Annals of Botany 78 : 675–685, 1996
Organic Matter and Nitrogen Cycles in a Pine Afforested Catchment with a Shrub
Layer of Adenocarpus decorticans and Cistus laurifolius in South-eastern Spain
M A R I! A J O S E! M O R O*‡, F R A N C I S C O D O M I N G O† and A N T O N I O E S C A R RE! *
* Departamento de EcologıU a, UniŠersidad de Alicante, 03080 Alicante, and † EstacioU n Experimental
de Zonas Aridas, CSIC, 04001 AlmerıU a, Spain
Received : 20 February 1996
Accepted : 28 May 1996
Organic matter and nitrogen cycles in two mediterranean woody shrubs (Adenocarpus decorticans Boiss. and Cistus
laurifolius L.) and two pine species were investigated during 1987–1989 in a small, recently pine-afforested catchment
in Sierra de los Filabres (Almerı! a Province, south-eastern Spain). Pine cover was sparse because canopy closure was
not yet completed, allowing strong shrub colonization in the clearings. The aim of this study was to compare the
contribution of different annual fluxes and the distribution of organic matter and nitrogen in both shrub and pine
components for the entire catchment. Special emphasis was placed on the N use strategy shown by the two shrub
species, a symbiotic N fixing species (A. decorticans) and a non-fixing species (C. laurifolius).
#
Our results showed that the characteristics of C and N cycling in the Nacimiento catchment are mainly determined
by the early stage of pine layer development and the significant contribution of the two shrub species differing with
respect to C acquisition and N use.
The pine layer was characterized by a low standing biomass, substantial percentages of needle biomass and high
(net production}biomass) and (needle production}total net production) ratios. N uptake was mainly diverted to
biomass increment, as shown by the substantial allocation found in this study. Overall, these results are consistent with
the patterns described for even-aged stands during the early-growth phase. Retranslocation supplied 21 % of the
annual N requirements for pine above-ground biomass production.
C. laurifolius showed low litter-fall return, strong retranslocation, efficient utilization of N in bulk deposition and
slow decomposition, suggesting a closer, self-regulated organic matter and N-conserving behaviour than A.
decorticans. On the contrary, A. decorticans showed high leaf turnover, strong litter-fall return, low retranslocation
and fast mineralization of organic matter and nitrogen, indicating that internal organic matter and N cycling is less
efficient, and thus, that this species is more dependent on the soil to meet its N requirements.
# 1996 Annals of Botany Company
Key words : Adenocarpus decorticans Boiss., biogeochemical cycles, Cistus laurifolius L., mediterranean shrubs,
nitrogen fixation, nitrogen use, pine afforestation, south-eastern Spain, woody legumes.
INTRODUCTION
In the last decade a great deal of research has been done on
organic matter and mineral cycling in Mediterranean
ecosystems, such as holm-oak forest (Romane and Terradas,
1992), Quercus coccifera garrigue (Rapp and Lossaint,
1981) or California chaparral (Gray and Schlesinger, 1981).
Besides these natural or semi-natural ecosystems, artificial
afforestations also occupy extensive areas in Mediterranean
landscapes but few serious attempts have focused on
determining a general overview of their biogeochemical
properties.
In south-eastern Spain, the objective of pine afforestation
has frequently been the protection of soil rather than timber
production, thus bush clearing practices are habitually
lacking. Depending on soil and climate characteristics, pine
canopy closure may be delayed for many years and
sometimes complete canopy closure is never reached. During
this stage, pines form a close association with woody shrubs
providing a pine}shrub mosaic-type vegetation where
functional aspects are poorly known. In these sites, shrub
‡ For correspondence.
0305-7364}96}120675­11 $25.00}0
layer contribution to total biomass can be significant, but its
role upon the overall nutrient regime has not been studied
in depth.
Typical pine afforestations with a well-developed shrub
layer are found along extensive areas of the Sierra de los
Filabres (Almerı! a, south-eastern Spain). These plantations
were established in the early 1970s at an altitude ranging
from 1400 to 2200 m above sea level. The pine layer is
composed of Pinus pinaster Aiton and Pinus nigra Arnold,
while gaps among pine individuals have been successfully
colonized mainly by two perennial shrubs, Adenocarpus
decorticans (Leguminosae), an N fixing species, and Cistus
#
laurifolius (Cistaceae). The present study was part of an
integrated research programme designed to determine the
role of pines and accompanying shrubs on hydrological and
nutrient budgets, which was initiated in 1986 in a small
catchment in Sierra de los Filabres. This paper reports on
the significance of the differences of both the biogeochemical
fluxes on an area basis and the C and N use strategy shown
by the pine layer as well as by the two shrub populations.
This study had the following objectives : (1) to evaluate the
organic matter and nitrogen pools and fluxes in the
aboveground biomass, both of the pine and shrub layers,
# 1996 Annals of Botany Company
676
Moro et al.—Biogeochemical Cycles in a Mediterranean EnŠironment
for the entire catchment ; (2) to examine the relative
contribution of the two shrub species to the organic matter
and nitrogen budgets ; (3) to assess the importance of
external nitrogen inputs into the nitrogen cycle and (4) to
evaluate nitrogen-use in these species. Special emphasis was
given to the comparison between the two shrub species.
MATERIAL AND METHODS
Study site
The field site was the 34 ha ‘ Nacimiento ’ micaschist
catchment, located in the Sierra de los Filabres (Almerı! a
Province, south-eastern Spain). The elevation of the
‘ Nacimiento ’ catchment ranges from 1560 to 1740 m above
sea level. The climate is Mediterranean with an average
annual temperature of 11 °C, and a marked summer drought
period (Domingo et al., 1994). The mean annual precipitation during the study period (1987–1990) was 700 mm
in ‘ Nacimiento ’ concentrated mainly in autumn and winter.
