Open Journal of Forestry
2012. Vol.2, No.4, 187-199
Published Online October 2012 in SciRes (http://www.SciRP.org/journal/ojf) http://dx.doi.org/10.4236/ojf.2012.24023
Nutrient Use Efficiency of Three Fast Growing Hardwood Species
across a Resource Gradient
Dawn E. Henderson1, Shibu Jose2
1Open Rivers and Wetlands Field Station, Missouri Department of Conservation, Jackson, USA
2Department of Forestry, University of Missouri, Columbia, USA
Received August 18th, 2012; revised September 23rd, 2012; accepted October 10th, 2012
Attitudes regarding traditional energy sources have shifted toward renewable resources. Specifically,
short-rotation woody crop supply systems have become more prevalent for biomass and biofuel produc-
tion. However, a number of factors such as environmental and inherent resource availability can limit tree
production. Given the intensified demand for wood biomass production, forest and plantation manage-
ment practices are focusing on increasing productivity. Fertilizer application, while generally one of the
least expensive silvicultural tools, can become costly if application rates exceed nutrient uptake or de-
mand of the trees especially if it does not result in additional biomass production. We investigated the ef-
fect of water and varying levels of nitrogen application (56, 112, and 224 kg·N·ha–1·yr–1) on nutrient con-
tent, resorption efficiency and proficiency, N:P and the relationship with ANPP, as well as leaf- and can-
opy-level nutrient use efficiency of nitrogen, phosphorus, and potassium for Populus deltoides, Quercus
pagoda, and Platanus occidentalis. P. deltoides and P. occidentalis reached their maximum nitrogen
budget with the application of water suggesting old agricultural fields may have sufficient nutrient levels
to sustain short-rotation woody crops negating the application of additional nitrogen for these two species.
Additionally, for P. deltoides and Q. pagoda application of nitrogen appeared to increase the uptake of
phosphorus however, resorption efficiency for these two species were more similar to studies conducted
on nutrient poor sites. Nutrient resorption proficiency for all three nutrients and all three species were at
levels below the highest rates of nitrogen application. These findings suggest maximum biomass produc-
tion may not necessarily be tied to maximum nutrient application.
Keywords: Nutrient Use Efficiency; Resorption; N:P; Biomass Production
Introduction
Changes in attitudes about energy production have shifted
interest from traditional energy sources and techniques toward
renewable resources in recent years (Dickmann, 2006). One
target of the focus on renewable energy is fast growing hard-
wood species with the concentration placed on species that
could be harvested on rotations ranging from as little as six
(Tuskan, 1998) or up to 15 years (Dickmann, 2006). The con-
cept of short-rotation woody crop (SRWC) supply systems
were first formalized nearly 50 years ago (Tuskan, 1998). In
some areas of the United States, forest management practices
that had previously focused on extensive management for fiber
production have shifted to intensive management for biomass
and biofuel production using SRWC systems (Geyer &
Melichar, 1986; Coyle & Coleman, 2005; Augusto et al., 2009).
Techniques for increasing production potential of SRWC
suchas high stocking rates, hybrid selection/development, and
intensive stand management have become industry standards
(Dickmann, 2006). However, our knowledge about fertilizer
uptake patterns and use by these fast growing species for pro-
duction purposes is limited at best.
Tree production can be limited by a number of factors such
as light (Wang et al., 1991; Ellsworth & Reich, 1992; Jose &
Gillespie, 1997; Jokela & Martin, 2000; Henderson & Jose,
2005), water (Lockaby et al., 1997; Albaugh et al., 1998; King
et al., 1999; Allen et al., 2002; Albaugh et al., 2004), and
growing space (Cochran et al., 1991; Schubert et al., 2004;
Lockhart et al., 2006; Clark et al., 2008; Curtis, 2008) or en-
hanced by practices such as fertilization (Singh, 1998; Will et
al., 2002; Bekele et al., 2003; Allen et al., 2004; Samuelson et
al., 2004a), or irrigation (Allen et al., 2005; Stape et al., 2008;
Zalesny et al., 2007; Zalesny et al., 2008). Most frequently,
biomass accumulation and stand development are restricted to
inherent resource availability within a site or by community
composition (Wang et al., 1995; Wang et al., 1996; Smith et al.,
1998; Vogel & Gower, 1998; Blanco et al., 2006; Schilling &
Lockaby, 2006; Yan et al., 2006).
As a counter to nutrient losses, plants have mechanisms to
minimize nutrient losses such as nutrient resorption or retrans-
location (Vitousek, 1982; Berendse & Aerts, 1987; Aerts & Be-
rendse, 1988; Aerts, 1996; Aerts, 1997; Wright & Westoby,
2001). Although it would seem somewhat intuitive, the nature
of, and driving force behind, nutrient availability, uptake, and
resorption are not well understood as is indicated by inconsis-
tent findings between studies. Some studies indicate nutrient
limitation should lead to higher rates of resorption efficiency
and proficiency (actual nutrient level within leaf litter; a reflec-
tion of soil resource) and that low rates of resorption could
contribute to nutrient limitations, reduced biomass production,
and survival (Boerner, 1984; Killingbeck, 1984; Killingbeck,
1986; Killingbeck, 1993; Killingbeck, 1996). Other studies
suggest higher leaf level nutrient status (Lathja, 1987) or re-

D. E. HENDERSON, S. JOSE
source availability (Xu & Timmer, 1999) is linked to higher or
lower (Aerts & de Caluwe, 1994; Vitousek, 1998) resorption
ratios or may have no effect on the ratios (Chapin & Kedrowski,
1983; Birk & Vitousek, 1986; Aerts, 1996; Wright & Westoby,
2003; Yuan & Chen, 2010). However, it appears that reaction
to and indications of nutrient use can vary in response to site
fertility (Bloom et al., 1985; Wright & Westoby, 2003), water
availability (Boerner, 1985; del Arco et al., 1991; Escudero et
al., 1992, Wright & Westoby, 2003), soil chemistry (del Arco et
al., 1991; Bridgham et al., 1995; Choi et al., 2005; Campo et al.,
2007) as well as between members of the same species (Birk &
Vitousek, 1986; Aerts & de Caluwe, 1994; Bungart & Hüttl
2004). Nutrient resorption proficiency (NRP), has been de-
scribed as a way to measure the success of nutrient conserva-
tion and to reflect environmental constraints of site conditions
(Killingbeck, 1996), particularly for nitrogen (N) and phospho-
rus (P). NRP can be described as the realized resorption or the
quantity of nutrient remaining in senesced tissue after retrans-
location. NRP trends between species (deciduous versus ever-
greens) across varying levels of environmental limitations (nu-
trients and water) appear to influence processes such as nutrient
uptake and productivity (Killingbeck, 1996). Killingbeck,
(1996) further pointed out that the variation found within his
results could be attributed to forest stand conditions as well as
the relationship between inter-nutrient dependence (i.e. N and P
levels).
Given the intensified demand for SRWC worldwide and in-
terest in increasing wood biomass production, determining
ways to enhance yield is paramount for plantation development
(Chang, 2003; Bungart & Hüttl, 2004; Coyle & Coleman, 2005;
DesRochers et al., 2006). Intensive culture of hardwoods is
often accompanied by site preparation, competition control,
genetically improved planting stock, and selection of fast-
growing species to increase the production potential (Fang et al.,
1999; Chang, 2001; Samuelson et al., 2001; Bungart & Hüttl,
2004; Lee & Jose, 2005; DesRochers et al., 2006). By far the
most advantageous of the silvicultural methods used to increase
production is fertilization (Allen, 1987). Fertilizer application,
while generally one of the least expensive silvicultural tools,
can become more costly than necessary if application rates
exceed nutrient uptake or demand of the trees, or does not result
in additional biomass production. When coupled with irrigation,
fertilization has the capability to increase production on infer-
tile sites, in areas where rainfall is limited, or on soils that lack
necessary water holding capacity (Axelsson & Axelsson, 1986;
Lockaby et al., 1997; King et al., 1999; Bekele et al., 2003,
Coyle & Coleman 2005). Many studies have indicated that
growth response to differing fertilization rates for economically
important tree species are species specific and/or vary with site
resource levels (Wienand & Stock, 1995; Jokela et al., 2004;
Prietzel et al., 2004; Sword Sayer et al., 2004; Ladanai et al.,
2006; Saarsalmi et al., 2006; Moscatelli et al., 2008). However,
questions remain regarding the extent that production could be
enhanced by increasing resource availability, and at what levels
additional resources become excessive or limit growth.
In the present study, we investigated the effect of water and
nutrient availability, on nutrient content (kg·ha–1), resorption
efficiency (%), resorption proficiency (g nutrient/kg leaf litter
(senesced tissue)), and leaf- and canopy-level nutrient use effi-
ciency of nitrogen (N), phosphorus (P), and potassium (K) for
Populus deltoidesBartr. (cottonwood), Quercus pagodaRaf.
(cherrybark oak, previously Quercus falcata Ell.) and Platanus
occidentalis L. (sycamore), (nomenclature follows USDA,
NRCS Plants Database 2009). Our objectives were to: 1) de-
termine the aboveground nutrient content for each nutrient for
each species across a nitrogen/water gradient; specifically, what
rates of fertilization are actually captured and utilized by the
canopy to influence production? 2) quantify the nutrient resorp-
tion efficiency and proficiency of N, P, and K for all three spe-
cies; specifically does an increase in foliar nutrient content
result in increased biomass production? 3) determine the nutri-
ent use efficiency on a leaf- and canopy-level basis for the three
nutrients and species. In particular, is nutrient use efficiency
decreased in similar magnitudes as the application of fertiliza-
tion? Are the amounts of fertilizer that are taken up reflected in
the magnitude of resorption? We hypothesized that nutrient
levels, budget, efficiencies, and ratios would peak well below
the maximum level of nitrogen supplied.
Methods
Study Site
Our study was conducted in a fertigation trial established on
an abandoned agricultural field (30.50'N, 87.11'W) in Santa
Rosa County, Florida, USA. The climate is temperate with mild
winters and hot, humid summers. Average rainfall is 1700 mm,
with average minimum and maximum temperatures of 10 and
27˚C, respectively (NOAA, 2003). The soil is characterized as a
well-drained, Redbay sandy loam (a fine-loamy, siliceous,
thermic, RhodicPaleudult) formed in thick beds of loamy ma-
rine deposits with an average water table depth of 1.8 m (Lee &
Jose, 2003). Soil variables calculated after this study ended
include pH (5.8, down from the original pH of 6.0), cation ex-
change capacity (4 CEC meq/100 g), and soil nutrient levels of
phosphorus (34 and 55), potassium (92 and 122), calcium (599),
and magnesium (179 and 146) (kg·ha–1). To our knowledge,
nitrogen levels were not measured prior to the study, but were
expected to be relatively high given the site was an abandoned
agricultural field. Nitrogen levels measured within the control
plots during a companion study indicated total inorganic nitro-
gen ranged from near 2.5 to 4.5 kg·ha–1 (Lee & Jose 2006).
