Functional and Phylogenetic Dimensions of Tree Diversity Across Environmental Gradients in Puerto Rico: Insights to community assembly processes

One goal central to ecology is to understand how species interactions and biophysical processes interact over vastly different scales to govern past, current, and future patterns of diversity. Today, this goal is particularly critical given the degree to which rapid environmental change is affecting species distributions and community composition. Natural environmental gradients provide excellent opportunities to uncover possible mechanistic links between species distributions and environmental conditions links that are invaluable for understanding how species may respond to environmental change. This dissertation builds on recent approaches that combine information on species' functional traits and evolutionary histories to refine our view of how contemporary and historical processes jointly govern the distribution of biodiversity. In the context of tropical tree communities of Puerto Rico, the following four chapters evaluate hypotheses about the distribution of different dimensions of diversity (i.e., species, functional, and phylogenetic) across regional abiotic gradients. In chapter 1, I develop an island-wide molecular phylogeny for the native and naturalized trees of Puerto Rico, and show preliminary evidence that dry forests comprise an evolutionarily clustered subset of the total island tree flora. In chapter 2, I examine functional and phylogenetic diversity across spatial resource gradients, and use these patterns to infer variation in community assembly processes along a gradient of water availability. In chapter 3, I use temporal shifts of functional and phylogenetic diversity during secondary succession to infer the shifts in the processes underlying successional change in wet forests of Puerto Rico. Finally, in chapter 4, I evaluate the linkages between species functional traits and their geographic distributions, and test the hypothesis that community-weighted mean trait values reflect the `optimal' strategy for a given set of abiotic conditions. A theme common to all chapters is the idea that functional and phylogenetic dimensions of diversity can shed light on the processes underlying patterns of diversity better than more traditional metrics of species diversity. I provide recommendations for future research directions at the end of each chapter and in the final conclusions

Hurricane-induced rainfall is a stronger predictor of tropical forest damage in Puerto Rico than maximum wind speeds

Projected increases in cyclonic storm intensity under a warming climate will have profound effects on forests, potentially changing these ecosystems from carbon sinks to sources. Forecasting storm impacts on these ecosystems requires consideration of risk factors associated with storm meteorology, landscape structure, and forest attributes. Here we evaluate risk factors associated with damage severity caused by Hurricanes María and Irma across Puerto Rican forests. Using field and remote sensing data, total forest aboveground biomass (AGB) lost to the storms was estimated at 10.44 (±2.33) Tg, ca. 23% of island-wide pre-hurricane forest AGB. Storm-related rainfall was a stronger predictor of forest damage than maximum wind speeds. Soil water storage capacity was also an important risk factor, corroborating the influence of rainfall on forest damage. Expected increases of 20% in hurricane-associated rainfall in the North Atlantic highlight the need to consider how such shifts, together with high speed winds, will affect terrestrial ecosystems

A Well-Resolved Phylogeny of the Trees of Puerto Rico Based on DNA Barcode Sequence Data

Background: The use of phylogenetic information in community ecology and conservation has grown in recent years. Two key issues for community phylogenetics studies, however, are (i) low terminal phylogenetic resolution and (ii) arbitrarilydefined species pools. Methodology/principal findings: We used three DNA barcodes (plastid DNA regions rbcL, matK, and trnH-psbA) to infer a phylogeny for 527 native and naturalized trees of Puerto Rico, representing the vast majority of the entire tree flora of the island (89%). We used a maximum likelihood (ML) approach with and without a constraint tree that enforced monophyly of recognized plant orders. Based on 50% consensus trees, the ML analyses improved phylogenetic resolution relative to a comparable phylogeny generated with PHYLOMATIC (proportion of internal nodes resolved:constrained ML = 74%, unconstrained ML = 68%, PHYLOMATIC = 52%). We quantified the phylogenetic composition of 15 protected forests in Puerto Rico using the constrained ML and PHYLOMATIC phylogenies. We found some evidence that tree communities in areas of high water stress were relatively phylogenetically clustered. Reducing the scale at which the species pool was defined (from island to soil types) changed some of our results depending on which phylogeny (ML vs. PHYLOMATIC) was used. Overall, the increased terminal resolution provided by the ML phylogeny revealed additional patterns that were not observed with a less-resolved phylogeny. Conclusions/significance: With the DNA barcode phylogeny presented here (based on an island-wide species pool), we show that a more fully resolved phylogeny increases power to detect nonrandom patterns of community composition in several Puerto Rican tree communities. Especially if combined with additional information on species functional traits and geographic distributions, this phylogeny will (i) facilitate stronger inferences about the role of historical processes in governing the assembly and composition of Puerto Rican forests, (ii) provide insight into Caribbean biogeography, and (iii) aid in incorporating evolutionary history into conservation planning

Edaphic heterogeneity and the evolutionary trajectory of Amazonian plant communities