Snow falls accounted for 25–30 % of the total annual
precipitation (Domingo, 1991). Long-term climatic data
from the nearest meterological station ‘ Calar Alto ’ (2000 m
elevation, 10 km from the field site), showed a mean annual
precipitation of 400 mm. This mean was calculated without
accounting for snow events which were not measured and,
hence under-estimating the total precipitation. Soils are
either eutric cambisols or eutric regosols, all relatively poor
in available nutrients (ICONA, 1987). The vegetation
consisted of a 13-year-old mixed plantation of Pinus pinaster
and Pinus nigra and two 11-year-old populations of the
mediterranean shrubs Adenocarpus decorticans and Cistus
laurifolius mainly growing in the clearings of the forest. A.
decorticans, a leguminous shrub, is an effective atmospheric
N fixer with mesophyllous leaves rich in nutrients (Moro,
#
1992 ; Moro, Domingo and Bermudez de Castro, 1992). Its
strong root system, with a deep tap root and a superficial
lateral root system, allows both superficial and deep water
to be reached. C. laurifolius has relatively superficial roots,
malacophyllous nutrient-poor leaves and apparently seems
to be adapted to oligotrophic and degraded soils, as are
other species of Cistaceae (Merino, 1986 ; Nun4 ez-Oliveira,
Martinez-Abaigar and Escudero-Garcı! a, 1993). The two
shrub species coexist in the catchment but C. laurifolius
dominates on the driest and poorest soils (developed directly
on mica-schists and quite shallow slope deposits), whereas
A. decorticans grows better on sites with a lower slope and
characterized by deeper, wetter and more fertile soils (A.
Sole! , pers. comm).
Field measurements
Density and dimensional measurements of the four species
(P. pinaster, P. nigra, A. decorticans and C. laurifolius) were
made during the summer of 1986 in 50 15¬15 m plots
selected to follow altitudinal and orientation gradients in
the catchment (Moro, 1992). In all plots, the number of
individual pines, their diameter at breast height (DBH),
height and projected canopy cover were measured. For the
shrub species, number of individuals, basal diameter (BD),
number and basal diameter of branches and projected
canopy cover were measured. Sixteen individuals of each
species, representative of range of size-classes of the
population, were harvested at the end of the 1986 growing
season. All branches from each tree or shrub were freshweighed and their basal diameters were measured. Four
branches and five stem discs were taken from each plant and
used to determine above-ground biomass (AGB) as well as
its nutrient content. The material collected was sorted into
needles}leaves of different age classes, twigs, stem wood and
stem bark. The data from destructive sampling were used to
find specific allometric relationships for each biomass
fraction as function of DBH or BD. Above-ground net
production (ANPP) was calculated in all species by adding
current foliage and twig biomass to perennial aboveground
biomass increment. Perennial biomass increment in pines
was calculated from 5-years’ radial wood increments and
the application of allometric relations on DBH to calculate
the 1982 accrued biomass. Perennial biomass increment was
calculated by the difference in accrued biomass estimates between 1982 and 1986 and was expressed per hectare per year.
Because of the difficulty in distinguishing the annual growth
rings in shrub species, annual increments of perennial parts
were determined from increments of basal area in repeated
shrub inventories. For this purpose, 20 plots utilized in 1986
were again measured in 1990. In the shrub species, net
production of the reproductive fractions was assumed to be
the same as that lost by litter-fall. Litter-fall was collected
monthly from 1986–1989 using 20 0±5¬0±5 m small square
litter-traps under bushes and 20 0±28 m# circular traps under
pines. Traps were placed below the canopy of ten randomly
selected individuals of each species. Collected plant material
was sorted into leaves, shoots, flowers, seeds, fruits and
branches.
Leaf litter decomposition was monitored over 2 years by
field incubation in confined litter bags of recently shed
leaf}needle litter from the four species. Further details are
described in Moro, Domingo and Bellot (1995).
The seasonal pattern of nitrogen fixing activity by nodules
of A. decorticans was estimated by the acetylene reduction
technique, ARA, (Hardy, Burns and Holsten, 1973).
Samples of excised nodules of Adenocarpus were taken
monthly from Oct. 1988 to Sep. 1989 in two representative
areas located at the top and bottom of the watershed.
Details of field measurements and procedures are presented
in Moro (1992) and Moro et al. (1992). From indirect
measurement of N fixation by such methods as ARA, it is
#
not possible to assess accurately the actual rate of
atmospheric N fixed by the legume-Rhizobium symbiosis.
#
Thus, in this paper we attempt only a gross approach to the
amount of atmospheric N entering the ecosystem in this
#
way. We utilized the average monthly ARA and nodule
density determined in the above mentioned studies and a
transformation factor C H : N ranging from 1±5 to 3
# # #
(Mu$ ller and Bermudez de Castro, 1987) to calculate input
by N fixation.
#
Through fall was measured in each species with polyethylene collectors placed at two distances from the trunk
below individuals representative of different sizes. Stemflow
was recorded under the same plants, using a PV-isocyanate
channel ring attached to the bottom of the trunk of
Moro et al.—Biogeochemical Cycles in a Mediterranean EnŠironment
P. pinaster, P. nigra and A. decorticans and around representative branches of C. laurifolius, because of its
multistemmed geometry. Bulk open-field deposition was
sampled for each event using polyethylene collectors located
in clearings 1±5 m above the ground. Snow events were
measured according to the recommended method of
Galloway and Likens (1976) by using five large containers
of polyethylene (150 l capacity and 60 cm diameter) to avoid
overflowing. The stream water was sampled during the
hydrological year 1988–1989 using a stage level recorder
(model f553-A, Weather Measure). The mineral soil and
litter layer were sampled in six 25¬25 m plots. Thirty-six
known volume mineral soil samples (six per plot) were taken
with an open sided corer from depths of 0–15 and 15–30 cm.
Samples from each plot were bulked to obtain two composite
samples for each depth. Soil litter was sampled in 60
50¬50 cm quadrats (ten per plot). Material was sorted by
species into entire leaves}needles, fragmented leaves}
needles, branches, flowers and fruits.