Treatment plots of P. deltoides and P. occidentalis consisted
of 40 trees plot–1 and Q. pagoda contained 16 trees plot–1; (al-
though the Q. pagoda plots were the smallest of the three spe-
cies, and need to be treated with caution, the results reflect data
collected within the study) Figure 1. All treatment plots were
planted at 2.13 m × 3.35 m spacing (1400 trees ha–1). The study
design was a randomized complete block (RCB) with four rep-
lications of each treatment. Site preparation included disking
and subsoiling to facilitate planting. Fertilization at the time of
planting included broadcast application of diammonium phos-
phate, dolomitic lime, potash, and a micronutrient mixture.
These treatments added elemental calcium, nitrogen, phospho-
rus, magnesium, zinc, copper, and manganese (1009, 50, 56,
126, 3, 3, and 2 kg·ha–1 respectively, Greg Leach, personal
communication). Soil pH was adjusted to 6.0, with 3363
kg·ha–1 of dolomitic lime, based on recommendations from a
similar trial at North Carolina State University Research Coop-
erative (Coleman et al., 2004; Samuelson et al., 2004a; Sam-
uelson et al., 2004b).
Herbaceous weed control consisted of combinations of
188

D. E. HENDERSON, S. JOSE
REP 1REP 2REP 3REP 4
IRRIGATION
ZONE 4
Irrigation Only
IRRIGATION
ZONE 1
56 kg N
IRRIGATION
ZONE 2
112 kg N
IRRIGATION
ZONE 3
224kg N
REP 1
REP 2
REP 2REP 3REP 4
REP 1REP 3REP 4
Control
Control
Control
Control
IRRIGATION
CENTER
UNDERGROUND WATER PIPE
BUD DIAMOND ROAD
BUD DIAMOND ROAD
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
O
A
K
Figure 1.
Study layout showing planting schematic and treatment applications. For this study, only P. deltoides (cottonwood), Q. pagoda (cherrybark oak re-
ferred to in graphic as oak), and P. occidentalis were studied. Image reproduced from first year growth of Hardwoods under fertigationin western
Florida. Unpublished international paper internal report 1996. Gregory N. Leach and Homer H. Gresham, southern forest resources technical services,
western Florida region, Cantonment, Florida.
chemical (sulfometuron methyl and glyphosate) and mechanical
(mowing and manual pulling) treatments during the first and
second growing seasons. Installation of the nutrient supply
system and planting of trees occurred during spring 1995. The
irrigation system operated for approximately two hours each
day (on average 390 mm water Greg Leach, personal commu-
nication) during the growing season (May-Sep.) with nitrogen
application occurring two to eight minutes each day creating
the nitrogen gradient across the treatments (Lee & Jose, 2003,
2006). Five treatments were established including control
(CON), irrigation only (IRR), and three nutrient supplements
supplied through irrigation including 56, 112, and 224 kg
N·ha–1·yr–1 (referred to as IRR + 56, IRR + 112, and IRR + 224,
respectively).
Data Collection
Leaf samples were collected from upper one-third (sun
leaves) and lower one-third (shade leaves) of the canopy on a
monthly basis during the eighth growing season. Samples were
collected within each plot for each species, bagged, labeled, and
placed in a cooler for transport. Leaf area (cm2) was determined
by passing each leaf through a Li-Cor LI-3300 Leaf Area Meter
and then weighed to the nearest 0.01 g. Specific leaf weight
(SLW) was determined by dividing the foliar weight by area.
Samples of bark, branches, and wood were collected in mid-
growing season. Ten trees per treatment, per each species were
randomly selected for woody component (bark, branch, and
bole) nutrient analysis and combined, to obtain a treatment
level sample for nutrient content for each tissue type. Bark
sample removal was completed by surficially scraping, cutting,
breaking, or peeling samples from the trees of each species.
Collection of branches from the same randomly selected trees,
were gathered by pruning newly formed branches from the
lower and upper third of the canopy for each species. Collection
of bole material consisted of coring each randomly selected tree
at DBH (diameter at breast height ~1.5 m above ground level)
with an increment borer. Foliar and woody samples were dried
at 70˚C for 48 hours, ground to a fine powder and analyzed for
total nitrogen (N) (Kjeldahl), phosphorus (P) (EPA Method
200.7—ICP (Inductively Coupled Plasma) Spectrophotometer),
and potassium (K) at the University of Florida Analytical Re-
search Laboratory (ARL).
For biomass calculations used with nutrient data, diameter at
breast height (DBH) and height of all trees in each plot within
each treatment were measured yearly. Standing biomass
(Mg·ha–1), ANPP (Mg·ha–1·yr–1, excluding herbivory or litter of
branches, bark, or fruits), LAI (m2 m–2, calculated by multiply-
ing weight (g) and area (m2) of leaf litter collected in litter trays
by SLA (m2·g–1) of randomly selected canopy leaves), for year
eight. Whole-tree allometric equations developed by Shelton et
al., (1982) were used to calculate volume and aboveground
woody biomass for P. deltoides. Their equations for P. del-
toides were developed from trees of comparable age range, and
soil type, grown in areas with similar longitude, latitude, and
climate as this study. Standing woody biomass consisted of all
woody components. Foliage biomass was determined by sum-
ming the weight of annual litter fall collected monthly (May to

D. E. HENDERSON, S. JOSE
January) from five litter traps (0.5 m2) for P. deltoides.
Biomass equations developed by Schlaegel & Kennedy,
(1986) were used to calculate volume and aboveground woody
biomass for both Q. pagoda and P. occidentalis. The original
Schlaegel & Kennedy, (1986) equations used diameter meas-
ured at approximately 15 cm above ground level. All Q. pagoda
and P. occidentalis DBH data were corrected to reflect the dbh
measurements of the equations at 15 cm height above ground
level, by using regression equations developed from sampling
100 trees per species measured at the appropriate height (data
not shown, R2 = 0.97 and 0.93 respectively for Q. pagoda and
P. occidentalis). Foliage biomass was determined similarly as
above from five and two litter traps (0.5 m2), for P. occidentalis
and Q. pagoda respectively in each plot.
To determine nutrient use on a leaf and canopy level, pro-
jected LAI, was calculated from the weight (g) and area (m2) of
the leaf litter trays and SLA (scaled to the canopy level, m2·g–1)
for each species within each treatment. Care was taken to en-
sure only leaf litter from the species within the plot was proc-
essed. If litter from other species fell or were blown into the
tray, it was removed prior to collection.
Nutrient content of each species for each aboveground com-
ponent was calculated for N, P, and K using the equations used
for the purpose of biomass production estimation developed by
Shelton et al., (1982) and Schlaegel& Kennedy, (1986) and for
the calculation of the nutrient concentrations for woody and
foliar components (Equation (1)). The RE was calculated by
determining the difference between peak nutrient concentration
of green leaves and those found in fresh leaf litter (Equation (2)).
Leaf level nutrient use efficiency LNUE was calculated using
leaf level nutrient content and leaf litter resorption rates (Equa-
tion (3)). Canopy nutrient use efficiency (CNUE) was calculated
using aboveground biomass produced in year eight divided by
the peak production (peak foliar production was determined
from monthly leaf litter collection), and nutrient content of
green leaves for each species in each treatment (Equation (4)).
Resorption proficiency was reported as the nutrient content in
senesced leaves (g·N·kg–1 litter, i.e. realized resorption).
1) Nutrient content (kg·ha–1) = kg·ha–1(biomass) × kg·kg–1(nutrient )
2) Resorption (%) = (foliar(live) – foliar(litter)/foliar(live)) × 100
3) Leaf nutrient use efficiency (g·g–1) =1 /((g·g–1) × (1 – re-
sorption))
4) Canopy nutrient use efficiency (Mg·kg–1) = Mg/(kg foliage ×
kg·kg–1(nutrient))
Analysis
All the measured and calculated variables were compared
among treatments using analysis of variance (ANOVA) (SAS
Institute Inc., 2001) with treatment assigned as a random effect
in the model. If significant differences (α = 0.05) among treat-
ments were revealed, multiple pairwise comparisons of means
were performed using Tukey’s multiple mean test for mean
separation and determining significance. Linear regression was
used to analyze the relationships between ANPP and N:P. It has
been suggested that as soil nitrogen levels increase, uptake of
nitrogen can be limited by the availability of other nutrients
(Aber et al., 1989). Furthermore, because of results from stud-
ies like Pastor & Bridgham, (1999) and Bridgham et al., (1995)
we hypothesized that the highest rate of nitrogen application
would be far greater than the trees could utilize. As such, curvi-
linear functions were chosen a priori to ANOVA analysis and
in accordance with our hypothesis that nutrient use variable
responses were likely to plateau well below the maximum level
of N supplied by the treatments.
Results
Nutrient Con te nt
The N content of aboveground components (bole, branch,
bark and foliage: 4.0, 17.1, 1.8, and 217.7 kg·ha–1, respectively)
and the total N (240.5 kg·ha–1) of the combined aboveground
biomass in P. deltoides were significantly lower in the control
(CON) treatment compared to that of the IRR and IRR + Fer-
tilizer treatments (IRR + 56, IRR + 112, and IRR + 224). IRR
and IRR + 56, IRR + 112, and IRR + 224 treatments had simi-
lar total N content (502.9, 415.8, 422.1, and 439.0 kg·ha–1, re-
spectively, Table 1). In other words, N content for year eight
reached its highest at a level below the maximum N application
(502.9 kg·ha–1 in the IRR treatment). The overall trend for each
component (branch, bark, foliage) or total tree was to reach the
highest N content in the IRR treatment with significant differ-
ences found among the CON and all IRR treatments. The only
exception to this trend was for the bole content, which reached
its peak at the IRR + 56 treatment (10.5 kg·ha–1, Table 1)
which was not significantly different from the other IRR or IRR
+ Fertilizer treatments.
Branch, foliar, and total tree P nutrient budget for P. del-
toides exhibited similar trends as N by reaching its peak in the
IRR treatment (11.9, 37.6, and 50.6 kg·ha–1, respectively) with
significant differences found among treatments for each com-
ponent. Bole and bark P content reached their peaks in the IRR
+ 224, which was significantly different from all other treat-
ments, and IRR + 122 treatments (1.4 and 0.3 kg·ha–1, respec-
tively, Table 1). Significant differences were found among the
CON and all other IRR treatments. P. deltoides branch, bark
and total tree components for K reached its maximum content
in the IRR treatment, (70.6, 1.2, and 353.0 kg·ha–1, respectively,
Table 1), and were significantly different from the CON treat-
ment. Maximum K content for the bole and foliar components
were found in the IRR + 56 and IRR + 224 treatments (29.9 and
267.8 kg·ha–1, respectively) with significant differences found
among treatments.
