Eds. T C Hutchinson and M. Havas. Plenum Press, New York, 654 p. 5 Alexander M and Clark F E 1965 Nitrifying bacteria. In Methods of Soil Analysis. Part 2.
Plant and Soil 88, 2 5 9 - 2 6 7 (1985). 9 1985 Martinus Ni/hoffPublishers, Dordrecht. Printed in the Netherlands.
Ms. 6192
The influence of western hemlock and western redcedar on microbial numbers, nitrogen mineralization, and nitrification DAVID P. TURNER and ELDON H. FRANZ
Environmental Research Center, Washington State University, Pullman, WA 99164-4430, USA Received 29 November 1984. Revised April 1985
Key words Bacteria Fungi Mineralization Nitrification Thu]aplicata
Tsuga heterophylla Summary Microbial numbers in the forest floor and mineral soil (A1 horizon) under large individual western hemlock (Tsuga heterophylla) and western redcedar (Thuja plicata) trees were compared. The lower pH and base saturation of hemlock samples was associated with higher fungal spore counts while cedar samples had higher total microbial counts and populations of ammonium oxidizing bacteria. Nitrogen mineralization rates were gxeater in laboratory incubations of hemlock soil but nitrification was only observed in incubations of cedar soil. These differences in nitrogen mineralization and nitrification are aspects of species-specific nutrient cycling regimes.
Introduction Species-specific soil patches in forested ecosystems have been described both in terms of inorganic soil properties 29,35,s2 and microbial populations12,30. The linkages among ecosystem components by which such differentiation is generated and maintained, however, are not well studied. Direct influences of trees on the microbial environment include effects of (i) the canopy on microclimate (ii) litter quantity and quality on substrate availability (iii) leachates and exudates from leaves and roots on microbial nutrition and possible allelochemical inhibition (iv) ion exchanges by the roots on solution chemistry and (v) mixing by the roots on soil aeration and structure. These influences are significant determinants of the microbial environment and, therefore, of the microbial community. Micro-organisms in turn act as both immobilizers and releasers of plant nutrients and to a great extent regulate nutrient availability in many ecosystems. Evidence from both fiel& 3 and laboratory 28,36 studies suggests that tree species exhibit differences in their patterns of nutrient uptake. There may thus be a relationship between the species-specific influences of trees on the microbial environment, the kinds of micro-organisms that are favored, and the mineral nutrition of the trees. These relationships were investigated in a stand codominated by western hemlock 259
260
TURNER AND FRANZ
(Tsuga heterophylla Sarg.) and western redcedar (Thu]a plicata Donn.) in which there is strong soil differentiation associated with large trees. Fungal spores, heterotrophic bacteria and nitrifying bacteria were monitored in the forest floor and mineral soil horizons under individual cedar and hemlock trees. Nitrogen mineralization and nitrification potentials of the mineral soil horizons were also determined using laboratory incubations.
Study area The mixed stand o f old growth western hemlock and western redcedar is located on a glaciofluvial flat one km south o f the Roosevelt Grove o f Ancient Cedars in northwestern Washington (48'43" N 117'5" W). Elevation is approximately 1 0 7 0 m and annual precipitation averages about 115 cm 1 . No weather stations are maintained locally b u t extrapolation from isotherms published by t h e US Weather Bureau 4a suggests mean minimum and maximum temperatures in July o f less than 9 ~ and 29~ and in January o f less than - - 9 ~ and - - 2 ~ 1 . Trees of both species with diameter at breast height (dbh) greater than 1 m are c o m m o n and the vegetation is classified as the Tsuga heterophylla/Pachistima myrsinites habitat t y p e 17 . Ages of the oldest trees are estimated to be greater than 500 years based on their sizes 29 . Soil profiles under cedar and hemlock trees in Roosevelt Grove are described b y Alban 2 . Methods
Collection of soil samples Three individuals of each species with dbh greater than I m were sampled at monthly intervals during the 1983 growing season. Subsamples of the litter and the AI horizon were collected 1 m from the bole at the four cardinal points and composited. All samples were refrigerated at 0 - 5 ~ for transport to the laboratory and storage prior to analysis.
