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Plant and Soil 252: 279290, 2003. 2003 Kluwer Academic Publishers. Printed in the Netherlands.
The production of ectomycorrhizal mycelium in forests: Relation betweenforest nutrient status and local mineral sources
David Hagerberg1,3, Gunnar Thelin2 & Hkan Wallander11Dept. of Microbial Ecology, Lund University, Sweden. 2Dept. of Plant Ecology, Lund University, Sweden.3Corresponding author
Received 4 June 2002. Accepted in revised form 28 November 2002
Key words: Apatite, biotite, ectomycorrhizal fungi, forest, nutrient status, Pinus sylvestris
Due to acid rain and nitrogen deposition, there is growing concern that other mineral nutrients, primarily potassiumand phosphorus, might limit forest production in boreal forests. Ectomycorrhizal (EcM) fungi are important forthe acquisition of potassium and phosphorus by trees. In a field investigation, the effects of poor potassium andphosphorus status of forest trees on the production of EcM mycelium were examined. The production of EcMmycelium was estimated in mesh bags containing sand, which were buried in the soil of forests of differentpotassium and phosphorus status. Mesh bags with 2% biotite or 1% apatite in sand were also buried to estimate theeffect of local sources of nutrients on the production of EcM mycelium. No clear relation could be found betweenthe production of EcM mycelium and nutrient status of the trees. Apatite stimulated the mycelial production,while biotite had no significant effect. EcM root production at the mesh bag surfaces was stimulated by apatiteamendment in a forest with poor phosphorus status. The contribution of EcM fungi to apatite weathering wasestimated by using rare earth elements (REE) as marker elements. The concentration of REE was 10 times higherin EcM roots, which had grown in contact with the outer surface of apatite-amended mesh bags than in EcM rootsgrown in contact with the biotite amended or sand-filled mesh bags. In a laboratory study, it was confirmed thatREE accumulated in the roots with very low amounts (
balance calculations in southern Sweden indicates thatpotassium will be an element in short supply in thefuture (Barkman and Sverdrup, 1996).
The nutrient concentrations of the needles are of-ten used to determine deficiency (Foerst et al., 1987).However, the ratios of nutrients to nitrogen are of-ten used instead of absolute concentrations since theyare naturally less variable and at least as importantfor tree vitality (Linder, 1995; Thelin, 2000). In thisstudy, we employed four forest sites with varying po-tassium and phosphorus status, including sites withpotassium or phosphorus levels below the deficiencyvalues reported by Linder (1995) and Thelin et al.(2002).
Ectomycorrhizal (EcM) fungi live in symbiosiswith trees and colonise the soil forming an externalmycelium which contributes to the absorbing surfaceover which mineral nutrients can be taken up by thetrees (Bowen, 1973; Schack-Kirchner et al., 2000).The mineral nutrients are transported to the root tips,where they are translocated into the plant root in ex-change for photosynthetically derived carbon (Smithand Read, 1997). In a boreal forest, close to 100% ofthe fine roots may be colonised by EcM fungi (e.g.Kren and Nylund, 1997).
Studying EcM fungi in the field has been problem-atic since it is difficult to discriminate between my-celia of EcM and saprophytic fungi. However recently,ingrowth mesh bags have been shown to provide goodestimates of EcM fungal growth (Wallander et al.,2001). Wallander et al., (2001) and Hagerberg andWallander (2002) found that 85% of the myceliumcontained in such mesh bags could be related to EcMfungi by comparing the mycelial production in meshbags inside and outside trenched plots. Soil trench-ing inhibits the growth of EcM fungi since the rootsof the host trees are excluded. They also investigatedthe 13C value, which showed that the mycelia insidemesh bags had 13C values similar to values of EcMfruit bodies and distinctly different from the values offruit bodies of saprophytic fungi
EcM fungi are able to mobilise and take up ni-trogen from organic matter (Read, 1991), and theyhave also been reported to supply the trees with po-tassium and phosphorus (reviewed by Marschner andDell, 1994) and magnesium (Jentschke et al., 2000). Inlaboratory experiments, EcM fungi have been shownto improve the uptake of potassium and phosphorusfrom poorly soluble minerals (Wallander, 2000a, b;Wallander and Wickman, 1999; Wallander et al.,1997) and van Breemen et al., (2000) suggest that EcM
fungi are able to selectively weather soil minerals inorder to release mineral nutrients.
In laboratory studies, Ekblad et al. (1995) andWallander and Wickman (1999) have found that po-tassium limitation decreases the growth of myceliumfrom EcM Pinus sylvestris. In contrast, the growth ofEcM mycelium was found to be stimulated by phos-phorus limitation (Ekblad et al., 1995; Wallander andNylund, 1992). This might reflect reduced carbon al-location to the roots in plants growing under potassiumlimitation and an increased allocation to roots in plantsgrowing under phosphorus limitation, as discussed byEricsson (1995).
