Environmental heterogeneity influences liana community differentiation across a Neotropical rainforest landscape.

We examined the variation in liana community composition and structure across geopedological land units to test the hypothesis that environmental heterogeneity is a driving force in liana community assembly. The study site was the Los Tuxtlas Tropical Biology Station, SE Mexico, a reserve that encompasses 640 ha of tropical rainforest. We sampled all lianas with basal diameter ≥1 cm in three 0.5-ha plots established in each of five land units (totaling 15 plots and 7.5 ha). We censused 6055 individuals and 110 species. Overall, the most speciose families were also the most abundant ones. Density and basal area of some dominant liana species differed among land units, and a permutational multivariate analysis of variance (PERMANOVA) and a non-metric multidimensional scaling ordination (NMDS) revealed differences in the presence, density, and basal area of liana species across the landscape. Liana composition and structure were highly heterogeneous among land units, suggesting that variations in soil water availability and relief are key drivers of liana community spatial differentiation. By showing that soil and topography play an important role at the landscape scale, we underscore the ecological relevance of environmental heterogeneity for liana community assembly. In the future, as our ability to assess the local environmental complexity increases, we will gain a better understanding of the liana community assembly process and their heterogeneous distribution in tropical forests.

Genomic diversity and structure of a Neotropical microendemic fig tree.

Genetic diversity is a key component of evolution, and unraveling factors that promote genetic differentiation in space and time is a central question in evolutionary biology. One of the most diverse and ecologically important tree genera in tropical forests worldwide is Ficus (Moraceae). It has been suggested that, given the great dispersal capacity of pollinating fig wasps (Chalcidoidea; Agaonidae), the spatial genetic structure, particularly in monoecious fig species, should be weak. However, no studies have addressed the factors that determine the genetic structure of Ficus species in regions of high geological, geographic, and climatic complexity, such as the Mexican Transition Zone. Using nuclear single nucleotide polymorphisms (5311 SNPs) derived from low-coverage whole genomes and 17 populations, we analyzed the population genomics of Ficus pringlei to characterize neutral and adaptive genetic variation and structure and its association with geographic barriers such as the Trans-Mexican Volcanic Belt, environmental heterogeneity, and wind connectivity. From genomic data of 71 individuals, high genetic diversity, and the identification of three genomic lineages were recorded (North, South, and Churumuco). The results suggest that genetic variation is primarily determined by climatic heterogeneity. Ficus pringlei populations from the north and south of the Trans-Mexican Volcanic Belt also exhibited minimal genetic differentiation (F ST = 0.021), indicating that this mountain range may not act as an insurmountable barrier to gene flow. Wind connectivity is also highlighted in structuring putative adaptive genetic variation, underscoring the intricate complexity of the various factors influencing genetic variation in the species. This study provides information on the possible mechanisms underlying the genetic variation of endemic species of the tropical dry forest of Western Mexico, such as F. pringlei.

Underlying and proximate drivers of biodiversity changes in Mesoamerican biosphere reserves.

Protected areas are of paramount relevance to conserving wildlife and ecosystem contributions to people. Yet, their conservation success is increasingly threatened by human activities including habitat loss, climate change, pollution, and species overexploitation. Thus, understanding the underlying and proximate drivers of anthropogenic threats is urgently needed to improve protected areas' effectiveness, especially in the biodiversity-rich tropics. We addressed this issue by analyzing expert-provided data on long-term biodiversity change (last three decades) over 14 biosphere reserves from the Mesoamerican Biodiversity Hotspot. Using multivariate analyses and structural equation modeling, we tested the influence of major socioeconomic drivers (demographic, economic, and political factors), spatial indicators of human activities (agriculture expansion and road extension), and forest landscape modifications (forest loss and isolation) as drivers of biodiversity change. We uncovered a significant proliferation of disturbance-tolerant guilds and the loss or decline of disturbance-sensitive guilds within reserves causing a "winner and loser" species replacement over time. Guild change was directly related to forest spatial changes promoted by the expansion of agriculture and roads within reserves. High human population density and low nonfarming occupation were identified as the main underlying drivers of biodiversity change. Our findings suggest that to mitigate anthropogenic threats to biodiversity within biosphere reserves, fostering human population well-being via sustainable, nonfarming livelihood opportunities around reserves is imperative.