Maximum N content for bole, branch and bark for Q. pagoda
(6.3, 8.9, and 4.8 kg·ha–1, respectively) was found in the IRR +
224 treatment and significant differences were found among
treatments for these components (Table 1). Maximum N for the
foliar and total tree occurred in the IRR + 112 treatment (367.1
and 382.2 kg·ha–1 , respectively) with significant differences
found only between the control and IRR + 112 treatments. For
P, the bole and bark components were greatest in the IRR + 224
treatment (0.3 and 0.2 kg·ha–1, respectively) while branch and
foliar components reached the highest levels in the IRR + 56
and IRR + 112 treatments (0.8 and 22.7 kg·ha–1, respectively).
Significant differences for the bole component were found
among the CON and IRR + 224 treatments and among treat-
ments for the branch component. The total tree peak P was
found in the IRR + 122 treatment, and was likely influenced by
the foliar P content level (23.7 kg·ha–1), although no significant
differences were found among treatments. For Q. pagoda, the
highest K for bole, branch, and bark in the IRR + 224 treatment
(5.9, 6.6, and 1.7 kg·ha–1, respectively). Foliar and total tree
peak K nutrient content was found in the IRR + 112 treatment
190

D. E. HENDERSON, S. JOSE
Table 1.
Average nutrient and standard deviation for nitrogen, phosphorus, and potassium content of bole, main branches, bark, foliage, and
total tree for P. deltoides, Q. pagoda, and P. occidentalis during year eight (2003) of the study. Letters indicate significant differ-
ences among treatments.
P. deltoides
N Bole kg·ha–1 Branch kg·ha–1 Bark kg·ha–1 Foliar kg·ha–1 Total
CON 4.0 (1.5)a 17.1 (6.2)a 1.8 (0.6)a 217.7 (44.1)a 240.5 (50.1)a
IRR 9.2 (2.0)b 56.1 (17.5)b 4.8 (1.4)b 432.8 (115.4)b 502.9 (135.8)b
IRR+56 10.5 (3.0)b 46.5 (13.2)b 4.4 (1.2 b 354.4 (45.6)b 415.8 (62.2)b
IRR+112
9.1 (2.2)b 42.8 (9.9)b 4.2 (0.9)b 366.0 (26.5)b 422.1 (36.1)b
IRR+224
10.0 (2.0)b 48.7 (9.5)b 3.8 (0.7)b 376.5 (34.0)b 439.0 (37.6)b
P
CON 0.5 (0.2)a 3.6 (13.3)a 0.1 (0.0)a 18.4 (3.7)a 22.6 (5.0)a
IRR 0.8 (0.2)a 11.9 (3.7)c 0.3 (0.1)b 37.6 (10.0)b 50.6 (13.9)b
IRR+56 0.8 (0.2)a 8.4 (2.4)bc 0.2 (0.1)b 26.8 (3.4)ab 36.2 (6.0)ab
IRR+112
0.7 (0.2)a 7.6 (1.8)ab 0.3 (0.1)b 27.9 (2.0)ab 36.6 (3.6)ab
IRR+224
1.4 (0.3)b 9.4 (1.8)bc 0.3 (0.1)b 28.2 (2.5)ab 39.3 (3.6) b
K
CON 8.3 (3.1)a 20.0 (7.3)a 0.4 (0.1)a 139.5 (28.3)a 168.1 (37.1)a
IRR 19.5 (4.2)b 70.6 (22.0)b 1.2 (0.3)b 261.9 (69.8)b 353.0 (95.5)b
IRR+56 29.9 (8.6)c 60.7 (17.3)b 1.1 (0.3)b 220.6 (28.4)b 312.2 (53.6)b
IRR+112
17.4 (4.1)ab 61.8 (14.4)b 1.0 (0.2)b 236.5 (17.1)b 316.8 (32.4)b
IRR+224
23.9 (4.7)bc 57.7 (11.2)b 1.1 (0.2)b 267.8 (24.2)b 350.6 (30.9)b
Q. pagoda
N Bole kg·ha–1 Branch kg·ha–1 Bark kg·ha–1 Foliar kg·ha–1 Total
CON 1.7 (0.5)a 2.9 (0.9)a 1.6 (0.5)a 153.0 (124.4)a 159.3 (126.2)a
IRR 2.9 (1.0)a 5.4 (1.5)ab 3.0 (1.0)ab 266.1 (102.8)ab 277.4 (105.6)ab
IRR+56 2.9 (0.9)a 5.0 (1.5)ab 2.9 (0.9)ab 308.8 (58.6)ab 319.7 (61.5)ab
IRR+112
4.6 (0.8)b 6.4 (1.4)b 4.1 (0.7)bc 367.1 (33.7)b 382.2 (31.8)b
IRR+224
6.3 (0.4)c 8.9 (0.6)c 4.8 (0.3)c 294.0 (68.1)ab 314.0 (69.0)ab
P
CON 0.2 (0.1)a 0.5 (0.1)a 0.1 (0.0)a 11.0 (9.0)a 11.7 (9.2)a
IRR 0.3 (0.1)ab 0.7 (0.2)a 0.1 (0.0) a 16.6 (6.4)a 17.7 (6.7)a
IRR+56 0.2 (0.1)ab 0.8 (0.2)a 0.1 (0.0)ab 19.0 (3.6)a 20.2 (3.9)a
IRR+112
0.2 (0.0)ab 0.6 (0.1)a 0.2 (0.0)bc 22.7 (2.1)a 23.7 (2.0)a
IRR+224
0.3 (0.0)b 0.7 (0.1)a 0.2 (0.0)c 18.1 (4.2)a 19.3 (4.3)a
K
CON 2.3 (0.8)a 2.5 (0.7)a 0.3 (0.1)a 64.9 (52.8)a 70.0 (54.3)a
IRR 3.1 (1.1)ab 3.6 (1.0)ab 0.5 (0.2)a 100.4 (38.8)b 107.5 (40.6)ab
IRR+56 3.6 (1.1)ab 4.2 (1.3)ab 0.9 (0.3)b 104.5 (19.8)b 113.2 (22.2)ab
IRR+112
4.3 (0.7)bc 4.9 (1.0)bc 1.3 (0.2)bc 151.6 (13.9)b 162.1 (12.6)b
IRR+224
5.9 (0.4)c 6.6 (0.5)c 1.7 (0.1)c 122.0 (28.2)b 136.2 (28.9)ab
P. occide ntalis
N Bole kg·ha–1 Branch kg·ha–1 Bark kg·ha–1 Foliar kg·ha–1 Total
CON 6.2 (0.8)a 4.3 (0.6)a 2.4 (0.3)a 278.6 (41.9)a 291.4 (41.1)a
IRR 9.0 (0.2)b 8.9 (0.8)c 4.7 (0.2)c 536.6 (73.2)b 559.1 (74.1)b
IRR+56 9.1 (0.6)b 8.6 (0.5)c 4.6 (0.3)c 511.5 (31.8)b 534.0 (31.9)b
IRR+112
11.9 (0.3)c 6.7 (0.2)b 3.7 (0.1)b 470.9 (14.1)b 493.1 (13.9)b
IRR+224
9.9 (1.3)b 8.5 (1.0)c 4.2 (0.5)bc 482.0 (47.5)b 504.6 (49.1)b
P
CON 1.0 (0.1)a 0.3 (0.1)a 0.4 (0.0)a 24.8 (3.7)a 26.9 (3.6)a
IRR 2.1 (0.1)b 1.6 (0.2)b 0.0 (0.0)c 41.7 (5.7)c 45.6 (5.8)c
IRR+56 2.2 (0.2)b 1.5 (0.1)b 0.0 (0.0)c 39.7 (2.5)bc 43.7 (2.5)c
IRR+112
2.2 (0.1)b 0.9 (0.0)a 0.0 (0.0)b 34.6 (1.0)bc 38.0 1.0)bc
IRR+224
1.3 (0.2)b 0.9 (0.1)a 0.3 (0.0)b 33.1 (3.3)c 35.5 (3.4)b
K
CON 6.7 (0.9)a 3.6 (0.5)a 0.3 (0.0)a 146.0 (22.0)a 156.7 (21.3)a
IRR 10.3 (0.2)b 6.6 (0.6)c 1.3 (0.1)c 257.5 (35.1)b 275.7 (35.8)b
IRR+56 10.5 (0.7)c 6.4 (0.4)c 1.3 (0.1)c 245.5 (15.1)b 263.7 (15.5)b
IRR+112
12.3 (0.3)c 4.2 (0.2)a 1.3 (0.0)c 226.0 (6.8)b 243.7 (6.6)b
IRR+224
10.6 (1.4)c 5.1 (0.6)b 1.0 (0.1)b 213.0 (21.0)b 229.2 (22.1)b

D. E. HENDERSON, S. JOSE
with significant differences found among the CON and IRR +
112 treatments (151.6 and 162.1 kg·ha–1, respectively).
P. occidentalis had its highest N and K contents in the IRR
treatment for branch, bark, foliar, and total tree components
(8.9, 4.7, 536.6, and 559.1 kg·N·ha–1 and 6.6, 1.3, 257.5 and
275.7 kg·K·ha–1, respectively) with significant differences
found among treatments. Both N and K bole content were
greatest in the IRR + 112 treatment (11.9 and 12.3 kg·N·ha–1
and kg·K·ha–1, respectively) with significant differences found
among treatments. Maximum P content for P. occidentalis oc-
curred in the IRR + 56, IRR, CON, and IRR treatments for bole,
branch, bark, foliar and total content (2.2, 1.6, 0.4, 41.7, and
45.6 kg·P·ha–1, respectively) with significant differences found
among treatments.
Nutrient Us e, Resorption Effici en cy an d P r o f ic ie ncy
No significant differences were found for RE or LNUE for
any of the three species across all treatments for N, P, or K
(Table 2, RE ranged from 65.1 CON to 57.0% IRR + 112, 57.6
CON to 52.8% IRR + 112 and 85.2 CON to 72.2% IRR + 56,
for N, P, and K, and LNUE ranged from 136.3 CON to 106.6
g·g–1 IRR + 112, 1231.7 CON to 1103.2 g·g–1 IRR + 56, and
732.4 CON to 331.2 g·g–1 IRR + 224 for N, P, and K, respec-
tively). CNUE for all three species and nutrients (Table 3)
followed irregular patterns. Only N and K for P. deltoides,
exhibited significant differences between treatments. N and K
peaked in the IRR + 56 (5.1 and 5.6 Mg·kg–1, respectively) and
IRR treatments respectively. For both nutrients, CNUE was
lowest in the IRR + 112 treatment (3.3 and 3.8 g·g–1, respec
tively). For RP no significant differences were found for any of
the three species across all treatments for N, P, or K (Figure 2).
