Prairie restoration promotes the abundance and diversity of mutualistic arbuscular mycorrhizal fungi.

Predicting how biological communities assemble in restored ecosystems can assist in conservation efforts, but most research has focused on plants, with relatively little attention paid to soil microbial organisms that plants interact with. Arbuscular mycorrhizal (AM) fungi are an ecologically significant functional group of soil microbes that form mutualistic symbioses with plants and could therefore respond positively to plant community restoration. To evaluate the effects of plant community restoration on AM fungi, we compared AM fungal abundance, species richness, and community composition of five annually cultivated, conventionally managed agricultural fields with paired adjacent retired agricultural fields that had undergone prairie restoration 5-9 years prior to sampling. We hypothesized that restoration stimulates AM fungal abundance and species richness, particularly for disturbance-sensitive taxa, and that gains of new taxa would not displace AM fungal species present prior to restoration due to legacy effects. AM fungal abundance was quantified by measuring soil spore density and root colonization. AM fungal species richness and community composition were determined in soils and plant roots using DNA high-throughput sequencing. Soil spore density was 2.3 times higher in restored prairies compared to agricultural fields, but AM fungal root colonization did not differ between land use types. AM fungal species richness was 2.7 and 1.4 times higher in restored prairies versus agricultural fields for soil and roots, respectively. The abundance of Glomeraceae, a disturbance-tolerant family, decreased by 25% from agricultural to restored prairie soils but did not differ in plant roots. The abundance of Claroideoglomeraceae and Diversisporaceae, both disturbance-sensitive families, was 4.6 and 3.2 times higher in restored prairie versus agricultural soils, respectively. Species turnover was higher than expected relative to a null model, indicating that AM fungal species were gained by replacement. Our findings demonstrate that restoration can promote a relatively rapid increase in the abundance and diversity of soil microbial communities that had been degraded by decades of intensive land use, and community compositional change can be predicted by the disturbance tolerance of soil microbial taxonomic and functional groups.

Independent evolutionary changes in fine-root traits among main clades during the diversification of seed plants.

Changes in fine-root morphology are typically associated with transitions from the ancestral arbuscular mycorrhizal (AM) to the alternative ectomycorrhizal (ECM) or nonmycorrhizal (NM) associations. However, the modifications in root morphology may also coincide with new modifications in leaf hydraulics and growth habit during angiosperm diversification. These hypotheses have not been evaluated concurrently, and this limits our understanding of the causes of fine-root evolution. To explore the evolution of fine-root systems, we assembled a 600+ species database to reconstruct historical changes in seed plants over time. We utilise ancestral reconstruction approaches together with phylogenetically informed comparative analyses to test whether changes in fine-root traits were most strongly associated with mycorrhizal affiliation, leaf hydraulics or growth form. Our findings showed significant shifts in root diameter, specific root length and root tissue density as angiosperms diversified, largely independent from leaf changes or mycorrhizal affiliation. Growth form was the only factor associated with fine-root traits in statistical models including mycorrhizal association and leaf venation, suggesting substantial modifications in fine-root morphology during transitions from woody to nonwoody habits. Divergences in fine-root systems were crucial in the evolution of seed plant lineages, with important implications for ecological processes in terrestrial ecosystems.

Population-level variation in host plant response to multiple microbial mutualists.

PREMISE: Multipartite mutualisms are widespread in nature, but population-level variation in these interactions is rarely quantified. In the model multipartite mutualism between legumes, arbuscular mycorrhizal (AM) fungi and rhizobia bacteria, host responses to microbial partners are expected to be synergistic because the nutrients provided by each microbe colimit plant growth, but tests of this prediction have not been done in multiple host populations. METHODS: To test whether plant response to associations with AM fungi and rhizobia varies among host populations and whether synergistic responses to microbial mutualists are common, we grew 34 Medicago truncatula populations in a factorial experiment that manipulated the presence or absence of each mutualist. RESULTS: Plant growth increased in response to each mutualist, but there were no synergistic effects. Instead, plant response to inoculation with AM fungi was an order of magnitude higher than with rhizobia. Plant response to AM fungi varied among populations, whereas responses to rhizobia were relatively uniform. There was a positive correlation between plant host response to each mutualist but no correlation between AM fungal colonization and rhizobia nodulation of plant roots. CONCLUSIONS: The greater population divergence in host response to AM fungi relative to rhizobia, weak correlation in host response to each microbial mutualist, and the absence of a correlation between measures of AM fungal and rhizobia performance suggests that each plant-microbe mutualism evolved independently among M. truncatula populations.

Endopolyploidy is associated with leaf functional traits and climate variation in Arabidopsis thaliana.

