Chapter 2　The Function of Mycorrhizas to CO₂ Efflux in Ecosystem

Section 1:The influence of mycorrhizal fungi on soil respiration

1.Introduction

Soil,as a main part of terrestrial ecosystem,is one of the planet's largest carbon reserves,and soil respiration is one of the largest CO₂ fluxes from terrestrial biosphere to the atmosphere(Schimel et al.,2001).It is well known,CO₂ was fixed through photosynthesis,which is the only approach that CO₂ enter into earth.However,CO₂ was emitted into atmosphere by several ways,such as soil respiration,ecosystem respiration and fossil fuel,etc..During these courses,ecosystem respiration is the most important course.At the same time,the dominant terrestrial source of CO₂ is soil.CO₂ is produced in soils by plant roots and heterotrophic organisms,and most CO₂ is release to the atmosphere.The process of soil respiration produces more than 11 times the current rate of fossil fuel combustion and shows about 10％ of atmosphere CO₂ cycles each year(Schimel et al.,2001;Raich et al.,2002).The CO₂ quantity of emission by soil respiration is about 20％ ～40％ of total CO₂ releasing into atmospheres from earth(Raich and Schelesinger,1992).Environmental changil rees that alter rates of sospiration thus have a strong potential to influence atmosphere CO₂ level.Therefore,the slim change of soil respiration will lead to the dramatic fluctuation of the atmospheric CO₂ concentration(Rustad et al.,2000;Schlesinger,2000).However,soil respiration is assessed as the most uncertainty in all factors that influenced climate-carbon cycle projections associated with the sensitivity of soil respiration(Jones et al.,2003).As a result,soil CO₂ flux was paid more and more attentions by numerous ecologists,environmentalists and pedologist with the high opinion of the world every state nation in global changes.

After photosynthesis,CO₂ flux from soil remains the second largest carbon(C)flux in most ecosystems,and can account for 60％ ～90％ of total ecosystem respiration(Goulden et al.,1996;Longdoz et al.,2000).Recently,the researches on soil respiration focused on the following aspects.(1)The participations of soil respiration attract the attentions of many ecologists because of the various sources of soil respiration,soil autotrophic respiration(root respiration),soil biological respiration including the respiration from soil protozoan and microorganisms.In addition,soil respiration is also influenced by soil physical and chemical characteristics.Therefore,soil CO₂ emission changed with the variation of environment and seasons,even day and night.As a result,soil respiration and their participations exits spatial and temporal variability(Ryan and Law,2005;Trumbore,2006).Kuzyakov(2006)reviewed the former studies and pointed out five sources of soil respiration(Figure 2-1).(2)The impacting factors of soil respiration are another topic under climate changes.Recent attention to spatial and temporal variability of forest Rs has arisen from disagreements over a variety of factors influencing the variability of Rs at different temporal or spatial scales(Allison et al.,2008,Zheng et al.,2010).However,because of its high variability on spatial-temporal scales,inaccessibility of the soil medium,and high cost of measurement instruments,Rs remains the least characterized component of the terrestrial C cycle(Savage et al.,2008).Because the temporal and spatial dynamics of Rs are the integrated result of a broad spectrum of respiratory processes operating under wildly varying environmental constraints,they remain difficult to model or predict(Zobitz et al.,2008).So far,the soil respiration on large scale was mainly evaluated by indirect(e.g.FLUX data)or meta-analysis methods(Bond-Lamberty and Thomson,2010;Zheng et al.,2010).Campbell and Law(2005)indicated that understanding the temporal and spatial changing trends of soil respiration are substantial in exploring soil respiration in large scales.Moreover,in all factors,soil temperature and water content obtained currently most studies.With the further studies,the biological factors especially soil microorganisms have attracted to attentions of a lot of researches in recent years(Monson et al.,2006;Kuzyakov and Larionova,2006;Hartley et al.,2008;Allison et al.,2008).Amongst them,mycorrhizas,as the widest symbiosis on the earth,have been testified to influence soil respiration.Hughes et al.(2008)pointed out mycorrhizal and non-mycorrhizal root respirations differ in their response to nutrient supply;and that the impact of colonization on repiration is related to fungal biomass.Failure to examine properly the role of colonization in determining root respiration means those current interpretations of root and soil respiration data might be flawed(Hughes et al.,2008).

