Key words: Kctomycorrhizas, soil moisture, growth, Descolea maculata, Pisolithus tinctorius, Laccaria laccata. Eucalyptus diversicolor.
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1 Ne7v Phytol. (1990), 114, Effects of high soil moisture on formation of ectomycorrhizas and growth of karri (Eucalyptus diversicolor) seedhngs inoculated with Descolea maculata, Pisolithus tinctorius and Laccaria laccata BY N. L. BOUGHER AND N. MALAJCZUK Division of Forestry and Forest Products, CSIRO Private Bag, P.O. Wembley, Western Australia 6014 {Received 10 May 1989 ; accepted 6 Septejnber 1989) SUMMARY Seedlings of Eucalyptus diversicolor F. MuelL inoculated with the ectomycorrhizal fungi Descolea maculata Bougher (two isolates), Pisolithus tinctorius (Pers.) Coker & Couch and Laccaria laccata (Scop, ex Fr.) Berk. & Br. were raised under glasshouse conditions in a yellow sand at a gradient of four soil moisture levels ranging from above field capacity to near waterlogged. All fungi enhanced growth of seedlings above that of uninoculated seedlings, but in soils near saturation there was no response to inoculation. Reduced mycorrhizal formation in relation to increasing soil moisture occurred to various degrees for all fungi. This was particularly marked with Pisolithus tinctorius. In contrast, Laccaria laccata maintained a relatively high number of mycorrhizal roots at all moisture levels applied, except at the wettest soil treatment. An isolate of Z). maculata from a swamp environment did not produce a greater number of mycorrhizal roots at high soil moisture than an isolate of this species from a forest environment. Key words: Kctomycorrhizas, soil moisture, growth, Descolea maculata, Pisolithus tinctorius, Laccaria laccata. Eucalyptus diversicolor. INTRODUCTION Various soil moisture regimes. Worley & Hacskaylo (1959) reported that frequency of watering in- Mycorrhizal fungi and tree root activity are adversely fluenced infection rate by two ectomycorrhizal fungi affected by extremes of soil moisture. At low soil on P;>n«uzVg/w/awa Mill, seedlings, with each fungus moisture loss of cell turgidity may occur (Mexal & responding differently. In a study of ectomycorrhizas Reid, 1973) while in very wet soils, oxygen deficiency of Piims radiata D. Don the colonization of roots by severely limits fungal activity (Slankis, 1974). Ecto- various fungi varied with soil moisture, although the mycorrhizal fungi are strongly aerobic (Melin, 1953; activity of all fungi was depressed in near-saturated Harley & Smith, 1983) and good aeration is required soils (Theodorou, 1978). for their development on roots (Read & Armstrong, Few studies have simultaneously examined the 1972; Meyer, 1974; Mosse, Stribley & LeTacon, effect of soil moisture on both plant growth and 1981). Depletion of oxygen in soil not only alters the development of ectomycorrhizal roots. The objective chemical and physical properties of the soil of this study was to determine the effect of a range of (Ponnamperuma, 1984) but also root physiology soil moisture levels on mycorrhizal root formation such as permeability to nutrients (Slankis, 1974). and plant growth stimulation by four isolates of Consequently, mycorrhizal infection, development, ectomycorrhizal fungi inoculated onto seedlings of and subsequent phosphorus uptake are restricted by karri (Eucalyptus diversicolor F. MuelL). These excessive moisture (Wojciechowska, 1960; Gadgil, included, two isolates of D«To/ea «(aa</a/a collected 972; Theodorou, 1978). from paperbark {Melaleuca) swamp and Eucalyptus As is the case with plants, individual species of forest sites respectively. Other fungi were Pisolithus mycorrhizal fungi also have different tolerances to tinctorius (Pers.). Coker & Couch, which often
2 88 ^, Bougher and N. Malajczuk produces fruit bodies in quite dry environments, and Laccaria laccata (Scop, ex Fr,) Berk, & Br,, which most often occurs in wetter environments. MATERIAI.S AND METHODS Soil preparation A P-deficient yellow sand from the Spearwood dune system north of Perth, Western Australia (ph 5-4; Bray-extractable P less than 2 mg P kg"^ soil, G, M, Dimmock personal communication) was steam sterilized at 80 C for 1 h, and then oven-dried at 70 C, The sand was sieved through a 2-5 mm mesh and 2500 g placed in each plastic pot which was lined with a plastic bag. Nutrients were applied in solution to the soil surface at the following rates: 50 mg K, 29 mg Ca, 18 mg N, 4-2 mg Mn, 3-3 mg Mg, 2-1 mg