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Leaf shedding, crown condition and element return in two mixed holm oak forests in Tuscany, central Italy
Forest Ecology and Management 176 (2003) 273±285
Leaf shedding, crown condition and element return in two mixed holm oak forests in Tuscany, central Italy Filippo Bussottia,*, Francesca Borghinib, Carlo Celestib, Claudio Leonziob, Alberto Cozzic, Davide Bettinic, Marco Ferrettic a
Department of Plant Biology, University of Florence, Piazzale delle Cascine 28, I 50144 Firenze, Italy b Department of Environmental Sciences, University of Siena, Via Mattioli 4, I 53100 Siena, Italy c Linnaea-ambiente srl, Via G. Sirtori 37, I 50137 Firenze, Italy Received 19 September 2001; received in revised form 27 March 2002; accepted 13 May 2002
Abstract Litterfall (leaves, ¯owers, fruits, twigs) was collected every month in two mixed Mediterranean forests of Quercus ilex (holm oak) in central Italy differing for their ecological features: a mesic site (Colognole, CL) and a xeric one (Cala Violina, CV). The survey period lasted 8 years (1992±2000) at CL and 4 years at CV. Chemical analysis of the litterfall was performed in 1997 and 1998. In these 2 years living leaves were also collected for chemical analysis. The main ®ndings were: (i) the litter production was lower and the leaf percentage in the total litterfall was smaller at CV than at CL; (ii) the phenological behavior differed in the two sites and the leaves had greater longevity at CV, whereas at CL trees renewed their crown almost completely each spring; (iii) the chemical composition of the living leaves re¯ected the edaphic differences between the two sites; (iv) the chemical composition of the senescent leaves and the litter in the two sites was very different; (v) crown transparency and defoliation followed the same pattern of the leaf shedding; (vi) transparency was greater at CL, where the litter production was higher, because of the different shape of the crowns. The differences between the two study areas have been discussed in the light of the different ecology of the two sites, since leaf lifespan is greater in dry and infertile soils. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Bioelements; Crown productivity; Crown transparency; Defoliation; Leaf lifespan; Litterfall; Phenology; Mediterranean vegetation; Quercus ilex
1. Introduction Leaf lifespan is in¯uenced by environmental factors: in dry and infertile soils trees maintain their leaves longer than trees growing in more favorable conditions (Mooney, 1981; Gutschick, 1999). In unfavorable environments leaves develop thicker mesophyll and *
Corresponding author. Tel.: 39-055-3288369; fax: 39-055-360137. E-mail address: [email protected] (F. Bussotti).
cuticle (Margaris, 1981) and have high metabolic construction costs (in terms of photosynthetic energy demand) that can be compensated by means of their longevity. Besides, in adverse conditions evergreenness represents the way to exploit also short and sudden periods when photosynthesis is possible. In the Mediterranean environment the most favorable conditions for photosynthesis and metabolic activities are found during the equinoctial periods (spring and autumn), i.e. when in the deciduous broad-leaved trees the vegetative apparatus is lacking (De Lillis and Federici, 1993). On
0378-1127/02/$ ± see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 0 2 ) 0 0 2 8 3 - 9
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F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285
