Photosynthesis, nitrogen-use efficiency, and water-use efficiency of ...

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2014

Photosynthesis, nitrogen-use efficiency, and water-use efficiency of jack pine seedlings in competition with four boreal forest plant species Darren E. Robinson, Robert G. Wagner, F. Wayne Bell, and Clarence J. Swanton

Abstract: The objective of this study was to understand the mechanism underlying nitrogen (N) and water competition between jack pine (Pinus banksiana Lamb.) and four boreal forest species. Large-leaved aster (Aster macrophyllus L.), Canada blue-joint grass (Calamagrostis canadensis (Michx.) Beauv.), trembling aspen (Populus tremuloides (Michx.), and red raspberry (Rubus idaeus L.) were planted at a range of densities (0–8 plants/m2) with jack pine seedlings. Net photosynthesis (Pn), nitrogen-use efficiency (NUE), water-use efficiency (WUE) of each species were monitored over three consecutive growing seasons. Changes in available soil N and water were also measured. Jack pine Pn, NUE, and WUE decreased as competitor density increased, but these effects varied among species (p < 0.001) and over time (p < 0.001). The influence of density on jack pine Pn decreased over time for aster and blue-joint grass and increased over time for aspen and raspberry (p < 0.001). At most sample times, jack pine Pn correlated with available soil N. In contrast, the correlation between jack pine Pn and soil water was rarely significant. Résumé : L’objectif de cette étude consistait à comprendre le mécanisme sous-jacent à la compétition pour l’azote (N) et l’eau entre le pin gris (Pinus banksiana Lamb.) et quatre espèces de la forêt boréale. L’aster à grandes feuilles (Aster macrophyllum L.), le calamagrostis du Canada (Calamagrostis canadensis (Michx.) Beauv.), le peuplier fauxtremble (Populus tremuloides Michx.) et le framboisier (Rubus idaeus L.) ont été plantés à des densités variant de 0 à 8 plants/m2 avec des semis de pin gris. La photosynthèse, l’efficacité d’utilisation de l’azote et l’efficacité d’utilisation de l’eau de chaque espèce ont été suivies pendant trois saisons de croissance consécutives. Les changements dans la disponibilité en azote et en eau du sol ont également été mesurés. Chez le pin gris, la photosynthèse ainsi que l’efficacité d’utilisation de l’azote et de l’eau diminuaient à mesure que la densité des espèces compétitrices augmentait; mais ces effets variaient en fonction de l’espèce (p < 0,001) et du temps (p < 0,001). L’effet de la densité sur le pin gris diminuait avec le temps dans le cas de l’aster et du calamagrostis et augmentait avec le temps dans le cas du peuplier et du framboisier (p < 0,001). Lors de la plupart des moments d’échantillonnage, la photosynthèse chez le pin gris était corrélée avec l’azote disponible dans le sol alors qu’elle l’était rarement avec l’eau du sol. [Traduit par la Rédaction]

Robinson et al.

2025

Introduction Herbaceous and woody plants comprising early successional forest vegetation reduced survival and growth of jack Received October 31, 2000. Accepted July 17, 2001. Published on the NRC Research Press Web site at http://cjfr.nrc.ca on October 31, 2001. D.E. Robinson.1,2 Crop and Plant Management, Plant Sciences Division, Alberta Research Council, P.O. Bag 4000, Vegreville, AB T9C 1T4, Canada. R.G. Wagner. Department of Forest Ecosystem Science and Cooperative Forestry Research Unit, University of Maine, Orono, ME 04469-5755, U.S.A. F.W. Bell. Ontario Forest Research Institute, 1235 Queen Street East, Sault Ste. Marie, ON P6A 2E5, Canada. C.J. Swanton. Plant Agriculture Department, University of Guelph, Guelph, ON N1G 2W1, Canada. 1 2

Corresponding author. Present address: Weed Management – Horticulture, Agronomy Building, Ridgetown College, P.O. Box 400, Main Street East, Ridgetown, ON N0P 2C0, Canada (e-mail: [email protected]).

Can. J. For. Res. 31: 2014–2025 (2001)

I:\cjfr\cjfr31\cjfr-11\X01-133.vp Friday, October 26, 2001 11:32:53 AM

pine (Pinus banksiana Lamb.) seedlings by 50–90%, as a result of interspecific competition (Chrosciewicz 1963; Farmer et al. 1988; Longpré et al. 1994; Wagner et al. 1996). Bell et al. (2000) presented a predictive means to objectively compare and contrast competitive effect of boreal forest plants on jack pine seedling growth. An assessment of the influence of competing species on nitrogen (N) and moisture availability, and the resulting influence on jack pine nitrogen- and water-use efficiency, will improve our understanding of the competitive mechanisms that underpin this model. Conifer growth response to neighboring forest plants is often influenced by the N or water competition (Morris et al. 1993; Nambiar and Sands 1993). A reduction in foliar N in conifer seedlings competing with grasses and herbaceous broadleaf plants (forbs) was observed (Elliott and White 1987). Reductions in soil moisture limited the growth of young conifers growing in association with neighboring plants (Larson and Schubert 1969). Competition for soil water increased plant water-saturation deficits and reduced needle water potential and stomatal conductance (Sands and Nambiar 1984). Nitrogen and (or) water uptake of pine has been correlated with growth when competing vegetation re-

DOI: 10.1139/cjfr-31-11-2014

© 2001 NRC Canada


Robinson et al.