Laboratory procedures
Soil samples were air-dried and sieved with a 2 mm
screen, dried at 105 °C and pulverized. The total C and N
contents were determined by combustion in an elemental
Autoanalyser (NA 1500 Carlo Erba Instrumentazione,
Italy). We used a conversion factor of 1±72 to transform
carbon to organic matter (Hesse, 1971). No analyses of
available N in mineral soil were performed, therefore it was
assumed to be near to the lower range given for
Mediterranean ecosystems (Read and Mitchell, 1983), i.e.
1 % of the total N.
Plant material was oven-dried at 70 °C and weighed. Ash
content was determined in pulverized subsamples after
combustion at 400 °C in a muffle furnace for 12 h. N
concentration in different fractions of biomass, litter-fall,
litter layer and decomposing litter were determined using an
automatic Kjeldahl autoanalyser (TECATOR Analyzer
model 1030) and used to calculate the amount of total N in
the several fractions of pools or fluxes measured.
Ammonium in water samples was measured by the
distillation method (ASTM Standard methods) and colorimetric determination with Nessler reagent. Nitrate nitrogen
(N-NO ) was determined by liquid chromatography
$
(DIONEX, Ion chromatograph 10 model, UK). Gas
samples from incubated A. decorticans nodules were
analysed with a KONIC KNF-2000 gas chromatograph
equipped with a PORAPAK R column. Results of
nitrogenase activity were expressed as nmol C H g−" nodule
# %
d.wt h−".
Decomposition data processing
Weight loss from decomposition samples in the four
species and N loss from A. decorticans leaf litter were fitted
to simple exponential models (Olson, 1963) after transformation by the formula :
ln Wt ¯ ln W ®kt
!
where Wt is the percentage of initial mass remaining, W the
!
percentage of initial mass, k the decay constant (year−") and
677
t is elapsed time (years). Decay constants in the species
studied were compared by t-test.
N-flux calculations
To calculate internal above ground N fluxes at the
catchment level for the populations studied, the following
parameters were calculated in kg ha−" year−".
Allocation. Amount of N inmobilized in perennial
structures and foliage increment. Calculated as the annual
net increment in N pool of perennial tissues (stem, branches
and new twigs) and foliage (i.e. steady state biomass
conditions were not assumed) minus N loss in gross litter
fall. Annual net increment in N pool was calculated from
the average N concentration (mg N g−" d.wt) in stemwood,
stembark, branches, twigs and new leaves and the corresponding biomass increments.
Return. Amount of N lost in litterfall and leaching from
canopy.
Requirement. Amount of N required to build up new
structures, accounting for N associated with the mass
increment of perennial structures as well as N in net
production of leaves (both for maintenance and leaf biomass
increment) and reproductive organs. To this quantity, N
loss from canopy leaching must be added.
Uptake. N taken up by the root system and calculated as
return plus allocation.
Retranslocation. The amount of N required by the plant
which is not taken up by the root system but reabsorbed
from old tissues, calculated as the difference between
requirement and uptake.
Net rainfall and foliar absorption. Net amount of rainfall
N-NH or N-NO reaching the soil or taken up by the plant
%
$
after passing through canopy (through fall) and stem (stem
flow). Calculated as N in rainfall minus N in through fall
plus stem flow. A positive quantity indicates net rainfall,
negative amounts indicate foliar absorption. The two
components of net rainfall (wash-off dry deposition and
leaching) were determined applying the model of Lovett and
Lindberg (1984).
RelatiŠe requirements. N requirement for maintenance per
unit of biomass (mg N g−" d.wt year−"). Calculated as N
annual return divided by the above-ground biomass.
N turn-oŠer rate (Ln) : N requirement for maintenance per
unit of N in the aerial biomass. Calculated as N return per
unit of N in the plant (g N g−" N year−").
N mean residence time. (1}Ln).
Nitrogen use efficiency (NUE) was calculated by two
methods. The first, proposed by Vitousek (1982), is expressed
as the ratio between the dry mass lost in litterfall and the N
returned to the soil in this way. The second method,
modified from the index proposed by Berendse and Aerts
(1987), is expressed as the product of the aboveground N
productivity, A, (rate of dry matter production per unit of
N in the plant) and the mean residence time of N in aerial
parts (1}Ln).
Data processing
All results on population structure, as well as those for
compartments and fluxes are averaged for the whole
678
Moro et al.—Biogeochemical Cycles in a Mediterranean EnŠironment
watershed to reflect a general picture of the behaviour of the
major species with regard to organic matter and N cycle.
Organic matter pools and fluxes as well as hydrological
fluxes are expressed in kg ha−" or kg ha−" year−" taking into
account the average density and the surface covered by each
species in the watershed.
RESULTS
T     2. RelatiŠe distribution (%) of the aboŠe-ground
biomass for Adenocarpus decorticans, Cistus laurifolius and
the pine layer
A. decorticans
C. laurifolius
Pines
Leaves}needles
Twigs
Branches
Stem
13
23
30
4
5
3
77
70
27
6
2
40
Organic matter pools and fluxes
Total above-ground biomass accounted for 24 350 kg ha−",
30 % corresponding to the shrub layer (Table 1). An
elevated pine density was obtained in this study, but because
of the low age of afforestation, only 17 333 kg ha−" were
accumulated in the aerial biomass. Above-ground biomass
in both shrub species for the whole catchment was similar :
3860 kg ha−" for A. decorticans and 3390 kg ha−" for C.
laurifolius, but in the former it was accumulated in far fewer
individuals (Table 1). The average basal diameter was
higher and the density lower in the A. decorticans population
than in C. laurifolius, while canopy cover was similar. The
relative aerial biomass distribution in pines and shrub
species is shown in Table 2. Needle biomass accounted for
30 % of the total above-ground biomass in pines, whereas
stem fraction only constituted 40 %. Leaf biomass accounted
for 13 and 23 % of the total biomass in A. decorticans and
C. laurifolius, respectively. Both species produced similar
amounts of leaves although the foliar productivity (leaf
production}leaf biomass ; Table 1) was higher in A.
decorticans than in C. laurifolius due to a more rapid leaf
renovation.