N:P and AN PP
No significant relationship was found for N:P and above-
ground net primary productivity (ANPP) for P. deltoides (Fig-
ure 3). The trend for Q. pagoda and P. occ i de nt al i s for N:P and
ANPP (Figure 4) was a significant (p > 0.05) curvilinear rela-
tionship with the peak occurring at or near the N:P ratio of 17
and 14 respectively. For both species, when N:P increased past
these points, ANPP tended to decrease.
Discussion
We wanted to determine how resources were utilized for
biomass production, with respect to varying levels of irrigation,
nitrogen, or the combined application of irrigation and nitrogen
application (fertigation, IRR + 56, IRR + 112, and IRR + 224).
The differences between N uptake and utilization, reflected in
the N content of the combined aboveground parts, for P. del-
toides and P. occidentalis was likely influenced by the greater
biomass production of these two species than was seen in Q.
pagoda, and was more highly influenced by the irrigation
treatment for P. deltoides and P. occidentalis than for Q. pa-
goda (Table 1). Despite these differences, N content in Q. pa-
goda were greater at higher N application rates. Rowe et al.,
(2002) found a similar relationship for loblolly pine but found
Table 2.
Average % nutrient resorption efficiency (RE%) and leaf level nutrient use efficiency (LNUE g·g–1) for nitrogen (N), phosphorus
(P), and potassium (K) with standard deviation for P. deltoides), Q. pagoda, and P. occidental during year eight (2003) of the study.
Letters indicate significant differences among treatments.
RE LNUE
P. deltoides N P K N P K
CON 65 (9)a 58 (11)a 85 (8)a 136 (13)a 1250 (76)a 732 (182)a
IRR 62 (4)a 56 (6)a 81 (14)a 116 (20)a 1232 (299)a 418 (345)a
IRR+56 60 (3)a 56 (7)a 72 (8)a 112 (19)a 1103 (88)a 363 (158)a
IRR+112
57 (2)a 53 (7)a 72 (9)a 107 (7)a 1118 (74)a 361 (118)a
IRR+224
63 (5)a 57 (7)a 83 (8)a 111 (15)a 1037 (182)a 331 (183)a
Q. pagoda
CON 62 (4)a 40 (6)a 64 (22)a 140 (7)a 1107 (131)a 274 (80)a
IRR 60 (5)a 39 (6)a 57 (11)a 114 (12)a 1092 (84)a 265 (31)a
IRR+56 60 (7)a 37 (2)a 54 (18)a 114 (12)a 1031 (72)a 270 (125)a
IRR+112
62 (7)a 37 (5)a 51 (8)a 113 (21)a 1049 (84)a 214 (63)a
IRR+224
61 (7)a 45 (16)a 52 (18)a 111 (23)a 1035 (95)a 218 (72)a
P. occide ntalis
CON 74 (4)a 57 (13)a 85 (3)a 176 (37)a 944 (112)a 476 (76)a
IRR 72 (6)a 51 (3) a 83 (6)a 144 (7)a 886 (42)a 404 (79)a
IRR+56 70 (5)a 50 (4)a 83 (5)a 132 (26)a 866 (81)a 373 (92)a
IRR+112
70 (7)a 52 (10)a 82 (4)a 126 (22)a 863 (97)a 376 (107)a
192

D. E. HENDERSON, S. JOSE
Table 3.
Canopy nutrient use efficiency (CNUE) of unit woody biomass (Mg)
per unit nitrogen, phosphorus, and potassium (kg) for P. deltoides, Q.
pagoda, and P. occidentalis for year eight (2003) of the study for each
treatment. Letters indicate significant differences among treatments.
CNUE
P. deltoides N (Mg·kg–1) P (Mg·kg–1) K (Mg·kg–1)
CON 3.5 (0.3)a 40.5 (3.3)a 4.8 (1.2)ab
IRR 4.9 (0.3)b 55.6 (9.4)a 6.3 (1.0)a
IRR+56 5.1 (0.6)b 63.6 (9.9)a 5.6 (1.0)ab
IRR+112
3.3 (0.5)a 43.5 (8.9)a 3.8 (0.7)b
IRR+224
4.1 (1.2)ab 59.8 (28.4)a 4.4 (3.5)ab
Q. pagoda
CON 2.1 (0.3)a 26.3 (1.9)a 4.2 (0.4)a
IRR 1.5 (0.2)a 23.3 (4.4)a 4.0 (1.3)a
IRR+56 1.3 (0.4)a 23.2 (5.1)a 3.9 (0.7)a
IRR+112
1.3 (0.4)a 20.9 (5.1)a 3.2 (0.7)a
IRR+224
1.5 (0.7)a 23.3 (3.3)a 2.9 (0.6)a
P. occidentalis
CON 1.9 (0.5)a 23.1 (7.5)a 3.0 (0.7)a
IRR 1.8 (0.8)a 22.1 (7.6)a 3.1 (1.8)a
IRR+56 1.6 (0.4)a 20.4 (2.5)a 2.6 (0.6)a
IRR+112
1.3 (0.3)a 19.6 (3.9)a 2.6 (0.7)a
IRR+224
1.8 (0.1)a 23.2 (3.7)a 3.4 (1.8)a
that genetic differences among families resulted in greater
number of shoots in stem cuttings. Our hypothesis of nutrient
levels peaking well below the maximum rate of N application
was true for two of the three species.
For the combined aboveground parts N, P, and K nutrient
content were highly affected by the large foliar fraction for all
three species (Table 1). Water availability necessary for nutri-
ent uptake (Lambers et al., 1998) regulates foliar production
(Jose & Gillespie, 1996, 1997) and therefore the amount of
woody biomass that can be produced (Henderson & Jose, 2010).
Soils for this area are sandy and well drained; suggesting, for
this combination of species and soil parameters, low water
storage capacity and therefore water availability may be as
limiting for growth and production as N for these early succes-
sional species. In fact, the last five years of this study
(1999-2003), combined irrigation application and annual rain-
fall totals were either below or consistent with historic rainfall
averages for this site (Henderson & Jose, 2010). Lockaby et al.,
(1997) suggested that cultural treatments could exacerbate
moisture needs of early successional species in well-drained
soils. P. deltoides and P. occidentalis reached their maximum N
budget in the IRR treatment. Given the inherent fertility of an
abandoned agriculture field, these species may have had their
nutrient requirements met by past land management techniques.
From our analysis, it appears that not only did the fertigation
treatments not significantly alter nutrient uptake or biomass
production in year eight, (Henderson & Jose, 2010) but also the
N treatments may have increased water requirements, which
may not have been met by the fertigation treatments. Wilson et
al. (2012) suggested that microbial and soil chemical processes
influence plant N uptake such that colloidal soil particles or
Figure 2.
Average and standard error of nutrient resorption proficiency (g
nutrient kg–1 dry weight) of litterfall nitrogen (A), phosphorus (B),
and potassium (C) for P. deltoides (square), Q. pagoda (triangle),
and P. occi- dentalis (circle).
Figure 3.
N:P foliar ratios for P. deltoides, Q. pagoda, and P. occidentalis for
each treatment during year eight (2003) of the study. Letters above
the treatments indicate significant differences.

D. E. HENDERSON, S. JOSE
Figure 4.
Biomass production (Mg·ha–1·yr–1) and foliar N:P for year eight
(2003) of the study for P. deltoides (A), Q. pagoda (B), and P.
occidentalis (C) for all treatments (circle = CON, square = IRR,
triangle = IRR + 56 kg N·ha–1·yr–1, diamond = IRR + 112 kg
N·ha–1·yr–1, and X = IRR + 224 kg N·ha–1·yr–1).
microbes competed for N if additional amino acids were not
supplied in addition to fertilization. Our findings were substan-
tiated by the lack of significant differences between the treat-
ments.
In a companion study, Lee & Jose, (2005) found that after
seven years of fertigation treatments, between 46 - 60
kg·N·ha–1·yr–1 was lost in groundwater on an annual basis in the
IRR + 56 treatment. They found that between 65% and 96% of
the nitrate applied in the P. deltoides treatments was leached
from the site and suggested that N application rates above the
IRR + 56 treatment could not be utilized for increased growth
exceeding the biological and non-biological N retention capac-
ity of the system (Lee & Jose, 2005). These findings suggest
that nutrient availability in old agricultural fields may be suffi-
cient for maximum production, and depending on the desired
length of rotation for short-rotation woody crops (SRWC), it
could be suggested from this study that by year eight, any ad-
vantage of N application would not be realized in additional
uptake or biomass production (Henderson & Jose, 2010). It
could also be suggested that thinning should occur to relieve
below ground competition, release the most desirable trees
within the stands, and that then additional N application might
be utilized for additional biomass production.
The distributions and amount of N, P, and K (Table 1)
within each tissue component for these three species are reflec-
tive of both the range in biomass produced between the treat-
ments and the nutrient availability supplied by each treatment.
Other studies have found similar nutrient content values, on an
area basis, for the same set of tissue components to those found
in the CON and IRR treatments. For these studies, direct com-
parisons of nutrient content values are marginal at best, as spe-
cies, site conditions, and treatments were dissimilar. For in-
stance, Lugo et al., (2011) found similar N, P, and K (kg·ha–1)
for Spathodea campanulata in north central Puerto Rico that
were harvested from karst and volcanic sites which were com-
parable to the whole tree values found in this study.
A few studies have investigated the effects of thinning
(Blanco et al., 2006), mixed species stands (Vogel & Gower
1998; Wang et al., 2000), or multiple aged trees (Miller et al.,
1993), chronosequence studies of single species (Wang et al.,
1995, 1996), or the effect of elevated CO2 on nutrient contents
(Calfapietra et al., 2007) but did not entail analysis of nutrient
budgets across a fertilization gradient. In a thinning study of
unfertilized 32-year old stand of Pinus sylvestris L., conducted
by Blanco et al., (2006), they found N total content values ten
times higher than were found in this study (4193 - 5641 kg·ha–1
versus our 240 - 502 kg·ha–1 for P. deltoides). A study con-
ducted by Wang et al., (1996) consisting of a mixed Betula
papyrifera Marsh and Abies lasiocarpa (Hook) Nutt., total tree
N content for 75-year old B. papyrifera were similar to the
values found in the IRR + 224 treatment in this study (431
kg·ha–1 versus 439 kg·ha–1 found in our study). The values of P
and K reported by these authors were higher and lower, respec-
tively, than were found in our study (65 and 217 kg·ha–1 versus
22.6 - 50.6 and 168.1 - 353 kg·ha–1 of P and K. respectively).
