species, and tracked temporal changes in phylogenetic community structure within secondary forest plots and between seedling and tree stages, in a lowland Neotropical rainforest. By integrating the current knowledge in successional ecology (Finegan 1996, Chazdon 2008) and prior S71 information from studies evaluating community phylogenetic structure in disturbed systems (Verdú and Pausas 2007, Knapp et al. 2008, Helmus et al. 2010, Letcher 2010), we propose a likely scenario for the temporal changes in the phylogenetic structure of successional communities. Assuming that early-successional species are clustered within the angiosperm phylogeny and that late-successional species show a more even phylogenetic distribution, we expect phylogenetic evenness to increase over succession. Such a pattern can be the result of two simultaneous processes: the recruitment of distantly related late-successional species/individuals, and the death of closely related early-successional species/individuals. As part of the same process, small size classes, which represent future tree recruits, and thus reflect the species composition of more advanced successional stages (Norden et al. 2009), should also show higher phylogenetic evenness than the standing tree community. How recruitment and mortality affect the phylogenetic structure of the community not only depends upon relatedness among species/ individuals entering or leaving the community, but also on the relatedness among these groups and the group of survivors. For instance, we expect increasing evenness over succession to be partially associated with the recruitment of distantly related species/individuals. However, increased evenness can also be the outcome of the recruitment of species/individuals that are closely related to one another, but distantly related to the pool of survivors. We tested these different scenarios using robust successional data on seedling and tree dynamics from lowland forest plots in northeastern Costa Rica (see Plate 1). Specifically, we quantified the phylogenetic relatedness of early- and late-successional species using static data from several studies conducted in both second- and old-growth forests in this area. This information provided us with an appropriate framework to interpret temporal changes in the phylogenetic structure of secondary forest communities. We used long-term data on recruitment and mortality of trees (12 years) and seedlings (5 years) in four secondary-forest permanent plots in this same region to assess changes in phylogenetic structure over time. We compared the temporal trends in tree assemblages with those observed in mature forests to evaluate whether phylogenetic structure in secondary forests approaches that of mature forest as succession unfolds. Then, we evaluated how recruitment and mortality contribute to the temporal changes observed in the phylogenetic structure of the plant community over succession. MATERIALS AND METHODS Study site The study was conducted at La Selva Biological Station and surrounding areas of northeastern Costa Rica. This region is classified as tropical lowland wet forest, with an annual precipitation of ;3900 mm and S72 NATALIA NORDEN ET AL. an average annual temperature of 26.58C (McDade et al. 1994). The landscape matrix is composed of old-growth and second-growth forest patches surrounded by agricultural lands, pastures, and cash crops. Site elevations range from 40 to 200 m above sea level. Land-use history was similar within all secondary sites. Phylogenetic dispersion in ecological syndromes We tested the assumptions that early-successional species are phylogenetically clustered within the regional flora and that late-successional species are phylogenetically even by evaluating the phylogenetic dispersion in a categorical variable defining species as second-growth specialists or old-growth specialists. To do so, we assessed whether early-successional species tended to be more closely related than expected by chance, and latesuccessional species more distantly related than expected by chance. Because the pioneer vs. non-pioneer categorization is seen as false dichotomy (Wright et al. 2003), we defined a third category, the generalists, for which we did not have any particular expectation regarding its phylogenetic dispersion. To assign species to one of these three categories, we used data on species abundance in mature and secondary stands throughout the study area from various sources (Chazdon et al. 2011). This data set was composed of trees 10 cm diameter at breast height (dbh) sampled in 18.3 ha of old-growth forest and 11.3 ha of secondary forest. Secondary forests ranged from 5 to 45 years since abandonment and included forests regenerating on abandoned pastures and in cleared areas that were never grazed. Second-growth and old-growth sites were interspersed across a broad landscape, thereby avoiding the pitfalls of confounding habitat differences with spatial variables (Chazdon et al. 2011). A previous study using part of the data used here showed that