Directory UMM :Data Elmu:jurnal:T:Tree Physiology:Vol16.1996:

Tree Physiology 16, 949--956
© 1996 Heron Publishing----Victoria, Canada

Assessment of nitrogen, phosphorus, and potassium uptake capacity
and root growth in mature alternate-bearing pistachio (Pistacia vera)
trees
R. C. ROSECRANCE, S. A. WEINBAUM and P. H. BROWN
Pomology Department, University of California Davis, Davis, CA 95616, USA

Received November 1, 1995

Summary We examined interrelationships between crop
load, nitrogen (N), phosphorus (P), and potassium (K) uptake,
and root growth in mature, alternate-bearing pistachio (Pistacia vera L.) trees. Pistachio trees bear heavy (on-year) and
light (off-year) fruit crops in alternate years. Uptake and partitioning of N, P, and K among tree parts were determined during
(a) spring flush (mid-March to late May), (b) nut fill (late May
to early September), and (c) postharvest--leaf senescence (late
September to early December). Nutrient uptake occurred primarily during nut fill in both on-year and off-year trees. In
on-year trees, N and K uptake increased by 35 and 112%,
respectively, during nut fill compared with off-year trees. During this period, nutrients were allocated largely to embryo
development in on-year trees and to storage in perennial tissues

in off-year trees. Nutrient uptake was negligible between harvest and leaf senescence. Although root growth was reduced
during nut fill in on-year trees compared with off-year trees,
there was no relationship between root growth and the uptake
of N, P or K from the soil. Our data support the hypothesis that
sink demand regulates the uptake and distribution of N, P, and
K in pistachio trees.
Keywords: crop yield, nutrient use efficiency, sink demand.

Introduction
Knowledge of seasonal patterns of N, P, and K uptake in
mature trees is an important component of fertilizer management and can be used to increase nutrient use efficiency (i.e.,
nutrient recovered/nutrient applied) by matching fertilizer applications with periods of high nutrient uptake capacity. Little
is known, however, about the seasonal patterns of nutrient
uptake in mature trees. In pistachio (Pistacia vera L.), nutrient
uptake is influenced by: (1) nutrient storage in perennial tree
parts over winter (Rosecrance 1996); and (2) differential crop
load (Weinbaum et al. 1994b, Brown et al. 1995). Pistacia vera
trees are pronounced alternate bearers (Crane and Iwakiri
1981), producing yields that are 3 to 5 times larger in heavyfruiting on-years than in light-fruiting off-years (Johnson and
Weinbaum 1987).

Studies with trees grown in pots or sand culture have been
conducted to determine the periodicity of N uptake capacity in
citrus (Legaz et al. 1982, Dasberg et al. 1983), peaches (Stassen et al. 1981, Munoz et al. 1993), apples (Hansen 1971b,
1973, Millard and Neilsen 1989), and grapes (Conradie 1992).
High N uptake rates during fruiting were observed in some
studies (Legaz et al. 1982, Conradie 1992, Munoz et al. 1993),
but not in others (Hansen 1971b, 1973). The restricted rooting
volumes, light fruit loads, and small N reserves, which are
characteristics of potted and sand-grown trees but not of mature, field-grown trees, may account for the discrepancies.
Furthermore, it is unlikely that nutrient uptake by mature trees
can be extrapolated from studies performed using young, nonbearing or potted trees because total nutrient uptake (Smith et
al. 1988) and storage reserves (Miller 1995) change as trees
mature. Thus, there is a need for field studies with mature trees.
Fruiting is reported to depress root growth in apple (Maggs
1963, Head 1969, Hansen and Grauslund 1978, Heim et al.
1979), peach (Chalmers and van den Ende 1975, Williamson
and Coston 1989, Nii 1993), and citrus (Smith 1976, Golomb
and Goldschmidt 1987). Little is known, however, about the
relationship between root growth and nutrient uptake in mature

trees.
Alternate bearing strongly influences tree demand for nitrogen and phosphorus, as indicated by the severely reduced
nutrient content in perennial tissues of mature fruit trees following heavy fruiting (Golomb and Goldschmidt 1987, Weinbaum et al. 1994b, Brown et al. 1995). However, it is not
known how alternate bearing influences N, P, and K uptake or
how uptake capacity varies seasonally in alternate-bearing
trees. We hypothesized that N, P, and K demand (primarily
determined by fruit growth) regulates N, P, and K uptake in
pistachio. The objectives of this study were: (1) to determine
seasonal patterns of N, P, and K uptake by measuring wholetree N, P, and K accumulation and isotopically labeled fertilizer N uptake over the alternate-bearing cycle; and (2) to relate
the seasonal patterns of root growth in heavy-fruiting (on-year)
and light-fruiting (off-year) pistachio trees with seasonal patterns of N, P, and K uptake. We also assessed the role of sink
demand and root growth on the patterns of N, P, and K uptake
in pistachio.