the other hand, during senescence leaves lose their physiological ef®ciency and the metabolic costs for their maintenance can be high. In favorable edaphic conditions foliar turnover is quicker than in infertile soils (Maurer et al., 1997). In Quercus ilex L. (holm oak) leaf lifespan is currently considered 2±3 years, but may be longer (4±5 years) under worse environmental conditions (Sabate et al., 1999). In Mediterranean stands with Q. ilex L. or other Mediterranean evergreen oaks (Quercus suber L., Quercus coccifera L.) leaf shedding does not occur at a single time during the year: alongside the usual springtime peak, there is normally also a loss of leaves in autumn and winter (Rapp, 1969; Poli et al., 1970; Rapp and Lossaint, 1981; Arianoutsou, 1989; Bellot et al., 1992; Escudero et al., 1992; Hernandez et al., 1992; Oliveira et al., 1994; MartõÂn et al., 1996). Leaf shedding affects the whole mineral nutrient cycle. In the oligotrophic Mediterranean ecosystems, ef®ciency in nutrient use (see Gallardo et al., 1999), i.e. the biomass production by plants (in terms of ®xed C) per unit of nutrient uptake, is presumably a response to decreased soil nutrient availability. Resorption, i.e. the translocation by young tissue of nutrients from senescent tissues such as mature leaves, is a means of re-using the same elements. Within a programme aimed at assessing forest condition in Tuscany (MONITO, Intensive Monitoring of Forest in Tuscany, see Bartolozzi et al., 1996; Ferretti et al., 1999) an apparent anomaly was detected in the phenological pattern of Q. ilex trees in some permanent areas of the regional monitoring network (Bussotti et al., 1995), where the plants renewed their crown completely each year and therefore carried almost exclusively current-year (C) leaves. The aim of the present survey was to ascertain whether such a pattern was determined by natural ecological factors (such as climate, availability of water and nutrients) or was to be considered a pathological stress condition. The selected areas are to be considered as a ``case study'' and do not claim to represent the whole Q. ilex population in Tuscany. 2. Materials and methods 2.1. Study areas The study areas are Colognole (CL) and Cala Violina (CV), both located in Tuscany, near the Tyr-
rhenian coast. The distance between the two plots is about 100 km. In both, the forest vegetation consists of an adult (40±60 years) holm-oak stand mixed with different broad-leaved species (see Table 1); the canopy is fully closed, the soil is deep and the morphology nearly ¯at. CL is characterized by a high water table, spatially irregular trend always in the root zone, guaranteeing a constant water supply even in the warmest and driest months. The CV stand, on the other hand, grows in very xeric conditions, with 5 months of water de®cit in the soil (Bigi and Rustici, 1984). In
Table 1 Characteristics of the study areas (Bigi and Rustici, 1984; Cozzi, 1996; Anonymous, 1998; Bussotti et al., 2000, 2002)a
Physical features UTM X UTM Y Altitude (m a.s.l.) Exposure Slope (%) Bedrock Tree features Main species Other species Age of the dominant trees (years) Stem ha 1 (Q. ilex, %) Basal area, m2 ha 1 (Q. ilex) Mean diameter, cm (Q. ilex) Height of the dominant trees (m) Meteorological data Mean annual rainfall, mm (historical mean 1955±1974) Mean annual temperature, 8C (historical mean 1955±1974) Data on soil (0±20 cm depth) pH N (%) P2O5 (%) K2O (%) Ca (%) Mg (%)
CL
CV
1616000 4818480 250 NE Variable Claiey Schist; Ophiolitic
1645300 4745700 5 N±NW 5 Sandstone
Q. ilex Q. pubescens A. unedo Q. crenata 40±60
Q. ilex Q. pubescens A. unedo F. ornus 40±60
1545 (39) 16.7 (6.2) 16.7 (19.5) 15±18
2080 (69) 13.4 (5.9) 13.4 (14.9) 15±18
978
637
14.7
15.1
5.9 2.0 17.5 0.5 2.5 32.3
5.7 1.3 25.5 1.4 19.3 2.4
a The ®gures exclusively relative to Q. ilex are given in parenthesis.
F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285
275
Fig. 1. Daily pattern of temperatures (minimum and mean) during December 1996.