PREMISE: Endopolyploidy is widespread throughout the tree of life and is especially prevalent in herbaceous angiosperms. Its prevalence in this clade suggests that endopolyploidy may be adaptive, but its functional roles are poorly understood. To address this gap in knowledge, we explored whether endopolyploidy was associated with climatic factors and correlated with phenotypic traits related to growth. METHODS: We sampled stem and leaf endopolyploidy in 56 geographically separated accessions of Arabidopsis thaliana grown in a common garden to explore species variation and to determine whether this variation was correlated with climatic variables and other plant traits. RESULTS: Stem endopolyploidy was not associated with climate or other traits. However, leaf endopolyploidy was significantly higher in accessions from drier and colder environments. Moreover, leaf endopolyploidy was positively correlated with apparent chlorophyll content and leaf dry mass. CONCLUSIONS: Endopolyploidy may have a functional role in the storage of chloroplasts and starch, and it may offer an adaptive avenue of tissue growth in cold and dry environments.

Variation in mycorrhizal growth response influences competitive interactions and mechanisms of plant species coexistence.

Plant species vary in their growth response to arbuscular mycorrhizal (AM) fungi, with responses ranging from negative to positive. Differences in response to AM fungi may affect competition between plant species, influencing their ability to coexist. We hypothesized that positively responding species, whose growth is stimulated by AM fungi, will experience stronger intraspecific competition and weaker interspecific competition in soil containing AM fungi, while neutrally or negatively responding species should experience weaker intraspecific and stronger interspecific competition. We grew Plantago lanceolata, which responds positively to AM fungi, and Bromus inermis, which responds negatively to AM fungi, in an additive response surface competition experiment that varied the total density and relative frequency of each species. Plants were grown in sterilized background soil that had been inoculated with whole soil biota, which includes AM fungi, or a microbial wash, that contained other soil microbes but no AM fungi, or in sterilized soil that contained no biota. The positively responding P. lanceolata was more strongly limited by intraspecific than interspecific competition when AM fungi were present. By contrast, the presence of AM fungi decreased the strength of intraspecific competition experienced by the negatively responding B. inermis. Because AM fungi are almost always present in soil, strong intraspecific competition in positively responding species would prevent them from outcompeting species that respond neutrally or negatively to AM fungi. The potential for increased intraspecific competition to offset growth benefits of AM fungi could, therefore, be a stabilizing mechanism that promotes coexistence among plant species.

Vestured pits and scalariform perforation plate morphology modify the relationships between angiosperm vessel diameter, climate and maximum plant height.

Shared ancestry among species and correlation between vessel diameter and plant height can obscure the mechanisms linking vessel diameter to current climate distributions of angiosperms. Because wood is complex, various traits may interact to influence vessel function. Specifically, pit vesturing (lignified cell wall protuberances associated with bordered pits) and perforation plate morphology could alter the relationships between vessel diameter, climate and plant height. Using phylogenetically informed analyses, we tested for associations between vessel diameter, climate and maximum plant height across angiosperm species with different pit vesturing (presence/absence) and perforation plate morphology (simple/scalariform and quantitative variation). We show significantly larger changes in vessel diameter and maximum plant height across climates for species with vestures and simple perforation plates, compared to nonvestured species and those with scalariform plates. We also found a significantly greater increase in height for a given increase in vessel diameter with lower percentage of scalariform plates. Our study provides novel insights into the evolution of angiosperm xylem by showing that vessel pit vesturing and perforation plate morphologies can modify relationships among xylem vessels, climate and height. Our findings highlight the complexity of xylem adaptations to climate, substantiating an integrative view of xylem function in the study of wood evolution.

Local adaptation to mycorrhizal fungi in geographically close Lobelia siphilitica populations.

Mutualism between plants and arbuscular mycorrhizal (AM) fungi is common, and plant populations are expected to have adapted to the AM fungal communities occupying their roots. Tests of this hypothesis have frequently been done with plant populations that are tens to hundreds of kilometers apart. However, because AM fungal community composition differs at scales < 1 km, local adaptation of plant populations to AM fungi may occur at small spatial scales, but this prediction has not been tested. Furthermore, prior experiments do not often experimentally identify whether adaptation is related to specific mycorrhizal functions. To test for plant adaptation to AM fungal communities at small spatial scales, and whether adaptation is associated with the nutritional benefits that AM fungi provide to plants, we grew Lobelia siphilitica plants from two geographically close populations (1.4 km apart) in a greenhouse reciprocal transplant experiment with soil biota that either included (whole soil) or excluded AM fungi (microbial wash) at both low and high soil phosphorus availability. Though both plant populations responded positively to the presence of AM fungi in the whole soil biota treatment relative to the microbial wash treatment, the average growth response of plant populations to mycorrhizal fungi was highest when local populations were grown with local AM fungi. In addition, local adaptation was only observed in the presence of AM fungi at low phosphorus levels. Thus, local adaptation of plant populations to AM fungi is present at spatial scales that are much smaller than previously demonstrated and occurred primarily to enhance phosphorus acquisition.

