Influence of nutrient availability and tree wildling density on nutrient uptake by Oxalis acetosella and Acer saccharum

Environmental and Experimental Botany 45 (2001) 11 – 20 www.elsevier.com/locate/envexpbot

Influence of nutrient availability and tree wildling density on nutrient uptake by Oxalis acetosella and Acer saccharum Jack T. Tessier a,*, Samuel J. McNaughton b, Dudley J. Raynal a a

State Uni6ersity of New York College of En6ironmental Science and Forestry, Syracuse, NY 13210, USA b Biological Research Labs, Syracuse Uni6ersity, Syracuse, NY 13244, USA Received 18 August 1999; received in revised form 16 August 2000; accepted 29 August 2000

Abstract Loss of nutrients following pulses of nutrient input in northern hardwood forests and the general effects of atmospheric deposition on forest communities are of concern. Uptake of nutrients by ground layer vegetation, including herbs and tree wildlings, may be important in both of these processes. We brought plants from the field (Catskill Mts, New York) and grew them under controlled environment conditions at two nutrient input levels to determine responses of Oxalis acetosella and Acer saccharum to increased nutrient input and tree wildling density. Oxalis nutrient concentration increased for many nutrients compared to field plants. Both species doubled their P concentration when P input doubled. Biomass of Oxalis was unaffected by both nutrient input level and Acer wildling density. Acer showed a similar response to increased nutrient input and its density did not affect the response of Oxalis to increased nutrient input. Results indicate that both species may be important to nutrient retention in northern hardwood forests. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Herb layer; Nitrogen; Nutrient input; Nutrient retention; Phosphorus; Plant competition

1. Introduction Increasing concentrations of nitrogen and phosphorus in soil solution and surface waters in forest ecosystems constitute a serious environmental problem (Vitousek et al., 1997; Carpenter et al., 1998). Understanding the mechanisms of mineral nutrient movement in forests is essential if drinking water quality and the health of aquatic and terrestrial biota are to be protected. Nutrient * Corresponding author. Tel.: +1-315-4706760. E-mail address: [email protected] (J.T. Tessier).

release from northern hardwood forest ecosystems is particularly high in the spring (Mitchell et al., 1992) and in association with runoff from agricultural fields (Carpenter et al., 1998). Muller (1978) proposed that spring ephemeral herbs act as a ‘vernal dam’, reducing nutrient loss that accompanies the spring flush of nutrients. Although they have received little attention, other herbs may be important for retention of nutrients provided in pulses to natural systems (Bilbrough and Caldwell, 1997; Mullen et al., 1998). Tree wildlings may serve as an additional sink for nutrients or interfere with the functioning of herbs.

S0098-8472/01/$ - see front matter © 2001 Elsevier Science B.V. All rights reserved. PII: S 0 0 9 8 - 8 4 7 2 ( 0 0 ) 0 0 0 7 5 - 7

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Investigation of nutrient uptake potential by nonephemeral herbs and the importance of interactions between these species and tree wildlings could yield new insights concerning nutrient retention in northern hardwood forests. Interactions between herbs and tree wildlings may affect nutrient capture by both groups of plants. Herbaceous cover can decrease tree wildling growth yet may also enhance wildling survival (Berkowitz et al., 1995). However, this competitive/ facilitative interaction is not straightforward. Davis et al. (1998) showed that competition intensity between tree wildlings and herbs is not necessarily related to biomass. They also demonstrated that competition for nutrients was greatest when resources were in short supply. Therefore, at times of high nutrient availability (spring or fertilization of adjacent agricultural fields), tree wildlings may not compete intensely with herbs for nutrients. Also, competition may be more related to interactions within the rooting zone and not simply to neighboring biomass. Acer saccharum Marshall (nomenclature follows Gleason and Cronquist, 1991) is one of the dominant tree species in northern hardwood forests. It is shade tolerant and maintains a temporally variable and transient seed bank (Houle, 1994). The seed bank and wildling distribution are spatially variable (Houle, 1994) and tend to be concentrated in areas of deciduous litter (Collins, 1990). Therefore, years of high seed production can result in large quantities of wildlings with an important temporal and spatial influence on structure and function of ground layer vegetation. Oxalis acetosella L. is an herbaceous plant common in the understory of northern hardwood forests. It produces seed earlier in its life span than many other herbaceous plants (Bierzychudek, 1982) and has both chasmogamous and cleistogamous flowers (Berg and Redbo-Torstensson, 1998). It is wintergreen, having leaves that survive the winter but which are replaced by new leaves in the spring (Kudish, 1992). The frequent co-occurrence of Acer and Oxalis make them appropriate for evaluating interactions between herbs and tree wildlings in response to increased levels of nutrient input.

