Ecosystems (1998) 1: 401407

ECOSYSTEMS

1998 Springer-Verlag

Foliar and Litter Nutrients, Nutrient Resorption, and Decomposition in Hawaiian Metrosideros polymorpha
Peter M. Vitousek
Department of Biological Sciences, Stanford University, Stanford, California 94305, USA

ABSTRACT
The native tree Metrosideros polymorpha dominates Hawaiian forests across a very wide range of soil fertility, including both sites where forest production is limited by nitrogen (N) and others where it is limited by phosphorus (P). Five long-term fertilization experiments have further broadened the range of nutrient availabilities experienced by Metrosideros. Adding P to P-limited sites increased foliar P concentrations threefold and litter P concentrations up to 10-fold; lignin concentrations decreased, and the decomposability of leaf litter increased from 32% 35% to 36%46% mass loss in the first year. Adding N to N-limited sites increased leaf and litter N concentrations by only 15%20%, with little or no effect on the decomposability of tissue. Key words: nutrient cycling; nitrogen; phosphorus; decomposition; lignin; resorption; Hawaii; Metrosideros; fertilization.

INTRODUCTION
Numerous studies demonstrate that, within a species, plants growing in sites with low levels of available nutrients produce leaves with low nutrient concentrations; indeed, foliar analysis is widely used to diagnose nutrient deficiency so that it can be corrected by fertilization (van den Driessche 1974). How nutrient availability affects the resorption of nutrients from senescing leaves has been less certain, but recent reviews (Aerts 1996; Killingbeck 1996) make clear that any association between nutrient availability and the proportion of leaf nutrients resorbed is weak. Consequently, higher nutrient concentrations in leaves at sites with more available nutrients generally lead to higher nutrient concentrations in litter, a pattern that would be expected to make that litter more readily decomposable (Vitousek 1982; Hobbie 1992). Indeed, the leaf litter of species that occupy nutrient-rich sites tends to decompose more rapidly than that of those
Received 22 January 1998; accepted 4 May 1998. *Corresponding author; e-mail: vitousek@leland.stanford.edu

occupying nutrient-poor sites (van Vuuren and others 1993). However, relatively few studies have evaluated variation in decomposition within a species grown across a range of sites that differ in nutrient availability, and those studies have not yielded consistent results (Berg and Tamm 1991; Prescott and others 1993; OConnell 1994; Vitousek and others 1994; Crews and others 1995). In the Hawaiian Islands, the native tree Metrosideros polymorpha (Myrtaceae) dominates a very broad range of sites that differ widely in nutrient availability (Vitousek 1995). This variation is wide enough that the extreme sites almost certainly would support different species in a more diverse continental region. Moreover, the range of soil nutrient availability has been broadened still further by several long-term fertilization experiments in Metrosiderosdominated sites (Raich and others 1996; Vitousek and Farrington 1997). I made use of both natural and fertilizer-induced variation in nutrient availability to determine the effects of nutrient availability on leaf and litter chemistry, nutrient resorption, and the decomposability of leaf litter of M. polymorpha.

401

402

P. M. Vitousek

Table 1. Characteristics of the Sites in Which the Fertilizer Experiments Were Carried Out a
Site Characteristic Volcano Substrate age (years) Annual precipitation (mm) Date initiated b Limiting nutrients(s) c Reference Pahoehoe Mauna Loa 140 4400 1991 N, P Raich et al. 1996 Coarse Aa Mauna Loa 143 4400 1991 N, P Raich et al. 1996 Substrate texture Thurston Kilauea 300 2500 1985 N Vitousek et al. 1993 Fine Young Substrate age Old Laupahoehoe Mauna Kea 20,000 2500 1993 Vitousek and Farrington 1997 Kokee Kauai 4,100,000 2500 1991 P Herbert and Fownes 1995

Gradients

aAll

sites were at about 1200-m elevation, with mean annual temperature around 16C. All received additions of nitrogen, phosphorus, and a combined treatment containing nutrients other than nitrogen and phosphorus, alone and in all factorial combinations. bYear that the experiment was installed. cNutrients that increase rates of tree growth; significant main effects from analysis of variance.

