Maria N. Miriti

When Seed Dispersal Matters

Abstract A profusion of fruit forms implies that seed dispersal plays a central role in plant ecology, yet the chance that an individual seed will ultimately produce a reproductive adult is low to infinitesimal. Extremely high variance in survival implies that variations in fruit production or transitions from seed to seedling will contribute little to population growth. The key issue is that variance in survival of plant life-history stages, and therefore the importance of dispersal, differs greatly among and within plant communities. In stable communities of a few species of long-lived plants, variances in seed and seedling survival are immense, so seed-to-seedling transitions have little influence on overall population dynamics. However, when seedlings in different circumstances have very different chances of survival—in ecological succession, for example, or when dispersed seeds escape density-dependent mortality near parent trees—the biased survival of dispersed seeds or seedlings in some places rather than others results in pervasive demographic impacts.

Decoupling of soil nutrient cycles as a function of aridity in global drylands

The biogeochemical cycles of carbon (C), nitrogen (N) and phosphorus (P) are interlinked by primary production, respiration and decomposition in terrestrial ecosystems. It has been suggested that the C, N and P cycles could become uncoupled under rapid climate change because of the different degrees of control exerted on the supply of these elements by biological and geochemical processes. Climatic controls on biogeochemical cycles are particularly relevant in arid, semi-arid and dry sub-humid ecosystems (drylands) because their biological activity is mainly driven by water availability. The increase in aridity predicted for the twenty-first century in many drylands worldwide may therefore threaten the balance between these cycles, differentially affecting the availability of essential nutrients. Here we evaluate how aridity affects the balance between C, N and P in soils collected from 224 dryland sites from all continents except Antarctica. We find a negative effect of aridity on the concentration of soil organic C and total N, but a positive effect on the concentration of inorganic P. Aridity is negatively related to plant cover, which may favour the dominance of physical processes such as rock weathering, a major source of P to ecosystems, over biological processes that provide more C and N, such as litter decomposition. Our findings suggest that any predicted increase in aridity with climate change will probably reduce the concentrations of N and C in global drylands, but increase that of P. These changes would uncouple the C, N and P cycles in drylands and could negatively affect the provision of key services provided by these ecosystems.

EPISODIC DEATH ACROSS SPECIES OF DESERT SHRUBS

Extreme events shape population and community trajectories. We report episodic mortality across common species of thousands of long-lived perennials individually tagged and monitored for 20 years in the Colorado Desert of California following severe regional drought. Demographic records from 1984 to 2004 show 15 years of virtual stasis in populations of adult shrubs and cacti, punctuated by a 55-100% die-off of six of the seven most common perennial species. In this episode, adults that experienced reduced growth in a lesser drought during 1984-1989 failed to survive the drought of 2002. The significance of this event is potentially profound because population dynamics of long-lived plants can be far more strongly affected by deaths of adults, which in deserts potentially live for centuries, than by seedling births or deaths. Differential mortality and rates of recovery during and after extreme climatic events quite likely determine the species composition of plant and associated animal communities for at least decades. The die-off recorded in this closely monitored community provides a unique window into the mechanics of this process of species decline and replacement.

Increasing aridity reduces soil microbial diversity and abundance in global drylands.

Significance Climate change is increasing the degree of aridity in drylands, which occupy 41% of Earth’s surface and support 38% of its population. Soil bacteria and fungi are largely responsible for key ecosystem services, including soil fertility and climate regulation, yet their responses to changes in aridity are poorly understood. Using a field survey conducted in drylands worldwide and DNA-sequencing approaches, we found that increases in aridity reduce the diversity and abundance of soil bacteria and fungi. This study represents an important advancement in our understanding of soil microbial communities and their likely responses to ongoing climate change. Soil bacteria and fungi play key roles in the functioning of terrestrial ecosystems, yet our understanding of their responses to climate change lags significantly behind that of other organisms. This gap in our understanding is particularly true for drylands, which occupy ∼41% of Earth´s surface, because no global, systematic assessments of the joint diversity of soil bacteria and fungi have been conducted in these environments to date. Here we present results from a study conducted across 80 dryland sites from all continents, except Antarctica, to assess how changes in aridity affect the composition, abundance, and diversity of soil bacteria and fungi. The diversity and abundance of soil bacteria and fungi was reduced as aridity increased. These results were largely driven by the negative impacts of aridity on soil organic carbon content, which positively affected the abundance and diversity of both bacteria and fungi. Aridity promoted shifts in the composition of soil bacteria, with increases in the relative abundance of Chloroflexi and α-Proteobacteria and decreases in Acidobacteria and Verrucomicrobia. Contrary to what has been reported by previous continental and global-scale studies, soil pH was not a major driver of bacterial diversity, and fungal communities were dominated by Ascomycota. Our results fill a critical gap in our understanding of soil microbial communities in terrestrial ecosystems. They suggest that changes in aridity, such as those predicted by climate-change models, may reduce microbial abundance and diversity, a response that will likely impact the provision of key ecosystem services by global drylands.