However, the findings from the Wang et al., (1996) study were
based on soils without any amendments. Vogel & Gower,
(1998) found much lower total N values in a mixed stand of
Pinus banksiana Lamb. and Alnus crispus (Ait.) Pursh. than
were found for P. deltoidesin our study but were similar to
those found for Q. pagoda in the CON treatment (170 versus
168 kg·ha–1 found in our study). The conditions for their study
consisted of a much shorter growing season and degraded soils
making direct links between the two studies only superficially
comparable. In a study designed to determine NUE for Euca-
lyptus spp., Safou-Matondo et al., (2005) found similar total N,
P, and K content for a similarly aged plantations that had been
fertilized at the time of planting. Their findings suggest that
species or clones selected for superior growth produce high
quantities of biomass with low levels of nutrient availability. If
the species selected for this study had been hybrid or clonal
varieties, it is likely much greater amounts of biomass could
have been produced.
Lambers et al., (1998), suggests that at least on a short-term
basis, the application of one nutrient can force additional uptake
of other nutrients. Further, Van Den Driessche, (2000) sug-
gested that increased P could result in copper or zinc deficien-
cies after 14 weeks resulting in decreased leaf and root biomass.
The question could then be asked, can the application of one
specific nutrient (N) not only alter the rates of uptake of other
nutrients (P and K), but would these effects be long-term so that
194

D. E. HENDERSON, S. JOSE
increased nutrient contents are reflected in the content of bole,
branches, and bark components? For our study, when compared
to CON, it appears that increased levels of N application in-
creased the P content of all components of P. deltoides and Q.
pagoda for all treatments. P. occidentalis had similar results,
with the exception of P content for branches in the IRR+112
and IRR+224 treatments (Table 1). For K, when comparing
the CON to all other treatments, all three species had increased
K content with increased N application (Table 1). Our hy-
pothesis of aboveground nutrient content for N, P, and K peak-
ing well below the maximum input of N can only be partially
supported.
In general, studies have found that plants growing in nutrient
poor habitats have mechanisms to conserve and recycle nutri-
ents more efficiently than those found in nutrient rich environ-
ments (Aerts, 1996; Feller et al., 1999; May et al., 2005). No
significant differences were found for RE in our study (Table 2)
and the relationships in our findings were not strong enough to
support our hypothesis of RE peaking below the maximum
level of N application. The RE levels we found for N, P, and K
for all three species were similar to other studies for N. Pug-
naire and Chapin, (1993) found RE levels ranging from just
over 60% and up to slightly greater than 80%. P. occidentalis
had the highest rates of RE ranging from 66% in the IRR + 224
treatment to 74% in the CON treatment (Table 2) while P.
deltoides (57% to 65%) and Q. pagoda (60% to 62%) RE were
similar to the lower ranges Pugnaire & Chapin (1993) found for
several chaparral species grown in nutrient poor soils. Other
authors (Eckstein et al., 1999; Drenovsky & Richards, 2006;
May et al., 2000; Cai & Bongers, 2007; Calfapietra et al., 2007)
have reported similar RE values. Feller et al., (1999) found P
RE values for P fertilized Rhizophora mangle (red mangrove)
trees (approximately 48% to 55%) similar to P. deltoides (53 to
58%) and P. occidentalis (51% to 57%). These values agree
with Aerts & Chapin, (2000) for deciduous species and Ko-
zovits et al., (2007) for two savanna tree species Qualea par-
viflora and Schefflera macrocarpa for P RE. Hagen-Thorn et al.,
(2006) and Chatain et al., (2009) found K RE values for Quer-
cus robur L., (English oak) and Nothofagus species (approxi-
mately 38% and 40%, respectively) that were similar for Q.
pagoda in this study (37% to 45%). Blanco et al., (2009) found
K RE values that were more similar (upwards of 80%) to those
found for P. deltoides (72% to 85%) and P. occidentalis (73%
to 85%). The three species in this study could be described as
being moderately efficient at resorption (Killingbeck, 1993).
When these findings are considered singularly, a slight decrease
in nutrient resorption might seem unimportant and would sug-
gest that the nutrient levels in an abandoned agricultural field
would be sufficient to allow biomass production for SRWC.
However, when compared to the IRR and fertigation treatments
for all three species, significant biomass production differences
were found (Henderson & Jose, 2010). Together these findings
indicate that while RE was not significantly altered by the ap-
plication of N, which would suggest ample nutrient availability,
for P. deltoides RE for all three nutrients was very similar be-
tween the CON and IRR+224 treatments suggesting something
other than N supply may have been controlling RE for this
species. This relationship was not reflected in the RE patterns
for the other two species, with the exception of N for Q. pagoda,
indicating a species-specific mechanism for P. deltoides RE. If
the sink strength (Nambiar & Fife, 1991) of the woody biomass
produced were the constraint for nutrient resorption, then the
trends of RE should mirror the trends we found for biomass.
Although the relationship appears to be minor, the additional
biomass in the IRR fertigation treatments did not appear to be
the cause of similar RE values across treatments.
Nutrient resorption proficiency (NRP) can be used as a
measure to judge the level by which species reduce nutrients in
their senescing leaves (Killingbeck, 1996). To this end, NRP
can be utilized as an index of soil fertility, site ability to supply
adequate nutrients in proper ratios for biomass production, and
determine potential and realized resorption (Killingbeck, 1996;
Drenovsky & Richards, 2006). The values we found for N in
the leaf litter, for all three species, agree with the findings of
other authors (Yuan & Li, 2007(for N 6 g·kg–1)). Most studies
report NRP either as a percentage or on an area basis. However,
due to lack of leaf area data for the litter, we report NRP on the
dry weight basis similar to the above studies. Although the lack
of significant findings suggests our results cannot support the
hypothesis of NRP peaking well below the maximum level or
N application, we did find that the highest N, P, and K NRP
were at levels below the highest rate of N application (Figure
2). While no studies could be found that reported P and K NRP
on a dry weight basis, we suggest that because the N-, P-, and
K-NRP values for all three species were so similar between the
species, no one species appeared to minimize nutrient loss for
these specific nutrients. Percent resorption for all three nutrients
and all three species exceeded the >1.0% Killingbeck, (1996)
used to describe incomplete resorption (data not shown). It
appears that adequate balance of all three nutrients were avail-
able such that the trees were not attempting to conserve any one
specific nutrient.
Our LNUE (Table 2) values agree with the findings of other
studies (Tateno & Kawaguchi, 2002 (70 to 130 g·N·g–1 leaf
litter)). However, LNUE does not necessarily correspond to
patterns found for CNUE (Table 3). LNUE appeared to be
more closely related to regulating nutrient balance, as supported
by the lack of significance for resorption, while CNUE appear
to be more highly influenced by the amount foliar biomass
needed to support the woody biomass accrued, although sink
strength would not appear to be the driving factor. For this
study, it could be suggested that the decomposition and nutrient
release from leaf litter was N dependent, such that because of
the apparent increased rates of P and K found with increased N
application (within various woody components) were needed to
retain nutrient balance. Both foliar and woody components
influenced and were integral in the calculation of CNUE. With
these findings, we cannot fully support our hypothesis of
CNUE peaking well below the maximum input of N, as P.
occidentalis P- and K-CNUE peaked in the IRR+224 treatment,
but not significantly.
Our findings for the N:P (Figure 3) suggests that as more N
was applied through the fertigation system, more P was taken
up. All three species, although not significant for P. deltoides or
Q. pagoda, show slightly increased N:P with increased N ap-
plication (11 - 13, 13 - 16, 11 - 14 for P. deltoides, Q. pagoda,
and P. occidentalis CON vs IRR+224). N:P ratios have been
used to identify nutrient limitations that limit plant growth in-
dicating either N or P deficient growing conditions. Several
authors have suggested ranges of N:P that indicate nutrient
deficiencies (<ranging from 8.3 to 10.9 Millner & Kemp, 2012),
(11 - 18 Graciano et al., 2006), ≤14 were likely to be N limited
and ≥16 were likely P limited (Koerselman & Meuleman, 1996;
Aerts & Chapin, 2000; and <10 or >10 Lambers et al., 1998),

D. E. HENDERSON, S. JOSE
although a few studies have indicated rations a high as 27 (Vogt
et al., 1986).
Knecht & Goransson, (2004) suggest that plants require nu-
trients in optimal ratios, but that these ratios may not be con-
stant across species depending on which nutrients are limiting
for growth. They also suggest that nutrients may be taken up in
excess of the levels required for growth. Further, Song et al.,
(2010) found that moderate application of N increased the P
concentrations in leaves and roots of Bauhinia faberi seedlings
with the addition of water, but also noted that high levels of N
application decreased growth. In another study, Graciano et al.,
(2006) found that the addition of P increased the absorption of
N in young Eucalyptus grandis. On an unfertilized site in New
Zealand, Millner & Kemp, (2012) found N:P ratios were spe-
cies specific and indicated some Eucalyptus had intrinsic abili-
ties to accumulate macronutrients such that some could more
readily accumulate P than N. When comparing the relationship
between N and P and N and K nutrient content for the wood
component in our study, regression analysis indicates strong
relationships for all three species (R2 0.51, 0.87, 0.78, 0.95,
0.45, and 0.96 for P. deltoides, Q. pagoda, and P. occidentalis,
respectively, data not shown). Relationships for the other com-
ponents would be expected to be similar as the nutrient content
for N, P, and K in the wood component was the lowest for all
of the components investigated. Our findings would support the
need for plants to maintain nutrient balance.
In further support of these findings, when ANPP was plotted
against N:P (Figure 4) particular trends become apparent. At
the lower bounds of the N:P for P. deltoides (CON and IRR),
production was lowest suggesting N may be limiting biomass
production. At the point where N and P would appear to be in
the correct ratio, the largest ANPP gains were detected. Sig-
nificant trends were apparent for Q. pagoda and P. occidentalis.
For both species, the lowest rates of ANPP were in the range of
N:P that would suggest N limitation. As N:P reached the range
of balance, maximum production was observed for these spe-
cies. ANPP then declined when N:P was higher (≥16) suggest-
ing P was becoming more limiting for growth or that the higher
rates of N application wee growth limiting. At this point in the
correlation, N application for both species was at IRR + 112 or
224 N·ha–1·yr–1, further supporting the hypothesis of a pla-
teauing response to N application.
Bungart & Hüttl, (2004) report both biomass production and
N:P for Poplar clones. Although their data suggests greater
biomass production may have been related to clonal differences,
the N:P between plots of varying hybrids also indicates a com-
pensatory mechanism of nutrient uptake and balance to biomass
production for this species. Lockaby & Conner, (1999) also
found that within an optimum range of N:P (approximately 12),
greater leaf biomass was produced. Like our study, other au-
thors have found that these relationships are likely species spe-
cific (Lockaby & Conner, 1999; Aerts & Chapin, 2000; Dre-
novsky & Richards, 2006; Specht & Turner, 2006; Millner &
Kemp, 2012) and are potentially tied to genotype. It could be
suggested that periodic testing of N:P in SRWC would assist
fertilization management to obtain maximum biomass by cir-
cumventing nutrient imbalance.