STUDY SITES
As part of a study evaluating the nature and consequences of nutrient limitation to forest ecosystems, five factorial fertilization experiments were established along two environmental gradients (substrate age and parent material texture) in Hawaii. Each experiment included additions of nitrogen (N; 100 kg ha 1 year 1), phosphorus (P; 100 kg ha 1 year 1), and a combined treatment designated T that included all other plant nutrients [100 kg ha 1 year 1 of calcium and potassium, proportionately less of other nutrients as described by Vitousek and others (1993)], applied singly and in all factorial combinations to replicated plots. The ratio of N to P (N/P) applied (1:1) was made much narrower than the N/P ratio in plants (about 13:1) to compensate for P adsorption by these volcanic soils (Uehara and Gillman 1981). Nutrients were added twice each year through 1996 in all five sites. The forms of nutrients added and details of the experimental design in each site are summarized by Raich and others (1996) and Vitousek and Farrington (1997); major features of the sites and experiments are summarized in Table 1. One set of three experiments was arrayed on a gradient of substrate or parent material age across the Hawaiian Islands. The sites on this sequence are at the same elevation (1200 m) and have the same climate (16C mean annual temperature, about 2500 mm year 1 rainfall), parent material, topographic position, and dominant species, but they vary in substrate age from 300 years to 4.1 million years (Crews and others 1995; Vitousek and others

1997). One experiment was established on the Thurston site, the youngest (300 years) in this sequence; forest production there was limited by N (Vitousek and others 1993). The experiment on the oldest site (4.1 million years), at Kokee on the island of Kauai, found that P additions stimulated production (Herbert and Fownes 1995). Finally, an experiment on the intermediate-aged Laupahoehoe site (20,000 years), where soil nutrient availability was greater than in either of the extreme sites, yielded the result that neither N nor P additions (alone) stimulated tree growth, although in combination they did so (Vitousek and Farrington 1997). The combined treatment of nutrients other than N and P had no significant main or interactive effect on growth-related measurements in any of the experiments. The texture of the underlying parent material provided the basis for the second environmental gradient. Hawaiian volcanoes produce both finely divided tephra (volcanic ash and cinders) and lava flows; the flows can be subdivided further into aa (rough, rubbly clinkers, with surfaces consisting of unconsolidated rocks) and pahoehoe (relatively smooth-surfaced and massive flows). Although these three substrates differ substantially in texture (as a consequence of the temperature, flow rate, and extent of degassing of the lava), and hence in the surface area available for chemical weathering, they do not differ chemically (Wright and Helz 1987). The youngest site on the substrate age gradient also was used as the tephra (finest textured) site on the texture gradient. The other two experiments

Nutrient Availability and Decomposition were at the same elevation as the tephra site, but received more rainfall (about 4400 mm year 1). The aa experiment was established on an 1852 flow and the pahoehoe experiment on an 1855 flow. Tree growth in both sites was stimulated by both N and P additions, individually and (on pahoehoe) interactively (Raich and others 1996). Additions of N alone had a much greater effect than P on the aa site, but growth responses to N and P additions were more nearly equivalent (and their interaction stronger) on the coarsest-textured pahoehoe site. In addition to these experimental sites, I used the 2100-year-old Olaa site from the substrate age gradient (Crews and others 1995) as a wellprotected common site within which decomposition of litter from all the sites could be measured under comparable conditions.

403

Alpkem autoanalyzer (Alpkem, Wilsonville, OR, USA). Another subsample was dry ashed in a muffle furnace, and calcium, magnesium, and potassium were determined by using an atomic absorption spectrophotometer. Finally, the concentration of lignin in leaf litter was determined by using the acetylbromide procedure (Iiyama and Wallis 1990). All statistical analyses were carried out using SYSTAT (SYSTAT, Evanston, IL, USA); most involved complete factorial analysis of variance by site. Where necessary, data were log transformed prior to analysis.