Twenty years of changes in spatial association and community structure among desert perennials

I present results from analyses of 20 years of spatiotemporal dynamics in a desert perennial community. Plants were identified and mapped in a 1-ha permanent plot in Joshua Tree National Park (California, USA) in 1984. Plant size, mortality, and new seedlings were censused every five years through 2004. Two species, Ambrosia dumosa and Tetracoccus hallii, were dominant based on their relative abundance and ubiquitous distributions. Spatial analysis for distance indices (SADIE) identified regions of significantly high (patches) or low (gaps) densities. I used SADIE to test for (1) transience in the distribution of patches and gaps within species over time and (2) changes in juvenile-adult associations with conspecific adults and adults of the two dominant species over time. Plant performance was quantified in patches and gaps to determine plant responsiveness to local spatial associations. Species identity was found to influence associations between juveniles and adults. Juveniles of all species showed significant positive spatial associations with the dominant A. dumosa but not with T. hallii. The broad distribution of A. dumosa may increase the spatial extent of non-dominant species that are facilitated by this dominant. The spatial location of patches and gaps was generally consistent over time for adults but not juveniles. Observed variability in the locations of juvenile patches and gaps suggested that suitable locations for establishment were broad relative to occupied regions of the habitat, and that conditions for seed germination were independent of conditions for seedling survival. A dramatic change in spatial distributions and associations within and between species occurred after a major drought that influenced data from the final census. Positive associations between juveniles and adults of all species were found independent of previous associations and most species distributions contracted to areas that were previously characterized by low density. By linking performance to spatial distribution, results from this study offer a spatial context for plant-plant interactions within and among species. Community composition could be influenced both by individual species tolerances of abiotic conditions and by the competitive or facilitative interactions individuals exert over neighbors.

Climate and soil attributes determine plant species turnover in global drylands

AIM Geographic, climatic, and soil factors are major drivers of plant beta diversity, but their importance for dryland plant communities is poorly known. This study aims to: i) characterize patterns of beta diversity in global drylands, ii) detect common environmental drivers of beta diversity, and iii) test for thresholds in environmental conditions driving potential shifts in plant species composition. LOCATION 224 sites in diverse dryland plant communities from 22 geographical regions in six continents. METHODS Beta diversity was quantified with four complementary measures: the percentage of singletons (species occurring at only one site), Whittakes beta diversity (β(W)), a directional beta diversity metric based on the correlation in species occurrences among spatially contiguous sites (β(R2)), and a multivariate abundance-based metric (β(MV)). We used linear modelling to quantify the relationships between these metrics of beta diversity and geographic, climatic, and soil variables. RESULTS Soil fertility and variability in temperature and rainfall, and to a lesser extent latitude, were the most important environmental predictors of beta diversity. Metrics related to species identity (percentage of singletons and β(W)) were most sensitive to soil fertility, whereas those metrics related to environmental gradients and abundance ((β(R2)) and β(MV)) were more associated with climate variability. Interactions among soil variables, climatic factors, and plant cover were not important determinants of beta diversity. Sites receiving less than 178 mm of annual rainfall differed sharply in species composition from more mesic sites (> 200 mm). MAIN CONCLUSIONS Soil fertility and variability in temperature and rainfall are the most important environmental predictors of variation in plant beta diversity in global drylands. Our results suggest that those sites annually receiving ~ 178 mm of rainfall will be especially sensitive to future climate changes. These findings may help to define appropriate conservation strategies for mitigating effects of climate change on dryland vegetation.