In terrestrial ecosystem,more than 90％ plants are able to be colonized by mycorrhizal fungi in soil and form mycorrhizal associations(Allen,1991).Although there are several distinct types association(Smith &Read,2008)we focused on arbuscularof mycorrhizal mycorrhizal(AM)and ectomycorrhizal(EM)associations because they are the two most common and best studied types in terrestrial ecosystems.AM fungi are widespread,forming symbiotic associations with c.85％ of all terrestrial plants(Smith and Read,2008).By contrast,EM fungi are restricted to a smaller number of host plant species(Allen et al.,1995)and are best known from studies in northern temperate and boreal forests.According to the widely accepted theory proposed by Read(1991),the quantity of organic matter and the quality of nutrients in the soil are the key factors governing the global distribution of AM-and EM-dominated vegetation types.At the global scale,shifts from lower to higher latitudes or altitudes lead to fundamental changes in the nature of the soil as a nutrient source for plants(Read,1991;Read and Perez-Moreno,2003).Here,we explored the influence of AM and EM on soil respiration in different level.

2.Effect of mycorrhizas on root respiration

Generally,mycorrhizal respiration is considered as aitotrophic repiration due to mycorrhizas associated with plant roots.Few studies differentiate mycorrhizal respiration from root respiration.However,mycorrhizal contribution to soil respiration intrigue several researches,for example Routien and Dawson(1943)showed that mycorrhizas can improve root respiration.By far,10 plant species are reported on the effect of mycorrhizas on root respiration(Table 2-1).

It is well known,there are about 200 arbuscular mycorrhizal fungal species.Few AM fungal species were studied in influencing soil or root respiration.The report on ecto-mycorrhizal fungal species is fewer comparing to AM species.By far,only one species of ecto-mycorrhizal fungal species is reported to effect soil respiration.In large ecosystem level,one study has shown that ECM played a key role in soil respiration in forest systems(Högberg et al.,2001).By tree-girdling involves stripping the stem barks to the depth of the current xylem at breast height,they terminated the supply of current photosynthates to roots and their mycorrhizal fungi without physically disturbing the delicate root-microbe-soil system.Their results showed that girdling reduced soil respiration within 1～2 months by about 54％ relative to respiration on ungirdled control plots,and that decreases of up to 37％ were detected within 5 days.

The majority results showed that mycorrhizas enhanced root respiration of hostplants(Table 2-1).When different mycorrhizal types were considered,all ecotomycorrhizas and almost all arbuscular mycorrhizas improved root respiration.The root respiration was enhanced from −29.0 to 94.3 in arbuscular mycorrhizas.The biggest increase of ectomycorrhiza to soil respiration was 709.4％ comparing to nonmycorrhizal respiration.And the minimum increase is also to 17.0％.The all studies showed that mycorrhizas can influence root respiration.

3.Effect of mycorrhizas on temperature sensitivity of soil respiration(Q₁₀)

The response of soil respiration to climate warming,which usually is called apparent temperature sensitivity of soil respiration(Q₁₀ value)and estimated based on empirical functions,is of importance in predicting the direction and magnitude of terrestrial carbon cycle feedback to climate warming(Davidson et al.,2006;Zhou et al.,2009).Therefore,empirical response functions are still a valid method to derive annual estimates of soil respiration based on specific field measurements(Savage et al.,2008).Currently,The Q₁₀ of RS has been a focus of soil respiration research and is widely reported in numerous literatures.

Boone et al.(1998)indicated that root played a valuable role in affecting Q₁₀ value by comparing root-zone soil with the Q₁₀ of 4.6 and non-rhizosphere soil.Our results also showed that the effect of mycorrhizal colonization on Q₁₀ of soil respiration is varied(Table 2-2).The host plant of Picea abies inoculated Piloderma croceum(ectomycorrhizal fungi)increased 20％ of Q₁₀ of soil respiration.However,other studies including arbuscular-and ecto-mycorrhizas do not significantly change the Q₁₀ of soil respiration.