Laboratory analyses Cones and branches greater than 4 mm in diameter were removed from aft samples and the mineral horizon material was passed through a 2 mm sieve. A 20 g subsample was taken from each sample and dry weight determined at 105~ Total microbial population and fungal spore content were estimated for all fresh litter and soil samples using plate counts la,a2, with five replicates per dilution. Rose bengal streptomyacin agar was used as a medium in the fungal spore counts. Populations of ammonium oxidizing bacteria were estimated using the most probable number technique 3,s with six dilutions and five replicates per dilution. Nitrogen mineralization and nitrification potentials of A1 horizon material were determined by a laboratory incubation technique. The following three treatments were tested using August collected soils: undried soil, air dried soil, air dried soft amended with 20tzg g-1 ammonium-N. The soil for each incubation was subsampled from a composite sample consisting of equal portions of soft from the three field collected samples. The composite sample was moistened to field capacity and sixteen 15 g subsamples were prepared, eight of which were extracted immediately for nitrate, nitrite and ammonium in a 4 : 1 (v/w)saturated CaSO, mixture (2.25 g 1-~ ).
MINERALIZATION IN FOREST SOILS
261
The remaining subsamples were placed in 150 ml polyethylene cups and covered with a double layer of parafilm. These subsamples were incubated in the dark at 25~ and monitored gravimetrically for loss of water. At the end of three weeks they were extracted as described. Extracts were frozen until concentrations were determined using a Technicon Autoanalyzer. Nitrite concentrations were always less than 1 ~g g-i and are not reported. All laboratory work involving micro-organisms was initiated within three days of collection. For determination of chemical properties, litter and soil from the June collection were dried at 30~C to a constant weight, pH was measured with glass electrodes using 0.01 M CaC12 at a 2/1 (v/w) ratio after 1/2 hr equilibration. Sodium acetate (0.73 N) extractable phosphorus and ammonium acetate (1 N) extractable cations were determined at the University of Idaho Soil Testing Laboratory, using inductively coupled plasma analysis for the cations. Cation exchange capacity (CEC) was based on the method of Chapman H , organic carbon on a modified Walkey-Black procedures and total nitrogen on Kjeldahl digestion ~~.
Results
Soil characteristics Forest floor and upper mineral horizon (A1) characteristics are summarized in Table 1. Samples from under large cedar trees had consistently higher pH, extractable calcium and base saturation than those from under hemlock trees. The results are similar to those of Alban 2 w h o also reported higher exchange acidity due to aluminum in hemlock soils. Soil from between trees has intermediate properties 1 which supports the conclusion that individual trees strongly influence soil development in their proximity. Microbial analyses Microbial population sizes fluctuated from m o n t h to m o n t h but the pattern in their relative proportions remained constant and only results from the July sampling are reported here. Overstory tree species had significant effects on composition and relative dominance of the microbial community (Table 2). Consistently higher total microbial counts and greater numbers of ammonium oxidizing bacteria were associated with cedar trees. Fungal spore counts on the other hand were higher under hemlock. In comparisons between the forest floor and the mineral soil total microbial counts were higher in the forest floor. A similar pattern was observed for the fungal spores with the exception of hemlock in July. For ammonium oxidizing bacteria, populations were higher in the A1 horizon than the forest floor. Counts of all micro-organisms were highest in June and lowest in August during the relatively dry part of the year. Laboratory incubations Net production of ammonium and nitrate by soil type and treatment are given in Table 3. Nitrogen transformation rates were lowest
262
T U R N E R AND F R A N Z
Table 1. Forest floor a n d mineral soil (A1 horizon) characteristics Ca Location
Mg
NaOAc-P /zgg-I
pH
K
CEC
Base Total Organic saturation nitrogen carbon
(meq/100g)
(%)
Forest floor Cedar Hemlock
4.7 a* n.d. 3.9 b n.d.