Leaf morphometric analysis and potential distribution modelling contribute to taxonomic differentiation in the Quercus microphylla complex.

Mexico is a major center of evolutionary radiation for the genus Quercus, with oak species occurring across different habitat types and showing a wide variation in morphology and growth form. Despite representing about 20% of Mexican species, scrub oaks have received little attention and even basic aspects of their taxonomy and geographic distribution remain unresolved. In this study, we analyzed the morphological and climatic niche differentiation of scrub oak populations forming a complex constituted by six named species, Quercus cordifolia, Quercus frutex, Quercus intricata, Quercus microphylla, Quercus repanda, Quercus striatula and a distinct morphotype of Q. striatula identified during field and herbarium work (hereafter named Q. striatula II). Samples were obtained from 35 sites covering the geographic distribution of the complex in northern and central Mexico. Morphological differentiation was analyzed through geometric morphometrics of leaf shape and quantification of trichome traits. Our results indicated the presence of two main morphological groups with geographic concordance. The first was formed by Q. frutex, Q. microphylla, Q. repanda and Q. striatula, distributed in the Trans-Mexican Volcanic Belt, the Sierra Madre Occidental and a little portion of the south of the Mexican Altiplano (MA). The second group consists of Q. cordifola, Q. intricata and Q. striatula II, found in the Sierra Madre Oriental and the MA. Therefore, our evidence supports the distinctness of the Q. striatula II morphotype, indicating the need for a taxonomic revision. Within the two groups, morphological differentiation among taxa varied from very clear to low or inexistent (i.e. Q. microphylla-Q. striatula and Q. cordifolia-Q. striatula II) but niche comparisons revealed significant niche differentiation in all pairwise comparisons, highlighting the relevance of integrative approaches for the taxonomic resolution of complicated groups such as the one studied here.

The roles of the ostiole in the fig-fig wasp mutualism from a morpho-anatomical perspective.

The syconium is the urn-shaped inflorescence shared by all species of the genus Ficus. The orifice at the apex of the syconium is called the ostiole, and it is covered by interlocking bracts. The ostiolar bracts can have different arrangements, which only allow the entry of mutualist wasps and promote reproductive isolation among Ficus species. Here, we analyze the ostiolar structures that could play a role as selective filter and therefore impact the fig-fig wasp mutualism in the neotropical Ficus sections Americanae and Pharmacosycea. Samples of syconia with pistillate flowers during the receptive phase of seven species of Ficus were examined using light and scanning electron microscopy. Tests for histolocalization of substances were employed to detect secretory activity throughout the ostiolar tissues. Our results indicated that the ostiole has two components: ostiolar bracts and the periostiolar zone. Interspecies variation in ostiolar bract arrangement in both sections studied was broader than previously reported. We report for the first time for Ficus: (i) two types of ostiolar osmophores (mesophyll and diffuse), that could be a source of volatile compounds for attracting fig wasps; (ii) colleters in the axil of ostiolar bracts, which probably lubricate and facilitate the entry of pollinating wasps into the syconial cavity; (iii) secretory trichomes around the ostiolar bracts, and (iv) syconium basal bracts (F. isophlebia) covering the ostiole, which are the first physical barrier that the fig wasps must overcome to access receptive pistillate flowers. We describe the zones that compose the ostiole, which support the hypothesis that the ostiole is a selective filter in the interactions of fig trees with Agaonidae fig wasps. We also suggest that ostiolar osmophores, colleters, the periostiolar zone, and the arrangements of the ostiolar bracts may be informative with respect to Ficus systematics.

Biogeographic regionalization by spatial and environmental components: Numerical proposal.

