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.     

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.     

Effects of seed dispersal by animals on the regeneration of Bursera graveolens (Burseraceae) on Santa Fe Island,Galápagos

Summary The importance of animals as seed dispersers for Bursera graveolens (Burseraceae) was assessed by analysis of juvenileadult interplant distances on Santa Fe Island, Galápagos. The Santa Fe Bursera population consists of two non-overlapping classes old, large adults, and juveniles recruited since the exermination of feral goats in 1971. Juveniles occurred on a variety of substrate types, as well as under and away from woody vegetation. Most juveniles arise from seeds dispersed by animals; 86% of the juveniles were 3 m away from the crown of the nearest adult, and half were 7 m away. Although all juveniles occurred within 35 m of an adult Bursera, seed dispersal by animals is an important factor in the regeneration of B. graveolens on Santa Fe.     

Seed weight increases with altitude in the Swiss Alps between related species but not among populations of individual species

Seed weight is a crucial plant life history trait, determining establishment success and dispersal ability. Especially in stressful environments, larger seeds may be selected at the expense of seed number, because larger seeds have a better chance of giving rise to an established offspring. We tested the hypotheses that between related species-pairs and among populations of single species a similar trend for increasing seed weight with increasing altitude should be present. Firstly, we measured seed weights from 29 species-pairs, with one species occurring in lowland areas and a congeneric species from high altitudes. Seeds of the alpine species were 28±8% larger than seeds from lowland species (P<0.01). Compared to the related lowland species, 55% of the alpine species had heavier seeds, 3% (one species) had lighter, and 41% had seeds of approximately equal weight. Secondly, we compared seed weights among populations of four species from different habitats and with different life histories. Seeds from between 11 and 34 populations per species were sampled along altitudinal gradients of 800–1,500 m (ca. 800 m in Scabiosa lucida, ca. 1,000 m in Saxifraga oppositifolia, ca. 1,000 m in Epilobium fleischeri, and ca. 1,500 m in Carex flacca). In all the four species, we found no indication for heavier seeds at higher altitudes. Our results indicate a selection pressure for species with heavier seeds at higher altitude, but the trend does not seem to operate across all cases. Phylogenetic constraints may limit the correlation among altitude and seed weight, operating particularly against selection for larger seed size, the closer populations and species are related to each other.     

Bursera pereirae,a new species and generic record for the Cerrado complex of Brazil. Studies in neotropical Burseraceae XVIII

Bursera pereirae is described and illustrated, and an updated key to Bursera in South America is provided. This new species, which should be considered threatened, is the first record of Bursera for the Cerrado region and the only species of tribe Bursereae endemic to Brazil.     

Influence of temporal fluctuations in seed abundance on the foraging behaviour of harvester ants (Pogonomyrmex spp.) in the central Monte desert,Argentina

The simultaneous study of the temporal dynamics of foraging behaviour, diet and seed abundance is essential to assess the way in which resources affect the behaviour and ecology of harvester ants. Here, we evaluate how fluctuations in grass seed abundance during three consecutive growing seasons influenced the foraging behaviour and diet of the harvester ants Pogonomyrmex rastratus, P. mendozanus and P. inermis in the central Monte desert, Argentina. Seed abundance of the most consumed grasses varied greatly through ant activity season, and ants altered their foraging behaviour in response to those changes. Foragers spent more time travelling and searching for food, and their foraging trips took longer during the low seed availability season. Foraging distance was very similar among species and, contrary to our expectations, did not vary between seasons. Foraging success of P. rastratus and P. inermis increased during the high availability season. This matched the seasonal pattern of foraging activity, suggesting that colonies may detect seed abundance and regulate their foraging effort with the rate of forager success. Although grass seeds were the main item in the diet of the three species, P. mendozanus, and to a lesser extent P. rastratus, turned more generalist when grass seeds were scarce. In contrast, P. inermis showed a very narrow diet breadth, only harvesting grass seeds in both seasons. Our results indicate the relevance of seed availability on foraging behaviour of harvester ants, which should be taken into account when predicting and evaluating the effect of ants on seed resources as well as numerical responses of harvester ant populations to the temporal and spatial variations in grass seed abundance.     