Long‐term plant responses to climate are moderated by biophysical attributes in a North American desert

Summary 1. Recent elevated temperatures and prolonged droughts in many already water-limited regions throughout the world, including the southwestern United States, are likely to intensify according to future climate-model projections. This warming and drying can negatively affect perennial vegetation and lead to the degradation of ecosystem properties. 2. To better understand these detrimental effects, we formulate a conceptual model of dryland ecosystem vulnerability to climate change that integrates hypotheses on how plant species will respond to increases in temperature and drought, including how plant responses to climate are modified by landscape, soil and plant attributes that are integral to water availability and use. We test the model through a synthesis of fifty years of repeat measurements of perennial plant species cover in large permanent plots across the Mojave Desert, one of the most water-limited ecosystems in North America. 3. Plant species ranged in their sensitivity to precipitation in different seasons, capacity to increase in cover with high precipitation and resistance to decrease in cover with low precipitation. 4. Our model successfully explains how plant responses to climate are modified by biophysical attributes in the Mojave Desert. For example, deep-rooted plants were not as vulnerable to drought on soils that allowed for deep-water percolation, whereas shallow-rooted plants were better buffered from drought on soils that promoted water retention near the surface. 5. Synthesis. Our results emphasize the importance of understanding climate–vegetation relationships in the context of biophysical attributes that influence water availability and provide an important forecast of climate-change effects, including plant mortality and land degradation in dryland regions throughout the world.

Demographic consequences of greater clonal than sexual reproduction in Dicentra canadensis.

Abstract Clonality is a widespread life history trait in flowering plants that may be essential for population persistence, especially in environments where sexual reproduction is unpredictable. Frequent clonal reproduction, however, could hinder sexual reproduction by spatially aggregating ramets that compete with seedlings and reduce inter‐genet pollination. Nevertheless, the role of clonality in relation to variable sexual reproduction in population dynamics is often overlooked. We combined population matrix models and pollination experiments to compare the demographic contributions of clonal and sexual reproduction in three Dicentra canadensis populations, one in a well‐forested landscape and two in isolated forest remnants. We constructed stage‐based transition matrices from 3 years of census data to evaluate annual population growth rates, λ. We used loop analysis to evaluate the relative contribution of different reproductive pathways to λ. Despite strong temporal and spatial variation in seed set, populations generally showed stable growth rates. Although we detected some pollen limitation of seed set, manipulative pollination treatments did not affect population growth rates. Clonal reproduction contributed significantly more than sexual reproduction to population growth in the forest remnants. Only at the well‐forested site did sexual reproduction contribute as much as clonal reproduction to population growth. Flowering plants were more likely to transition to a smaller size class with reduced reproductive potential in the following year than similarly sized nonflowering plants, suggesting energy trade‐offs between sexual and clonal reproduction at the individual level. Seed production had negligible effects on growth and tuber production of individual plants. Our results demonstrate that clonal reproduction is vital for population persistence in a system where sexual reproduction is unpredictable. The bias toward clonality may be driven by low fitness returns for resource investment in sexual reproduction at the individual level. However, chronic failure in sexual reproduction may exacerbate the imbalance between sexual and clonal reproduction and eventually lead to irreversible loss of sex in the population.

Relative Performance of Non-Local Cultivars and Local, Wild Populations of Switchgrass (Panicum virgatum) in Competition Experiments.

The possibility of increased invasiveness in cultivated varieties of native perennial species is a question of interest in biofuel risk assessment. Competitive success is a key factor in the fitness and invasive potential of perennial plants, and thus the large-scale release of high-yielding biomass cultivars warrants empirical comparisons with local conspecifics in the presence of competitors. We evaluated the performance of non-local cultivars and local wild biotypes of the tallgrass species Panicum virgatum L. (switchgrass) in competition experiments during two growing seasons in Ohio and Iowa. At each location, we measured growth and reproductive traits (plant height, tiller number, flowering time, aboveground biomass, and seed production) of four non-locally sourced cultivars and two locally collected wild biotypes. Plants were grown in common garden experiments under three types of competition, referred to as none, moderate (with Schizachyrium scoparium), and high (with Bromus inermis). In both states, the two “lowland” cultivars grew taller, flowered later, and produced between 2x and 7.5x more biomass and between 3x and 34x more seeds per plant than local wild biotypes, while the other two cultivars were comparable to wild biotypes in these traits. Competition did not affect relative differences among biotypes, with the exception of shoot number, which was more similar among biotypes under high competition. Insights into functional differences between cultivars and wild biotypes are crucial for developing biomass crops while mitigating the potential for invasiveness. Here, two of the four cultivars generally performed better than wild biotypes, indicating that these biotypes may pose more of a risk in terms of their ability to establish vigorous feral populations in new regions outside of their area of origin. Our results support an ongoing assessment of switchgrass cultivars developed for large-scale planting for biofuels.

