How can plants move without muscles, nerves and technical hinge analogies? Carnivorous bladderworts (Utricularia spp., Lentibulariaceae) perform one of the fastest movements known in the plant kingdom by capturing their prey (mainly small crustaceans) with suction traps. Capture lasts only half a millisecond, and animals are sucked into the trap with an acceleration of 600 g, which leaves no chance of escape. We review the current state of knowledge about these sophisticated trapping devices, highlight their biomechanical, functional-morphological and physiological peculiarities and discuss open questions for possible future studies.
Understanding the physics of plant movements, which describe the interplay between plant architecture, movement speed and actuation principles, is essential for the comprehension of important processes like plant morphogenesis. Recent investigations especially on rapid plant movements at the interface of biology, physics and engineering sciences highlight how such fast motions can be achieved without the presence of muscles, nerves and technical hinge analogies. The suction traps (bladders) of carnivorous bladderworts (Utricularia spp., Lentibulariaceae, Lamiales) are considered as some of the most elaborate moving structures in the plant kingdom. A complex interplay of morphological and physiological adaptations allows the traps to pump water out of their body and to store elastic energy in the deformed bladder walls. Mechanical stimulation by prey entails opening of the otherwise watertight trapdoor, followed by trap wall relaxation, sucking in of water and prey, and consecutive trapdoor closure. Suction can also occur spontaneously in non-stimulated traps. We review the current state of knowledge about the suction trap mechanism with a focus on architectonically homogeneous traps of aquatic bladderwort species from section Utricularia (the so-called ‘Utricularia vulgaris trap type’). The functional morphology and biomechanics of the traps are described in detail. We discuss open questions and propose promising aspects for future studies on these sophisticated ultra-fast trapping devices.
Biomechanics; bladderwort; carnivorous plant; functional morphology; prey; suction trap; Utricularia
In this study Tyagi et al. determined the genetic diversity and population structure of the model plant, Arabidopsis thaliana. These populations inhabit west Himalaya, an undersampled region. Using 19 genomic SSR and 11 chloroplast markers they determined that these populations are highly structured and genetically distinct from the rest of the world populations. They also observed that the populations were structured at the altitudinal level. Additionally their molecular clock analysis showed that these populations are not recent introductions and have inhabited the Himalayan region for about 130,000 years.
The natural genetic variation within a plant species is primarily a consequence of its phylogeography and evolutionary history. This variation largely determines its present-day population structure. Arabidopsis thaliana, as a model plant, has been studied in great detail including its probable origin, local as well as global genetic diversity pattern, population structure, adaptation, etc. However, no such studies have so far been reported from the Indian Himalayan region. Here, we describe a comprehensive study on the genetic diversity and population structure of A. thaliana from an altitudinal range of 700–3400 m above mean sea level the highest altitudinal range reported so far. We also compare these populations with previously reported worldwide populations. A total of 48 accessions representing six populations were analysed using 19 microsatellites and 11 chloroplast markers. Genetic diversity analysis indicated populations to be highly diverse and comparable with worldwide populations. STRUCTURE, principal coordinate and isolation by distance (IBD) analyses showed that genetic variation in different populations is structured at geographical and altitudinal level. Further analyses indicate that these populations are genetically distinct from the rest of the world populations. Different parameters of the demographic expansion model support a rapid expansion. Based on mismatch distribution, the initial time of expansion of west Himalayan populations was found to be about 130 000 years. Bayesian analysis of divergence time indicated that these populations have a long evolutionary history in this region. Based on the results of genetic diversity parameters, demographic expansion and divergence time estimation, it appears that west Himalayan populations may be the source of the west–east expansion model.
Chloroplast loci; evolution; genetic diversity; Indian Arabidopsis; microsatellite markers; phylogeography; population structure
There is a strong incentive to predict which species will become invasive before they become too widespread and unmanageable. In this study, we conducted a multi-year, temporally replicated, greenhouse and field experiment based on plant functional traits, quantifying competitive ability, and phylogenetic comparison to determine the invasive potential of four closely related species varying in invasion status, life history and habitat. Our results suggest that these closely related species do exhibit similar competitive abilities and that the invasiveness and not the life history or habitat of these species appear to be the driving factor of competitiveness.
Invasive species are a threat to every ecosystem. There is a strong incentive to predict which species will become invasive before they become too widespread and unmanageable. Different approaches have been advocated to assess invasive species potential. These include examining plant functional traits, quantifying competitive ability and phylogenetic comparison. In this study, we conducted experiments based on the above approaches in a multi-year, temporally replicated, set of experiments to compare these assessment methods to determine the invasive potential of Japanese chaff flower (Achyranthes japonica). We compared plant traits and competitive ability of Japanese chaff flower with two agricultural invasive species, Palmer amaranth (Amaranthus palmeri) and tall waterhemp (Amaranthus tuberculatus), and one endangered plant species, bloodleaf (Iresine rhizomatosa), in the Amaranthaceae. Additionally, we assessed the invasive potential based on each of these approaches and determined the degree of agreement between them. A relatively conservative assessment integrating all three approaches would be that the competitive ability of closely related individuals with similar functional traits would share invasive potential. In a greenhouse experiment, each of the study species and soya beans were grown as monocultures and were evaluated to assess the drawdown of an aboveground (light) and a belowground (nitrogen) resource. In a field experiment, each study species was grown at varying densities per 15-cm-diameter pot with or without one or two soya bean plants, to simulate relative densities for soya beans grown in 38- and 76-cm-wide row spacing, respectively. In addition, Japanese chaff flower seedlings were planted either as un-manipulated seedlings or as a seedling cut back to the soil surface at the four-node stage (cut Japanese chaff flower) at which point seedlings have reached a perennial growth stage. The greenhouse experiment showed that each species drew down light differently, but not nitrogen. Shading decreased the aboveground biomass of the species in comparison with unshaded controls. Nitrogen, however, increased the aboveground biomass of Palmer amaranth and Japanese chaff flower. In the field experiment, a competitive effect ranking was determined to be: tall waterhemp ≥ Palmer amaranth = cut Japanese chaff flower ≥ uncut Japanese chaff flower ≥ bloodleaf, with the competitive response ranking being the inverse. These results suggest that under specific conditions, these closely related species do exhibit similar competitive abilities. Furthermore, the invasiveness and not the life history or habitat of these closely related species appeared to be the driving factor of competitiveness.