ANPP was 3190 kg ha−" year−" in the pine layer, 1110 kg
ha−" year−" and 760 kg ha−" year−" in A. decorticans and C.
laurifolius, respectively. A considerable proportion of ANPP
in pines (50 %) was diverted to needle production. The
foliage production accounted for 44 and 50 % of the total
aerial net production in Adenocarpus and Cistus, respectively. The annual mean litterfall was 1430 kg ha−" year−"
in the pine layer, practically identical to that of the total
shrub layer (Table 3). The shrub litterfall accounted for
933 kg ha−" year−" in A. decorticans and 477 kg ha−" year−"
in C. laurifolius. Leaves}needles were the major fraction in
the litterfall of the four species (Table 3) accounting for
percentages ranging from 59 to 91 %. The reproductive
fraction was higher in the litterfall of A. decorticans than C.
laurifolius, but had a higher annual variability (Table 3).
The seasonal pattern of the A. decorticans leaf litter-fall
showed a maximum in summer, concentrated in one month
(1987 and 1988) or distributed over July and August (1986
and 1989) with winter peaks of varying intensity (Fig. 1 B).
C. laurifolius leaf litterfall followed a regular pattern,
mainly concentrated in one summer month (except in 1989)
and negligible the rest of the year (Fig. 1 B). There was a
significant correlation between mean monthly temperature
and leaf litterfall in the two shrub species : r ¯ 0±50, (P !
T     1. Structural attributes, pools and fluxes of organic matter for Adenocarpus decorticans, Cistus laurifolius and the
pine layer in the Nacimiento watershed
Density (no. ha−")
Cover (%)
Basal area (m# ha−")
DBH (cm)
Basal diameter (cm)
Leaf specific weight (mg cm−#)
C}N in leaf litter
LAI (m# m−#)
N content in green leaves (mg N g−" d.wt)
N content in leaf litterfall (mg N g−" d.wt)
Total above ground biomass (kg ha−") (1)
Leaf biomass (kg ha−") (2)
ANPP (kg ha−" year−") (3)
Leaf net production (kg ha−" year−") (4)
Litterfall (kg ha−" year−") (5)
Litter layer (kg ha−")
Biomass}net production (1)}(3) (year)
Leaf net production}ANPP (4)}(3)
Leaf productivity (4)}(2) (year−")
Organic matter turnover (5)}(1) (year−")
Mean leaf life span (months)
Mean residence time of organic matter (MRT) (year)
* At 130 cm.
Pines
A. decorticans
C. laurifolius
3220
48
5±88*
4±3
—
45
169
1±20
8±4
3±0
17 100
5370
3190
1630
1430
3000
5±4
0±50
0±30
0±08
48
12±5
1832
35
5±66
—
5±53
14
31
0±34
29±0
17±5
3860
500
1110
490
933
1030
3±5
0±44
0±90
0±24
15
4±2
4080
28
7±14
—
4±32
17
145
0±50
13±7
4±0
3390
810
760
410
477
1544
4±4
0±53
0±50
0±14
24
7±1
Moro et al.—Biogeochemical Cycles in a Mediterranean EnŠironment
679
T     3. Annual litterfall (kg ha−") for Adenocarpus decorticans, Cistus laurifolius, Pinus pinaster and Pinus nigra from Jul.
1986 to Jun. 1989. Means³1 s.e. (n ¯ 3)
A. decorticans
C. laurifolius
P. pinaster
P. nigra
Leaves
Reproduction
Others
Total
553±3³115
391±9³22
586±3³86
695±9³74
251±9³96
53±6³11
89³11
61³48
126±4³60
21±9³10
6±1³1±5
5±2³3±2
933±7³219
477±4³35
681±2³86
762±1³69
T     4. Leaf}needle decomposition rates (k) calculated
from the exponential simple model in Pinus pinaster, Pinus
nigra, Adenocarpus decorticans and Cistus laurifolius. rw,
estimated percentage of initial weight remaining after 2 years
A
1.6
g m–2 d–1
1.2
0.8
n
r#
P!
rw (%)
®0±127a
®0±169b
®0±535c
®0±211d
24
24
24
26
0±83
0±92
0±85
0±90
0±001
0±001
0±001
0±001
73±5
65±6
26±4
60±3
0.4
P. pinaster
P. nigra
A. decorticans
C. laurifolius
0.0
Numbers superscripted by different letters are significantly different
(P ! 0±05).
7
10
1
4
7
10
1
4
7
10
1
4
7
1.2
B
1.0
0.8
g m–2 d–1
k (year−")
0.6
0.4
0.2
0.0
7
10
1
4
7
10
1 4
Months
7
10
1
4
7
F. 1. Monthly variation of leaf litterfall rate (g m−# d−") from Jul.
1986 to Sep. 1988 in the Nacimiento catchment. A, Pine species : (E)
Pinus pinaster : (D) Pinus nigra ; and B, shrub species : (E) Cistus
laurifolius ; (*) Adenocarpus decorticans.
0±005, n ¯ 36) for A. decorticans and r ¯ 0±70, (P ! 0±001,
n ¯ 36) for C. laurifolius.
Seasonal pattern of needle litterfall differed between the
two pine species (Fig. 1 A). Phenological abscission of P.
pinaster needles is concentrated in summer. Although needle
litter-fall in P. nigra eventually started in August, the
maximum needle fall was achieved in Oct. and overall, the
maximum rates in the period Sep. to Nov. As shown in Fig.
1 A, additional quantities of needles reached the forest floor
during the winter months in both species. It was observed
that only a small percentage of this litter was green material.
The rest was composed of senescent needles detached before
winter and which had become trapped among the lower
branches of individuals. Accidental factors, such as wind
and snow storms then lowered this material causing the
strong and irregular peaks.
