Catherine A. Zabinski

MYCORRHIZAE INDIRECTLY ENHANCE COMPETITIVE EFFECTS OF AN INVASIVE FORB ON A NATIVE BUNCHGRASS

Mycorrhizae are important mediators of plant competition, but little is known about the role of mycorrhizae in the intense competitive effects that exotic plants can have on native species. In the greenhouse, we tested the effect of arbuscular mycorrhizal (AM) fungi on interspecific competition between Cerztaur-ea maculosu and Fest~ccu idahoensis, on intraspecific competition between individuals of both species, and the growth of C. rnac~closawith either inorganic or organic phosphorus. Mycorrhizae had no direct effect on either species, but mycorrhizae increased C. maculosas negative effect on F. iduhoe~zsis. When competing with C. rnac-ulosa, nonmycorrhizal F. idahoensis were 171% larger than they were when mycorrhizae were present. In a second experiment, C. maculosa grown with larger F. idahoe~zsis were 66% larger, in the presence of AM fungi, than when AM fungi were absent. Centaurea maculosu biomass was not affected by AM fungi, in either phosphorus treatment, in the absence of F. idahoensis. Root: shoot ratios differed between phosphorus treatments, but this difference seemed to be a result of slower growth in the organic phosphorus treatment. Our results were unusual in that the direct effects of my- corrhizae on both species were weak, but the indirect effect of AM fungi on the interactions between C. muc~tlosa and F. idahoerzsis was strong. Our results suggest that AM fungi strongly enhance the ability of C. ~naculosa to invade native grasslands of western North America. Key ~.ord.~: nrb~isclllcir rrrycoi-rhieal (AM) ,fuizgi; Centaurea maculosa; conzperition; exotic plants; Festuca idahoensis; interi7lor~tanr, gra.sslunris; iiz~,a.sion; mycorrhizae. ~~~~~~~~i~~~ between pairs of speciesare often me- diated by other species (Kareiva 1994, Miller 1994). Well documented indirect interactions include those be- tween sea otters, kelp and sea urchins 19781, starfish, molluscs and algae (Paine 1966),parasitic and autotrophic plants (Pennings and Callaway 1996), plants and soil microflora, (van der Putten et al, 1993. Bever 1994) and plants and mycorrhizal fungi (Grime

SOIL FUNGI AND THE EFFECTS OF AN INVASIVE FORB ON GRASSES: NEIGHBOR IDENTITY MATTERS

We studied the effects of soil fungi on interactions between Centaurea mel- itensis, an exotic invasive weed in central California, and two co-occurring grasses, Nassella pulchra and Avena barbata. The fungicide benomyl reduced the abundance of arbuscular mycorrhizal (AM) fungi in plant roots but did not affect non-AM fungi. Centaurea plants grown alone were >50% smaller with the resident microbial community intact than when benomyl was applied. When grown with Nassella, the effect of benomyl was reversed. Centaurea grew almost five times larger with the resident microbial community intact. Fungicide had no effect on the biomass of Centaurea grown with Avena, but biomass of Centaurea was significantly lower when grown with Avena than when grown with Nassella or alone. Photosynthetically fixed carbon may have been transferred from Nassella via soil fungi to Centaurea, constituting a form of soil fungi-mediated parasitism, but such a transfer did not occur from Avena to Centaurea. Second, Nassella may have been more inhibited by soil pathogens in the presence of Centaurea than when alone, and the inhibition of Nassella may have released Centaurea from competition. A third possibility is that Nassella has strong positive effects on the growth of soil fungi, but the positive feedback of beneficial soil fungi to Nassella is less than the positive feedback to Centaurea. Regardless of the mechanism, the difference in soil fungicide treatment effects on competition between Cen- taurea and Nassella vs. Centaurea and Avena has important implications for the invasion of California grasslands.

Arbuscular mycorrhizal fungi ameliorate temperature stress in thermophilic plants.