2015 Table 1. Mean and standard deviations of pH; organic matter; cation exchange capacity (CEC); ratios of percent clay, silt, and sand; and net N mineralization rates for each soil type.

pH Organic matter (%) CEC (mequiv.·100 g soil–1) Clay, silt, sand (%) Net N mineralization (mg·kg soil–1·day–1)

Clay

Silt loam

Sand loam

5.7±0.4 1.8±0.2 21±5 45, 30, 25 0.12±0.08

5.1±0.7 1.6±0.3 13±6 10, 60, 30 0.07±0.05

4.9±0.5 1.0±0.1 5±2 5, 35, 60 0.05±0.03

Note: Data are based on three soil cores taken from each competitor treatment (0 plants/m2) at a depth of 45 cm once per growing season. Each set of three soil cores was bulked prior to analysis.

duced N and moisture availability (Larson and Schubert 1969; Sands and Nambiar 1984; Elliott and White 1987; Morris et al. 1993; Nambiar and Sands 1993). Mitchell et al. (1999) concluded that response of Pinus spp. to competition was associated with the physiological response of species to available light and water, as well as the ability to acquire resources. Nitrogen assimilation varies among species primarily as a result of differences in leaf longevity and N productivity or the amount of biomass produced per unit of N over the lifetime of a given tissue (Berendse and Aerts 1987). Chapin et al. (1987) considered photosynthetic nitrogen-use efficiency (NUE) to be a useful starting point for examining N assimilation. This provides an instantaneous measure of the N cost required to assimilate carbon dioxide (CO2) at the tissue level. Considered in conjunction with plant growth and net photosynthesis (Pn), NUE is a useful indicator of plant performance in relation to competition-mediated soil fertility (Chapin and Shaver 1989; Reich et al. 1991; Knops et al. 1997). Water-use efficiency (WUE), defined as the ratio of net CO2 uptake by photosynthesis to water transpired, underpins plant response to competition for water under moisturelimiting conditions (Sinclair et al. 1984). Sullivan et al. (1997) found that jack pine Pn was due primarily to stomatal limitations, where water limited growth. This study indicated that drought avoidance by stomatal closure was important for survival and growth, but they did not determine how competition influenced water availability or WUE. Since growth is strongly correlated with WUE under moisturelimiting conditions (Jones 1993), an evaluation of the influence of competing species on available moisture and WUE may provide a physiological explanation for growth response of jack pine to competition. Little is known of the influence of competition from neighbouring plants on NUE and WUE of pine seedlings, although they have both been shown to be important to conifer growth response to N and moisture limitations (Field et al. 1983). This study addresses the importance of Pn to N and water competition in the context of the interspecific competition model derived from growth response data by Bell et al. (2000), a justifiable approach given the strong correlation between Pn and growth of jack pine (Mohammed et al. 1998). Light attenuation was detailed in a related study (Shropshire 1999). This paper also discusses the influence of commonly associated herbaceous (large-leaved aster, Aster macrophyllus L. (ASTMA), and Canada blue-joint grass, Calamagrostis canadensis (Michx.) Beauv. (CALCA)) and

woody (trembling aspen, Populus tremuloides Michx. (POPTR), and red raspberry, Rubus idaeus L. (RUBID)) plant species at a range of densities on jack pine seedling Pn, NUE, and WUE. NUE and WUE of competing species are presented to compare their physiological response to competition with jack pine. We also assessed the relationship between jack pine photosynthetic response to changes in soil N and moisture availability caused by each competing species. It was hypothesized that jack pine Pn would decrease with increasing competitor density and with decreasing soil N and water. These reductions in jack pine Pn were hypothesized to be greater in the herbaceous competitor treatments because of their greater N and water demands (Arnup et al. 1995).