Amaranthaceae; competition; early vegetative growth; invasive species; resource drawdown
Phylogeography above the species level is a powerful tool for investigating patterns and processes at the boundary between divergent and reticulate relationships. We examined the evolutionary history of perennial species in the western Mediterranean composite genus Helminthotheca using DNA sequence and fingerprint data. The origin of the group was in western North Africa, a region of intensive Pleistocene speciation. From here it expanded to the Iberian Peninsula and Sicily. The inferred evolutionary history is compatible with the concept of ecogeographic isolation, which refers to the fact that geographic ranges of diverging lineages are largely non-overlapping due to adaptive differentiation.
In phylogeography, DNA sequence and fingerprint data at the population level are used to infer evolutionary histories of species. Phylogeography above the species level is concerned with the genealogical aspects of divergent lineages. Here, we present a phylogeographic study to examine the evolutionary history of a western Mediterranean composite, focusing on the perennial species of Helminthotheca (Asteraceae, Cichorieae). We used molecular markers (amplified fragment length polymorphism (AFLP), internal transcribed spacer and plastid DNA sequences) to infer relationships among populations throughout the distributional range of the group. Interpretation is aided by biogeographic and molecular clock analyses. Four coherent entities are revealed by Bayesian mixture clustering of AFLP data, which correspond to taxa previously recognized at the rank of subspecies. The origin of the group was in western North Africa, from where it expanded across the Strait of Gibraltar to the Iberian Peninsula and across the Strait of Sicily to Sicily. Pleistocene lineage divergence is inferred within western North Africa as well as within the western Iberian region. The existence of the four entities as discrete evolutionary lineages suggests that they should be elevated to the rank of species, yielding H. aculeata, H. comosa, H. maroccana and H. spinosa, whereby the latter two necessitate new combinations.
Amplified fragment length polymorphism; Helminthotheca; Iberian Peninsula; phylogeography; Strait of Gibraltar; western Mediterranean region; western North Africa
Offspring phenotypes may be altered by environments that their parents lived in. These environmentally-induced trans-generational effects may be mediated by epigenetic mechanisms such as DNA methylation. Little is known about the role of such epigenetic effects in evolution; however, it is expected to facilitate evolution. To expand geographic range, it is thought that most species would have to adapt via evolution by natural selection to stressful environments beyond range boundaries. Contrary to expectations, we show that DNA methylation in an upland mustard species may underlie a drought-induced trans-generational tradeoff that may constrain the process of adaptation to stressful environments at lower elevations.
Genetic variation gives plants the potential to adapt to stressful environments that often exist beyond their geographic range limits. However, various genetic, physiological or developmental constraints might prevent the process of adaptation. Alternatively, environmentally induced epigenetic changes might sustain populations for several generations in stressful areas across range boundaries, but previous work on Boechera stricta, an upland mustard closely related to Arabidopsis, documented a drought-induced trans-generational plastic trade-off that could contribute to range limit development. Offspring of parents who were drought treated had higher drought tolerance, but lower levels of glucosinolate toxins. Both drought tolerance and defence are thought to be needed to expand the range to lower elevations. Here, we used methylation-sensitive amplified fragment length polymorphisms to determine whether environmentally induced DNA methylation and thus epigenetics could be a mechanism involved in the observed trans-generational plastic trade-off. We compared 110 offspring from the same self-fertilizing lineages whose parents were exposed to experimental drought stress treatments in the laboratory. Using three primer combinations, 643 polymorphic epi-loci were detected. Discriminant function analysis (DFA) on the amount of methylation detected resulted in significant combinations of epi-loci that distinguished the parent drought treatments in the offspring. Principal component (PC) and univariate association analyses also detected the significant differences, even after controlling for lineage, planting flat, developmental differences and multiple testing. Univariate tests also indicated significant associations between the amount of methylation and drought tolerance or glucosinolate toxin concentration. One epi-locus that was implicated in DFA, PC and univariate association analysis may be directly involved in the trade-off because increased methylation at this site on the genome decreased drought tolerance, but increased glucosinolate concentration.
Boechera stricta; DNA methylation; drought tolerance; epigenetic association analysis; glucosinolate chemical defence; MS-AFLP; range limits; trade-off
This is the introductory paper of the special issue emerging from the First Island Biology Symposium hosted in Honolulu on July 2014. The 18 papers compiled present data from multiple archipelagos across the world and from different disciplines within plant sciences, showing us how much island biology has advanced since Carlquist's inspiring contribution Island Biology. Such advance has been possible mostly thanks to the increasing availability and richness of island data, new information from the geosciences, phylogenetics, and palaeoecology, and new methodological advances in analyzing data at large spatial scales. A group of papers deal with issues to which Carlquist contributed most: long-distance dispersal, adaptive radiation, and plant reproductive biology, whereas others cover a range of topics related to plant conservation on islands.
Sherwin Carlquist's seminal publications—in particular his classic Island Biology, published in 1974—formulated hypotheses specific to island biology that remain valuable today. This special issue brings together some of the most interesting contributions presented at the First Island Biology Symposium hosted in Honolulu on 7–11 July 2014. We compiled a total of 18 contributions that present data from multiple archipelagos across the world and from different disciplines within the plant sciences. In this introductory paper, we first provide a short overview of Carlquist's life and work and then summarize the main findings of the collated papers. A first group of papers deals with issues to which Carlquist notably contributed: long-distance dispersal, adaptive radiation and plant reproductive biology. The findings of such studies demonstrate the extent to which the field has advanced thanks to (i) the increasing availability and richness of island data, covering many taxonomic groups and islands; (ii) new information from the geosciences, phylogenetics and palaeoecology, which allows us a more realistic understanding of the geological and biological development of islands and their biotas; and (iii) the new theoretical and methodological advances that allow us to assess patterns of abundance, diversity and distribution of island biota over large spatial scales. Most other papers in the issue cover a range of topics related to plant conservation on islands, such as causes and consequences of mutualistic disruptions (due to pollinator or disperser losses, introduction of alien predators, etc.). Island biologists are increasingly considering reintroducing ecologically important species to suitable habitats within their historic range and to neighbouring islands with depauperate communities of vertebrate seed dispersers, and an instructive example is given here. Finally, contributions on ecological networks demonstrate the usefulness of this methodological tool to advancing conservation management and better predicting the consequences of disturbances on species and interactions in the fragile insular ecosystems.
