Justine Karst

FERN COMMUNITY ASSEMBLY: THE ROLES OF CHANCE AND THE ENVIRONMENT AT LOCAL AND INTERMEDIATE SCALES

We evaluated the roles of the abiotic environment and dispersal in the as- sembly of fern communities at contrasting spatial scales within an old-growth, temperate deciduous forest. Specifically, we examined correlations among the geographic location of sampling plots separated by either 135-3515 m (mesoscale) or 4-134 m (fine scale), the abiotic environmental characteristics of the plots, and their constituent fern species. Ferns had predictable distributions along a soil moisture gradient at both spatial scales: six of eight common fern species showed repeatable environmental optima along the soil moisture gradient. By sampling in such a way as to decouple the correlation between distance and environmental variation, we showed the dominant role of environmental variables such as soil moisture in determining fern distributions at the mesoscale. At the fine scale, however, strong spatial autocorrelation in the abiotic environment precluded assigning any definitive role for either dispersal or environmental determinism alone in affecting fern distributions. The expectations of neutral theory that are rooted in dispersal limitation and those of niche theory that are rooted in environmental adaptation converge at fine spatial scales where natural environments have strong spatial structure. The structure of the environment at fine spatial scales may foster the persistence of dispersal-limited plants in the community; neighboring environments are likely to be similar, and thus suitable for propagules dis- persing short distances. While patterns of fern distribution in this locality are not consistent with purely neutral or random models of species coexistence, alternative models that rely on strict niche requirements without accounting for dispersal effects and the inherent spatial structure of the environment are inadequate because they neglect the important interaction of these factors. This outcome supports the relevance of developing theory that considers the joint effects of environmental determinism and dispersal on the distribution and abun- dance of plant species.

THE MUTUALISM–PARASITISM CONTINUUM IN ECTOMYCORRHIZAS: A QUANTITATIVE ASSESSMENT USING META‐ANALYSIS

Context dependency is deemed to position the outcomes of species interactions along a continuum of mutualism to parasitism. Thus, it is imperative to understand which factors determine where a particular interspecific interaction falls along the continuum. Over the past 20 years research on the ectomycorrhizal symbiosis has resulted in sufficient independent studies to now generalize about the factors and mechanisms that affect host response to ectomycorrhizas. Using meta-analysis we quantitatively evaluated the role of biotic (partner identity and colonization levels of ectomycorrhizal fungi) and abiotic (phosphorus levels) factors in determining host biomass, height, and shoot:root responses to ectomycorrhizal associations. On average, seedlings across multiple host genera increased in total biomass when inoculated with ectomycorrhizal fungi regardless of the identity of the fungal associate; host genera differed in the magnitude of response for both total biomass and shoot:root ratio. Association with different fungal genera modified only host allocation of biomass to shoots and roots. Neither level of colonization on inoculated seedlings nor the level of contamination on control seedlings relative to colonization levels by target fungi on inoculated seedlings was important in explaining variation in effect sizes for any growth response. None of our proposed factors (identity of partners, colonization level, magnitude of contamination, or duration of association) explained variation in effect sizes for shoot height, although in general seedlings were taller when inoculated with ectomycorrhizal fungi. Phosphorus additions did not influence effect sizes. Although the general trend across studies was for a positive response of hosts to ectomycorrhizal inoculation, publication bias and methodological issues effectively reduce and distort the spectrum on which we evaluate host responses to ectomycorrhizal inoculation. Our results indicate that the variation in ectomycorrhizal fungi perceived by the host may be of a discrete (presence/absence of ectomycorrhizal fungi) rather than continuous nature (variation in identity or abundance of ectomycorrhizal fungi).