Zn, 2-1 mg Cu, 0-25 mg Mo, 0-12 mg B and 0-08 mg Co (all kg"' soil). After the soils were dried at 35 C, these nutrients and phosphorus as powdered Ca(H2POj2.H2O were thoroughly mixed into the soil. A rate of 24 mg P kg"' soil was applied to all pots. This rate of soil P was selected to facilitate mycorrhizal root formation (tbe main emphasis of the experiment), while also allowing only relatively small difterences in plant size due to the various inoculation treatments (based on Bougher, Grove & Malajczuk, 1990), All soils were maintained at Held capacity ( 20 kpa, 2-5 % soil moisture content) for 28 days after planting before establishment of 4 moisture regimes: level 1, 4-5 kpa ( 6 % soil moisture content); level 2, 2-25kPa ( 8 % soil moisture); level 3, 0-63 kpa (12% soil moisture); level 4, 0-14kPa (20% soil moisture). Saturation point of the soil was approximately 23 % soil moisture. Soil moisture levels were maintained by regular watering to weight every 24 h (48 h initially when water loss was very slow). associated with Melaleuca preissiana Shau,, Eucalyptus marginata Donn ex Smith, and Astartea sp, near Jandakot, W.A, The other fungi used were an isolate of Pisolithus tinctorius (Pers,) Coker & Couch culture H98 from a E. marginata woodland near Busselton, W.A,, and an isolate of Laccaria laccata (Scop, ex Fr.) Berk. & Br. CLilture E439 from a E. microcorys F. Muell. plantation near Dwellingup, W.A. The ability of all fungal isolates to form ectomycorrhizal roots with karri was determined in preliminary trials. Control seedlings did not receive inoculum. Dishes were incubated at 25 C under a daily 18 b pbotoperiod giving 121 /te s"' m"'. Fungal colonization on roots was monitored regularly. After 15 days incubation seedlings from tbe P. tinctorius inoclilation treatment were planted in pots. All otber inoculation treatments were transplanted after 20 days to account for the slower growth of these fungi. Three seedlings were planted in each pot. Following establishment seedlings were thinned to two per pot. Nitrogen was applied in a solution of NH^NO., at 3-weekly intervals (18 mg N kg"' soil). There were four replicate pots of each fungus-moisture treatment combination. Pots were randomly arranged, and glassbouse benches were rotated weekly. Seedling heights were recorded at 15-day intervals. Average daily glasshouse temperatures ranged from 18 C n-iinimum, to 27 C maximum. Plant harvest and measurements Seedlings were harvested (in mid-april) 100 days after planting. Shoots were excised at the soil surface and dried at 70 C. Four soil cores (20 mm diam.) extending to the bottom of tbe pot were removed from each pot. Soil cores (minus a subsample) and tbe remaining roots in the pots were washed free of soil and oven-dried. A subsample g extracted from washed cores was stained in 0-1 % Fungal inoculum and plant culture trypan blue in lactic acid for min and the total Eucalyptus diversicolor seed was surface sterilised by root length (L,^) estimated by a line intercept metbod shaking in a solution of H,,O,j/absolute etbanol (1 :1 (Newman, 1966), modified to account for the v/v) for 15 min. After five rinses in sterile distilled presence of large coarse roots in the pots, by relating water, seeds were transferred to Fetri dishes with the total root length of the core sample to that of the potato dextrose agar, and incubated in darkness at total pot by volume of soil rather than by weigbt of 24 C for 4-5 days. Germinated seedlings were then roots: transferred aseptically in batches of 10 to dishes with actively growing 20- to 30-day-old fungal colonies Total /L, core / vol. of soil in pot I I " I.. 1 on a modified Melin-Norkrans medium. Fungal sample/1 V vol. of soil in core/ Liipot/ isolates used included two isolates of Descolea maculata Bougher - culture E477* from litter in An estimate of total ectomycorrbizal root lengtb was forest dominated by Eucalyptus jacksonii Maiden and obtained by multiplying total L,^ by tbe proportion E. diversicolor, near Walpole, Western Australia, and of root tips tbat were ectomycorrbizal. Sbort roots culture UWA 337Ot from a paperbark swamp with complete development of a fungal mantle were scored as mycorrhizas. * E and II codes refer to CSIRO Division of P^orestry and Treatment effects were assessed using analysis of Forest Products fungal collection, t UWA = University of Western Australia MycoloKy variance and Duncan's new multiple range test Herbarium, (Duncan, 1955).