Materials and methods Site preparation and field layout The experiment was established at the Ontario Forest Research Institute Arboretum, located 3 km west of Sault Ste. Marie (46°33′N, 84°27′W) on Dystric Brunisols (pH 4.5–5.5, 1–1.5% organic matter). In September 1993, glyphosate (Roundup®) was broadcast over all study sites at 1.6 kg a.i.·ha–1 using a conventional agricultural boom sprayer, and the fields were plowed to control any existing weeds. An additional glyphosate application at the same rate as above was made the following spring, followed by disking. A randomized complete block split-plot design with three replications was blocked by soil texture (clay, silt loam, and sandy loam) to account for its influence on soil texture and chemistry (Table 1) and available N and water. The main plot factor was competing species: large-leaf aster, Canada blue-joint grass, trembling aspen, and red raspberry. The split-plot factor was planting density, which included two gradients based on densities commonly found in nature: 0, 0.5, 1, 2, 4, and 8 plants/m2 for ASTMA, CALCA, and RUBID and 0, 0.25, 0.5, 1, 2, and 4 plants/m2 for POPTR. These species were selected, because they often dominate early successional plant communities in the boreal forest, represent a wide array of growth forms (i.e., herb, grass, shrub, and tree), and exist in habitats of varying nutrient and moisture levels (OMNR 1997). In each replicate, a 7 m × 42 m main plot was designated for each of the plant species. The density treatments were assigned randomly to six 7 m × 7 m subplots. Forty-nine jack pine seedlings (1+0 container stock) were planted at a 1 m × 1 m spacing into each subplot. Each species of competing plant was planted from zero to eight positions (0, 45, 90, 135, 180, 225, 270, and 315° orientation) around each conifer seedling, depending on planting density. The eight planting positions were half the distance between the conifer stem and the 1-m2 border of the growing space allocated to each conifer. Competitor plants were planted at every sec© 2001 NRC Canada



2016 ond or fourth jack pine seedling to simulate densities of 0.25 and 0.5 plants/m2. Using this systematic planting scheme, the spatial arrangement of each competing species was held constant (see TerMikaelian et al. (1997) for diagram of design). The outer 1-m border of each 7 m × 7 m subplot was designated as a buffer zone. Measurements were made on the innermost 25 jack pine seedlings. Aspen were grown from seed for 2 months in Jiffy pots in greenhouses located at the Ontario Forest Research Institute. Vegetative propagules of aster, Canada blue-joint grass, and red raspberry were collected in the early spring of 1994 from naturally occurring populations, kept moist, and stored at –2 to 2°C in burlap bags or buckets covered with burlap until planting. Every effort was made to ensure that the starting biomass of jack pine seedlings and competing plants was similar, so no species had an early competitive advantage based on initial biomass. All species were hand planted from May to July 1994. Survival in midsummer 1994 ranged from 65 to 84% for jack pine and from 28 to 97% for the competing species. Dead jack pine and competitor plants were replaced to establish a complete design by May 1995. No fill planting occurred after that time. Invading weeds were controlled using both chemical (glyphosate (Vision®) or 2,4-dichlorophenoxyacetic acid (2,4D) + mecoprop + dicamba (Killex®)) and manual (hoeing and hand weeding) methods. In 1994 and 1995, competing species and conifers were covered with plastic bags or cups prior to herbicide application. In 1996 and 1997, glyphosate was applied prior to leaf flush to control invading grasses. Competitors were allowed to spread naturally both above- and below-ground within subplots, but the borders were rototilled regularly to prevent spread between adjacent subplots.

Physiological measurements

Net photosynthesis (µmol CO2·m leaf area–2·s–1), transpiration (E, mmol H2O·m leaf area–2·s–1), and nitrogen content (NC, g N·g dry matter–1) were measured from May to July in 1996, and from May to August in 1997 and 1998. Three jack pine seedlings in four density subplots (0, 0.5, 2, and 8 plants/m2 for ASTMA, CALCA, and RUBID; 0, 0.5, 2, and 4 plants/m2 for POPTR) were selected randomly for a total of 144 subsamples at each sampling date in 1996. The subsample size was increased to six seedlings per subplot (288 subsamples per sampling date) during 1997 and 1998. Pn and E were measured over a 4-day period, once per month, using a LI-COR 6200 portable photosynthesis meter (LI-COR Inc., Lincoln, Nebr.) in a 500-mL Plexiglas cuvette. Sun-exposed foliage from the apical 10 cm of new shoot growth was sealed in the cuvette for approximately 20 s. PPFD levels at the height of sampling ranged from 1400 to 2100 µmol·m–2·s–1, and temperatures within the chamber ranged from 19 to 34°C. Gas-exchange data from five jack pine seedlings in four of the 0 plants/m2 control treatments in all three blocks were analyzed to determine the influence of PPFD and temperature on Pn in the absence of competition (maximum photosynthesis, Pmax). PPFD levels between 1400 and 1750 µmol·m–2·s–1 and temperatures between 19 and 24°C influenced jack pine Pmax. Calibrations were applied to the measurements to avoid confounding the influence of competition with suboptimal PPFD and leaf temperature (Table 2). The CO2 levels in the cuvette were held within 20 ppm of the ambient concentration, which ranged from 340 to 360 ppm during the measurements. Humidity levels within the chamber were maintained within 1% of the ambient level by adjusting the flow of gas through the desiccant. Measurements were made on clear days between 10:00 and 14:00. The measured foliage was clipped, bagged, and stored at 2°C for 48 h. Projected leaf area was measured in the laboratory using a LI-COR 3100 leaf area meter. A regression function based on needle length, width, and thickness of 10 needles sampled from three trees in each subplot at each sample time was used to predict total leaf area from projected leaf area. The measured foliage then was dried at 60°C to a constant mass and analyzed for NC using a dry combustion N analyzer followed by N detection with