Home-field advantage? evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis

BackgroundLocal adaptation, the differential success of genotypes in their native versus foreign environment, arises from various evolutionary processes, but the importance of concurrent abiotic and biotic factors as drivers of local adaptation has only recently been investigated. Local adaptation to biotic interactions may be particularly important for plants, as they associate with microbial symbionts that can significantly affect their fitness and may enable rapid evolution. The arbuscular mycorrhizal (AM) symbiosis is ideal for investigations of local adaptation because it is globally widespread among most plant taxa and can significantly affect plant growth and fitness. Using meta-analysis on 1170 studies (from 139 papers), we investigated the potential for local adaptation to shape plant growth responses to arbuscular mycorrhizal inoculation.ResultsThe magnitude and direction for mean effect size of mycorrhizal inoculation on host biomass depended on the geographic origin of the soil and symbiotic partners. Sympatric combinations of plants, AM fungi, and soil yielded large increases in host biomass compared to when all three components were allopatric. The origin of either the fungi or the plant relative to the soil was important for explaining the effect of AM inoculation on plant biomass. If plant and soil were sympatric but allopatric to the fungus, the positive effect of AM inoculation was much greater than when all three components were allopatric, suggesting potential local adaptation of the plant to the soil; however, if fungus and soil were sympatric (but allopatric to the plant) the effect of AM inoculation was indistinct from that of any allopatric combinations, indicating maladaptation of the fungus to the soil.ConclusionsThis study underscores the potential to detect local adaptation for mycorrhizal relationships across a broad swath of the literature. Geographic origin of plants relative to the origin of AM fungal communities and soil is important for describing the effect of mycorrhizal inoculation on plant biomass, suggesting that local adaptation represents a powerful factor for the establishment of novel combinations of fungi, plants, and soils. These results highlight the need for subsequent investigations of local adaptation in the mycorrhizal symbiosis and emphasize the importance of routinely considering the origin of plant, soil, and fungal components.

Decline of ectomycorrhizal fungi following a mountain pine beetle epidemic

Forest die-off caused by mountain pine beetle (MPB; Dendroctonus ponderosa) is rapidly transforming western North American landscapes. The rapid and widespread death of lodgepole pine (Pinus contorta) will likely have cascading effects on biodiversity. One group particularly prone to such declines associated with MPB are ectomycorrhizal fungi, symbiotic organisms that can depend on pine for their survival, and are critical for stand regeneration. We evaluated the indirect effects of MPB on above- (community composition of epigeous sporocarps) and belowground (hyphal abundance) occurrences of ectomycorrhizal fungi across 11 forest stands. Along a gradient of mortality (0-82% pine killed), macromycete community composition changed; this shift was driven by a decrease in the species richness of ectomycorrhizal fungi. Both the proportion of species that were ectomycorrhizal and hyphal length in the soil declined with increased MPB-caused pine mortality; < 10% of sporocarp species were ectomycorrhizal in stands with high pine mortality compared with > 70% in stands without MPB attacks. The rapid range expansion of a native insect results not only in the widespread mortality of an ecologically and economically important pine species, but the effect of MPB may also be exacerbated by the concomitant decline of fungi crucial for recovery of these forests.

Rapid Increases in Forest Understory Diversity and Productivity following a Mountain Pine Beetle ( Dendroctonus ponderosae ) Outbreak in Pine Forests

The current unprecedented outbreak of mountain pine beetle (Dendroctonus ponderosae) in lodgepole pine (Pinus contorta) forests of western Canada has resulted in a landscape consisting of a mosaic of forest stands at different stages of mortality. Within forest stands, understory communities are the reservoir of the majority of plant species diversity and influence the composition of future forests in response to disturbance. Although changes to stand composition following beetle outbreaks are well documented, information on immediate responses of forest understory plant communities is limited. The objective of this study was to examine the effects of D. ponderosae-induced tree mortality on initial changes in diversity and productivity of understory plant communities. We established a total of 110 1-m2 plots across eleven mature lodgepole pine forests to measure changes in understory diversity and productivity as a function of tree mortality and below ground resource availability across multiple years. Overall, understory community diversity and productivity increased across the gradient of increased tree mortality. Richness of herbaceous perennials increased with tree mortality as well as soil moisture and nutrient levels. In contrast, the diversity of woody perennials did not change across the gradient of tree mortality. Understory vegetation, namely herbaceous perennials, showed an immediate response to improved growing conditions caused by increases in tree mortality. How this increased pulse in understory richness and productivity affects future forest trajectories in a novel system is unknown.

Ectomycorrhizal fungi mediate indirect effects of a bark beetle outbreak on secondary chemistry and establishment of pine seedlings

Dendroctonus ponderosae has killed millions of Pinus contorta in western North America with subsequent effects on stand conditions, including changes in light intensity, needle deposition, and the composition of fungal community mutualists, namely ectomycorrhizal fungi. It is unknown whether these changes in stand conditions will have cascading consequences for the next generation of pine seedlings. To test for transgenerational cascades on pine seedlings, we tested the effects of fungal inoculum origin (beetle-killed or undisturbed stands), light intensity and litter (origin and presence) on seedling secondary chemistry and growth in a glasshouse. We also tracked survival of seedlings over two growing seasons in the same stands from which fungi and litter were collected. Fungal communities differed by inoculum origin. Seedlings grown with fungi collected from beetle-killed stands had lower monoterpene concentrations and fewer monoterpene compounds present compared with seedlings grown with fungi collected from undisturbed stands. Litter affected neither monoterpenes nor seedling growth. Seedling survival in the field was lower in beetle-killed than in undisturbed stands. We demonstrate that stand mortality caused by prior beetle attacks of mature pines have cascading effects on seedling secondary chemistry, growth and survival, probably mediated through effects on below-ground mutualisms.