RESULTS
Additions of nutrients other than N and P increased foliar concentrations of potassium significantly in every site and increased foliar magnesium significantly in some sites; they rarely and inconsistently affected LMA, N and P concentrations in leaves or litter, lignin concentrations, or decomposition, either alone or interactively with N and P; and they did not affect plant growth significantly in any of the sites. Accordingly, I combined the results of the T and T treatments, and report the effects of factorial fertilization experiments with N and P additions as the main factors.

METHODS
All of the experiments were sampled during July August 1995. Leaves were obtained from full-sun positions within each plot in each experiment. In the shorter-statured sites (the pahoehoe and aa experiments on the texture gradient), leaves were collected by hand; in taller vegetation, small canopy branches were collected by using a shotgun or slingshot. In all sites, I used leaves from the youngest fully expanded flush (behind a developing flush or a formed leaf bud). Leaf area was determined within 24 h using a Delta-T leaf-area meter; leaves were then dried at 70C and weighed to determine leaf mass per unit area (LMA). Senesced leaves also were collected by hand in the aa and pahoehoe experiments; I used litter traps (emptied every 24 weeks) to collect leaf litter in the taller forests. LMA of leaf litter was determined on a subsample of litter from each plot; these subsamples were then retained for chemical analyses. The remainder of the litter was composited by treatment within each experiment and air dried for several weeks. Subsamples were oven dried at 70C to calculate air/oven dry-weight ratios. About 2 g of each composite was placed into each of six litterbags (1-mm mesh), yielding 240 litterbags in all (5 experiments 8 treatments 6 replicates). Litterbags were all placed out onto the soil surface in the secure Olaa site in January 1996; they were collected in January 1997, oven dried at 70C, and weighed to determine mass loss. Leaf and leaf-litter samples from each treatment plot in each experiment were ground in a ball mill and subsampled; one subsample was digested using a persulfateperoxide procedure in a block digestor and analyzed colorimetrically for N and P with an

Leaves
Foliar N and P concentrations in unfertilized plots of the experiments differed among sites by a factor of 2, as reported previously (Vitousek and others 1995), reflecting differences between the sites in soil fertility (Table 2). Additions of N increased foliar N concentrations moderately (and significantly); additions of P increased foliar P very substantially. The latter effect was particularly striking in the three experimental sites in which P supply limited plant growth; there, foliar P concentrations increased threefold following fertilization with P. The increase in foliar P was smaller in sites where P additions did not stimulate plant production; no comparable difference in foliar N between N-limited and other sites was observed (Table 2). I found no consistent decrease of either N or P concentrations when the other element was added alone, regardless of which element limited plant growth in that site (Table 2). Adding N together with P decreased foliar P concentrations (relative to adding P alone), as would be expected if increased plant growth in the N P plots diluted P concentrations. However, foliar N concentrations often were higher in N P plots than in plots that received N alone. Overall, foliar N concentrations were regulated to a narrower range (within a site) than were P