The organic matter turnover in A. decorticans was about
twice that in C. laurifolius and three times higher than in the
pine layer (Table 1). Accordingly, mean residence time of
organic matter in the aerial parts was much longer in pines
and C. laurifolius. The faster carbon turnover in A.
decorticans with respect to the other species was also reflected
in its high decomposition rate (Table 4). The decay constant
(k) of A. decorticans leaf litter was significantly higher than
the other species [C. laurifolius (t ¯ 6±69, P ! 0±001), P.
pinaster (t ¯ 8±25, P ! 0±001), P. nigra (t ¯ 7±44, P ! 0±001)].
Consequently, 75 % of dry mass in recently fallen leaf litter
decomposed within 2 years against only 40 % in C.
laurifolius, 35 % in P. nigra and 27 % in P. pinaster
(Table 4).
Nitrogen
Distribution, requirements, uptake and atmospheric N
#
fixation. The major biogeochemical N fluxes and pools are
represented in Fig. 2 and Table 5. The largest store of total
N was the soil, though only 1 % was assumed to be plantavailable. The average soil pool of total N up to 30 cm
deep was 1740 kg ha−" for the overall watershed. Organic
layers accumulated 9 kg N ha−" of needle litter and 22 kg N
ha−" of shrub litter, 75 % corresponding to A. decorticans.
The total N storage in aerial biomass was 141 kg ha−"
year−". The shrub component contributed to the N aerial
pool with 71 kg ha−", as much as the pine layer (Fig. 2 A).
Annual pine requirements were 21 kg ha−" year−" covering
the maintenance costs and the annual aerial increment in the
N mass (including N in needle increment). N allocation to
perennial structures and foliage increment was 10±4 kg ha−"
680
Moro et al.—Biogeochemical Cycles in a Mediterranean EnŠironment
A
B
Rainfall 5·1
Rainfall 5·1
Foliar absorption (N–NO3) –0.4
Foliar absorption (N–NH4) –0·3
Washing dry dep. (N–NO3) 0·4
Leaching (N–NO3) 0·2
Biomass 70
Requirement 21
Allocation 10·4
Retranslocation 4·5
Washing dry dep.
Leaching
Net rainfall 0·6
Biomass 47
Requirement 23·3
Allocation 4·1
Retranslocation 1·1
Available soil
Litterfall 5·9
Net rainfall
0·3 (N–NH4)
Litterfall 17·8
N2
Fixation
1
Uptake 16·5
Mineralization
Available soil
17·4 ?
Runoff
Organic sources
0·6
Uptake 22·2
Litter 9·1
Mineralization >5·3
Available soil
17·4 ?
Mineral soil 1740
Runoff
Organic sources
0·6
Litter 16·5
Mineral soil 1740
C
Foliar absorption
Rainfall 5·1
–0·4 (N–NH4)
–0·3 (N–NO3)
Washing dry dep. 0
Leaching 0
Biomass 24
Requirement 7·6
Allocation 1·9
Retranslocation 3·4
Litterfall 2·3
Uptake 14·2
Available soil
17·4 ?
Runoff
Net rainfall 0
Mineralization
Organic sources
0·6
Litter 5·3
Mineral soil 1740
F. 2. N biogeochemical cycle in a catchment basis in the Nacimiento watershed. A, Pine layer ; B, A. decorticans population and C, Cistus
laurifolius population. Data are kg ha−" for pools and kg ha−" year−" for fluxes.
T     5. General parameters related to N use in Adenocarpus decorticans, Cistus laurifolius and the pine layer
Relative requirement (mg N g−" d.wt year−")
Turnover rate (Ln) (g N g−" N y−")
Mean residence time (MRTn) (year)
Leaf retranslocation (%)*
Retranslocation}requirement (%)
N mineralized from litter after 1 year (%)
N mineralized from litter after 2 years (%)
A. decorticans
C. laurifolius
Pines
4±7
0±38
2±6
25
4±7
30
50
0±67
0±09
10
67
45
®48
®46
0±35
0±087
11±5
48
21
®30
®61
* From Moro (1992).
year−" which represents a substantial percentage of annual
uptake. Return to the soil was 6±1 kg ha−" year−" accounting
for 8±7 % of N accumulated in the aboveground biomass of
the pine layer (Fig. 2 A). N in needle litter was immobilized
during the first year of decomposition and at least until the
end of the second year (Table 5). Pine uptake of N reached
16±5 kg ha−" year−". Consequently, requirement minus uptake budget was 4±5 kg ha−" year−" (21±4 % of the
requirements) which must be supplied by retranslocation
mechanisms (Fig. 2 A, Table 5). N resorption from old
Moro et al.—Biogeochemical Cycles in a Mediterranean EnŠironment
needles before abscission is a well-developed mechanism in
the pine layer as shown by its elevated foliar retranslocation
efficiency (48 % ; Table 5).
The amount of N stored in A. decorticans was 47 kg ha−",
about twice that accumulated by C. laurifolius (24 kg ha−"),
despite their similarity in the above-ground biomass (Table
1). Therefore, the nitrogen demand in A. decorticans was
much higher than C. laurifolius, as indicated by both the
absolute and relative requirements for this element (Fig. 2
and Table 5). The annual A. decorticans requirement
supplied by uptake and retranslocation accounted for
23±3 kg ha−" year−", similar to that found in the pine layer. A
relatively small percentage of foliar N (25 %) was reabsorbed
from old leaves before abscission in A. decorticans (Table 5).
As shown in Fig. 2 B and Table 5, retranslocation on a
catchment basis (requirements minus uptake) must supply
only 4±7 % of the requirements. Additional quantities of
nitrogen entered to the system through atmospheric N
#
fixation by A. decorticans nodules. The input by symbiotic
N fixation was estimated to be 1 kg ha−" year−", only 4±8 %
#
of Adenocarpus requirements. N return in this species was
very fast and accounted for 38 % of N stored in aboveground parts. The low rate of N conservation was reflected
by the high turn-over rate and consequently the lower MRT
of N (Table 5), being only 2±6 years in A. decorticans. The
comparison of MRT of organic matter and N in A.
decorticans shows that N is lost twice as fast as organic
matter.
