Mycorrhizal networks in ecosystem structure and functioning
Edited by Katie Field
Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN
The vast majority of land plants (> 80%) form mutualistic symbioses with soil-dwelling fungi known as mycorrhizas. Such symbioses typically involve the reciprocal exchange of fungal-acquired nutrients for plant-fixed carbohydrates (Smith and Read 2008). As mycorrhizal fungi tend to be non-specific in their choice of hosts, many plants can be linked through fungal hyphae in a common mycelial network (CMN). These networks can be enormous, with around 200m of mycorrhizal fungal hyphae present in a single gram of typical forest soil (Dickie, 2006). The flow of nutrients between plants and mycorrhiza and the resulting redistribution of nutrients throughout a community is an area of much recent research with important contributions having been made by publications in Functional Ecology. This Virtual Issue highlights those contributions covering three major themes in mycorrhizal research, namely; the movement of plant-fixed carbon, reciprocal exchange of nutrients, and the wider impacts on biodiversity and ecosystem function.
Carbon flow within mycorrhizal networks
The majority of mycorrhizal fungi are obligately biotrophic i.e. they are entirely reliant on their plant partner for their organic carbon assimilation. By understanding the flow of carbon throughout a mycorrhizal network that links together many individuals from multiple plant species, it is possible to start to understand the wider impacts on ecosystem structure and function. In their classic paper, Fitter et al. (1998) assessed the flow of plant-fixed carbon into mycorrhizal fungi and then into neighbouring plants using the stable isotope 13C. They showed transfer of carbon between plants via the CMN, although this carbon remained within the roots. These findings were extremely influential in mycorrhizal research, suggesting a novel mechanism by which mycorrhizal fungi acquire and mobilise plant-fixed carbon from roots containing younger fungal structures such as arbuscules and hyphae, to roots containing older structures including vesicles. While important in mycorrhizal ecology, these results were viewed as less significant in wider ecology given that carbon was postulated to remain within fungal structures rather than having any measurable impact on plant fitness. In contrast, Zabinski et al. (2002) later also investigated the interspecific movement of 13C but reported no detectable fungal-mediated transfer of carbon between neighbouring plants. Instead, they suggest a novel hypothesis; that mycorrhiza-enhanced growth is the result of increased access to phosphorus, causing increased plant-tissue phosphorus content and enhanced growth in plants with mycorrhizal access to a greater volume of soil than those without. This then impacts upon the surrounding plant community, with interspecific variation in utilisation of mycorrhizal networks and perhaps an influence on wider community composition. Talbot et al. (2008) contributed significantly to this topic a few years later with their synthesis examining the role of mycorrhizas in soil carbon dynamics, proposing novel mechanisms underpinning the role of mycorrhizal fungi in decomposition of organic carbon compounds. More recently Pollierer et al. (2012), again using 13C, analysed fatty acids to tease apart the movement of carbon via bacteria and mycorrhizas on an even wider scale: the forest soil food web. Their findings show that the microbes can play a major part in carbon flow between trophic levels, something which had until then been largely overlooked. This suggests that the flux of carbon through both fungal and bacterial channels is essential to stabilising the tropical forest food webs and is certainly something that should be borne in mind in future studies within this branch of ecology.
Reciprocal exchange of fungal-acquired nutrients
Mycorrhizal fungi are, for the most part, mutualistic and accordingly the carbon invested in mycorrhizal fungi by their host plant(s) is exchanged for mineral nutrients, with mycorrhizas providing wider access to soil resources. After nitrogen, phosphorus is usually the most limiting nutrient for plants and enhanced access to phosphorus via a CMN usually has a beneficial effect on plant productivity (Smith and Read, 2008). Increased phosphorus mobilisation through mycorrhizal associations indirectly influences community structure and function by changing the balance of competitive interactions. The role of CMNs in inter-plant phosphorus transfer was investigated by Wilson et al. (2006) by tracing the movement of the radio-isotope 32P from a “donor” plant to a “receiver” via a mycorrhizal network. The successful experiments showed that the effectiveness of the isotope uptake in receiver-plants is species specific. By demonstrating that CMNs alter the distribution of phosphorus throughout a community, these findings were among the first to illustrate a mechanism by which mycorrhizal networks influence community composition and wider ecosystem functioning. The recent synthesis by Hodge & Fitter (2013) discusses in depth the importance of the interactions between plants and soil micro-organisms (and the interactions therein) in determining plant diversity through nutrient mobilisation, with particular reference to nitrogen, and forms an important part of this virtual issue. Their suggestion that the functioning of a CMN is linked to the nutrient status of the soil is reflected in the findings of Gross et al. (2010) who aimed to establish the role of mycorrhizal fungi in forming single-species dominant communities (i.e. monopolistic species) on ex-agricultural land. They found that rather than plants benefitting most from mycorrhizal associations under low-nutrient conditions as might be expected, monopolistic plant species responded to mycorrhiza most positively under an intermediate nutrient regime similar to the fertility levels of ex-agricultural land. This provides an explanation as to why monopolistic species are so successful in such environments. Experiments to trace the fate of plant-essential nutrients within a variety of soil and atmospheric conditions are now needed to resolve the potential power of CMNs as ecosystem engineers.