950

ROSECRANCE, WEINBAUM AND BROWN

Materials and methods
Plant material and experimental manipulation

Forty-two 20-year-old Kerman pistachio trees on Pistacia atlantica Desf. rootstock were selected in 1992, an on-year. In
May 1992, 21 of the trees were defruited to transform them to
off-year trees. Thus, environmental effects were standardized
by comparing on-year and off-year trees in the same year. Tree
yields were measured in 1992 and 1993. Of the 42 trees, 18
(nine off- and nine on-year trees) were selected for 15N application and subsequent tree excavation and 12 (six off- and six
on-year trees) were selected for root growth measurements
based on similar fruit yields and trunk cross-sectional areas.
Trees were spaced 3 m apart within rows and 10 m between
rows with a population of 212 female trees ha −1. The trial was
located in a commercial orchard (S & J Ranch, Madera, CA).
The Ramona series soils at the site were coarse textured and
well drained, with a pH of 6.0. Trees were kept well watered
with a micro-sprinkler irrigation system.
Root growth measurements
Root growth was determined in root observation boxes (rhizotrons). Six rhizotrons were installed in February 1994. Each
rhizotron was located between an on-year and an off-year tree,
about 1 m from each tree trunk. Each rhizotron had two glass
windows, one facing an on-year tree and the other facing an
off-year tree. The windows were 61 cm wide and 92 cm high

and installed in wood boxes that were 1.0 m long by 0.75 m
wide and 1.5 m deep. Rhizotron covers were constructed from
10.5-cm thick Reflectix (Rockland, CA) insulating material.
Some back filling of soil was necessary to ensure good contact
between the soil and the windows. The area around the rhizotrons was kept weed free to ensure that all roots at the
rhizotron faces were pistachio roots.
Roots of 12 trees (six fruiting and six nonfruiting) were
measured every two weeks between fruit set and leaf senescence (April 15 to November 15, 1994). Visible roots were
traced onto clear acetate sheets; the tracings were digitized and
the lengths computed. Cumulative root growth was determined
by the difference in root lengths from one measurement period
to the next. Root growth rate was calculated from the cumulative root growth data divided by the number of intervening
days (usually 14 days). Both cumulative root growth and root
growth rate data are expressed per square centimeter of window. The number of newly initiated, white roots growing
against the rhizotron windows was also counted.
Determination of nitrogen uptake
Tree phenology and recovery of 15N fertilizer Isotopically labeled N fertilizer ((15NH4)2SO4, 0.01 atom% 15N) was applied
to both on- and off- year pistachio trees during three periods in
1994: (1) spring flush and pericarp development, March 17 to
May 24, 1994; (2) nut fill, July 8 to September 8; and (3)

postharvest--leaf senescence, September 25 to December 13,
1994. At the end of the spring flush (mid-May), the fruit
pericarp had attained full size, and shoot extension growth and
leaf area development were completed (Crane and Iwakiri

1981). Following spring flush, embryo development occurred
between mid-June and September. Nutrient resorption and leaf
senescence occurred between harvest (mid-September) and
leaf abscission (mid-November).
Three on-year and three off-year trees were fertilized with
15
N fertilizer (applied as a 40% (w/v) (15NH4)2SO4 solution) at
the start of each of the three study periods (March 17, July 8
and September 25 and 29, 1994). Two circular holes, approximately 25 cm deep and 1 m in diameter, were dug 1 m away
from either side of the trees. Isotopic N was applied to the holes
at a rate of 970 g N per tree. After application, the holes were
refilled with soil to minimize ammonia volatilization, and the
trees were immediately irrigated. In commercial orchards,
pistachio trees are typically fertilized with 1.0 to 1.5 kg N per
tree per year (200 to 300 kg N ha −1 year −1) (L. Ferguson,

personal communication).
Application of ammonium sulfate fertilizer on July 8 (nut
fill) resulted in severe leaf burn and so these trees were excluded from the study. Four nonlabeled trees (two on-year and
two off-year) were selected several days later and excavated in
September. Nitrogen uptake by these nonlabeled trees was
calculated by the difference method (see below). During postharvest--leaf senescence, the application of 15N was split; half
the fertilizer was applied on September 25 and the other half
was applied on September 29. No leaf burn was observed
during this period.
Trees were excavated with a backhoe two months after
isotope application (May 24, September 8 and December 13,
1994) and each tree was separated into eight fractions: (1) fine
roots < 1 cm diameter; (2) roots > 1 cm diameter; (3) rootstock;
(4) trunk; (5) canopy branches; (6) current-year wood; (7)
leaves; and (8) fruit (cropping trees only). The various tree
fractions were weighed and perennial tree parts were mechanically chipped. Subsamples were weighed fresh, dried to a
constant weight at 60 °C, reweighed, ground in a Wiley mill to
pass a 30-mesh screen, and analyzed for nutrient content.
Because of the small amounts of N, P, and K in the fine roots
and rootstock fractions, the three root fractions were combined.

