30 Years of postdisturbance recruitment in a Neotropical forest

Abstract Questions Long‐term community response to disturbance can follow manifold successional pathways depending on the interplay between various recruitment processes. Analyzing the succession of recruited communities provides a long‐term perspective on forest response to disturbance. Specifically, postdisturbance recruitment trajectories assess (a) the successive phases of postdisturbance response and the role of deterministic recruitment processes, and (b) the return to predisturbance state of recruits taxonomic/functional diversity/composition. Location Amazonian rainforest, Paracou station, French Guiana. Methods We analyzed trajectories of recruited tree communities, from twelve forest plots of 6.25 ha each, during 30 years following a disturbance gradient that ranged from 10% to 60% of aboveground biomass removed. We measured recruited community taxonomic composition turnover, compared to whole predisturbance community, and assessed their functional composition by measuring the community weighted means for seven leaf, stem, and life‐history functional traits. We also measured recruited community taxonomic richness, taxonomic evenness, and functional diversity and compared them to the diversity values from a random recruitment process. Results While control plots trajectories resembled random recruitment trajectories, postdisturbance trajectories diverged significantly. This divergence corresponded to an enhanced recruitment of light‐demanding species that became dominant above a disturbance intensity threshold. After breakpoints in time, though, recruitment trajectories returned to diversity values and composition similar to those of predisturbance and control plots community. Conclusions Following disturbance, recruitment processes specific to undisturbed community were first replaced by the emergence of more restricted, deterministic recruitment processes favoring species with efficient light use and acquisition. Then, a second phase corresponded to a decades‐long recovery of recruits predisturbance taxonomic and functional diversity and composition that remained unachieved after 30 years.


| INTRODUC TI ON
Determining the response of tropical forests to disturbance is key for predicting their fate in the context of global climate change. In recent decades, tropical forests have experienced a wide range of disturbances, from radical land-use changes for agriculture or mining (Dezécache, Faure, et al., 2017; to more insidious changes following climate change or human activities like selective logging (Aubry-Kientz et al., 2015;Baraloto et al., 2012). In that respect, a vast literature has successfully modeled community response to disturbance in terms of tree growth, tree height, and fluxes of carbon, water, and nutrients (Gourlet-Fleury & Houllier, 2000;Piponiot et al., 2016;Putz et al., 2012;Rutishauser et al., 2016). Tree community diversity and composition, however, proved more complex to predict as forest succession is driven both by deterministic, predictable, and by random, varying processes (Brokaw & Busing, 2000;Norden et al., 2015).
Deterministic processes would correspond to recruitment processes depending on the species resources use strategy and competitive abilities. Following disturbance, species benefiting the most from higher resources availability and reduced competition would be favored in the first place (Adler et al., 2007;Chesson, 2000;Rees et al., 2001), before stand maturation progressively allows latesuccessional species to recruit and restore predisturbance composition and diversity (Denslow & Guzman, 2000). In the very diverse tropical forests, however, while several studies revealed predictable and homogeneous successional phases restoring predisturbance community characteristics (Letcher et al., 2015), others revealed diverging postdisturbance trajectories and different equilibrium states (Longworth et al., 2014). Specifically, the Neotropical forests studied here revealed complex trajectories at the scale of the whole community, that is, considering both recruited and predisturbance surviving trees, with a divergence between taxonomic and functional trajectories and a challenging estimation of the time to recover initial state (Mirabel et al., 2020). Following on these conclusions, a focus on recruitment trajectories would better assess the differences among successional pathways and the corresponding recruitment processes. Clarifying recruitment trajectories would also help to give an idea of what would be the diversity and composition of future communities (Clark et al., 1998;Grubb, 1977;Hurtt & Pacala, 1995). We aimed here to focus on recruitment processes driving a Neotropical forest response to disturbance: We assessed the successional phases of postdisturbance recruitment (Chazdon, 2008;Norden et al., 2015) and determined whether they allow the recovery of community predisturbance state.
Two major facets of communities' description are their taxonomic characteristics, corresponding to species composition and diversity, and their functional characteristics, accounting for species ecology and functioning (Kunstler et al., 2016;MacArthur & Levins, 1967;Violle et al., 2007). Deterministic processes correspond to a recruitment depending on species competitive ability determined by their functional characteristics (Perronne et al., 2017;Rees et al., 2001).
In wet tropical forests, where light is hypothesized to be the main limiting resource, deterministic processes might be revealed by community functional trajectories considering a set of key functional traits assessing species ecology and resources acquisition strategy, such as leaf, wood, and life-history functional traits (Chave et al., 2009;Hérault et al., 2011;Wright et al., 2004). Such studies have revealed a successional sequence in functional composition from fast-growing species with "acquisitive" resource use, capable of significant and rapid acquisition of light, to slow-growing, longlived species with "conservative" resource use (Bongers et al., 2009;Denslow, 1980;Molino & Sabatier, 2001). Then, while deterministic recruitment would result in taxonomic and functional trajectories restricted to certain species or functional strategies, nondeterministic recruitment would correspond to a recruitment independent of species functional characteristics. A combination of taxonomic and functional approaches can thus reveal both deterministic and nondeterministic recruitment processes driving community response to disturbance (Cequinel et al., 2018;Chalmandrier et al., 2015;Fukami et al., 2005).
Here, we followed recruitment trajectories in a 75-ha area, cumulated over experimental plots, of Neotropical forest subject to a gradient of disturbance intensities. The gradient corresponded to a removal by logging and girdling of 10%-60% of aboveground standing biomass. We first investigated community composition, richness, and evenness of recruited trees over 30 years, and their taxonomic composition turnover compared to the predisturbance community. We considered both taxonomic aspects, that is, tree species diversity and composition, and functional aspects, accounting for seven major leaf, stem, and life-history traits.
Breakpoints analysis allowed us to specify the different phases of the observed trajectories. We compared the recruitment trajectories to a nondeterministic recruitment, obtained from null models corresponding to a random sampling of recruits and a randomization of species functional traits. Specifically, we (a) determined postdisturbance successional phases and analyzed the role of deterministic processes along time and (b) examined the return of recruited community to predisturbance taxonomic and functional characteristics.