Mycorrhizal networks themselves function differently according to surrounding plant assemblages. Teste et al. (2014) clearly demonstrate this through carefully designed ‘common garden’ experiments comprising nutrient-rich and nutrient-poor microcosms. Their findings have clear significance in a variety of different ecological scenarios, including within an agri-environmental context, and provide novel insights into potential mechanisms by which mycorrhizal fungi are effective ecosystem engineers and may be utilised in land remediation practices.
Influence of mycorrhizas on wider community structure and function
The movement and redistribution of carbon and mineral nutrients that characterises CMNs have the potential to strongly influence both above- and below-ground community biodiversity and function. Mycorrhizal hyphae and the extensive networks they form are known to be an effective mediators not only of plant nutrients, but also water and phytochemicals. Kannadan and Rudgers (2008) showed significantly greater shoot and root biomass in droughted Poa alsodes that was associated with mycorrhizal fungi compared to neighbouring, non-mycorrhizal plants of the same species. This research highlights the water-conserving properties mycorrhizal colonisation may convey upon a host plant. Achatz et al. (2014) raise the interesting hypothesis that in addition to essential nutrients, mycorrhizal networks also facilitate the transport of allelopathic phytochemicals such as juglone. In an elegant set of ecologically relevant glasshouse and field experiments, they demonstrate that mycorrhizal hyphal networks increase the zone of influence of these chemicals, facilitating a 271% increase in accumulation of juglone in mycorrhiza-inoculated soil versus non-mycorrhizal soil. Together these studies elegantly demonstrate how below-ground interactions play a key role in regulating plant community structure and composition.
The often-enhanced morphological characteristics of plants associating with mycorrhizas can increase reproductive output of some plant species, as demonstrated by Varga and Kytöviita (2010) in a common garden experiment with Geranium sylvaticum. In this experiment, Varga and Kytöviita report that mycorrhiza-mediated increases in flower size and pollen production influences behaviour of key pollinator species, although this effect is likely to be species-specific. Other plant-insect interactions are also affected by associations with mycorrhizal fungi, and Kempel et al. (2010) demonstrated that induction of plant defences in the presence of mycorrhizal fungi resulted in a reallocation of plant resources away from growth, presumably towards defence compound production, and subsequent decrease in herbivore performance. Non-mycorrhizal fungi respond negatively to colonisation of host plants by mycorrhizas, as demonstrated by Liu et al. (2011). Reduced concentrations of the foliar endophyte Neotyphodium were shown in two ryegrass cultivars when colonised by mycorrhizal fungi of the Glomeromycota, and vice versa. This suggests such interactions are complex and the benefits of both endosymbionts must be balanced with environmental constraints. Schausberger et al. (2012) report mycorrhiza-induced changes to the composition of herbivore-induced volatile organic compounds (VOCs). These compounds are attractive to predatory spider mites that prey upon herbivore pests, providing a mechanism for inter-trophic level signalling as part of plant defence systems. Babikova et al (2014) investigated the effect of mycorrhizal colonisation on the production of other plant VOCs and their attractiveness to sap-sucking aphids. They found that colonisation by mycorrhizal fungi actually increased the attractiveness of plants to aphids through enhanced nutrition leading to production of more attractive VOCs, although this was dependent on timing of initiation of fungal colonisation. In all treatments aphid infestation led to reduction in mycorrhizal colonisation of host plants, creating a potential feedback loop. Further research of multi-trophic levels by Kempel et al. (2013) using invasive and non-invasive alien plant species found high diversity in plant responses to mycorrhizal inoculation in terms of biomass and induction of defences against herbivory. This suggests that while fungi-plant-herbivore interactions are diverse in nature, there is scope for mycorrhizas having far-reaching impacts on surrounding communities of plants, insects and micro-organisms, even in recently introduced species. Together, this collection of research demonstrate how below-ground microbial processes can heavily influence above-ground interactions, a mechanism influencing community structure and function that is all too often overlooked.
