Insights into the historical construction of species-rich biomes from dated plant phylogenies, neutral ecological theory and phylogenetic community structure

Analytical methods are now available that can date all nodes in a molecular phylogenetic tree with one calibration, and which correct for variable rates of DNA substitution in different lineages. Although these techniques are approximate, they offer a new tool to investigate the historical construction of species-rich biomes. Dated phylogenies of globally distributed plant families often indicate that dispersal, even across oceans, rather than plate tectonics, has generated their wide distributions. By contrast, there are indications that animal lineages have undergone less long distance dispersal. Dating the origin of biome-specific plant groups offers a means of estimating the age of the biomes they characterize. However, rather than a simple emphasis on biome age, we stress the importance of studies that seek to unravel the processes that have led to the accumulation of large numbers of species in some biomes. The synthesis of biological inventory, systematics and evolutionary biology offered by the frameworks of neutral ecological theory and phylogenetic community structure offers a promising route for future work.     

Holocene southward expansion in seasonally dry tropical forests in South America: phylogeography of Ficus bonijesulapensis (Moraceae)

We conducted a phylogeographical and niche modelling study of the tree Ficus bonijesulapensis, endemic to Brazilian seasonally dry tropical forests (SDTFs), in order to evaluate the effects of Quaternary climatic fluctuations on population dynamics. The trnQ–5′rps16 region of plastid DNA was sequenced from 15 populations. Three phylogeographical groups were identified by the median‐joining algorithm network and spatial analysis of molecular variance (SAMOVA) (F_CT = 0.591): a central‐west, a central‐east and a scattered group. The central groups had higher total haplotype and nucleotide diversities than the scattered group. Ecological niche modelling suggested that, since the Last Interglacial (130 kyr bp ), the central and north regions have been relatively stable, whereas the southern region of the species distribution has been less stable. The phylogeographical groups showed concordance with the floristic units described for SDTFs. The low genetic diversity, unimodal mismatch distribution and unfavourable climatic conditions in the southern region suggest a recent southward expansion of the range of the species during the Holocene, supporting the hypothesis of the southward expansion of SDTFs during this period. The central and northern regions of the current distribution of F. bonijesulapensis, which are consistent with arboreal caatinga and rock outcrop floristic units, were potential refugia during Quaternary climatic fluctuations. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 177 , 189–201.     

Beta-diversity in seasonally dry tropical forests (SDTF) in the Caatinga Biogeographic Domain, Brazil, and its implications for conservation

Tropical biomes are species rich, but some biomes such as seasonally dry tropical forests (SDTFs) are still inadequately studied compared to their co-occurring rain forest and savanna. SDTFs occur in areas of high environmental heterogeneity, resulting in high beta (β)-diversity or species turnover, but this has so far only been accessed using a single β-diversity measure, and at a spatial scale that is of limited applicability for reserve planning. The Caatinga Biogeographic Domain in Brazil contains the largest known extent of SDTF which are poorly studied and inadequately reserved. We therefore studied the variation in species richness and species turnover among SDTF between localities and between known floristic communities. From six localities within the Caatinga Biogeographic Domain we recorded all tree species with a circumference at breast height equaling or exceeding 10 cm within 106 400 m² survey plots. From the species presence/absence data we calculated three measures of β-diversity between pairs of study localities and between different floristic communities representing: (i) species similarity, (ii) differences between species richness, and (iii) species gain and loss. Our results confirm the high β-diversity of SDTFs and species turnover between localities and also between floristic communities. The three indices were also complementary to each other and can be used to maximize accuracy in β-diversity studies. The implications of our study for conservation and reserve planning of SDTFs are discussed.     

Dynamics of viable nitrifier community, N-mineralization and nitrification in seasonally dry tropical forests and savanna

The study was conducted in Vindhyan region, to assess the N-mineralization, nitrification and size of viable community of ammonium- and nitrite-oxidizing bacteria as affected by different sites and seasons. Six different ecosystems (four forests and two savannas), which differ in terms of topography, vegetation and moisture status, were selected for the present study. The soils of the study sites differ significantly in its physico-chemical properties. The savanna site had significantly higher pH (7.2), bulk density (1.37 g cm(-3)) and silt content (67.80%) but lower water holding capacity (1.37%), total-C (16,356 microg g(-1) dry soil), N (1090 microg g(-1) dry soil) and P (213 microg g(-1) dry soil) than forest sites. The soil moisture content, N-mineralization, nitrification rates and numbers of ammonium- and nitrite-oxidizing bacteria were highest in the wet season and lowest in dry season, while the size of mineral-N (NH4(+)-N and NO3(-)-N) showed a reverse trend at the sites. The N-mineralization, nitrification and nitrifier population size differ significantly across the site and season. The numbers of free-living cells of ammonium- and nitrite-oxidizing bacteria were significantly related to each other and to N-mineralization, nitrification, soil moisture and mineral-N components. The N-mineralization, nitrification and the viable number of nitrifying cells were consistently higher for forest soils compared to savanna sites. It was concluded that soil microbial process (N-mineralization and nitrification) and nitrifier population size were dependent on site topography, vegetation cover and soil moisture status.     

