Amazon plant diversity revealed by a taxonomically verified species list.

Recent debates on the number of plant species in the vast lowland rain forests of the Amazon have been based largely on model estimates, neglecting published checklists based on verified voucher data. Here we collate taxonomically verified checklists to present a list of seed plant species from lowland Amazon rain forests. Our list comprises 14,003 species, of which 6,727 are trees. These figures are similar to estimates derived from nonparametric ecological models, but they contrast strongly with predictions of much higher tree diversity derived from parametric models. Based on the known proportion of tree species in neotropical lowland rain forest communities as measured in complete plot censuses, and on overall estimates of seed plant diversity in Brazil and in the neotropics in general, it is more likely that tree diversity in the Amazon is closer to the lower estimates derived from nonparametric models. Much remains unknown about Amazonian plant diversity, but this taxonomically verified dataset provides a valid starting point for macroecological and evolutionary studies aimed at understanding the origin, evolution, and ecology of the exceptional biodiversity of Amazonian forests.

Implications of lemuriform extinctions for the Malagasy flora.

Madagascar's lemurs display a diverse array of feeding strategies with complex relationships to seed dispersal mechanisms in Malagasy plants. Although these relationships have been explored previously on a case-by-case basis, we present here the first comprehensive analysis of lemuriform feeding, to our knowledge, and its hypothesized effects on seed dispersal and the long-term survival of Malagasy plant lineages. We used a molecular phylogenetic framework to examine the mode and tempo of diet evolution, and to quantify the associated morphological space occupied by Madagascar's lemurs, both extinct and extant. Using statistical models and morphometric analyses, we demonstrate that the extinction of large-bodied lemurs resulted in a significant reduction in functional morphological space associated with seed dispersal ability. These reductions carry potentially far-reaching consequences for Malagasy ecosystems, and we highlight large-seeded Malagasy plants that appear to be without extant animal dispersers. We also identify living lemurs that are endangered yet occupy unique and essential dispersal niches defined by our morphometric analyses.

Fruit Morphology and Anatomy of the Spondioid Anacardiaceae.

The Spondioideae subfamily of the Anacardiaceae is widely distributed today in tropical regions. Recent molecular phylogenetic investigations indicate that the Spondioideae are not monophyletic, but rather comprise at least two separate clades that are difficult to distinguish using vegetative and floral characters. Nevertheless, the syndrome of fruit characters traditionally used in identifying the subfamily is useful in discriminating genera of these clades and for identification of both modern and fossil anacardiaceous fruits. Here we document the morphology and anatomy of endocarps for representatives of all extant genera traditionally treated as Spondioideae, plus two genera that have been placed close to them in molecular investigations, Buchanania and Campnosperma. All genera are characterized by drupe-like fruits with sclerified stones that vary from uni- to multilocular depending on the genus. Germination modes vary throughout the Spondioideae. Some have characteristic plug-like opercula; others have recessed bilabiate germination valves, and still others open by apical flaps or simple slits. Although most currently recognized genera appear to be monophyletic, fruit morphology indicates that current circumscriptions of Cyrtocarpa, Poupartia and Tapirira are in need of revision.

Topological Phenotypes Constitute a New Dimension in the Phenotypic Space of Leaf Venation Networks.

The leaves of angiosperms contain highly complex venation networks consisting of recursively nested, hierarchically organized loops. We describe a new phenotypic trait of reticulate vascular networks based on the topology of the nested loops. This phenotypic trait encodes information orthogonal to widely used geometric phenotypic traits, and thus constitutes a new dimension in the leaf venation phenotypic space. We apply our metric to a database of 186 leaves and leaflets representing 137 species, predominantly from the Burseraceae family, revealing diverse topological network traits even within this single family. We show that topological information significantly improves identification of leaves from fragments by calculating a "leaf venation fingerprint" from topology and geometry. Further, we present a phenomenological model suggesting that the topological traits can be explained by noise effects unique to specimen during development of each leaf which leave their imprint on the final network. This work opens the path to new quantitative identification techniques for leaves which go beyond simple geometric traits such as vein density and is directly applicable to other planar or sub-planar networks such as blood vessels in the brain.

