Horacio Paz

Are functional traits good predictors of demographic rates? Evidence from five neotropical forests

A central goal of comparative plant ecology is to understand how functional traits vary among species and to what extent this variation has adaptive value. Here we evaluate relationships between four functional traits (seed volume, specific leaf area, wood density, and adult stature) and two demographic attributes (diameter growth and tree mortality) for large trees of 240 tree species from five Neotropical forests. We evaluate how these key functional traits are related to survival and growth and whether similar relationships between traits and demography hold across different tropical forests. There was a tendency for a trade-off between growth and survival across rain forest tree species. Wood density, seed volume, and adult stature were significant predictors of growth and/or mortality. Both growth and mortality rates declined with an increase in wood density. This is consistent with greater construction costs and greater resistance to stem damage for denser wood. Growth and mortality rates also declined as seed volume increased. This is consistent with an adaptive syndrome in which species tolerant of low resource availability (in this case shade-tolerant species) have large seeds to establish successfully and low inherent growth and mortality rates. Growth increased and mortality decreased with an increase in adult stature, because taller species have a greater access to light and longer life spans. Specific leaf area was, surprisingly, only modestly informative for the performance of large trees and had ambiguous relationships with growth and survival. Single traits accounted for 9-55% of the interspecific variation in growth and mortality rates at individual sites. Significant correlations with demographic rates tended to be similar across forests and for phylogenetically independent contrasts as well as for cross-species analyses that treated each species as an independent observation. In combination, the morphological traits explained 41% of the variation in growth rate and 54% of the variation in mortality rate, with wood density being the best predictor of growth and mortality. Relationships between functional traits and demographic rates were statistically similar across a wide range of Neotropical forests. The consistency of these results strongly suggests that tropical rain forest species face similar trade-offs in different sites and converge on similar sets of solutions.

Ecological differentiation in xylem cavitation resistance is associated with stem and leaf structural traits

Cavitation resistance is a critical determinant of drought tolerance in tropical tree species, but little is known of its association with life history strategies, particularly for seasonal dry forests, a system critically driven by variation in water availability. We analysed vulnerability curves for saplings of 13 tropical dry forest tree species differing in life history and leaf phenology. We examined how vulnerability to cavitation (P₅₀) related to dry season leaf water potentials and stem and leaf traits. P₅₀-values ranged from -0.8 to -6.2 MPa, with pioneers on average 38% more vulnerable to cavitation than shade-tolerants. Vulnerability to cavitation was related to structural traits conferring tissue stress vulnerability, being negatively correlated with wood density, and surprisingly maximum vessel length. Vulnerability to cavitation was negatively related to the Huber-value and leaf dry matter content, and positively with leaf size. It was not related to SLA. We found a strong trade-off between cavitation resistance and hydraulic efficiency. Most species in the field were operating at leaf water potentials well above their P₅₀, but pioneers and deciduous species had smaller hydraulic safety margins than shade-tolerants and evergreens. A trade-off between hydraulic safety and efficiency underlies ecological differentiation across these tropical dry forest tree species.

Successional changes in functional composition contrast for dry and wet tropical forest

We tested whether and how functional composition changes with succession in dry deciduous and wet evergreen forests of Mexico. We hypothesized that compositional changes during succession in dry forest were mainly determined by increasing water availability leading to community functional changes from conservative to acquisitive strategies, and in wet forest by decreasing light availability leading to changes from acquisitive to conservative strategies. Research was carried out in 15 dry secondary forest plots (5-63 years after abandonment) and 17 wet secondary forest plots (< 1-25 years after abandonment). Community-level functional traits were represented by community-weighted means based on 11 functional traits measured on 132 species. Successional changes in functional composition are more marked in dry forest than in wet forest and largely characterized by different traits. During dry forest succession, conservative traits related to drought tolerance and drought avoidance decreased, as predicted. Unexpectedly acquisitive leaf traits also decreased, whereas seed size and dependence on biotic dispersal increased. In wet forest succession, functional composition changed from acquisitive to conservative leaf traits, suggesting light availability as the main driver of changes. Distinct suites of traits shape functional composition changes in dry and wet forest succession, responding to different environmental filters.