K E Y W O R D S
community composition, community diversity, disturbance response, functional trait, Neotropical forests, postdisturbance recovery, recruitment, successional pathway, taxonomy, tree community 2 | MATERIAL AND ME THODS

| Study site
The Paracou station is located in a lowland tropical rainforest in French Guiana (5°18′N and 52°53′W). The climate is tropical wet with mean annual precipitation averaging 2,980 mm/year (30-year period) and a 3-month dry season (<100 mm/month) from mid-August to mid-November and a one-month dry season in March . The mean annual temperature is 26°C. Elevation ranges from 5 to 50 m. Across all the study plots, the topography mainly corresponds to hilltops or hillsides, while bottomlands account for The experiment comprises a network of twelve 6.25-ha plots (Table 1) with three replicates of three disturbance treatments applied in 1987 according to a randomized plot design , and three control plots. The treatments included successively, along the intensity gradient, the logging of a set of 58 commercially exploited species, the thinning by poison-girdling of noncommercially exploited species, with thinned trees left standing in the plots, and eventually the additional logging of noncommercially exploited species (Gourlet-Fleury et al., 2004). Disturbance intensity was measured considering the silvicultural treatments and the resulting damage through the percentage of aboveground standing biomass of trees above 10 cm DBH (%AGB) lost between the first inventory in 1984 and that conducted five years after disturbance, when we considered that tree mortality induced by disturbance had ended (Piponiot et al., 2016). Above ground biomass was estimated using the BIOMASS R package (Réjou-Méchain et al., 2017, without accounting for lianas. We considered six functional traits representing leaf economics: leaf thickness, toughness, total chlorophyll content, and specific leaf area; and stem economics: wood-specific gravity and bark thickness.

| Inventory protocol and data collection
These traits were obtained from the BRIDGE project (http://www. ecofog.gf/Bridg e/), which reliably measured species functional traits and community functional diversity (Paine et al., 2015), as detailed below. Trait values were measured from a selection of individuals located in nine permanent plots in French Guiana, including two in Paracou, and comprised 294 species belonging to 157 genera.
Between 1 and 159 individuals were sampled per species, and for each individual, three new but fully expanded leaves were collected. Guianan tropical trees (Coste et al., 2010); and the leaf specific area, computed as the ratio between leaf area measured from digital scan and dry mass measured following drying to constant mass at 50°C.
Mean foliar trait values of sampled leaves were used as tree-level  et al., 2007) and comprises 362 species belonging to 188 genera.
All composition and diversity metrics were obtained after 100 iterations of the uncertainty propagation framework.