The biogeographic origin of a radiation of trees in Madagascar: implications for the assembly of a tropical forest biome.

BACKGROUND: Madagascar's rain forests are characterized by extreme and uneven patterns of species richness and endemicity, the biogeographic and evolutionary origins of which are poorly understood. METHODS: Here we use a time-calibrated phylogeny of a dominant group of trees in Madagascar's eastern rain forests, Canarium, and related Burseraceae (Canarieae), to test biogeographic hypotheses regarding the origin and radiation of the flora of this unique biome. RESULTS: Our findings strongly support the monophyly of Malagasy Canarium, suggesting that this clade represents a previously undocumented in situ radiation. Contrary to expectations of dispersal from Africa during the Oligocene, concurrent with the formation of Madagascar's rain forest biome, our analyses support a late Miocene origin for Malagasy Canarium, probably by long distance dispersal from Southeast Asia. DISCUSSION: Our study illustrates the importance of considering long distance dispersal as a viable explanation for clades with pantropical distributions diversifying subsequent to the Oligocene, and it highlights the formation of the Indo-Australian Archipelago and associated fast-moving equatorial surface currents, suggesting an under-appreciated evolutionary link among tropical centers of endemism. CONCLUSIONS: We postulate that the relatively recent establishment and radiation of Canarium in Madagascar may have been facilitated by the highly stochastic climates associated with these forest ecosystems.

Revisiting the hyperdominance of Neotropical tree species under a taxonomic, functional and evolutionary perspective.

Recent studies have leveraged large datasets from plot-inventory networks to report a phenomenon of hyperdominance in Amazonian tree communities, concluding that few species are common and many are rare. However, taxonomic hypotheses may not be consistent across these large plot networks, potentially masking cryptic diversity and threatened rare taxa. In the current study, we have reviewed one of the most abundant putatively hyperdominant taxa, Protium heptaphyllum (Aubl.) Marchand (Burseraceae), long considered to be a taxonomically difficult species complex. Using morphological, genomic, and functional data, we present evidence that P. heptaphyllum sensu lato may represent eight separately evolving lineages, each warranting species status. Most of these lineages are geographically restricted, and few if any of them could be considered hyperdominant on their own. In addition, functional trait data are consistent with the hypothesis that trees from each lineage are adapted to distinct soil and climate conditions. Moreover, some of the newly discovered species are rare, with habitats currently experiencing rapid deforestation. We highlight an urgent need to improve sampling and methods for species discovery in order to avoid oversimplified assumptions regarding diversity and rarity in the tropics and the implications for ecosystem functioning and conservation.

Leaf Transcriptome Assembly of Protium copal (Burseraceae) and Annotation of Terpene Biosynthetic Genes.

Plants in the Burseraceae are globally recognized for producing resins and essential oils with medicinal properties and have economic value. In addition, most of the aromatic and non-aromatic components of Burseraceae resins are derived from a variety of terpene and terpenoid chemicals. Although terpene genes have been identified in model plant crops (e.g., Citrus, Arabidopsis), very few genomic resources are available for non-model groups, including the highly diverse Burseraceae family. Here we report the assembly of a leaf transcriptome of Protium copal, an aromatic tree that has a large distribution in Central America, describe the functional annotation of putative terpene biosynthetic genes and compare terpene biosynthetic genes found in P. copal with those identified in other Burseraceae taxa. The genomic resources of Protium copal can be used to generate novel sequencing markers for population genetics and comparative phylogenetic studies, and to investigate the diversity and evolution of terpene genes in the Burseraceae.

Reconciling species diversity in a tropical plant clade (Canarium, Burseraceae).

