Brenda B. Casper

Plant-soil feedbacks: The past, the present and future challenges

Summary Plant–soil feedbacks is becoming an important concept for explaining vegetation dynamics, the invasiveness of introduced exotic species in new habitats and how terrestrial ecosystems respond to global land use and climate change. Using a new conceptual model, we show how critical alterations in plant–soil feedback interactions can change the assemblage of plant communities. We highlight recent advances, define terms and identify future challenges in this area of research and discuss how variations in strengths and directions of plant–soil feedbacks can explain succession, invasion, response to climate warming and diversity-productivity relationships. While there has been a rapid increase in understanding the biological, chemical and physical mechanisms and their interdependencies underlying plant–soil feedback interactions, further progress is to be expected from applying new experimental techniques and technologies, linking empirical studies to modelling and field-based studies that can include plant–soil feedback interactions on longer time scales that also include long-term processes such as litter decomposition and mineralization. Significant progress has also been made in analysing consequences of plant–soil feedbacks for biodiversity-functioning relationships, plant fitness and selection. To further integrate plant–soil feedbacks into ecological theory, it will be important to determine where and how observed patterns may be generalized, and how they may influence evolution. Synthesis. Gaining a greater understanding of plant–soil feedbacks and underlying mechanisms is improving our ability to predict consequences of these interactions for plant community composition and productivity under a variety of conditions. Future research will enable better prediction and mitigation of the consequences of human-induced global changes, improve efforts of restoration and conservation and promote sustainable provision of ecosystem services in a rapidly changing world.

Diversity of ageing across the tree of life

Evolution drives, and is driven by, demography. A genotype moulds its phenotype’s age patterns of mortality and fertility in an environment; these two patterns in turn determine the genotype’s fitness in that environment. Hence, to understand the evolution of ageing, age patterns of mortality and reproduction need to be compared for species across the tree of life. However, few studies have done so and only for a limited range of taxa. Here we contrast standardized patterns over age for 11 mammals, 12 other vertebrates, 10 invertebrates, 12 vascular plants and a green alga. Although it has been predicted that evolution should inevitably lead to increasing mortality and declining fertility with age after maturity, there is great variation among these species, including increasing, constant, decreasing, humped and bowed trajectories for both long- and short-lived species. This diversity challenges theoreticians to develop broader perspectives on the evolution of ageing and empiricists to study the demography of more species.

Coordinated distributed experiments: an emerging tool for testing global hypotheses in ecology and environmental science

There is a growing realization among scientists and policy makers that an increased understanding of todays environmental issues requires international collaboration and data synthesis. Meta-analyses have served this role in ecology for more than a decade, but the different experimental methodologies researchers use can limit the strength of the meta-analytic approach. Considering the global nature of many environmental issues, a new collaborative approach, which we call coordinated distributed experiments (CDEs), is needed that will control for both spatial and temporal scale, and that encompasses large geographic ranges. Ecological CDEs, involving standardized, controlled protocols, have the potential to advance our understanding of general principles in ecology and environmental science.

INTRASPECIFIC AM FUNGAL VARIATION CONTRIBUTES TO PLANT-FUNGAL FEEDBACK IN A SERPENTINE GRASSLAND

Feedback between plants and arbuscular mycorrhizal (AM) fungi can affect species diversity in plant and fungal communities. Feedback depends on (1) some specificity between plants and fungi and (2) fungi exhibiting specificity either improving (positive feedback) or decreasing (negative feedback) host performance relative to other fungi. Associations between AM fungi and plant species in a serpentine grassland dominated by Andropogon gerardii, Schizachyrium scoparium, Sorghastrum nutans, and Sporobolus heterolepis were examined, and their performance consequences were evaluated. Specificity was determined from AM fungal spore abundance under plants in the field and from trap cultures established by inoculating greenhouse plants with field-collected roots containing fungal material. Seven AM fungal species were unevenly distributed among plant species, with differences in total spore numbers and evenness. In the field, Gigaspora gigantea exhibited specificity to Sporobolus compared to Andropogon and Sorgha...