Plants respond to additions of macronutrients by altering nutrient concentration (Ljungstro¨m and Nihlga˚rd, 1995; Quoreshi and Timmer, 1998) and allocation (Albaugh et al., 1998) as well as common growth responses (Albaugh et al., 1998). Plants in the field may respond similarly to natural episodes of enhanced nutrient availability, such as those associated with spring, as well as fertilizer application to adjacent agricultural fields (McMahon and Harned, 1998; Wear et al., 1998). Nitrogen and phosphorus are the two nutrients that most commonly limit plant growth in natural ecosystems (Marschner, 1995). Experimental additions of these nutrients have resulted in increases in plant growth (Witkowski, 1989), biomass (Albaugh et al., 1998; Huberty et al., 1998), and reproductive output (Griffith, 1998). However, responses may be species and individual specific (Stanturf et al., 1989; Milberg et al., 1998); for example, herbs tend to be more responsive to N enrichment than trees and shrubs (Witkowski, 1989; De Visser et al., 1994). We hypothesized that non-ephemeral herbs and tree wildlings are important in reducing nutrient loss from northern hardwood forests. We predicted that herbs and tree wildlings are capable of enhanced nutrient uptake when availability of N and P increases. Secondly, we predicted that tree wildlings compete with herbs for those nutrient resources. The objective of this study was to test the ability of Oxalis and Acer to respond to increased N and P input and to examine the influence of Acer wildling density on that uptake. The questions we addressed using a controlled environment experiment were (1) will Oxalis and Acer respond with increased biomass or nutrient concentration to increased nutrient availability? (2) Does Acer wildling density affect the growth and uptake of nutrients by Oxalis or Acer? and (3) Does nutrient availability affect the influence of Acer wildling density on Oxalis and Acer?

2. Materials and methods We collected plants in September 1998 from a second growth northern hardwood forest near Frost Valley in the Catskill Mountains, Ulster

J.T. Tessier et al. / En6ironmental and Experimental Botany 45 (2001) 11–20

County, New York. Thirty-five patches of Oxalis exhibiting maximal density over 100 cm2 were harvested and placed into a plastic bag for transport. Wildlings of Acer were located within the same stand and removed carefully to minimize damage to roots. The wildlings were roughly 10 cm tall and ranged in age from 3 to 7 years. We collected these wildlings in groups of five and ten and placed them in plastic bags for transport. In the laboratory, we removed soil from the Oxalis patches and rinsed the plants in distilled water and planted them in 30, 10 cm plastic pots (10 000 cm3 volume) containing PlayBall!, a calcined diatomaceous earth medium used commercially for water percolation and absorption (source: Northern Nurseries, Cicero, NY). We chose PlayBall! to serve as a mostly inert medium (89.0% SiO2, 4.8% Al2O3, 1.4% Fe2O3, 1.0% CaO, 0.3% MgO, and 1.6% Na2O). The nutrients applied during watering were the only nutrients that the plants received. We rinsed units of five Acer wildlings in distilled water and planted them in one-third of the pots. Units of ten Acer wildlings were also rinsed in distilled water and potted in another third of the pots. Thus, out of 30 pots, ten had only Oxalis, ten had Oxalis plus five maple wildlings and ten had Oxalis plus ten Acer wildlings. Plants were randomly chosen for assignment to treatments. We randomly selected five units each of Oxalis, five wildlings, and ten wildlings at the time of planting to serve as reference plants during analysis. These reference plants were dried at 65°C, ground in a Wiley Mill to pass through a 20-mesh screen, and stored until the end of the nutrient addition experiment. There were two nutrient addition treatments. We treated half of the described pots with a standard Hoagland’s growth solution (Jones, 1997), referred to in tables and figures as Hoagland’s Strength 1× (see Table 1 for contents). The other half was treated with a similar solution with twice the input of ammonium phosphate, referred to in tables and figures as Hoagland’s Strength 2× (see Table 1 for contents). Both Hoagland’s solutions were standardized to pH of 6 by adding necessary quantities of 1 M NaOH to eliminate effects of acidity. To summarize, there were six treatments with five