The challenges associated with sampling rare species or populations can limit our ability to make accurate and informed estimates of biodiversity for clades or ecosystems. This may be particularly true for tropical trees, which tend to be poorly sampled, and are thought to harbor extensive cryptic diversity. Here, we integrate genomics, morphology, and geography to estimate the number of species in a clade of dioecious tropical trees (Canarium L.; Burseraceae) endemic to Madagascar, for which previous taxonomic treatments have recognized between one and 33 species. By sampling genomic data from even a limited number of individuals per taxon, we were able to clearly reject both previous hypotheses, and support instead an intermediate number of taxa. We recognize at least six distinct clades based on genetic structure and species delimitation analyses that correspond clearly with geographic and discrete morphological differences. Two widespread clades co-occur broadly throughout eastern wet forests, one clade is endemic to western dry forests, and several slightly admixed clades are more narrowly distributed in mountainous regions in the north. Multiple previously described taxa were recovered as paraphyletic in our analyses, some of which were associated with admixed individuals, suggesting that hybridization contributes to taxonomic difficulties in Canarium. An improved understanding of Canarium species diversity has important implications for conservation efforts and understanding the origins of diversity in Madagascar. Our study shows that even limited genomic sampling, when combined with geography and morphology, can greatly improve estimates of species diversity for difficult tropical clades.

The Paucity of Frugivores in Madagascar May Not Be Due to Unpredictable Temperatures or Fruit Resources.

The evolution of ecological idiosyncrasies in Madagascar has often been attributed to selective pressures stemming from extreme unpredictability in climate and resource availability compared to other tropical areas. With the exception of rainfall, few studies have investigated these assumptions. To assess the hypothesis that Madagascar's paucity of frugivores is due to unreliability in fruiting resources, we use statistical modeling to analyze phenology datasets and their environmental correlates from two tropical wet forests, the Réserve Naturelle Intégrale Betampona in Madagascar, and Kibale National Park in Uganda. At each site we found that temperature is a good environmental predictor of fruit availability. We found no evidence of a significant difference in the predictability of fruit availability between the two sites, although the shorter duration of phenological monitoring at Betampona (two years, versus 15 years at Kibale) limits our ability to infer long-term patterns. Comparisons of long-term temperature data from each site (15 years from Kibale and 14 from Betampona) indicate that temperature is more predictable at Betampona than at Kibale. However, there does appear to be a difference between the two sites in the total fruit availability at any given time, with fruit being generally less abundant at Betampona. Our results appear contrary to the prevailing hypothesis of a selective force imposed by unpredictable resource availability or temperature, and we suggest other possible explanations for Madagascar's unique biota.

The contribution of edaphic heterogeneity to the evolution and diversity of Burseraceae trees in the western Amazon.

Environmental heterogeneity in the tropics is thought to lead to specialization in plants and thereby contribute to the diversity of the tropical flora. We examine this idea with data on the habitat specificity of 35 western Amazonian species from the genera Protium, Crepidospermum, and Tetragastris in the monophyletic tribe Protieae (Burseraceae) mapped on a molecular-based phylogeny. We surveyed three edaphic habitats that occur throughout terra firme Amazonia: white-sand, clay, and terrace soils in eight forests across more than 2000 km in the western Amazon. Twenty-six of the 35 species were found to be associated with only one of three soil types, and no species was associated with all three habitats; this pattern of edaphic specialization was consistent across the entire region. Habitat association mapped onto the phylogenetic tree shows association with terrace soils to be the probable ancestral state in the group, with subsequent speciation events onto clay and white-sand soils. The repeated gain of clay association within the clade likely coincides with the emergence of large areas of clay soils in the Miocene deposited during the Andean uplift. Character optimizations revealed that soil association was not phylogenetically clustered for white-sand and clay specialists, suggesting repeated independent evolution of soil specificity is common within the Protieae. This phylogenetic analysis also showed that multiple cases of putative sister taxa with parapatric distributions differ in their edaphic associations, suggesting that edaphic heterogeneity was an important driver of speciation in the Protieae in the Amazon basin.

A revision of Spondias L. (Anacardiaceae) in the Neotropics.

