Biodiversity effects on yield and unsown species invasion in a temperate forage ecosystem

Background and Aims

Current agricultural practices are based on growing monocultures or binary mixtures over large areas, with a resultant impoverishing effect on biodiversity at several trophic levels. The effects of increasing the biodiversity of a sward mixture on dry matter yield and unsown species invasion were studied.

Methods

A field experiment involving four grassland species [two grasses – perennial ryegrass (Lolium perenne) and cocksfoot (Dactylis glomerata) – and two legumes – red clover (Trifolium pratense) and white clover (Trifolium repens)], grown in monocultures and mixtures in accordance with a simplex design, was carried out. The legumes were included either as single varieties or as one of two broad genetic-base composites. The experiment was harvested three times a year over three years; dry matter yield and yield of unsown species were determined at each harvest. Yields of individual species and interactions between all species present were estimated through a statistical modelling approach.

Key Results

Species diversity produced a strong positive yield effect that resulted in transgressive over-yielding in the second and third years. Using broad genetic-base composites of the legumes had a small impact on yield and species interactions. Invasion by unsown species was strongly reduced by species diversity, but species identity was also important. Cocksfoot and white clover (with the exception of one broad genetic-base composite) reduced invasion, while red clover was the most invaded species.

Conclusions

The results show that it is possible to increase, and stabilize, the yield of a grassland crop and reduce invasion by unsown species by increasing its species diversity.Key words: Cocksfoot, Dactylis glomerata, diversity effect, invasion, legumes, perennial ryegrass, Lolium perenne, red clover, Trifolium pratense, simplex design, statistical modelling, transgressive over-yielding, white clover, T. repens     

The potential of plant viruses to promote genotypic diversity via genotype x environment interactions

Background and Aims

Genotype by environment (G × E) interactions are important for the long-term persistence of plant species in heterogeneous environments. It has often been suggested that disease is a key factor for the maintenance of genotypic diversity in plant populations. However, empirical evidence for this contention is scarce. Here virus infection is proposed as a possible candidate for maintaining genotypic diversity in their host plants.

Methods

The effects of White clover mosaic virus (WClMV) on the performance and development of different Trifolium repens genotypes were analysed and the G × E interactions were examined with respect to genotype-specific plant responses to WClMV infection. Thus, the environment is defined as the presence or absence of the virus.

Key Results

WClMV had a negative effect on plant performance as shown by a decrease in biomass and number of ramets. These effects of virus infection differ greatly among host genotypes, representing a strong G × E interaction. Moreover, the relative fitness and associated ranking of genotypes changed significantly between control and virus treatments. This shift in relative fitness among genotypes suggests the potential for WClMV to provoke differential selection on T. repens genotypes, which may lead to negative frequency-dependent selection in host populations.

Conclusions

The apparent G × E interaction and evident repercussions for relative fitness reported in this study stress the importance of viruses for ecological and evolutionary processes and suggest an important role for viruses in shaping population dynamics and micro-evolutionary processes.     

Temporal changes in population genetic diversity and structure in red and white clover grown in three contrasting environments in northern Europe

Backgound and Aims

Extending the cultivation of forage legume species into regions where they are close to the margin of their natural distribution requires knowledge of population responses to environmental stresses. This study was conducted at three north European sites (Iceland, Sweden and the UK) using AFLP markers to analyse changes in genetic structure over time in two population types of red and white clover (Trifolium pratense and T. repens, respectively): (1) standard commercial varieties; (2) wide genetic base (WGB) composite populations constructed from many commercial varieties plus unselected material obtained from germplasm collections.

Methods

At each site populations were grown in field plots, then randomly sampled after 3–5 years to obtain survivor populations. AFLP markers were used to calculate genetic differentiation within and between original and survivor populations.

Key Results

No consistent changes in average genetic diversity were observed between original and survivor populations. In both species the original varieties were always genetically distinct from each other. Significant genetic shift was observed in the white clover ‘Ramona’ grown in Sweden. The WGB original populations were more genetically similar. However, genetic differentiation occurred between original and survivor WGB germplasm in both species, particularly in Sweden. Regression of climatic data with genetic differentiation showed that low autumn temperature was the best predictor. Within the set of cold sites the highest level of genetic shift in populations was observed in Sweden.