SEED MASS, SEEDLING EMERGENCE, AND ENVIRONMENTAL FACTORS IN SEVEN RAIN FOREST PSYCHOTRIA (RUBIACEAE)

We examined the effects of seed mass on performance between the time of seed dispersal and emergence within seven sympatric rain forest woody species of Psy- chotria in two contrasting natural habitats: gaps and shaded forest. We determined the effects of seed mass on emergence (the total proportion of emerged seedlings) and on the speed of emergence (the time necessary to reach 50% total emerged seedlings) in both greenhouse and field conditions, and we observed the effects of seed mass on the risk of removal by animals in the field. The effects of seed mass on performance were specific to species and habitat. For example, in two species, seed mass had a positive effect on emer- gence, while another showed a negative effect; for most of the species, effects on perfor- mance restricted to only one habitat (shaded forest or gap). Similarly, the results for effects of seed mass on the risk of removal were species- and habitat-specific. In the greenhouse, seed mass did not affect either emergence or the speed of emergence under either high or low light conditions. Our results suggest that: (i) seed mass did not have a general effect on emergence success and (ii) the effects of seed mass on seedling emergence are driven by external ecological factors more than by intrinsic effects of seed mass. Seed-removing animals appear to be an important ecological agent operating on intraspecific seed mass variation.

Coordinated evolution of leaf and stem economics in tropical dry forest trees

With data from 15 species in eight families of tropical dry forest trees, we provide evidence of coordination between the stem and leaf economic spectra. Species with low-density, flexible, breakable, hydraulically efficient but cavitationally vulnerable wood shed their leaves rapidly in response to drought and had low leaf mass per area and dry mass content. In contrast, species with the opposite xylem syndrome shed their costlier but more drought-resistant leaves late in the dry season. Our results explain variation in the timing of leaf shedding in tropical dry forests: selection eliminates combinations such as low-productivity leaves atop highly vulnerable xylem or water-greedy leaves supplied by xylem of low conductive efficiency. Across biomes, rather than a fundamental trade-off underlying a single axis of trait covariation, the relationship between leaf and stem economics is likely to occupy a wide space in which multiple combinations are possible.

Temporal variation in the pollen:ovule ratios of Clarkia (Onagraceae) taxa with contrasting mating systems: field populations

Among plants, pairs of selfing vs. outcrossing sister taxa provide interesting systems in which to test predictions concerning the magnitude and direction of temporal changes in sex allocation. Although resource availability typically declines towards the end of the growing season for annual taxa, temporal changes in mating opportunities depend on mating system and should change less in selfing taxa. Consequently, given that the pollen:ovule (P:O) ratio of flowers reflects the investment in (and potential fitness pay‐off due to) male vs. female function, we predicted that the P:O ratio should also be less variable among and within selfers than in closely related outcrossers. To test these predictions, we measured temporal changes in sex allocation in multiple field populations of two pairs of sister taxa in the annual flowering plant genus Clarkia (Onagraceae). In the outcrossing Clarkia unguiculata and the selfing Clarkia exilis, ovule production declined similarly from early to late buds, whereas pollen production remained constant or increased in the outcrosser but remained constant or decreased in the selfer. Consequently, the P:O ratio increased within unguiculata populations but marginally increased or stayed constant in exilis populations. In all populations of the selfing Clarkia xantiana spp. parviflora and the outcrossing C. x. spp. xantiana, both ovule and pollen production per flower declined over time. The effects of these declines on the P:O ratio, however, differed between subspecies. In each xantiana population, the mean P:O ratio did not differ between early and late flowers, although individuals varied greatly in the direction and magnitude of phenotypic change. By contrast, parviflora populations differed in the mean direction of temporal change in the P:O ratio. We found little evidence to support our initial predictions that the P:O ratio of the selfing taxa will consistently vary less than in outcrossing taxa.

Leaf phenology is associated with soil water availability and xylem traits in a tropical dry forest

In tropical dry forests, spatial heterogeneity in soil water availability is thought to determine interspecific differences in key components of resource use strategies, such as leaf phenology and xylem function. To understand the environmental drivers of variation in leaf phenology and xylem function, we explored the relation of soil water potential to topographic metrics derived from a digital elevation model. Subsequently, we compared nine xylem hydraulic, mechanical and storage traits in 18 species in three phenological classes (readily deciduous, tardily deciduous, and evergreen) in the dry tropical forest of Chamela, Mexico. Soil water potential was negatively correlated with elevation, insolation and water flow accumulation. Evergreen species characterized low-elevation moist sites, whereas deciduous species dominated hills and dry sites. Overall, evergreen species had lower xylem specific conductivity than deciduous species, and tardily deciduous species were different from readily deciduous and evergreen species in five of eight xylem traits. In dry tropical forests, water availability promotes divergence in leaf phenology and xylem traits, ranging from low wood density, evergreen species in moist sites to a combination of low wood density, readily deciduous species plus high wood density, tardily deciduous species in dry sites.