The role of the tolerance–fecundity trade‐off in maintaining intraspecific seed trait variation in a widespread dimorphic herb

Coexistence of species with different seed sizes is a long‐standing issue in community ecology, and a trade‐off between fecundity and stress tolerance has been proposed to explain co‐occurrence in heterogeneous environments. Here we tested an intraspecific extension of this model: whether such trade‐off also explains seed trait variation among populations of widespread plants under stress gradients. We collected seeds from 14 populations of Plantago coronopus along the Atlantic coast in North Africa and Europe. This herb presents seed dimorphism, producing large basal seeds with a mucilaginous coat that facilitates water absorption (more stress tolerant), and small apical seeds without coats (less stress tolerant). We analysed variation among populations in number, size and mucilage production of basal and apical seeds, and searched for relationships between local environment and plant size. Populations under higher stress (higher temperature, lower precipitation, lower soil organic matter) had fewer seeds per fruit, higher predominance of basal relative to apical seeds, and larger basal seeds with thicker mucilaginous coats. These results strongly suggest a trade‐off between tolerance and fecundity at the fruit level underpins variation in seed traits among P. coronopus populations. However, seed production per plant showed the opposite pattern to seed production per fruit, and seemed related to plant size and other life‐cycle components, as an additional strategy to cope with environmental variation across the range. The tolerance–fecundity model may constitute, under stress gradients, a broader ecological framework to explain trait variation than the classical seed size–number compromise, although several fecundity levels and traits should be considered to understand the diverse strategies of widespread plants to maximise fitness in each set of local conditions.     

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.     

Seed weight and germination behavior of the submerged plant Potamogeton pectinatus in the arid zone of northwest China

Variation in seed weight is common within and among plant species, but few studies have attempted to document the pattern of seed weight and germination attributes for aquatic macrophytes at a large scale. This study examined within‐species variation in seed weight and germination attributes and the effects of environmental factors on seed traits of the submerged plant Potamogeton pectinatus in the arid zone of northwest China. Our results showed that the average seed weight was 0.24 g per 100 seeds with a coefficient of variation (CV) of 28.4% among the eight P. pectinatus populations. The total germination fraction of seeds of P. pectinatus was relatively poor, less than 35% in seven P. pectinatus populations, and the lowest germination percentage found was only 2%. There were significant differences in seed weight, time to onset of germination, and total germination fraction among the eight different populations. Hierarchical partitioning analysis showed a strongly positive correlation between seed weight and water temperature and pH. Seed weight and the maternal environmental factors significantly affected both time to initiation of germination and total germination fraction. Our results suggest that (1) seed weight variation in P. pectinatus primarily is the result of temperature variation during fruit development; (2) relatively poor germination fraction suggests that seeds are relatively unimportant in the short‐term survival of populations and that it may be another adaptive trait allowing plants to take place in the right place and at the right time, especially in harsh environment; and (3) variation in seed germination traits should be determined by local environmental and intrinsic factors that interact in a complex fashion.     

Interannual variations in the seed production of Pinus Banksiana at the limit of the species distribution in northern Québec,Canada

Interannual variations in cone and seed production of Pinus banksiana Lamb, were studied at the species northern limit of distribution in Québec (Canada). Cone number per cone-bearing branch, potential number of seeds per cone, number of formed, filled, and viable seeds per cone, and seed viability, germination rate, and mass were determined for two populations of the species, over a 9-year series. There were significant differences among years, but not between populations, in all the variables considered. The populations were well synchronized with each other, suggesting that climatic influence on the variables considered might be significant. Apparent periodicity in reproductive output also suggests the existence of some internal cycle, possibly in relation to tree reserves. Annual viable seed production is the result of a combination of events in the reproductive cycle of an individual (i.e., cone initiation, pollination, fertilization, and embryo maturation), each one specifically affected by climate. There are no apparent trade-offs between seed mass and number of filled seeds per cone over time; moreover, there seems to be a positive relationship between seed mass and number of viable seeds per cone. Climate conditions during fertilization and embryo maturation (both of which occur during the same season) appear to significantly influence the species reproductive output. We present regression models based on meteorological variables to estimate cone and viable seed production, and seed mass.     