Conclusions

The results suggest that changes in population structure can occur within a short time span in forage legumes, resulting in the rapid formation of distinct survivor populations in environmentally challenging sites.     

Variable response of three Trifolium repens ecotypes to soil flooding by seawater

Background and Aims

Despite concerns about the impact of rising sea levels and storm surge events on coastal ecosystems, there is remarkably little information on the response of terrestrial coastal plant species to seawater inundation. The aim of this study was to elucidate responses of a glycophyte (white clover, Trifolium repens) to short-duration soil flooding by seawater and recovery following leaching of salts.

Methods

Using plants cultivated from parent ecotypes collected from a natural soil salinity gradient, the impact of short-duration seawater soil flooding (8 or 24 h) on short-term changes in leaf salt ion and organic solute concentrations was examined, together with longer term impacts on plant growth (stolon elongation) and flowering.

Key Results

There was substantial Cl^– and Na⁺ accumulation in leaves, especially for plants subjected to 24 h soil flooding with seawater, but no consistent variation linked to parent plant provenance. Proline and sucrose concentrations also increased in plants following seawater flooding of the soil. Plant growth and flowering were reduced by longer soil immersion times (seawater flooding followed by drainage and freshwater inputs), but plants originating from more saline soil responded less negatively than those from lower salinity soil.

Conclusions

The accumulation of proline and sucrose indicates a potential for solute accumulation as a response to the osmotic imbalance caused by salt ions, while variation in growth and flowering responses between ecotypes points to a natural adaptive capacity for tolerance of short-duration seawater soil flooding in T. repens. Consequently, it is suggested that selection for tolerant ecotypes is possible should the predicted increase in frequency of storm surge flooding events occur.     

Impacts of seedling herbivory on plant competition and implications for species coexistence

Background and Aims

Although the causes and consequences of seedling herbivory for plant community composition are well understood, the mechanisms by which herbivores influence plant species recruitment to the established phase remain less clear. The aim was to examine how variation in the intensity of seedling herbivory interacts with growth-defence trade-offs and herbivore feeding preferences to affect plant community development.

Methods

Using 14-d-old seedlings of Trifolium pratense and T. repens, relative growth and susceptibility to herbivory by the snail Helix aspersa was quantified to elucidate putative growth-defence trade-offs for these species. Then mixed assemblages of 14-d-old Trifolium seedlings were exposed to herbivory by zero, two, five or ten snails and determined how variation in the intensity of herbivory affected competitive interactions into the mature phase (as measured by total plant biomass at 120 d old).

Key Results

In the absence of herbivory, communities were dominated by T. pratense; a result expected on the basis that it yielded larger and presumably more competitive seedlings. However, when seedlings were exposed to herbivory, the balance of competition shifted. At low levels of herbivory (two snails), both Trifolium species contributed equally to total plant biomass. More intense herbivory (five snails) resulted in almost total mortality of T. pratense and dominance of the mature community by T. repens. The most intense herbivory (ten snails) effectively removed all seedlings from the experimental community.

Conclusions

The study illustrates a mechanism whereby spatio-temporal fluctuations in seedling herbivory, when coupled with species-specific variation in competitive ability and sensitivity to herbivore attack, can differentially influence plant recruitment into the mature phase. This mechanism may be a key element in our attempts to understand plant species coexistence, since fluctuations in plant recruitment are fundamental to the many theories that view coexistence as a consequence of a spatio-temporal lottery for dominance over regeneration micro-sites.Key words: Growth-defence trade-off, lottery models, plant–animal interactions, plant size variability, seedling acceptability, seedling defence, spatio-temporal niches, Trifolium pratense, Trifolium repens     

Variation in flooding-induced morphological traits in natural populations of white clover (Trifolium repens) and their effects on plant performance during soil flooding

Background and Aims

Soil flooding leads to low soil oxygen concentrations and thereby negatively affects plant growth. Differences in flooding tolerance have been explained by the variation among species in the extent to which traits related to acclimation were expressed. However, our knowledge of variation within natural species (i.e. among individual genotypes) in traits related to flooding tolerance is very limited. Such data could tell us on which traits selection might have taken place, and will take place in future. The aim of the present study was to show that variation in flooding-tolerance-related traits is present among genotypes of the same species, and that both the constitutive variation and the plastic variation in flooding-induced changes in trait expression affect the performance of genotypes during soil flooding.

