Aspen-associated mycorrhizal fungal production and respiration as a function of changing CO2, O3 and climatic variables
Introduction
Understanding the regulators of soil respiration is critical for our ability to model ecosystem carbon (C) cycling within a global change context. Although traditionally not executed, the components of soil respiration should be partitioned into autotrophic and heterotrophic sources, with the latter encompassing organisms directly associated with autotrophs (such as rhizosphere-associated organisms, including mycorrhizal fungi) as well as free-living heterotrophic organisms (such as saprotrophs). Partitioning the heterotrophic and autotrophic components of soil respiration in field studies can be quite challenging (Ekblad et al., 2013, Hanson et al., 2000, Heinemeyer et al., 2011), with the fungal component of soil respiration rarely quantified (but see Heinemeyer et al., 2007, Heinemeyer et al., 2012).
Fungal respiration by different tissue types (e.g., hypha, mycorrhiza and sporocarp) is even less quantified, even though mycorrhizal fungi comprise a significant portion of microbial biomass within forest soils (Cairney, 2012, Ekblad et al., 2013, Högberg and Högberg, 2002, Wallander et al., 2001). Net primary production (NPP) allocated to the fungal components of mycorrhizal fungi ranges from less than 5 % to, more commonly, around 20 % (Hobbie, 2006, Smith and Read, 2008 and references within). Considering that 27–67 % of NPP is partitioned as belowground NPP (BNPP) (Hobbie, 2006), mycorrhizal fungi clearly represent a large fraction of BNPP. Hence, their growth and activities should represent a significant source of CO2 flux from ecosystems.
Atmospheric change, whether physical or chemical, can affect carbon cycling by altering production, storage, allocation, or respiration (Comstedt et al., 2006, Karnosky, 2003, Karnosky et al., 2005, King et al., 2001, Loya et al., 2003, Miller and Fitzsimmons, 2011, Podila et al., 2011, Pregitzer et al., 2008, Schlesinger and Lichter, 2001). If elevated levels of CO2 or O3 influence how primary producers gain and allocate photosynthate to belowground structures, including the supply of carbon to their fungal symbionts, then the end result could be a change in ecosystem C storage. While increased CO2 typically amplifies NPP, O3 acts in an opposing manner and will, at least initially, dampen such effects (Karnosky et al., 2003). Studies of enhanced CO2 and O3 concentrations within Free-Air Carbon dioxide Enrichment (FACE) systems have already found effects on mycorrhizal fungi, especially at the community level and in the production of sporocarps (Andrew and Lilleskov, 2009, Parrent et al., 2006, Parrent and Vilgalys, 2007, Podila et al., 2011). Consequently, any change in mycelial production and respiration due to altered CO2 or O3 concentrations could affect future soil C sequestration (Alberton et al., 2005, Andersen, 2003, Fransson, 2012, Pickles et al., 2012, Rygiewicz and Andersen, 1994, Treseder and Allen, 2000, Schlesinger and Andrews, 2000) as well as the retention of fungal derived C in the soil.
It is important to note that respiration rates are strongly affected by both temperature and moisture (Heinemeyer et al., 2007, Heinemeyer et al., 2012, Koch et al., 2007, López-Gutiérrez et al., 2008, Malcolm et al., 2008). While the effect of temperature is broadly captured in Q10 values, reviews of soil respiration literature have indicated that Q10 values are not constant with changing temperature. This limits the conceptual adequacy of a single Q10 for modeling respiration (Davidson et al., 2006, Lloyd and Taylor, 1994). A variety of factors, such as biochemical reaction rates, physiological acclimation, substrate limitation, thermal stress and moisture stress can alter temperature respiration relationships (Davidson et al., 2006). Although much effort has been applied to characterizing temperature–respiration relationships of soils (Boone et al., 1998, Davidson et al., 2006, Kätterer et al., 1998, Lloyd and Taylor, 1994, Winkler et al., 1996), much less has been applied to field studies of fungal temperature–respiration relationships.
Water availability additionally affects soil respiration and can confound estimates of temperature effects (Davidson et al., 2006). Surprisingly, very little is known about moisture impacts on field respiration rates of fungi, although they appear to be physiologically active, albeit at very low rates, at lower water potentials than bacteria (Wilson and Griffin, 1975). It is important to quantify field respiration rates in order to better understand how site variables, such as temperature and moisture, can interact to affect fungal contributions to ecosystem respiration.