Regionalization through the analysis of species groups offers important advantages in conservation biology, compared to the single taxon approach in areas of high species richness. We use a systematic framework for biogeographic regionalization at a regional scale based on species turnover and environmental drivers (climate variables and soil properties) mainly of herbaceous plant species richness. To identify phytogeographic regions in the Balsas Depression (BD), we use Asteraceae species, a family widely distributed in Seasonally Dry Tropical Forest (SDTF) and the most diverse of the vascular plants in Mexico. Occurrence records of 571 species were used to apply a quantitative analysis based on the species turnover, the rate of changes in their composition between sites (ß-Simpson index) and the analysis of the identified environmental drivers. Also, the environmental predictors that influence species richness in the SDTF were determined with a redundancy analysis. We identified and named two phytogeographic districts within the SDTF of the BD (Upper Balsas and Lower Balsas). According to the multi-response permutation procedure, floristic composition of the two districts differs significantly, and the richness of exclusive species in Upper Balsas was higher (292 species) than in the Lower Balsas (32 species). The proportion of Mg and Ca in the soil and the precipitation of the driest three-month period were the environmental factors with greatest positive influence on species richness. The division of geographic districts subordinated to the province level, based on diverse families such as Asteraceae, proved to be appropriate to set up strategies for the conservation of the regional flora, since at this scale, variation in species richness is more evident. Our findings are consistent with a growing body of biogeographic literature that indicates that the identification of smaller biotic districts is more efficient for the conservation of biodiversity, particularly of endemic or rare plants, whose distribution responds more to microhabitats variation.

Timber and non-timber forest products in the northernmost Neotropical rainforest: Ecological factors unravel their landscape distribution.

The benefits provided by tropical rainforests are unevenly distributed throughout the landscape and are shaped by abiotic and biotic components that influence the spatial distribution and functional traits of the species involved. We tested whether environmental stratification of the rainforest in biophysical Landscape Units (LU), defined by topography and soil, is related to the spatial distribution of diversity, abundance and productivity (standing biomass) of tree assemblages that provide potential forest products (PFP). Considering that different PFP are associated with specific plant traits, we also tested whether a phylogenetic signal exists among the species that comprise specific use categories. Non-metric multidimensional scaling ordinations and permutational analysis of variance were based on the frequency, abundance and productivity of 129 species, the PFP of which were classified as fodder, food, fuelwood, medicinal, melliferous, ornamental, plywood and timber in 15 plots of 0.5 ha each. We constructed a phylogenetic tree of the studied species and analyzed the phylogenetic signal strength (D-statistic) among them. The spatial distribution of diversity and abundance of useful species changes among the LU. Specific PFP can be provided in contrasting habitat conditions, but generally not by the same species. The PFP categories that presented a phylogenetic signal were associated with wood characteristics (fuelwood and plywood) and the palatability of the leaves and reproductive structures (fodder). The Moraceae family was significantly related to fodder and plywood, whereas Meliaceae, Myrtaceae and Sapotaceae were mostly used for fuelwood. The medicinal species presented convergent traits distributed throughout the phylogeny. However, since our study included a broad variety of plant structures, it is possible that phylogenetic dispersion can change if we consider the specific uses within each category. Our findings show that the assemblages of PFP suppliers can be clustered through biophysical units based on soil and topography, and specific categories of PFP are often supplied by phylogenetically related species. This knowledge is fundamental in order to incorporate the high diversity of tree species and their potential uses into productive reforestation and agroforestry programs.

Disentangling the influence of ecological and historical factors on seed germination and seedling types in a Neotropical dry forest.