Notes on Bursera in South America,including a new species. Studies in Neotropical Burseraceae VII

Bursera inversa is the first new species of the genus to be described from South America in 90 years. The ecology of this species is remarkable because it is a large (to 25 m × 40 cm or greater) canopy tree of primary moist to wet lowland forest. It is easily distinguished from its congeners by its large, obovoid fruits and bony pyrene. A key to the South American species ofBursera is provided.     

Nuclear ribosomal DNA phylogeny and its implications for evolutionary trends in Mexican Bursera (Burseraceae)

The genus Bursera (Burseraceae) is one of the most diversified and abundant groups of plants of the tropical dry forests of Mexico. In order to provide a basis for better understanding of its evolutionary biology, we reconstructed a phylogeny of 57 species and varieties using the nucleotide sequences of the internal transcribed spacer regions (ITS1 and ITS2) of 18S–26S and the 5.8S coding region of nuclear ribosomal DNA. We used four species of the allied genera Commiphora and Boswellia and one species of Spondias (Anacardiaceae) as outgroups. Our results support the views that Bursera is monophyletic and more closely related to Commiphora than to Boswellia. The division of Bursera into sections Bullockia and Bursera is also strongly supported by our phylogeny. Several other subclades also had high bootstrap values, especially within section Bursera. We use the phylogeny as a basis for discussing evolutionary tendencies in bark, leaves, breeding systems, and fruits.     

Propagation of Rare Plants from Historic Seed Collections: Implications for Species Restoration and Herbarium Management

Herbaria are potentially important repositories of living seeds that could be useful for recovery of rare plant species. To examine this capacity, we tested seed germination of rare milkweed (Asclepias) and milkvetch (Astragalus) species representing different collection dates and different herbaria. These groups have contrasting seed characteristics, with greater potential for longevity in the nonpermeable hard-coated milkvetch seeds. Twelve-year-old Asclepias lanuginosa seeds failed to germinate. However, we achieved 45% germination from three-year-old Asclepias meadii seeds, but germination dropped to 0% after ages of four to five years. Astragalus neglectus seeds germinated from 97-, 48-, and 28-year-old herbarium specimens, and Astragalus tennesseensis seeds germinated from a four-year-old collection. Seedlings produced from these experiments were incorporated into ex situ garden populations for recovery or restoration of rare species populations. Different herbarium pest control techniques may have significant bearing on the viability of seeds stored on herbarium specimens. Microwaving can cause precipitous loss of seed viability, while deep-freezing appears to allow some seeds to remain viable. Potentially live seeds of rare species should be stored under conditions that enhance their long-term viability.     

Reproductive ecology of a federally endangered legume, Baptisia arachnifera, and its more widespread congener, B. lanceolata (Fabaceae)

Comparisons between rare species and their more common congener species can provide valuable information for conservation. Reproductive traits have previously been shown to be critical for reproductive success and persistence of rare species. In this study, we compared floral, seedpod, and seed traits of two Baptisia species (one endangered and one common) to assess differences in reproduction between species and among populations. Because heat can trigger germination in hard-seeded legumes, we also exposed Baptisia seeds to a range of high temperatures (60-100°C) and determined seed viability. The rare Baptisia arachnifera had significantly greater pod damage by insects and produced significantly fewer, yet heavier, seeds than B. lanceolata. While B. arachnifera seeds were seldom viable at temperatures above 80°C, approximately 40% of B. lanceolata seeds maintained viability up to 100°C. Our various seed trait measurements suggest that B. arachnifera may be a poorer colonizer than the more widespread B. lanceolata. Additionally, B. arachnifera's reduced tolerance for high temperatures may have implications for appropriate fire management regimes for this endangered species.     