3 Effect of soil moisture on formation of ectomycorrhizal karri seedlings 89 RESULTS At the lowest soil moisture used (level 1, 4-5 kpa), the biomass of uninoculated seedlings was less {P < 0-05) than with all other inoculation treatments (Table 1). At moisture levels 2 and 3 seedlings inoculated with P. tinctorius were heaviest, but at the highest soil moisture applied (level 4, 0-14kPa), inoculated seedlings were no heavier than uninoculated seedlings. Seedlings inoculated with the D. macidata sv^'amp isolate were taller than all others in the driest soil after about 60 days following planting (Fig. 1 a). In contrast, at soil moisture levels 3 and 4, seedlings of this inoculation treatment were the shortest [Fig. 1 c, d)]. P. tinctorius seedlings were the tallest at soil moisture levels 2 and 3 [Fig. b, c)]. Seedlings of all inoculation treatments, except for the D. maculata forest isolate, had a declining frequency of mycorrhizal root formation in relation to increasing soil moisture, and this was particularly marked with Pisolithus tinctorius (Fig. 2). Seedlings inoculated with the forest isolate of D. maculata had the greatest frequency of mycorrhizal roots (Fig. 2) and the greatest length of mycorrhizal roots (Fig. 3) at soil moisture level 2. L. laccata produced the greatest frequency of mycorrhizal roots at all soil moistures. A similar pattern to that which occurred with frequency of mycorrhizal roots in relation to soil moisture (Fig. 2), was also evident with ectomycorrhizal root length data (Fig. 3). The mycorrbizal root length of seedlings inoculated with the D. maculata swamp isolate was lower than tbat of seedlings witb all other fungi at all soil moisture levels. Seedlings inoculated with L. laccata had greater mycorrhizal root length at all soil moistures than seedlings of all other fungal treatments except at level 1 (at which P. tinctorius seedlings had the largest mycorrhizal root length). DISCUSSION Fnhancement of plant growth, which is a major effect of mycorrhizal infection in general (see Harley Seedling age (days) Figure 1. Height of karri (Eucalyptus diversicolor) seedlings at 15-day intervals for each mycorrhizal fungus inoculation treatment. Seedlings growing in soil at (a) moisture level 1 ; (b) moisture level 2; (c) moisture level 3; (d) moisture level 4. Each point represents the mean of data for 8 seedlings. Bars represent standard error of the mean. D, Descolea macidata (forest); O, D. maculata (swamp); O, Pisolithus tinctorius; A, Laccaria laccata; %, Control (LJninoculated).