404

Table 2. Characteristics of Metrosideros Leaves and Leaf Litter Collected in Fertilizer Experiments Carried Out in Five Sites Within the Hawaiian Islands a
Leaves LMA c (g/m2 ) N (%) 0.63 (0.01) 0.75 (0.01) 0.67 (0.01) 0.97 (0.03) N,*** P,*** NP*** 0.61 (0.01) 0.77 (0.02) 0.63 (0.02) 0.86 (0.03) N,*** P* 0.74 (0.04)* 0.84 (0.03) 0.67 (0.03) 0.82 (0.05) N** 1.17 (0.03) 1.30 (0.03) 1.26 (0.04) 1.32 (0.03) N** 0.94 (0.04) 1.04 (0.05) 0.88 (0.05) 1.16 (0.07) N** 0.061 (0.003) 0.067 (0.004) 0.212 (0.031) 0.148 (0.018) N, P,*** NP* 0.090 (0.003) 0.098 (0.005) 0.115 (0.006) 0.119 (0.008) P*** 128 (3) 129 (3) 125 (3) 127 (3) 161 (2) 165 (4) 156 (4) 155 (4) P* 0.062 (0.003) 0.055 (0.002) 0.111 (0.014) 0.081 (0.004) N,* P*** 203 (6) 194 (4) 211 (4) 191 (4) N** 0.36 (0.02) 0.36 (0.01) 0.32 (0.01) 0.38 (0.02) N,* NP* 0.73 (0.02) 0.81 (0.02) 0.82 (0.03) 0.85 (0.03) N,* P* 0.30 (0.01) 0.37 (0.01) 0.31 (0.02) 0.32 (0.01) N,** NP* 0.047 (0.002) 0.047 (0.002) 0.143 (0.010) 0.085 (0.005) N,*** P,*** NP*** 237 (6) 208 (6) 229 (7) 198 (9) N*** 0.29 (0.02) 0.36 (0.01) 0.29 (0.01) 0.39 (0.04) N** 0.030 (0.002) 0.025 (0.001) 0.220 (0.017) 0.072 (0.013) N,*** P,*** NP*** 0.024 (0.001) 0.021 (0.001) 0.042 (0.004) 0.030 (0.002) N,** P,*** NP 0.046 (0.002) 0.049 (0.002) 0.061 (0.005) 0.062 (0.003) P*** 0.020 (0.002) 0.018 (0.001) 0.144 (0.023) 0.070 (0.011) N,** P,*** NP** 0.047 (0.002) 0.046 (0.002) 0.145 (0.012) 0.095 (0.004) N,*** P,*** NP*** 239 (2) 227 (6) 222 (4) 211 (5) N,* P*** 0.28 (0.01) 0.35 (0.01) 0.32 (0.01) 0.36 (0.02) N,*** P* 0.022 (0.001) 0.020 (0.001) 0.256 (0.037) 0.083 (0.014) N,*** P,*** NP*** 18.9 (0.6) 21.4 (0.8) 18.2 (0.7) 19.0 (0.7) N,* P 17.8 (0.6) 20.3 (0.9) 17.5 (0.5) 17.5 (0.5) P 21.5 (0.8) 19.8 (0.5) 22.4 (1.0) 21.2 (0.8) N* 26.6 (1.7) 27.6 (1.0) 22.2 (1.6) 28.0 (1.1) N,** P* 19.4 (0.4) 18.9 (0.4) 17.4 (0.9) 16.9 (0.7) P** P (%) N (%) P (%) Lignin (%) 257 (5) 257 (6) 240 (5) 222 (2) N, P,*** NP 247 (4) 231 (3) 244 (7) 209 (9) N,*** P* 255 (9) 247 (8) 248 (11) 240 (6) 147 (3) 148 (3) 145 (4) 140 (3) 171 (2) 170 (7) 170 (5) 157 (6) LMA c (g/m2 ) Leaf Litter Decomposition (% mass loss) 35.2 (2.2) 37.3 (1.8) 42.8 (1.6) 44.4 (1.7) P*** 35.4 (2.1) 36.7 (1.3) 36.2 (1.6) 45.6 (1.4) N,** P,** NP** 37.6 (1.4) 32.8 (2.1) 34.5 (2.0) 36.5 (1.9) NP 40.0 (2.5) 40.0 (1.7) 41.6 (2.3) 40.9 (1.6) 31.8 (1.9) 30.6 (1.7) 36.7 (1.1) 42.1 (1.7) P,*** NP*

P. M. Vitousek

Experiment

Treatment b

Pahoehoe

Control N P N P Significance d

Aa

Control N P N P Significance

Tephra/Thurston (300 years)