Biogeography; island ecology and conservation; oceanic islands; palaeoecology; phylogeography
Ecological restoration is often conducted with limited consideration of genetic diversity and the environmental factors that drive variation within species. We studied genetic diversity and environmental variation among 16 populations of Stylidium hispidum, an endemic southwestern Australian triggerplant. As a result we were able to estimate the seed transfer distance within which genetic divergence is low and population fitness less likely to be impacted by maladaptation, and identify environmental variables that may be relevant for future restoration of this species.
Efforts to re-establish native plant species should consider intraspecific variation if we are to restore genetic diversity and evolutionary potential. Data describing spatial genetic structure and the scale of adaptive differentiation are needed for restoration seed sourcing. Genetically defined provenance zones provide species-specific guidelines for the distance within which seed transfer likely maintains levels of genetic diversity and conserves locally adapted traits. While a growing number of studies incorporate genetic marker data in delineation of local provenance, they often fail to distinguish the impacts of neutral and non-neutral variation. We analysed population genetic structure for 134 amplified fragment length polymorphism (AFLP) markers in Stylidium hispidum (Stylidiaceae) along a north–south transect of the species' range with the goal to estimate the distance at which significant genetic differences occur among source and recipient populations in restoration. In addition, we tested AFLP markers for signatures of selection, and examined the relationship of neutral and putatively selected markers with climate variables. Estimates of population genetic structure revealed significant levels of differentiation (ΦPT = 0.23) and suggested a global provenance distance of 45 km for pairwise comparisons of 16 populations. Of the 134 markers, 13 exhibited evidence of diversifying selection (ΦPT = 0.52). Using data for precipitation and thermal gradients, we compared genetic, geographic and environmental distance for subsets of neutral and selected markers. Strong isolation by distance was detected in all cases, but positive correlations with climate variables were present only for markers with signatures of selection. We address findings in light of defining local provenance in ecological restoration.
AFLP; BayeScan; ecological restoration; southwestern Australia; spatial genetic structure; Stylidium hispidum
A weed or not a weed? Many plant species grow somewhere on the continuum from undisturbed to very disturbed vegetation. Deciding on the degree of weediness is not an easy task, and often based only on subjective observations. In this work, we compare data obtained during systematic field surveys with the habitats recorded on herbarium specimen labels, for a group of more-or-less weedy tropical species. We show that herbarium data reflect the collection bias favouring natural vegetation, but also, that the relative weediness hierarchy stays in place. The study is relevant for other ecological studies based on herbarium specimens.
It is often desirable to quantify a plant's relative weediness or synanthropy, that is, the degree to which a species associates with human-caused disturbance, in order to study and understand the biology, ecology and evolution of weeds and invasive plants. Herbarium specimens are among the most accessible and verifiable sources of data on distribution and habitat. However, the habitat distribution of species may not be reflected accurately by herbarium specimen data, due to well-known biases in plant collection. Here, we assess how well herbarium specimens reflect species' weediness, when compared with direct field surveys. We used five species of Melampodium (Asteraceae) and classified their degree of weediness with a modification of Nuorteva's synanthropy index, based on herbarium specimens. We then modelled the distribution of our focal species in Mexico using MaxEnt and identified a polygon of ∼3000 km2 in the state of Nayarit, Mexico, where there was a high probability of finding all five species. Systematic field searches in the target area documented all visible populations of four species along major and minor roads. Then we, again, classified their degree of weediness with the synanthropy index, based now on field data, and compared. We found that herbarium data were an accurate predictor of a species' weediness relative to its congeners despite the well-documented skew of herbarium data towards natural areas, which our data reflected as well. So, herbarium data can be used to classify species' weediness relative to each other, but not in absolute terms, if the specimens were correctly identified and none of the species were subject to particular collection bias. This study is the first attempt to compare herbarium and field data on this subject and may be relevant for other types of investigations based on herbarium data. Our work also highlights the usefulness of distribution models based on herbarium specimens.
Distribution modelling; disturbed habitat; herbarium specimen data; MaxEnt; ruderal plants; synanthropy; weed; weediness index
In the maize landraces from Northeastern Argentina inter and even intra-populational genome size variations were detected. Moreover, high variation in number, positions, percentage of heterochromatin as well in size and sequence compositions of knobs were detected. Since knobs would be an important cause of the observed differences in DNA content, the absence of a significant relationship between the percentage of heterochromatin and genome size suggests that other non-coding repetitive DNA sequences contribute to genome size variation. The positive correlations between the length of the vegetative cycle and percentage of heterochromatin found allowed us to attribute an adaptive effect to the heterochromatin, since the vegetative cycle time would be optimized via selection for an appropriate percentage of heterochromatin.
Genome size variation accompanies the diversification and evolution of many plant species. Relationships between DNA amount and phenotypic and cytological characteristics form the basis of most hypotheses that ascribe a biological role to genome size. The goal of the present research was to investigate the intra-specific variation in the DNA content in maize populations from Northeastern Argentina and further explore the relationship between genome size and the phenotypic traits seed weight and length of the vegetative cycle. Moreover, cytological parameters such as the percentage of heterochromatin as well as the number, position and sequence composition of knobs were analysed and their relationships with 2C DNA values were explored. The populations analysed presented significant differences in 2C DNA amount, from 4.62 to 6.29 pg, representing 36.15 % of the inter-populational variation. Moreover, intra-populational genome size variation was found, varying from 1.08 to 1.63-fold. The variation in the percentage of knob heterochromatin as well as in the number, chromosome position and sequence composition of the knobs was detected among and within the populations. Although a positive relationship between genome size and the percentage of heterochromatin was observed, a significant correlation was not found. This confirms that other non-coding repetitive DNA sequences are contributing to the genome size variation. A positive relationship between DNA amount and the seed weight has been reported in a large number of species, this relationship was not found in the populations studied here. The length of the vegetative cycle showed a positive correlation with the percentage of heterochromatin. This result allowed attributing an adaptive effect to heterochromatin since the length of this cycle would be optimized via selection for an appropriate percentage of heterochromatin.
DAPI staining; DNA content variation; FISH; Guarani's maize landraces; heterochromatic knobs; karyotype parameters
The strawberry tree diverged into two groups during the Quaternary, but before the LGM, surviving in refugia located in the western end of the Mediterranean region and with the Eastern Mediterranean being colonized more recently. This migration was possible because Europe and North Africa were occasionally connected through the straits of Gibraltar and Sicily. Likewise, our evidence supports arrival in Ireland from northern Iberia in post-glacial times. Altogether, our results reveal the considerable ability of the strawberry tree for dispersal, allowing it to migrate over thousands of kilometres and cross stretches of sea, which may be crucial for its future survival.