Demographic consequences of drought in the herbaceous perennial Cryptantha flava : effects of density, associations with shrubs, and plant size

The demographic consequences of a severe drought year were examined for two experimental plantings of the herbaceous desert perennial Cryptantha flava(Boraginaceae) in northeastern Utah, United States. A total of 6680 nutlets were planted individually or in clusters of four both under shrubs and in open microhabitats within two natural populations. Survival, growth, and flowering as a function of density and microhabitat were followed for 7 years, including 1 year when precipitation just before and during the growing season was 74.5% below normal. The design permitted assessment of how intraspecific density and shrub cover affect demographic response to drought. Mortality increased and flowering decreased dramatically during drought but neither varied with density or between shrub and open microhabitats. For plants growing under shrubs, survival (at Site 1) and growth (at Site 2) varied with shrub species. Average aboveground plant size also decreased during drought. Population size hierarchies were rearranged because larger plants lost leaf rosettes while many smaller plants grew. Density and microhabitat affected plant performance in non-drought years but more often at Site 1 than at Site 2. Individuals growing alone often were more likely to flower and/or produced more inflorescences when they did flower than did individuals growing with at least one other plant. However, for 2 years, survival rates at Site 1 were higher for plants growing in clumps than for single individuals. Shrubs also had mixed effects on plant performance. In some years, survival was higher under shrubs, but at Site 1 plants in the open often were more likely to flower and/or produced more inflorescences. Thus despite severe demographic consequences of drought, the study provided no evidence that intraspecific competition, interference by shrubs, or facilitation by shrubs increases under limited soil water.

THE HERBIVORY UNCERTAINTY PRINCIPLE: VISITING PLANTS CAN ALTER HERBIVORY

In 1927, Werner Heisenberg proposed that there are fundamental limitations to the study of subatomic particles, as the act of measuring them affects their behavior. Here we show that experimenter-induced uncertainty also applies in plant ecology, with potentially dramatic consequences for field biologists. We tested whether the simple act of visiting marked plants once per week for eight weeks influenced the intensity of herbivory experienced by six plant species in an old field community. Half of the plants were touched once per week to simulate taking morphological measures, while the other half were left undisturbed (neither visited nor touched). After eight weeks, visitation resulted in (1) decreased leaf damage by insects on one species, (2) increased leaf damage on a second species, (3) a marginally significant increase in survival for a third species, and (4) no effect on the remaining three species. These results serve as an important reminder that seemingly benign experimental methods may themselves dramatically affect the performance of experimental subjects. Our results raise concern about studies that use repeated visitation of focal plants either to compare rates of herbivory among species or to investigate some factor that can either directly or indirectly be influenced by the rate of herbivory (e.g., seed production, competition, etc.). Since the six species in our study responded differently to visitation, visitation effects must be accounted for in the design of future field experiments.

Differential host plant performance as a function of soil arbuscular mycorrhizal fungal communities: experimentally manipulating co-occurring Glomus species

In order to evaluate host plant performance relative to different soil arbuscular mycorrhizal fungal (AMF) communities, Andropogon gerardii seedlings were grown with nine different AMF communities. The communities consisted of 0, 10, or 20 spores of Glomus etunicatum and 0, 10, or 20 spores of Glomus intraradices in all possible combinations. Spores were produced by fungal cultures originating on A. gerardii in a serpentine plant community; seeds of A. gerardii were collected at the same site. The experiment was performed in the greenhouse using a mixture of sterilized serpentine soil and sand to which naturally occurring non-mycorrhizal microbes were added. There was no difference in root AMF colonization rates between single species communities of either G. etunicatum or G. intraradices, but G. intraradices enhanced plant growth and G. etunicatum did not. However, plants grew larger with some combinations of G.␣intraradices plus G. etunicatum than with the same quantity of G. intraradices alone. These results suggest the potential for niche complementarity in the mycorrhizal fungi. That G. etunicatum only increased plant growth in the presence of G. intraradices could be illustrative of why AMF that appear to be parasitic or benign when examined in isolation are maintained within multi-species mycorrhizal communities in nature.