Global convergence in the vulnerability of forests to drought.

Shifts in rainfall patterns and increasing temperatures associated with climate change are likely to cause widespread forest decline in regions where droughts are predicted to increase in duration and severity. One primary cause of productivity loss and plant mortality during drought is hydraulic failure. Drought stress creates trapped gas emboli in the water transport system, which reduces the ability of plants to supply water to leaves for photosynthetic gas exchange and can ultimately result in desiccation and mortality. At present we lack a clear picture of how thresholds to hydraulic failure vary across a broad range of species and environments, despite many individual experiments. Here we draw together published and unpublished data on the vulnerability of the transport system to drought-induced embolism for a large number of woody species, with a view to examining the likely consequences of climate change for forest biomes. We show that 70% of 226 forest species from 81 sites worldwide operate with narrow (<1 megapascal) hydraulic safety margins against injurious levels of drought stress and therefore potentially face long-term reductions in productivity and survival if temperature and aridity increase as predicted for many regions across the globe. Safety margins are largely independent of mean annual precipitation, showing that there is global convergence in the vulnerability of forests to drought, with all forest biomes equally vulnerable to hydraulic failure regardless of their current rainfall environment. These findings provide insight into why drought-induced forest decline is occurring not only in arid regions but also in wet forests not normally considered at drought risk.

Evolutionary asymmetry in the arbuscular mycorrhizal symbiosis: conservatism in fungal morphology does not predict host plant growth.

Although arbuscular mycorrhizal (AM) fungi are obligate symbionts that can influence plant growth, the magnitude and direction of these effects are highly variable within fungal genera and even among isolates within species, as well as among plant taxa. To determine whether variability in AM fungal morphology and growth is correlated with AM fungal effects on plant growth, we established a common garden experiment with 56 AM fungal isolates comprising 17 genera and six families growing with three plant host species. Arbuscular mycorrhizal fungal morphology and growth was highly conserved among isolates of the same species and among species within a family. By contrast, plant growth response to fungal inoculation was highly variable, with the majority of variation occurring among different isolates of the same AM fungal species. Our findings show that host performance cannot be predicted from AM fungal morphology and growth traits. Divergent effects on plant growth among isolates within an AM fungal species may be caused by coevolution between co-occurring fungal and plant populations.

Arbuscular mycorrhizal fungi alter the competitive hierarchy among old-field plant species.

Inoculation with arbuscular mycorrhizal (AM) fungi is known to increase the species diversity of plant communities. One mechanism that can increase the likelihood of species co-existence, and thus species diversity, is a trade-off between competitive ability and the magnitude of plant growth response to AM fungal inoculation. By suppressing the growth of strong competitors while simultaneously enhancing the growth of weak competitors, this trade-off would cause the competitive hierarchy to be less pronounced in soil inoculated with AM fungi relative to non-inoculated conditions. To test whether such a trade-off exists, we quantified competitive abilities and mycorrhizal growth response (MGR) among 21 species that co-occur in old fields in southern Ontario. Competitive ability was determined by calculating competitive effect (CE), or the degree to which each species suppressed the biomass of a common phytometer species, Plantago lanceolata. Higher CE values represent stronger competitive ability. Old-field species varied in their ability to suppress the biomass of the phytometer and MGR was generally positive. There was a statistically significant negative correlation between CE in non-inoculated soil and MGR (r = -0.49, P = 0.02). In addition, variance in CE was 73% lower in soil inoculated with AM fungi compared to non-inoculated soil (P = 0.0023). These findings support the hypothesis that AM fungi weaken strong competitors while enhancing the performance of weak competitors. Because this trade-off compressed the competitive hierarchy among old-field species in soil inoculated with AM fungi, it may be a mechanism by which mycorrhizal fungi enhance species evenness and diversity.

Mutualism Persistence and Abandonment during the Evolution of the Mycorrhizal Symbiosis.