Phylogeography of palo santo trees (Bursera graveolens and Bursera malacophylla; Burseraceae) in the Galápagos archipelago

Two species of palo santo trees are distributed in the Galápagos archipelago, the native Bursera graveolens and the endemic Bursera malacophylla (Burseraceae). However, a zone of individuals morphologically intermediate between the two exists on northern Santa Cruz Island and south‐eastern Santiago Island, suggesting that they may not be reproductively isolated. Here we review the species' distributional and morphological differences and test for evidence of hybridization between the two species using DNA sequence and AFLP data. We find that the species lack distinguishing synapomorphies across the five nuclear and plastid regions examined. Population assignment tests and population genetic analyses of AFLP data indicate that genetically similar palo santo individuals (N = 87), including putative hybrids, partition into two genealogical groups that do not uniformly correspond to island‐ or taxon‐based membership. Furthermore, genotypic admixture levels among morphologically intermediate individuals do not indicate widespread hybridization. Thus, we recommend recognizing the endemic palo santo taxon as B. graveolens subspecies malacophylla (B.L.Rob.) A. Weeks & Tye comb. & stat. nov. in light of its close genetic relationship to B. graveolens subsp. graveolens and its distinctive morphology and distribution. Future research should quantify phenotypic variation in palo santo populations as another means for understanding the basis of morphological differences between the subspecies. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 161 , 396–410.     

Historical biogeographical patterns of the species of Bursera (Burseraceae) and their taxonomic implications

Aim The plant genus Bursera, with 104 species of trees and shrubs, has been used as a model for biogeographical analyses because of its high species richness and large number of endemic species. The biogeographical patterns of Bursera and their implications for its phylogenetic classification are reviewed in order that some hypotheses on the historical biogeography of tropical Mexico can be proposed. Location Bursera is found in the south‐western USA, most of Mexico, mainly below 1700 m elevation in tropical forests, with some species in xeric shrublands, diversifying along the Pacific slope, Central America, and north‐western South America. A few species occur on the Galapagos and Revillagigedo archipelagos, some of which are endemics, whereas in the Antilles species are distributed extensively, with several endemics in the Bahamas, Cuba, Jamaica, and Hispaniola. Methods Data from specimens in herbaria and the literature were used to construct a matrix of 104 species in 160 areas. Distributional patterns of the species of Bursera were inferred applying track analysis, parsimony analysis of endemicity (PAE), and Brooks parsimony analysis (BPA). Results Track analysis revealed four individual tracks: (1) a circum‐Caribbean track, comprising species of the Bursera simaruba species group; (2) an Antillean track, including species that have been transferred to Commiphora based on their pollen traits; (3) a Mexican Pacific track, including species of the B. fragilis, B. microphylla, and B. fagaroides species groups, called ‘cuajiotes’; and (4) a Neotropical Pacific track, including the two species groups assigned to section Bullockia, in which the individual track of the Bursera copallifera species group is nested within the track of the B. glabrifolia species group. The four tracks overlap in a node in the Mexican Pacific slope, where they are highly diversified. PAE allowed us to identify 22 areas of endemism: 12 in Mexico (11 along the Mexican Pacific slope), six in the Antilles, two in Central America, one in South America, and one in the Galapagos. The general area cladogram obtained by BPA has two main clades: one includes the greater Antilles; and the other, 12 Mexican areas of endemism. Main conclusions Bursera fragilis, B. microphylla, and B. fagaroides species groups can be treated together as a new section within Bursera, sect. Quaxiotea, because they are segregated from the other groups of sect. Bursera based on morphological, anatomical, molecular and geographical evidence.     

The relationship of terpene composition,morphology, and distribution of populations of Bursera microphylla (Burseraceae)

On the basis of terpene composition, populations ofB. microphylla show north to south affinities on both the Baja California peninsula and the northwest coast of Mexico. The lack of east to west population affinities corresponds with the presumed absence of land connections between the peninsula and mainland throughout the history of this taxon. Morphological similarities between populations in an east-west direction are explained on the basis of contemporary parallel selective influences and not by the closeness of relationship.     