patterns of floristic similarity among tree plots were independent of spatial distance (Norden et al. 2009). Thus, the potential biasing effect of spatial autocorrelation seems to be minimal. Our statistical approach classified each species into one of each of the three categories based on its abundance in secondary and mature stands (Chazdon et al. 2011). If a species is a second-growth specialist, then we would expect that pi, the relative abundance of this species in second-growth forests, is sufficiently higher than pi, the relative abundance in this species in old-growth forests; or equivalently, the ratio pi/( pi þ pi ) is sufficiently higher than a constant k. Using a multinomial model, this statistical test procedure determines for each species whether the observed data provide sufficient evidence that their ratio is statistically higher than this pre-specified constant k. Here, k was designated as 0.5, a liberal threshold based on a ‘‘simple majority’’ rule, which allowed us to classify most species into one of these categories (Chazdon et al. 2011). Oldgrowth forest specialists are similarly classified as species with a statistically higher ratio of individuals in oldgrowth than in second-growth forest stands, and Ecology Special Issue generalists are classified as those that have statistically indistinguishable relative abundance in old-growth and second-growth stands. Among the 359 species occurring in these plots, 203 could be assigned with certainty to one of these categories using this statistical procedure, and the remaining species were too rare to classify. We constructed the phylogenetic supertree of these 203 species using the database Phylomatic (Webb and Donoghue 2005). Phylomatic starts with the familylevel tree of angiosperms and considers genera as polytomies within families and species as polytomies within genera. The latest Angiosperm Phylogeny Group (APG) classification (Phylomatic tree version R20080417; P. F. Stevens, available online)6 was used for the supertree backbone. The BLADJ algorithm was implemented in the community phylogenetic software Phylocom (v. 4.0.b; Webb et al. 2008) to calibrate the species pool supertree by applying known molecular and fossil dates (Wikstrom et al. 2001) to nodes in the supertree, and to reduce variance among branch lengths by evenly spacing nodes of unknown ages. The same procedure was used in the subsequent analyses. The degree of phylogenetic dispersion in each of the three ecological syndromes defined was assessed by measuring the mean phylogenetic distance (MPD) among the 58 species classified as second-growth specialists, among the 107 species classified as oldgrowth specialists, and among the 38 species classified as generalists. We assessed significance for each category by comparing the observed value of MPDs to the null distribution of MPD values obtained by shuffling the species names across the tips of the phylogeny 999 times (Chazdon et al. 2003). Early-successional species were considered significantly clustered within the regional species pool of 203 species if the observed MPD of the 58 second-growth specialists was in the lower 5% of the null distribution (one-tailed test). Likewise, late-successional species were considered significantly even within the regional species pool if the observed MPD of the 107 old-growth specialists was in the higher 5% of the null distribution. Because we did not have any particular expectation for generalists, these species were considered significantly clustered or even within the regional species pool if the observed MPD of the 38 generalists was in the lower or higher 2.5% of the null distribution (twotailed test). Although there are numerous analytical methods to measure phylogenetic dispersion in a trait (Blomberg et al. 2003, Webb et al. 2008, Fritz and Purvis 2010), we believe this method to be the most appropriate considering the presence of polytomies in our tree, and the fact that we are analyzing a categorical variable. Calculations were performed with the R statistical software (v. 2.11.1; R Development Core Team 2010). 6 http://www.mobot.org/MOBOT/research/APweb/ August 2012 PHYLOGENETIC STRUCTURE OVER SUCCESSION S73 TABLE 1. Site descriptions of 1-ha monitoring plots in northeastern Costa Rica. Plot name and abbreviation Lindero Sur, LSUR Tirimbina, TIR Lindero El Peje, LEPS Cuatro Rios, CR Location La Selva Biological Station Finca de Arturo Salazar, adjacent to Tirimbina Research Center La Selva Biological Station La Virgen de Sarapiquı́ Age in 1997 (yr) Previous land use 12 cattle pasture for 5–6 yr 15 cattle pasture for .6 years; may have been cut twice 20 cattle pasture for 5–6 yr 25 cleared for cattle pasture, little or no grazing (,3 yr) no history of logging, but area has been subject to hunting no history of logging, protected from hunting Selva Verde, SV Chilamate mature forest LEP primary, LEPP La Selva Biological Station mature forest Temporal changes in phylogenetic community structure To evaluate temporal changes in phylogenetic structure within sites and