30.0 a 8.8 b
3.99 a 2.18 b
1.17 a 48.6 a 1.26 a 46.4 a
74.2 a 26.7 b
1.09 a 1.25 b
30.4 a 34.2 a
5.0 a 3.5 b
40.3 a 9.5 b
4.17 a 2.10 b
0.78 a 60.0 a 1.09 b 52.9 a
76.7 a 23.8 b
1.20 a 0.95 b
28.3 a 27.7 a
Mineral soil Cedar Hemlock
20.5 a 10.5 b
* Different superscripts in two w a y comparisons indicate significantly different m e a n s (P < 0.05/t-test). Table 2. A m m o n i u m oxidizing bacteria, fungal spores a n d total microbial c o u n t s for July, 1983
Location
% H20 (field)
Ammonium oxidizing bacteria X 10 ~ g-l
Fungal spore count X 104 g-i
Total microbial count X 10 ~ g-i
74.8 a* 74.7 a
3.13"* 0.51
22.4 a 34.3 b
6.48 a 4.91 b
65.0 a 72.9 b
4.86 0.81
20.5 a 38.6 b
3.28 a 2.76 a
Forest floor Cedar Hemlock
A1 horizon Cedar Hemlock
* Different superscripts within comparisons of cedar and hemlock indicate significantly different m e a n s (P < 0.05/t-test). ** The 95% confidence limits are determined b y multiplying a n d dividing by 3.3. Table 3. Mineralization a n d nitrification potentials o f softs in three week incubations. Nitrification % = nitrate production]total nitrogen mineralized
Treatment
Final ~ g g-J )
Production Ozg g-i d-I )
NO3-N
NO3-N
NH4-N
Sum
Nitrification (%)
0.01 a 0.02 a
0.17 a 4.02 b
0.18 a 4.04 b
5.5 0.5
0.65 a 0.00 b
0.66 a 6.54 b
1.31 a 6.54 b
49.6 0.0
2.84 a 8.26 b
54.9 0.0
NH,-N
Field soil brought to ~ield capacity Cedar Hemlock
1.27 a 1.11 a
12.7 a 91.9 b
Air.dried soil brought to field capacity Cedar Hemlock
15.3 a 0.82 b
26.1 a 157.1 b
Air-dried soil brought to field capacity ยง 20 t~gg-1 NI1,-N Cedar Hemlock
34.0 a 0.67 b
53.3 a 211.3 b
1.56 a 0.05 b
1.28 a 8.21 b
* Different superscripts within comparisons o f cedar a n d h e m l o c k indicate significantly different m e a n s (P < 0.05/t-test).
MINERALIZATION IN FOREST SOILS
263
in samples not dried before incubation. Both the drying and the drying plus 20ggg -1 ammonium-N amendment increased nitrogen mineralization. Hemlock soil had consistently higher mineralization rates than cedar soil. Significant nitrification did not occur in hemlock soils under any of the treatments despite ammonium-N levels as high as 211 ggg-1. Ceder soil, however, exhibited nitrification when pre-dried, and nitrate production tracked the higher ammonium levels associated with the ammonium amendment.
Discussion The western h e m l o c k n u t r i e n t cycling regime
An absence of nitrification is one of the characteristic features of the hemlock nutrient cycling regime. Hemlock litter in Alaska4s and hemlock soil from coastal environments in the Pacific northwest 7 have also been shown to have low nitrification potentials, though others have reported nitrification in some hemlock soils 24'5~ The mechanism by which nitrification is inhibited under hemlock trees in the northern Rocky Mountains may involve several factors, particularly the low pH of the soil and forest floor. Soil pH below 4.5 tends to inhibit nitrifying bacteria al and liming has been shown to increase nitrification in many soils where nitrification is otherwise l o w 2s'4~ Higher phenolic contents in leaf and litter leachate may also inhibit nitrifying bacteria a'9. Our assays for total phenolics in extracts of dried leaf material using the Folin-Denis reagent31 showed that hemlock samples contained significantly more tannic acid equivalents per mg (22 vs 4) than cedar samples. The low nitrification in hemlock soil reported here is not due to ammonium limitation. No nitrification was observed in the hemlock incubations with over 200/ag g-1 ammonium-N and some nitrifiers present. This contrasts with the studies using a similar aerobic incubation method by Vitousek et al. s~ in which threshold effects were observed. It is also unlikely that phosporus was limiting to nitrification in this study. Available phosphorus in hemlock samples was higher than the 6/,tg g-i reported by Purchase a7 to restrict nitrification. Phosphorus additions to hemlock soil were not effective in stimulating nitrification in the study of Anderson et al. 7. Mineral nutrition studies 28 have shown greater biomass production by western hemlock seedlings with ammonium as the sole source of nitrogen than with only nitrate. Western hemlock seedlings also responded negatively to liming of the soil~ which was associated with
