Aspen-associated mycorrhizal fungal production and respiration as a function of changing CO2, O3 and climatic variables

doi:10.1016/j.funeco.2013.10.005

Fungal Ecology

Volume 10, August 2014, Pages 70-80

https://doi.org/10.1016/j.funeco.2013.10.005 Get rights and content

Highlights

•
We quantify mycorrhizal respiration & hyphal production with elevated CO₂ and O₃.
•
We characterize temperature and moisture variability related to respiration.
•
Sporocarp respiration was strongly affected by temperature and moisture content.
•
Hyphal respiration comprised 31 % of soil respiration.
•
The ratio of hyphal respiration to soil respiration declined with elevated CO₂.

Abstract

The relationships of mycorrhizal fungal respiration and productivity to climate and atmospheric chemistry remain under characterized. We quantified mycorrhizal sporocarp and hyphal respiration, as well as growing season net hyphal production, under ambient and elevated carbon dioxide (CO₂) and ozone (O₃) in relation to natural temperature and moisture variation. Hyphal respiration did not respond significantly to elevated CO₂ and O₃. Sporocarp respiration was affected by temperature and moisture content while hyphal respiratory response to temperature was undetected over the narrower range of soil temperatures captured. Hyphal respiration comprised 31 % of soil respiration, and the ratio of hyphal respiration to soil respiration declined with elevated CO₂. Hyphal biomass was reduced under all treatments though not statistically significant. Given the large fraction of soil respiration represented by mycorrhizal fungi and its sensitivity to climate, a small change in fungal respiration could strongly affect carbon budgets and cycling under climate change.

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, O_3, 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

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Aspen-associated mycorrhizal fungal production and respiration as a function of changing CO2, O3 and climatic variables

Highlights

Abstract

Introduction

Section snippets

Study area

Hyphal production

Hyphal respiration per unit area

Mycorrhizal respiration and production with elevated CO2 and O3

Conclusions

Acknowledgments

Postharvest Biology and Technology

Journal of Invertebrate Pathology

Soil Biology & Biochemistry

Soil Biology and Biochemistry

Fungal Ecology

Agricultural and Forest Meteorology

Soil Biology and Biochemistry

Environment International

Fungal Ecology

Postharvest Biology and Technology

Fungal Ecology

Soil Biology and Biochemistry

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

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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

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Growth and respiration of psychrophilic species of the genus Typhula

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Aspen-associated mycorrhizal fungal production and respiration as a function of changing CO₂, O₃ and climatic variables

Mycorrhizal respiration and production with elevated CO₂ and O₃

Taking mycocentrism seriously: mycorrhizal fungal and plant responses to elevated CO₂

Productivity and community structure of ectomycorrhizal fungal sporocarps under increased atmospheric CO₂ and O₃

Can isotopic fractionation during respiration explain the ¹³C-enriched sporocarps of ectomycorrhizal and saprotrophic fungi?

Fungal community composition and metabolism under elevated CO₂ and O₃

Effects of elevated atmospheric carbon dioxide and temperature on soil respiration in a boreal forest using δ¹³C as a labeling tool

On the variability of respiration in terrestrial ecosystems: moving beyond Q₁₀

Forest Atmosphere Carbon Transfer and Storage (FACTS-II) the Aspen Free-air CO₂ and O₃ Enrichment (FACE) Project: an Overview

Contrasting effects of low and high nitrogen additions on soil CO₂ flux components and ectomycorrhizal fungal sporocarp production in a boreal forest

Forest soil CO₂ flux: uncovering the contribution and environmental responses of ectomycorrhizas

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

Exploring the “overflow tap” theory: linking forest soil CO₂ fluxes and individual mycorrhizosphere components to photosynthesis