Mutualistic symbioses with mycorrhizal fungi are widespread in plants. The majority of plant species associate with arbuscular mycorrhizal (AM) fungi. By contrast, the minority associate with ectomycorrhizal (EM) fungi, have abandoned the symbiosis and are nonmycorrhizal (NM), or engage in an intermediate, weakly AM symbiosis (AMNM). To understand the processes that maintain the mycorrhizal symbiosis or cause its loss, we reconstructed its evolution using a ∼3,000-species seed plant phylogeny integrated with mycorrhizal state information. Reconstruction indicated that the common ancestor of seed plants most likely associated with AM fungi and that the EM, NM, and AMNM states descended from the AM state. Direct transitions from the AM state to the EM and NM states were infrequent and generally irreversible, implying that natural selection or genetic constraint could promote stasis once a particular state evolved. However, the evolution of the NM state was more frequent via an indirect pathway through the AMNM state, suggesting that weakening of the AM symbiosis is a necessary precursor to mutualism abandonment. Nevertheless, reversions from the AMNM state back to the AM state were an order of magnitude more likely than transitions to the NM state, suggesting that natural selection favors the AM symbiosis over mutualism abandonment.

Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species.

The evolution of lignified xylem allowed for the efficient transport of water under tension, but also exposed the vascular network to the risk of gas emboli and the spread of gas between xylem conduits, thus impeding sap transport to the leaves. A well-known hypothesis proposes that the safety of xylem (its ability to resist embolism formation and spread) should trade off against xylem efficiency (its capacity to transport water). We tested this safety-efficiency hypothesis in branch xylem across 335 angiosperm and 89 gymnosperm species. Safety was considered at three levels: the xylem water potentials where 12%, 50% and 88% of maximal conductivity are lost. Although correlations between safety and efficiency were weak (r(2)  < 0.086), no species had high efficiency and high safety, supporting the idea for a safety-efficiency tradeoff. However, many species had low efficiency and low safety. Species with low efficiency and low safety were weakly associated (r(2)  < 0.02 in most cases) with higher wood density, lower leaf- to sapwood-area and shorter stature. There appears to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge for understanding the evolution of xylem.

Phylogenetic conservatism in plant-soil feedback and its implications for plant abundance.

We examined whether plant-soil feedback and plant-field abundance were phylogenetically conserved. For 57 co-occurring native and exotic plant species from an old field in Canada, we collected a data set on the effects of three soil biota treatments on plant growth: net whole-soil feedback (combined effects of mutualists and antagonists), feedback with arbuscular mycorrhizal fungi (AMF) collected from soils of conspecific plants, and feedback with Glomus etunicatum, a dominant mycorrhizal fungus. We found phylogenetic signal in both net whole-soil feedback and feedback with AMF of conspecifics; conservatism was especially strong among native plants but absent among exotics. The abundance of plants in the field was also conserved, a pattern underlain by shared plant responses to soil biota. We conclude that soil biota influence the abundance of close plant relatives in nature.

Is there an association between root architecture and mycorrhizal growth response?

The symbiosis between arbuscular mycorrhizal (AM) fungi and plants is evolutionarily widespread. The response of plant growth to inoculation by these fungi (mycorrhizal growth response; MGR) is highly variable, ranging from positive to negative. Some of this variation is hypothesized to be associated with root structure and function. Specifically, species with a coarse root architecture, and thus a limited intrinsic capacity to absorb soil nutrients, are expected to derive the greatest growth benefit from inoculation with AM fungi. To test this hypothesis, previously published literature and phylogenetic information were combined in a meta-analysis to examine the magnitude and direction of relationships among several root architectural traits and MGR. Published studies differed in the magnitude and direction of relationships between root architecture and MGR. However, when combined, the overall relationship between MGR and allocation to roots, root diameter, root hair length and root hair density did not differ significantly from zero. These findings indicate that possessing coarse roots is not necessarily a predictor of plant growth response to AM fungal colonization. Root architecture is therefore unlikely to limit the evolution of variation in MGR.

Climatic niche differences between diploid and tetraploid cytotypes of Chamerion angustifolium (Onagraceae).

PREMISE OF THE STUDY: Polyploidy-the possession of more than two copies of each chromosome in the nucleus-is common in flowering plants. Polyploid plants can occupy different geographic ranges than their diploid progenitors, but the factors responsible for maintaining these range differences are poorly understood. Polyploidy can have significant physiological consequences, and the present study aims to determine whether previously described physiological differences between cytotypes are correlated with climatic niches and geographic distributions. METHODS: Prior research indicates that tetraploid plants of Chamerion angustifolium (Onagraceae) are more tolerant of drought and less tolerant of freezing than diploids, which suggests that they should occupy a niche that is warmer and drier than that of diploids. We extracted climate data for 134 populations of C. angustifolium classified as pure diploid, pure tetraploid, or mixed-ploidy. We compared climatic conditions between these population categories and generated ecological niche models to compare their geographic distribution with prior qualitative estimates. KEY RESULTS: Pure tetraploid populations occupy habitats that are warmer and drier than those of pure diploid populations. Mixed-ploidy populations occur in habitats that are not strictly intermediate between pure diploid and pure tetraploid populations, but are as cold as pure diploid populations and have intermediate soil moisture deficits. Our niche models were similar to previous qualitative estimates of cytotype geographic distribution. CONCLUSIONS: The correspondence between the physiological tolerances of cytotypes, their climatic niches, and their geographic distributions suggests that physiological traits are at least partially responsible for differences in the realized climatic niches of diploid and tetraploid C. angustifolium.