264
TURNER ANDFRANZ
increased nitrification25. A preference for ammonium has been suggested for other coniferous tree species33 and has been discussed in terms of the lower energy cost of ammonium assimilation compared to nitrate assimilation22 . Relatively acid soil is associated with individual trees of other coniferous species such as Pinus c o n t o r t a s2 and P s e u d o t s u g a m e n z i e s i i ~4 . This pattern is in part a function of organic acids leached from the canopy and decomposing litter on the forest floor. Our laboratory determinations found air dried hemlock leaf material at a 5:1 ratio (v/w) to have a pH of 4.4 after a one hour equilibration period while that of cedar was 6.6. Fungi also exude organic acids 2~ and the acids leached from the canopy, which create an environment favoring fungi over bacteria4, may enhance this production. Other studies 12'19 have shown relatively high fungal/bacterial biomass or spore count ratios in acid forest soils. In addition temporal uncoupling of H-ion generation in the soil due to nutrient uptake, and H-ion consumption associated with organic matter mineralization47, contributes to Hion accumulation, particularly in the case of predominantly ammonium uptake 46 and when the ratio of H-ions extruded to ammonium ions taken up is high, as with hemlock4a . One effect of organic acids in forest soils is to promote podzolization. Metal-organic complexes, resulting from the dissociation of the acids and subsequent chelation of aluminium and iron by the anion, are moved down the profile in the soil solution 44. Alban ~ reported that extracts of western hemlock foilage solubilized more iron than similar extracts of western redcedar, suggesting that the stronger podzolization under hemlock trees was in part a product of organic acids and polyphenols in these extracts. T h e w e s t e r n redcedar n u t r i e n t cycling regime
The litter and mineral soil under cedar has higher pH, exchangeable calcium, base saturation, bacterial populations and nitrification potential than hemlock litter and soil. In sand culture cedar seedlings provided solely with nitrate had greater biomass production than seedlings provided exclusively with ammonium 28 , indicating that nitrate might be preferred. Nitrate nutrition is associated with increased uptake of cations compared with ammonium nutrition 27'36, a relationship apparently based on maintenance of electrical neutrality during nutrient uptake and the involvement of cations in cellular pH regulation during nitrate assimilation 18,38 . The relatively high calcium content of fresh and fallen cedar litter 1,1s and high level of exchangeable calcium in cedar soil suggest the importance of this nutrient to cedar metabolism.
MINERALIZATION IN FOREST SOILS
265
A high level of exchangeable calcium in the soil also acts to buffer the system 49 thus maintaining a pH favorable to nitrifying bacteria. Higher numbers of heterotrophic bacteria in cedar litter are probably a response to both higher pH and substrate differences, with more recalcitrant litter associated with hemlock. In a laboratory comparison 16 of litter decomposition, weight loss of western hemlock litter was appreciably slower than that o f western redcedar litter. Changes in soil properties and nutrient cycling patterns occur at various scales along both temporal a4,ag,4~ and spatiaP 7,z3,z6 gradients. The differentiation in soil properties and microbial communities in mixed stands of western hemlock and western redcedar occurs on a microsite scale. The observation that species-specific patterns in mineral nutrition can be related to such microsite differentiation suggests coevolved linkages between these long lived plants and their associated microbial populations sl . Acknowledgements We thank James Harsh, Phillip SoUins, Richard Mack and John Thompson for reviewing earlier drafts of this paper. Support was provided by the National Science Foundation (Grant DEB 8214285) and the Botany Department at Washington State University.