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replicates each. We designed the two levels of nutrient input to test the ability of Oxalis and Acer to respond to increased nutrient availability. Table 2 compares the experimental nutrient concentrations to actual field measurements. This experimental duration represents environmental pulses associated with snowmelt and fertilization of adjacent cropland. We included the two levels of Acer density to determine their influence on Oxalis and Acer growth and nutrient uptake. Pots were placed randomly in a growth chamber set at 23°C, 16-h days, and an average light intensity of 23.27 mmol m − 2 s − 1 (as measured using a Li-Cor LI-181 light meter). A warm temperature and long day were used to delay any oncoming senescence of the plants (McGraw et al., 1983; Rosenthal and Camm, 1996). The light intensity used was similar to those observed under intact forest canopies where these plant species naturally grow (Moore and Vankat, 1986; Brach et al., 1993). Two hundred milliliters of nutrient solution was added to each pot approximately every other day (enough to keep the medium moist) for 6 weeks. We re-randomized the placement of the pots within the growth chamber weekly to minimize the effects of spatial variation. Plants were harvested after 6 weeks. They were removed from the pots and all medium was cleaned from the roots. After drying the plants for 1 week at 65°C, we weighed and ground them in a Wiley Mill to pass through a 20-mesh screen. All plant tissues (including the reference plants) were analyzed for total N using a CE Instruments NC 2100 Soil Analyzer. All plant tissues were also analyzed for P using a Leeman Labs ICP. Table 1 Hoagland’s solutions compositions Amounts in 1 liter of solution Ingredient

1×Solution

2×Solution

1 M KNO3 1 M Ca(NO3)2 1 M NH4H2PO4 1 M MgSO4 micronutrient solution FeEDTA solution

6 4 2 1 1 1

6 4 4 1 1 1

ml ml ml ml ml ml

ml ml ml ml ml ml

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Table 2 Comparison of Hoagland’s solutions to field soil solution chemistries Study

Location

[N]

Present, 1×Hoagland’s Present, 2×Hoagland’s Mitchell et al. (1992) Shepard et al. (1990) Yanai (1991) Zhang and Mitchell (1995)

Laboratory Laboratory Adirondack Mts, New York Adirondack Mts, New York White Mts, New Hampshire Adirondack Mts, New York

16 18 40 10 – –

Statistical analyses were performed using SAS version 6.12 (SAS Institute, Inc., 1997). Biomass, nitrogen concentration, and phosphorus concentration of reference plants were compared to those of experimental plants using a t-test. A 2× 3 factorial (Hoagland’s concentration× wildling density) Analysis of Variance (ANOVA) was used to detect differences among experimental treatments for Oxalis biomass and concentrations of nitrogen and phosphorus. Differences among treatment effects for Acer biomass and concentrations of nitrogen and phosphorus were determined using a 2×2 factorial (Hoagland’s concentration×wildling density) ANOVA. Differences indicated by the ANOVAs were isolated using a Tukey’s HSD. All statistical tests were performed using h= 0.05.

3. Results Both Oxalis and Acer (Table 3) responded to experimental nutrient availability by increasing N and P concentrations. Neither species exhibited a significant change in biomass (Table 3) despite visible signs of root growth in all Oxalis plants and some Acer plants. Oxalis showed no signs of increased growth among the experimental treatments [Fig. 1(a)]. Likewise, N concentration of Oxalis tissue was not different among the treatments [Fig. 1(b)]. P concentration, on the other hand, doubled in response to increased P availability in the 2× solution [Fig. 2(c)] regardless of Acer density. As expected, Acer biomass was doubled in the ten wildling pots compared to the five wildling pots since twice as many wildlings were present,

[P] mol/l mol/l mmol/l mmol/l

2 mol/l 4 mol/l – – 1.9 mmol/l 0.5 mmol/l

but there was no indication of significant increased growth in response to experimental nutrient treatment [Fig. 2(a)]. Similar to Oxalis, Acer N concentration did not increase with increased N availability [Fig. 2(b)]. Acer P concentration did increase with increased P availability and this increase was not affected by Acer wildling density [Fig. 2(c)].

4. Discussion Changes in nutrient input and wildling density had no effect on biomass of Oxalis. Acer biomass was higher in the ten wildling pots than in the five wildling pots since there were twice as many wildlings present in the former by design. Nutrient input level, however, did not affect Acer biomass. This corroborates findings that light is a more influential resource than nutrients for the success of Acer (Horn, 1985; Sipe and Bazzaz, 1994, 1995) and Oxalis (Kuusipalo, 1987). It is Table 3 Comparison of reference and experimental plantsa,b.