As part of an ongoing study of Anacardiaceae subfamily Spondioideae, the ten native and one introduced species of Spondias in the Neotropics are revised. The genus is circumscribed. Three new species, Spondiasadmirabilis, Spondiasexpeditionaria, and Spondiasglobosa, are described and illustrated; a key to the taxa found in the Neotropics and distribution maps are provided. The Paleotropical species and allied genera are reviewed. Diagnostic character sets include leaf architecture, habit, flower morphology, and gross fruit morphology. Notes on the ecology and economic botany of the species are provided.

Preparation of samples for leaf architecture studies, a method for mounting cleared leaves.

PREMISE OF THE STUDY: Several recent waves of interest in leaf architecture have shown an expanding range of approaches and applications across a number of disciplines. Despite this increased interest, examination of existing archives of cleared and mounted leaves shows that current methods for mounting, in particular, yield unsatisfactory results and deterioration of samples over relatively short periods. Although techniques for clearing and staining leaves are numerous, published techniques for mounting leaves are scarce. • METHODS AND RESULTS: Here we present a complete protocol and recommendations for clearing, staining, and imaging leaves, and, most importantly, a method to permanently mount cleared leaves. • CONCLUSIONS: The mounting protocol is faster than other methods, inexpensive, and straightforward; moreover, it yields clear and permanent samples that can easily be imaged, scanned, and stored. Specimens mounted with this method preserve well, with leaves that were mounted more than 35 years ago showing no signs of bubbling or discoloration.

Investigating processes of neotropical rain forest tree diversification by examining the evolution and historical biogeography of the Protieae (Burseraceae).

Andean uplift and the collision of North and South America are thought to have major implications for the diversification of the Neotropical biota. However, few studies have investigated how these geological events may have influenced diversification. We present a multilocus phylogeny of 102 Protieae taxa (73% of published species), sampled pantropically, to test hypotheses about the relative importance of dispersal, vicariance, habitat specialization, and biotic factors in the diversification of this ecologically dominant tribe of Neotropical trees. Bayesian fossil-calibrated analyses date the Protieae stem at 55 Mya. Biogeographic analyses reconstruct an initial late Oligocene/early Miocene radiation in Amazonia for Neotropical Protieae, with several subsequent late Miocene dispersal events to Central America, the Caribbean, Brazil's Atlantic Forest, and the Chocó. Regional phylogenetic structure results indicate frequent dispersal among regions throughout the Miocene and many instances of more recent regional in situ speciation. Habitat specialization to white sand or flooded soils was common, especially in Amazonia. There was one significant increase in diversification rate coincident with colonization of the Neotropics, followed by a gradual decrease consistent with models of diversity-dependent cladogenesis. Dispersal, biotic interactions, and habitat specialization are thus hypothesized to be the most important processes underlying the diversification of the Protieae.

To move or to evolve: contrasting patterns of intercontinental connectivity and climatic niche evolution in "Terebinthaceae" (Anacardiaceae and Burseraceae).

Many angiosperm families are distributed pantropically, yet for any given continent little is known about which lineages are ancient residents or recent arrivals. Here we use a comprehensive sampling of the pantropical sister pair Anacardiaceae and Burseraceae to assess the relative importance of continental vicariance, long-distance dispersal and niche-conservatism in generating its distinctive pattern of diversity over time. Each family has approximately the same number of species and identical stem age, yet Anacardiaceae display a broader range of fruit morphologies and dispersal strategies and include species that can withstand freezing temperatures, whereas Burseraceae do not. We found that nuclear and chloroplast data yielded a highly supported phylogenetic reconstruction that supports current taxonomic concepts and time-calibrated biogeographic reconstructions that are broadly congruent with the fossil record. We conclude that the most recent common ancestor of these families was widespread and likely distributed in the Northern Hemisphere during the Cretaceous and that vicariance between Eastern and Western Hemispheres coincided with the initial divergence of the families. The tempo of diversification of the families is strikingly different. Anacardiaceae steadily accumulated lineages starting in the Late Cretaceous-Paleocene while the majority of Burseraceae diversification occurred in the Miocene. Multiple dispersal- and vicariance-based intercontinental colonization events are inferred for both families throughout the past 100 million years. However, Anacardiaceae have shifted climatic niches frequently during this time, while Burseraceae have experienced very few shifts between dry and wet climates and only in the tropics. Thus, we conclude that both Anacardiaceae and Burseraceae move easily but that Anacardiaceae have adapted more often, either due to more varied selective pressures or greater intrinsic lability.