Methods

Clones of Trifolium repens originating from a river foreland were subjected to either drained, control conditions or to soil flooding. Constitutive expression of morphological traits was recorded on control plants, and flooding-induced changes in expression were compared with these constitutive expression levels. Moreover, the effect of both constitutive and flooding-induced trait expression on plant performance was determined.

Key Results

Constitutive and plastic variation of several morphological traits significantly affected plant performance. Even relatively small increases in root porosity and petiole length contributed to better performance during soil flooding. High specific leaf area, by contrast, was negatively correlated with performance during flooding.

Conclusions

The data show that different genotypes responded differently to soil flooding, which could be linked to variation in morphological trait expression. As flooded and drained conditions exerted different selection pressures on trait expression, the optimal value for constitutive and plastic traits will depend on the frequency and duration of flooding. These data will help us understanding the mechanisms affecting short- and long-term dynamics in flooding-prone ecosystems.Key words: Secondary roots, aerenchyma, genotypic variation, petiole length, plant performance, root porosity, selection, soil flooding, specific leaf area (SLA), Trifolium repens, white clover     

Extra petals in the buttercup (Ranunculus repens) provide a quick method to estimate the age of meadows

Background and Aims

There is a widely used crude method to estimate the age of hedgerows (Hooper''s rule) based on species'' richness. The aim of this study was to try and establish a similar field method for estimating the age of grasslands based on the accumulation of macro-somatic mutations.

Methods

A countrywide survey was carried out by the British public to investigate the relationship between grassland age and the number of Ranunculus repens (creeping buttercup) plants with extra petals. In addition the relationship between grassland age and R. repens pollen viability was also investigated.

Key Results

Each plant with flowers with additional petals in a sample of 100 was found to equate to approx. 7 years. A higher significant correlation was observed between pollen viability and population age; however, this is not amenable to providing field estimates.

Conclusions

The age of British grasslands can be easily and reliably estimated in the field by counting the number flowers with additional petals in R. repens in meadows up to 200 years old. An attempt to estimate the heritability of extra petals suggests that the phenotype results from the slow accumulation of somatic mutations in a species that primarily reproduces vegetatively.Key words: Conservation, meadow, Müller''s ratchet, petal number, pollen viability, Ranunculus repens, buttercup, somatic mutation     

Eco-geographically divergent diploids, Caucasian clover (Trifolium ambiguum) and western clover (T. occidentale), retain most requirements for hybridization

Background and Aims

DNA sequence similarities and hybridization patterns in Trifolium (clovers) section Trifoliastrum suggest that rapid radiation from a common ancestral source led to this complex of diverse species distributed across Europe, western Asia and North Africa. Two of the most geographically and ecologically divergent of these species are the rhizomatous T. ambiguum from high altitudes in eastern Europe and western Asia and the stoloniferous T. occidentale from sea level in western Europe. Attempts were made to hybridize these species to ascertain whether, despite this separation, gene flow could be achieved, indicating the retention of the genetic factors necessary for hybridization.

Methods

Three F₁ hybrids formed after embryo rescue were described, characterized by conventional and molecular cytogenetics, subjected to fertility tests and progeny generations were developed.

Results and Conclusions

Partially fertile hybrids between Trifolium ambiguum and T. occidentale were obtained for the first time. The F₁ hybrids produced seeds after open-pollination, and also produced triploid progeny in backcrosses to T. occidentale from the functioning of unreduced gametes in the hybrids. These plants were fertile and produced progeny with T. occidentale and with T. repens. Meiotic chromosome pairing in the F₁ showed six to eight bivalents per pollen mother cell, indicating pairing between the parental genomes. A chromosome-doubled form of one hybrid, produced using colchicine, showed some multivalents, indicative of interspecific chromosome pairing. The hybrid plants were robust and combined phenotypic characteristics of both species, having stolons, thick roots and a few rhizomes. Results show that despite separation by the entire breadth of Europe, the speciation process is incomplete, and these taxa have partially retained most of the genetic compatibilities needed for hybridization (possibly except for endosperm development, which was not tested). The fertile progeny populations could lead to new clover breeding strategies based on new hybrid forms.     