The effect of endophyte presence on Schedonorus arundinaceus (tall fescue) establishment varies with grassland community structure.

The endophyte Neotyphodium coenophialum in Schedonorus arundinaceus (tall fescue) may alter host interactions with specific resident species or shift the host's niche. These effects can be quantified by assessing tall fescue responses to, and effects on, the variation among resident species (selection) and resident species interactions (complementarity). To determine how N. coenophialum affects tall fescue, grassland microcosms containing 16 transplants of two, four, or eight resident species were seeded with endophyte-infected (E+) or endophyte-free (E-) Kentucky-31 (KY-31) tall fescue. All resident species were also grown in monoculture. Aboveground biomass was harvested 9 weeks after tall fescue was added (18 weeks' total growth). At harvest, more E+ than E- individuals were present and they represented a larger portion of the aboveground biomass across richness treatments, despite similar germination in concurrent trials. Tall fescue individuals were larger in microcosms dominated by more productive resident species (greater selection). In contrast, fewer E-, but not E+, individuals were present in microcosms with more facilitative interactions among the resident species (greater complementarity). E- and E+ tall fescue also affected resident species differently. High-richness E+ microcosms were more diverse and less dominated by productive species (lower selection) than E- microcosms. Thus, E+ KY-31 may more readily establish in, and affect, species-rich, functionally diverse communities as a result of niche shifts during establishment and negative effects on specific resident species. Although results need to be further tested under field conditions, it appears that endophyte presence may only facilitate KY-31 invasion into a limited suite of community types.

Mycorrhizal fungal growth responds to soil characteristics, but not host plant identity, during a primary lacustrine dune succession.

Soil factors and host plant identity can both affect the growth and functioning of mycorrhizal fungi. Both components change during primary succession, but it is unknown if their relative importance to mycorrhizas also changes. This research tested how soil type and host plant differences among primary successional stages determine the growth and plant effects of arbuscular mycorrhizal (AM) fungal communities. Mycorrhizal fungal community, plant identity, and soil conditions were manipulated among three stages of a lacustrine sand dune successional series in a fully factorial greenhouse experiment. Late succession AM fungi produced more arbuscules and soil hyphae when grown in late succession soils, although the community was from the same narrow phylogenetic group as those in intermediate succession. AM fungal growth did not differ between host species, and plant growth was similarly unaffected by different AM fungal communities. These results indicate that though ecological filtering and/or adaptation of AM fungi occurs during this primary dune succession, it more strongly reflects matching between fungi and soils, rather than interactions between fungi and host plants. Thus, AM fungal performance during this succession may not depend directly on the sequence of plant community succession.

The welfare problems of wide-ranging Carnivora reflect naturally itinerant lifestyles.

Carnivora with naturally small home ranges readily adjust to the evolutionarily new environment of captivity, but wider-ranging species seem prone to stress. Understanding why would advance both collection planning and enclosure design. We therefore investigated which aspects of wide-ranging lifestyles are key. We identified eight correlates of home range size (reflecting energetic needs, movement, intra-specific interactions, and itinerant lifestyles). We systematically assessed whether these correlates predict welfare better than range size per se, using data on captive juvenile mortality (from 13 518 individuals across 42 species) and stereotypic route-tracing (456 individuals, 27 species). Naturally itinerant lifestyles (quantified via ratios of daily to annual travel distances) were found to confer risk, predicting greater captive juvenile losses and stereotypic time-budgets. This finding advances our understanding of the evolutionary basis for welfare problems in captive Carnivora, helping explain why naturally sedentary species (e.g. American mink) may breed even in intensive farm conditions, while others (e.g. polar bears, giant pandas) can struggle even in modern zoos and conservation breeding centres. Naturally itinerant lifestyles involve decision-making, and strategic shifts between locations, suggesting that supplying more novelty, cognitive challenge and/or opportunities for control will be effective ways to meet these animals' welfare needs in captivity.