Oxalis biomass (g) Oxalis% N Oxalis% P Acer biomass (g) Acer% N Acer% P a

Reference plants

Experimental plants

1.13 2.08 0.24 1.40 1.15 0.12

1.00 4.18 1.50 1.75 2.81 0.43

(0.12) (0.07) (0.01) (0.19) (0.11) (0.01)

a b b a b b

(0.05) (0.17) (0.10) (0.14) (0.23) (0.04)

a a a a a a

Numbers in parentheses represent one standard error. Means followed by letters are significantly different at = h0.05 b

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Although the 6 week duration of the experiment may have precluded a biomass response, both Oxalis and Acer increased in nutrient con-

Fig. 1. Response of Oxalis acetosella to experimental nutrient addition with Hoagland’s solution strengths 1 × and 2 × and Acer saccharum wildling densities of 0, 5, and 10 wildlings per pot. Means with different letters are significantly different at h= 0.05. (a) Biomass response. (b) Nitrogen concentration response. (c) Phosphorus concentration response.

also possible that the 6 week duration of this experiment limited any increase in biomass. Visible new roots in both species suggest that future growth enhancement would have been likely given sufficient time.

Fig. 2. Response of Acer saccharum to experimental nutrient addition with Hoagland’s solution strengths 1 × and 2 × and wildling densities of 5 and 10 per pot. Means with different letters are significantly different at h =0.05. (a) Biomass response. (b) Nitrogen concentration response. (c) Phosphorus concentration response.

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centration during this experiment. The similar responses of these two species suggest a mechanism for the lack of successional change seen by Huberty et al. (1998) given increased nutrient input. It is possible that some groups of species respond similarly to increases in the availability of nutrients and thus a community made up of like species would not show dramatic compositional change in response to increased nutrient availability. Alternatively, a diversity of functional types within a community may ultimately produce changes in timing and trajectory of succession given altered nutrient input (Tilman, 1993). The large increases in nitrogen and phosphorus concentration observed in the experimental plants suggest that they may a play a valuable role in nutrient retention in northern hardwood forests. This increase offers a mechanism for observed nitrogen retention within forests beyond that expected given current rates of atmospheric deposition. Stoddard (1994) points out that there are few examples of nitrogen saturation in the northeast United States. Aber et al. (1998) agree and suggest that there is an unknown sink for these high levels of atmospheric nitrogen deposition (Lovett, 1994). Nadelhoffer et al. (1999) suggested that this sink is more likely to be soils than trees, but did not evaluate ground layer vegetation in their study. The dramatic nutrient uptake observed in this study suggests that the ground layer may be an important component of the missing sink despite its low biomass compared to overstory vegetation. Increased phosphorus uptake at the high input level (and N compared to reference plants) suggests that these plants were not saturated even at input levels two and three orders of magnitude above those seen in the field (Shepard et al., 1990; Yanai, 1991; Mitchell et al., 1992; Zhang and Mitchell, 1995) and those associated with the regional atmospheric deposition of roughly 20 meq NO− 3 /l of precipitation in the region (National Atmospheric Deposition Program (NRSP-3)/National Trends Network, 1998). Continued nutrient uptake by the plants in this study highlights their substantial uptake capability. This study documents a potentially critical role for these species in nutrient capture and retention in a forest setting. Thus, management

efforts to preserve and facilitate growth of these species may be important to water quality and nutrient cycling and retention. Changes in pH may be more influential to plants than are changes in nutrient availability. While experimental acidification and liming have produced changes in Oxalis biomass (Brach and Raynal, 1992; Rodenkirchen, 1992; Okland, 1995), leaf area (Brach and Raynal, 1992), and foliar nutrient concentration (Brach and Raynal, 1992), nutrient addition in the current experiment resulted in changes only in nutrient concentration. A similar field response by ferns was found by Hurd et al. (1998). Since more responses occur due to changes in pH than to changes in nutrient input, the response of plants in the field to atmospheric deposition may be more related to acidification than to increased availability of nutrients per sae. The pH of Hoagland’s solutions used in this study was standardized to 6.0. This is well above the mean annual pH of 4.3 for precipitation (Driscoll, 1991) and steam water (Stoddard and Murdoch, 1991) in the Catskill Mts. The standardized pH of the solutions in this study may have precluded responses other than increased tissue nutrient concentrations. Responses to pH may be partly related to mycorrhizal associations since they increase nutrient uptake (Quoreshi and Timmer, 1998) and are negatively affected by acidification (De Visser et al., 1994). Therefore, analysis of damage from the onset of nitrogen saturation (Aber et al., 1989, 1998; Fenn et al., 1998) in an ecosystem may be best served by examining pH as a direct measure of susceptibility along with examining nitrogen dynamics and Ca:Al (Cronan and Grigal, 1995) as surrogate measures of ecosystem health. Future studies should factorially address the response of these species to pH and availability of nutrients in an experimental and field setting. Both Acer and Oxalis took up more phosphorus at the higher input level than at the lower input level, but no such difference was evident for nitrogen. Two factors may account for this response. First, doubling the ammonium phosphate in the higher input treatments only slightly increased the total input of nitrogen, since it was also available from calcium nitrate and potassium