4 " " ^ - v ^ '. 90 ^. Bougher and N. Malajczuk Table 1. Dry weight (g) of karri (Eucalyptus diversicolor) seedlings for each mycorrhizal fungus treatment/soil moisture level combination Inoculation treatment Soil moisture Level...! Content... (6%) (8%) 3 (12%) 4 (20%) Descolea maculata (forest) D. maculata (swamp) Pisolithus tinctorius Laccaria laccata Control 8-51 a 7-23 a 899a 1-11-A 3-84b 6-06 a 6-66 a 1007 b 7-24a 6-65ab 4-49 a 10-97c 7-97 b 5-56ab 3-22 a 7-47 b 6-04 b Each value represents the mean of data for 8 seedlings. Means within columns with the same letter are not significantly different (P < 0-05) by Duncan's (1955) new multiple range test. In analysis of variance there was no significant interaction, the fungal treatment was significant, and the soil moisture treatment was not significant. & Smith, 1983), occurred for some karri seedlings with mycorrhizal roots in the present experiment. In a previous study with karri (Bougher, Grove & Malajczuk, 1990), a yellow sand with 16mgPkg"^ soil or higher did not yield larger mycorrhizal than non-mycorrhizal plants. However, in that study P. tinctorius was inactive (due to low temperature). The absence of a plant growth response with D. maculata and L. laccata in soil with 16 mg P kg"' soil or higher in the previous study may be attributable to a soil moisture eftect, because in the present study growth responses with these fungi occurred only in the driest soil. This experiment has shown that the ability of a fungus to form mycorrhizal roots under any given set of conditions does not always equate with AI I I I increased growth of the host. For example, at soil moisture levels 2 and 3, mycorrhizas of all fungi tested were present, but only Pisolithus tinctorius conveyed a growth response to the seedlings. Another example is that a plant growth response with Laccaria laccata occurred only at tbe lowest soil moisture applied, despite tbe maintenance of a relatively large number of mycorrhizas for this fungus at all soil moistures except tbe wettest soil. In the case of Pisolithus tinctorius, there was a sharp reduction in mycorrbizal roots in relation to increasing soil moisture, as would be expected in line witb its preference for drier environments compared with those in which Laccaria laccata is usually present in tbe field. However despite tbe reduction in mycorrhizas, Pisolithus tinctorius stimulated the growtb of seedlings at moisture levels 2 and 3, in addition to level 1. The swamp isolate of D. maculata did not produce more mycorrbizal roots tban tbe forest isolate of this & 25 o "S 20 I 10 X X X X X. X. - o n -- ' 4-5 Soil moisture level Level 2 Soil water potential (-kpa) A n. OA. o o-.. n Level 3 Level 4 Figure 2. Proportion of karri (Eucalyptus diversicolor) seedling short roots which were ectomycorrhizal, in relation to soil moisture. Each point represents the mean of data for 8 seedlings. Bars represent standard error of the mean. D, Descolea maculata (forest); O, D- maculata (swamp); O, Pisolithus tinctorius; A, Laccaria laccata. C O ~ O T3 > a> E "» o ^ CJ CJ CD CL E OJ O O^ A D- - O 4-5 Soil moisture level 1 ^ x.^ I A'''". ^ ^ -. " ~ 225 Level 2 Soil water potential (-kpa) 11 I A o ": Level 3 Level 4 Figure 3. Total ectomycorrhizal root length of karri (Eucalyptus diversicolor) seedlings, in relation to soil moisture. Each point represents the mean of data for 8 seedlings. Bars represent standard error of the mean. Symbols are as given in Fig. 2, legend.
5 Effect of soil moisture on formation of ectomycorrhizal karri seedlings 91 species (or any of the other fungi tested) in wet soil, this work was carried out during the tenure by the senior in spite of its prolific basidiome production in author of a Commonwealth Postgraduate Award. swampy habitats (Bougher & Malajczuk, 1985). In other fungi there is not always a direct relationship between numbers of mycorrhizas and numbers of basidiomes (e.g. Menge & Grand, 1978). However, R E F E R E N C E S the results of this experiment may also imply that ANDERSON, R. C, EBBERS, B. C. & L I B E R M, A. E. (1986). Soil moisture influences colonisation of prairie cordgrass (Spartina other key factors besides soil moisture may be pectinata Lind.) by vesicular-arbuscular mycorrhizal fungi. involved in governing its proliferation in the field. Neiv Phytologist 102, One such factor could be the extreme seasonal ANDERSON, R. C, LIDERTA, A. E. & DICKM.^N, L. A. (1984). Interaction of vascular plants and vesicular-arbuscular mycorfluctuations in soil moisture characteristic of the rhizal fungi across a soil moisture-nutrient gradient. Oecologia periphery of paperbark {Melaleuca) swamps. 