Conclusion
We found that aboveground nutrient content, nutrient resorp-
tion efficiency and proficiency, and leaf- and canopy-level
nutrient use efficiency are not necessarily influenced by in-
creased nitrogen availability. Although nutrient contents and
levels tracked over several growing seasons might indicate
differing levels of nutrient uptake, use, storage, and remobiliza-
tion, we believe our findings are representative of this entire
study length as nutrient application was consistent across years.
While many plants have adaptations to conserve nutrients when
nutrient levels are low, the available resources supplied by an
abandoned agricultural field appear to be sufficient as to not
alter the mechanism for nutrient conservation. Additionally, we
found that maximum biomass production was not necessarily
tied to maximum nutrient input. Production as well as nutrient
requirements are species specific and may include a compensa-
tory mechanism providing sufficient resources available from
the site, to deter nutrient imbalance. These findings could sug-
gest that if N and P are supplied simultaneously, regular inspec-
tion of the N:P should occur throughout a rotation to ensure
nutrient uptake remained balanced for maximum biomass pro-
duction for SRWC species.
Acknowledgements
This project was funded in part by the School of Natural Re-
sources and Environment at the University of Florida, the Wil-
liam Paul Shelly Sr. Memorial Fund at the School of Forest
Resources and Conservation and International Paper.
REFERENCES
Aber, J. D., Nadelhoffer, K. J., Steudler, P., & Melillo, J. M. (1989).
Nitrogen saturation in northern forest ecosystems. Biological Sci-
ences, 39, 378-386. doi:10.2307/1311067
Aerts, R. (1996). Nutrient resorption from senescing leaves of perenni-
als: Are there general patterns? Journal of Ecology, 84, 597-608.
doi:10.2307/2261481
Aerts, R. (1997). Nitrogen partitioning between resorption and decom-
position pathways: A trade-off between nitrogen use efficiency and
litter decomposability. Oikos, 80, 603-606. doi:10.2307/3546636
Aerts, R. & Berendse, F. (1988). The effect of increased nutrient avail-
ability on vegetation dynamics in wet heathlands. Vegetatio, 76, 63-
69.
Aerts, R., & Chapin III, F. S. (2000). The mineral nutrition of wild
plants revisited. A re-evaluation of processes and patterns. Advances
in Ecological Research, 3 0, 1-67.
doi:10.1016/S0065-2504(08)60016-1
Aerts, R. & de Caluwe, H. (1994). Nitrogen use efficiency of Carex
species in relation to nitrogen supply. Ecology, 75, 2362-2372.
doi:10.2307/1940890
Albaugh, T. J., Allen, H. L., Dougherty, P. M., & Johnsen, K. H. (2004).
Long term responses of loblolly pine to optimal nutrient and water
resource availability. Forest Ecology and Management, 192, 3-19.
doi:10.1016/j.foreco.2004.01.002
Albaugh, T. J., Allen, H. L., Dougherty, P. M., Kress, L. W., & King, J.
S. (1998). Leaf area and above- and belowground growth responses
of loblolly pine to Nutrient and water additions. Forest Science, 44,
317-328.
Allen, C. B., Will, R. E., McGravey, R. C., Coyle, D. R., & Coleman,
M. D. (2005). Radiation-use efficiency and gas exchange responses
to water and nutrient availability in irrigated and fertilized stands of
sweetgum and P. occidentalis. Tree Physiology, 25, 191-200.
doi:10.1093/treephys/25.2.191
Allen, C. B., Will, R. E., Sarigumba, T., Jacobson, M. A., Daniels, R. F.
& Kennerly, S. A. (2004). Relationships between canopy dynamics
and stem volume production of four species receiving irrigation and
fertilization. In K. F. Connor (Ed.), Proceedings of the 12th biennial
southern silviculture research conference (p. 594), Asheville, 24-28
196

D. E. HENDERSON, S. JOSE
February 2003.
Allen, H. L. (1987). Forest fertilizers. Journal of Science and Technol-
ogy for Forest Products and Processes, 85, 37-46.
Allen, H. L., Albaugh, T. J., & Johnsen, K. (2002). Water and nutrient
effects on loblolly pine production and stand development on a san-
dhill site. General. Asheville, NC: Department of Agriculture, Forest
Service, Southern Research Station.
Augusto, L., Bakker, M. R., de Lavaissiere, C., Meille, L., & Saur, E.
(2009). Estimation of nutrient content of woody plants using al-
lometric relationships: Quantifying the difference between concen-
tration values from the literature and actual. Forest, 82, 463-477.
Axelsson, E., & Axelsson, B. (1986). Changes in carbon allocation
patterns in spruce and pine trees following irrigation and fertilization.
Tree Physiology, 2, 189-204.
Bekele, A., Hudnall, W. H., & Tiarks, A. E. (2003). Response of den-
sely stocked loblolly pine (Pinus taeda L.) to applied nitrogen and
phosphorus. Southern Journal of Applied Forestry, 27, 180-189.
Berendse, F., & Aerts, R. (1987). Nitrogen use efficiency: A biologi-
cally meaningful definition? Functional Ecology, 1, 293-296.
Birk, E. M., & Vitousek, P. M. (1986). Nitrogen availability and nitro-
gen use efficiency in loblolly pine stands. Ecology, 67, 69-79.
doi:10.2307/1938504
Blanco, J. A., Imbert, J. B., & Castillo, F. J. (2006). Effects of thinning
on nutrient content pools in two Pinus sylvestris forests in the west-
ern Pyrenees. Scandinavian Journal of Forest Research, 21, 143-
150. doi:10.1080/02827580600559726
Blanco, J. A., Imbert, J. B., & Castillo, F. J. (2009). Thinning affects
nutrient resorption and nutrient-use efficiency in two Pinus sylvestris
stands in the Pyrenees. Journal of Applied Ecology, 19, 682-698.
doi:10.1890/1051-0761-19.3.682
Bloom, A. J., Chapin III, F. S., & Mooney, H. A. (1985). Resource
limitation in plants—An economic analogy. Annual Review of Ecol-
ogy, Evolution, and Systematics, 16, 363-392.
Boerner, R. E. J. (1984). Foliar nutrient dynamics and nutrient use effi-
ciency of four deciduous tree species in relation to site fertility.
Journal of Applied Ec ol o gy , 21, 1029-1040. doi:10.2307/2405065
Boerner, R. E. J. (1985). Foliar nutrient dynamics, growth, and nutrient
use efficiency of Hammamelis virginiana in three forest microsites.
Canadian Journal of Botany, 63, 1476-1481. doi:10.1139/b85-204
Bridgham, S. D., Pastor, J., McClaugherty, C. A., & Richardson, C. J.
(1995). Nutrient-use efficiency: A litterfall index, a model and test-
ing along a nutrient-availability gradient in North Carolina peatlands.
American Naturalist, 145, 1-21. doi:10.1086/285725
Bungart, R., & Hüttl, R. F. (2004). Growth dynamics and biomass ac-
cumulation of 8-year-old hybrid clones in a short-rotation plantation
on clayey-sandy mining substrate with respect to plant nutrition and
water budget. European Journ a l of Forest Research, 123, 105-115.
Cai, Z., & Bongers, F. (2007). Contrasting nitrogen and phosphorus
resorption efficiencies in trees and lianas from a tropical montane
rain forest in Xishuangbanna, south-west China. Journal of Tropical
Ecology, 23, 115-118. doi:10.1017/S0266467406003750
Calfapietra, C., DeAngelis, P., Gielen, B., Lukac, M., Moscatelli, M.,
Avino, G., Lagomarsion, A., Polle, A., Ceulemans, R., Mugnozza, G.,
Hoosbeek, M., & Cotrufo, M. (2007). Increased nitrogen-use effi-
ciency of a short-rotation poplar plantation in elevated CO2 concen-
tration. Tree Physiology, 27, 1153-1163.
doi:10.1093/treephys/27.8.1153
Campo, J., Solis, E., & Valencia, M. G. (2007). Litter N and P dynam-
ics in two secondary tropical dry forests after relaxation of nutrient
availability constraints.For. Forest Ecology and Management, 252,
33-40. doi:10.1016/j.foreco.2007.06.022
Chang, S. X. (2001). Seedling sweetgum (Liquidambar styraciflua L.)
half-sib family response to N and P fertilization: Growth, leaf area,
net photosynthesis and nutrient uptake. Forest Ecology and Man-
agement, 173, 281-291. doi:10.1016/S0378-1127(02)00007-5
Chapin, F. S., & Kedrowski, R. A. (1983). Seasonal changes in nitrogen
and phosphorus fractions and autumn retranslocation in evergreen
and deciduous taiga trees. Ec ology, 64, 376-391.
doi:10.2307/1937083
Chatain, A., Read, J., & Jaffre, T. (2009). Does leaf-level nutrient-use
efficiency explain Nothofagu-dominace of some tropical rain forests
in New Caledonai? Plant Ecology, 201, 51-66.
doi:10.1007/s11258-008-9477-z
Choi, W-J., Chang, S. X., Allen, H. L., Kelting, D. L., & Ro, H. (2005).
Irrigation and fertilization effects on foliar and soil carbon and nitro-
gen isotope ratios in a loblolly pine stand. Forest Ecology and Man-
agement, 213, 90-101. doi:10.1016/j.foreco.2005.03.016
Clark III, A., Jordan, L., Schimleck, L., & Daniels, R. F. (2008). Effect
of initial planting spacing on wood properties of unthinned loblolly
pine at age 21. Journal of Natur al Products, 58, 78-83.
Coleman, M. D., Friend, A. L., & Kern, C. C. (2004). Carbon allocation
and nitrogen acquisition in a developing populus deltoides plantation.
Tree Physiology, 24, 1347-1357. doi:10.1093/treephys/24.12.1347
Cochran, P. H., Newman, R. P., & Barrett, J. W. (1991). Fertilization
and spacing effects on growth of planted ponderosa pine. Portland,
OR: USDA Forest Service, Pacific Northwest Research Station.
Coyle, D. R., & Coleman, M. D. (2005). Forest production responses to
irrigation and fertilization are not explained by shifts in allocation.
Forest Ecology and Management, 208, 137-152.
doi:10.1016/j.foreco.2004.11.022
Curtis, R. O. (2008). True fir spacing trials: 10-year results. Portland,
OR: USDA Forest Service, Pacific Northwest Research Station.
del Arco, J. M., Escudero, A., & Garrido, M. V. (1991). Effects of site
characteristics on nitrogen retranslocation from senescing leaves.