By forming a dense mycelium, EcM fungi are ableto respond to local sources of organic matter (Bendingand Read, 1995; Carleton and Read, 1991; Finlay andRead, 1986), apatite (Bidartondo et al., 2001), woodash (Mahmood et al., 2001; Hagerberg and Wallander,2002), inorganic nitrogen and phosphorus (Brandes etal., 1998) and local areas of elevated pH (Erland etal. 1990). The dense mycelium is believed to promotethe uptake of elements (Unestam and Sun, 1995) andthe release of organic acids, which can increase thedegradation of organic matter and mineral weathering(reviewed by Dutton and Evans, 1996; Landeweert etal., 2001). Similarly, fine roots of Norway spruce re-spond to local sources of higher nutrient availabilityby increased root proliferation (George et al., 1997).
Dissolution of minerals is a slow process. It is thusdifficult to estimate the contribution of EcM fungi tothe weathering rate over short time periods. Since min-eral nutrients are continuously transported from theroots to the crown, the measurement of nutrient con-tent in EcM root tips is not a good way to estimate theflux of nutrients from a mineral source to the trees. Inthe present study, we investigated the possibility of us-ing rare earth elements (REE) as markers for mineralweathering. REE content can be very high in certainminerals such as apatite. Lanthanum has been shownto be taken up by EcM fungi and is transported tothe root tips. It accumulates in the fungal tissue androot cortex but does not easily penetrate into the stele(Robards and Robb, 1974; Vesk et al., 2000). Con-sequently, lanthanum is primarily found in the plantroots rather than in the foliage or stems, and the otherREE have the same distribution (Fu et al. 2001), in-dicating that they might also be retained in the rootcortex.
The aims of this study were to investigate (1) howthe production of EcM mycelium was affected by thepotassium and phosphorus status of their host trees in
Table 1. Description of the forest sites used in this study
Forest site and Plantation Needle K content Needle K:N Needle P content Needle P:N pHKCl in the organic
reference number year (mg g1) (Thelin et al., (mg g1) (Thelin et al., horizon 1988(Anonymous, 1986) (Thelin et al., 2002) (Thelin et al., 2002) (Berggren et al.,
2002) 2002) 1992)
1994 2000 1994 2000 1994 2000 1994 2000
Bjrstorp (L 3:1) 1941 3.83 4.20 31.2% 36.6% 1.36 1.20 11.1% 10.4% 2.4
Dyneboda (L 6:4) 1936 5.38 4.38 43.5% 49.8% 1.16 0.82 9.4% 9.3% 2.4
Ignaberga (L 7:1) 1951 3.66 3.92 29.6% 32.6% 1.89 1.46 15.3% 12.2% 2.4
Vstra Torup (L 8:4) 1946 1.66 4.97 13.6% 41.4% 1.22 1.24 10.1% 10.4% 2.5
Deficiency levels 4.5 35% 1.3 10%
(Linder, 1995; Thelin
et al., 2002)
the field, (2) how the production of EcM myceliumwas affected by local mineral sources (biotite or apat-ite added to the mesh bag substrate), and how thecolonisation was related to the nutrient status of thetrees, (3) if REE originating from the added miner-als could be detected in root tips growing in contactwith the mesh bags and if we could use these elementsas a measure of mineral dissolution induced by theEcM fungi and (4) if the elemental composition ofthe mineral-amended substrates was changed by theactivity of EcM fungi.
Materials and methods
The field studies were conducted during the years1997 2000. Four monitoring sites in the countyof Skne in southern Sweden used previously forinvestigations of forest damage (Anonymous, 1986)were selected for this study. All of them are plantedwith Norway spruce (Picea abies (L.) Karst.) on aspodosol. The sites were selected in order to be able toinvestigate forest stands with varying K and P statusaccording to Linder (1995) and Thelin et al. (2002).Table 1 shows the nutrient status at the different sitesin the years 1994 and 2000. At Bjrstorp, the K statuswere below the deficiency level for both of the years,although the K:N in the year of 2000 indicated animprovement of the status. The P status of the samesite was slightly above the deficiency level 1994, but
showed a decreasing trend with a P content slightly be-low deficiency level 2000. At Dyneboda, the K statuswas above the deficiency level both years, althoughthe K content had decreased towards the deficiencylevel between 1994 and 2000, whereas the P statuswas below deficiency level both years. At Ignaberga,the potassium status was below and the phosphorusstatus above the deficiency levels both of the years.Vstra Torup exhibited a sufficient P status for bothyears, whereas the K status was below the deficiencylevel in 1994, but not i