We investigated how the phylogenetic structure of Amazonian plant communities varies along an edaphic gradient within the non-inundated forests. Forty localities were sampled on three terrain types representing two kinds of soil: clayey soils of a high base cation concentration derived from the Solimões formation, and loamy soils with lower base cation concentration derived from the Içá formation and alluvial terraces. Phylogenetic community metrics were calculated for each locality for ferns and palms both with ferns as one group and for each of three fern clades with a crown group age comparable to that of palms. Palm and fern communities showed significant and contrasting phylogenetic signals along the soil gradient. Fern species richness increased but standard effect size of mean pairwise distance (SES.MPD) and variation of pairwise distances (VPD) decreased with increasing soil base cation concentration. In contrast, palm communities were more species rich on less cation-rich soils and their SES.MPD increased with soil base cation concentration. Species turnover between the communities reflected the soil gradient slightly better when based on species occurrences than when phylogenetic distances between the species were considered. Each of the three fern subclades behaved differently from each other and from the entire fern clade. The fern clade whose phylogenetic patterns were most similar to those of palms also resembled palms in being most species-rich on cation-poor soils. The phylogenetic structuring of local plant communities varies along a soil base cation concentration gradient within non-inundated Amazonian rain forests. Lineages can show either similar or different phylogenetic community structure patterns and evolutionary trajectories, and we suggest this to be linked to their environmental adaptations. Consequently, geological heterogeneity can be expected to translate into a potentially highly diverse set of evolutionarily distinct community assembly pathways in Amazonia and elsewhere.</p

Interspecific functional convergence and divergence and intraspecific negative density dependence underlie the seed-to-seedling transition in tropical trees

The seed-to-seedling transition constitutes a critical bottleneck in the life history of plants and represents a major determinant of species composition and abundance. However, we have surprisingly little knowledge regarding the forces driving this ontogenetic transition. Here we utilize information regarding organismal function to investigate the strength of intra- and interspecific negative density dependence during the seed-to-seedling transition in Puerto Rican tree species. Our analyses were implemented at individual sites and across an entire 16-ha forest plot, spanning 6 years. The functional richness of seedling assemblages was significantly lower than expected given the seed assemblages, but the functional evenness was significantly higher than expected, indicating the simultaneous importance of constraints on the overall phenotypic space and trait differences for successful transitions from seed to seedling. The results were consistent across years. Within species, we also found evidence for strong intraspecific negative density dependence, where the probability of transition was proportionally lower when in a site with high conspecific density. These results suggest that filtering of similar phenotypes across species and strong negative density dependence within and among species are simultaneously driving the structure and dynamics of tropical tree assemblages during this critical life-history transition

Height–diameter allometry for a dominant palm to improve understanding of carbon and forest dynamics in forests of Puerto Rico

Tropical forests play a major role in the global carbon cycle but their diversity and structural complexity challenge our ability to accurately estimate carbon stocks and dynamics. Palms, in particular, are prominent components of many tropical forests that have unique anatomical, physiological, and allometric differences from dicot trees, which impede accurate estimates of their aboveground biomass (AGB) and population dynamics. We focused on improving height estimates and, ultimately, AGB estimates for a highly abundant palm in Puerto Rico, Prestoea acuminata. Based on field measurements of 1003 individuals, we found a strong relationship between stem height and diameter. We also found some evidence that height–diameter allometry of P. acuminata is mediated by various sources of environmental heterogeneity including slope and neighborhood crowding. We then examined variability in AGB estimates derived from three models developed to estimate palm AGB. Finally, we applied our novel height:diameter allometric model to hindcast dynamics of P. acuminata in the Luquillo Forest Dynamics Plot during a 27-year period (1989–2016) of post-hurricane recovery. Overall, our study provides improved estimates of AGB in wet forests of Puerto Rico and will facilitate novel insights to the dynamics of palms in tropical forests

Ontogenetic shifts in trait-mediated mechanisms of plant community assembly

Identifying the processes that maintain highly diverse plant communities remains a central goal in ecology. Species variation in growth and survival rates across ontogeny, represented by tree size classes and life history stage-specific niche partitioning, are potentially important mechanisms for promoting forest diversity. However, the role of ontogeny in mediating competitive dynamics and promoting functional diversity is not well understood, particular in high-diversity systems such as tropical forests. The interaction between interspecific functional trait variation and ontogenetic shifts in competitive dynamics may yield insights into the ecophysiological mechanisms promoting community diversity. We investigated how functional trait (seed size, maximum height, SLA, leaf N, and wood density) associations with growth, survival, and response to competing neighbors differ among seedlings and two size classes of trees in a subtropical rain forest in Puerto Rico. We used a hierarchical Bayes model of diameter growth and survival to infer trait relationships with ontogenetic change in competitive dynamics. Traits were more strongly associated with average growth and survival than with neighborhood interactions, and were highly consistent across ontogeny for most traits. The associations between trait values and tree responses to crowding by neighbors showed significant shifts as trees grew. Large trees exhibited greater growth as the difference in species trait values among neighbors increased, suggesting trait-associated niche partitioning was important for the largest size class. Our results identify potential axes of niche partitioning and performance-equalizing functional trade-offs across ontogeny, promoting species coexistence in this diverse forest community