Postdispersal seed predation and seed viability in forest soils: implications for the regeneration of tree species in Ethiopian church forests

Almost all dry Afromontane forests of Northern Ethiopia have been converted to agricultural, grazing or scrub lands except for small fragments left around churches (‘Church forests’). Species regeneration in these forests is limited. We investigated (i) how intense postdispersal seed predation was in church forest, and if this seed predation varied with species and/or habitat, and (ii) for how long tree seeds maintained their viability while buried in forest soil. In the seed predation experiment, we monitored seeds of six tree species in four habitats for a period of 14 weeks (the peak seeding season). In the seed viability experiment, we assessed seed viability of five species in four habitats after being buried 6, 12, or 18 months. Ninety‐two percent of the tree seeds were predated within 3.5 months. Predation was mainly dependent on species whereas habitat had a weaker effect. Seed viability decreased sharply with burial time in soil for all species except for Juniperus. To minimize seed availability limitation for regeneration of such species in the forest, the standing vegetation needs to be persistently managed and conserved for a continuous seed rain supply. Additional seed sowing, and seed and seedling protection (by e.g. animal exclosures) may increase successful regeneration of important species in these forests.     

Seed viability and seed dormancy of non-native Phragmites australis in suburbanized and forested watersheds of the Chesapeake Bay, USA

The non-native, invasive haplotype of Phragmites australis is rapidly invading tidal and non-tidal wetlands across North America. Phragmites has the potential to spread by seeds and rhizomes. Seed viability and dormancy differences were quantified among 18 patches of non-native Phragmites in subestuarine wetlands in developed (i.e., suburbanized) vs. forested watersheds of the Chesapeake Bay. We used tetrazolium and germination assays to assess seed viability and compared germination percentages and rate of germination among fresh seeds, cold–moist treated seeds, and warm–dry treated seeds to evaluate seed dormancy. Seed viability was <1% in most patches but a few patches produced abundant viable seeds (5–21%). Seed viability, however, did not differ significantly between wetlands in forested vs. developed watersheds. Contrary to studies of Phragmites seed dormancy in European populations, some Phragmites seeds were dormant at maturity; cold–moist treated seeds germinated faster and to higher percentages than fresh seeds or warm–dry treated seeds.     

Colonization of wounded peanut seeds by soil fungi: selectivity for species from Aspergillus section Flavi

Soil is a source of primary inoculum for Aspergillus flavus and A. parasiticus, fungi that produce highly carcinogenic aflatoxins in peanuts. Aflatoxigenic fungi commonly invade peanut seeds during maturation, and the highest concentrations of aflatoxins are found in damaged seeds. A laboratory procedure was developed in which viable peanut seeds were wounded and inoculated with field soil containing natural populations of fungi, then incubated under different conditions of seed water activity and temperature. Densities of Aspergillus section Flavi in soil used for inoculating seeds were low relative to the total numbers of filamentous fungi (<1%). Aspergillus species from section Flavi present in soil included A. flavus morphotypes L and S strains, A. parasiticus, A. caelatus, A. tamarii and A. alliaceus. Wounding was required for high incidences of fungal colonization; viability of wounded seeds had little effect on colonization by Aspergillus species. Peanut seeds were colonized by section Flavi species as well as A. niger over broad ranges of water activity (0.82-0.98) and temperature (15-37 C), and the highest incidences of seed colonization occurred at water activities of 0.92-0.96 at 22-37 C. A. parasiticus colonized peanut seeds at lower temperatures than A. flavus, and cool soil temperatures relative to temperatures of aerial crop fruits might explain why A. parasiticus is found mostly in peanuts. Other fungi, dominated by the genera Penicillium, Fusarium and Clonostachys, colonized seeds primarily at water activities and temperatures suboptimal for section Flavi species and A. niger. Eupenicillium ochrosalmoneum frequently sporulated on the conidial heads of section Flavi species and showed specificity for these fungi. The inoculation of wounded viable peanut seeds with soil containing natural populations of fungi provides a model system for studying the infection process, the interactions among fungi and those factors important in aflatoxin formation.     