Control N P N P Significance

Laupahoehoe (20,000 years)

Control N P N P Significance

Kokee (4.1 million years)

Control N P N P Significance

aAll LMA and chemical values are means of replicate plots (812) within treatments, with standard errors in parentheses; decomposition values are means ( SE) of mass loss after 1 year for 6 litterbags per treatment. Significances from analysis of variance: no asterisk 0.1, * 0.05, ** 0.01, *** 0.001. bN, nitrogen; P, phosphorus. cLeaf mass per area. dSignificance of main effect or interaction, from analysis of variance.

Nutrient Availability and Decomposition concentrationsand there is a suggestion that foliar N concentrations may be constrained in part by those of P, while P concentrations were not constrained by those of N. Finally, even where fertilization of the low-nutrient Thurston site with N and P had continued for more than 10 years, foliar N concentrations never approached those observed in unfertilized plots of the 20,000-year-old Laupahoehoe site, where natural soil fertility is relatively high (Table 2).

405

with the Laupahoehoe site particularly high; lignin also varied within some of the experiments as a consequence of fertilization. Additions of N affected lignin significantly in three sites, but inconsistently increasing lignin concentrations in the pahoehoe and 20,000-year Laupahoehoe site, and decreasing lignin in the 300-year Thurston site. The effects of P were more consistent: P additions significantly decreased lignin concentrations in two sites, and decreases on the borderline of significance (P 0.1) were observed in two more (Table 2).

Nutrient Resorption
The resorption of N and P from senescing leaves was calculated based on nutrient content per unit leaf area, to correct for the (observed) decrease in LMA during senescence. Metrosideros generally withdraws 40%70% of its foliar N and P prior to leaf abscission, consistent with woody plants elsewhere (Aerts 1996). Earlier studies on the substrate age gradient suggested that the proportion of N and P resorbed by Metrosideros varies inversely with nutrient availability, from about 40% in the relatively fertile intermediate-aged sites to nearly 70% in the low-nutrient youngest and oldest sites (Herbert 1995; Riley and Vitousek 1995). I observed the same pattern in these sitesbut I also found that the extremely nutrientlimited pahoehoe and aa sites have intermediate levels of nutrient resorption (about 50%) (calculated from Table 2). Additions of N had no consistent or significant effects on the resorption of foliar N; additions of P decreased P resorption substantially only in those P-limited sites where very high P concentrations accumulated following fertilization. Indeed, P concentrations in the pahoehoe and aa sites were higher in leaf litter than in live leaves, reflecting continued P accumulation through the life of the leaves. Overall, these results are consistent with Aerts (1996) conclusion that nutrient availability does not strongly affect nutrient resorptionexcept under extreme conditions, as occurred following P additions to P-limited sites.

Decomposition
Rates of decomposition in a common site provide a direct measure of the inherent decomposability of plant tissue; they can also be used to evaluate how changes in nutrient and lignin concentrations [which are widely used as predictors of decomposability see Melillo and others (1982)] affect rates of decomposition. Leaf litter from the relatively fertile 20,000year Laupahoehoe site decomposed more rapidly than that from other sites, as had been observed previously (Crews and others 1995). This relatively high decomposability of Laupahoehoe leaf litter presumably reflects its high nutrient content, despite its having the highest lignin concentrations among the five experimental sites. Fertilization with P increased the decomposability of plant tissue significantly in the three experimental sites in which P limited plant production prior to fertilization, and where P concentrations increased markedly following fertilization (Table 2). P additions decreased lignin concentrations in all three of these sites. No comparable effects of N on tissue decomposability were observed in N-limited sites, although additions of N with P further increased the decomposability of leaf litter in the aa and pahoehoe sites, where plant production was limited both by N and P. These effects of fertilization on decomposability are large relative to those observed in other studies (Berg and Tamm, 1991, Prescott and others, 1993), which were carried out in sites where N limited tree growth.