Age and historical biogeography of the pantropically distributed Spathelioideae (Rutaceae,Sapindales)

Aim The family Rutaceae (rue family) is the largest within the eudicot order Sapindales and is distributed mainly in the tropical and subtropical regions of both the New World and the Old World, with a few genera in temperate zones. The main objective of this study is to present molecular dating and biogeographical analyses of the subfamily Spathelioideae, the earliest branching clade (which includes eight extant genera), to interpret the temporal and spatial origins of this group, ascertaining possible vicariant patterns and dispersal routes and inferring diversification rates through time. Location Pantropics. Methods A dataset comprising a complete taxon sampling at generic level (83.3% at species level) of Spathelioideae was used for a Bayesian molecular dating analysis (beast ). Four fossil calibration points and an age constraint for Sapindales were applied. An ancestral area reconstruction analysis utilizing the dispersal–extinction–cladogenesis model and diversification rate analyses was conducted. Results Dating analyses indicate that Rutaceae and Spathelioideae are probably of Late Cretaceous origin, after which Spathelioideae split into a Neotropical and a Palaeotropical lineage. The Palaeotropical taxa have their origin inferred in Africa, with postulated dispersal events to the Mediterranean, the Canary Islands, Madagascar and Southeast Asia. The lineages within Spathelioideae evolved at a relatively constant diversification rate. However, abrupt changes in diversification rates are inferred from the beginning of the Miocene and during the Pliocene/Pleistocene. Main conclusions The geographical origin of Spathelioideae probably lies in Africa. The existence of a Neotropical lineage may be the result of a dispersal event at a time in the Late Cretaceous when South America and Africa were still quite close to each other (assuming that our age estimates are close to the actual ages), or by Gondwanan vicariance (assuming that our age estimates provide minimal ages only). Separation of land masses caused by sea level changes during the Pliocene and Pleistocene may have been triggers for speciation in the Caribbean genus Spathelia.     

Estimation of gene flow into fragmented populations of Bursera simaruba (Burseraceae) in the dry-forest life zone of Puerto Rico

We examined the impact of habitat fragmentation on gene flow in populations of the neotropical tree Bursera simaruba. In particular, we compared the effectiveness of three common techniques to estimate gene flow in the context of a highly disturbed system. Paternity analysis on emerging seedlings from eight small (N = 3 to 9) stands of trees showed that between 45% and 100% of seedlings were sired from outside their stand, indicating pollen moved readily over the isolation distances examined. Based on six populations of 21-24 trees each, estimates of allozyme genetic diversity (P(s) = 73.3%; H(e) = 0.244) were higher than those reported for species with similar life history traits. Indirect, F(ST)-based gene flow estimates for these six populations yielded an estimate of 3.57 migrants per generation, although possible violations of model assumptions limit the reliability of the estimate. A twogener analysis showed pollen moved either 320 m or 361 m and that there were only 2.46 effective pollen donors per maternal tree. Despite the potential for long-distance pollen movement, seed abortion was high, especially in stands with fewer than four trees. Population size, rather than isolation distance, appears to limit reproduction in the populations examined.     

Identity and relationships of the Arboreal Caatinga among other floristic units of seasonally dry tropical forests (SDTFs) of north-eastern and Central Brazil

The tree species composition of seasonally dry tropical forests (SDTF) in north-eastern and central Brazil is analyzed to address the following hypotheses: (1) variations in species composition are related to both environment (climate and substrate) and spatial proximity; (2) SDTF floristic units may be recognized based on peculiar composition and environment; and (3) the Arboreal Caatinga, a deciduous forest occurring along the hinterland borders of the Caatinga Domain, is one of these units and its flora is more strongly related to the caatinga vegetation than to outlying forests. The study region is framed by the Brazilian coastline, 50th meridian west and 21st parallel south, including the Caatinga Domain and extensions into the Atlantic Forest and Cerrado Domains. Multivariate and geostatistic analyses were performed on a database containing 16,226 occurrence records of 1332 tree species in 187 georeferenced SDTF areas and respective environmental variables. Tree species composition varied significantly with both environmental variables and spatial proximity. Eight SDTF floristic units were recognized in the region, including the Arboreal Caatinga. In terms of species composition, its tree flora showed a stronger link with that of the Cerrado Dry Forest Enclaves. On the other hand, in terms of species frequency across sample areas, the links were stronger with two other units: Rock Outcrops Caatinga and Agreste and Brejo Dry Forests. There is a role for niche-based control of tree species composition across the SDTFs of the region determined primarily by the availability of ground water across time and secondarily by the amount of soil mineral nutrients. Spatial proximity also contributes significantly to the floristic cohesion of SDTF units suggesting a highly dispersal-limited tree flora. These units should be given the status of eco-regions to help driving the conservation policy regarding the protection of their biodiversity.     