Phylogeographic studies give us the opportunity to reconstruct the historical migrations of species and link them with climatic and geographic variation. They are, therefore, a key tool to understanding the relationships among biology, geology and history. One of the most interesting biogeographical areas of the world is the Mediterranean region. However, in this area, the description of concordant phylogeographic patterns is quite scarce, which limits the understanding of evolutionary patterns related to climate. Species with one-dimensional distribution ranges, such as the strawberry tree (Arbutus unedo), are particularly useful to unravel these patterns. Here, we describe its phylogeographic structure and check for concordance with patterns seen in other Mediterranean plants: longitudinal/latitudinal clines of diversity, evidence for glacial refugia and the role of sea straits in dispersal. We also identify the most likely source for the disjunct Irish population. With this aim, we sequenced four chloroplast non-coding fragments of A. unedo from 23 populations covering its whole distribution. We determined the genetic diversity, population structure, haplotype genealogy and time to the most recent common ancestor. The genealogy revealed two clades that separated during the last 700 ky but before the last glacial maximum. One clade occupies Atlantic Iberia and North Africa, while the other occurs in the Western Mediterranean. The Eastern Mediterranean is inhabited by newer haplotypes derived from both clades, while the Irish population is closely related to Iberian demes. The straits of Sicily and Gibraltar partially restricted the gene flow. We concluded that a vicariance event during the Late Quaternary in the western end of the species' range followed by eastward migration seems a likely explanation for the observed phylogeographic pattern. The role of straits indicates an occasional communication between Europe and North Africa, suggesting that the latter was a novel refugia. The East–West genetic split in Iberia is consistent with the refugia-within-refugia model. Finally, the strawberry tree possibly reached Ireland from Iberia instead of throughout the maritime fringe of France as previously thought.
Arbutus unedo; clades; cpDNA; Lusitanian; Mediterranean; refugia; strait; vicariance
Petunia secreta is a rare and endemic species, that was found in two different landscapes, approximately 21 Km apart from each other. In this study we showed that P. secreta presented high genetic diversity that was equivalent to or even higher than that of widespread Petunia species. Two evolutionary lineages were found and they are correlated to the different landscapes where P. secreta grows: open areas in conglomerate sandstone towers at an elevation of approximately 300-400 m or along the road growing in an open vegetation flat area. Therefore the major risk to P. secreta maintenance is its rarity, suggesting the necessity of a preservation program.
The analysis of genetic structure and variability of isolated species is of critical importance in evaluating whether stochastic or human-caused factors are affecting rare species. Low genetic diversity compromises the ability of populations to evolve and reduces their chances of survival under environmental changes. Petunia secreta, a rare and endemic species, is an annual and heliophilous herb that is bee-pollinated and easily recognizable by its purple and salverform corolla. It was described as a new species of the Petunia genus in 2005. Few individuals of P. secreta have been observed in nature and little is known about this species. All the natural populations of P. secreta that were found were studied using 15 microsatellite loci, two intergenic plastid sequences and morphological traits. Statistical analysis was performed to describe the genetic diversity of this rare species and the results compared with those of more widespread and frequent Petunia species from the same geographic area to understand whether factors associated with population size could affect rare species of this genus. The results showed that despite its rarity, P. secreta presented high genetic diversity that was equivalent to or even higher than that of widespread Petunia species. It was shown that this species is divided into two evolutionary lineages, and the genetic differentiation indices between them and other congeneric species presented different patterns. The major risk to P. secreta maintenance is its rarity, suggesting the necessity of a preservation programme and more biological and evolutionary studies that handle the two evolutionary lineages independently.
Conservation; genetic diversity; microendemic; microsatellites; plant evolution; plastid sequences
Mediterranean high-mountain ecosystems are increasingly threatened by climate change, causing biodiversity loss, habitat degradation and landscape modifications. In this work, we used phytosociological relevés to conduct a re-visitation study in order to analyze changes in floristic composition over the last 42 years in the central Apennines (Majella National Park). We observed changes in floristic composition, along with a significant increase in thermophilic and nutrient-demanding species. Such changes are likely attributable to the combined effect of higher temperatures and the increase in soil nutrients triggered by global change.
High-mountain ecosystems are increasingly threatened by climate change, causing biodiversity loss, habitat degradation and landscape modifications. However, very few detailed studies have focussed on plant biodiversity in the high mountains of the Mediterranean. In this study, we investigated the long-term changes that have occurred in the composition, structure and ecology of high-mountain vegetation in the central Apennines (Majella) over the last 42 years. We performed a re-visitation study, using historical and newly collected vegetation data to explore which ecological and structural features have been the most successful in coping with climatic changes. Vegetation changes were analysed by comparing geo-referenced phytosociological relevés collected in high-mountain habitats (dolines, gentle slopes and ridges) on the Majella massif in 1972 and in 2014. Composition analysis was performed by detrended correspondence analysis, followed by an analysis of similarities for statistical significance assessment and by similarity percentage procedure (SIMPER) for identifying which species indicate temporal changes. Changes in ecological and structural indicators were analysed by a permutational multivariate analysis of variance, followed by a post hoc comparison. Over the last 42 years, clear floristic changes and significant ecological and structural variations occurred. We observed a significant increase in the thermophilic and mesonitrophilic plant species and an increment in the frequencies of hemicryptophytes. This re-visitation study in the Apennines agrees with observations in other alpine ecosystems, providing new insights for a better understanding of the effects of global change on Mediterranean high-mountain biodiversity. The observed changes in floristic composition, the thermophilization process and the shift towards a more nutrient-demanding vegetation are likely attributable to the combined effect of higher temperatures and the increase in soil nutrients triggered by global change. The re-visitation approach adopted herein represents a powerful tool for studying climate-related changes in sensitive high-mountain habitats.