Litter Chemistry
Given the relatively small variation in nutrient resorption, patterns of N and P concentrations in litter reflected those in live leaves (Table 2). Nutrient concentrations were higher in fertilized and unfertilized plots of the 20,000-year-old Laupahoehoe site than elsewhere, and fertilization with N increased litter N concentrations moderately (and significantly), while P fertilization increased P concentrations very substantiallyup to 10-fold. Lignin concentrations in Metrosideros litter varied among sites,

DISCUSSION
The results of this study suggest that there could be a striking contrast between the consequences of N additions in N-limited ecosystems and those of P additions in P-limited systems. Fertilization of Plimited Hawaiian systems with P leads to very high foliar and litter P concentrations, much higher than those in sites that are not P limited (as might be expected if simple passive uptake were involved).

406

P. M. Vitousek cal comments on an earlier draft, and Lawrence Bond prepared the manuscript for publication.

This effect is much greater than that observed for N accumulation in N (or P)-limited Hawaiian ecosystems. Studies of young eucalyptus plantations in Australia also have reported a large increase in foliar P concentrations following P additions, and a lesser increase in foliar N following N addition (Bennett and others 1996; Judd and others 1996). For Eucalyptus globulus, the increase in both foliar N and P was enhanced when N and P were added together. The litter produced by P-fertilized trees in these P-limited Hawaiian sites is significantly more decomposable than is litter from unfertilized plots. I cannot determine whether the increased decomposability of litter produced in P-fertilized plots results from the increased concentrations of P itself (a direct nutrient limitation to decomposition), whether it reflects the decreased lignin concentrations in such litter (an indirect consequence of fertilization), or both. I suspect that the decrease in lignin at least makes a substantial contribution to this effect. Again, fertilization with N has no comparable direct or indirect effect on tissue decomposability, whether or not N is limiting forest growth. Overall, if the more rapid initial rates of decomposition that I observed in litter from fertilized plots continue, then these results suggest that, even within a species, P-limited sites could exhibit a positive feedback from enhanced P availability to more rapid decomposition/P mineralization to a further enhancement in P availability. Similar dynamics have been demonstrated for N, but the largest effects have occurred with species replacement from low-N to high-N sites (Wedin and Tilman 1990; Berendse 1993; Vinton and Burke 1995). Greater rates of decomposition of P-enriched litter also could lead to more rapid cycling of N and perhaps other nutrients, possibly preventing or delaying the onset of limitation by other nutrients following P fertilization. I evaluated just one species, albeit across a very wide range of nutrient availability, so the results of this study should not be generalized broadly. However, these processes and their implications would be worth pursuing in other regions where P limits forest production. ACKNOWLE D G M E N T S This research was supported by a USDA-NRI grant and by National Science Foundation grant DEB 9628803 to Stanford University. Douglas Turner carried out most of the chemical analyses, Sarah Hobbie assisted with field work and lignin analyses, Sarah Hobbie and Mary Ann Vinton provided criti-