Survival and growth of dominant tree seedlings in seasonally tropical dry forests of Yucatan: site and fertilization effects

Aims Seasonally tropical dry forests of the Yucatan Peninsula are typically found in sites with nutrient-poor soils because of the recent geological origin of the region. The landscape is dominated by extensive karstic plates that shape environments where vegetation regeneration through seed germination may be limited by the availability of suitable microsites. In this study, we documented the survival and growth of seedlings from three dominant tree species (Bursera simaruba, Piscidia piscipula and Lysiloma latisiliquum) in seasonally tropical dry forests in Yucatan. Specifically, we evaluated the effect of nutrient addition (N and P, separately and in combination) on seedling survival and growth across three sites with differing levels of precipitation.Methods We conducted a nutrient addition experiment, whereby we established 12 plots of dimensions 10×10 m (100 m 2) at each site, from which three plots were randomly selected to receive one of four treatments: N addition, P addition, N and P addition and no nutrient addition (controls). Prior to treatment application, in each plot, we planted 10 seedlings of each species in October 2010 and subsequently conducted surveys of plant growth and survival every 20 days from November 2010 to April 2011.Important findings Overall, nutrient addition increased seedling survival and the magnitude of this effect was similar among sites. We did not observe an additive effect of the N + P treatment on survival. Similarly, we observed a positive effect of nutrient addition on seedling growth, but this effect was contingent upon site; regarding survival, the effects of N and P on seedling growth were not additive. These results suggest that seedling recruitment and growth in the three dominant species of trees in Yucatan are limited by nutrient availability but that the magnitude of this effect, particularly on seedling growth, is specific for species and site.     

Evolution of Mexican Bursera (Burseraceae) inferred from ITS,ETS, and 5S nuclear ribosomal DNA sequences

I reconstructed a phylogeny of 66 species and varieties of Bursera and 9 outgroup species using sequences of the internal transcribed spacer region (ITS), the 5S non-transcribed region (5S-NTS), and the external transcribed region (ETS) of nuclear ribosomal DNA. This study extends a previously proposed parsimony-based phylogenetic study that used the ITS sequences of 57 Bursera species and five outgroups. Parsimony and maximum likelihood methods were used to infer the phylogeny in this new study. Analyses of the combined data sets largely confirmed the phylogenetic relationships proposed by the previous molecular study but generated a considerably more robust topology. The new phylogenies corroborate the monophyly of the genus, and its division into the two monophyletic subgenera or sections, Bursera and Bullockia. The current analyses also identify four main groups of species in section Bursera, and two in section Bullockia, confirming some of the previously proposed groups based on fruit, flower, and leaf morphology. One previously problematic species B. sarcopoda, which has sometimes been placed in Commiphora, is shown to belong in Bursera. Another controversial species, Commiphora leptophloeos, which was thought to belong to Bursera, falls within Commiphora.     

Frugivory and Seed Fate in Bursera inversa (Burseraceae) at Tinigua Park,Colombia: Implications for Primate Conservation1

The large ateline primates are efficient seed dispersers in Neotropical forests and hunting is driving their populations to extinction, but we do not know whether other frugivores could substitute primates in their ecological role as seed dispersers. In this study we test this possibility using a potential keystone species (Bursera inversa) at Tinigua Park, Colombia. This plant species allows us to compare seed removal rates between emergent, isolated trees, without primate visitors and trees with connected crowns. We used traps to estimate fruit production and seed removal rates in six different trees, and fruiting trees were observed during 2 yr to quantify the number of seeds manipulated by different animal species. We carried out seed predation experiments to test if seed removal by predators was affected by distance or density effects. We found that the most productive trees attracted more visiting species and seed removal rates differed among trees, the lowest corresponding to trees without primate access. Seed removal rates from the ground by predators were not higher below parental trees than away from them, but the distribution of saplings in the forest suggests that seed dispersal is advantageous. Although it is likely that the effect of primate extinctions will vary depending on tree species traits, conserving the populations of primate seed dispersers is critical to maintain the ecological processes in this forest.     