The decay constant of N in A. decorticans leaf litter,
estimated by the exponential model, was ®0±31 year−" (r# ¯
0±81, P ! 0±001, n ¯ 26) and thus, about 50 % of the initial
mass of N in leaf litter could be mineralised at the end of the
second year in this species (Table 5). Considering only
current leaf litter-fall, amounts equivalent to 31 % of the N
available in mineral soil could be added after 1 year of
decomposition (Fig. 2 B).
Conservative C. laurifolius behaviour concerning N was
reflected in the relative and absolute N requirement (Table
5, Fig. 2 C). The absolute annual C. laurifolius requirement
was about three times lower that for A. decorticans. In C.
laurifolius, N was transferred mostly by retranslocation.
Leaf retranslocation efficiency before abscission was about
67 % in C. laurifolius (Table 5). Calculating the
retranslocation on a catchment basis (requirement minus
uptake), it was 45 % of the annual requirements (Fig. 2 C)
of the C. laurifolius population. Nitrogen MRT in aerial
parts was 10 years in C. laurifolius which is much longer
than in A. decorticans (Table 5). The return of N from
annual litterfall accounted for 2±3 kg ha−" year−" (9±7 % of
the total above-ground N pool) in C. laurifolius that was
immobilized for at least the first 2 years of decomposition
(Table 5).
Precipitation, net rainfall and streamflow. The annual
precipitation was 651 mm and streamflow output 85 mm
during the hydrological year 1988–1989 in the Nacimiento
catchment. The amount of mineral nitrogen in annual bulk
deposition was 5±1 kg ha−" year−" while only 0±6 kg ha−"
year−" were found in streamflow (Fig. 2). 68±6 % of the
mineral N in bulk deposition was as ammonium nitrogen
(N-NH ) and 31±4 % as nitrate nitrogen (N-NO ).
%
$
T
681
6. Nitrogen use efficiency in Adenocarpus
decorticans, Cistus laurifolius and pine layer
A. decorticans
C. laurifolius
Pines
A
1}Ln
NUE*
NUE†
23±6
32
45±6
2±6
10
11±5
62
320
524
52
207
230
* Calculated from Berendse and Aerts (1987) : NUE ¯ A 1}Ln
where : A ¯ N productivity (g d.wt g−" N year−") and Ln ¯ Turn-over
rate of N (year−").
† Calculated from Vitousek (1982) : Dry matter in litterfall}N in
litterfall.
Comparisons between bulk deposition and through fall
plus stem-flow fluxes indicated that foliar leaching or dry
deposition wash-off of N-NH occurred, while N-NO was
%
$
retained by A. decorticans canopies. It has been calculated
that foliar absorption contributes 0±40 kg ha−" year−" in an
available form (Fig. 2 B), while 0±3 kg ha−" year−" of N-NH
%
was leached from canopies of this species. N uptake from
rain has been shown to operate much more efficiently in C.
laurifolius than in A. decorticans (Fig. 2 C). Direct input of
available N to the C. laurifolius canopies from foliar uptake
accounted for 0±7 kg ha−" year−" (Fig. 2 C) and thus 9±2 % of
the annual N requirements. Through fall plus stem-flow
water from pine canopy had 5 % less N-NH than rainfall
%
but showed a net N-NO enrichment of 0±6 kg ha−" year−"
$
(Fig. 2 A) which was originated, mainly from dry deposition
wash-off.
Nitrogen use efficiency. Pines showed the highest NUE
among the species studied. NUE (Table 6) was about four
to five times higher in C. laurifolius than in A. decorticans,
depending on the method of calculation. The N productivity
of pines and Cistus was higher than Adenocarpus (Table 6).
However, differences in NUE were mainly caused by the
MRT of N in the former species exceeding that in
Adenocarpus considerably.
DISCUSSION
Organic matter
Early stages of forest development are mainly characterized
by an elevated investment in foliage production (Waring
and Schlesinger, 1985) for both maintenance costs and
increment on leaf area. In this study, the pine net production
is of the order of other slightly more mature pine forests in
the Spanish mediterranean area (CREAF, 1992) ; but the
foliar net production}total net production ratio is much
higher, reflecting an initial phase of rapid growth. The
pattern of above-ground biomass distribution found in the
pine afforestation studied is also typical of even-aged stands
during their early stages of development before maximum
leaf area is attained (Miller, 1995). The lack of data on
Spanish areas afforested with the same pine species makes
comparisons difficult. For other species, such as Pinus
halepensis Miller., Lledo! (1982) reported a similar biomass
distribution and relative foliar productivity figures for a
young stand in the semi-arid area of south-eastern Spain.
682
Moro et al.—Biogeochemical Cycles in a Mediterranean EnŠironment
Compared with data reported in the literature for other
pine species growing in the Mediterranean area (Dannaoui,
1981 ; Leonardi, Rapp and De la Rosa, 1988 ; Garcia Ple,
Vanrell and Morey, 1995), pine litterfall in this study seems
relatively low. However, litterfall is known to be affected by
a variety of factors (e.g. site quality, species, age, density
and rainfall), and this kind of comparison is thus difficult to
interpret. In the pines studied, organic matter turn-over was
0±08. According to Rodin and Bazilevich (1967), ratios from
0±07 to 0±12 are typical of immature plantations, while ratios
from 0±015 to 0±02 are characteristic of mature ones.
The total shrub ANPP is comparable to the 1100 kg ha−"
year−" given by Rapp and Lossaint (1981) for Quercus
coccifera garrigue in southern France. Specht (1969)
reported average production varying from 880 to 1500 kg
ha−" year−" in Mediterranean shrublands during the first 10
years of development, and Mooney (1981) 1100 to 2000 in
California chaparral. A similar ANPP (1800 kg ha−" year−")
was found by Puidefa! bregas et al. (1996) in sparse
formations of the woody legume Anthyllis cytisoides in
south-eastern Spain. In this study, the leaf production
accounted for about 50 % of the total aerial net production
in both shrub species. Similar percentages have been found
in a wide range of Mediterranean shrublands (Ma! rquez,
Nun4 ez and Escudero, 1989 ; Terradas et al., 1989).