Population Genetics and Seed Set in Feral, Ornamental Miscanthus sacchariflorus

Ornamental grasses may become invasive weeds depending on their ability to naturalize and outcompete other species. Miscanthus sacchariflorus (Maxim) Franch. (Amur silvergrass) is a tall, self-incompatible, nonnative grass that has become naturalized in eastern North America, forming monospecific stands and raising concerns about its potential invasiveness. To understand the extent of clonal and sexual reproduction in feral populations, we examined their population genetic structure, seed production, and ploidy. We surveyed 21 populations in Iowa and Minnesota using eight polymorphic microsatellite markers. Only 34 multilocus genotypes (MLGs) were detected from a total of 390 samples. All of the study populations had more than one MLG, thereby allowing cross-pollination with near neighbors, but most were dominated by one or a few MLGs. Low genetic divergence suggests that all populations may have originated from similar cultivars. Cluster analysis showed that the six populations from Minnesota were extremely similar to each other, whereas the 15 populations from Iowa were somewhat more diverse. Seed production was quantified for 20 populations and ploidy for 11 populations. Average seed production was very low (< 0.30 seeds per panicle), although most populations did produce seeds. Because the populations were diploid (2x), they also may have the potential to hybridize with ornamental varieties of Miscanthus sinensis (Chinese silvergrass; eulaliagrass), a diploid close relative. Clonal growth, self-incompatibility, and spatial isolation of compatible clones may contribute to pollen-limited seed set in these populations. Low seed set may affect the rate of spread of feral M. sacchariflorus, which appears to disperse vegetatively as well as by seed. Although this species is not widely viewed as invasive, it is worth monitoring as a species that may become more widespread in the future. Nomenclature: Amur silvergrass, silver banner grass, Miscanthus sacchariflorus (Maxim.) Franch.; Chinese silvergrass, Miscanthus sinensis Anderss. Management Implications: Ornamental perennial grasses may have the potential to become invasive in areas where they can easily naturalize and disperse. In the nonnative genus Miscanthus, unwanted establishment of feral populations of ornamental M. sinensis (Chinese silvergrass) already has occurred in parklands and other areas, primarily in the eastern and southeastern United States. Its close relative, M. sacchariflorus (Amur silvergrass), also establishes feral populations, typically in more northern regions, but these stands are not as widespread as M. sinensis, nor do they produce abundant seeds. Low seed production could be a factor that limits population growth rates in feral M. sacchariflorus. The co-occurrence of genetically distinct individuals is a requirement for cross-pollination and seed set in this clonally reproducing, self-incompatible species. If several cross-compatible individuals occur in close proximity, this might lead to more abundant seed production and subsequent dispersal to other sites. In the current study, we found that feral populations of M. sacchariflorus in Iowa and Minnesota are genetically similar and highly clonal, but more than one genetic individual was present at each of our study sites. At present, we do not know whether M. sacchariflorus is in a temporary “lag phase” that precedes greater invasiveness. In any case, this tall, vigorously clonal perennial is able to establish extensive monospecific stands that crowd out other species, which is why managers of natural areas typically try to eradicate newly established populations. Ornamental plantings of M. sacchariflorus continue to be popular in northern areas of the United States and in southern Canada; this species is more cold tolerant than M. sinensis. The silvery inflorescences of M. sacchariflorus are attractive for landscaping, and the plant is easy to cultivate, but it has the potential to become a nuisance. Therefore, it is prudent to monitor the surrounding area for feral volunteers, which are much easier to eradicate at an early stage compared with after they have propagated clonally to form large stands along ditches, roadsides, wet meadows, and other areas.