Morphological and physiological differentiation of seedlings between dry and wet habitats in a tropical dry forest.

A common observation in tropical dry forests is the habitat preference of tree species along spatial soil water gradients. This pattern of habitat partitioning might be a result of species differentiation in their strategy for using water, along with competing functions such as maximizing water exploitation and tolerating soil water stress. We tested whether species from drier soil conditions exhibited a tolerance strategy compared with that of wet-habitat species. In a comparison of 12 morphophysiological traits in seedlings of 10 closely related dry and wet-habitat species pairs, we explored what trade-offs guide differentiation between habitats and species. Contrary to our expectations, dry-habitat species showed mostly traits associated with an exploitation strategy (higher carbon assimilation capacity, specific leaf area and leaf-specific conductivity and lower water-use efficiency). Strikingly, dry-habitat species tended to retain their leaves longer during drought. Additionally, we detected multiple strategies to live within each habitat, in part due to variation of strategies among lineages, as well as functional differentiation along the water storage capacity-stem density (xylem safety) trade-off. Our results suggest that fundamental trade-offs guide functional niche differentiation among tree species expressed both within and between soil water habitats in a tropical dry forest.

Stability of pollen–ovule ratios in pollinator‐dependent versus autogamous Clarkia sister taxa: testing evolutionary predictions

It has been proposed that natural selection should favor distinct temporal patterns of sex allocation in selfing vs pollinator-dependent taxa. In autogamous selfers in which pollen receipt is highly reliable, selection should favor genotypes that maintain low and stable pollen to ovule (P : O) ratios throughout flowering. By contrast, in outcrossers the optimum P : O ratio of an individuals flowers will depend on pollinator abundances and mating opportunities, both of which may vary over time. In this case, selection may favor temporal variation among flowers in the P : O ratio. An opposing prediction is that selfing taxa will be developmentally more unstable than outcrossers because of lower homeostasis caused by high homozygosity. We compared temporal changes in the P : O ratio in two pairs of sister taxa in the genus Clarkia. We examined hundreds of glasshouse-raised maternal families representing three wild populations each of the outcrossing, insect-pollinated Clarkia unguiculata, the facultatively autogamous Clarkia exilis and the outcrossing and selfing subspecies of Clarkia xantiana: ssp. xantiana and parviflora, respectively. Temporal change in the P : O ratio was significantly greater in both outcrossers than in their selfing sister taxa, although the proportional changes in the P : O ratio (relative to the first bud produced) did not differ significantly between sister taxa (0.07 < P < 0.10). Our results provide partial support for the hypothesis that the P : O ratio is more stable in selfing than in outcrossing taxa and reject the hypothesis that selfers are less stable.

Environmental gradients and the evolution of successional habitat specialization: a test case with 14 Neotropical forest sites

Successional gradients are ubiquitous in nature, yet few studies have systematically examined the evolutionary origins of taxa that specialize at different successional stages. Here we quantify successional habitat specialization in Neotropical forest trees and evaluate its evolutionary lability along a precipitation gradient. Theoretically, successional habitat specialization should be more evolutionarily conserved in wet forests than in dry forests due to more extreme microenvironmental differentiation between early and late-successional stages in wet forest. We applied a robust multinomial classification model to samples of primary and secondary forest trees from 14 Neotropical lowland forest sites spanning a precipitation gradient from 788 to 4000 mm annual rainfall, identifying species that are old-growth specialists and secondary forest specialists in each site. We constructed phylogenies for the classified taxa at each site and for the entire set of classified taxa and tested whether successional habitat specialization is phylogenetically conserved. We further investigated differences in the functional traits of species specializing in secondary vs. old-growth forest along the precipitation gradient, expecting different trait associations with secondary forest specialists in wet vs. dry forests since water availability is more limiting in dry forests and light availability more limiting in wet forests. Successional habitat specialization is non-randomly distributed in the angiosperm phylogeny, with a tendency towards phylogenetic conservatism overall and a trend towards stronger conservatism in wet forests than in dry forests. However, the specialists come from all the major branches of the angiosperm phylogeny, and very few functional traits showed any consistent relationships with successional habitat specialization in either wet or dry forests. Synthesis. The niche conservatism evident in the habitat specialization of Neotropical trees suggests a role for radiation into different successional habitats in the evolution of species-rich genera, though the diversity of functional traits that lead to success in different successional habitats complicates analyses at the community scale. Examining the distribution of particular lineages with respect to successional gradients may provide more insight into the role of successional habitat specialization in the evolution of species-rich taxa.