The reasons that Q₁₀ of soil respiration wasn't changed possibly attributed to other environment factors.We analyzed further the results of Q₁₀.We found that the results coming from field in-situ is significantly increased,but those conducting in control conditions with the sterilized soil are not(Table 2-2).Probably,the external hypha associated with plant roots are not limited under field conditions so that soil zone influenced is bigger than nonmycorrhizal controls,which result in abundant soil microorganisms in root and mycelium rhizosphere to absorb more carbohydrate from host plant(Staddon et al.,2003).Therefore,the process increased the breath and its sensitivity to temperature.

4.Effect of mycorrhizas on soil basal respiration

There are numerous external hypha of mycorrhizal fungi distributed in soil.Our study showed there is about 5 meter hypha each gram soil(Shi et al.,2011),which is a kind of important component of soil respiration.Moyano et al.(2007)compared the soil respiration between basal soil and external hyphal soil in a barley field,which had shown that the soil respiration rate was higher significantly in mycorrhizal hyphae soil than in basal soil without hyphae.Further,their study showed that respiration values for basal,rhizosphere and mycorrhizal respiration presented different trends with the increase of temperature from−2℃ to 22℃.Soil respiration with mycorrhizal hyphae did not increased with the increase of temperature.However,the soil respiration in basal soil without mycorrhizal hyphae enhanced markedly with the increase of temperature(Moyano et al.,2007).This conclusion may explain the reason why the change of Q₁₀ is slightly with the changes of temperature when roots are colonzed by mycorrhiza.Heinemeyer et al.(2006)confirmed the above hypothesis in AM by a heating trial.They found the respiration of mycorrhizal external hyphae increased in the early stage of heating.Then,the mycorrhizal hyphae presented adaptivity to heating.Malcolm et al.(2008)also got the similar conclusion in ectomycorrhizal by incubating hyphae of 12 isolates for a week at one of three temperatures and measuring respiration over a range of temperatures,which also showed that ECM acclimate to temperature and in their sensitivity to temperature.

5.Mycorrhizal fungal respirations

Mycorrhiza,as a kind of soil microorganisms,also released CO₂ by its breath,which influenced the soil respiration but its effects on roots and other soil microorganisms.Moreover,the respirations of mycorrhizas have caused the attention of ecologists.Moyano et al.(2007)measured the contribution of arbuscular mycorrhizal external hypha in filed,which showed that AM hyphal respiration reached the 6.1％ of total respiration in whole growing season with the maximum value of 19.1％ out of total soil respiration.Heinemeyer et al.(2006)studied the external hyphal respiration of AM fungal species of Glomus mosseae under ambient and warming temperature by a two-room root box.Their results showed that the mycorrhizal hyphal respiration got to 0.2 μg C/g/d and 0.003 μg C g⁻¹·d⁻¹ in ambient and warming temperature,respectively.At the same time,the ECM respiration was easier than AM due to its culture characteristics.Hacskaylo et al.(1965)had shown that the respiration values of six ECM species including Amanita rubescens,Suillus luteus,S.punctipes,Cenococcum graniforme,Rhizopogon roseolus and Russula emetic were 285.71µL/g,571.43µL/g,267.14µL/g,1708.57µL/g,1467.14µL/g and 524.29µL O₂/g Fresh weight/h at seven temperatures from 7℃ to 35℃.Souto et al.(2000)got the respirating value of Hymenoscyphus ericae and Hebeloma crustuliniforme were 2865 nmol O₂/g and 3914 nmol O₂/g fresh weight/min,respectoively.The basal rates of oxygen consumption of Laccaria laccata and Cenococcum graniforme were,respectively,(3134 ± 757)and(2790 ± 711)nmol/L O₂/g dry weight/rain(Boufalis et al.,1994).

Although previous studies showed that mycorrhizal respiration value varied with the mycorrhizal types and fungal species,they also confirmed mycorrhizal respiration was an important component of soil respiration.