Can. J. For. Res. Vol. 31, 2001 Table 2. Regression models used to calibrate jack pine and competitor photosynthetic rates as a function of daily fluctuations in air temperature and photosynthetic photon flux density (PPFD). Plant species* Jack pine ASTMA CALCA POPTR RUBID

Calibration model† Air temperature Y Y Y Y Y

= = = = =

–15.56 + 1.83X – 0.04X –5.86 + 0.49X 3.64 + 0.51X 9.03 – 0.08X 9.68 – 0.03X

PPFD 2

Y Y Y Y Y

= = = = =

–7.59 + 0.02X –1.89 + 0.005X 2.95 + 0.004X 0.95 + 0.004X 7.71 + 0.008X

*ASTMA, large-leaved aster (A. macrophyllus); CALCA, Canada bluejoint grass (C. canadensis); POPTR, trembling aspen (P. tremuloides); RUBID, red raspberry (R. idaeus). † Y is photosynthetic rate (µmol CO2·m–2·s–1), and X is either air temperature (°C) or PPFD (µmol photons·m leaf area–2·s–1).

thermoconductivity. Foliar N analyses were conducted by the Analytical Services Laboratory in the Department of Land Resources at the University of Guelph, Guelph, Ont. Physiology of competing plants was assessed monthly from May to August of 1997 and 1998 using the same protocol as for the jack pine. Pn, E, and NC of the competitors were assessed from six randomly selected individuals in the same density treatments and during the same 4-day periods as the jack pine measurements were made. NUE (µmol CO2·s–1·g N–1) was calculated by expressing Pn on a dry-mass basis and dividing by foliar NC (Chapin et al. 1987). WUE (µmol CO2·mmol H2O–1) was calculated as the ratio of net carbon dioxide uptake to transpiration (Sinclair et al. 1984).

Soil measurements Three soil samples at depths of 15 and 45 cm each were collected randomly from each subplot in May and August of each year. The samples were bagged and stored at 2°C for 48 h. Plant available N (i.e., NH4+ and NO3–) was extracted from fresh, moist samples in 1 M KCl and determined colorimetrically. The soil N analyses were also conducted at the Analytical Services Laboratory at the University of Guelph. Soil moisture content at depths of 15 and 45 cm was measured monthly from May to August using a Sentry 200-AP dielectric moisture probe (Troxler Electronic Laboratories, Inc., Research Triangle Park, N.C.). An auger was used to drill three randomly placed 1.35 m deep holes of 5.97 cm diameter into each 7 m × 7 m subplot. A 1.5-m length of 2-in. (1 in. = 2.54 cm) schedule 40 PVC pipe was placed into each hole to facilitate the measurement of soil moisture. To calibrate the moisture probe, one soil core (at each depth) was removed at a distance of 0.75 m from each access tube once per year. This core was then bagged and stored at 2°C for 48 h, weighed, then dried for 72 h at 80°C, and weighed again to calculate volumetric soil moisture content. The moisture probe readings were calibrated with these volumetric moisture contents using nonlinear regression.

Statistical analysis All statistical analyses were conducted using the SAS version 6.03 statistical program (SAS Institute Inc. 1988). Analyses were conducted on means of the subsamples (144 subsamples in 1996 and 288 sampling units in 1997 and 1998), giving n = 48 experimental units per treatment. Homogeneity of variance and normality were confirmed by subjecting the residuals to analysis of variance and employing the Shapiro–Wilk statistic (Shapiro and Wilk 1965), respectively, so no correction of error terms was required. Repeat-measures factorial ANOVA (PROC GLM; SAS Institute Inc. 1988) was used to test for effects of sampling time, plant species, density, and all interactions on jack pine and competitor Pn, © 2001 NRC Canada



Robinson et al.

2017

Fig. 1. The influence of ASTMA, CALCA, POPTR, and RUBID density on jack pine net photosynthesis (Pn) in June 1996–1998. Species abbreviations are given in Table 2. Error bars are SDs.