Ecology, 72, 701-708. doi:10.2307/2937209
DesRochers, A., van den Driessche, R., & Thomas, B. R. (2006). NPK
fertilization at planting of three hybrid poplar clones in the boreal re-
gion of Alberta. Forest Ecology and Management, 232, 216-225.
doi:10.1016/j.foreco.2006.06.004
Dickman, D. I., Steinbeck, K., & Skinner, T. (1985). Leaf area and
biomass in mixed and pure plantations of P. occidentalis and black
locust in the Georgia piedmont. Forest Science, 31, 509-517.
Drenovsky, R. E., & Richards, J. H. (2006). Low leaf N and P resorp-
tion to nutrient limitation in two desert shrubs. Plant Ecology, 183,
305-314. doi:10.1007/s11258-005-9041-z
Eckstein, R. L., Karlsson, P. S., & Weih, M. (1999). Research review:
Leaf life span and nutrient resorption as determinants of plant nutri-
ent conservation in temperate-artic regions. New Phytologist, 143,
177-189. doi:10.1046/j.1469-8137.1999.00429.x
Ellsworth, D. S., & Reich, P. B. (1992). Leaf mass per area, nitrogen
content and photosynthetic carbon gain in Acer saccharum seedlings
in contrasting forest light environments. Functional Ecology, 6, 423-
435. doi:10.2307/2389280
Escudero, A., del Aroc, J. M., Sanz, I. C., & Ayala, J. (1992). Effects of
leaf longevity and retranslocation efficiency on the retention time of
nutrients in the leaf biomass of different woody species. Oecologia,
90, 80-87. doi:10.1007/BF00317812
Fang, S., Xu, X., Lu, S., & Tang, L. (1999). Growth dynamics and
biomass production in short-rotation poplar plantations: 6-year re-
sults for three clones at four spacings. Biomass and Bioenergy, 17,
415-425. doi:10.1016/S0961-9534(99)00060-4
Feller, I. C., Whigham, D. F., O’Neill, J. P., & McKee, K. L. (1999).
Effects of nutrient enrichment on within-stand cycling in a mangrove
forest. Ecology, 80, 2193-2205.
doi:10.1890/0012-9658(1999)080[2193:EONEOW]2.0.CO;2
Geyer, W. A., & Melichar, M. W. (1986). Short-rotation forestry re-
search in the United States. Biomass, 9, 125-133.
doi:10.1016/0144-4565(86)90116-2
Graciano, C., Goya, J. F., Frangi, J. L., & Guiamet, J. J. (2006). Fertili-
zation with phosphorus increases soil nitrogen absorption in your
plants of Eucalyptus grandis. Forest Ecology and Management, 236,
202-210. doi:10.1016/j.foreco.2006.09.005
Hagen-Thorn, A., Varnagiryte, I., Nihlgard, B., & Armolaitis, K.
(2006). Autumn nutrient resorption and losses in four deciduous for-
est tree species. Forest Ecology and Management, 228, 33-39.
Henderson, D. E., & Jose, S. (2005). Production physiology of three
fast-growing hardwood species along a soil resource gradient. Tree
Physiology, 25, 1487-1494. doi:10.1093/treephys/25.12.1487
Henderson, D. E. & Jose, S. (2010). Biomass production potential of
three short rotation woody crop species under varying nitrogen and

D. E. HENDERSON, S. JOSE
water availability. Agroforestry Systems, 80, 259-273.
doi:10.1007/s10457-010-9283-1
Jokela, E. J., Dougherty, P. M., & Martin, T. A. (2004). Production dy-
namics of intensively managed loblolly pine stands in the southern
United States: A synthesis of seven long-term experiments. Forest
Ecology and Management, 192, 117-130.
doi:10.1016/j.foreco.2004.01.007
Jokela, E. J., & Martin, T. A. (2000). Effects of ontogeny and soil nu-
trient supply on production, allocation, and leaf area efficiency in
loblolly and slash pine stands. Canadian Journal of Forest Research,
30, 1511-1524. doi:10.1139/x00-082
Jose, S., & Gillespie, A. R. (1996). Aboveground production efficiency
and canopy nutrient contents of mixed-hardwood forest communities
along a moisture gradient in the central United States. Canadian
Journal of Forest Research, 26, 2214-2223.
Jose, S., & Gillespie, A. R. (1997). Leaf area-productivity relationships
among mixed-species hardwood forest communities of the central
hardwood region. Forest Sc ie nc e , 43, 56-64. doi:10.1139/x26-250
Killingbeck, K. (1984). Nitrogen and phosphorus resorption dynamics
of five tree species in a Kansas gallery forest. American Midland
Naturalist Journal, 111, 155-164. doi:10.2307/2425554
Killingbeck, K. (1986). Litterfall dynamics and element use efficiency
in a Kansas gallery forest. American Midland Naturalist Journal, 116,
180-189. doi:10.2307/2425950
Killingbeck, K. (1993). Inefficient nitrogen resorption in genets of the
actinorhizal nitrogen fixing shrub Comptoniaperegrina: Physiological
ineptitude or evolutionary tradeoff? Oecolgia, 94, 542-549.
doi:10.1007/BF00566970
Killingbeck, K. (1996). Nutrients in senesced leaves: Keys to the search
for potential resorption and resorption proficiency. Ecology, 77,
1716-1727. doi:10.2307/2265777
King, J. S., Albaugh, T. J., Allen, H. L., & Kress, H. L. (1999). Stand-
level allometry in Pinus taeda as affected by irrigation and fertiliza-
tion. Tree Physiology, 19, 769-778. doi:10.1093/treephys/19.12.769
Knecht, M. F., & Goransson, A. (2004). Terrestrial plants require nu-
trients in similar proportions. Tree Physiology, 24, 447-460.
doi:10.1093/treephys/24.4.447
Koerselman, A., & Meuleman, A. F. (1996). The vegetation ratio: A
new tool to detect the nature of nutrient limitation. Journal of Ap-
plied Ecology, 33, 1441-1450. doi:10.2307/2404783
Kozovits, A. R., Bustamante, M. M., Garofalo, C. R., Buccis, S.,
Franco, A. C., Goldstein, G., & Meinzer, F. C. (2007). Nutrient re-
sorption and patterns of litter production and decomposition in a
neotropical savanna. Functional Ecology, 21, 1034-1043.
doi:10.1111/j.1365-2435.2007.01325.x
Ladanai, S., Agren, G. I., Hyconen, R., & Lundkvist, H. (2006). Nitro-
gen budgets for scots pine and Norway spruce ecosystems 12 and 7
years after the end of long-term fertilization. Forest Ecology and
Management, 2338, 130-140.
Lambers, H., Chapin III, F. S., & Pons, T. L. (1998). Plant physiologi-
cal ecology. New York, NY: Springer-Verlag New York Inc.
Lathja, K. (1987). Nutrient resorption efficiency and the response to
phosphorus fertilization in the desert shrub Larreatridentata (DC.)
Cov. Biogeochemistry, 4, 265-276. doi:10.1007/BF02187370
Lee, K. H., & Jose, S. (2003). Soil respiration, fine root production, and
microbial biomass in P. deltoides and loblolly pine plantations along
a nitrogen fertilization gradient. Forest Ecology and Management,
185, 263-273. doi:10.1016/S0378-1127(03)00164-6
Lee, K. H., & Jose, S. (2005). Nitrate leaching in P. deltoides and lob-
lolly pine biomass plantations along a nitrogen fertilization gradient.
Agriculture, Ecosystems & Environment, 105, 615-623.
doi:10.1016/j.agee.2004.08.004
Lee, K. H., & Jose, S. (2006). Nitrogen mineralization in short-rotation
tree plantations along a soil nitrogen gradient. Canadian Journal of
Forest Research, 36, 1236-1242. doi:10.1139/x06-019
Lockaby, B. G., Clawson, R. G., & Baker, T. (1997). Response of three
hardwood species to irrigation and fertilization on an upland site.
South. Journal of Applied Physics, 21, 123-129.
Lockaby, B. G., & Conner, W. H. (1999). N:P balance in wetland for-
ests: Productivity across a biogeochemical continuum. Botanical Re-
view, 65, 171-185. doi:10.1007/BF02857626
Lockhart, B. R., Ezell, A. W., Hodges, J. D., & Clatterbuck, W. K.
(2006). Using natural stand development patterns in artificial mix-
tures: A case study with cherrybark oak and sweetgum in east-central
Mississippi, USA. Forest Ecology and Management, 222, 202-210.
doi:10.1016/j.foreco.2005.09.029
Lugo, A. E., Abelleira, O. J., Collado, A., Viera, C. A., Veles, D. O.,
Soto, S., Amaro, G., Charon, G., Colon Jr., H., Santans, J., Morales, J.
L., Rivera, K., Ortiz, L., Rivera, L., Maldonado, M., Rivera, N., &
Vazquez, J. J. (2011). Allometry, biomass, and chemical content of
novel African tulip tree (Spathodea campanulata) forests in Puerto
Rico. New Forests, 42, 267-283. doi:10.1007/s11056-011-9258-8
May, J. D., Burdette, S. B., Gilliam, F. S., & Adams, M. B. (2005).
Interspecific divergence in foliar nutrient dynamics and stem growth
in a temperate forest in response to chronic nitrogen inputs. Cana-
dian Journal of Forest Research, 35, 1023-1030.
doi:10.1139/x05-036
Millner, J. P., & Kemp P. D. (2012). Foliar nutrient in Eucalyptus
species in New Zealand. New Forests, 43, 255-266.
doi:10.1007/s11056-011-9279-3
Moscatelli, M. C., Lagomarsino, A., De Angelis, P., & Grego, S. (2008).
Short- and medium-term contrasting effects of nitrogen fertilization
on C and N cycling in a poplar planation soil. Forest Ecology and
Management, 255, 447-454. doi:10.1016/j.foreco.2007.09.012
Nambiar, E. K., & Fife, D. N. (1991). Nutrient translocation in tem-
perate conifers. Tree Physiolog y, 9, 185-207.