Plant response to climate change varies with topography, interactions with neighbors, and ecotype

Predicting the future of any given species represents an unprecedented challenge in light of the many environmental and biological factors that affect organismal performance and that also interact with drivers of global change. In a three-year experiment set in the Mongolian steppe, we examined the response of the common grass Festuca lenensis to manipulated temperature and water while controlling for topographic variation, plant-plant interactions, and ecotypic differentiation. Plant survival and growth responses to a warmer, drier climate varied within the landscape. Response to simulated increased precipitation occurred only in the absence of neighbors, demonstrating that plant-plant interactions can supersede the effects of climate change. F. lenensis also showed evidence of local adaptation in populations that were only 300 m apart. Individuals from the steep and dry upper slope showed a higher stress/drought tolerance, whereas those from the more productive lower slope showed a higher biomass production and a greater ability to cope with competition. Moreover, the response of this species to increased precipitation was ecotype specific, with water addition benefiting only the least stress-tolerant ecotype from the lower slope origin. This multifaceted approach illustrates the importance of placing climate change experiments within a realistic ecological and evolutionary framework. Existing sources of variation impacting plant performance may buffer or obscure climate change effects.

Plant-soil feedback: testing the generality with the same grasses in serpentine and prairie soils

Plants can alter soil properties in ways that feed back to affect plant performance. The extent that plant-soil feedback affects co-occurring plant species differentially will determine its impact on plant community structure. Whether feedback operates consistently across similar plant communities is little studied. Here, the same grasses from two eastern U.S. serpentine grasslands and two midwestern tallgrass prairie remnants were examined for plant-soil feedback in parallel greenhouse experiments. Native soils were homogenized and cultured (trained) for a year with each of the four grasses. Feedback was evaluated by examining biomass variation in a second generation of (tester) plants grown in the trained soils. Biomass was lower in soils trained by conspecifics compared to soils trained by heterospecifics in seven of 15 possible cases; biomass was greater in conspecific soils in one other. Sorghastrum nutans exhibited lower biomass in conspecific soils for all four grasslands, so feedback may be characteristic of this species. Three cases from the Hayden prairie site were explained by trainer species having similar effects across all tester species so the relative performance of the different species was little affected; plants were generally larger in soils trained by Andropogon gerardii and smaller in soils trained by S. nutans. Differences among sites in the incidence of feedback were independent of serpentine or prairie soils. To explore the causes of the feedback, several soil factors were measured as a function of trainer species: nutrients and pH, arbuscular mycorrhizal (AM) spore communities, root colonization by AM fungi and putative pathogens, and functional diversity in bacterial communities as indicated by carbon substrate utilization. Only variation in nutrients was consistent with any patterns of feedback, and this could explain the greater biomass in soils trained by A. gerardii at Hayden. Feedback at Nottingham (one of the serpentine sites) differed, most notably for A. gerardii, from that of similar past studies that used different experimental protocols. To understand the consequences of feedback for plant community structure, it is important to consider how multiple species respond to the same plant-induced soil variation as well as differences in the feedback detected between greenhouse and field settings.

Population-level responses to nutrient heterogeneity and density by Abutilon theophrasti (Malvaceae): an experimental neighborhood approach

An experimental approach was used to examine the effects of spatial nutrient heterogeneity and planting density on the sizes of plants within populations of Abutilon theophrasti. Planting locations were generated using random numbers and replicated among populations growing on two different scales of heterogeneity and homogeneous soils. The same quantity of nutrients (dehydrated cow manure) was added to each population, regardless of the spatial nutrient distribution. The higher density was achieved by adding additional planting locations to those present at the lower density. Plant biomass was compared among ten planting locations present in all populations. Plants in seven locations were smaller at the higher density, but the spatial distribution of nutrients affected plant size in only two locations. At the population level, the higher density reduced mean plant biomass and increased both total biomass and the coefficient of variation in biomass, a measure of size inequality. Only when populations on both scales of heterogeneity were together compared with those on homogeneous soils were population-level measurements found to be significantly affected by soil treatment; heterogeneity resulted in decreased total biomass and an increase in the coefficient of variation, apparently due to an increase in the number of small plants in the population. These results, together with the finding that fine root biomass increased in nutrient-enriched patches, suggest that on heterogeneous soils most plants were able to access nutrient patches.