Large-leaved aster

Canada blue-joint grass

9

Net Pn (µmol CO 2·m-2·s-1)

7

5

3 9

Trembling aspen

Red raspberry

7

5

3 0

0.5

2

4

8

0

0.5

2

4

8

Competitor density (plants/m2) 1996 foliar NC, NUE, WUE, and E. Time and competitor species were treated as fixed factors, and density, as a random factor. Full models including all treatments and possible interactions, including time interactions were evaluated. Fisher’s protected least squares difference (LSD; α = 0.05) were used to determine differences in each of the three dependent variables as a function of competitor species and density. Soil N and water availability were regressed against density of each competitor species in each study year (PROC REG, stepwise option; SAS Institute Inc. 1988). Lack-of-fit was assessed by ANOVA of the error terms. The best fit for available N included density alone, while soil texture and density provided the best model fit for the relation between competitor density and water availability. Density was treated as a random factor and soil texture as a fixed factor for these analyses. The slopes of the regression lines were contrasted using Fisher’s protected LSD (α = 0.05). Regression analysis was used to model Pn based on available N or moisture as a function of increasing competitor density (PROC NLIN; SAS Institute Inc. 1988). Analyses were pooled across all species at all sample times in each year of the study (α = 0.10). Density was treated as a random factor. Lack-of-fit was assessed by ANOVA of the error terms. The quadratic terms were included in the models, as the linear effects explained less than 10% of the residual error.

Results Jack pine photosynthesis Jack pine Pn decreased as competitor density increased (p < 0.001), and this decline increased over time as competition continued to develop (p < 0.001) (Fig. 1). Data shown are for the June sample period, at which point jack pine Pn

1997

1998

reached its seasonal maximum, and are similar to an earlier study conducted on jack pine seedlings in northern Ontario (Mohammed et al. 1998). In 1996, jack pine Pn decreased as density increased from 0 to 2 plants/m2 for all competitor species (p < 0.001). In 1997, however, the influence of density was less apparent, with differences occurring only between 0.5 and 2 plants/m2 (p < 0.001). These relationships were observed for all species in 1996 and 1997. In 1998, Pn decreased more with increasing density of the woody species than the herbaceous species (p < 0.001). The influence of species on jack pine Pn changed with year after establishment. In 1996, ASTMA and CANCA reduced jack pine Pn by 47 and 49%, respectively. POPTR and RUBID reduced Pn by only 27 and 30%, respectively. By 1998, the woody species had the greatest negative influence on jack pine Pn (p < 0.001), causing decreases of 52 and 42%, respectively. The Pn of jack pine competing with ASTMA and CANCA was reduced by 13 and 40%, respectively. Jack pine foliar NC Jack pine foliar NC decreased as competitor density increased from 0 to 8 plants/m2 in each year of the study (p < 0.001). Foliar NC was greatest in CALCA, intermediate in ASTMA, and lowest in RUBID and POPTR treatments (Fig. 2). In 1996, the influence of species was observed only in June and July as reflected in the significant time by species interaction (p = 0.032). A seasonal decline in foliar NC was observed in each year of the study (Fig. 2). This decline was independent of com© 2001 NRC Canada



2018

Can. J. For. Res. Vol. 31, 2001

Fig. 2. The influence of ASTMA, CALCA, POPTR, and RUBID density on monthly foliar nirogen concentration (NC) of jack pine from May to August 1996–1998. Species abbreviations are given in Table 2. Error bars are SDs.

ASMTA

CALCA

POPTR

RUBID

1996 4

4

4

4

3

3

3

3

2

2

2

2

1

1

1

1

0

0

Jack pine NC (%)

0.0 0.5 2.0 4.0 8.0

0 0.0 0.5 2.0 4.0 8.0

1997

0 0.0 0.5 2.0 4.0 8.0

0.0 0.5 2.0 4.0 8.0

4

4

4

4

3

3

3

3

2

2

2

2

1

1

1

1

0

0

0

0

0.0 0.5 2.0 4.0 8.0

0.0 0.5 2.0 4.0 8.0

1998

0.0 0.5 2.0 4.0 8.0

0.0 0.5 2.0 4.0 8.0

4

4

4

4

3

3

3

3

2

2

2

2

1

1

1

1

0

0 0

0.5

2

4

8

0 0

0.5

2

4

8

0 0

0.5

2

4

8

0

0.5

2

4

8

2

Competitor density (plants/m ) May

June

petition. In all plots, foliar NC decreased between May and June of 1996 (p < 0.001) and 1997 (p < 0.001) and between May and August of 1998 (p < 0.001). The seasonal decline in foliar NC was associated with increasing needle length. At the first sample time in May, needle growth was approximately 65% complete. By the final sample interval, needle elongation was complete or nearly complete. Jack pine NUE The effect of density on jack pine NUE decreased with time (1996, p = 0.003; 1997, p = 0.086; 1998, p = 0.003). In 1996, jack pine NUE decreased as density increased from 0 to 8 plants/m2 in all competitor treatments (p < 0.001) (Fig. 3). In 1997, however, this density effect on jack pine NUE was apparent only between 0 and 2 plants/m2 and during the months of June, July, and August for each species. In 1998, jack pine NUE decreased between densities of 0.5 and 2 plants/m2 for the herbaceous species at all sample times. There was an additional decrease in NUE above 2 plants/m2 for jack pine competing with the woody species in 1998 (p < 0.001). The influence of the herbaceous species on jack pine NUE was greater than that of the woody species in 1996 (p = 0.002) and decreased throughout the experiment. In 1996, jack pine NUE was reduced by 64 and 62% in ASTMA and CALCA treatments, respectively. The influence of ASTMA