Total N concentration was determined in subsamples by
macro-Kjeldhal following the procedures of Weinbaum and
Neumann (1977). Potassium in subsamples was extracted with
acetic acid and measured by flame emission with a Varian
Techtron AA 120 atomic absorption spectrometer (Sunnyvale,
CA). To determine phosphorus concentrations, 1-g subsamples
were ashed overnight (560 °C), extracted with 1 N HN03 and
measured by plasma emission spectrometry (Model 3510, Applied Research Laboratories, Sunland, CA). Duplicate samples
were run for each tree fraction.
Analysis of 15N was performed by Isotope Services, Los
Alamos, NM. Samples were oxidized to N2 gas before isotopic
composition was determined by mass spectrometry. The results are expressed as percentage of 15N derived from fertilizer
based on standard conversions (Cabrera and Kissel 1989,
Hauck and Bremner 1976). The percent 15N derived from
fertilizer in each tree part was then multiplied by its N content

N, P, AND K UPTAKE AND ROOT GROWTH IN PISTACHIO TREES

to determine the amount of 15N recovered. Total N was determined by macro-Kjeldahl as decribed above.
The difference method: sequential excavations and N, P, and

K analyses of mature trees Tree N, P, and K accumulation
during the spring flush, nut fill, and postharvest--leaf senescence periods were determined by difference following sequential tree excavations and N, P, and K analyses. Trees were
paired according to their crop yields determined in 1992 and
1993 to reduce variance due to differences in tree size. In
addition, there was a significant linear relationship between
trunk cross-sectional area (TCA) and tree biomass (r 2 = 0.56).
Thus, TCA was used to normalize trees of varying sizes, following procedures similar to Kappel (1991). Leaf dry weight, for
example, was normalized using the following formula:
Leaf adj = Leaf i × TCAavg / TCA i ,

where Leafi and TCAi denote the measured tree part. Other
variables were adjusted similarly. After correcting for tree size,
no significant differences were found in total tree weight
between on- and off-year trees in May or September; however,
in December, off-year trees were 8% heavier than on-year
trees.

951

off-year trees (Table 1). Total root length (cm cm −2 of rhizotron

window) was 30% greater in on-year trees than in off-year
trees in mid-April (Figure 1a). By June, shortly before the
initiation of nut fill, a transition occurred and root length, root
growth rate, and the number of white roots declined in on-year
trees compared with off-year trees (Figures 1a and 1b and
Table 1). Root growth rates of off-year trees were nearly twice
those of on-year trees during the end of the spring flush and

Table 1. Effects of alternate bearing and season on the number of white
roots growing against the rhizotron windows (no. per cm 2) during the
annual cycle.1
Cropping
status

Spring flush
April 22

Nut fill
June 16

Nut maturity
August 30

Postharvest
October 13

On-year
Off-year

38.1 a2
11.5 b

15.4 a
52.2 b

26.7 a
6.8 b

14.1
14.2

1
2

Each value is the mean of six replicates on a day representative of
that growth period.
Within a column, values followed by different letters are significantly different at P < 0.05, according to the F test.

Determination of nutrient removal in leaf litter
Annual N, P, and K removal in abscised leaves of both on- and
off-year trees was calculated as the product of average leaf N,
P, and K concentrations of eight sampled branches and the
estimated leaf biomass per tree at the time of leaf abscission.
Estimated total leaf dry weight at abscission was based on total
leaf weight on September 8, because all the leaves had fallen
from the trees by December. The estimate was calculated from
the product of total tree leaf dry weight on September 8 and the
fraction of leaf dry weight retained after nutrient resorption in
the fall. This fraction was determined by sampling 15 leaflets
from eight shoots per tree from three on- and three off-year
trees on September 8 and December 13 (mesh bags were used
to catch senescing leaflets in December) and calculating the
average dry weight per leaflet from both sampling periods.
Abscised leaves were analyzed for N, P, and K, and these
concentrations were multiplied by their respective total tree
dry weights.
Statistical analysis
The experiment was set up as a completely randomized design
and one-way analyses of variance were performed by
SAS/GLM procedures (SAS Institute 1988, Cary, NC).
Results
Root growth dynamics over the alternate bearing cycle
Root growth varied seasonally and was influenced by alternate
bearing. On-year trees initiated root growth one week earlier
than off-year trees (data not shown) and, by the third week
following anthesis (April 22), on-year trees had three times
more white roots growing against the rhizotron windows than

Figure 1. Relationship between cumulative root length (A) and root
growth rate (B) versus time in mature on- and off-year pistachio trees.
Each value is the mean ± SE of six tree replicates. In some cases, the
SE is not visible. An asterisk indicates a significant difference at
P < 0.05 according to the F test.

952

ROSECRANCE, WEINBAUM AND BROWN

On-year trees took up more than twice as much 15N than
off-year trees during the spring flush period (March 17--May
24; Figure 2a). Substantially greater amounts of 15N accumulated in the fruit and roots of on-year trees compared with
off-year trees. Moreover, leaves from on-year trees contained
70% more 15N than leaves from off-year trees, even though
off-year trees had 13% greater leaf area and 11% greater leaf
N content (Rosecrance 1996). Fruits and leaves of on-year
trees accounted for 67% of the 15N taken up by the tree
compared with 38% for fruits and leaves of off-year trees.
Although the proportion of 15N found in fruits was high, the
actual amount of label only represented 5.5% of the total N in
the fruit (26 g out of a total of 469 g per tree; see Figure 2a and
Table 2). Overall recoveries of 15N for off- and on-year trees
were 3 and 9%, respectively (data not shown). These relatively
low N recovery rates likely reflect: (1) dilution of 15N caused
by non-labeled N uptake from the soil (see below); and (2) the
short labeling periods used.
Total N uptake between December 13 and May 24 (estimated from the difference in total tree N contents) was three to
10 times greater than 15N uptake (cf. Figure 2a and Table 3).