Origin, diversification, and historical biogeography of the genus Trachurus (Perciformes: Carangidae)

We addressed phylogenetic relationships in the genus Trachurus using cytochrome b gene and D-loop sequences. The trees showed five groups: (1) the Southwest Pacific species (T. japonicus, T. novaezelandiae, and T. declivis); (2) The Mediterranean Sea and Eastern Atlantic species (T. mediterraneus); (3) The Atlantic Ocean species (T. lathami and T. trecae); (4) Eastern Atlantic species (T. trachurus and T. capensis); and (5) a group of highly mobile pelagic species, two from the Eastern Pacific (T. symmetricus and T. murphyi) and one from the Eastern Atlantic (T. picturatus). The phylogeny based on Cyt b, supports the molecular clock hypothesis and our results agree with the reported fossil indicating that the origin of this genus occur when the Thetys Sea closed (around 18.4 MYA). In addition, a very slow neutral substitution rate is reported identified only two periods of maximum diversification: the first occurring between 18.4 and 15.0 MYA and the second between 8.4 MYA and present day.     

Neighbour-regulated mortality: the influence of positive and negative density dependence on tree populations in species-rich tropical forests

Density‐dependent mortality has long been posited as a possible mechanism for the regulation of tropical forest tree density. Despite numerous experimental and phenomenological investigations, the extent to which such mechanisms operate in tropical forests remains unresolved because the demographical signature of density dependence has rarely been found in extensive investigations of established trees. This study used an individual‐based demographical approach to investigate the role of conspecific and heterospecific neighbourhood crowding on tree mortality in a Panamanian and a Malayan tropical forest. More than 80% of the species investigated at each site were found to exhibit density‐dependent mortality. Furthermore, most of these species showed patterns of mortality consistent with the Janzen–Connell hypothesis and the rarely explored hypothesis of species herd protection. This study presents some of the first evidence of species herd protection operating in tree communities.     

Temporal patterns of diversification in Andean Eois, a species-rich clade of moths (Lepidoptera, Geometridae)

The timing of the origin of present day Neotropical animal diversity is still a matter of debate. For a long time, a preponderance of glacial (i.e. Pleistocene) radiations has been proposed. However, recent data from molecular clock studies indicate a preglacial origin for most of the examined taxa. We performed a fossil-calibrated molecular dating analysis of the genus Eois, which is a major component of one of the world's most diverse assemblages of herbivorous insects. We found that diversification of Eois took place in the Miocene following a pattern best explained by density-dependent diversification. A strong slowdown of diversification towards the present was detected. Diversification of Eois does overlap with increased Andean uplift and diversification of the most commonly used host plant genus Piper. These findings match the patterns found for the majority of Neotropical tetrapods and for three other unrelated, ecologically different lepidopteran genera.     

Phylogeny, diversification rates and species boundaries of Mesoamerican firs (Abies, Pinaceae) in a genus-wide context

The genus Abies is distributed discontinuously in the temperate and subtropical montane forests of the northern hemisphere. In Mesoamerica (Mexico and northern Central America), modern firs originated from the divergence of isolated mountain populations of migrating North American taxa. However, the number of ancestral species, migratory waves and diversification speed of these taxa is unknown. Here, variation in repetitive (Pt30204, Pt63718, and Pt71936) and non-repetitive (rbcL, rps18-rpl20 and trnL-trnF) regions of the chloroplast genome was used to reconstruct the phylogenetic relationships of the Mesoamerican Abies in a genus-wide context. These phylogenies and two fossil-calibrated scenarios were further employed to estimate divergence dates and diversification rates within the genus, and to test the hypothesis that, as in many angiosperms, conifers may exhibit accelerated speciation rates in the subtropics. All phylogenies showed five main clusters that mostly agreed with the currently recognized sections of Abies and with the geographic distribution of species. The Mesoamerican taxa formed a single group with species from southwestern North America of sections Oiamel and Grandis. However, populations of the same species were not monophyletic within this group. Divergence of this whole group dated back to the late Paleocene and the early Miocene depending on the calibration used, which translated in very low diversification rates (r_0.0 = 0.026-0.054, r_0.9 = 0.009-0.019 sp/Ma). Such low rates were a constant along the entire genus, including both the subtropical and temperate taxa. An extended phylogeographic analysis on the Mesoamerican clade indicated that Abies flinckii and A. concolor were the most divergent taxa, while the remaining species (A. durangensis, A. guatemalensis, A. hickelii, A. religiosa and A. vejari) formed a single group. Altogether, these results show that divergence of Mesoamerican firs coincides with a model of environmental stasis and decreased extinction rate, being probably prompted by a series of range expansions and isolation-by-distance.