| Recruitment trajectories
To explore recruitment trajectories in time, trees that survived the disturbance were discarded from the following analyses. Our observation of recruitment diversity trajectories and turnover started from the fifth year after disturbance, when we considered that tree mortality induced by disturbance had ended (Piponiot et al., 2016).
Trajectories then considered the trees recruited at 2-year intervals (i.e., for time T, the trees that were under 10 cm DBH 2 years before but above 10 cm DBH at T). For control plots, the starting point of recruitment trajectories was the same year as for disturbed plots, that is, five years after disturbance was applied.
Taxonomic diversity (H q obs ) trajectories were examined through species richness and the Hill number transformation of the Simpson index assessing communities evenness. The later will be designated as "taxonomic evenness" (Chao & Jost, 2015;Marcon & Hérault, 2015). The two diversity measures derived from the set of generalized entropy measures, also called Tsallis entropy, and respectively correspond to the zero and two order of diversity. The order of diversity emphasizes species importance according to their stem density. Community richness and evenness account for the structure of dominance in the community and their use can measure changes in community abundance distribution. The two diversity metrics are complementary for the detection of changes in community structure (Magurran, 2004) and will directly be referred to as richness and evenness thereafter. The functional null models maintained the community abundance distribution while randomizing the relative abundance of trait values (Mason et al., 2013). Trajectories of null diversity (hereafter H q null ) were similarly obtained after 100 iterations of the random sampling models. For each iteration of the null model, we computed the difference between null and observed trajectories. The 100 iterations made it possible to calculate a 95% confidence interval of the difference between null and observed trajectories.
We tested whether disturbance intensity, in terms of AGB lost, was correlated with diversity and composition using Spearman's test.  (Wood, 2011). With T ab the turnover between communities a and b, n the total number of species in the two communities and x a/b i the abundance of species i in community a or b.
Postdisturbance diversity, composition, and turnover trajectories were analyzed to detect their shifts via breakpoints analysis derived from methods developed in Bai and Perron (2003).
Observed trajectories were partitioned into two or three intervals, each fit by linear regression models. Intervals were defined by one or two different points in time, representing potential breakpoints of the trajectories. For each trajectory, the number and time of breakpoints and the corresponding linear models that minimized the mean square error for the whole trajectory were retained.

| RE SULTS
The average number of recruited trees per plot and per year throughout the survey increased with increasing disturbance intensity. Over the 30-year period, a total of 602 species were recruited across the 12 plots. Among these species, 26% only occurred in one plot and 7% occurred in all plots.
The propagation framework for botanical uncertainties returned an estimation of community diversity with a 95% confidence interval that remained below 10% of the estimated value. Taxonomic diversity estimations showed significantly distinct trajectories among plots with no overlapping confidence intervals (Figure 1a,b), while functional trajectories were not as distinctly separated (Figure 1c),

| Taxonomic richness and evenness
In undisturbed communities, the taxonomic richness and evenness of the recruited trees remained stable over the 30-year period, with values equivalent to those of the taxonomic null model (Figure 1a,b). In all disturbed communities, the taxonomic evenness decreased over the 30 years whenever the disturbance intensity, but the maximum decrease was not correlated with disturbance intensity ( Evenness Spearman = 0.03, p-value = 9.2 × 10 −1 ). The comparison with the null model showed an observed taxonomic evenness significantly lower than what would be expected from the observed community. The difference between the observed and null model evenness followed a hump-shaped trajectory with a maximum difference reached between 20 and 25 years after disturbance, and the maximum difference was positively correlated with disturbance intensity ( Evenness Spearman = 0.45, p-value = 1.5 × 10 −1 ). The breakpoint analysis of evenness trajectories revealed a single breakpoint occurring between 10 and 23 years following disturbance (Appendix S2).

| Functional diversity
The functional diversity in the undisturbed plots changed little and remained equivalent to that of the functional null model over the 30-year period. In the plots with the least disturbance, below 30% of lost AGB, functional diversity remained stable or increased slightly and, for two plots, was higher than that of the null model.
In disturbed plots with higher disturbance intensity, functional diversity decreased until 15 years after disturbance and then started to recover initial values (Figure 1c). The maximum change F I G U R E 2 The trajectories of community weighted means (CWM) over the 30-year period of the seven functional traits measured in the populations recruited by 2-years intervals. Lines represent the observed trajectories fit from GAM models at plot level and the colors stand for the disturbance intensity in percentage of AGB lost, including control plots in green. From top left to bottom right, the graphs correspond to leaf thickness, leaf chlorophyll content, leaf toughness, specific leaf area (SLA), wood specific gravity (WSG), bark thickness and maximum height at the adult stage (H max ) in community functional diversity over the 30 years was positively correlated with the disturbance intensity (ρ Functional diversity = 0.24, p-value = 4.4 × 10 −1 ). The observed functional diversity remained lower than that of the null model over the 30-year period (Figure 1c).
The maximum difference between observed and null trajectories was positively but not significantly correlated with the disturbance intensity (ρ Functional diversity = 0.06, p-value = .8). The breakpoints point analysis of functional diversity revealed a single breakpoint occurring from 10 to 23 years following disturbance (Appendix S2).