most of the nut fill periods. Toward the end of the nut fill period
as seed reached maturity, root growth rates in both on- and
off-year trees decreased (Figure 1b), increased again after
harvest and then declined in November. Root growth rates after
harvest in September tended to be greater (P < 0.10) in on-year
trees than in off-year trees.
Effect of alternate bearing on tree nutrient contents at the
end of the spring flush, nut fill, and postharvest--leaf
senescence periods
Spring flush No significant differences in tree N, P, and K
contents (the product of dry weight and nutrient concentration)
were found between on- and off-year trees during the spring
flush period (Table 2). The distribution of N, P, and K within
the trees, however, varied dramatically. Fruits of on-year trees,
for example, comprised approximately 30% of the total tree N,
P, and K contents, respectively, whereas fruit in off-year trees
represented only 1--2%. In contrast, canopy branches contained a much greater proportion of the total tree nutrient
content in off-year trees than in on-year trees (Table 2).

Table 2. Effect of tree cropping status on distribution of N, P, and K and total tree N, P, and K contents in mature ‘‘Kerman’’ pistachio trees.1 Months
indicate harvest dates.
Cropping

May (spring flush)

status

N

P

September (nut fill)
K

N

P

December (postharvest)
K

N

P

K

Leaves (% of total)
On-year
Off-year

20.7
28.3

16.1
21.6

11.7 a2
20.3 b

12.0 a
22.8 b

6.9 a
14.1 b

11.7 a
29.6 b

---

---

---

Fruit (% of total)
On-year
Off-year

28.6 a
1.4 b

32.1 a
2.1 b

31.1 a
2.3 b

45.7 a
3.3 b

52.8 a
5.3 b

43.5 a
4.6 b

---

---

---

1.2
1.7

1.3
2.4

1.1 a
2.1 b

1.1
2.1

1.1 a
2.7 b

0.8
1.5

3.1
3.5

3.4
4.1

1.4
2.2

24.7 a
37.8 b

26.5 a
41.3 b

24.4 a
34.1 b

21.2 a
47.7 b

18.7 a
55.5 b

19.6 a
31.7 b

51.7
56.2

49.9
56.1

41.9
43.5

Trunk (% of total)
On-year
Off-year

2.4
3.7

3.1
4.4

5.7
6.6

1.9 a
3.3 b

3.1
3.7

3.6 a
6.2 b

5.4
5.6

5.6
4.9

7.4
9.1

Roots (% of total)
On-year
Off-year

22.5
27.1

20.7
27.9

26.2
34.8

49.3
45.2

1637.9
1335.1

148.9
116.3

1003.2
1076.5

Current-year wood (% of total)
On-year
Off-year
Canopy branches (% of total)
On-year
Off-year

Tree total (g per tree)
On-year
Off-year
1
2

18.1
20.9

18.2
18.6

20.7
26.5

39.8
34.7

41.2
35.0

2180.9 a
1738.0 b

203.3 a
162.7 b

2017.6 a
1555.8 b

1017.8 a
1395.3 b

89.9 a
145.9 b

1073.6
1022.4

Each value is the mean of three tree replicates, except from September 10 harvest where only two tree replicates were used.
For each tree part on the same sampling date, pairs of on-year and off-year values followed by different letters are significantly different at
P ≤ 0.05 according to the F test.

N, P, AND K UPTAKE AND ROOT GROWTH IN PISTACHIO TREES

953

Postharvest--leaf senescence Little or no nutrient uptake occurred during the postharvest--leaf senescence period (Table 3).
Nutrients did accumulate in perennial tissues during this period; however, leaf nutrient resorption rather than uptake from
the soil could account for this accumulation (Rosecrance
1996). Uptake of 15N was also low during this period and there
were no differences between on- and off-year trees (Figure 2b).
On-year trees took up 40% less 15N during the postharvest--leaf
senescence period than during spring flush (Figures 2a and 2b).
On- and off-year trees recovered 4 to 5% of the 15N applied,
and of the 15N recovered, > 50% of it remained in the roots in
both on- and off-year trees.
Effects of alternate bearing on nutrient distribution, uptake,
and removal

Figure 2. Recovery of 15N during the spring flush, pericarp enlargement period (March 17 to May 24) (A), and during the postharvest-leaf senescence period (September 25 and 29 to December 13) (B).
Each value is the mean ± SE of three tree replicates. An asterisk
indicates a significant difference at P < 0.05 according to the F test.