between life stages, we used longterm data on seedling and tree dynamics. Permanent plots of 1 ha were established in 1997 in four secondary forest sites, and two additional 1-ha plots were established in 2005 within mature forest patches (Table 1). In each plot, all trees with dbh of 5 cm were tagged, mapped, and measured for diameter at 1.3 m height. Thereafter, censuses were completed annually. In each census, new recruits into the 5 cm diameter class were tagged, mapped, and measured; and stems were recorded as dead if no living tissues could be observed. The final tree census of all plots was completed in 2008. In each of the secondary forest sites, 144 seedling plots of 1 3 5 m were created in 1998 (Capers et al. 2005). In each plot, all woody stems 20 cm in height and ,1 cm dbh were tagged and identified. Subsequently, seedling censuses were conducted every 8 months. During each census, newly recruited seedlings were tagged and identified, and missing seedlings were recorded as dead. Individuals that moved into the next size class (.1 cm dbh) during the census period were considered as survivors. The final seedling census was completed in August 2003 (Capers et al. 2005). We did not include seedling data from mature forest plots since these data are not available. Trees and seedlings were identified by experienced field assistants, and vouchers were collected to compare with botanical specimens at the La Selva Herbarium and the Instituto Nacional de Biodiversidad in Costa Rica (INBio). Although seedlings of all life forms were censused, here we consider only the canopy and subcanopy trees and palms, as well as treelet species reaching the .5 cm dbh size class, to be consistent with tree censuses. We constructed an appropriate regional species pool including all the canopy tree, palm, and treelet species that reach dbh 5 cm and that could potentially colonize Landscape matrix adjacent to large tract of old-growth forest surrounded by matrix of pasture and second-growth forest adjacent to large tract of old-growth forest surrounded by matrix of pasture and second-growth forest surrounded by pasture and second-growth forest surrounded by oldgrowth forest on three sides the plots based on a database of vascular plants occurring in the Sarapiquı́ region (Proyecto Flora Digital de La Selva 2009). We excluded non-angiosperm taxa because they are rare in the region and could contribute disproportionally to phylogenetic structure owing to their low relatedness with most of the species. The final list for the community species pool included a total of 603 species. The total number of species used for this phylogenetic supertree was higher than the one used in the previous analysis, which only included species for which we had information about their life-history status. A phylogenetic tree for those species was constructed using Phylomatic (Webb and Donoghue 2005) according to the methods described in the section Phylogenetic dispersion of ecological syndromes. Because the Phylomatic algorithm maps unknown relationships as polytomies on the supertree, measures of phylogenetic structure using these phylogenies may have potential biases and loss of statistical power (Swenson 2009). Letcher (2010) tested for this issue using a very similar species regional pool to ours, and found that the phylogenetic measures calculated using the Phylomatic tree were highly correlated to those obtained using a tree where all families were collapsed into polytomies. Indeed, loss of phylogenetic resolution generally causes false negative results, rather than false positives (Swenson 2009), which would underestimate the strength of our results. We evaluated temporal changes in the phylogenetic structure of tree and seedling assemblages in each plot by calculating the net relatedness index (NRI; Webb 2000) using the package ‘‘picante’’ (Kembel et al. 2010) in the R statistical software (v. 2.11.1; R Development Core Team 2010). Similar results were obtained using the nearest taxon index, and are not reported here. Over the timescale of our study, floristic changes during succession might reflect changes in species’ relative abundance more than the gain and/or loss of species. We thus performed this analysis using both abundanceand incidence-based data. NRI for each local assem- S74 NATALIA NORDEN ET AL. blage was calculated using the following formula (Webb et al. 2002): NRI ¼ MPD MPDrnd sdMPDrnd where MPD is the mean phylogenetic distance of cooccurring taxa in local assemblages, MPDrnd is the mean and sdMPDrnd the standard deviation of 999 MPDs obtained from randomly generated local assemblages. We used the Phylogeny Tip Shuffle null model in Phylocom, which shuffles species labels across the entire phylogeny. Although permuting elements within the community data matrix is a more conservative method for avoiding Type I error (Hardy 2008), randomizing relatedness among species and/or individuals is a more appropriate null model in temporal analyses. Randomizing elements within the community data matrix changes the identity