Global change; Landolt indicators; life forms; Mediterranean mountains; phytosociological relevés; re-visitation study
Using previously identified Phragmites clonal genotypes we investigated differences in their phenotypic plasticity through measurements of the lengths and densities of stomata on both the abaxial (lower) and adaxial (upper) surfaces of leaves, and synthesized these measurements to estimate impacts on maximum stomatal conductance to water (gwmax). Results demonstrated that at three marsh sites invasive lineages have consistently greater gwmax than their native congeners, as a result of greater stomatal densities and smaller stomata. Our analysis also suggests that phenotypic plasticity, determined as within genotype variation in gwmax, of the invasive lineage is similar to, or exceeds that shown by the native lineage.
The fitness costs of reproduction by clonal growth can include a limited ability to adapt to environmental and temporal heterogeneity. Paradoxically, some facultatively clonal species are not only able to survive, but colonize, thrive and expand in heterogeneous environments. This is likely due to the capacity for acclimation (sensu stricto) that compensates for the fitness costs and complements the ecological advantages of clonality. Introduced Phragmites australis demonstrates great phenotypic plasticity in response to temperature, nutrient availability, geographic gradient, water depths, habitat fertility, atmospheric CO2, interspecific competition and intraspecific competition for light. However, no in situ comparative subspecies studies have explored the difference in plasticity between the non-invasive native lineage and the highly invasive introduced lineage. Clonality of the native and introduced lineages makes it possible to control for genetic variation, making P. australis a unique system for the comparative study of plasticity. Using previously identified clonal genotypes, we investigated differences in their phenotypic plasticity through measurements of the lengths and densities of stomata on both the abaxial (lower) and adaxial (upper) surfaces of leaves, and synthesized these measurements to estimate impacts on maximum stomatal conductance to water (gwmax). Results demonstrated that at three marsh sites, invasive lineages have consistently greater gwmax than their native congeners, as a result of greater stomatal densities and smaller stomata. Our analysis also suggests that phenotypic plasticity, determined as within-genotype variation in gwmax, of the invasive lineage is similar to, or exceeds, that shown by the native lineage.
Clonal plant; invasive; Phragmites; plasticity; stomata
Climbing monocots can develop into large bodied plants despite being confined by primary growth. In our study on Flagellaria indica we measured surprisingly high stem biomechanical properties (in bending and torsion) and we show that the lack of secondary growth is overcome by a combination of tissue maturation processes and attachment mode. This leads to higher densities of mechanically relevant tissues in the periphery of the stem and to the transition from self-supporting to climbing growth. The development of specialised attachment structures has probably underpinned the evolution of numerous other large bodied climbing monocot taxa.
Plants with a climbing growth habit possess unique biomechanical properties arising from adaptations to changing loading conditions connected with close attachment to mechanical supports. In monocot climbers, mechanical adaptation is restricted by the absence of a bifacial vascular cambium. Flagellaria indica was used to investigate the mechanical properties and adaptations of a monocot climber that, uniquely, attaches to the surrounding vegetation via leaf tendrils. Biomechanical methods such as three-point bending and torsion tests were used together with anatomical studies on tissue development, modification and distribution. In general, the torsional modulus was lower than the bending modulus; hence, torsional stiffness was less than flexural stiffness. Basal parts of mature stems showed the greatest stiffness while that of more apical stem segments levelled off. Mechanical properties were modulated via tissue maturation processes mainly affecting the peripheral region of the stem. Peripheral vascular bundles showed a reduction in the amount of conducting tissue while the proportion and density of the bundle sheath increased. Furthermore, adjacent bundle sheaths merged resulting in a dense ring of fibrous tissue. Although F. indica lacks secondary cambial growth, the climbing habit is facilitated by a complex interaction of tissue maturation and attachment.
Biomechanics; climbing plants; Flagellaria indica; functional morphology; monocotyledons; structural bending modulus; structural modulus of torsion; three-point bending; twist-to-bend ratio
The optimal level of Bt toxin in Bt cotton is imperative for sustainability and adoption of Bt cotton under water stressed and non-stressed environments. We investigated the mode of inheritance and association of various drought tolerance biochemicals traits with Bt toxin under normal and water stressed conditions. We observed non-additive gene action coupled with low heritability estimates for all studied biochemical traits. The different kinds of association between Bt toxin and biochemical traits proved to be a simple innovative strategy. Furthermore, it is concluded that different biochemical traits can serve as a potential biochemical markers in future for breeding drought tolerant Bt cotton.
Drought is an abiotic environmental stress that can significantly reduce crop productivity. We examined the mode of inheritance for different biochemical traits including total soluble proteins, chlorophyll a, chlorophyll b, total chlorophyll, carotenoids, total phenolic contents and enzymatic antioxidants (superoxide dismutase, peroxidase and catalase), and their relationship with Bacillus thuringiensis (Bt) toxin under control and drought conditions. Eight genetically diverse cotton genotypes were selfed for two generations to ensure homozygosity. Fifteen F1 hybrids were developed by crossing five non-Bt female lines with three Bt male testers. The F1 hybrids and eight parents were finally evaluated under control (100 % field capacity (FC)) and drought (50 % FC) conditions in 2013. The biochemical traits appeared to be controlled by non-additive gene action with low narrow sense heritability estimates. The estimates of general combining ability and specific combining ability for all biochemical traits were significant under control and drought conditions. The genotype-by-trait biplot analysis showed the better performance of Bt cotton hybrids when compared with their parental genotypes for various biochemical traits under control and drought conditions. The biplot and path coefficient analyses revealed the prevalence of different relationships between Cry1Ac toxin and biochemical traits in the control and drought conditions. In conclusion, biochemical traits could serve as potential biochemical markers for breeding Bt cotton genotypes without compromising the optimal level of Bt toxin.
Biochemical markers; carotenoids; Cry1Ac toxin; enzymatic antioxidants; non-additive gene action
Plants that flower for long periods are ideal organisms in which to test whether the timing and duration of flowering adjust to the seasonal timing of biotic and abiotic resources, and whether that influences their reproductive success. Hypericum balearicum is an evergreen endemic shrub that flowers all year round but mainly during spring and summer. We found that those plants inhabiting a locality with lower rainfall had the capacity to flower longer. During spring and summer, the reproduction of plants that flowered earlier depended on both pollinators and rainfall, whereas the reproduction of plants that flowered later depended more upon rainfall scarcity.