2, 64, Seasonal conditions such as prolonged drought or BOUGHER, N. L., GROVE, T. S. & MALAJCZUK, N. (1990). Growth and phosphorus acquisition of karri (Eucalyptus diversicolor F. other stress conditions are considered important Muell.) seedlings inoculated with ectomycorrhizal fungi in factors in determining colonization of roots by VA relation to soil phosphorus supply. New Phvtologist 114, fungi (Anderson, Liberta & Dickman, 1984; Ander- BOUGHER, N. L. & MALAJCZUK, N. (1985). A new species of Descolea (Agaricales) from Western Australia, and aspects of its son, Ebbers & Liberta, 1986). Another factor may be ectomyeorrhizal status. Australian Journal of Botany 33, the amount of organic matter in the soil. The sand used in this experiment may have favoured mycor- DUNCAN, D. B. (1955). Multiple range and multiple F tests. Biometrics 11, rhiza formation by L. laccata and P. tinctorius over D. maculata, since the former two fungi are often GADGIL, P. D. (1972). Effect of waterlogging on mycorrhizas of radiata pine and douglas fir. New Zealand Journal of Forest common in areas low in organic matter such as road Science 2, sides and mine sites. Components of the natural soil HARLEY, J. L. & SMITH, S. E. (1983). Mycorrhizal Symbiosis. Academic Press, New York. microflora (which may have been absent from the MELIN, E. (1953). Physiology of mycorrhizal relations in plants. steam-sterilized pot soil used in this study) may be Annual Revietv of Plant Physiology 4, required to stimulate more extensive mycorrhizal MENGE, J. A. & GRAND, L. F. (1978). Effect of fertilization on production of epigeous basidiocarps by mycorrhizal fungi m formation by all or some of the fungi (Slankis, 1974; loblolly pine plantations. Canadian Journal of Botiinv 56, Mosse, Stribley & LeTacon, 1981). In addition, MEXAL, J. & REID, C. P. P. (1973). The growth of selected other abiotic soil factors may be involved. mycorrhizal fungi in response to induced w ater stress. Canadian All fungi formed fewest mycorrhizal roots in the Journal of Botany 5, Wettest soil tested in this experiment. Growth of MEYER, F. H. (1974). Physiology of mycorrhiza. Annual Review of Plant Physiology 25, ectomycorrhizal fungi may be curtailed by conmosse, B., STRIBLEY, D. P. & LETACON, F. (1981). Ecology of tinuous (Theodorou, 1978) or intermittent watermycorrhizae and myeorrhizal fungi. In Advances in Microbial logging (Gadgil, 1972), and this can be attributed to Ecology (Ed. by M.Alexander), pp Plenum Press, New York. the deleterious effects of a reduction in free oxygen NEWMAN, E. I. (1966). A method for estimating the total length of on ectomycorrhizal formation and efficient nutrient a root in a sample. Journal of Applied Ecology 3, uptake (Read & Armstrong, 1972; Slankis, 1974). In PONNAMPERUMA, F. N. (1984). Effects of flooding on soils. In Flooding and Plant Growth (Ed. by T. T. Kozlowski), pp the wettest soil treatment, reducing soil conditions Academic Press, New York. possibly developed : the odour of HjS was evident READ, D. J. & ARMSTRONG, W. (1972). A relationship between during the harvest of these pots. In addition, oxygen transport and the formation of the ectotrophic mycorrhizal sheath in conifer seedlings. New Phytologist 71, impaired seedling performances may also have SLANKIS, V. (1974). Soil factors influencing formation of mycorcontributed to the inability of the mycorrhizal fungi rhizae. Annual Review of Phytopathology 12, to increase the growth of karri seedlings in the THEODOROU, C. (1978). Soil moisture and the mycorrhizal association of Pinus radiata D. Don. Soil Biology and BioWettest soil. However, since the size of uninoculated chemistry 10, seedlings was not reduced at the highest soil moisture WOJCIECHOWSKA, H. (1960). Studien uber den mykotrophismus applied (in comparison with seedlings at other soil der fichte (Picea excelsa Link.) in den nordlichen verbreitungsgrenzen mit besonderer berueksichtigung des mykotrophismus moistures), this was evidently not a major factor. ACKNOWLEDGEMENTS We thank Shirley Snelling for her technical assistance, and I lm Grove for his advice on the study. The major part of der phanzengesell-schaften in der forsterie lipowo, oberforsterei sadlowo bei der ortschaft biskupiec reszelski. Folia Forestalia Polonica Series A 2, WORLEY, J. E. & HACSKAYLO, E. (1959). Effect of available soil moisture on the mycorrhizal association of Virginia pine. Forest Science 5,
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