Plant and Soil 160: 193-199, 1994. © 1994 Kluwer Academic Publishers. Printed in the Netherlands.

PLSO 3183

Nutrient uptake in eastern deciduous tree seedlings K. L A J T H A

Department of Biology, Boston University, Boston, MA 02215, USA Received 27 April 1993. Accepted in revised form 15 November 1993

Key words:

gaps, ion uptake, nitrogen, nutrient acquisition, phosphorus

Abstract

Tree seedlings that colonize large treefall gaps are generally shade-intolerant species with high potential relative growth rates. Nutrient availability may be significantly elevated in disturbance-induced gaps, however, little is known about the role of differences in nutrient uptake capacities of different species in structuring the community response to gap openings in eastern North American deciduous forests. Seven tree species were grown from seed under both a high and a low nutrient regime, and uptake kinetics of phosphate, ammonium, and nitrate were studied. Yellow birch, a species with intermediate shade tolerance and relative growth rate, had the highest maximum rates of uptake of all ions, while tulip tree, a gap-colonizing species with high relative growth rate, had the lowest rate of phosphate uptake and intermediate rates of ammonium and nitrate uptake. Beech and hickory, which have low relative growth rates and are not gap-colonizing species, had intermediate levels of nutrient uptake. There was no evidence that species with the highest maximum uptake rates measured at high supply concentrations had relatively low uptake at low nutrient supply concentrations. Although birch increased phosphate absorption capacity when grown under a low nutrient regime, this pattern did not hold for nitrate or ammonium uptake, and other species showed no change in nutrient uptake capacity according to nutrient growth regime. Clearly, factors other than nutrient absorption capacity, such as nutrient use efficiency or allocation to root vs. shoot biomass, underlie differences in species' capacities to colonize and maintain a high relative growth rate in canopy gaps.

Introduction

The size frequency distributions of canopy gaps in mesic forests have important consequences for forest community structure. Small, single tree gaps are often closed by branch and root extension of neighboring trees. As gap size increases, the frequency of establishment of new trees from seed increases, and the similarity between gap flora and that of neighboring undisturbed patches decreases. Tree seedlings that colonize larger, multiple treefall gaps in deciduous forests of eastern North America are generally fastgrowing, shade intolerent species such as pin cherry and tulip tree (Fowells, 1965; Runkle, 1985). These invading species may experience at

least temporary increases in nutrient availability, as increased decomposition and nitrogen mineralization in larger, disturbance-induced gaps and decreased competition from surrounding plants can lead to higher soil nutrient concentrations (Matson and Vitousek, 1981; Matson and Boone, 1984; Vitousek, 1985). Maximum photosynthetic rates per unit leaf area or weight, light compensation points, and light saturation intensities tend to be higher in species that colonize canopy openings and that have high relative growth rates ( R G R sensu Grime and Hunt, 1975: biomass increment per unit plant N per unit time; Bazzaz, 1979; Logan and Krotkov, 1968). Less is known about the role of nutrient uptake capacity of different

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species in structuring the community response to gap openings in deciduous forests, and experimental results have proven controversial. Several studies have suggested that species with low RGR are more tolerant of low nutrient supply than fast-growing species (Clarkson, 1967; Rorison, 1968; White, 1972) but are less responsive to increases in nutrient availability (Chapin et al., 1982; Nassery, 1970; Veerkamp and Kuiper, 1982). Tilman (1986) demonstrated that species that colonize low fertility grassland soils are able to grow more rapidly at low nitrogen levels and to acquire more nitrogen per plant than can species adapted to higher fertility sites; similarly, Chiba and Hirose (1993) demonstrated that the order of species' colonization of low-nutrient primary succession sites on Mt. Fuji was determined by the capacity to maintain high RGR under N-limited conditions. Other studies have suggested that inherently fast-growing species may maintain higher growth rates than slow-growing species even at low nutrient supply (Bradshaw et al., 1964; Hull and Mooney, 1990; Poorter et al., 1990; Van der Werf et al., 1993). However, plants adapted to highly fertile soils, or with a high genetic potential for rapid growth, usually have greater growth responses to added nutrients than closely related species adapted to low fertility soils (Elberse and Berendse, 1993; Koch et al., 1991; Lambers and Dijkstra, 1987; McGraw and Chapin, 1989; Van der Weft et al., 1993; Veerkamp and Kuiper, 1982). Results of root nutrient uptake studies are few, and have produced inconsistent results. Plants from nutrient-poor habitats have either lower capacities for phosphate absorption than plants from fertile habitats (Chapin, 1980; Chapin et al., 1982; Chapin, 1983; Chapin et al., 1986; Rorison, 1968) or similar capacities (Veerkamp and Kuiper, 1982), or else uptake capacities were greatest in populations with the highest genetic potentials for growth, and were not necessarily related to habitat fertility (Chapin and Oechel, 1983). Studies of uptake rates of ammonium and nitrate are more limited, and generally have not shown clearly defined differences among edaphically adapted species (Chapin et al., 1986; Koch et al., 1991), although Chiba and Hirose (1993) present evidence that primary succession colonizers with