Flowering phenology and synchrony with biotic and abiotic resources are crucial traits determining the reproductive success in insect-pollinated plants. In seasonal climates, plants flowering for long periods should assure reproductive success when resources are more predictable. In this work, we evaluated the relationship between flowering phenology and synchrony and reproductive success in Hypericum balearicum, a shrub flowering all year round but mainly during spring and summer. We studied two contrasting localities (differing mostly in rainfall) during 3 years, and at different biological scales spanning from localities to individual flowers and fruits. We first monitored (monthly) flowering phenology and reproductive success (fruit and seed set) of plants, and assessed whether in the locality with higher rainfall plants had longer flowering phenology and synchrony and relatively higher reproductive success within or outside the flowering peak. Secondly, we censused pollinators on H. balearicum individuals and measured reproductive success along the flowering peak of each locality to test for an association between (i) richness and abundance of pollinators and (ii) fruit and seed set, and seed weight. We found that most flowers (∼90 %) and the highest fruit set (∼70 %) were produced during the flowering peak of each locality. Contrary to expectations, plants in the locality with lower rainfall showed more relaxed flowering phenology and synchrony and set more fruits outside the flowering peak. During the flowering peak of each locality, the reproductive success of early-flowering individuals depended on a combination of both pollinator richness and abundance and rainfall; by contrast, reproductive success of late-flowering individuals was most dependent on rainfall. Plant species flowering for long periods in seasonal climates, thus, appear to be ideal organisms to understand how flowering phenology and synchrony match with biotic and abiotic resources, and how this ultimately influences plant reproductive success.
Balearic Islands; flower synchrony; flower visitors; Hypericum balearicum; Mediterranean plants; rainfall effect on reproduction; resource limitation
Anyone interested in plants may already have asked themselves why some trees host a wide diversity and large numbers of epiphytes while others have none. This may occur by chance or could be derived from specific patterns driven by tree traits. Here we evaluated how individual and species characteristics affect the number and location of atmospheric bromeliads. We found that the presence of bromeliads is not stochastic, and that tree traits have a great influence on the presence and abundance of bromeliad species. Additionally, trees can be categorized as worse or better hosts to shelter these plants based on their canopy and trunk characteristics.
Epiphytes are strongly dependent on the conditions created by their host's traits and a certain degree of specificity is expected between them, even if these species are largely abundant in a series of tree hosts of a given environment, as in the case of atmospheric bromeliads. Despite their considerable abundance in these environments, we hypothesize that stochasticity alone cannot explain the presence and abundance of atmospheric bromeliads on host trees, since host traits could have a greater influence on the establishment of these bromeliads. We used secondary and reforested seasonal forests and three distinct silvicultures to test whether species richness, phylogenetic diversity and functional diversity of trees can predict the differential presence, abundance and distribution of atmospheric bromeliads on hosts. We compared the observed parameters of their assemblage with null models and performed successive variance hierarchic partitions of abundance and distribution of the assemblage to detect the influence of multiple traits of the tree hosts. Our results do not indicate direct relationships between the abundance of atmospheric bromeliads and phylogenetic or functional diversity of trees, but instead indicate that bromeliads occurred on fewer tree species than expected by chance. We distinguished functional tree patterns that can improve or reduce the abundance of atmospheric bromeliads, and change their distribution on branches and trunk. While individual tree traits are related to increased abundance, species traits are related to the canopy distribution of atmospheric bromeliad assemblages. A balance among these tree functional patterns drives the atmospheric bromeliad assemblage of the forest patches.
Atmospheric bromeliads; canopy ecology; epiphyte assemblage; functional ecology; host preference; phorophyte; Tillandsia
This study examines the biochemical basis of red flowers in the tomato family, Solanaceae. We show that red-flowered species have converged on the same floral hue using either the sole production of red anthocyanin pigments or, more commonly, the dual production of purple or blue anthocyanins and orange carotenoid pigments. The use of blue anthocyanins in red flowers appears to differ from other groups, and suggests that the genetic changes underlying evolutionary transitions to red flowers may not be as predictable as previously suggested.
Red flowers have evolved repeatedly across angiosperms and are frequently examined in an ecological context. However, less is known about the biochemical basis of red colouration in different taxa. In this study, we examine the spectral properties, anthocyanin composition and carotenoid expression of red flowers in the tomato family, Solanaceae, which have evolved independently multiple times across the group. Our study demonstrates that Solanaceae typically make red flowers either by the sole production of red anthocyanins or, more commonly, by the dual production of purple or blue anthocyanins and orange carotenoids. In using carotenoids to modify the effect of purple and/or blue anthocyanins, these Solanaceae species have converged on the same floral hue as those solely producing red anthocyanins, even when considering the visual system of pollinators. The use of blue anthocyanins in red flowers appears to differ from other groups, and suggests that the genetic changes underlying evolutionary shifts to red flowers may not be as predictable as previously suggested.
Anthocyanins; biochemical pathway; carotenoids; flower colour; pigments; Solanaceae
Xylem vulnerability to cavitation is an important trait in characterizing woody species' drought tolerance. However, artifacts arise for long-vesselled species when using the in situ flow centrifuge method, also known as the Cavitron. We tested the role of microbubbles as a potential mechanism for this bias by constructing vulnerability and xylem water extraction curves for species with different maximum vessel lengths in different rotor sizes. Our results show a major difference in xylem vulnerability to cavitation for long-vesselled species between methods and support the microbubble effect hypothesis.
Plant resistance to xylem cavitation is a major drought adaptation trait and is essential to characterizing vulnerability to climate change. Cavitation resistance can be determined with vulnerability curves. In the past decade, new techniques have increased the ease and speed at which vulnerability curves are produced. However, these new techniques are also subject to new artefacts, especially as related to long-vesselled species. We tested the reliability of the ‘flow rotor’ centrifuge technique, the so-called Cavitron, and investigated one potential mechanism behind the open vessel artefact in centrifuge-based vulnerability curves: the microbubble effect. The microbubble effect hypothesizes that microbubbles introduced to open vessels, either through sample flushing or injection of solution, travel by buoyancy or mass flow towards the axis of rotation where they artefactually nucleate cavitation. To test the microbubble effect, we constructed vulnerability curves using three different rotor sizes for five species with varying maximum vessel length, as well as water extraction curves that are constructed without injection of solution into the rotor. We found that the Cavitron technique is robust to measure resistance to cavitation in tracheid-bearing and short-vesselled species, but not for long-vesselled ones. Moreover, our results support the microbubble effect hypothesis as the major cause for the open vessel artefact in long-vesselled species.