Biophysical and Socioeconomic Factors Associated with Forest Transitions at Multiple Spatial and Temporal Scales

Forest transitions (FT) occur when socioeconomic development leads to a shift from net deforestation to reforestation; these dynamics have been observed in multiple countries across the globe, including the island of Puerto Rico in the Caribbean. Starting in the 1950s, Puerto Rico transitioned from an agrarian to a manufacturing and service economy reliant on food imports, leading to extensive reforestation. In recent years, however, net reforestation has leveled off. Here we examine the drivers of forest transition in Puerto Rico from 1977 to 2000 at two subnational, nested spatial scales (municipality and barrio) and over two time periods (1977-1991 and 1991-2000). This study builds on previous work by considering the social and biophysical factors that influence both reforestation and deforestation at multiple spatial and temporal scales. By doing so within one analysis, this study offers a comprehensive understanding of the relative importance of various social and biophysical factors for forest transitions and the scales at which they are manifest. Biophysical factors considered in these analyses included slope, soil quality, and land-cover in the surrounding landscape. We also considered per capita income, population density, and the extent of protected areas as potential factors associated with forest change. Our results show that, in the 1977-1991 period, biophysical factors that exhibit variation at municipality scales (~100 km²) were more important predictors of forest change than socioeconomic factors. In this period, forest dynamics were driven primarily by abandonment of less productive, steep agricultural land in the western, central part of the island. These factors had less predictive power at the smaller barrio scale (~10 km²) relative to the larger municipality scale during this time period. The relative importance of socioeconomic variables for deforestation, however, increased over time as development pressures on available land increased. From 1991-2000, changes in forest cover reflected influences from multiple factors, including increasing population densities, land development pressure from suburbanization, and the presence of protected areas. In contrast to the 1977-1991 period, drivers of deforestation and reforestation over this second interval were similar for the two spatial scales of analyses. Generally, our results suggest that although broader socioeconomic changes in a given region may drive the demand for land, biophysical factors ultimately mediate where development occurs. Although economic development may initially result in reforestation due to rural to urban migration and the abandonment of agricultural lands, increased economic development may lead to deforestation through increased suburbanization pressures

Shifts in wood anatomical traits after a major hurricane

•1. Trait variation across individuals and species influences the resistance and resilience of ecosystems to disturbance, and the ability of individuals to capitalize on postdisturbance conditions. In trees, the anatomical structure of xylem directly affects plant function and, consequently, it is a valuable lens through which to understand resistance and resilience to disturbance. •2. To determine how hurricanes affect wood anatomy of tropical trees, we characterized a set of anatomical traits in wood produced before and after a major hurricane for 65 individuals of 10 Puerto Rican tree species. We quantified variation at different scales (among and within species, and within individuals) and determined trait shifts between the pre- and posthurricane periods. We also assessed correlations between traits and growth rates. •3. While the majority of anatomical trait variation occurred among species, we also observed substantial variation within species and individuals. Within individuals, we found significant shifts for some traits that generally reflected increased hydraulic conductivity in the posthurricane period. We found weak evidence for an association between individual xylem anatomical traits and diameter growth rates. •4. Ultimately, within-individual variation of xylem anatomical traits observed in our study could be related to posthurricane recovery and overall growth (e.g. canopy filling). Other factors, however, likely decouple a relationship between xylem anatomy and diameter growth. While adjustments of wood anatomy may enable individual trees to capitalize on favourable postdisturbance conditions, these may also influence their future responses or vulnerability to subsequent disturbances

Associations among arbuscular mycorrhizal fungi and seedlings are predicted to change with tree successional status

Arbuscular mycorrhizal (AM) fungi in the soil may influence tropical tree dynamics and forest succession. The mechanisms are poorly understood, because the functional characteristics and abundances of tree species and AM fungi are likely to be codependent. We used generalized joint attribute modeling to evaluate if AM fungi are associated with three forest community metrics for a sub-tropical montane forest in Puerto Rico. The metrics chosen to reflect changes during forest succession are: the abundance of seedlings of different successional status, the amount of foliar damage on seedlings of different successional status, and community-weighted mean functional trait values (adult specific leaf area (SLA), adult wood density, and seed mass). We used high-throughput DNA sequencing to identify fungal operational taxonomic units (OTUs) in the soil. Model predictions showed that seedlings of mid- and late-successional species had less leaf damage when the 12 most common AM fungi were abundant compared to when these fungi were absent. We also found that seedlings of mid-successional species were predicted to be more abundant when the 12 most common AM fungi were abundant compared to when these fungi were absent. In contrast, early-successional tree seedlings were predicted to be less abundant when the 12 most common AM fungi were abundant compared to when these fungi were absent. Finally, we showed that, among the 12 most common AM fungi, different AM fungi were correlated with functional trait characteristics of early- or late-successional species. Together, these results suggest that early-successional species might not rely as much as mid- and late-successional species on AM fungi, and AM fungi might accelerate forest succession