In tropical dry forests, although seed germination and seedling establishment are in general limited by the seasonal availability of water, high interspecific variability, nonetheless, exists in terms of seedling traits and germination dynamics. Differences among species in seed germination and seedling traits may be related to other plant life-history traits, such that assessing these relationships may increase our understanding of factors influencing plant establishment, which would affect the regeneration pathways of tropical dry forest communities. In this study, taking into consideration the effect species' phylogeny, we evaluated the relationships of seed germination metrics (percentage, lag time, and rate of germination) and seedling types (i.e. cotyledons functional morphology), with plant life-history traits (growth form, seed mass, dispersal syndrome and dispersal phenology) for 110 species in a Neotropical dry forest in Mexico. A total of 92% of the species studied disperse their seeds during the dry season, mainly at the beginning of this season (66%), a strategy mostly associated with autochorous herbs. Seed germination was more frequent in species that dispersed seeds at the end of the dry season. Germination percentage was not related to any of the traits studied. However, germination lag time and rate were negatively related to seed mass, a trait that in turn depended on growth form and dispersal syndrome. The dominant seedling type in the community was phanerocotylar epigeal with foliaceous cotyledons (56%), which was mostly associated with small seed mass and herbaceous growth form. Our results provide evidence that several plant life-history traits explain an important part of the variation in seed germination and seedling characteristics observed among species. Therefore, these plant life-history traits may be useful for grouping species in terms of their establishment strategies and roles on the regeneration of tropical dry communities.

Phylogeny, fruit traits, and ecological correlates of fruiting phenology in a Neotropical dry forest.

In tropical dry forests, a high interspecific variation in the strategies of fruiting phenology has been documented. Therefore, phenological responses may be mediated by influence of environmental variables, functional plant attributes or phylogenetic inertia. During 2 years, we recorded the fruiting phenology of 151 species belonging to 5 different growth forms of a Neotropical dry forest in Mexico. We evaluated the relationships between fruiting phenology, abiotic factors (precipitation, temperature, day-length) and functional attributes (growth form, dispersal syndrome, size and time for fruit development) using phylogenetic least squares models (PGLS). More species had ripe fruits during the dry season (92%) than during rainy months and dispersed their seeds by autochory and endozoochory. We found that fruit development time was positively correlated with fruit size and together the morphological fruit traits (size and dispersal syndrome) showed an important relationship with the growth form, but with a strong phylogenetic signal. Environmental seasonality had a strong influence on fruit ripening time, without a relevant association to the phylogeny of plant species. However, the phenological response to the environment (rainfall and day-length) at the community level was mediated by growth form. In woody species, we documented a high interspecific fruiting variation linked with the different dispersal syndromes. In herbaceous species, fruiting phenology is a trait restricted by the duration of their life cycle by rainfall seasonality, which in turn might have selected some traits (e.g., dry fruit, presence of spines, explosive dehiscence) for maximizing seed dispersal during the dry season.

Flowering phenology, growth forms, and pollination syndromes in tropical dry forest species: Influence of phylogeny and abiotic factors.

PREMISE OF THE STUDY: Analyses of the influence of temporal variation in abiotic factors on flowering phenology of tropical dry forest species have not considered the possible response of species with different growth forms and pollination syndromes, while controlling for phylogenetic relationships among species. Here, we investigated the relationship between flowering phenology, abiotic factors, and plant functional attributes, while controlling for phylogenetic relationship among species, in a dry forest community in Mexico. METHODS: We characterized flowering phenology (time and duration) and pollination syndromes of 55 tree species, 49 herbs, 24 shrubs, 15 lianas, and 11 vines. We tested the influence of pollination syndrome, growth form, and abiotic factors on flowering phenology using phylogenetic generalized least squares. KEY RESULTS: We found a relationship between flowering duration and time. Growth form was related to flowering time, and the pollination syndrome had a more significant relationship with flowering duration. Flowering time variation in the community was explained mainly by abiotic variables, without an important phylogenetic effect. Flowering time in lianas and trees was negatively and positively correlated with daylength, respectively. CONCLUSIONS: Functional attributes, environmental cues, and phylogeny interact with each other to shape the diversity of flowering patterns. Phenological differentiation among species groups revealed multiples strategies associated with growth form and pollination syndromes that can be important for understanding species coexistence in this highly diverse plant community.