high RGR under N-limited conditions have greater N uptake capacities at low N than late succession colonizers. Confounding most nutrient kinetic experiments is the fact that uptake rate can be an ecologically plastic character, dependent as much on plant nutrient status as on nutrient availabilty in the immediate growth environment (Atwell et al., 1980; Harrison and Helliwell, 1979). Roots increase their capacity to absorb limiting nutrients as reserves of that nutrient decline in the plant (Chapin et al., 1987). It is possible that there are ion specific relationships among these factors as well. Chapin et al. (1986) hypothesized that a high ion uptake capacity is an important component of root competition in infertile soils only in the case of mobile ions such as potassium and nitrate where diffusion in soil is relatively rapid, but not for immobile ions such as phosphate and ammonium for which diffusion would be the rate-limiting step. They suggested that there would be strong selection for high phosphate uptake rate in plants adapted to fertile soils, but not in plants adapted to infertile soils because diffusion limitation would override variation in uptake capacity. However, high uptake rates of mobile ions such as nitrate would be advantageous in all soils and should be greatest in species adapted to infertile soils. In this study I examined the root uptake kinetics of ammonium, nitrate, and phosphate in several forest tree species grown from seed under both high and low nutrient conditions, that varied greatly in both relative growth rate and canopy gap colonization ability. Initial hypotheses were that: 1. Shade tolerant, slowly-growing species would have higher rates of ion uptake at low nutrient availabilities than fast-growing, gap colonizing species, but this pattern would reverse at high rates of nutrient supply; 2. gap colonizing species with high RGR would have higher maximum rates of phosphate and ammonium uptake at the highest supply rates but lower maximum rates of nitrate absorption than slowly-growing species; 3. maximum nutrient uptake rates would be greater for seedlings grown under low nutrient conditions than under high nutrient

Nutrient uptake in eastern deciduous tree seedlings

195

transferred to individual 4-inch pots in the same soil:sand mixture, and randomly assigned to either the high or low nutrient treatment. All pots received 50 mL of the assigned nutrient treatment every 3 days, and were watered with DI as needed twice daily on the alternate days. Pots were maintained on greenhouse benches under ambient (25°C) temperature and light conditions and were randomly rotated to avoid location effects. The high and low nutrient treatments approximated 3/4 and 1/4 strength Hoagland for ammonium-N, nitrate-N, and phosphate concentrations, with other nutrients brought to approximately 3/4 strength Hoagland levels (Table 2). In order to reduce nitrate concentrations but keep calcium constant in the low nutrient treatment, calcium was added as CaSO 4 and thus sulfate differed between treatments as well. Seedlings were grown under these conditions for approximately 4 months prior to harvest. The "teabag" method of Epstein et al. (1963) was used to determine uptake kinetics of ammonium, nitrate, and phosphate over a range of concentrations for low to high (0.5-40/xM for 32po4, 50-4000/xM f o r 15NO3 and 15NH4). Upon harvest, roots were gently rinsed in 0.5 mM CaCI 2 to remove adhering soil particles. Approximately 5 - 7 g (wet weight) fine roots

conditions, and this rate increase (or ecological plasticity) would be greatest for species with the highest RGR.

Materials and methods

Seeds were bought from the Schumacher Seed Co., Sandwich, Ma. All seeds from each species were collected from one location but from several parent trees. Seven tree species of the hardwood deciduous forest ecosystem were used that vary in shade tolerance and growth rate (Table 1). Liriodendron tulipifera (tulip polar) is a very fast-growing species common to canopy gaps; Fraxinus americana (white ash), Prunus serotina (black cherry), Betual aUeghaniensis (yellow birch), and Quercus phellos (willow oak) are of intermediate shade tolerance and growth rate, while Carya ovata (shagbark hickory) and Fagus sylvatica (European beech) are more shade-tolerant and have slower growth rates (Canham and Marks, 1985; Dirr, 1983; Elias, 1980; Runkle, 1985). Birch seeds were stratified in sterilized, moist sand; all other seeds were stratified in sterilized, moist peat, and all seeds were kept in the dark at 4°C for 90 days or until some seeds began to break dormancy. Seeds were transferred to fiats containing a 60:40 sterile, fertilizer-free mineral soil:sand mixture, watered with a dilute (1/6) strength Hoagland solution, and grown in the Ohio State University greenhouse until a first set of leaves were developed and lateral roots were present. Seedlings from each species were selected if they fell within a relatively narrow and relatively uniform size distribution after 4 weeks,