of surviving stems between consecutive censuses, inflating the temporal turnover in the null model, and biasing the observed result toward a lower than expected turnover. Randomizing species labels across the phylogeny avoids this problem and has the additional benefit of maintaining the observed occupancy rates, the plot abundance distribution and plot species richness. Thus, if individuals within a species are dispersal limited or have spatial contagion in their observed distribution, this observed pattern will be maintained in all null communities generated. Alternative null models, such as a swap algorithm, maintain occupancy rates, species richness, and abundances, but they do not necessarily conserve patterns of spatial contagion of species. Negative values of NRI indicate higher MPD than expected, and are indicative of phylogenetic evenness, whereas positive values of NRI indicate phylogenetic clustering (Webb 2000). To test for significant deviations of NRI from a null expectation, we calculated a P value by dividing the number of null communities with MPD values that were lower than or greater than the observed by the number of runs þ1. For each plot and each census, we used this metric to evaluate phylogenetic structure for tree and seedling assemblages. Relative contribution of recruited and dead individuals To assess the relative contribution of recruitment and mortality to the dynamics of phylogenetic structure over succession, we calculated NRI for the subset of survivors, recruited, and dead trees and seedlings at each census. The reference species pool was the same regional pool used in the previous analysis. Although the most logical species pool for measuring phylogenetic relatedness among dead trees in a particular plot is arguably the pool of species occurring in that plot, we used the same species pool across all analyses to obtain comparable NRI values across all analyses. Based on the predicted scenario described in the Introduction, we expected recruited individuals to be more phylogenetically even than the pool of survivors and dead Ecology Special Issue individuals to show the opposite pattern. We tested for the significance of this pattern using a one-tailed, paired t test for each life stage. To have a deeper understanding of how tree recruitment and mortality, as well as future seedlingto-tree transitions, potentially alter the phylogenetic composition of the community, we assessed phylogenetic similarity among recruited, dead, and surviving trees and seedlings within plots, over time. To do so, we performed an ordination analysis based on the MPD between all pairs of possible combinations of recruited, dead, and surviving trees and species across censuses. We standardized the observed matrix of MPD scores between pairwise samples by generating 999 random phylogenetic distance matrices using a randomization equivalent to the Phylogeny Tip Shuffle null model. For each null model iteration, we calculated the MPD of all possible pairs of taxa in one sample to the taxa in the other to generate a null distribution. This null distribution was used to calculate a pairwise distance matrix based on a standardized MPD: MPDstd ¼ MPD MPDrnd : sdMPDrnd We then performed a nonmetric multidimensional scaling analysis (NMDS) based on these values to illustrate phylogenetic similarity among all possible combinations. When compared to an ordination analysis based on species composition, this analysis reflects the shared evolutionary history among sites, rather than the shared presence or absence of species, therefore emphasizing the similarity in deep phylogenetic structure, even when no species are shared. RESULTS Phylogenetic dispersion in ecological syndromes As expected, species classified as second-growth specialists were significantly clustered within the 203species phylogeny (MPDsec ¼ 227.92) when compared with a null model distribution based on species names shuffling (95% confidence interval ¼ 230.5–258.6). Species classified as old-growth specialists showed tendency to evenness within the same phylogeny (MPDold ¼ 242.97) when compared with the same type of null model (95% confidence interval ¼ 225.47–244.90). Finally, species distribution of generalists within this phylogeny was within the null expectation (MPDgen ¼ 229.22, 95% confidence interval ¼ 224.17–254.37). Temporal changes in phylogenetic structure Based on species incidence data, we did not observe any temporal trend in the phylogenetic structure of the tree assemblages (Fig. 1b). Only Cuatro Rios (CR), the oldest secondary-forest plot, showed significant evenness in some censuses. The other plots did not show any significant pattern. In contrast, abundance-based analyses showed that the phylogenetic evenness of trees August 2012 PHYLOGENETIC STRUCTURE OVER SUCCESSION S75 FIG. 1. Temporal changes in the net relatedness index (NRI) based on both species incidence and species abundance of trees in four secondary and two mature forest plots and of seedlings in the four secondary plots in northeastern Costa Rica. Open