Secondary Metabolites of Micromycetes in Plants of the Family Fabaceae,Genus <Emphasis Type="Italic">Trifolium</Emphasis>

The component composition and content of mycotoxins in perennial grasses of five species of the genus Trifolium, selected from natural biocenoses in different periods of vegetation, were studied. In the terrestrial parts of plants, the permanent presence of alternariol, cyclopiazonic acid, and emodin was shown. It was noted that differences in contamination are most clearly expressed in meadow clover Trifolium pratense L. and white clover Trifolium repens L., while alsike clover Trifolium hybridum L. occupies an intermediate position. It was found that zigzag clover Trifolium medium L. and mountain clover Trifolium montanum L., morphologically close to meadow clover, practically did not differ in the composition of toxic metabolites. The ways of formation of metabolic equilibrium in plants with participation of microscopic fungi are discussed.     

Host-specific races in the holoparasitic angiosperm Orobanche minor: implications for speciation in parasitic plants

Background and Aims

Orobanche minor is a root-holoparasitic angiosperm that attacks a wide range of host species, including a number of commonly cultivated crops. The extent to which genetic divergence among natural populations of O. minor is influenced by host specificity has not been determined previously. Here, the host specificity of natural populations of O. minor is quantified for the first time, and evidence that this species may comprise distinct physiological races is provided.

Methods

A tripartite approach was used to examine the physiological basis for the divergence of populations occurring on different hosts: (1) host–parasite interactions were cultivated in rhizotron bioassays in order to quantify the early stages of the infection and establishment processes; (2) using reciprocal-infection experiments, parasite races were cultivated on their natural and alien hosts, and their fitness determined in terms of biomass; and (3) the anatomy of the host–parasite interface was investigated using histochemical techniques, with a view to comparing the infection process on different hosts.

Key Results

Races occurring naturally on red clover (Trifolium pratense) and sea carrot (Daucus carota ssp. gummifer) showed distinct patterns of host specificity: parasites cultivated in cross-infection studies showed a higher fitness on their natural hosts, suggesting that races show local adaptation to specific hosts. In addition, histological evidence suggests that clover and carrot roots vary in their responses to infection. Different root anatomy and responses to infection may underpin a physiological basis for host specificity.

Conclusions

It is speculated that host specificity may isolate races of Orobanche on different hosts, accelerating divergence and ultimately speciation in this genus. The rapid life cycle and broad host range of O. minor make this species an ideal model with which to study the interactions of parasitic plants with their host associates.Key words: Parasitic plant, Orobanche, speciation, divergence, host-specificity, host-specific races     

Genomic regions involved in yield potential detected by genome-wide association analysis in Japanese high-yielding rice cultivars

Background

High-yielding cultivars of rice (Oryza sativa L.) have been developed in Japan from crosses between overseas indica and domestic japonica cultivars. Recently, next-generation sequencing technology and high-throughput genotyping systems have shown many single-nucleotide polymorphisms (SNPs) that are proving useful for detailed analysis of genome composition. These SNPs can be used in genome-wide association studies to detect candidate genome regions associated with economically important traits. In this study, we used a custom SNP set to identify introgressed chromosomal regions in a set of high-yielding Japanese rice cultivars, and we performed an association study to identify genome regions associated with yield.