Table 2. Final concentrations (mg L ~) of ammonium-N, nitrate-N, P and S in the high and low nutrient treatments

NO3-N NH4-N PO4-P SO4-S

High

Low

162.8 37.1 47.7 49.56

54.3 12.5 15.9 113.51

Table i. Species used for nutrient ion absorption kinetics studies Code

Species

Common name

Where collected

Rate of growth

HIC BEE BIR ASH

Carya ovata Fagus sylvatica Betula alleghaniensis Fraxinus americana

Shagbark hickory European beech Yellow birch White ash

NY England NY PA

OAK CHE TUL

Quercus phellos Prunus serotina Liriodendron tulipifera

Willow oak Black cherry Tulip tree

LA MA NC

Very slow Slow (+-1 ft/yr) Slow (-+1 ft/yr) Slow in sapling stage, then med.-fast (+-1-2 ft/yr first 10 yrs) Med. to fast (+-2 ft/yr first 10 yrs) Fast ( > 2 fl/yr) Very fast (2-3 ft/yr)

Notes on growth rates compiled from Dirr (1983) and Elias (1980).

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were carefully excised with scissors while in the CaCI 2 solution and enclosed in small (10cm × 10 cm, 2 mm mesh) acid-washed nylon bags without blotting or exposure to air. Roots were allowed to equilibrate in 0.5 mM CaCI 2 at 24°C for 30 minutes to exchange off any unlabeled nutrients in the root free space. All uptake solutions were 0.5 mM CaC12 at pH 6.0, 24°C. Five replicate teabags per species were used for each concentration. Because seedling mortality was greater than expected, roots from single plants were used to make teabags for more than one ion if enough fine root material was available, but roots from single plants were never used for more than one teabag for a given ion to avoid genetic correlation effects. All species were used for phosphate uptake experiments, whereas a subsample of species was used for nitrate and ammonium uptake experiments. Roots were exposed to the labeled solutions for 10 minutes and rinsed in a 4°C concentrated, unlabeled solution (0.5raM KH2PO 4 for 32p trials and 40 mM KCI for XSN trials) for 1 minute to exchange off adsorbed and root free-space label. Roots exposed to 32p were dried, weighed to determine total root dry weight per bag, and counted by liquid scintillation using Cerenkov radiation (Chapin and Holleman, 1974). Roots exposed to 15N were dried, ground, and analyzed for total N and N isotope ratio by Isotec Inc., Miamisburg, OH. All nutrient uptake rates were expressed on a root dry weight basis. Summary statistics and ANOVA's to differentiate among uptake rates of species at each ion supply concentration were performed using

0.800

O ASH • BEE

'O) I"1

SYSTAT software (Wilkinson 1990). When the ANOVA indicated statistical significance at p < 0.05, Tukey's multiple range test was used to separate differences among categories, Differences between uptake rates at high vs. low nutrient growth conditions were analyzed with T-tests in SYSTAT.

Results

Rates of phosphate absorption varied more than three-fold among the species studies at the highest P supply rates (Fig. 1). Birch had the highest maximum rates of phosphate uptake, and tulip tree had the lowest. Differences among other species were not significant. Birch grown under low nutrient conditions had higher rates of phosphate uptake than when grown under high rates of phosphate supply; uptake rates of low and high nutrient grown seedlings of other species did not significantly differ. Rates of ammonium and nitrate uptake did not vary significantly over the concentration ranges of supply solution in this experiment (Fig. 2, 3). There were no significant differences in uptake kinetics of ammonium or nitrate between high versus low nutrient grown plants, even though virtually all species grown under the lownutrient treatment showed visible signs of nutrient stress, such as pale green or yellowing leaves and reduced growth. Birch had the highest rates of nitrate uptake as well as ammonium uptake at the highest supply concentration.

B.Low

A. Htgh

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0.400

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z ~

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0.200 0.000 0

,

f

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10

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15

20

F

25

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30

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35

40

Uptake Solution ( pM PO4 - P )

450

T

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5

10

15

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20

,

25

,

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35

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40

45

Uptake Solution ( IJM P04 - P )

Fig. 1. Rate of phosphate uptake in relation to phosphate concentration by roots of tree seedlings grown in the greenhouse under (A) high and (B) low nutrient conditions. Values are means of 5 replicates (---SE).

Nutrient uptake in eastern deciduous tree seedlings

'r

A. High

'o) 48 Z -~ 36

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,

1000

20[]0

3000

,

4030

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Uptake Solution ( p M N O 3 - N )

Uptake Solution ( p M N O 3 - N )

Fig. 2. Rate of nitrate uptake in relation to nitrate concentration by roots of tree seedlings grown in the greenhouse under (A) high and (B) low nutrient conditions. Values are means of 5 replicates (-+SE).