symbols correspond to secondary forest plots, and solid symbols correspond to mature forest plots. Site abbreviations are: LSUR, Lindero Sur; TIR, Tirimbina; LEPS, Lindero El Peje; CR, Cuatro Rios; LEPP, LEP primary; and SV, Selva Verde. * P , 0.05. increased over time in all the secondary sites (Fig. 1a). In the youngest plot, Lindero Sur (LSUR), the abundancebased NRI indicated that the tree assemblage was initially phylogenetically clustered, although nonsignificantly, and then became significantly even over time. The two oldest plots (Lindero El Peje [LEPS] and CR) were phylogenetically even throughout the whole monitoring period and showed a decreasing pattern in NRI until reaching the phylogenetic evenness level of old-growth forest plots (Fig. 1a). Tirimbina (TIR) was the only plot with significant phylogenetic clustering of trees throughout the census period. Patterns of increasing phylogenetic evenness among tree individuals over time were due to both recruitment and mortality processes (Fig. 2). Although the NRI of recruited and dead trees showed large variation between consecutive censuses, dead trees were significantly more closely related than survivors, which, in turn, were significantly more closely related than recruited trees in all plots (Fig. 2, Table 2). Seedling assemblages tended to show greater phylogenetic evenness than tree assemblages throughout the whole monitoring period (Fig. 1c, d). They showed a sharp decrease in NRI between the third and the fourth censuses, a phenomenon occurring across all plots, and particularly pronounced in incidence-based data (Fig. 1d), suggesting that this pattern was the result of species level population dynamics. Indeed, a previous study reported the simultaneous colonization of several canopy palm species that were absent in the previous censuses in these same plots (Capers et al. 2005). Because palms (Arecaceae) belong to an early branching S76 NATALIA NORDEN ET AL. Ecology Special Issue FIG. 2. Temporal changes in the net relatedness index (NRI) of surviving (solid circles), recruited (open circles), and dead (crossed circles) trees in each of the four study plots, based on species abundance. Note that the points of the graph are shifted one year to the right with respect to Fig. 1, since these data refer to recruited, dead, and surviving individuals. See Fig. 1 for site abbreviations. angiosperm clade, the arrival of these species into the community has a large effect on the calculation of phylogenetic structure. If palms are taken out of the analysis, the phylogenetic structure of seedling assemblages within each plot was stable over time (data not shown). In terms of seedling dynamics, the NRI of recruited and dead individuals showed large variation between consecutive censuses. Unlike trees, both dead and recruited individuals tended to be significantly more phylogenetically clustered than survivors (Fig. 3, Table 2). Recruited seedlings showed the same decrease in NRI scores as the one observed for the standing seedling assemblage in all plots, but this was only observed in LSUR and LEPS for dead individuals (Fig. 3). In all plots, trees were more phylogenetically dissimilar to seedlings than recruited and dead individuals were to survivors within each life stage (Fig. 4). For trees, none of the different groups (deads, recruits, survivors) overlapped with each other in any of the plots except for CR (the oldest site), where recruited individuals overlapped with survivors in the last six censuses (Fig. 4d). LSUR (the youngest site) showed high phylogenetic similarity among cohorts of dead trees. For seedlings, dead and recruited individuals exhibited some overlap in all plots (Fig. 4). DISCUSSION Phylogenetic dispersion in ecological syndromes The degree of relatedness among early-successional species has never been addressed quantitatively, partly because species show a continuous distribution in their trait values rather than a multimodal shape, and it is often difficult to place species into a pioneer category with high certitude (Hubbell and Foster 1992, Wright et al. 2003). Our study is the first to provide evidence that a subset of species rigorously classified as second-growth specialists in northeastern Costa Rica are more closely related than expected by chance, and that those classified as old-growth specialists tend to converge in August 2012 PHYLOGENETIC STRUCTURE OVER SUCCESSION their shade-tolerant strategy. Early-successional species require extreme traits conferring them high dispersal abilities and high growth rates in disturbed environments. Seed size (Moles et al. 2005) and wood density (Chave et al. 2006, Swenson and Enquist 2007), two traits especially involved in the success of this ecological syndrome, have consistently shown phylogenetic conservatism across a wide range of floras. Since many other traits have shown similar patterns (Prinzing et al. 2001, Chazdon et al. 2003, Swenson et al. 2007, Kraft et al. 2010), phylogenetic constraints might have favored niche conservatism in the pioneer