The roles of mycorrhizal fungi in regulating community and wider ecosystem structure, both directly and indirectly, and the mechanisms by which it may occur have major implications for their use within sustainable agriculture. Since the post-war Green Revolution, agricultural productivity has increased dramatically in terms of crop yield and predictability, dependent largely on the development and application of novel pesticides and nitrogen- and phosphorus-based fertilisers, coupled to advances in plant breeding and genetic technologies. However, in the last 15 years key crop yields have plateaued and we must now look to more sustainable agricultural solutions to secure global food supplies in a more environmentally sustainable fashion. Application of mycorrhizal inoculum to crop plants may help reduce use of chemical fertilisers by providing alternative routes for enhancing crop nutrition, however much of the research surrounding this is concentrated on short-term experimental evidence. Antunes et al. (2012) redress this imbalance by considering the consequences of long-term nutrient manipulation – such as that existing in agricultural land – for mycorrhizal fungal community structure and symbiotic functioning. Their findings demonstrate significant flexibility in mycorrhizal functioning and emphasise the importance of considering long-term site history in using such inocula.
The research highlighted in this Virtual Issue of Functional Ecology illustrates that mycorrhiza-plant-community interactions are a critically important and dynamic component of ecosystem structure and function. These often multi-trophic interactions have, until relatively recently, been largely overlooked by ecologists seeking to understand why and how plant communities are structured, and the implications of this within the wider context of future climate change and the global need for improved land remediation and improved and sustainable agricultural practices. As such, critical knowledge-gaps still exist in this area. The part(s) played by mycorrhizas in relaying inter- and intra-specific plant signalling/phytochemicals, the precise mechanisms of mycorrhizal-mediated plant defence and immunity and the functional significance of these within wider plant communities are only now starting to be elucidated and should form an integral part of future mycorrhizal research. Future research should also focus on improving our understanding of the processes by which mycorrhizas access and distribute soil resources, how this is affected by pollutants and atmospheric CO2 and the resulting impacts on community composition and function in natural and agricultural systems.
Image caption: Orchid is an Early Marsh Orchid (Dactylorhiza incarnata). Photo credited Dr Samuel Taylor, who took it during fieldwork in dune slacks in Aberffraw, Anglesey.
Soil hypha‐mediated movement of allelochemicals: arbuscular mycorrhizae extend the bioactive zone of juglone
Achatz M., Morris E.K., Müller F., Hilker M., Rillig M.C.
Long‐term effects of soil nutrient deficiency on arbuscular mycorrhizal communities
Antunes P.M., Lehmann A., Hart M.M., Baumecker M., Rillig M.C.
Arbuscular mycorrhizal fungi and aphids interact by changing host plant quality and volatile emission
Babikova Z., Gilbert L., Bruce T., Dewhirst S.Y., Pickett J.A., Johnson D.
Carbon transfer between plants and its control in networks of arbuscular mycorrhizas
Fitter A., Graves J., Watkins N., Robinson D., Scrimgeour C.
Trait-mediated effect of arbuscular mycorrhiza on the competitive effect and response of a monopolistic species
Gross N., Le Bagousse-Pinguet Y., Liancourt P., Urcelay C., Catherine R., Lavourel S.
Microbial mediation of plant competition and community structure
Hodge A., Fitter A.H.
Endophyte symbiosis benefits a rare grass under low water availability
Kannadan S., Rudgers J.
Plant‐microbe‐herbivore interactions in invasive and non‐invasive alien plant species
Kempel A., Nater P., Fischer M., Kleunen M.
Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi
Kempel A., Schmidt A.K., Brandl R., Schädler M.
Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content
Liu Q., Parsons A.J., Xue H., Fraser K., Ryan G.D., Newman J.A., Rasmussen S.
Mycorrhiza changes plant volatiles to attract spider mite enemies
Schausberger P., Peneder S., Juerschik S., Hoffmann D.
Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change
Talbot J., Allison S., Treseder K.
Complementary plant nutrient‐acquisition strategies promote growth of neighbour species
Teste F.P., Veneklaas E.J., Dixon K.W., Lambers H.
Mycorrhizal‐mediated phosphorus transfer between tallgrass prairie plants Sorghastrum nutans and Artemisia ludoviciana
Wilson G., Hartnett D., Rice C.
Achatz M., Morris E.K., Müller F., Hilker M., Rillig M.C. 2014. Soil hypha‐mediated movement of allelochemicals: arbuscular mycorrhizae extend the bioactive zone of juglone. Functional Ecology
Antunes P.M., Lehmann A., Hart M.M., Baumecker M., Rillig M.C. 2012. Long‐term effects of soil nutrient deficiency on arbuscular mycorrhizal communities. Functional Ecology 26(2): 532-540.
Babikova Z., Gilbert L., Bruce T., Dewhirst S.Y., Pickett J.A., Johnson D. 2014. Arbuscular mycorrhizal fungi and aphids interact by changing host plant quality and volatile emission. Functional Ecology 28(2): 375-385.
Dickie I. 2006. Mycorrhiza of Forest Ecosystems. pp 1111-1114, In: Encyclopedia of Soil Science Ed. R. Lal. Taylor & Francis Group, New York.
Fitter A., Graves J., Watkins N., Robinson D., Scrimgeour C. 1998. Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Functional Ecology 12(3): 406-412.
Gross N., Le Bagousse-Pinguet Y., Liancourt P., Urcelay C., Catherine R., Lavourel S. 2010. Trait-mediated effect of arbuscular mycorrhiza on the competitive effect and response of a monopolistic species. Functional Ecology 24(5): 1122-1132.
Hodge A., Fitter A.H. 2013. Microbial mediation of plant competition and community structure. Functional Ecology 27(4): 865-875.
Kannadan S., Rudgers J. 2008. Endophyte symbiosis benefits a rare grass under low water availability. Functional Ecology 22(4): 706-713.
Kempel A., Nater P., Fischer M., Kleunen M. 2013. Plant‐microbe‐herbivore interactions in invasive and non‐invasive alien plant species. Functional Ecology 27(2): 498-508.
Kempel A., Schmidt A.K., Brandl R., Schädler M. 2010. Support from the underground: induced plant resistance depends on arbuscular mycorrhizal fungi. Functional Ecology 24(2): 293-300.
Liu Q., Parsons A.J., Xue H., Fraser K., Ryan G.D., Newman J.A., Rasmussen S. 2011. Competition between foliar Neotyphodium lolii endophytes and mycorrhizal Glomus spp. fungi in Lolium perenne depends on resource supply and host carbohydrate content. Functional Ecology 25(4): 910-920.
Pollierer M.M., Dyckmans J., Scheu S., Haubert D. 2012. Carbon flux through fungi and bacteria into the forest soil animal food web as indicated by compound‐specific 13C fatty acid analysis. Functional Ecology 26(4): 978-990.
Schausberger P., Peneder S., Juerschik S., Hoffmann D. 2012. Mycorrhiza changes plant volatiles to attract spider mite enemies. Functional Ecology 26(2): 441-449.
Smith SE, Read DJ. 2008. Mycorrhizal Symbiosis. Academic press, Oxford, UK.
Talbot J., Allison S., Treseder K. 2008. Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Functional Ecology 22(6): 955-963.
Teste F.P., Veneklaas E.J., Dixon K.W., Lambers H. 2014. Complementary plant nutrient‐acquisition strategies promote growth of neighbour species. Functional Ecology.
Varga S., Kytöviita M.M. 2010. Gender dimorphism and mycorrhizal symbiosis affect floral visitors and reproductive output in Geranium sylvaticum. Functional Ecology 24(4): 750-758.
Wilson G., Hartnett D., Rice C. 2006. Mycorrhizal‐mediated phosphorus transfer between tallgrass prairie plants Sorghastrum nutans and Artemisia ludoviciana. Functional Ecology 20(3): 427-435.
Zabinski C, Quinn L, Callaway R. 2002. Phosphorus uptake, not carbon transfer, explains arbuscular mycorrhizal enhancement of Centaurea maculosa in the presence of native grassland species. Functional Ecology 16(6): 758-765.
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