Bamboo-dominated forests of the southwest Amazon: detection, spatial extent, life cycle length and flowering waves.

We map the extent, infer the life-cycle length and describe spatial and temporal patterns of flowering of sarmentose bamboos (Guadua spp) in upland forests of the southwest Amazon. We first examine the spectra and the spectral separation of forests with different bamboo life stages. False-color composites from orbital sensors going back to 1975 are capable of distinguishing life stages. These woody bamboos flower produce massive quantities of seeds and then die. Life stage is synchronized, forming a single cohort within each population. Bamboo dominates at least 161,500 km(2) of forest, coincident with an area of recent or ongoing tectonic uplift, rapid mechanical erosion and poorly drained soils rich in exchangeable cations. Each bamboo population is confined to a single spatially continuous patch or to a core patch with small outliers. Using spatial congruence between pairs of mature-stage maps from different years, we estimate an average life cycle of 27-28 y. It is now possible to predict exactly where and approximately when new bamboo mortality events will occur. We also map 74 bamboo populations that flowered between 2001 and 2008 over the entire domain of bamboo-dominated forest. Population size averaged 330 km(2). Flowering events of these populations are temporally and/or spatially separated, restricting or preventing gene exchange. Nonetheless, adjacent populations flower closer in time than expected by chance, forming flowering waves. This may be a consequence of allochronic divergence from fewer ancestral populations and suggests a long history of widespread bamboo in the southwest Amazon.

A pilot study associating urinary concentrations of phthalate metabolites and semen quality.

Phthalates are ubiquitous industrial chemicals that are reported to adversely affect human reproductive outcomes. Divergent effects on semen quality have been reported in a limited number of studies. To assess the possible contribution of regional differences in phthalate exposure to these results, we wished to determine if ambient phthalate exposure of men from the Great Lakes region was associated with human sperm parameters. Male partners (N=45) of subfertile couples presenting to a Michigan infertility clinic were recruited. Urinary concentrations of several phthalate metabolites were measured in these men. Semen parameters, measured according to the World Health Organization [WHO 1999] protocols, were divided into those at or above WHO cutoffs for motility (50% motile), concentration (20 million/mL) and morphology (4% normal) and those below. Phthalate metabolite concentrations were divided into those concentrations above the median and those at or below the median. Specific gravity was used as a covariate in the regression models to adjust for urine dilution. Low sperm concentration was significantly associated with above median concentrations of monoethyl phthalate (MEP) (OR=6.5, 95% CI: 1.0-43.6) and low morphology with above median concentrations of mono-3-carboxypropyl phthalate (OR=7.6, 95% CI: 1.7-33.3). Increased odds for low concentration and above median concentrations of metabolites of di(2-ethylhexyl) phthalate (DEHP) (OR=5.4, 95% CI: 0.9-30.8) and low morphology and above median concentrations of MEP (OR=3.4, 95% CI: 0.9-13.8) were also found. A significant trend was observed for tertiles of MEP and low sperm concentration (p=0.05). Results suggest that ambient phthalate metabolite concentrations may adversely affect human semen quality.

Ambient manganese exposure is negatively associated with human sperm motility and concentration.

BACKGROUND: Occupational and experimental animal studies indicate that exposure to high levels of manganese impairs male fertility, but the effects of ambient manganese in humans are not known. METHODS: We measured blood levels of manganese and selenium in 200 infertility clinic clients in a cross-sectional study. Correlations between metals and semen variables were determined, adjusting for other risk factors. Outcomes were low motility (<50% motile), low concentration (<20 million/mL), or low morphology (<4% normal). We also investigated dose-response relationships between quartiles of manganese exposure and sperm parameters. RESULTS: High manganese level was associated with increased risk of low sperm motility (odds ratio = 5.4; 95% confidence interval = 1.6-17.6) and low sperm concentration (2.4; 1.2-4.9). We saw a U-shaped dose-response pattern between quartiles of manganese exposure and all 3 sperm parameters. CONCLUSION: Ambient exposure to manganese levels is associated with a reduction in sperm motility and concentration. No adverse effects were seen for high selenium.