References 1 2 3
4
5 6 7
8 9 10 11 12
Alban D H 1967 The influence of western hemlock and western redcedar on soil properties. Dissertation. Washington State University, Pullman. Alban D H 1969 The influence of western hemlock and western redcedar on soil properties. Soil Sei. Soc. Am. J. 3 3 , 4 5 3 - 4 5 9 . Alexander M 1965 Most-probable-number method for microbial populations. In Methods of Soil Analysis. Part 2. Ed. C A Black. American Society of Agronomy, Madison, Wisconsin, 1572 p. Alexander M 1980 Effects of acidity on micro-organisms and microbial processes in soil. In Effects of Acid Precipitation on Terrestrial Ecosystems. Eds. T C Hutchinson and M Havas. Plenum Press, New York, 654 p. Alexander M and Clark F E 1965 Nitrifying bacteria. In Methods of Soil Analysis. Part 2. Ed C A Black. American Society of Agronomy, Madison, Wisconsin, 1572 p. Allison L E 1965 Organic carbon. In Methods of Soil Analysis. Part 2. Ed. C A Black, American Society of Agronomy, Madison, Wisconsin, 1572 p. Anderson S, Zasoski R J and Gessel S P 1982 Phosphorus and lime response of Sitka spruce, western hemlock seedlings and romaine lettuce on two coastal Washington soils. Can. J. Forest Res. 12, 9 8 5 - 9 9 1 . Baldwin I T, Olson R K and Reiners W A 1983 Protein binding phenolics and the inhibition of nitrification in subalpine balsam fir soils. Soil Biol. Biochem. 1 5 , 4 1 9 - 4 2 3 . Basabara J 1964 The influence of vegetable tannins on nitrification in soil. Plant and Soil 21, 8 - 1 6 . Bremner J M 1965 Total nitrogen. In Methods of Soil Analysis. Part 2. Ed. C A Black American Society of Agronomy, Madison, Wisconsin, 1572 p. Chapman H O 1965 Cation exchange capacity. In Methods of Soil Analysis. Ed C A Black. American Society of Agronomy, Madison, Wisconsin, 1572 p. Chase R E and Baker G 1954 A comparison of microbial activity in an Ontario forest soil under pine, hemlock and maple cover. Can. J. Microbiol. 1 , 4 5 - 5 4 .
266 13 14 15 16 17
18 19
20 21 22 23
24 25 26 27
28
29
30
31
32 33 34 35 36
TURNER AND FRANZ Clark F E 1965 Agar-plate method for total microbial count. In Methods of Soil Analysis Part 2. Ed. C A Black, American Society of Agronomy, Madison, Wisconsin, 1572 p. Crampton C B 1982 Podzolization of softs under individual tree canopies in southwestern British Colombia, Canada. Geoderma 28, 5 7 - 6 1 . Daubenmire R 1953 Nutrient content of leaf litter of trees in the northern Rocky Mountains. Ecology 3 4 , 7 8 6 - 7 9 3 . Daubenmire R and Prusso D C 1963 Studies of the decomposition rates of tree litter. Ecology 4 4 , 5 8 9 - 5 9 2 . Daubenmire R and Daubenmire J B 1968 Forest vegetation of eastern Washington and northern Idaho. Tech. Bull, 60, Washington Agricultural Experimental Station, Washington State University, Pullman. Dijkshoorn W 1962 Metabolic regulation of the alkaline effect of nitrate utilization of plants. Nature 194, 1656-1660. Flanagan P W and VanCleve K 1977 Microbial biomass, respiration and nutrient cycling in a black spruce talga ecosystem. In Soil Organisms as Components of Ecosystems. Eds. T Persson and U Lohm. Ecol. Bull. (Stockholm) 25,614 p. Franklin J F and Dyrness C T 1973 Natural vegetation of Oregon and Washington. USDA Forest Serv. Gen. Tech. Rep. PNW-8, Griffen P M 1972 Ecology of soil fungi. Richard Clay, Ltd., Suffolk; England, 193 p. Gutschick V P 1981 Evolved strategies of nitrogen aquisition by plants. Am. Natur. 118, 607-637. Hansen A P 1982 Nitrification potentials in softs from climax communities along a gradient from mesophytic forest to xerophytic steppe in eastern Washington. Thesis, Washington State University, Pullman. Heilman P E 1974 Effect of urea fertilization on nitrification in soils of the Pacific Northwest. Soil Sci. See. Am. Prec. 3 8 , 6 6 4 - 6 6 7 . Heilman P E and Ekuan G 1973 Response of Douglas-fir and western hemlock seedlings to lime. Forest Sci. 1 9 , 2 2 0 - 2 2 4 . Jordan C F and Herrera R 1981 Tropical rain forests: Are nutrients really critical. Am. Natur. 