The objectives of this study were to: (1) quantify the effects of changes in atmospheric carbon dioxide (CO2) and ozone (O3) concentrations on mycorrhizal fungal sporocarp and hyphal respiration in vivo; while (2) simultaneously quantifying the effect of natural variation in temperature and water availability on fungal respiration; and to (3) determine treatment effects on net hyphal biomass production. We hypothesized that: (1) fungal respiration would increase under elevated CO2 and decrease under elevated O3; (2) fungal respiration would increase under higher temperatures, and decrease as a result of lower water availability; and (3) high CO2 treatments would increase hyphal biomass production, and elevated O3 would decrease hyphal biomass production.
Section snippets
Study area
The Aspen FACE study began in 1997 with the trees planted from seedling stage. It was located on the Harshaw Experimental Farm of the USDA Forest Service, Wisconsin, USA (45° 40′ 48″ N, 89° 37′ 48″ W). The climate is cool continental with summer temperatures averaging 18.3 °C and an average of 106.7 mm of precipitation falling per month from Jul. to Sep.. Prior to the implementation of a forestry research site in the early 1970's, the land was a potato farm. Hybrid poplar and larch trees were
Hyphal production
Net hyphal biomass production over the growing season averaged 9.33 (SE ± 0.46) g m−2. Treatment and block effects on mean production were not significant (CO2 p = 0.146; O3 p = 0.235; CO2xO3 p = 0.805; block p = 0.712). Mean (±SE) hyphal production was 10.79 (±1.73), 9.29 (±0.44), 9.66 (±0.73) and 7.60 (±0.31) g m−2 within control, CO2, O3, and CO2 + O3 plots, respectively. Production was 86 %, 90 %, and 70 % of the control plots under elevated CO2, O3 and CO2 + O3, respectively.
Hyphal respiration per unit area
CO2 and O3
Mycorrhizal respiration and production with elevated CO2 and O3
The lack of a hyphal production response to the CO2 and O3 treatment contrasts with our earlier finding of significantly increased sporocarp production under elevated CO2 (Andrew and Lilleskov, 2009). Whether this is due to better sampling of sporocarp than hyphal production, interannual variation, or real differences between sporocarps and hyphae in production responses to the treatments is not certain. We can say that interannual variation in sporocarp production effects can be quite large (
Conclusions
Whereas studies of sporocarp production indicated that the transfer of carbon to the fungus is increased under elevated CO2 and, at least initially, decreased under elevated O3 (Andrew and Lilleskov, 2009), this pattern does not hold true for mycelial production within the same study system. This suggests that sporocarp production may be more sensitive to changing atmospheric chemistry than is hyphal production.
There is potential for C cycling within forest ecosystems to be affected by
Acknowledgments
We extend our gratitude to AJ Burton for advice on past manuscripts and study designs, to both AJ Burton & KS Pregitzer for sharing Aspen FACE soil respiration data, and to anonymous reviewers of this manuscript. We appreciate field help contributed by Bob Andrew and Joy Andrew. Funding was provided by the USDA Forest Service, Northern Research Station, an Ecosystem Science Center (MTU) research grant awarded to C Andrew in 2006, and a Finishing Fellowship Grant awarded to C Andrew through the
References (87)
- et al.
Sensory shelf life of shiitake mushrooms stored under passive modified atmosphere
Postharvest Biology and Technology
(2006) - et al.
Oxygen consumption by Metarhizium anisopliae during germination and growth on different carbon sources
Journal of Invertebrate Pathology
(1999) Extramatrical mycelia of ectomycorrhizal fungi as moderators of carbon dynamics in forest soil
Soil Biology & Biochemistry
(2012)- et al.
Riparian soil response to surface nitrogen input: temporal changes in denitrification, labile and microbial C and N pools, and bacterial and fungal respiration
Soil Biology and Biochemistry
(1999) Elevated CO2 impacts ectomycorrhiza-mediated forest soil carbon flow: fungal biomass production, respiration and exudation
Fungal Ecology
(2012)- et al.
Seasonal variation and partitioning of ecosystem respiration in a southern boreal aspen forest
Agricultural and Forest Meteorology
(2004) - et al.
Nine years of CO2 enrichment at the alpine treeline stimulates soil respiration but does not alter soil microbial communities
Soil Biology and Biochemistry
(2013) Impacts of elevated atmospheric CO2 on forest trees and forest ecosystems: knowledge gaps
Environment International
(2003)- et al.