Conserving tropical tree diversity and forest structure: the value of small rainforest patches in moderately-managed landscapes.

Rainforests are undergoing severe deforestation and fragmentation worldwide. A huge amount of small forest patches are being created, but their value in conserving biodiversity and forest structure is still controversial. Here, we demonstrate that in a species-rich and moderately-managed Mexican tropical landscape small rainforest patches (<100 ha) can be highly valuable for the conservation of tree diversity and forest structure. These patches showed diverse communities of native plants, including endangered species, and a new record for the country. Although the number of logged trees increased in smaller patches, patch size was a poor indicator of basal area, stem density, number of species, genera and families, and community evenness. Cumulative species-area curves indicated that all patches had a similar contribution to the regional species diversity. This idea also was supported by the fact that patches strongly differed in floristic composition (high ß-diversity), independently of patch size. Thus, in agreement with the land-sharing approach, our findings support that small forest patches in moderately-managed landscapes should be included in conservation initiatives to maintain landscape heterogeneity, species diversity, and ecosystem services.

Contagious deposition of seeds in spider monkeys' sleeping trees limits effective seed dispersal in fragmented landscapes.

The repeated use of sleeping sites by frugivorous vertebrates promotes the deposition and aggregation of copious amounts of seeds in these sites. This spatially contagious pattern of seed deposition has key implications for seed dispersal, particularly because such patterns can persist through recruitment. Assessing the seed rain patterns in sleeping sites thus represents a fundamental step in understanding the spatial structure and regeneration of plant assemblages. We evaluated the seed rain produced by spider monkeys (Ateles geoffroyi) in latrines located beneath 60 sleeping trees in two continuous forest sites (CFS) and three forest fragments (FF) in the Lacandona rainforest, Mexico. We tested for differences among latrines, among sites, and between forest conditions in the abundance, diversity (α-, ß- and, γ-components) and evenness of seed assemblages. We recorded 45,919 seeds ≥ 5 mm (in length) from 68 species. The abundance of seeds was 1.7 times higher in FF than in CFS, particularly because of the dominance of a few plant species. As a consequence, community evenness tended to be lower within FF. ß-diversity of common and dominant species was two times greater among FF than between CFS. Although mean α-diversity per latrine did not differ among sites, the greater ß-diversity among latrines in CFS increased γ-diversity in these sites, particularly when considering common and dominant species. Our results support the hypothesis that fruit scarcity in FF can 'force' spider monkeys to deplete the available fruit patches more intensively than in CFS. This feeding strategy can limit the effectiveness of spider monkeys as seed dispersers in FF, because (i) it can limit the number of seed dispersers visiting such fruit patches; (ii) it increases seed dispersal limitation; and (iii) it can contribute to the floristic homogenization (i.e., reduced ß-diversity among latrines) in fragmented landscapes.

Plant reproductive phenology in a temperate forest of the monarch butterfly biosphere reserve Mexico

Para documentar la fenología reproductiva de las especies más importantes (11 hierbas anuales, 72 hierbas perennes, 21 arbustos y 8 árboles) del bosque templado en la zona núcleo Cerro Altamirano, Reserva de la Biosfera Mariposa Monarca, México, se realizaron observaciones mensuales durante 2004. La sincronía intraespecífica de floración y fructificación se estimó en ocho especies leñosas por medio de la observación de 20 individuos por especie. La floración y fructificación ocurrió principalmente durante la estación de lluvias e inicios de la estación seca (jul-dic), con baja estacionalidad. Las formas de crecimiento mostraron diferencias temporales en su actividad reproductiva: i) las hierbas anuales y perennes florecieron principalmente durante la estación de lluvias e inicios de la seca, mientras que la mayoría de especies con frutos fue observada en la estación seca; ii) los arbustos presentaron flores y frutos a lo largo del año, sin máximo en alguna época particular, y iii) la mayoría de los árboles concentraron su actividad reproductiva en la época de menor precipitación. El número de especies en floración a nivel comunitario y de hierbas perennes se correlacionó positivamente con la precipitación, y el número de especies arbustivas y arbóreas en fructificación mostró una correlación negativa con la precipitación. Se determinó una alta sincronía reproductiva (>60 por ciento de los individuos en una fase fenológica específica) en cinco de las especies arbóreas. Los patrones fenológicos reproductivos en el área, un bosque templado de elevada altitud en una zona tropical, fueron similares a los documentados para bosques tropicales estacionales de bajas altitudes, y explicados principalmente por la precipitación total anual y la forma de crecimiento de las especies.