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nitrate. This small increase in total nitrogen may not have been enough to result in an appreciable increase in uptake. Second, some plants prefer nitrogen as nitrate (Nadelhoffer et al., 1984; Falkengren-Grerup and Lakkenborg-Kristensen, 1994; Marschner, 1995) and these species may not be capable of responding to increased availability + of ammonium. The ratio of NO− 3 to NH4 (mg/g dry soil) at the field site in the spring of 1999 was 2.05 (standard error= 0.38, unpublished data). The plants from this site may be more responsive + to input of NO− 3 than to inputs of NH4 . Thus an important new research topic is to isolate the responsiveness of these species to forms of nitrogen availability. Doubling the ammonium phosphate input, on the other hand, did double the phosphorus input, since this was the only input form for phosphorus. Correspondingly, the increases in plant phosphorus concentrations were near doublings between the two input levels. Neither intraspecific nor interspecific competition affected nutrient uptake. Both densities of Acer responded by doubling or tripling nutrient concentration compared to reference plants. Therefore, even densities of wildlings well above those seen in the field do not inhibit nutrient uptake by Acer. Oxalis was able to assimilate nitrogen and phosphorus irrespective of the presence of Acer wildlings. This suggests a lack of competitive interaction among plants for nitrogen and phosphorus in this situation. Two explanations may account for this observation. First, spatial separation of the rooting systems of these two species in the pots may have precluded interspecific competitive interactions. We potted the plants at depths observed in the field during the initial harvest. Therefore, the Oxalis roots were above most of the root systems of the wildlings. This is contrary to the findings of Witkowski (1989) who found that response to nitrogen addition depended on rooting depth of different species. In this study, both species responded to nutrient addition despite dissimilarity in rooting depth. Also, during the first year of a wildling’s life its roots will be passing through the rooting zone of Oxalis and may indeed interact more strongly with Oxalis during that year. Therefore, a second and more likely explanation for the lack of

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an observable competitive interaction is that the concentration of nutrients provided during this experiment was sufficient to minimize competition. This corroborates the findings of Davis et al. (1998) who found that competition for nutrients was greatest at low availabilities. Thus, future experiments should address nutrient availabilities closer to field values and examine the critical first year of wildling development. Mycorrhizal connections among these plants and others in the field may be important for ecosystem level nutrient retention and exchange. Connections among ectomycorrhizal plants can conduct photosynthetic materials among plants (Read, 1997; Simard et al., 1997). Vessicular Arbuscular Mycorrhizae (VAM) may have the ability to perform similar transfers via their external hyphal fan (Harley and Harley, 1987). Both Acer (Cooke et al., 1992, 1993; Klironomos, 1995) and Oxalis (Harley and Harley, 1987) form VAM. Thus, nutrients absorbed by these species during pulses of nutrient availability may be transferred to other plants and species at later time periods. This suggests the possibility of community level resource capacitance (Bazzaz, 1996).

5. Conclusions Increased ammonium phosphate input resulted in higher phosphorus concentrations in Oxalis and Acer tissue. Biomass of the two species was not affected by nutrient availability. Density of Acer wildlings did not decrease the nutrient uptake. A lack of nutrient uptake suppression by the Acer wildlings occurred at all levels of nutrient input. Oxalis and Acer are capable of substantial nutrient uptake when provided with pulses of high nutrient availability. This uptake ability indicates a potential importance for these species in nutrient retention in northern hardwood forest settings. Competitive interactions were not evident at very high nutrient availabilities. Future studies should examine effects of lower nutrient concentrations, variations in nitrogen availability form, and interactions of pH and nutrient availability on herb layer plants and determine the interactions of first year wildlings with herbaceous plants.

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Acknowledgements The authors thank the following for their assistance with this project. The New York City Department of Environmental Protection provided partial funding for the project. The Frost Valley YMCA permitted the use of their land and plants. Lisa Tessier provided field assistance. Thomas Touchet assisted with potting the plants. Paul Manion and Bruce Race permitted the use of laboratory and growth facilities. Dale Tuttle at Northern Nurseries, Inc., Cicero, NY donated the PlayBall!. Margaret McNaughton and Bill Hamilton assisted with laboratory analyses. Doug Frank permitted the use of analytical equipment. The students of Bio 627 (Physiological Plant Ecology) and ESF’s Ecolunch provided intellectual input. Don Leopold and three anonymous reviewers made comments that significantly improved the manuscript.

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