Cavitation resistance; embolism; plant hydraulics; vessel length artefact; water relations
Non-native plant invasions and changing management activities have altered the structure and composition of forests. Invasive shrubs and fire suppression have led to increased densification and biomass accumulation in forest ecosystems of the southeastern United States. Notably, the encroachment of non-native privets has altered ecosystem processes and caused changes in community structure. The latter has become manifest through decreases in fine herbaceous fuels concurrent with increases in coarse woody fuels in forest understories. These alterations in fuel structure will potentially lead to less frequent, but more severe forest fires, which threaten forest resources during extreme weather conditions.
Non-native plant invasions and changing management activities have dramatically altered the structure and composition of forests worldwide. Invasive shrubs and fire suppression have led to increased densification and biomass accumulation in forest ecosystems of the southeastern USA. Notably, Chinese and European privets are rapid growing, shade-tolerant shrubs which number among the most aggressive invasive species in these forests. Privet encroachment has caused losses of native diversity, alteration of ecosystem processes and changes in community structure. The latter has become manifest through decreases in fine herbaceous fuels concurrent with increases in coarse woody fuels in forest understoreys. These alterations in fuel structure will potentially lead to less frequent, but more severe forest fires, which threaten important forest resources during extreme weather conditions. Drawing on extensive data sets compiled by the US Forest Service, we integrated statistical forecasting and analytical techniques within a spatially explicit, agent-based, simulation framework to predict potential range expansion of Chinese and European privet (Ligustrum sinense and L. vulgare) and the associated increase in crown fire risk over the next two decades in forestlands of Mississippi and Alabama. Our results indicate that probability of invasion is positively associated with elevation, adjacency (within 300 m) to water bodies, mean daily maximum temperature, site productivity and private land ownership, and is negatively associated with slope, stand age, artificial regeneration, distance to the nearest road and fire disturbance. Our projections suggest the total area invaded will increase from 1.36 to ≈31.39% of all forestlands in Mississippi and Alabama (≈7 million hectares) and the annual frequency of crown fires in these forestlands will approximately double within the next two decades. Such time series projections of annual range expansions and crown fire frequency should provide land managers and restoration practitioners with an invasion chronology upon which to base proactive management plans.
Biological invasion; dispersal model; habitat quality; invasive plants; invasive species; logistic regression; zero-inflated negative binomial regression
There are several emerging generalizations in invasion biology, but often the factors determining invasiveness are group-specific. Similar to other plant families, Araceae species (arums or aroids) with large native ranges and that have been widely introduced are more likely to become invasive. What is unique to the family is the great diversity of growth forms, some more likely to become invasive than others. We identify nine lineages in the family that have a greater tendency to invasiveness (including the duckweed lineage, as well as the genera Alocasia and Epipremnum). A precautionary approach should be taken for such clades.
Significant progress has been made in understanding biological invasions recently, and one of the key findings is that the determinants of naturalization and invasion success vary from group to group. Here, we explore this variation for one of the largest plant families in the world, the Araceae. This group provides an excellent opportunity for identifying determinants of invasiveness in herbaceous plants, since it is one of the families most popular with horticulturalists, with species occupying various habitats and comprising many different life forms. We first developed a checklist of 3494 species of Araceae using online databases and literature sources. We aimed to determine whether invasiveness across the introduction–naturalization–invasion continuum is associated to particular traits within the family, and whether analyses focussed on specific life forms can reveal any mechanistic correlates. Boosted regression tree models were based on species invasion statuses as the response variables, and traits associated with human use, biological characteristics and distribution as the explanatory variables. The models indicate that biological traits such as plant life form and pollinator type are consistently strong correlates of invasiveness. Additionally, large-scale correlates such as the number of native floristic regions and number of introduced regions are also influential at particular stages in the invasion continuum. We used these traits to build a phenogram showing groups defined by the similarity of characters. We identified nine groups that have a greater tendency to invasiveness (including Alocasia, the Lemnoideae and Epipremnum). From this, we propose a list of species that are not currently invasive for which we would recommend a precautionary approach to be taken. The successful management of plant invasions will depend on understanding such context-dependent effects across taxonomic groups, and across the different stages of the invasion process.
Araceae; biological invasions; boosted regression trees; invasiveness; predictions; stages of invasion; traits
To clarify the significant genomic events of the tribe Parideae, we analysed the complete chloroplast genome sequences of two Trillium species representing two subgenera: Trillium and Phyllantherum. The results showed that the cpDNAs of Parideae are highly conserved across genome structure, gene order and contents. However, the chloroplast genome of T. maculatum contained a 3.4kb inverted sequence between ndhC - rbcL in the LSC region. In addition, we found three different types of trnI-CAU duplication. These genomic features provide informative molecular markers for identifying the infrageneric taxa of Trillium and improve our understanding of the evolution patterns of Parideae.
Genomic events including gene loss, duplication, pseudogenization and rearrangement in plant genomes are valuable sources for exploring and understanding the process of evolution in angiosperms. The family Melanthiaceae is distributed in temperate regions of the Northern Hemisphere and divided into five tribes (Heloniadeae, Chionographideae, Xerophylleae, Melanthieae and Parideae) based on the molecular phylogenetic analyses. At present, complete chloroplast genomes of the Melanthiaceae have been reported from three species. In the previous genomic study of Liliales, a trnI-CAU gene duplication event was reported from Paris verticillata, a member of Parideae. To clarify the significant genomic events of the tribe Parideae, we analysed the complete chloroplast genome sequences of two Trillium species representing two subgenera: Trillium and Phyllantherum. In Trillium tschonoskii (subgenus Trillium), the circular double-stranded cpDNA sequence of 156 852 bp consists of two inverted repeat (IR) regions of 26 501 bp each, a large single-copy (LSC) region of 83 981 bp and a small single-copy (SSC) region of 19 869 bp. The chloroplast genome sequence of T. maculatum (subgenus Phyllantherum) is 157 359 bp in length, consisting of two IRs (25 535 bp), one SSC (19 949 bp) and one LSC (86 340 bp), and is longer than that of T. tschonoskii. The results showed that the cpDNAs of Parideae are highly conserved across genome structure, gene order and contents. However, the chloroplast genome of T. maculatum contained a 3.4-kb inverted sequence between ndhC and rbcL in the LSC region, and it was a unique feature for subgenera Phyllantherum. In addition, we found three different types of gene duplication in the intergenic spacer between rpl23 and ycf2 containing trnI-CAU, which were in agreement with the circumscription of subgenera and sections in Parideae excluding T. govanianum. These genomic features provide informative molecular markers for identifying the infrageneric taxa of Trillium and improve our understanding of the evolution patterns of Parideae in Melanthiaceae.