| Functional composition
Functional traits CWM in undisturbed plots remained stable over the 30-year period whereas in all the disturbed plots traits CWM trajectories were hump-shaped, with the exception of leaf chlorophyll content (Figure 2). The trajectories of SLA and bark thickness initially increased before decreasing toward initial values. Conversely, trajectories of leaf thickness, leaf toughness, wood-specific gravity, and maximum height first decreased and then started returning to their initial values but their recovery was still not complete at the end of the 30-year period (Figure 2).

| Recruitment turnover
The turnover of recruited species in control plots compared to the initial community remained low over the 30-year period (Figure 3).
In disturbed plots, the turnover of the recruited species followed a marked hump-shaped trajectory, with a maximum reached about 15 years after the disturbance. The maximum turnover was positively correlated with disturbance intensity ( Turnover Spearman = 0.93, pvalue = 1.3 × 10 −5 ). The breakpoints analysis of taxonomic turnover revealed a single breakpoint occurring from 17 to 23 years following disturbance (Appendix S2). Thirty years after the disturbance, the turnover had returned to low values.
The dominant species recruited in disturbed plots were Miconia tschudyoides, Inga sp., Oenocarpus bataua, Licania alba, and Xylopia sp.. We besides analyzed the dominant species of recruited communities in disturbed plots, considering the years before or after the breakpoints detected for each plot trajectory with the breakpoint analysis. During the years before the breakpoints, the dominant species recruited in disturbed plots were Vismia spp., Cecropia obtusa, Oxandra asbeckii, Cecropia sciadophylla, and Lecythis persistens.

| D ISCUSS I ON
Our study showed that recruitment trajectories followed a twophased successional pathway. First, trajectories were defined by the emergence, a decade after disturbance, of deterministic competition for light. Then, nondeterministic, broader recruitment processes recovered progressively (Clements, 1916;Denslow & Guzman, 2000;Meiners et al., 2015). The first phase, which length and extent depended on the disturbance intensity, corresponded to the dominance of pioneers and light-demanding species in recruited communities.
The second phase was a progressive return to the recruitment processes specific to undisturbed communities, corresponding to a dominance of shade-tolerant, late-successional species.
The propagation framework of botanical uncertainties proved accurate enough to discriminate and analyze postdisturbance trajectories of recruited communities in the long-term trends.

| The emergence of deterministic successional pathway
A first phase was defined by an increase of the taxonomic turnover between recruited trees and initial communities ( Figure 3) and by the divergence between observed and null trajectories (Figure 1). Just after disturbance, the functional composition shifted from a broad panel of species functional strategies to more "resource-acquisitive" species ( Figure 2). Recruits specifically displayed higher light acquisition efficiency, that is, high SLA and low maximum height, leaf toughness, and wood-specific gravity (Chave et al., 2009;Hérault et al., 2011;Wright et al., 2004). This shift toward "light-acquisitive" functional strategies was coherent with the assumed role of light F I G U R E 3 Trajectories over the 30 years of the relativized abundance-based turnover between recruited populations and the whole pre-disturbance communities. Recruited populations were analyzed at 2-year intervals at plot level and compared to the plot inventory carried out before the disturbance. The colored lines stand for the disturbance intensity in precentage of AGB lost, including control plots in green. Shaded areas are the 95% confidence intervals, CI 95%, measured from the 100 iterations of the null models, when not visible on the figure, intervals are too small availability in the successional pathways followed by postdisturbance recruitment processes, as already demonstrated in temperate and tropical forests (Both et al., 2019;Carreño-Rocabado et al., 2012;Kunstler et al., 2016;Peña-Claros et al., 2008). During the first decades following disturbance, recruits comprised mainly species belonging to Cecropia or Vismia genera, recognized as pioneers in former studies, or species belonging to Miconia, Oxandra, or Xylopia genera, recognized as nonpioneer light-demanding species (Fortunel et al., 2014;Molino & Sabatier, 2001). Postdisturbance trajectories hence revealed, during a first phase, the emergence of deterministic recruitment processes based on species light acquisition strategy which favored only a restricted pool of pioneers and light-demanding species (Figures 1 and 2). These postdisturbance recruitment processes resulted in a decrease of the taxonomic richness and evenness of the recruited communities. Changes in community diversity and composition were all the more significant that disturbance had been intense, suggesting an increasing importance of postdisturbance deterministic processes (Bongers et al., 2009).