strategy. Our findings indicate the presence of a phylogenetic signal in early-successional species, a pattern that, although often interpreted as niche conservatism, does not necessarily imply an adaptive process (Losos 2008, Revell et al. 2008). Phylogenetic niche conservatism explicitly implies that ‘‘some factor is causing closely related species to be more ecologically similar that would be expected by simple Brownian motion descent with modification’’ (Losos 2008). Our current analysis does not allow us to draw such a conclusion, but it is a first step toward a better understanding of the evolution of the pioneer strategy. Has this ecological syndrome evolved many times from different lineages, or is it a conserved strategy that arose from few lineages? The pioneer strategy probably arose from mature forest species in response to transient disturbances (Graham and Janzen 1969, Gomez-Pompa 1971). If our results can be generalized to larger geographical and taxonomic scales, early-successional species might have appeared in few lineages, which diversified thereafter to become clades showing high niche conservatism, as is the case of Cecropia. It is important to note that most plant families are not exclusively composed of early-successional species, even if they have a predominance of this syndrome (e.g., Melastomataceae, Urticaceae, or Piperaceae; P. Stevenson, personal communication). For instance, the Urticaceae is known to be a pioneer family because it contains the genera Cecropia and Pourouma. Yet Pourouma shows important variation in shade tolerance, with species such as P. minor commonly occurring in old-growth forests. Another issue is geographical scale. Here, we are focusing on a single lowland tropical forest region, and it would be ideal to extend our analysis to a larger data set including the global pool of species occurring in lowland tropical forests across Central and South America. A global analysis including all the Neotropical angiosperms could, however, lead to equivocal interpretations, as it would include species having very different evolutionary histories (e.g., the Andes orogeny vs. the Amazon basin formation), and occurring in a variety of habitats. Investigating further patterns of niche conservatism in species’ successional status will provide key elements for understanding the evolution of plant functional traits in relation to community assembly during succession. S77 TABLE 2. Results of the paired t test analysis comparing net relatedness index (NRI) values between dead and surviving trees and seedlings, and recruited and surviving trees and seedlings. Dead vs. survivors Recruited vs. survivors Site and life stage t df t df LSUR Trees Seedlings 3.42** 4.96*** 10 7 8.82*** 1.5 10 7 TIR Trees Seedlings 6.14*** 2.00 10 7 8.25*** 0.35 10 7 LEPS Trees Seedlings 1.98* 4.03** 10 7 6.49*** 1.37 10 7 CR Trees Seedlings 1.79* 6.80*** 10 7 3.82*** 2.96 10 7 Notes: The tests for dead trees and seedlings determined phylogenetic clustering compared with survivors, whereas recruited trees and seedlings were tested for phlogenetic evenness compared with survivors. See Table 1 for site abbreviations. * P 0.05; ** P 0.01; *** P 0.001. Temporal changes in the phylogenetic structure of tree assemblages All plots exhibited increasing phylogenetic evenness among tree individuals over time, indicating that, at small spatial scales (1 ha), the probability of cooccurrence among closely related individuals declines as succession unfolds. In contrast, the probability of tree species co-occurrence was unrelated to their phylogenetic background, and did not show any temporal trend. Such discrepancy between abundance- and incidencebased analyses can be explained by differences between individual and species turnover throughout succession. The first decades of succession typically show high species turnover due to the replacement of short-lived pioneers by long-lived pioneers and some shade-tolerant species (Finegan 1996, Anderson 2007). Then, species turnover decreases as the pool of potential new colonizers diminishes, and because late-successional species have higher longevity than early colonizers. In contrast, rates of recruitment and mortality stay elevated, maintaining high individual turnover (Chazdon 2003). Our results therefore suggest that rates of change in species composition in these successional stands at relatively short timescales are the result of shifts in species abundance during succession, rather than of the gain or loss of species (van Breugel et al. 2007, Chazdon et al. 2007). Our monitoring period of 12 years, although quite long for a successional study, may not be sufficient to discern noticeable patterns of species turnover that lead to changes in phylogenetic structure. Letcher (2010) did find an increased phylogenetic evenness based on species occurrence data across a S78 NATALIA NORDEN ET AL. Ecology Special Issue FIG. 3. Temporal changes in the net relatedness index (NRI) of surviving (solid circles), recruited (open circles), and dead (crossed circles) seedlings