July

August

and CALCA ranged between 36 and 42%, respectively, in 1998. The decline in jack pine NUE as a result of competition from POPTR increased from 50 to 54% between 1996 and 1998 (p < 0.001). From 1996 to 1998, NUE of jack pine was reduced by 57 and 48% in the RUBID treatments. Competitor NUE Patterns of NUE among the four species varied through the growing season (Fig. 4) and corresponded to phenological stages of development (p < 0.001). NUE of ASTMA increased as plants progressed from basal rosettes (May) to stem elongation (July) and then decreased with onset of flowering (August). NUE of CALCA decreased from the three- to five-leaf stage in mid-May of each year through to flowering (July) and subsequent seed production (August). A seasonal decline in NUE with leaf expansion of seedling POPTR was also apparent in both years of the study. These seedlings never entered reproductive development during the experiment. NUE of red raspberry declined from the time of early leaf expansion (May) through to flowering (July) and fruit production (August). Jack pine transpiration Jack pine E varied seasonally in the 3 years of the study (Fig. 5). Jack pine E was not influenced by sample date in 1996 (p = 0.986). In 1997, however, rates of transpiration in© 2001 NRC Canada



Robinson et al.

2019

Fig. 3. The influence of ASTMA, CALCA, POPTR, and RUBID density on monthly jack pine nitrogen-use efficiency (NUE) from May to August 1996–1998. Species abbreviations are given in Table 2. Error bars are SDs.

ASTMA

CALCA

0.3 1996

1997

1998

1996

1997

1998

-1 -1 Jack pine NUE (µmol CO2 · s · g N )

0.2

0.1

0.0

POPTR

RUBID

0.3 1996

1997

1998

1996

1997

1998

0.2

0.1

0.0 0

0.5 2

4

8

0

0.5 2

4

8

0

0.5 2

4

8

0

0.5 2

4

8

0

0.5 2

4

8

0

0.5 2

4

8

2


June

July

August

creased between July and August (p < 0.001) for all species and density treatments. In 1998, jack pine transpiration increased between June and July (p < 0.001) for all treatment combinations and then decreased between July and August (p < 0.001). The influence of competitor species on jack pine E varied among sample times and study years. Rates of jack pine transpiration did not differ among species treatments in the first year of the study (p = 0.962). In 1997, jack pine E was lowest when competing with RUBID during the months of May and June. During this time interval, E was greatest for ASTMA. In 1998, E was lower in the RUBID treatments than each of the other competing species (p < 0.001).

trast, the reduction in jack pine WUE increased with time in the CALCA and POPTR treatments. For example, the reduction caused by POPTR increased from 30 to 51% during the study. The influence of sample time on jack pine WUE varied with study year (p < 0.001). In 1996, jack pine WUE increased between May and July. In 1997, WUE decreased from May through to August (p < 0.001) for all species except CALCA. WUE of jack pine competing with CALCA increased from June to July at 0 and 0.5 plants/m2 (p = 0.008). In 1998, WUE declined between June and July but increased again in the month of August (p = 0.007) for all species and density combinations.

Jack pine WUE Jack pine WUE decreased as competitor density increased from 0 to 2 plants/m2 (Fig. 6). In 1996, WUE decreased from 23 to 32% across all species and sample times (p < 0.001). Similar reductions were observed in 1997 (p < 0.001) and 1998 (p < 0.001). The influence of species on jack pine WUE changed with year after establishment (p < 0.001). The reduction in WUE in ASTMA treatments decreased from 46% in 1996 to 21% in 1998. A similar trend was observed for RUBID. In con-

Competitor WUE WUE of ASTMA and CALCA decreased between June and July and between July and August, which corresponded to the phase from stem elongation to flowering and flowering to seed production, respectively (Fig. 7). Meanwhile, WUE of RUBID decreased between June and July, which corresponded to vegetative phase of growth for each species. WUE of POPTR also declined from June to July, although there is no evidence to support this decrease corresponded to a shift in reproductive status of the plant. © 2001 NRC Canada



2020


Fig. 4. The influence of plant density on monthly NUE of ASTMA, CALCA, POPTR, and RUBID from May to August in 1996 and 1997. Species abbreviations are given in Table 2. Error bars are SDs.