Moreover, there was a trend for off-year trees to take up more
N than on-year trees (P < 0.10) during the spring flush period
(Table 3), which is the reverse of the trend noted for uptake of
15
N. However, total N uptake and 15N uptake are not directly
comparable, because the time periods of N uptake differed (see
Discussion).
Nut fill On-year trees took up 35% more N (P < 0.10), 112%
more K, and similar amounts of P than off-year trees during the
nut fill period (Table 3), resulting in 25 to 30% greater wholetree N, P, and K contents in on-year trees than in off-year trees
(Table 2). In on-year trees, nutrients accumulated mainly in the
fruit: N, P, and K contents of fruit increased 53, 55, and 65%,
respectively, between the end of spring flush and nut maturity
(calculated from Table 2). In off-year trees, canopy branches
accumulated 80, 89, and 27% of the total N, P, and K absorbed
during this period. Moreover, canopy branches of off-year trees
contained 78 and 137% more N and P, respectively, than
on-year trees at nut maturity in September. Thus, on-year trees
accumulated nutrients in fruit, whereas off-year trees stored
nutrients in perennial tissues during the nut fill period.

Alternate bearing had a marked influence on nutrient distribution, but had little effect on the periodicity of nutrient uptake.
Nutrients accumulated in the fruits of on-year trees and in the
perennial tree parts of off-year trees over the entire season.
However, nutrient uptake occurred primarily during the nut fill
period in both on- and off-year trees. Thus, on-year trees took
up 69, 95, and 93% of their total annual accumulation of N, P,
and K, respectively, during nut fill (Table 3). The corresponding values for off-year trees are 56, 64, and 99%. Nutrient
uptake was negligible during the postharvest--leaf senescence
period irrespective of crop load.
On-year trees removed 4, 6, and 3 times more N, P, and K,
respectively, in fruits plus abscised leaves than off-year trees
(Table 3). For the orchard (212 trees ha −1), the fruit removed
211 kg ha −1 of N, 23 kg ha −1 of P, and 186 kg ha −1 of K at
harvest. At the tree level, fruit removed 46, 52, and 43% of the
total N, P, and K present in a 20-year-old heavily cropping
pistachio tree (calculated from Table 2).
Crop load influenced the annual accumulation and reduction
of N and P in perennial tree parts (Table 3). During an on-year,
fruits and abscised leaves removed more N (47%) and P (98%)
than was taken up from the soil, indicating that substantial
amounts of nutrients were redistributed from storage during
the on-year. Conversely, during an off-year, N and P uptake
was greater than nutrient removal and pistachio trees accumulated nutrients.
The quantities of N, P, and K removed and taken up were
similar over the 2-year alternate-bearing cycle (Table 3). That
is, the sum of the nutrients removed over a 2-year alternatebearing cycle equalled the sum of the nutrients taken up by
these trees over the same period. These data indicate that
off-year trees accumulated nutrients that were used during the
following on-year, and that net nutrient accumulation and
retention in tree structure were minimal in these mature pistachio trees.
Discussion
Fruiting effects on root growth
There was a negative relationship between nutrient uptake and
root growth. During nut fill in mid-June, for example, roots
from on-year trees had 1.5 times less root length, a 50% lower

954

ROSECRANCE, WEINBAUM AND BROWN

Table 3. Uptake of N, P, and K (g per tree) during spring flush, nut fill and postharvest--leaf senescence periods and removal in fruits and leaf litter
in on- and off-year trees.1
Cropping

Nitrogen
On-year
Off-year
Phosphorus
On-year
Off-year
Potassium
On-year
Off-year

Nutrient uptake

Nutrient

Annual

Spring flush

Total

removal

change2

Nut fill

Postharvest

243
317

543
403

3
0

789
720

1167 a3
264 b

--378
+456

3
26

54
47

0
0

57
73

113 a
18 b

--54
+55

0
3

1014 a
479 b

74 a
0b

1088 a
482 b

1019 a
387 b

+69
+95

1

Nutrient uptake determined from differences in tree nutrient contents from sequential tree excavations.
Difference between total annual nutrient uptake and removal in fruits and abscised leaves.
3
Within a column, values followed by different letters are significantly different at P ≤ 0.05, according to the F test.

2

root growth rate, and 4 times fewer white roots growing against
the rhizotron windows than off-year trees. Nevertheless, between May 24 and September 8, N and K uptake were 35 and
112% greater, respectively, in on-year trees than in off-year
trees. Moreover, following nut harvest in September, root
growth increased 2--3-fold in both on- and off-year trees,
although nutrient uptake was negligible during this period.
Similar results have been reported in mature prune trees, where
heavy-fruiting trees took up 17% more K and had less root
growth than trees that were defruited two months earlier
(Weinbaum et al. 1994a). In coffee trees, the relationship
between root growth and N uptake is also poor (Canell and
Kimeu 1971). A negative relationship between root growth and
N uptake has been observed in some herbaceous species
(Caldwell et al. 1981).
For decoupling between root growth and nutrient uptake to
occur, the rate of nutrient uptake per unit of root length in
fruiting trees must be higher than that of light-fruiting or
defruited trees. Rates of N uptake by roots are reported to be
50% higher in fruiting apple (Hansen 1971a, 1971b), and
coffee (Cannell and Kimeu 1971) trees relative to non-fruiting
trees. Simulation models have shown that doubling root uptake
kinetics is as effective as doubling root growth in increasing N
(Barber 1995) and P uptake (Caldwell et al. 1992). Moreover,
changes in root uptake rates are more rapid than changes in
root proliferation rates (Jackson et al. 1990). Thus, increases in
root nutrient uptake rates can compensate for a lack of root
growth.
Nitrogen uptake during the spring
During the spring, 15N uptake was twice as high in on-year
trees as in off-year trees, whereas total N uptake was 31%
higher in off-year trees than in on-year trees (cf. Figure 2a and
Table 3). The different time periods over which 15N uptake
(between mid-March and late May) and total N uptake (be-