The phylogenetic history and biogeography of the frankincense and myrrh family (Burseraceae) based on nuclear and chloroplast sequence data.

Generalized hypotheses for the vicariant, Gondwanan origin of pantropically distributed eudicotyledon families must be refined to accommodate recently revised dates that indicate major continental rifting events predate the evolution of many tricolpate angiosperm clades. Here, we use molecular phylogenies of an eudicotyledon family previously hypothesized to have a Gondwanan origin, the Burseraceae, to test this and other alternative biogeographical hypotheses in light of recalibrated geological events. Phylogenies based on nuclear and chloroplast data were reconstructed for 13 of the 18 genera (50 spp. total) of Burseraceae using parsimony, maximum likelihood, and Bayesian methods. Ages of all lineages were estimated using penalized likelihood and semiparametric rate smoothing [Bioinformatics 2003 (19) 301], which allows the user to calibrate phylogenies based on non-clock-like DNA sequence data with fossil information. Biogeographical hypotheses were tested by comparing ages of species and more inclusive lineages with their extant and most parsimonious ancestral distributions. Our data support a North American Paleocene origin for the Burseraceae followed by dispersal of ancestral lineages to eastern Laurasia and Southern Hemisphere continents.

Measuring scientists’ performance: a view from organismal biologist / Midiendo el desempeño de los científicos: un punto de vista de biólogos organísmicos / Medindo desempeenho dos cientistas: um ponto de vista de biólogos organísmioss

Increasingly, academic evaluations quantify performance in science by giving higher rank to scientists (as well as journals and institutions) who publish more articles and have more citations. In Mexico, for example, a centralized federal agency uses such bibliometric statistics for evaluating the performance of all Mexican scientists. In this article we caution against using this form of evaluation as an almost exclusive tool of measuring and comparing scientists’ performance. We argue that from an economic viewpoint, maximizing the number of journal articles and their citations does not necessarily correspond to the preferences and needs of society. The traditional peer review process is much better suited for that purpose, and we propose "rule-based peer review" for evaluating a large number of scientists.

En la ciencia hay una fuerte tendencia global de cuantificar el desempeño de los científicos (así como a las revistas e instituciones), dando mayor jerarquía a aquellos científicos que publican más artículos y son más citados. En México, por ejemplo, una institución federal centralizada usa tales estadísticas bibliométricas para evaluar el desempeño de todos los científicos del país. En este artículo advertimos sobre los inconvenientes de esta forma de evaluación como una herramienta casi única para medir y comparar el desempeño de los científicos. Argumentamos que, desde un punto de vista económico, la maximización del número de artículos científicos y de la frecuencia de sus citas no necesariamente corresponde a las preferencias y necesidades de la sociedad en general. El proceso tradicional de arbitraje por pares es más adecuado para este propósito, y proponemos el "arbitraje por pares basado en reglas" para evaluar a un número alto de científicos.

Há uma forte tendência global para avaliações acadêmicas que quantifiquem o desempenho nas ciências através de ranquear os cientistas (assim como revistas e instituições) que publicam mais artigos e têm mais citações. No México, por exemplo, um órgão centralizado do governo utiliza tais estatísticas bibliomêtricas para avaliar o desempenho de todos os cientistas mexicanos. No presente artigo, chamamos atenção ao uso desta forma de avaliação como ferramenta quase que exclusiva para medir e comparar o desempenho dos cientistas. Argumentamos de um ponto de vista econômico que maximizar o número de artigos e as suas citações não corresponde necessariamente às preferências e necessidades da sociedade. O processo tradicional de avaliação pelos pares é mais apropriado para esta finalidade, e propomos um sistema baseado em "avaliação pelos pares seguindo regras", que podem avaliar um grande numéro de cientistas.