in each of the four study plots, based on species abundance. Note that the points of the graph are shifted one year to the right with respect to Fig. 1, since these data refer to recruited, dead, and surviving individuals. See Fig. 1 for site abbreviations. chronosequence spanning 40 years. Such a long time period covered more successional phases, resulting in a better ability to detect species turnover. Combining long-term and demographic data in phylogenetic studies is therefore a critical step for developing a clear understanding of the processes driving community assembly (see also Cadotte et al. 2012, Cavender-Bares and Reich 2012). In all four secondary plots, the pool of dead trees consistently showed higher phylogenetic clustering than the pool of survivors, which, in turn, showed higher phylogenetic clustering than the pool of recruited trees. These results clearly indicate that both recruitment and mortality jointly promoted the increased phylogenetic evenness among co-occurring trees observed over succession. Since we provide evidence that earlysuccessional species are significantly clustered, and late-successional species tend to evenness within the angiosperm phylogeny, we can say confidently that the increased phylogenetic evenness observed here and in Letcher’s (2010) study is the result of the replacement of individuals of early-successional species, comprising many closely related species, by late-successional individuals belonging to a wider diversity of lineages. This is well illustrated by the patterns observed in LSUR, where the repeated death of even-aged cohorts of earlysuccessional species translated to a high phylogenetic similarity among all cohorts of dead trees. Cohorts of recruited trees, in contrast, were more phylogenetically even in this plot. This pattern was apparent only in this, the youngest plot, as the other plots represent later successional stages where tree cohorts are no longer even-aged. In CR, the oldest plot, recruited trees overlapped with surviving trees at the last censuses, indicating that, later in succession, phylogenetic composition of recruited trees is not distinguishable from that of surviving trees. This pattern corroborates previous findings showing a rapid floristic recovery in secondary stands in this area (Letcher and Chazdon 2009, Norden et al. 2009). August 2012 PHYLOGENETIC STRUCTURE OVER SUCCESSION S79 FIG. 4. Nonmetric multidimensional scaling (NMDS) analysis illustrating pairwise phylogenetic distances among censuses and plots for surviving (solid symbols), recruited (open symbols), and dead (crossed symbols) trees (circles) and seedlings (squares) for each plot, based on abundance data. See Fig. 1 for site abbreviations. Projecting changes into the future: phylogenetic structure across life stages We extended the temporal scale of this study by assessing the community phylogenetic structure at early life stages too. In the same study area, Letcher (2010) showed that small stem size classes (0.5–5 cm dbh) were more phylogenetically even than large stem size classes (.5 cm dbh). Here, we went further by comparing seedling and tree assemblages. These two life stages showed a clear phylogenetic differentiation, indicating that the initial colonizers that form early tree cohorts come from different lineages than the propagules colonizing a few decades later. Because seedling and sapling layers are comprised of many shade-tolerant species that do not occur in the canopy of secondary forests (van Breugel et al. 2007, Norden et al. 2009), the species pool of these young life-history stages is likely to be much larger than the one of adult stages, therefore exhibiting higher phylogenetic diversity. Increased phylogenetic evenness in seedlings compared to trees indicates that species colonization is an important ecological process shaping the phylogenetic structure of successional assemblages. Since species colonization is directly related to distance from seed sources, to dispersal limitation, and to the regional species pool, our results indicate that the surrounding vegetation matrix has important effects in the temporal dynamics of local phylogenetic structure. Such landscape effects were also reflected in the variation of the temporal patterns in phylogenetic structure observed among plots. LSUR and LEPS, the secondary plots located within the more forested landscape of La Selva Biological Station, showed the most substantial increase in phylogenetic evenness during the monitoring period compared to CR and TIR. As TIR is a young stand (15 years old since abandonment at the beginning of the monitoring), one would have expected this plot to show high individual and species turnover (Anderson 2007). Indeed, species gain exceeded rates of species loss in LSUR and TIR, but not in LEPS and CR (Chazdon et al. 2007). Yet, the TIR plot exhibits the highest phylogenetic clustering among all plots, and very low changes in phylogenetic evenness over time. This might be due to the fact that TIR has the longest history of disturbance and