1 1 7 , 1 6 7 - 1 8 0 . Kirkby E A and Knight A H 1977 Influence of the level of nitrate nutrition on ion uptake and assimilation, organic acid accumulation, and cation-anion balance in whole tomato plants. Plant Physiol. 6 0 , 3 4 9 - 3 5 3 . Krajina V J, Madoc-Jones S and Mellor G 1973 Ammonium and nitrate in the nitrogen economy of some conifers growing in Douglas-fir communities of the Pacific northwest of America. Soil Biol. Biochem. 5 , 1 4 3 - 1 4 7 . Lodhi M A K 1977 The influence and comparison of individual forest ~ees on soil properties and possible inhibition of nitrification due to intact vegetation. Am. J. Bet. 64, 260-264. Lodhi M A K 1978 Comparative inhibition of nitrifiers and nitrification in a forest community as a result of the allelopathic nature of various tree species. Am. J. Bet. 65, 1 1 3 5 1147. Martin J S and Martin M M 1982 Tannin assays in ecological studies: lack of correlation between phenolics, proanthocyanidins and protein-precipitating constituents in mature foliage of six oak species. Oecologia 5 4 , 2 0 5 - 2 1 I. Menzies J D 1965 Fungi. In Methods of Soil Analysis. Part 2. Ed. C A Black. American Society of Agronomy, Madison, Wisconsin, 1572 p. Nadelhoffer K J, Aber J D and Mellilo J M 1984 Seasonal patterns in ammonium and nitrate uptake in nine temperate forest ecosystems. Plant and Soft 80, 321-335. Odum E P 1969 The strategy of ecosystem development. Science 1 6 4 , 2 6 2 - 2 7 0 . Ovington J D 1953 Studies in the development of woodland conditions under different trees. I. Soil pH J. Ecol. 41, 13-34. Pharis R P, Barnes R L and Naylor A W 1964 Effects of nitrogen level, calcium level and nitrogen source on growth and composition ofPinus taeda L. Physiol. Plant. 1 7 , 5 6 0 - 5 7 2 .
MINERALIZATION IN FOREST SOILS 37 38 39 40 41 42 43 44 45
46
47
48 49 50
51 52
267
Purchase B S 1974 Influence of phosphate deficiency on nitrification. Plant and Soil 41,541-547. Raven J A and Smith F A 1976 Nitrogen assimilation and transport in vascular land plants in relation to intracellular pH regulation. New Phytol. 76, 4 1 5 - 4 3 1 . Rice E L and Pancholy S K 1972 Inhibition of nitrification by climax ecosystems. Am. J. Bot. 59, 1033-1040. Robertson G P 1982 Factors regulating nitrification in primary and secondary succession. Ecology 63, 1561-1573. Robertson G P 1982 Nitrification in forested ecosystems. Phil. Trans. R. Soc. Lond. B 296,445-457. Robertson G P and Vitousek P M 1981 Nitrification potentials in primary and secondary succession. Ecology 6 2 , 3 7 6 - 3 8 6 . Rygiewicz P T, Bledsoe C S and Zasoski R J 1984 Effects of ectomycorrhizae and solution pH on [~SN] ammonium uptake by coniferous seedlings. Can. J. For. Res. 1 4 , 8 8 5 - 8 9 2 . Stevenson F J 1982 Humus chemistry. Wiley-International Science, New York, 443 p. Taylor R F 1935 Available nitrogen as a factor influencing the occurrence of Sitka spruce and western hemlock seedlings in the forests of southeastern Alaska. Ecology 1 6 , 5 8 0 602. Ulrich B 1980 Production and consumption of hydrogen ions in the ecosphere. In Effects of Acid Precipitation on Terrestrial Ecosystems. Eds. T C Hutchinson and M Havas. Plenum Press, New York, 654 p. Ulrich B 1983 A concept of forest ecosystem stability and of acid deposition as driving force for destabilization. In Effects of Accumulation of Air Pollutants in Forest Ecosystems. Eds. B Ulrich and J Pankrath. D Reidel Publishing Co., Boston, 389 p. U.S. Weather Bureau 1960 Climate of the states-Washington. Dept. of Commerce, Climatology of the United States. No. 6 0 - 4 5 . Washington DC. Van Breemen N, Mulder J and Driscoll C T 1983 Acidification and alkalinization of soils. Plant and Soil 7 5 , 2 8 3 - 3 0 8 . Vitousek P M, Gosz J R, Grief C C, Mellilo J M and Reiners W A 1982 A comparative analysis of potential nitrification and nitrate mobility in forest ecosystems. Ecology 52, 155-177. Wilson D S 1980 The natural selection of populations and communities. Benjamin/Cummings, Menlo Park, California, 186 p. Zinke P J 1962 The pattern of influence of individual forest trees on soil properties. Ecology 4 3 , 1 3 0 - 1 3 3 .