6O ,_ -r"

A. High

"7

O) 48 Z

E -i

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36

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•

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24"

0 12" 0

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0 Uptake Solution ( pM NH 4 - N )

Uptake Solution ( pM NH4 - N )

Fig. 3. Rate of ammonium uptake in relation to ammonium concentration by roots of true seedlings grown in the greenhouse under (A) high and (B) low nutrient conditions. Values are means of 5 replicates (-+SE).

Beech had relatively high rates of ammonium acquisition at some test levels of ammonium supply, but results were not significantly different, on average, from other species due to large standard errors. When there were significant differences in nutrient uptake rate between species, these differences were evident at all uptake solution supply rates. For example, birch had the highest phosphate uptake rates at both the lowest (0.5 ~ M ) and the highest (40 ~ M ) phosphate supply rates, and tulip tree had the lowest uptake rates for both, although differences were significant only at maximum uptake rates. The same pattern generally held true for nitrate; there were no clear patterns for ammonium. Thus there was no evidence that species that could gain nutrients most rapidly at high nutrient concentrations could not effectively take up nutrients under low nutrient concentrations.

Discussion

Rates of phosphate absorption in these tree species were within the range, although near the low end, of rates observed for taiga trees by Chapin (1983) and Chapin et al. (1986). Rates of ammonium uptake were similar, although lower than rates observed by Chapin et al. (1986). In this study, uptakes rates of nitrate were similar to uptake rates of ammonium in all species, whereas Chapin et al. (1986) observed an order of magnitude lower uptake rates for nitrate than ammonium, perhaps reflecting species' adaptations to ammonium-dominated taiga soils in their study. Rates of ammonium and nitrate uptake did not vary significantly over the concentration ranges of supply in this experiment. The most likely explanation for this phenomenon is that maximum uptake capacities (Vmax) were reached

198

Lajtha

at even the lowest concentrations used in this experiment. Although the taiga species used by Chapin et al. (1986) did not show any indications of reaching Vmax over an identical range of concentrations, Koch et al. (1991) used a much lower range of nitrogen supply concentrations with two Alaskan sedges. These species showed signs of reaching Vmax at relatively low concentrations (100 ~M) of N, near the beginning of the range of N concentrations (50/~M) used in the present study. Maximum nitrate and ammonium uptake rates observed in their study were very similar to the rates observed in the current study, suggesting that uptake dynamics could be similar. Standard errors were much greater in the 15N experiments than in the 32p experiments, which also appeared to be true in the study of Chapin et al. (1986). Perhaps this inherent experimental variability also helped to obscure patterns across supply concentrations, but the similarity of uptake rates in this and in other studies suggest that rates observed here are real, and are not experimental artifacts of inactive uptake. The low uptake rates of phosphate by tulip tree at all supply concentrations, and the intermediate levels of nitrate and ammonium acquisition, ran counter to initial predictions, as this species can grow very rapidly in large, sunny gaps (Runkle, 1985). Similarly, the two slowgrowing, shade-tolerant species, beech and shagbark hickory, did not have high capacities for nutrient uptake at very low levels or low rates of nutrient acquisition at high nutrient concentrations as was initially predicted. Birch had the highest maximum uptake for all ions, and had equal or greater uptake rates than the other species at low nutrient supply concentrations. Thus there is no evidence, at least from nutrient uptake rates, that species with low RGR are poor competitors for high levels of available nutrients, just as there is no evidence that species that have high rates of uptake at the highest concentrations may be poor competitors at low nutrients concentrations. Nor were there large differences in uptake rates among ions with differences in soil mobility; rates of nitrate uptake were similar to those of ammonium uptake. Thus results of the current study cannot support the ion mobility hypothesis proposed by

Chapin et al. (1986), at least for the tree species that were examined here. Ecologists have long realized that photosynthetic rates cannot be used to predict wholeplant growth because total plant respiration in woody species can be quite high. However, photosynthesis is a major component of biomass accumulation, and there are strong ecological correlates to differences in rates of photosynthesis in different species. Similarly, maximum rates of nutrient uptake roots cannot be used to predict seedling growth rates; other ecological factors may decouple root uptake rates and whole-plant nutrient acquisition. Species that are adapted to low fertility soils may have a higher root:shoot allocation (Chapin, 1980; Tilman and Cowan, 1989; although see Elberse and Berendse, 1993; Chiba and Hirose, 1993), a greater root length:root weight ratio (Chiba and Hirose, 1993; Elberse and Berendse, 1993), lower specific leaf area (Elberse and Berendse, 1993; Poorter and Retakes, 1990), greater allocation to defensive compounds (Coley et al., 1985, although see Baldwin and Schultz, 1988), or a higher nutrient-use efficiency (defined as growth per unit plant N, Vitousek, 1982). Clearly, factors other than absolute rates of nutrient ion acquisition may underlie differences in species' capacities to colonize and maintain high RGR in canopy gaps.

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H Lumbers