Chloroplast genome; comparative genomics; gene duplication; single inversion; Trillium maculatum; Trillium tschonoskii, trnI-CAU
This study contributes to knowledge on the effect of the invasive N2-fixing tree, Acacia dealbata, on soil microbial communities and consequences on plant species that are dependent on symbiotic relationships as in the case of Plantago lanceolata. The main results of this work indicate that Acacia dealbata modifies the structure of arbuscular mycorrhizal fungi in the invaded shrublands and consequently the growth and development of plants that depend on AMF. Plantago lanceolata showed a substantial reduction in growth, biomass, fungal colonization and P content in the absence of native AMF species.
Arbuscular mycorrhizal fungi (AMF) are obligate soil biotrophs that establish intimate relationships with 80 % of terrestrial plant families. Arbuscular mycorrhizal fungi obtain carbon from host plants and contribute to the acquisition of mineral nutrients, mainly phosphorus. The presence of invasive plants has been identified as a soil disturbance factor, often conditioning the structure and function of soil microorganisms. Despite the investigation of many aspects related to the invasion of Acacia dealbata, the effect produced on the structure of AMF communities has never been assessed. We hypothesize that A. dealbata modifies the structure of AMF community, influencing the establishment and growth of plants that are dependent on these mutualisms. To validate our hypothesis, we carried out denaturing gradient gel electrophoresis (DGGE) analysis and also grew plants of Plantago lanceolata in pots using roots of native shrublands or from A. dealbata, as inoculum of AMF. Cluster analyses from DGGE indicated an alteration in the structure of AMF communities in invaded soils. After 15 weeks, we found that plants grown in pots containing native roots presented higher stem and root growth and also produced higher biomass in comparison with plants grown with A. dealbata inoculum. Furthermore, plants that presented the highest biomass and growth exhibited the maximum mycorrhizal colonization and phosphorus content. Moreover, fluorescence measurements indicated that plants grown with A. dealbata inoculum even presented higher photosynthetic damage. Our results indicate that the presence of the invader A. dealbata modify the composition of the arbuscular fungal community, conditioning the establishment of native plants.
Acacia dealbata; DGGE; microbial community structure; plant invasion; Plantago lanceolata; root inoculum; soil sterilization
Polyploidy (multiple copies of whole genomes) is over-represented in invasive plants and thought to promote their success in novel environments. Understanding functional traits supporting colonization can provide a foundation for development of effective management strategies. We compared how two aquatic invasive congeners differing in ploidy (diploid, decaploid) respond to resource availability (light, nutrients). Counter to our predictions, the diploid congener out-performed the decaploid with nutrient enrichment. Our results suggest the congeners have alternate colonization strategies, and trait responses underlying their success may change with ontogeny. Management strategies for invasive Ludwigia species should therefore be tailored for specific cytotypes and unique characteristics of their life stages.
Understanding traits underlying colonization and niche breadth of invasive plants is key to developing sustainable management solutions to curtail invasions at the establishment phase, when efforts are often most effective. The aim of this study was to evaluate how two invasive congeners differing in ploidy respond to high and lowresource availability following establishment from asexual fragments. Because polyploids are expected to have wider niche breadths than diploid ancestors, we predicted that a decaploid species would have superior ability to maximize resource uptake and use, and outperform a diploid congener when colonizing environments with contrasting light and nutrient availability. A mesocosm experiment was designed to test the main and interactive effects of ploidy (diploid and decaploid) and soil nutrient availability (low and high) nested within light environments (shade and sun) of two invasive aquatic plant congeners. Counter to our predictions, the diploid congener outperformed the decaploid in the early stage of growth. Although growth was similar and low in the cytotypes at low nutrient availability, the diploid species had much higher growth rate and biomass accumulation than the polyploid with nutrient enrichment, irrespective of light environment. Our results also revealed extreme differences in time to anthesis between the cytotypes. The rapid growth and earlier flowering of the diploid congener relative to the decaploid congener represent alternate strategies for establishment and success.
Aquatic plants; functional plant traits; invasion ecology; invasive plants; Ludwigia; polyploidy; reproductive allocation
Despite being a highly autogamous or self-pollinating species, the carnivorous plant Drosophyllum lusitanicum (Drosophyllaceae) produces large, bright-yellow flowers. Our results detected a significant increase (15-25%) in seed set of experimentally self-pollinated flowers and flowers exposed to insect visitation compared with bagged, untouched flowers whose seeds were produced only by spontaneous self-pollination. Given that the key life-history stage of this fire-adapted plant species is the formation of a persistent seed-bank, any increase in seed production through insect pollinator activity would increase plant fitness. This in turn would explain the maintenance of large, showy flowers in a highly autogamous plant.
Reproductive biology of carnivorous plants has largely been studied on species that rely on insects as pollinators and prey, creating potential conflicts. Autogamous pollination, although present in some carnivorous species, has received less attention. In angiosperms, autogamous self-fertilization is expected to lead to a reduction in flower size, thereby reducing resource allocation to structures that attract pollinators. A notable exception is the carnivorous pyrophyte Drosophyllum lusitanicum (Drosophyllaceae), which has been described as an autogamous selfing species but produces large, yellow flowers. Using a flower removal and a pollination experiment, we assessed, respectively, whether large flowers in this species may serve as an attracting device to prey insects or whether previously reported high selfing rates for this species in peripheral populations may be lower in more central, less isolated populations. We found no differences between flower-removed plants and intact, flowering plants in numbers of prey insects trapped. We also found no indication of reduced potential for autogamous reproduction, in terms of either seed set or seed size. However, our results showed significant increases in seed set of bagged, hand-pollinated flowers and unbagged flowers exposed to insect visitation compared with bagged, non-manipulated flowers that could only self-pollinate autonomously. Considering that the key life-history strategy of this pyrophytic species is to maintain a viable seed bank, any increase in seed set through insect pollinator activity would increase plant fitness. This in turn would explain the maintenance of large, conspicuous flowers in a highly autogamous, carnivorous plant.
Autogamous selfing; Drosophyllum lusitanicum; floral display; pollination biology; prey capture; pyrophyte; seed set