6.The factors to influence mycorrhizal respiration

The influences of mycorrhiza on root respiration were affected by other factors(Table 1-1).As the symbiotic association between roots and mycorrhizal fungi,it included two parts of plant roots and mycorrhizal fungi.Therefore,it is necessary that the species of plant roots and mycorrhizal fungi would affect the role of mycorrhiza to soil rescpiration.Martin and Stutz(2004)inoculated three kinds of mycorrhizal fungi(G.intraradices,G.AZ112 and a mixed inoculum of G.intraradices and G.AZ112)in Capsicum annuum to explore the effect of mycorrhizal fungi colonization on root respiration under two temperature conditions,which showed that root respiration rate were different with the variation of different mycorrhizal fungal inocula with the respiration of G.intraradices>mixed inoculum>G.AZ112.Langley et al.(2005)studied the effect of various mycorrhizal treatments to sunflowers(Helianthus annuus)in chambers and continuously monitored belowground(root+mycorrhizal+heterotrophic)CO₂ production during plant growth,death,and decomposition,which indicated that although mycorrhizal inoculation increased overall rhizocosm respiration,changes of respiration depended on different mycorrhizal fungal inoclua.Hacskaylo et al.(1965)analised six ECM fungal respirations and showed that Cenococcum graniforme and Rhizopogon roseolus respired at much greater rates at all temperatures during the 90 min than did the other four species.These previous studies showed that the effect of mycorrhiza depended on the fungal taxa.

On the other hand,host plant is another important factor to affect symbiotic respiration.Snellgrove et al.(1982),Valentine and Kleinert(2007)and Silsbury et al.(1983)inoculated the same mycorrhizal fungi of G.mossese to three different host plants(Allium porrum,Lycopersicon esculentum,Trifolium subterraneum)to monitor the changes of root respiration,which indicated that the root respiration of Allium porrum and Lycopersicon esculentum increased significantly,however,Trifolium subterraneum slightly decreased.The same conclusion was drawn when inoculated AM fungusof G.intraradices to different host plants.

Additionally,environmental factors also played vital roles in the effect of mycorrhiza on soil respiration.Martin and Stutz(1994)employed the same host plant of Capsicum annuum and mycorrhizal incolum to study the changes of root respiration at different temperature,which showed that colonized root respiration changes were affected by growing temperature.As to ECM,Hacskaylo et al.(1965)meased the fungal respiration of six fungi of Amanita rubescens,Suillus luteus,S.punctipes,Cenococcum graniforme,Rhizopogon roseolus and Russula emetic at seven different temperature of 7℃,13℃,18℃,24℃,29℃,32℃ and 35℃ and concluded that fungal respiration varied with the changes of temperature.Generally,nutrient status,especially phosphorus affected the form of mycorrhizal symbiosis between plant roots and soil fungi.However,the effect of P concentration on mycorrhizal respiration was uncertain(Table 2-1),while a lot of researches drew the contrary conclusion by the P trials(Mortimera et al.,2008;Baas et al.,1989;Raiesi and Ghollarata,2006).Routien and Dawson(1943)studied the effect of mycorrhizal fungus on the root repiration of Pinus echinata at different nitrogen levels,which demonstrated that the effect of mycorrhiza on root respiration increased with the raise of N level.Mortimera et al.(2008)showed that the different growing season was a factor that affects mycorrhizal respiration of Phaseolus vulgaris,which lead to the effect from positive to negative.

7.Conclusions

The slim change of soil respiration will lead to the dramatic fluctuation of the atmospheric CO₂ concentration.In terrestrial ecosystems,symbiotic associations between plant roots and mycorrhizal fungi are near ubiquitous,with 90 per cent of all plant species forming mycorrhizas.At the global scale,although there are seven type mycorrhizas,plants with arbuscular mycorrhizas(AM)and Ectomycorrhizas(EM)are the dominant components of the major world biomes today.A few studies have testified that mycorrhizas including AM and EM play indispensable role in soil respiration while it is difficult to be determined.The advances in the influence on mycorrhizas to soil respiration were summarized in this paper.The results have shown that mycorrhizas have greater enhancement on the soil respiratory and minor influence on temperature sensitivity(Q₁₀).The possible ways included(1)to improve the respiration of plant roots,(2)to consider mycorrhizas as a component of respiration,and(3)to enhance the respiration in bulk soil.Furthermore,the mycorrhizal function in soil respiration is affected by all kinds of factors including biotic and abiotic factors.Mycorrhizal external hyphae expressed the acclimation to the temperature.The reports about the mycorrhizal contribution to soil respiration are by far comparatively few.Recently,the key role of mycorrhizas in soil respiration has been gradually recognized.It will be helpful for us to predict the CO₂ flux from soil during the climatic changes if mycorrhizal roles in soil respiration are examined properly.