National Oceanic and Atmospheric Administration (2003). URL (last
checked 19 June 2003).
http://www7.ncdc.noaa.gov/IPS/cd/cd.html?_page=0&jsessionid=A5
0481FDDB5BC9A82BAC9B6604E51C59&state=FL&_target1=Nex
t
Pastor, J., & Bridgham, S. D. (1999). Nutrient efficiency along nutrient
availability gradients. Acta Oecologica, 118, 50-58.
doi:10.1007/s004420050702
Prietzel, J., Wagoner, G. L., & Harrison, R. B. (2004). Long-term ef-
fects of repeated urea fertilization in Douglas-fir stands on forest
floor nitrogen pools and nitrogen mineralization. Forest Ecology and
Management, 193, 413-426. doi:10.1016/j.foreco.2004.02.006
Pugnaire, F. I., & Chapin III, F. S. (1993). Controls over nutrient re-
sorption from leaves of evergreen Mediterranean species. Ecology,
74, 124-129. doi:10.2307/1939507
Rowe, D. B., Blazich, F. A., & Raper, C. D. (2002). Nitrogen nutrition
of hedged stock plants of loblolly Pine. I. tissue nitrogen concentra-
tions and carbohydrate status. New Forests, 24, 53-65.
doi:10.1023/A:1020555013964
Saarsalmi, A., Kukkola, M., Moilanen, M., & Arola, M. (2006). Long-
term effects of ash and N fertilization on stand growth, tree nutrient
status and soil chemistry in a Scots pine stand. Forest Ecology and
Management, 235, 116-128. doi:10.1016/j.foreco.2006.08.004
Safou-Matondo, R., Deleporte, P., Laclau, J. P., & Bouillet, J. P. (2005).
Hybrid and clonal variability of nutrient content and nutrient use ef-
ficiency in Eucalyptus stand in Congo. Forest Ecology and Man-
agement, 210, 193-204.
Samuelson, L. J., Johnsen, K., & Stokes, T. (2004a). Production, allo-
cation, and stemwood growth efficiency of Pinus taeda L. in re-
sponse to 6 years of intensive management. Forest Ecology and
Management, 192, 59-70. doi:10.1016/j.foreco.2004.01.005
Samuelson, L. J., Johnsen, K., Stokes, T., & Weinlang, L. (2004b.) In-
tensive management modifies soil CO2 efflux in a 6-year-old Pinus
taeda L. stands. Forest Ecology and Management, 200, 335-345.
doi:10.1016/j.foreco.2004.07.002
Samuelson, L., Stokes, T., Cooksey, T., & McLemore III, P. (2001).
Production efficiency of loblolly pine and sweetgum in response to
four years of intensive management. Tree Physiology, 21, 369-376.
doi:10.1093/treephys/21.6.369
SAS Institute (2001). SAS user guide: Statistics. Cary, NC: SAS Insti-
tute Inc.
Schilling, E. B., & Lockaby, B. G.(2006). Relationships between pro-
ductivity and nutrient circulation with two contrasting southeastern
US floodplain forests. Wetlands, 26 , 181-192.
198

D. E. HENDERSON, S. JOSE
doi:10.1672/0277-5212(2006)26[181:RBPANC]2.0.CO;2
Schlaegel, B. E., & Kennedy, H. E. (1986). Deriving biomass estima-
tions for seven plantation hardwood species. In D. L. Rockwood
(Ed.), Proceedings of the 1985 southern forest biomass workshop (pp.
31-39). Gainesville, 11-14 June 1985.
Schubert, M. R., Rennie, J. C., & Schlarbaum, S. E. (2004). Four pine
species grown at four spacings on the eastern highland rim, Tennes-
see, after 30 years. Asheville, NC: USDA Forest Service, Southern
Research Station.
Shelton. M. G., Switzer, G. L., Nelson, L. E., Baker, J. B., & Mueller,
C. W. (1982). The development of P. deltoides plantations on allu-
vial soils. Technical Bulletin, 1 13 , 47.
Singh, B. (1998). Biomass production and nutrient dynamics in three
clones of Populus deltoides planted on Indogangetic plains. Plant
and Soil, 203, 15-26. doi:10.1023/A:1004388903402
Smith, K., Gholz, H. L., & de Assis Oliveira, F. (1998). Litterfall and
nitrogen-use efficiency of plantations and primary forest in the east-
ern Brazilian Amazon. Forest Ecology and Management, 109, 209-
220. doi:10.1016/S0378-1127(98)00247-3
Song, C. J., Ma, K. M., Qu, L. Y., Liu, Y., Xu, X. L., Fu, B. J., &
Zhong, J. F. (2010). Interactive effects of water, nitrogen and phos-
phorus on the growth, biomass partitioning and water-use efficiency
of Bauhinia faberi seedlings. Journal of Arid Environments, 74,
1003-1012.
Specht, A., & Turner, J. (2006). Foliar nutrient concentrations in
mixed-species plantations of subtropical cabinet timber species and
their potential as a management tool. Forest Ecology and Manage-
ment, 233, 324-337. doi:10.1016/j.foreco.2006.05.029
Stape, J. L., Binkley, D. R., & Ryan, M. G. (2008). Production and
carbon allocation in a clonal Eucalyptus plantation with water and
nutrient manipulations. Forest Ecology and Management, 255, 920-
930. doi:10.1016/j.foreco.2007.09.085
Sword Sayer, M. A., Goelz, J. C. G., Chambers, J. L., Tang, Z., Dean, T.
J., Haywood, J. D., & Leduc, D. J. (2004). Long-term trends in lob-
lolly pine productivity and stand characteristics in response to thin-
ning and fertilization in the West Gulf region. Forest Ecology and
Management, 192, 71-96. doi:10.1016/j.foreco.2004.01.006
Tateno, R., & Kawaguchi, H. (2002). Differences in nitrogen use effi-
ciency between leaves from canopy and subcanopy trees. Ecological
Research, 17, 695-704. doi:10.1046/j.1440-1703.2002.00526.x
Tuskan, G. A. (1998). Short-rotation woody crop supply systems in the
Unites States: What do we know and what do we need to know?
Biomass and Bioenergy, 14, 307-315.
doi:10.1016/S0961-9534(97)10065-4
USDA, NRCS (2009). The PLANTS database. URL (2 December 2012).
http://plants.usda.gov
Van Den Driessche, R. (2000). Phsophorus, copper, and zinc supply
levels influence growth and nutrition of a young Populustrichocarpa
(Tott & Gray) × P. deltoides (Bartr. Ex Marsh) hybrid. New Forests,
19, 143-157. doi:10.1023/A:1006607410673
Vitousek, P. M. (1982). Nutrient cycling and nutrient use efficiency.
American Naturalist, 119, 553-572. doi:10.1086/283931
Vitousek, P. M. (1998). Foliar and nutrients, nutrient resorption, and
decomposition In Hawaiian Metrosideros Polymorpha. Ecosystems, 1,
401-407. doi:10.1007/s100219900033
Vogel, J. G., & Gower, S. T. (1998). Carbon and nitrogen dynamics of
boreal jack pine stands with and without green alder understory.
Ecosystems, 1, 386-400. doi:10.1007/s100219900032
Vogt, K. A., Grier, C. C., & Vogt, D. J. (1986). Production, turnover,
and nutrient dynamics of above- and belowground detritus of the
world forest. Advances in Ecological Research, 15, 303-377.
doi:10.1016/S0065-2504(08)60122-1
Wang, J. P., Jarvis, P. G., & Taylor, C. M. (1991). Par absorption and
its relation to above-ground dry matter production of Sitka Spruce.
Journal of Applied Ec ol o gy , 28, 547-560.
Wang, J. R., Letchford, T., Comeau, P., & Kimmins, J. P. (2000).
Above- and below-ground biomass and nutrient distribution of a pa-
per birch and subalpine fir mixed species stand in the Sub-Boreal
Spruce zone of British Columbia. Forest Ecology and Management,
130, 17-26. doi:10.2307/2404567
Wang, J. R., Zhong, A. L., Comeau, T. M., & Kimmins, J. P. (1995).
Aboveground biomass and nutrient accumulation in an age sequence
of aspen (Populustremuloides) stands in the boreal white and black
spruce zone, British Columbia. Forest Ecology and Management, 78,
127-138. doi:10.1016/0378-1127(95)03590-0
Wang, J. R., Zhong, A. L., Simard, S. W., & Kimmins, J. P. (1996).
Aboveground biomass and nutrient accumulation in an age sequence
of paper birch (Betula papyrifera) in the interior cedar hemlock zone,
British Columbia. Forest Ecol ogy a nd M an ag eme nt , 83, 27-38.
doi:10.1016/0378-1127(96)03703-6
Wienand, K. T., & Stock, W. D. (1995). Long-term phosphorus fertili-
zation effects on the litter dynamics of an age sequence of Pinus elli-
ottii plantations in Southern Cape of South Africa. Forest Ecology
and Management, 75, 135-146.
doi:10.1016/0378-1127(95)03528-I
Will, R. E., Munger, G. T., Zhang, Y., & Borders, B. E. (2002). Effects
of annual fertilization and complete competition control on current
annual increment, foliar development, and growth efficiency of
Pinus taeda stands. Canadian Journal of Forest Research, 32, 1728-
1740. doi:10.1139/x02-095
Wilson, A. R., Nzokou, P., Gűney, D., & Kulaç, Ş. (2012). Growth
response and nitrogen use physiology of Fraser fir (Abies fraseri),
red pine (Pinus resinosa) and hybrid poplar under amino acid nutri-
tion. New Forests, 1-15. doi:10.1007/s11056-012-9317-9
Wright, I. J., & Westoby, M. (2001). Understanding seedling growth
relationships through specific leaf areas and life nitrogen concentra-
tion: Generalizations across growth forms and growth irradiance.
Oecologia, 127, 21-29. doi:10.1007/s004420000554
Wright, I. J., & Westoby, M. (2003). Nutrient concentration, resorption
and lifespan: Leaf traits of Australian sclerophyll species. Functional
Ecology, 17, 10-19. doi:10.1046/j.1365-2435.2003.00694.x
Xu, X., & Timmer, V. R. (1999). Growth and nutrition of Chinese fir
seedlings exposed to nutrient loading and fertilization. Plant and Soil,
216, 83-91. doi:10.1023/A:1004733714217
Yan, E.-R., Wang, X., & Huang, J. (2006). Shifts in plant nutrient use
strategies under secondary forest succession. Plant and Soil, 289,
187-197. doi:10.1007/s11104-006-9128-x
Yuan, Z. Y., & Chen, H. Y. H. (2010). Changes in nitrogen resorption
of trembling aspen (Populus tremuloides) with stand development.
Plant and Soil, 327, 121.
Yuan, Z. Y., & Li, L. H. (2007). Soils water status influences plant
nitrogen use: A case study. Plant and Soil, 301, 303-313.
doi:10.1007/s11104-007-9450-y
Zalesny, J. A., Zalesny Jr., R.S., Coyle, D. R., & Hall, R. B. (2007).
Growth and biomass of populus irrigated with landfill leachate. For-
est Ecology and Management, 248, 143-152.
doi:10.1016/j.foreco.2007.04.045
Zalesny, J. A., Zalesny Jr., R. S., Wiese, A. H., Sexton, B. T., & Hall, R.
B. (2008). Uptake of macro- and micro-nutrients into leaf, woody,
and root tissue of Populus after irrigation with landfill leachate.
Journal of Sustainable Forestry, 27, 303-327.
doi:10.1080/10549810802256262