Shrub litterfall accounted for 933 kg ha−" year−" in A.
decorticans and 477 kg ha−" year−" in C. laurifolius, lower
than for other Mediterranean shrub ecosystems (e.g. Gray
and Schlesinger, 1981 ; Rapp and Lossaint, 1981 ; Merino et
al., 1990 ; Nun4 ez-Oliveira et al., 1993). However, those data
refer to more mature stands. In other areas of the Filabres
range, annual litterfall in sparse formations of 13-year-old
Anthyllis cytisoides was found to be similar to A. decorticans
(1000 kg ha−" year−", Puigdefa! bregas et al., 1996).
Read and Mitchell (1983) pointed out that summer litterfall constitutes a generalized pattern in many perennial
Mediterranean species and is caused mainly by water stress
and high temperatures that favour the synthesis of abscissic
acid. The consistent pattern of summer leaf fall in three of
the species studied, and the significant correlation between
temperature and leaf litterfall shown by the shrub species,
support the hypothesis that leaf loss is related to an
incapacity for maintaining a specific amount of foliar
biomass under conditions of water stress. However, summer
litterfall may also be influence by other factors. For example,
in C. laurifolius it could also be favoured by leaf nutrient
retranslocation to the new flowers that appear in June, just
before the maximum leaf fall (Moro, 1992).
Autumn fall of P. nigra needles contrasts with the typical
fall during the dry period in other Mediterranean pine
species (e.g. Dannaoui, 1981 ; Garcia Ple et al., 1995). P.
nigra seems more akin to other temperate coniferous forests
that shed foliage during the autumn (Bray and Gorham,
1964 ; Gosz, Likens and Bormman, 1972). Leonardi et al.
(1988) pointed out a similar pattern in a natural forest of
Pinus laricio Poir., a subspecies of P. nigra Arnold., in Sicily.
These authors argued the possible lack of water stress due to
the high altitude in their study area, (1800 m above sea
level). However in this study, all species are located at a
similar altitude and, with the exception of P. nigra, all
presented summer leaf fall, apparently supporting the
existence of water stress. Thus, the autumn fall of P. nigra
needles could be related to genetic factors.
Nitrogen
Distribution, requirements, uptake and return. Data from
this study support the existence of retranslocation satisfying
some of the pine N requirements. It has usually been
suggested that virtually none of the plant N requirement is
met by retranslocation during the early stages of forest
development (see Gholz and Fisher, 1985 ; Carlyle, 1986).
However, increasing evidence (e.g. Nambiar and Fife, 1991 ;
Miller 1995) shows that retranslocation occurs at all stages
of development, even during early growth and is not only
associated with maturity. Our results show that this process
can supply a substantial percentage, (21 %), of the pine N
requirement, close to that found by Switzer and Nelson
(1972) in 20-year-old stands of P. taeda (39 %) or by
Helmisaari (1995) in a 15-year-old stand of P. sylŠestris
(30 %).
The low retranslocation efficiency described in A.
decorticans (both at the catchment and leaf scale) contrasts
with that found in Cistus. High leaf N content combined
with little foliar N resorption before abscission allows the
legume to produce leaf litter with low C}N which, in turn,
seems to be strongly related to the rapid weight loss and the
N mineralization from recently fallen leaves (Moro et al.,
1995). Catchment N retranslocation (requirement minus
uptake), accounted for 45 % of the C. laurifolius annual N
requirements (Fig. 2 C), similar to that found in other
sclerophyllous Mediterranean shrubs (Gray and Schlesinger,
1981). In C. laurifolius, the long life span combined with the
slow turn-over rate and the significant amount of
retranslocated leaf N reduces nutrient losses from litterfall
and facilitates nutrient redistribution within the plant.
These traits allow C. laurifolius to be relatively independent
of the soil compartment and thus have a more self-regulated
N cycle, favouring its conservation within the plant system.
Elevated foliar retranslocation efficiency and NUE appear
to be a general pattern for species of the Cistus genus. As
shown in Fig. 3, Cistus shrublands have the highest NUE
(Vitousek sense) of Mediterranean shrublands. Merino et
al. (1990) found about 78 % foliage N resorption before
abscission in C. libanotis and Nun4 ez-Oliveira et al. (1993)
found 70 % in C. ladanifer.
Precipitation, net rainfall and streamflow. The low mineral
N output in streamflow water (Fig. 2), reflecting strong
conservation of this element in the ecosystem (Domingo,
1991), is similar to that found in other unperturbed,
Mediterranean sclerophyllous forests such as Montseny and
Prades in north-eastern Spain (Terradas et al., 1989).
Interaction between plant canopy and rainfall N differed
substantially among the species studied. Anatomical,
chemical and morphological differences in plant surfaces
probably account for much of this variation (Domingo,
1991 ; Domingo et al., 1991). C. laurifolius canopies act as
sinks for nitrate and ammonium nitrogen showing foliar
uptake for all these forms of nitrogen (Domingo, 1991 ;
Domingo et al., 1991). As shown in Fig. 2 C, this direct input
Moro et al.—Biogeochemical Cycles in a Mediterranean EnŠironment
the water table as is the case in some woody legumes in arid
areas (Virginia, 1986), and N fixation in this study may thus
#
have been underestimated.
300
Dry mass/N ratio in litterfall
683
250
P
200
Cl
Concluding remarks
150
100
50
0
Ad
20
40
60
80
100
–1
N in litterfall (kg ha
120
140
–1
year )
F. 3. Nitrogen use efficiency expressed by the ratio dry mass}N in
litterfall as function of N in litterfall (kg ha−" year−") for different
ecosystems. Data from Rapp, Leclerc and Lossaint (1979), Dannaoui
(1981), Gray and Schlesinger (1981), Vitousek (1982), Schwintzer
(1984), Verdu! (1984), Merino (1986), Weber (1987), Wheeler et al.