Ectomycorrhizas and climate change
Fungal Ecology
(2012) - et al.
Respiratory parameters and sugar catabolism of mushroom (Agaricus bisporus Lange)
Postharvest Biology and Technology
(1999)
Species richness and nitrogen supply regulate the productivity and respiration of ectomycorrhizal fungi in pure culture
Fungal Ecology
Water potential and the respiration of microorganisms in the soil
Soil Biology and Biochemistry
The Q10 relationship of microbial respiration in a temperate forest soil
Soil Biology & Biochemistry
Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO2
New Phytologist
Source-sink balance and carbon allocation below ground in plants exposed to ozone
New Phytologist
Productivity and community structure of ectomycorrhizal fungal sporocarps under increased atmospheric CO2 and O3
Ecology Letters
Response of root respiration to changes in temperature and its relevance to global warming
New Phytologist
A global relationship between the heterotrophic and autotrophic components of soil respiration?
Global Change Biology
Roots exert a strong influence on the temperature sensitivity of soil respiration
Nature
Can isotopic fractionation during respiration explain the 13C-enriched sporocarps of ectomycorrhizal and saprotrophic fungi?
New Phytologist
Allelopathic effects of phenolic mixtures on respiration of two spruce mycorrhizal fungi
Journal of Chemical Ecology
Respiratory costs of mycorrhizal associations
Fungal community composition and metabolism under elevated CO2 and O3
Oecologia
Effects of elevated atmospheric carbon dioxide and temperature on soil respiration in a boreal forest using δ13C as a labeling tool
Ecosystems
On the variability of respiration in terrestrial ecosystems: moving beyond Q10
Global Change Biology
Growth and respiration of psychrophilic species of the genus Typhula
Canadian Journal of Botany
Coarse and fine root respiration in aspen (Populus tremuloides)
Tree Physiology
Forest Atmosphere Carbon Transfer and Storage (FACTS-II) the Aspen Free-air CO2 and O3 Enrichment (FACE) Project: an Overview
The influence of nitrogen fertilization on the carbon economy of Paxillus involutus in ectomycorrhizal association with Betula pendula
New Phytologist
The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling
Plant Soil
Growth and mineral nutrition of non-mycorrhizal and mycorrhizal Norway spruce (Picea abies) seedlings grown in semi-hydroponic sand culture
New Phytologist
Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter
Plant and Soil
Changes in respiration and soluble carbohydrates during the post-harvest storage of mushrooms (Agaricus bisporus)
Journal of the Science of Food and Agriculture
Separating root and soil microbial contributions to soil respiration: a review of methods and observations
Biogeochemistry
A six-year study of sapling and large-tree growth and mortality responses to natural and induced variability in precipitation and throughfall
Tree Physiology
Carbon and nitrogen elemental and isotopic patterns in macrofungal sporocarps and trees in semiarid forests of the south-western USA
Functional Ecology
Contrasting effects of low and high nitrogen additions on soil CO2 flux components and ectomycorrhizal fungal sporocarp production in a boreal forest
Global Change Biology
Respiration of the external mycelium in the arbuscular mycorrhizal symbiosis shows a strong dependence on recent photosynthates and acclimation to temperature
New Phytologist
Forest soil CO2 flux: uncovering the contribution and environmental responses of ectomycorrhizas
Global Change Biology
Soil respiration: implications of the plant-soil continuum and respiration chamber collar-insertion depth on measurement and modeling of soil CO2 efflux rates in three ecosystems
European Journal of Soil Science
Exploring the “overflow tap” theory: linking forest soil CO2 fluxes and individual mycorrhizosphere components to photosynthesis
Biogeosciences
Mycorrhizal vs saprotrophic status of fungi: the isotopic evidence
New Phytologist
Carbon allocation to ectomycorrhizal fungi correlates with belowground allocation in culture studies
Ecology
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2017, Fungal EcologyCitation Excerpt :Although less commonly discussed, ‘plant’ respiration also contains fungal respiration, especially in roots because of mycorrhizal associations, but also other plant tissues because of the pervasive presence of fungal endophytes. Given the large differences noted between plant and fungal respiration rates (e.g., Andrew et al., 2014) even a small fungal component could contribute a significant fraction of empirical measurements of plant respiration. In addition it is likely that patterns of plant and fungal respiration respond differently to environmental cues such as temperature and moisture.