Relationships among ecologically important dimensions of plant trait variation in seven neotropical forests.

BACKGROUND AND AIMS: When ecologically important plant traits are correlated they may be said to constitute an ecological 'strategy' dimension. Through identifying these dimensions and understanding their inter-relationships we gain insight into why particular trait combinations are favoured over others and into the implications of trait differences among species. Here we investigated relationships among several traits, and thus the strategy dimensions they represented, across 2134 woody species from seven Neotropical forests. METHODS: Six traits were studied: specific leaf area (SLA), the average size of leaves, seed and fruit, typical maximum plant height, and wood density (WD). Trait relationships were quantified across species at each individual forest as well as across the dataset as a whole. 'Phylogenetic' analyses were used to test for correlations among evolutionary trait-divergences and to ascertain whether interspecific relationships were biased by strong taxonomic patterning in the traits. KEY RESULTS: The interspecific and phylogenetic analyses yielded congruent results. Seed and fruit size were expected, and confirmed, to be tightly related. As expected, plant height was correlated with each of seed and fruit size, albeit weakly. Weak support was found for an expected positive relationship between leaf and fruit size. The prediction that SLA and WD would be negatively correlated was not supported. Otherwise the traits were predicted to be largely unrelated, being representatives of putatively independent strategy dimensions. This was indeed the case, although WD was consistently, negatively related to leaf size. CONCLUSIONS: The dimensions represented by SLA, seed/fruit size and leaf size were essentially independent and thus conveyed largely independent information about plant strategies. To a lesser extent the same was true for plant height and WD. Our tentative explanation for negative WD-leaf size relationships, now also known from other habitats, is that the traits are indirectly linked via plant hydraulics.

Identifying priority areas for conservation in mexican tropical deciduous forest based on tree species

El objetivo principal del trabajo fue identificar y jerarquizar áreas prioritarias para la conservación de los árboles que se distribuyen de manera exclusiva o casi exclusivamente en el bosque tropical caducifolio en México, un tipo de vegetación seriamente amenazado a nivel mundial. La información se obtuvo a través de la consulta de literatura florística especializada, con la que se generó una lista de 425 especies arbóreas (67,5 por ciento endémicas de México), con 56 familias y 185 géneros registrados a nivel de estado. El grado de conservación de las especies se evaluó registrando su presencia en las Áreas Naturales Protegidas de México que incluyen dentro de sus límites porciones con bosque tropical caducifolio. Por análisis de parsimonia se determinaron 16 áreas de endemismo, sustentadas por 54 sinapomorfias y 73 autapomorfias (72,4 por ciento endémicas de México). Las áreas protegidas incluyen una baja a mediana proporción de las especies arbóreas de amplia distribución (129 especies, 30,3 por ciento) y de aquellas que caracterizan las áreas de endemismo (56 de 127 especies, 44,1 por ciento). En este último grupo, solo 7 especies están incluidas en una categoria de riesgo. El análisis de complementaridad (basado en la riqueza de especies y de aquellas localizadas en áreas de endemismo) y de diversidad filogenética (número de familias y géneros encontrados en cada estado) coinciden en asignar como áreas prioritarias para la conservación a los estados de Chiapas, Guerrero, Jalisco, Michoacán, Oaxaca y Yucatán. Con base en los resultados se proponen recomendaciones para el desarrollo de estrategias para asegurar la conservación de los árboles del bosque tropical caducifolio mexicano