isolation. These observations highlight S80 NATALIA NORDEN ET AL. Ecology Special Issue PLATE 1. A tree-fall gap in a lowland tropical secondary forest at La Selva Biological Station, Costa Rica. Photo credit: R. L. Chazdon. the importance of the presence of mature forests within agricultural matrices. Temporal variation in seed production also appeared to promote phylogenetic evenness at the seedling stage. For instance, the sharp decline in the NRI scores observed in all seedling assemblages occurred in a short time frame corresponding to the simultaneous arrival of palm propagules at the four secondary sites (Capers et al. 2005). Interannual fluctuations in seed production typically result in temporal pulses in recruitment, causing important changes in species richness (Norden et al. 2007), and thus in the phylogenetic structure of the seedling community. Moreover, even at late stages of succession, tree mortality can open new opportunities for the successful establishment of early-successional species (van Breugel et al. 2007). These processes underlie a certain level of unpredictability in the colonization process, resulting in a complex pattern. For instance, dead, recruited, and surviving seedlings did not show any phylogenetic differentiation. It is important to note that our study focused on recruitment of individuals into the 20 cm height class. Since early stages are extremely vulnerable (Harms et al. 2000, Muller-Landau et al. 2002), nonrandom patterns of mortality in early establishment could have also contributed to the observed changes in phylogenetic structure. Indeed, a recent study shows that phylogenetic relatedness decreases among seedlings after the first year of survival due to negative density dependence (Metz et al. 2010). Together, these processes lead to greater temporal fluctuations in phylogenetic structure in seedling than in tree assemblages. CONCLUSIONS To our knowledge, this is the first study to determine how demographic processes of mortality and recruitment drive changes in the phylogenetic structure of plant communities. Our results are supported by other successional studies in ruderal (Knapp et al. 2008) and zooplankton communities (Helmus et al. 2010), where species adapted to disturbance were more closely related than species occurring in non-perturbed ecosystems. We further show that the phylogenetic structure of secondary stands varies at two temporal scales. At short temporal scales, decreasing relatedness among tree individuals over succession is the joint result of the death of closely related early-successional individuals, and of the recruitment of distantly related late-successional individuals. At longer temporal scales, the colonization of propagules belonging to a wide array of lineages increases phylogenetic evenness in seedlings compared to trees at any one moment in succession. As these small stems grow, future tree assemblages are expected to exhibit higher species richness and phylogenetic evenness. Temporal fluctuation in seed production and species colonization are key elements contributing to increased phylogenetic evenness in these reassembling communities. Under the niche conservatism scenario, studies of community phylogenetics typically explain phylogenetic evenness as a consequence of biotic filtering mediated by competition or by shared pests among closely related species, and phylogenetic clustering as the result of environmental filtering (Webb et al. 2002, Kraft et al. 2010). These studies mostly rely on static data from August 2012 PHYLOGENETIC STRUCTURE OVER SUCCESSION mature tree communities where some assembly processes may not be as important as in more dynamic systems. Recent studies have shown that many processes can affect phylogenetic structure (Cavender-Bares et al. 2009). For instance, facilitation among distantly related species appeared to be an important driver of phylogenetic diversity in arid plant communities in Central Mexico (Valiente-Banuet and Verdú 2007) and in Mediterranean successional communities (Verdú et al. 2009). Here, we further show that other ecological processes, occurring during the regeneration stage, also drive successional changes in phylogenetic structure. Abundance data showed a much stronger signal than incidence data, suggesting that shifts in species abundance due to recruitment and mortality may show a concerted pattern of phylogenetic structure long before the loss and gain of species shows a signal. This finding is of critical importance, as many community phylogenetics studies have drawn conclusions about community assembly processes based solely upon species occurrence data. The field of community phylogenetics is a promising avenue for gaining insight into community reassembly. Future studies integrating well-resolved phylogenies (Kress et al. 2009, González et al. 2010), demographic data and long-term monitoring will provide increased sensitivity for unraveling the mechanisms that determine community assembly in successional forests. 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