tween mid December to late May) occurred may account for
this discrepancy. It is not clear when the 15N was taken up by
the pistachio trees, but it is likely that substantial amounts of
15
N were absorbed by on-year trees in May when developing
fruits became a major sink for nitrogen (Rosecrance 1996).
On- and off-year shoots (leaves, fruits, and current-year wood)
contained similar amounts of N before May; however, on-year
trees contained almost double the amount of N of shoots of
off-year trees by late May (Rosecrance 1996). Thus, as fruits
became a major nitrogen sink in late spring, 15N was likely
taken up from the soil.
The greater total N uptake in off- versus on-year trees
between December and May may reflect the potential sink
activity of the depleted N storage pools in off-year trees as a
result of fruiting the previous year (Rosecrance 1996). Weinbaum et al. (1994b) reported that the percentage of N derived
from 15N-labeled fertilizer applied in January to mature pistachio trees was twice as high in leaves of off-year trees as in
leaves of on-year trees when sampled 2 weeks after bud break.
We found that off-year pistachio trees had greater N uptake in
early spring, whereas on-year trees had greater N uptake in late
spring. This is consistent with demand-driven uptake because
storage N pools of trees entering an off-year are low (Rosecrance 1996), hence soil N uptake occurs in early spring to
support leaf area development. Trees entering an on-year,
however, contain significant amounts of storage N that can be
utilized for early spring growth and so N uptake from the soil
is delayed until late in the spring when internal N pools are
exhausted and N is needed for continuous fruit growth and
development.
Fruiting effects on N, P, and K uptake
Determination of annual nutrient uptake in mature fruit trees is
the first step in developing best management practices for these
nutrients to maintain high yields and to minimize fertilizer

N, P, AND K UPTAKE AND ROOT GROWTH IN PISTACHIO TREES

leaching to groundwater. Nutrients taken up during an on-year
were allocated primarily to the fruits, whereas perennial tissues were the major nutrient sink in off-year trees. On-year
trees took up 167, 12, and 227 kg ha −1 of N, P, and K,
respectively, over the season, whereas off-year trees absorbed
136, 15, and 71 kg ha −1 of N, P, and K.
Over the 2-year alternate bearing cycle, there was a balance
between nutrient uptake and removal in mature pistachio trees;
however, these processes were not balanced in either the offor on-year. In off-years, nutrient uptake was greater than removal, whereas during on-years, more nutrients were removed
than were taken up from the soil. Because the net result of these
fluctuations is that only small quantities of nutrients accumulate in perennial tissues over a 2-year alternate-bearing cycle,
nutrient removal measured over 2 years can provide a good
estimate of nutrient uptake over the same period.
The greater N uptake in on-year trees than in off-year trees
during nut fill may reflect a decrease in vascular cycling of
amino-N, coincident with the accumulation of N by the developing embryo. The reduction in the cycling of N in the xylem
and phloem between roots and shoots may stimulate wholeplant N uptake (Cooper and Clarkson 1989, Lee et al. 1992,
Imsande and Touraine 1994) and K uptake (Weinbaum et al.
1994a). It has been observed that pretreating maize roots with
amino acids (asparagine and glutamine) inhibited NO −3 and
NH +4 uptake, whereas decreasing root amino acids with specific N-assimilation inhibitors stimulated N uptake (Lee et al.
1992). In pistachio, it is possible that the removal of amino N
by reproductive structures (fruit, seed) stimulated N uptake in
on-year trees.
Crop load influenced K uptake more than the uptake of other
nutrients, with on-year trees taking up three times more K than
off-year trees (Table 3) (cf. Brown et al. 1995). Similarly,
heavy-fruiting prune trees took up significantly more K than
defruited trees (Weinbaum et al. 1994b). In pistachio, 95% of
the K uptake occurred during nut fill (Table 3), and may reflect
the roles of K in sugar transport which include: binding to
carboxylates and transport (mainly as potassium malate) in the
phloem to fruits and roots (Ben-Zioni et al. 1971, Casadesus et
al. 1995, Touraine et al. 1988); and acting as an osmoticum to
develop pressure gradients in the phloem for the transport and
storage of sugars (Giaquinta 1983).
Little nutrient uptake occurred during the postharvest--leaf
senescence period (mid-September to December). The substantial quantities of amino acids cycling within the plant
during leaf N resorption may have contributed to the low N
uptake from the soil during the postharvest--leaf senescence
period. Both on- and off-year trees resorbed approximately
50% of their leaf nitrogen during this period (Rosecrance
1996). In soybeans, amino-nitrogen resorbed from leaves inhibits N uptake (Imsande and Touraine 1994, Touraine et al.
1992).
Another possible cause for the low nutrient uptake during
the postharvest--leaf senescence period relates to pistachio’s
native range. Pistachio trees have evolved in climates where
little or no rainfall occurs during the autumn (Rao et al. 1976),

955

and, as a consequence, selection pressure for trees that absorb
nutrients during this period is likely to be low.
We conclude that the pronounced effect of alternate bearing
on tree nutrient demand and uptake has important implications
for fertilizer management. The greatest amount of soil nutrient
uptake occurred during the nut fill period in both on- and
off-year trees. Nutrient uptake in the postharvest--leaf senescence period was low in both on- and off-years indicating that
fertilizer application many not be effective at this time.