REFERENCES
Aerts R. 1996. Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597608. Bennett LT, Weston CJ, Judd TS, Attiwill PM, Whiteman PH. 1996. The effects of fertilizers on early growth and foliar nutrient concentrations of three plantation eucalypts on high quality sites in Gippsland, southeastern Australia. For Ecol Manage 89:21326. Berendse F. 1993. Ecosystem stability, competition, and nutrient cycling. In: Schulze ED, Mooney HA, editors. Biodiversity and ecosystem function. Berlin: Springer-Verlag. p 40931. Berg B, Tamm CO. 1991. Decomposition and nutrient dynamics of litter in long-term optimum nutrition experiments. Scand J For Res 6:30521. Crews TE, Fownes JH, Herbert DA, Kitayama K, MuellerDombois D, Riley RH, Vitousek PM. 1995. Changes in soil phosphorus and ecosystem dynamics across a long soil chronosequence in Hawaii. Ecology 76:140724. Herbert DA. 1995. Primary productivity and resource use in Metrosideros polymorpha forests as influenced by nutrient availability and Hurricane Iniki [PhD Dissertation]. Honolulu: University of Hawaii at Manoa. Herbert DA, Fownes JH. 1995. Phosphorus limitation of forest leaf area and net primary productivity on a weathered tropical soil. Biogeochemistry 29:22335. Hobbie SE. 1992. Effects of plant species on nutrient cycling. Trends Ecol Evol 7:3369. Iiyama K, Wallis A. 1990. Determination of lignin in herbaceous plants by an improved acetyl bromide procedure. J Sci Food Agric 51:14561. Judd TS, Bennett LT, Weston CJ, Attiwill PM, Whiteman PH. 1996. The response of growth and foliar nutrients to fertilizers in young Eucalyptus globulus (Labill) plantations in Gippsland, southeastern Australia. For Ecol Manage 82:87101. Killingbeck KT. 1996. Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:171627. Melillo JM, Aber JD, Muratore JF. 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:6216. OConnell AM. 1994. Decomposition and nutrient content of litter in a fertilized eucalypt forest. Biol Fertil Soils 17:15966. Prescott CE, MacDonald MA, Gessel SP, Kimmins JP. 1993. Long-term effects of sewage sludge and inorganic fertilizers on nutrient turnover in litter in a coastal Douglas fir forest. For Ecol Manage 59:14964. Raich JW, Russell AE, Crews TE, Farrington H, Vitousek PM. 1996. Both nitrogen and phosphorus limit plant production on young Hawaiian lava flows. Biogeochemisty 32:114. Riley RH, Vitousek PM. 1995. Nutrient dynamics and trace gas flux during ecosystem development in Hawaiian montane rainforest. Ecology 76:292304. Uehara G, Gillman G. 1981. The minerology, chemistry, and physics of tropical soils with variable-charge clays. Boulder (CO): Westview. Van den Driessche R. 1974. Prediction of mineral nutrient status of trees by foliar analysis. Bot Rev 40:34794.

Nutrient Availability and Decomposition

Van Vuuren HMI, Berendse F, De Vinner W. 1993. Species and site differences in the decomposition of litter and roots from wet heathlands. Can J Bot 71:16773. Vinton MA, Burke IC. 1995. Interactions between individual plant species and soil nutrient status in shortgrass steppe. Ecology 76:111635. Vitousek PM. 1982. Nutrient cycling and nutrient use efficiency. Am Nat 119:55372. Vitousek PM. 1995. The Hawaiian Islands as a model system for ecosystem studies. Pac Sci 49:216. Vitousek PM, Chadwick OA, Crews TE, Fownes JH, Hendricks DM, Herbert DA. 1997. Soil and ecosystem development across the Hawaiian Islands. GSA Today 7(9):18. Vitousek PM, Farrington H. 1997. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:6375.

407

Vitousek PM, Turner DR, Kitayama K. 1995. Foliar nutrients during long-term soil development in Hawaiian montane rain forest. Ecology 76:71220. Vitousek PM, Turner DR, Parton WJ, Sanford RL. 1994. Litter decomposition on the Mauna Loa environmental matrix, Hawaii: patterns, mechanisms, and models. Ecology 75:418 29. Vitousek PM, Walker LR, Whiteaker LD, Matson PA. 1993. Nutrient limitation to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry 23:197 215. Wedin DA, Tilman D. 1990. Species effects on nitrogen cycling: a test with perennial grasses. Oecologia (Berl) 84:43341. Wright TC, Helz RT. 1987. Recent advances in Hawaiian petrology and geochemistry. In: Decker RW, Wright TL, Stauffer PM, editors. Volcanism in Hawaii. USGS Professional Paper 1350. Washington (DC): US Geological Survey. p 62540.