Biotic interactions can affect the distribution of species across environmental gradients, and as air and soil temperatures increase, plant community response may depend on interactions with symbionts. We measured the effect of elevated soil temperatures on mycorrhizal function and on the response of both plant and fungal symbionts, using fungal inoculum isolated from either high-temperature thermal or nonthermal grassland soils. Our source for thermal soils was Yellowstone National Park, USA, where plants experience rooting zone temperatures of 45 degrees C or more. In the greenhouse, we grew three plant species (Dichanthelium lanuginosum, Agrostis scabra, and Mimulus guttatus) with three arbuscular mycorrhizal fungal (AMF) treatments (no AMF, nonthermal AMF, thermal AMF) and two soil temperatures (ambient, elevated). Biomass of the facultative thermal plants Agrostis scabra and Mimulus guttatus decreased by 50% in elevated-temperature soils, and AMF had no effect on measured plant traits. In contrast, the biomass and total root length of the obligate thermal plant Dichanthelium lanuginosum were greater at elevated soil temperatures, but only when mycorrhizal. Both mycorrhizal colonization levels and length of extraradical hyphae (ERH) increased with soil temperature across all host species. The source of the AMF inoculum, on the other hand, did not affect colonization level, ERH length, host plant biomass, or flowering for all host species in either temperature treatment, suggesting that AMF from thermal soils are not specifically adapted to higher temperatures. In the field we collected soil cores to measure in situ depth distributions of D. lanuginosum roots and ERH, and to determine which AMF species were active in plants growing in thermal soils. Roots were limited to soils with an average temperature < or =30 degrees C, while ERH existed in the hottest soils we sampled, averaging 35 degrees C. Molecular analyses of roots indicated that thermal AMF communities were composed of both generalist and possibly unique fungal species. The increase in host plant allocation to AMF, apparent lack of temperature adaptation by AMF, and differential host response to AMF suggest that AMF could be significant drivers of plant community response to increased soil temperature associated with global change.

From Lilliput to Brobdingnag: Extending Models of Mycorrhizal Function across Scales

ABSTRACT Mycorrhizae occur in nearly all terrestrial ecosystems. Resource exchange between host plants and mycorrhizal fungi influences community, ecosystem, and even global patterns and processes. Understanding the mechanisms and consequences of mycorrhizal symbioses across a hierarchy of scales will help predict system responses to environmental change and facilitate the management of these responses for sustainability and productivity. Conceptual and mathematical models have been developed to help understand and predict mycorrhizal functions. These models are most developed for individual- and population-scale processes, but models at community, ecosystem, and global scales are also beginning to emerge. We review seven types of mycorrhizal models that vary in their scale of resolution and dynamics, and discuss approaches for integrating these models with each other and with general models of terrestrial ecosystems.

Importance of dispersal and thermal environment for mycorrhizal communities: lessons from Yellowstone National Park

The relative importance of dispersal and niche restrictions remains a controversial topic in community ecology, especially for microorganisms that are often assumed to be ubiquitous. We investigated the impact of these factors for the community assembly of the root-symbiont arbuscular mycorrhizal fungi (AMF) by sampling roots from geothermal and nonthermal grasslands in Yellowstone National Park (YNP), followed by sequencing and RFLP of AMF ribosomal DNA. With the exception of an apparent generalist RFLP type closely related to Glomus intraradices, a distance-based redundancy analysis indicated that the AMF community composition correlated with soil pH or pH-driven changes in soil chemistry. This was unexpected, given the large differences in soil temperature and plant community composition between the geothermal and nonthermal grasslands. RFLP types were found in either the acidic geothermal grasslands or in the neutral to alkaline grasslands, one of which was geothermal. The direct effect of the soil chemical environment on the distribution of two AMF morphospecies isolated from acidic geothermal grasslands was supported in a controlled greenhouse experiment. Paraglomus occultum and Scutellospora pellucida were more beneficial to plants and formed significantly more spores when grown in acidic than in alkaline soil. Distance among grasslands, used as an estimate of dispersal limitations, was not a significant predictor of AMF community similarity within YNP, and most fungal taxa may be part of a metacommunity. The isolation of several viable AMF taxa from bison feces indicates that wide-ranging bison could be a vector for at least some RFLP types among grasslands within YNP. In support of classical niche theory and the Baas-Becking hypothesis, our results suggest that AMF are not limited by dispersal at the scale of YNP, but that the soil environment appears to be the primary factor affecting community composition and distribution.

Molecular Community Analysis of Arbuscular Mycorrhizal Fungi in Roots of Geothermal Soils in Yellowstone National Park (USA)

To better understand adaptation of plants and their mycorrhizae to extreme environmental conditions, we analyzed the composition of communities of arbuscular mycorrhizal fungi (AMF) in roots from geothermal sites in Yellowstone National Park (YNP), USA. Arbuscular mycorrhizal fungi were identified using molecular methods including seven specific primer pairs for regions of the ribosomal DNA that amplify different subgroups of AMF. Roots of Dichanthelium lanuginosum, a grass only occurring in geothermal areas, were sampled along with thermal and nonthermal Agrostis scabra and control plants growing outside the thermally influenced sites. In addition, root samples of Agrostis stolonifera from geothermal areas of Iceland were analyzed to identify possible common mycosymbionts between these geographically isolated locations. In YNP, 16 ribosomal DNA phylotypes belonging to the genera Archaeospora, Glomus, Paraglomus, Scutellospora, and Acaulospora were detected. Eight of these phylotypes could be assigned to known morphospecies, two others have been reported previously in molecular studies from different environments, and six were new to science. The most diverse and abundant lineage was Glomus group A, with the most frequent phylotype corresponding to Glomus intraradices. Five of the seven phylotypes detected in a preliminary sampling in a geothermal area in Iceland were also found in YNP. Nonthermal vegetation was dominated by a high diversity of Glomus group A phylotypes while nonthermal plants were not. Using multivariate analyses, a subset of three phylotypes were determined to be associated with geothermal conditions in the field sites analyzed. In conclusion, AMF communities in geothermal soils are distinct in their composition, including both unique phylotypes and generalist fungi that occur across a broad range of environmental conditions.