Acknowledgments
The study was supported by a grant from the California Pistachio
Industry. We greatly appreciate the help from the staff at S and J
Ranch, especially Jerry Allen, where this work was conducted. We
also thank Grant Aitken, Bob Beede, Al Bonin, Tony Cristler, Louise
Ferguson, Jennifer Katcher, Tom Muraoka, Franz Niederholzer,
Oswaldo Rubio, Hilary Sampson, Steve Sibbett, and Max Stevenson
for their help in the tree excavations.

References
Barber, S.A. 1995. Soil nutrient bioavailability. A mechanistic approach. John Wiley & Sons, New York, 414 p.
Ben-Zioni, A., Y. Vaadia, and S.H. Lips. 1971. Nitrate uptake by roots
as regulated by nitrate reduction products of the shoots. Physiol.
Plant. 24:288--290.
Brown, P.H., S.A. Weinbaum and G.A. Picchioni. 1995. Alternate
bearing influences annual nutrient consumption and the total nutrient content of mature pistachio trees. Trees 9:158--164.
Cabrera, M.L. and D.E. Kissel. 1989. Review and simplification of
calculations in 15N tracer studies. Fert. Res. 20:11--15.
Crane, J.C. and B.T. Iwakiri. 1981. Morphology and reproduction in
pistachio. Hort. Rev. 3:376--393.
Caldwell, M.M., L.M. Dudlye, and B. Lilieholm. 1992. Soil solution
phosphate, root uptake kinetics and nutrient acquisition: implications for a patchy soil environment. Oecologia 89:305--309.
Caldwell, M.M., J.H. Richards, D.A. Johnson, R.S. Nowak and R.S.
Dzurec. 1981. Coping with herbivory: photosynthetic capacity and
resoruce allocation in two semiarid Agropyron bunchgrasses. Oecologia 50:14--24.
Cannell, M.G.R. and B.S. Kimeu. 1971. Uptake and distribution of
macro-nutrients in trees of Coffea arabica L. in Kenya as affected
by seasonal climatic differences and the presence of fruits. Ann.
Appl. Biol. 68:213--230.
Casadesus, J., L. Tapia and H. Lambers. 1995. Regulation of K+ and
NO −3 fluxes in roots of sunflower (Helianthus annuus) after changes
in light intensity. Physiol. Plant. 93:279--285.
Chalmers, D.H. and B. Van Den Ende 1975. Productivity of peach
trees: Factors affecting dry-weight distribution during tree growth.
Ann. Bot. 38:423--432.
Conradie, W.J. 1992. Partitioning of nitrogen in grapevines during
autumn and utilization of nitrogen reserves during the following
growing season. S. Afr. J. Enol. Vitic. 13:45--51.
Cooper, H.D. and D.T. Clarkson. 1989. Cycling of amino-nitrogen and
other nutrients between shoots and roots in cereals----a possible
mechanism integrating shoot and root in the regulation of nutrient
uptake. J. Exp. Bot. 40:753--762.
Dasberg, S., H. Bielorai and Y. Erner. 1983. Nitrogen fertigation of
Shamouti oranges. Plant Soil 75:41--49.