| Return toward predisturbance recruitment processes
Following the first phase, lasting between 15 and 20 years depending on the disturbance intensity, recruitment trajectories showed a return toward predisturbance values of functional diversity and taxonomic richness (Fortunel et al., 2014;Fukami et al., 2005).
Taxonomic evenness and functional composition, however, remained altered (Figures 1 and 2). The second phase corresponded to the recruitment of both species with "acquisitive" strategies, resulting in an increase of leaf thickness and leaf toughness CWM values, and of species with "conservative" strategies, resulting in an increase of maximum height and bark thickness CWM values ( Figure 2). The changes in functional trajectories matched the changes in taxonomic composition. Although pioneers and light-demanding species were still dominant in recruited communities, as species belonging to Inga or Miconia genera, late-successional species as Licania alba progressively established (Fortunel et al., 2014). The recruitment of late successionals could reflect the progressive closing of the forest canopy and the increase in competition for light and space (Denslow & Guzman, 2000;Peet, 1992). During the second successional phase, lowly restrictive recruitment processes, specific to undisturbed forests, progressively offset the first postdisturbance deterministic processes (Chave, 2004;Lawton & Putz, 1988).
Does it mean that such a return toward predisturbance state would result in values of diversity and composition identical to the predisturbance community? Our results do not allow answering that, but they are coherent with the idea of significant dispersal limitations among tropical tree species, without which other species might have colonized the community and changed its composition and diversity (Svenning & Wright, 2005). Anyway, the general trend in return toward predisturbance state allows to take more perspectives on previous results obtained in the Paracou experiment, conducted 10 years (Molino & Sabatier, 2001) and 20 years (Baraloto et al., 2012) after disturbance. Both studies showed the consistent changes in community taxonomic and functional composition but the second study, conducted later, showed lower contrasts among disturbed plots. This was interpreted as early signs of a return toward predisturbance states, as species detected in the first study were short-lived pioneers that did not persist until the second study.
Our results confirm that these early signs corresponded well to a profound change in community trajectories. Although community trajectories returned toward predisturbance states, both taxonomic and functional characteristics remained different from predisturbance community and from control plot values 30 years after the disturbance. The higher the disturbance intensity, the more persistent the dominance of light-demanding species. Such a long-term impact raises questions for the management of tropical forests as most commercially valuable species are late-successional species.
Their exploitation would consequently require cutting cycles longer than 30 years, as it is currently applied in most tropics, as after this duration no plot had returned to predisturbance value (Putz et al., 2012). Furthermore, persistent changes in community composition likely alter community functioning (Díaz et al., 2005), and increase the risk of losing keystone species, with unexpected ecological consequences (Chazdon, 2003;Jones et al., 1994). Infrequent species might indeed have unique functional characteristics in the ecosystem, apart from the ones considered here, or be a key resource for some of the fauna (Schleuning et al., 2016).

| CON CLUS ION
Postdisturbance recruitment trajectories revealed a two-phase deterministic successional pathway driven by the emergence of traitbased deterministic processes favoring light-acquisitive species. The first phase corresponded to the recruitment of a restricted pool of pioneers and light-demanding species benefiting from the emergence of competitive exclusion for light. Above a disturbance intensity threshold, disturbed communities saw the dominance of short-lived, fast-growing pioneers that drastically changed community composition, diversity, and likely functioning of recruits. The second phase corresponded to the progressive recovery of broader recruitment processes specific to undisturbed communities and to a shift toward predisturbance taxonomic and functional diversity and composition.
However, the recovery toward predisturbance diversity and composition values took longer than 30 years after the original disturbance.
Concerning forest management, our results support cutting cycles longer than 30 years and demonstrate long-term impacts, underlining the need to evaluate forest management sustainability.

ACK N OWLED G M ENT
We are extremely grateful to all Paracou station technicians and colleagues who helped set up the plots and collected data over the years. Without their precious work, this study would have not been possible.