Geographic variation in seed traits within and among forty‐two species of Rhododendron (Ericaceae) on the Tibetan plateau: relationships with altitude,habitat, plant height,and phylogeny

Seed mass and morphology are plant life history traits that influence seed dispersal ability, seeding establishment success, and population distribution pattern. Southeastern Tibet is a diversity center for Rhododendron species, which are distributed from a few hundred meters to 5500 m above sea level. We examined intra‐ and interspecific variation in seed mass and morphology in relation to altitude, habitat, plant height, and phylogeny. Seed mass decreased significantly with the increasing altitude and increased significantly with increasing plant height among populations of the same species. Seed mass differed significantly among species and subsections, but not among sections and subgenera. Seed length, width, surface area, and wing length were significantly negative correlated with altitude and significantly positive correlated with plant height. Further, these traits differed significantly among habitats and varied among species and subsection, but not among sections and subgenera. Species at low elevation had larger seeds with larger wings, and seeds became smaller and the wings of seeds tended to be smaller with the increasing altitude. Morphology of the seed varied from flat round to long cylindrical with increasing altitude. We suggest that seed mass and morphology have evolved as a result of both long‐term adaptation and constraints of the taxonomic group over their long evolutionary history.     

Polyploidy: a missing link in the conversation about seed transfer of a commonly seeded native grass in western North America

The use of local, native plant materials is now common in restoration but testing for polyploidy in seed sources is not. Diversity in cytotypes across a landscape can pose special seed transfer challenges, because the methods used to determine genetically appropriate materials for seed transfer do not account for cytotypic variation. This lack of consideration may result in mixing cytotypes through revegetation, which could reduce long‐term population viability. We surveyed nine populations of a native bunchgrass, Pseudoroegneria spicata, in three EPA Level III Ecoregions in the western United States to determine the frequency of polyploidy, whether there are differences in traits (phenotype, fecundity, and mortality) among plants of different cytotypes, and whether cytotype frequency varies among ecoregions. We assessed trait variation over 2 years in a common garden and determined ploidy using flow cytometry. Polyploidy and mixed cytotype populations were common, and polyploids occurred in all ecoregions. Four of the nine populations were diploid. The other five had tetraploids present: three had only tetraploid individuals whereas two had mixed diploid/tetraploid cytotypes. There was significant variation in traits among cytotypes: plants from tetraploid populations were larger than diploid or mixed populations. The frequency and distribution of cytotypes make it likely that seed transfer in the study area will inadvertently mix diploid and polyploid cytotypes in this species. The increasing availability of flow cytometry may allow ploidy to be incorporated into native plant materials sourcing and seed transfer.     

Protocols for Use of Potamogeton perfoliatus and Ruppia maritima Seeds in Large‐Scale Restoration

Restoration of submerged aquatic vegetation from seed has been hampered by a lack of information on the appropriate conditions for collecting, processing, and storing seeds prior to dispersal. Seeds must be processed and stored under conditions that maintain seed viability, meet dormancy requirements, and prevent premature germination. This study examined the effects of collection date, processing technique, aeration, storage and induction temperature and salinity, and storage period on seed germination of two mesohaline aquatic species, Potamogeton perfoliatus and Ruppia maritima. Collection date and processing technique were significant factors affecting seed yield from donor populations. Seeds of both species remained viable and germinated best when stored at 4°C, and then exposed to freshwater induction conditions. However, their responses to other factors differed. Aeration during storage was necessary in order to maintain viability of P. perfoliatus seeds, whereas it was unnecessary for R. maritima seeds. Storage in freshwater at 4°C prevented germination of P. perfoliatus seeds, while high salinity during cold storage was necessary to minimize premature germination of R. maritima. Mean germination time of P. perfoliatus was dependent on storage salinity; in contrast, mean germination time of R. maritima seeds was dependent on induction salinity. These differences indicate that the methods required to produce large quantities of underwater plant seed amenable to large‐scale restoration efforts must be tailored to the specific requirements of individual species and must consider the range of processes from initial harvest through seed testing prior to field establishment.