956

ROSECRANCE, WEINBAUM AND BROWN

Giaquinta, R.T. 1983. Phloem loading of sucrose. Annu. Rev. Plant
Physiol. 34:347--387.
Golomb, A. and E.E. Goldschmidt. 1987. Mineral nutrient balance and
impairment of the nitrate-reducing system in alternate-bearing
Wilking mandarin trees. J. Am. Soc. Hort. Sci. 112:397--401.
Hansen, P. and J. Grauslund. 1978. Levels of sorbitol in bleeding sap
and in xylem sap in relation to leaf mass and assimilate demand in
apple trees. Physiol. Plant. 42:129--133.
Hansen, P. 1971a. The effects of cropping on the distribution of growth
in apple trees. Tidsskr. Planteavl 75:119--127.
Hansen, P. 1971b. The effects of cropping on the uptake, contents,
and distribution of nutrient in apple trees. Tidsskr. Planteavl
75:615--625.
Hansen, P. 1973. The effect of cropping on the growth and uptake of
nutrients by apple trees at different levels of nitrogen, potassium,
magnesium, and phosphorus. Acta Agric. Scand. 23:87--92.
Hauck, R.D. and J.M. Bremner. 1976. Uses of tracers for soil and
fertilizer nitrogen research. Adv. Agron. 28:219--266.
Head, G.C. 1969. The effects of fruiting and defoliation on seasonal
trends in new root production on apple trees. J. Hort. Sci. 44:175--81.
Heim, G., J.J. Landsberg, R.L. Watson and P. Brain. 1979. Eco-physiology of apple trees: dry matter production and partitioning by
young golden delicious trees in France and England. J. Appl. Ecol.
16:179--194.
Imsande, J. and B. Touraine. 1994. N demand and the regulation of
nitrate uptake. Plant Physiol. 105:3--7.
Jackson, R.B., J.H. Manwaring and M.M. Caldwell. 1990. Rapid
physiological adjustment of roots to localized soil enrichment.
Nature 344:58--60.
Johnson, R.S. and S.A. Weinbaum. 1987. Variation in the tree size,
yield, cropping efficiency, and alternate bearing among ‘‘Kerman’’
pistachio trees. J. Am. Soc. Hort. Sci. 112:942--945.
Kappel, F. 1991. Partitioning of above-ground dry matter in ‘‘Lambert’’
sweet cherry trees with and without fruit. J. Am. Soc. Hort. Sci.
116:201--205.
Legaz, F. E. Prim-Millo, E. Primo-Yufera, C. Gil, and J.L. Rubio.
1982. Nitrogen fertilization in citrus I. Absorption and distribution
of nitrogen in calamondin trees (Citrus mitis Bl.), during flowering, fruit set and initial fruit development periods. Plant Soil
66:339--351.
Lee, R.B, J.V. Purves, R.G. Ratcliffe and L.R. Saker. 1992. Nitrogen
assimilation and the control of ammonium and nitrate absorption by
maize roots. J. Exp. Bot. 43:1385--1396.
Maggs, D.H. 1963. The reduction in growth of apple trees brought
about by fruiting. J. Hort. Sci. 38:119--128.

Millard, P. and G.H. Neilsen. 1989. The influence of nitrogen supply
on the uptake and remobilization of stored N for the seasonal
growth of apple trees. Ann. Bot. 63:301--309.
Miller, H.G. 1995. The influence of stand development on nutrient
demand, growth and allocation. Plant Soil 169:225--232.
Munoz N, J. Guerri, F. Legaz, and E. Primo-Millo. 1993. Seasonal
uptake of 15N-nitrate and distribution of absorbed nitrogen in peach
trees. Plant Soil 150:263--269.
Nii, N. 1993. Fruiting effects on leaf characteristics, photosynthesis,
and root growth in peach trees. J. Jpn. Soc. Hort. Sci. 62:519--526.
Rao, M.S.V., W.V. Abbott, and J.S. Theon. 1976. Satellite-derived
global oceanic rainfall atlas (1973 and 1974). NASA Goddard
Space Flight Center. Washington, DC, 410 p.
Rosecrance, R.C. 1996. Effect of alternate bearing on nutrient uptake,
storage, and root growth in mature pistachio (Pistachia vera L.)
trees. Ph.D. Diss., Univ. California, Davis, 121 p.
Smith, P.F. 1976. Collapse of ‘‘Murcott’’ tangerines trees. J. Am. Soc.
Hort. Sci.101:23--35.
Smith, G.S., J.G. Buwalda and C.J. Clark. 1988. Nutrient dynamics of
a kiwifruit ecosystem. Sci. Hort. 37:87--109.
Stassen, P.J.C., H.W. Stindt, D.K. Strydom and J. H. Terblanche. 1981.
Seasonal changes in nitrogen fractions of young Kakamas peach
trees. Agroplantae 13:63--72.
Touraine, B., N. Grignon and C. Grignon. 1988. Charge balance in
NO −3 fed soybean. Estimation of K+ and carboxylate recirculation.
Plant Physiol. 88:605--612.
Touraine, B. B. Muller, and C. Grignon. 1992. Effect of phloemtranslocated malate on NO −3 uptake by roots of intact soybean
plants. Plant Physiol 93:1118--1123.
Weinbaum, S.A. and P.M. Neumann. 1977. Uptake and metabolism of
15
N-labeled potassium nitrate by French prune (Prunus domestica L.) leaves and the effects of two surfactants. J. Am. Soc. Hort.
Sci. 102:601--604.
Weinbaum, S.A., F.J.A. Niederholzer, S. Ponchner, R.C. Rosecrance,
R.M. Carlson, A.C. Whittlesey and T.T. Muraoka. 1994a. Nutrient
uptake by cropping and defruited field-grown ‘‘French’’ prune trees.
J. Am. Soc. Hort. Sci. 119:925--930.
Weinbaum, S.A., G.A. Picchioni, T.T. Muraoka, P.H. Brown and L.
Ferguson. 1994b. Nitrogen usage, accumulation of carbon and
nitrogen reserves, and the capacity for labelled fertilizer nitrogen
and boron uptake varies during the alternate-bearing cycle in
pistachio. J. Am. Soc. Hort. Sci. 119:24--31.
Williamson, J.G. and D.C. Coston. 1989. The relationship among root
growth, shoot growth, and fruit growth of peach. J. Am. Soc. Hort.
Sci. 114:180--183.