MycoDB, a global database of plant response to mycorrhizal fungi

Plants form belowground associations with mycorrhizal fungi in one of the most common symbioses on Earth. However, few large-scale generalizations exist for the structure and function of mycorrhizal symbioses, as the nature of this relationship varies from mutualistic to parasitic and is largely context-dependent. We announce the public release of MycoDB, a database of 4,010 studies (from 438 unique publications) to aid in multi-factor meta-analyses elucidating the ecological and evolutionary context in which mycorrhizal fungi alter plant productivity. Over 10 years with nearly 80 collaborators, we compiled data on the response of plant biomass to mycorrhizal fungal inoculation, including meta-analysis metrics and 24 additional explanatory variables that describe the biotic and abiotic context of each study. We also include phylogenetic trees for all plants and fungi in the database. To our knowledge, MycoDB is the largest ecological meta-analysis database. We aim to share these data to highlight significant gaps in mycorrhizal research and encourage synthesis to explore the ecological and evolutionary generalities that govern mycorrhizal functioning in ecosystems.

Ectomycorrhizal colonization and intraspecific variation in growth responses of lodgepole pine

Across different host plant species, the effects of mycorrhizal colonization on host growth parameters can vary, but intraspecific variation in this relationship has rarely been measured. We tested the direction and consistency of the relationship between ectomycorrhizal colonization level and growth responses across seed families of Pinus contorta var. latifolia. Root tips of seedlings from eight full sib seed families varied in levels of ectomycorrhizal fungal colonization from 39% to 100%. We observed positive, negative, or neutral relationships between colonization level and shoot mass, depending on plant family. For the majority of seed families no relationship was observed between colonization level and root mass; however, two seed families showed negative relationships. Shoot height differed only by seed family. Results from our study indicate that the relationship between colonization level and host growth depends on host genotype. We suggest that models of plant intraspecific interactions should consider ectomycorrhizal associations when assessing phenotypic variability.

No silver bullet: different soil handling techniques are useful for different research questions, exhibit differential type I and II error rates, and are sensitive to sampling intensity

The black box of soils has opened over the last decade, revealing critical microbe effects on plant growth, nutrient cycling, and community dynamics (Kardol et al., 2007; Hoeksema et al., 2010; Reinhart, 2012; Hodge & Fitter, 2013). In a recent issue of New Phytologist, Reinhart & Rinella (2016) highlight the importance of soil handling in experimental studies, and address the statistical implications of mixing soil samples from multiple experimental units (MSS) vs maintaining individual soil samples (ISS; Fig. 1 in Reinhart & Rinella, 2016). They use logical arguments and the results of a numerical simulation to support two statements:

Spatial Heterogeneity in Soil Microbes Alters Outcomes of Plant Competition

Plant species vary greatly in their responsiveness to nutritional soil mutualists, such as mycorrhizal fungi and rhizobia, and this responsiveness is associated with a trade-off in allocation to root structures for resource uptake. As a result, the outcome of plant competition can change with the density of mutualists, with microbe-responsive plant species having high competitive ability when mutualists are abundant and non-responsive plants having high competitive ability with low densities of mutualists. When responsive plant species also allow mutualists to grow to greater densities, changes in mutualist density can generate a positive feedback, reinforcing an initial advantage to either plant type. We study a model of mutualist-mediated competition to understand outcomes of plant-plant interactions within a patchy environment. We find that a microbe-responsive plant can exclude a non-responsive plant from some initial conditions, but it must do so across the landscape including in the microbe-free areas where it is a poorer competitor. Otherwise, the non-responsive plant will persist in both mutualist-free and mutualist-rich regions. We apply our general findings to two different biological scenarios: invasion of a non-responsive plant into an established microbe-responsive native population, and successional replacement of non-responders by microbe-responsive species. We find that resistance to invasion is greatest when seed dispersal by the native plant is modest and dispersal by the invader is greater. Nonetheless, a native plant that relies on microbial mutualists for competitive dominance may be particularly vulnerable to invasion because any disturbance that temporarily reduces its density or that of the mutualist creates a window for a non-responsive invader to establish dominance. We further find that the positive feedbacks from associations with beneficial soil microbes create resistance to successional turnover. Our theoretical results constitute an important first step toward developing a general understanding of the interplay between mutualism and competition in patchy landscapes, and generate qualitative predictions that may be tested in future empirical studies.