Results

An informative set of 1152 SNPs was established by screening 14 high-yielding or primary ancestral cultivars for 5760 validated SNPs. Analysis of the population structure of high-yielding cultivars showed three genome types: japonica-type, indica-type and a mixture of the two. SNP allele frequencies showed several regions derived predominantly from one of the two parental genome types. Distinct regions skewed for the presence of parental alleles were observed on chromosomes 1, 2, 7, 8, 11 and 12 (indica) and on chromosomes 1, 2 and 6 (japonica). A possible relationship between these introgressed regions and six yield traits (blast susceptibility, heading date, length of unhusked seeds, number of panicles, surface area of unhusked seeds and 1000-grain weight) was detected in eight genome regions dominated by alleles of one parental origin. Two of these regions were near Ghd7, a heading date locus, and Pi-ta, a blast resistance locus. The allele types (i.e., japonica or indica) of significant SNPs coincided with those previously reported for candidate genes Ghd7 and Pi-ta.

Conclusions

Introgression breeding is an established strategy for the accumulation of QTLs and genes controlling high yield. Our custom SNP set is an effective tool for the identification of introgressed genome regions from a particular genetic background. This study demonstrates that changes in genome structure occurred during artificial selection for high yield, and provides information on several genomic regions associated with yield performance.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-346) contains supplementary material, which is available to authorized users.     

Limitations to reproductive output and genetic rescue in populations of the rare shrub Grevillea repens (Proteaceae)

Background and Aims

When conserving rare plant species, managers are often faced with small and/or isolated populations displaying low levels of sexual reproduction and genetic variation. One option for reinvigorating these populations is the introduction of genetic material from other sites, but in some cases fitness may be reduced as a result of outbreeding depression. Here the pollination biology of the rare shrub Grevillea repens is studied across its natural range and reproductive responses following cross-pollination among populations are examined to determine factors that may be limiting sexual reproduction and the potential for genetic rescue.

Methods

Pollen manipulation treatments (self-, autogamous self-, cross- and open pollination) were applied to flowers to examine the breeding system and fruit and seed production in five populations of G. repens. Pollen production, presentation and viability were investigated and interpopulation crosses of increasing genetic distance performed among the populations.

Key Results

The study species is self-incompatible and displayed very low natural seed set over two seasons, due partly to low pollen viability in one of the populations. Within-population crossing increased fruit and seed production at some sites, indicating pollinator limitation. Interpopulation crosses further increased reproductive output in one population, suggesting mate limitation, and for this site there was a positive relationship between genetic distance among populations and the size of genetic rescue benefits. However, in other populations there was a decrease in fruit and seed set with increasing genetic distance.

Conclusions

The results highlight that management strategies involving interpopulation crosses can improve reproductive output in small, isolated populations of rare plants, but guidelines need to be developed on a population by population basis.Key words: Grevillea repens, Proteaceae, genetic rescue, pollination ecology, self-incompatibility, breeding system, interpopulation cross, outbreeding depression, pollinator limitation, mate limitation, resource limitation     

Quantitative historical change in bumblebee (Bombus spp.) assemblages of red clover fields

Background

Flower visiting insects provide a vitally important pollination service for many crops and wild plants. Recent decline of pollinating insects due to anthropogenic modification of habitats and climate, in particular from 1950''s onwards, is a major and widespread concern. However, few studies document the extent of declines in species diversity, and no studies have previously quantified local abundance declines. We here make a quantitative assessment of recent historical changes in bumblebee assemblages by comparing contemporary and historical survey data.

Methodology/Principal Findings

We take advantage of detailed, quantitative historical survey data from the 1930''s on bumblebee (Bombus spp.) abundances and species composition in red clover (Trifolium pratense) fields, an important floral resource and an attractant of all bumblebee species. We used the historical survey data as a pre-industrialization baseline, and repeated the same sampling protocol at nearly the same localities at present, hence setting up a historical experiment. We detected historical changes in abundances (bees/m²) of both workers (the “pollinatory units”) and queens (effective population size), in addition to species composition. In particular, long-tongued bumblebee species showed consistent and dramatic declines in species richness and abundances throughout the flowering season of red clover, while short-tongued species were largely unaffected. Of 12 Bombus species observed in the 1930''s, five species were not observed at present. The latter were all long-tongued, late-emerging species.

Conclusions/Significance

Because bumblebees are important pollinators, historical changes in local bumblebee assemblages are expected to severely affect plant reproduction, in particular long-tubed species, which are pollinated by long-tongued bumblebees.     