-1

Competitor NUE (µmol CO2 · s-1· g N )

ASTMA 1997

CALCA 1997

POPTR 1997

RUBID 1997

0.4

0.4

0.4

0.4

0.3

0.3

0.3

0.3

0.2

0.2

0.2

0.2

0.1

0.1

0.1

0.1

0.0

0.0

0.0

0.5

2

8

0.5

ASTMA 1998

2

0.0

8

0.5

CALCA 1998

2

4

0.5

POPTR 1998

0.4

0.4

0.4

0.3

0.3

0.3

0.3

0.2

0.2

0.2

0.2

0.1

0.1

0.1

0.1

0 0.5

2

0

8

0.5

2

8

RUBID 1998

0.4

0

2

0

8

0.5

2

4

0.5

2

8

Competitor density (plants/m2) May

June

July

August

Fig. 5. The influence of ASTMA, CALCA, POPTR, and RUBID density on monthly jack pine transpiration rates from May to August 1996–1998. Species abbreviations are given in Table 2. Error bars are SDs. ASTMA

CALCA

POPTR

RUBID

Transpiration (mmol H 2O · m-2 · s-1)

1996 10 8 6 4 2 0

10 8 6 4 2 0 0

0.5

2

4

8

10 8 6 4 2 0 0

0.5

2

4

8

1997

10 8 6 4 2 0 0

0.5

2

4

8

20

20

20

20

15

15

15

15

10

10

10

10

5

5

5

5

0

0

0

0.5

2

4

8

0 0

0.5

2

4

8

10 8 6 4 2 0

10 8 6 4 2 0 0 0.5 2

4

8

1998

0.5

2

4

8

0.5

2

4

8

0

0.5

2

4

8

0

0.5

2

4

8

0 0

0.5

2

4

8

10 8 6 4 2 0 0

0

10 8 6 4 2 0 0

0.5

2

4

8

2


June

July

August

© 2001 NRC Canada



Robinson et al.

2021

Fig. 6. The influence of ASTMA, CALCA, POPTR, and RUBID density on monthly jack pine water-use efficiency (WUE) from May to August in 1996, 1997, and 1998. Species abbreviations are given in Table 2. Error bars are SDs.

CALCA

ASTMA

6 1996

1997

1998

1996

5

1997

1998

4

Jack pine WUE (µmol CO2 · mmol H2O-1)

3 2 1 0

POPTR

RUBID

6 1996

1997

1998

1996

1997

1998

5 4 3 2 1 0 0

0.5 2

4

8

0

0.5 2

4

8

0

0.5 2

4

8

0

0.5 2

4

8

0

0.5 2

4

8

0

0.5 2

4

8

2


The influence of competing species on available soil N The influence of competing species on available soil NH4+ (p < 0.001) varied among the 3 years of the study (Table 3). The rate of decrease in soil NH4+ was greater in the ASTMA and CALCA plots than in the POPTR and RUBID plots in 1996 and 1997. In 1998, the decrease in soil NH4+ was greatest in the POPTR and RUBID treatments. The rate of decrease in soil NO3– differed among the four species studied (p = 0.032), but this effect was variable over time (Table 3). A decrease in soil NO3– with increasing competitor density was only measurable in RUBID (p = 0.03) treatment in 1996, and the POPTR (p = 0.054) and RUBID (p = 0.003) treatments in 1998. The influence of soil texture and competitor species on soil water availability The relation between soil water and competitor density varied among soil textures (p < 0.001). In the ASTMA treatments, available water decreased only on the silt loam soil. On clay and silt loam soils, soil water decreased in the CALCA and POPTR treatments (Table 4). Available water decreased with increasing RUBID density on the clay soil but not on the silt loam or sandy loam soils. The relation between increasing competitor density and available water at 45 cm depth varied among species in 1996

June

July

August

(p = 0.008), 1997 (p = 0.014), and 1998 (p < 0.001). CALCA and POPTR had a greater negative influence on available water than ASTMA and RUBID in all years of the study. The decrease in negative slope values from 1996 through to 1998 (p < 0.001) indicated that the negative influence of all species on available water decreased with time. There was not a consistent relationship between competitor density and soil water availability for ASTMA, POPTR, or RUBID. Available soil water decreased as the density of CALCA increased for all soil types in each year of the study (p < 0.001). The relation between jack pine Pn, and N and water availability Jack pine Pn was influenced by total available N (NH4+ + NO3–), but this relationship varied among sample dates and years (Table 5). In 1996, jack pine Pn was correlated with total soil N in May and June. In 1997, the correlation between Pn and available N was significant in May and July. Jack pine Pn and total available N were correlated in May and June of 1998. Jack pine Pn was positively correlated with available moisture at 45 cm depth during only a few sample dates (Table 5). The correlation between jack pine Pn and available water occurred during July 1996, June 1997, and July 1998. © 2001 NRC Canada



2022


Fig. 7. The influence of plant density on monthly WUE of ASTMA, CALCA, POPTR, and RUBID from May to August in 1997 and 1998. Species abbreviations are given in Table 2. Error bars are SDs.