(1987), Mayor and Roda! (1992), Nun4 ez-Oliveira et al. (1993) and this
study. Points toward the right on the x-axis correspond to tropical areas,
while Mediterranean and temperate areas are located to the left. (D)
Pine and other coniferous forests ; (*) Mediterranean holm-oak ; (+)
Mediterranean shrubs ; (_) Cistus spp. shrublands ; (y) N fixing
#
species. Ad, A. decorticans ; Cl, C. laurifolius, P, pine layer.
of available N to the C. laurifolius canopy accounted for an
appreciable percentage of its annual N requirements. NNO in net rainfall from pine canopies (Fig. 2 A) is
$
considered to originate mainly in wash-off of dry deposition
(Moro, 1992). Thus, internal leaching of nitrate nitrogen
from pine canopies only had a minor contribution to the N
return. Regardless of the interaction of rainfall with the
shrub and pine canopies, input from rainfall accounted for
substantial percentages of the annual N requirements of
species studied. However, because of the irregular rainfall
regime that characterizes the Mediterranean area, this
atmospheric input could be considerably reduced during
dry years.
Atmospheric nitrogen fixation. The maximum input from
N fixation in A. decorticans was estimated to be 1 kg ha−"
#
year−", which only represent 4±3 % of its annual N
requirements. This rate falls within the lowest range given
by Carlyle (1986) for leguminous species corresponding to
woody legumes. Other studies have shown that N fixation
#
in Australian woody legumes ranged form 0±1 kg ha−"
−
−
year " in dry, sparsely covered areas to 32 kg ha " year−" in
wet, densely covered areas (Hamilton et al., 1993).
The low fixation rate found in A. decorticans seems to be
due to its poor nodulation (Moro, 1992) rather than to low
nitrogenase activity (Moro et al., 1992). In legumes of semiarid and arid regions, an absence of the proper endophyte
frequently prevents nodule formation (West and
Klemedson, 1978). In A. decorticans, only young individuals
seems to be nodulated while in mature shrubs, root nodules
have been found only exceptionally on the surface root
system. It is also possible, however, that nodulation in older
A. decorticans shrubs might occur at deeper horizons near
The population of C. laurifolius studied in the
‘ Nacimiento ’ watershed revealed closed, self-regulated,
carbon and nitrogen conserving behaviour. This probably
makes this species less dependent on current nutrient uptake
and implies slower cycles of N and C in sites dominated by
C. laurifolius. Although C. laurifolius is not strictly
sclerophyllous, it shares most of the C and N strategies
described for typical evergreen sclerophyllous species which
usually colonise infertile or degraded soils (Read and
Mitchell, 1983 ; Carlyle, 1986). Moreover, similar trends
have been described for other Spanish Cistus shrublands
(Merino et al., 1990 ; Nu! n4 ez Oliveira et al., 1993). A.
decorticans has a higher potential growth rate, higher losses
and rapid turn-over of both C and N favoured by the greater
facility for decomposition of its litter. It possesses a more
open and thus, less efficient C and N cycle, being more
dependent on the soil system.
C and N cycle characteristics in the two shrub populations
are similar to those already described for other plant
communities growing in sites with contrasting nutrient
availability (Chapin, 1980 ; Aerts, 1989). The soils in the
study area are nutrient-poor, having low contents of organic
matter (ICONA, 1987). These traits seem more favourable
for species with closed and conservative cycles such as the
pine species or C. laurifolius, rather than for Adenocarpus.
However, microsites with contrasting fertility and clear
dominance of one or the other shrub species exist within the
watershed (Moro, unpubl. res.). C. laurifolius dominates on
the poorest and eroded soils, whereas A. decorticans grows
predominantly in less sloping microsites characterized by
deeper, wetter and more fertile soils. The dependence of A.
decorticans on the plant-soil system as well as its strong
nutritional demand probably allows it to maintain a dense
population only on the most fertile sites of the watershed.
Moreover, although their C and N use strategies are
opposite, both are included as pioneer species in moderately
acid soils of the supra-mesomediterranean climate of the
Betic mountains in southern Spain (Losa, Molero and
Casarles, 1986). Overall, these considerations suggest that
the coexistence of these two species in the watershed is
probably due to niche differentiation, but additional studies
(e.g. water use and nutrient cycles in specific microsites of
contrasting fertility) are needed to test this hypothesis.
In 1990 the pine canopy was nearing closure, and it is
generally accepted that it is at this point in forest development that the maximum nutrient demand is reached (Waring
and Schlesinger, 1985). Under these conditions, the sustainability and maintenance of the shrub species seems uncertain,
as it may be affected by the light deprivation and competition
with pines for water and nutrients. In recent years, a strong
degree of mortality, mainly in the oldest individuals of the
Adenocarpus population, has been observed. This mortality
is apparently supplanted by a considerable recruitment of
seedlings, the dynamics of which are so far unknown.
684
Moro et al.—Biogeochemical Cycles in a Mediterranean EnŠironment
Further research is needed to evaluate the evolution of the
A. decorticans population during and after canopy closure,
mainly their response to light deprivation and competitive
interaction with pines.
An interesting research topic for future management
would be the evaluation of net nitrogen balance in young A.
decorticans individuals in order to find out whether the soil
N pool below them increases significantly. If there were to
be a net gain in soil N, and canopy closure did not impede
maintenance of a dense population of young A. decorticans,
optimization of the seedlings with biotechnological manipulation, such as the mixed inoculation of selected
Rhizobia and mycorrhizal fungi (e.g. Herrera, Salamanca
and Barea, 1993), would be useful for building up a
productive understorey layer in forest reclamation
programmes.
A C K N O W L E D G E M E N TS
This work has been funded by the Commission of the
European Communities (Contract No. EV4V-0109-E) and
by ICONA-CSIC through the LUCDEME project. A.
Dura! n, C. Escarre! , S. Garcı! a, S. Ivars and N. Jimenez are
thanked for field assistance and sample processing. We are
also grateful to the laboratory of Plant Biology of Barcelona
University for soil analyses.
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