Stamen development and winter dormancy in apricot (Prunus armeniaca)

Background and Aims

In temperate woody perennials, flower bud development is halted during the winter, when the buds enter dormancy. This dormant period is a prerequisite for adequate flowering, is genetically regulated, and plays a clear role in possibly adapting species and cultivars to climatic areas. However, information on the biological events underpinning dormancy is lacking. Stamen development, with clear differentiated stages, appears as a good framework to put dormancy in a developmental context. Here, stamen developmental changes are characterized in apricot (Prunus armeniaca) and are related to dormancy.

Methods

Stamen development was characterized cytochemically from the end of August to March, over 4 years. Developmental changes were related to dormancy, using the existing empirical information on chilling requirements.

Key Results

Stamen development continued during the autumn, and the flower buds entered dormancy with a fully developed sporogenous tissue. Although no anatomical changes were observed during dormancy, breaking of dormancy occurred following a clear sequence of events. Starch accumulated in particular places, pre-empting further development in those areas. Vascular bundles developed and pollen mother cells underwent meiosis followed by microspore development.

Conclusions

Dormancy appears to mark a boundary between the development of the sporogenous tissue and the occurrence of meiosis for further microspore development. Breaking of dormancy occurs following a clear sequence of events, providing a developmental context in which to study winter dormancy and to evaluate differences in chilling requirements among genotypes.     

Winter Active Bumblebees (Bombus terrestris) Achieve High Foraging Rates in Urban Britain

Background

Foraging bumblebees are normally associated with spring and summer in northern Europe. However, there have been sightings of the bumblebee Bombus terrestris during the warmer winters in recent years in southern England. But what floral resources are they relying upon during winter and how much winter forage can they collect?

Methodology/Principal Findings

To test if urban areas in the UK provide a rich foraging niche for bees we set up colonies of B. terrestris in the field during two late winter periods (2005/6 & 2006/7) in London, UK, and measured their foraging performance. Fully automatic radio-frequency identification (RFID) technology was used in 2006/7 to enable us to record the complete foraging activity of individually tagged bees. The number of bumblebees present during winter (October 2007 to March 2008) and the main plants they visited were also recorded during transect walks. Queens and workers were observed throughout the winter, suggesting a second generation of bee colonies active during the winter months. Mass flowering shrubs such as Mahonia spp. were identified as important food resources. The foraging experiments showed that bees active during the winter can attain nectar and pollen foraging rates that match, and even surpass, those recorded during summer.

Conclusions/Significance

B. terrestris in the UK are now able to utilise a rich winter foraging resource in urban parks and gardens that might at present still be under-exploited, opening up the possibility of further changes in pollinator phenology.     

Ecological significance of seed desiccation sensitivity in Quercus ilex

Background and Aims

Several widespread tree species of temperate forests, such as species of the genus Quercus, produce recalcitrant (desiccation-sensitive) seeds. However, the ecological significance of seed desiccation sensitivity in temperate regions is largely unknown. Do seeds of such species suffer from drying during the period when they remain on the soil, between shedding in autumn and the return of conditions required for germination in spring?

Methods

To test this hypothesis, the Mediterranean holm oak (Quercus ilex) forest was used as a model system. The relationships between the climate in winter, the characteristics of microhabitats, acorn morphological traits, and the water status and viability of seeds after winter were then investigated in 42 woodlands sampled over the entire French distribution of the species.

Key Results

The percentages of germination and normal seedling development were tightly linked to the water content of seeds after the winter period, revealing that in situ desiccation is a major cause of mortality. The homogeneity of seed response to drying suggests that neither intraspecific genetic variation nor environmental conditions had a significant impact on the level of desiccation sensitivity of seeds. In contrast, the water and viability status of seeds at the time of collection were dramatically influenced by cumulative rainfall and maximum temperatures during winter. A significant effect of shade and of the type of soil cover was also evidenced.

Conclusions

The findings establish that seed desiccation sensitivity is a key functional trait which may influence the success of recruitment in temperate recalcitrant seed species. Considering that most models of climate change predict changes in rainfall and temperature in the Mediterranean basin, the present work could help foresee changes in the distribution of Q. ilex and other oak species, and hence plant community alterations.