-1

Competitor WUE (µmol CO2 · mmol H2O )

ASTMA 1997

CALCA 1997

10.0 8.0 6.0 4.0 2.0 0.0

10.0 8.0 6.0 4.0 2.0 0.0 0.5

2

8

10.0 8.0 6.0 4.0 2.0 0.0 0.5

ASTMA 1998

2

8

2

8

2

4

0.5

POPTR 1998

0.5

2

8

10.0 8.0 6.0 4.0 2.0 0.0 0.5

8

2

RUBID 1998

10.0 8.0 6.0 4.0 2.0 0.0

10.0 8.0 6.0 4.0 2.0 0.0 0.5

10.0 8.0 6.0 4.0 2.0 0.0 0.5

CALCA 1998

10.0 8.0 6.0 4.0 2.0 0.0

RUBID 1997

POPTR 1997

2

4

0.5

2

8

2 Competitor density (plants/m )

May

June

July

August

We did not observe a correlation between jack pine Pn and available N or water in August of any study year.

Table 3. Change in available soil ammonium (NH4+) and nitrate (NO3–) availability (b0) as a function of increasing density of each competing species in 1996–1998.

Discussion

Competitor species

The greatest decreases in jack pine Pn occurred between control plots and the lowest density treatments. These decreases in Pn follow diameter growth – density and yield– density relationships described in other studies (Shainsky and Radosevich 1991; Perry et al. 1993; Bell et al. 2000). The herbaceous species were most competitive early in the experiment. With time, however, the woody species had a greater influence on jack pine Pn than the herbaceous species. This agrees with Bell et al. (2000), who found that ASTMA and CALCA had a greater negative influence on jack pine diameter early in their study, which reflects the correlation between Pn and jack pine seedling growth (Mohammed et al. 1998). The increase in competitiveness of POPTR and RUBID may be attributed to the greater increase in percent cover in later study years (Bell et al. 2000), which was accompanied by an increase in light attenuation (Shropshire 1999) and less available N in the woody species treatments. Morris et al. (1993) also found that herbaceous plants reduced loblolly pine (Pinus taeda L.) stem diameter, water use, and nutrition more than woody plants in the first 2 years after establishment. The effect of competition on jack pine NC was less pronounced than for Pn, although our data showed foliar N decreased with increasing competitor density. As a result, jack pine NUE decreased as competitive stress increased. These

1996 ASTMA CALCA POPTR RUBID 1997 ASTMA CALCA POPTR RUBID 1998 ASTMA CALCA POPTR RUBID

NH4+

NO3– p

b0

r2

p

0.48 0.32 0.75 0.66

0.026 0.028 0.013 0.017

–0.04 –0.04 –0.01 –0.31

0.05 0.10 0.03 0.43

0.234 0.277 0.669 0.030

–0.17ab –0.18ab –0.13c –0.15bc

0.59 0.64 0.44 0.55

0.022 0.002 0.019 0.006

–0.02 –0.03 –0.02 –0.01

0.04 0.01 0.01 0.01

0.594 0.726 0.847 0.934

–0.14c –0.15c –0.37a –0.18bc

0.62 0.56 0.75 0.63

0.004 0.004 0.016 0.002

–0.07 –0.08 –0.15 –0.20

0.03 0.01 0.11 0.23

0.652 0.627 0.054 0.003

b0

r

–0.53a –0.40b –0.39b –0.22c

2

Note: Slopes for NH4+ followed by different letters within a given year are significantly different (Fisher’s Protected LSD α = 0.05); NO3– values were not significantly different. The slope values refer to the decrease in available soil N per unit increase in initial planting density (mg N·kg soil–1·plant–1·m–2). Species abbreviations are given in Table 2.

reductions in NUE when considered with mean residence time of foliar N may result in lower net biomass returns of jack pine in the presence of competition (Aerts 1995). These © 2001 NRC Canada



Robinson et al.

2023

Table 4. Change in soil moisture availability at depth of 45 cm (b0) with increasing competitor density (% moisture by volume per plant) pooled across the three soil types for each species. Competitor species ASTMA

CALCA

POPTR

RUBID

1996

1997

1998

Soil texture

r2

b0

p

r2

b0

p

r2

b0

p

Clay Silt loam Sandy loam Clay Silt loam Sandy loam Clay Silt loam Sandy loam Clay Silt loam Sandy loam

0.09 0.22 0.99 0.75 0.86 0.95 0.97 0.78 0.3 0.87 0.92 0.15

–0.5 –3.5 8.5 –10.0 –4.0 –3.4 –8.0 –9.3 –1.2 –5.8 12.6 1.1

0.605 0.01