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Soil Biology & Biochemistry 38 (2006) 2997–2998

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Letter to the Editor

Comments on Yakov Kuzyakov’s review ‘Sources of CO2

efflux from soil and review of partitioning methods’

[Soil Biology & Biochemistry 38, 425–448]

In a recent review Yakov Kuzyakov (2006) aims toidentify major sources of soil respiration, to clarify theterminology relevant in this context, and to point outadvantages and disadvantages of various approaches toestimate the fractional contributions of different sources ofthe soil CO2 efflux. He initially (p. 427) distinguishes fivemajor sources of soil respiration:

(1)

microbial decomposition of soil organic matter (SOM)in root-free soil,

(2)

microbial decomposition of SOM in root-affected soil(‘priming’),

(3)

microbial decomposition of dead plant remains (weunderstand this as meaning plant material added morerecently to the soil, and assume that the term SOMrefers to much older and more transformed plantremains),

(4)

rhizomicrobial respiration (microbial decomposition ofrhizodeposits from living roots) and

(5)

root respiration.

He then (p. 428 and 432) presents two classes ofsomewhat contradictory statements. Firstly, he states thatthere are, in reality, no sharp boundaries between thesesources (1–5) of respiration, e.g., because of the presence ofsymbiotic mycorrhizal fungi inside and just outside rootcells. He also advocates the use of the term ‘rhizosphererespiration’ as a collective term describing the sum of (2),(4) and (5), and thus lumps together truly autotrophicactivity (5) with activity many would consider hetero-trophic (2). Secondly, he adopts the contrasting view that,despite the difficulties to separate (4) and (5), the processescontributing to CO2 production in each pool are different,and hence that (4) and (5) should be treated separately.Following these lines of thought he then states that it ismisleading to say that tree-girdling, an approach employedby ourselves (Hogberg et al., 2001; Bhupinderpal-Singh etal., 2003; Subke et al., 2004; Olsson et al., 2005) and others(e.g., Andersen et al., 2006; Scott-Denton et al., 2006), doesseparate autotrophic from heterotrophic soil respiration inforests. He bases his criticism on the fact that the methodcannot separate the components (4) (rhizomicrobial

e front matter r 2006 Elsevier Ltd. All rights reserved.

ilbio.2006.04.001

respiration) and (5) (root respiration, the one and onlysignificant source of autotrophic respiration in soilaccording to Dr. Kuzyakov).We agree with the statement that tree-girdling terminates

the flux of photosynthate from the tree canopy not only toroots, but also to mycorrhizal fungi and other microorgan-isms in the rhizosphere, which depend on this flux of Cfrom the autotroph (note also that the treatment will alsoreduce priming (2)). As should be clear for readers of ourpapers (e.g., Hogberg et al., 2001), we consider soilautotrophic respiration as the sum of the respiratorycontributions from roots, their mycorrhizal fungi and otherrhizosphere microorganisms directly and predominantlydependent on the flux of recent labile C from tree canopyphotosynthesis. We understand that Dr. Kuzyakov andmany other soil microbiologists feel uncomfortable withthis idea of lumping together root respiration, with therespiration by what is taxonomically regarded as hetero-trophic microorganisms.Allow us, therefore, to explain why we do this. Our first

argument concerns the basic logic and biochemistry, andthe facts that the true autotrophic activity of terrestrialhigher plants is confined to their foliage, and that the rootcells are as dependent on recent canopy photosynthate fortheir respiratory activity as are their associated mycorrhizalfungi. The latter occur inside, or just outside the cell wallsof the root cells, separated from them only by thin cellmembranes and cell walls. The processes leading to CO2

efflux are, in our view, not that fundamentally different; inthe case of root cells sucrose from the canopy is the originalC source, whereas in the case of mycorrhizal fungi, thesame plant sucrose has first been converted by plantinvertases before the C enters the fungal cells as glucose(Smith and Read, 1997).Our second argument rests on naturally occurring

evidence that what we regard as the autotrophic domainextends considerably beyond the root. Consider theachlorophyllous mycoheterotrophic plants, of which thereare at least 400 species distributed through 10 plantfamilies. These obtain photosynthate from the same fungiconnecting them with a mycorrhizal autotrophic plant(Bjorkman, 1960; Leake, 1994). This complex dependencydemonstrates the presence of an autotrophic continuityextending beyond the plant root cells of the photosyntheticdonor plant, through the mycorrhizal mycelium, to therecipient sink plant well beyond the root of the autotrophicplant.

ARTICLE IN PRESSLetter to the Editor / Soil Biology & Biochemistry 38 (2006) 2997–29982998

Our third argument relates to the problem of technicallymaking a proper separation between the respiratoryactivities of the closely juxtaposed plant root cells and thoseof mycorrhizal fungi and other closely root-associatedmicroorganisms. In temperate and boreal coniferous forestsof the type, in which we did our girdling experiments, morethan 95% of the fine tree root tips are ensheathed byectomyorrhizal fungi, which also penetrate between thecortical cells of the plant root, forming the so-called Hartignet. The sheath and the Hartig net may contribute 20–40%of the biomass of the ectomycorrhizal root. Any attempt tophysically separate the two sources of respiration wouldinevitably disrupt the autotrophically driven C flux from theplant to the fungus. As a consequence, we, and many otherforest ecosystem ecologists working directly in the field (e.g.,Hanson et al., 2000), pragmatically combine root (5) and‘rhizomicrobial’ (4) respiration.

Fourthly, while we understand that it is possible tocontemplate the separation of (4) and (5), we suggest that itis more interesting for ecosystem ecologists to make aseparation between two major soil CO2 effluxes, the firstdriven by decomposition of litter and SOM ((1) and (3),with turnover times of the C of several months–years) andthe second driven by the flux of recent photosynthatethrough mycorrhizal roots ((4) and (5), with turnover timesof the C of a few days); tree-girdling was employed toattempt to do this (and nothing else) directly in the field. Itis by no means a perfect method, as discussed by Dr.Kuzyakov and ourselves (Hogberg et al., 2001, 2005). Forexample, it cannot, when employed alone, distinguish theCO2 efflux from priming (2), but, can, combined with othermethods, provide insights into that process (Subke et al.,2004). Nor should it work very well in case of tree specieswith large stores of non-structural carbohydrates in theirroots, e.g. eucalypts, in which root respiration shifts to thisC source when the trees are girdled (Binkley et al., 2006).However, in the case of temperate and boreal conifer trees,with less non-structural carbohydrates in their roots,declines of up to 40–65% in soil respiration after girdling(relative to in non-girdled plots) have very clearly demon-strated the immediate dependence of a substantial fractionof soil respiratory activity on the flux of recent photo-synthate (Hogberg et al., 2001; Bhupinderpal-Singh et al.,2003; Subke et al., 2004; Andersen et al., 2006; Olssonet al., 2005; Scott-Denton et al., 2006).

Lastly, we fully agree with Dr. Kuzyakov that progressin this field will require that different methods arecombined. A particularly interesting avenue is to combinephysiological manipulations with different C isotopelabeling techniques (e.g., Staddon, 2004; Hahn et al., 2006).

References

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Peter Hogberg�

Department of Forest Ecology, SLU, SE-901 83 Umea,

Sweden

E-mail address: Peter.Hogberg@sek.slu.se

Nina BuchmannInstitute of Plant Sciences,

Federal Institute of Technology LFW, Universitatsstr. 2,

CH-8092 Zurich, Switzerland

David J. ReadDepartment of Animal and Plant Sciences, University of

Sheffield, Sheffield, UK