Prairie ecosystems and the carbon problem

There has been great interest in carbon (C) storage in terrestrial landscapes and the potential for trading C released during fossil-fuel combustion for C stored in agricultural landscapes. This is particularly important in the Great Plains of North America, where increased C storage under conservation tillage represents millions of dollars in C credits. However, we contend that the logic behind such trading is imperfect on multiple levels. We suggest that increased C storage in Great Plains soils with conservation tillage can, at best, only partially replenish what was previously emitted by tillage of native prairies. Furthermore, there is disagreement on whether reduced tillage actually does increase C storage in prairie soils. Use of alternative agricultural practices that emulate natural prairie diversity, processes, and function, as well as the establishment of permanent prairie reserves, will aid in recovery of previously lost C and provide for increased biodiversity and resilience in the face of changing climate conditions.

Linking symbiont community structures in a model arbuscular mycorrhizal system

• The influence of plant communities on symbiotic arbuscular mycorrhizal fungal (AMF) communities is difficult to study in situ as both symbionts are strongly influenced by some of the same soil and environmental conditions, and thus we have a poor understanding of the potential links in community composition and structure between host and fungal communities. • AMF were characterized in colonized roots of thermal soil Mimulus guttatus in both isolated plants supporting AMF for only a few months of the growing season and plants growing in mixed plant communities composed of annual and perennial hosts. Cluster and discriminant analysis were used to compare competing models based on either communities or soil conditions. • Mimulus guttatus in adjacent contrasting plant community situations harbored distinct AMF communities with few fungal taxa occurring in both community types. Isolated plants harbored communities of fewer fungal taxa with lower diversity than plants in mixed communities. Host community type was more indicative than pH of AMF community structure. • Our results support an inherent relationship between host plant and AMF community structures, although pH-based models were also statistically supported.

Spatial heterogeneity of eukaryotic microbial communities in an unstudied geothermal diatomaceous biological soil crust: Yellowstone National Park, WY, USA

Knowledge of microbial communities and their inherent heterogeneity has dramatically increased with the widespread use of high-throughput sequencing technologies, and we are learning more about the ecological processes that structure microbial communities across a wide range of environments, as well as the relative scales of importance for describing bacterial communities in natural systems. Little work has been carried out to assess fine-scale eukaryotic microbial heterogeneity in soils. Here, we present findings from a bar-coded 18S rRNA survey of the eukaryotic microbial communities in a previously unstudied geothermal diatomaceous biological soil crust in Yellowstone National Park, WY, USA, in which we explicitly compare microbial community heterogeneity at the particle scale within soil cores. Multivariate analysis of community composition showed that while subsamples from within the same soil core clustered together, community dissimilarity between particles in the same core was high. This study describes a novel soil microbial environment and also adds to our growing understanding of microbial heterogeneity and the scales relevant to the study of soil microbial communities.

Host plant differences in arbuscular mycorrhizae: Extra radical hyphae differences between an invasive forb and a native bunchgrass

Arbuscular mycorrhizae affect grassland plant community composition and host plant nutrient uptake, and can mediate shifts in competitive outcome between plant species. Centaurea maculosa, an invasive forb from Eurasia, dominates more than 4 million hectares in the Rocky Mountain region of North America. We examined the role of AM for phosphorus (P) acquisition from a distant source for C. maculosa and Festuca idahoensis, a native bunchgrass. Plants were grown individually in pots divided by a barrier that either excluded plant roots and AM hyphae, or only plant roots. In the half of the pot without a plant, 1 of 3 P treatments was applied: no P, phosphate rock (PR) or triple superphosphate (TSP), applied at a rate of 144 mg P kg−1 soil. After 14 weeks of growth, C. maculosa was twice as large as F. idahoensis, and neither species’ biomass was affected by barrier type. Phosphorus fertilizer, and especially PR, moved across the barrier to the plant side of the pot. Tissue P concentration for C. maculosa was highest with the PR treatment, and was not affected by the barrier type. In contrast, F. idahoensis tissue P concentration did not vary with barrier or P treatments. There was more AM extra radical hyphae (ERH) associated with C. maculosa than F. idahoensis, suggesting that C. maculosa provides more carbon for the AM fungi, resulting in greater ERH production, ERH soil exploration and potential for soil nutrient pool exploitation. Although not tested in this study, differences between host plants may be the result of different physiological characteristics of the host plant or differences in AM fungal species that colonize the invader, with different fungal species accessing P from different distances.