August, after a prolonged dry period, the pre-dawn water potential (C) was 0.6 MPa at CV and 2.7 MPa at CL (Bussotti et al., 2002). Data on the meteorological behavior during the study period are available in Bussotti et al. (2000). Climate has a regular Mediterranean pattern in both sites, and the most important anomaly occurred in the last days of December 1996 with a sudden drop of temperature (Fig. 1) that was more pronounced at CV than CL. In both sites the mean daily temperature was below 0 8C for four consecutive days. The distance from the sea is about 5000 m for CL and only 200 m for CV. 2.2. Collection and analysis of samples The abscission of leaves, twigs, ¯owers and fruits was monitored from April 1992 to March 2000 at CL and from April 1996 to March 2000 at CV. In each study area nine litter traps were positioned according to a square grid with sides 10 m wide 3 3. Each litter trap had a collecting surface of 0.5 m2. They were emptied monthly and the litter collected was divided according to tree species and biological matrix (leaves, ¯owers, fruits, twigs). Dry weight of samples was determined (DW 72 h at 65 8C). Each time both DW and total surface (using an areameter LI-3100 Licor, Lincoln, NE) were measured on a sub-sample of
100 leaves for each of the main species (Q. ilex L., Quercus pubescens Willd., Quercus crenata Lam. and Arbutus unedo L. at CL; Q. ilex, Q. pubescens, Fraxinus ornus L. and A. unedo at CV). Leaf mass per area (LMA) was calculated as dry weight/leaf area (mg cm 2). This parameter allowed us to calculate the leaf area index (LAI) of the leaf litterfall. A subsample for each matrix was prepared every 3 months in the period 1997±1998. Crown transparency and defoliation were assessed visually both at CL and CV, on the same 30-tree sample in each area, according to the standard criteria used in the transitional network for forest condition assessment (ICP-Forests, see UN-ECE, 1994). Both these parameters are de®ned by a percent scale with 5% steps. Zero indicates an intact crown, whereas the value 100 indicates a crown without leaves. The transparency, de®ned as the percentage of gaps in a tree crown observed against the sky, was assessed monthly during the period July 1996±December 1998 using photographic references for Mediterranean trees (Ferretti, 1994). Defoliation rates were also assessed between July 1996 and April 1998. That assessment was based on the estimation of the number of years of leaves present in the crown. The French protocol (Chenal et al., 1997), in the case of several evergreen species, suggests that the absence of the
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F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285
previous-year leaves C 1 be considered as 20± 40% defoliation, and the absence of C 2 leaves as 15±20%. C leaves can be partially lacking because of dead branchlets, insects or other causes. Foliar nutrients were analyzed according to the methods and criteria used in the forest health assessment programmes (UN-ECE, 1994). During the 1997± 1998 and 1998±199 growing seasons, C living leaves were sampled four times: June (just after sprouting), August, February and April. C 1 leaves (senescent leaves) were also collected in August. Five sample trees were selected in each plot according to the standard procedures (UN-ECE, 1994). For each tree, 40 g of leaves were collected (10 g from the four different azimuth orientations) in the upper third of the crown and were pooled to obtain a composite sample for each tree. After collection, the samples were placed in polyethylene bags and stored in a refrigerated box until they reached the laboratory (that same day). About 150 mg of dry matter were mineralized in clean Te¯on vessels with 3 ml of HNO3 at 120 8C for 8 h. Each digestion included at least one blank test.
Analytical determinations were performed by atomic absorption spectrometry (AAS). An air±acetylene ¯ame (2280, Perkin-Elmer) was used for Ca, K and Mg. Pb was determined by electrothermal atomic absorption spectrometry with Zeeman background correction (ZETAAS). Al, B, Cu, Fe, Mn, Na, P and S were assayed by inductively coupled plasma atomic emission spectrometry (ICP/EAS; Plasma 400, Perkin-Elmer). Nitrogen was analyzed according to the Kjeldhal method (UN-ECE, 1994). Each determination was done in three replicates. The accuracy of analytical procedures was checked by simultaneous digestion and analysis of standard reference materials (SRMs). SRMs 1572 ``citrus leaves'' and 1547 ``peach leaves'' from the National Institute of Standards and Technology (NIST, Gaithersburg, MD) were used. Batches with accompanying SRMs outside the certi®ed range were repeated. Element concentrations were determined by the standard methodologies reported by UN-ECE (1994). Standard solutions of inorganic elements were prepared by serial dilution of stock standard solutions containing 1 g l 1 of the
Table 2 Yearly ¯uctuation of the shed biomass, according to the different matrices, from April to March of the following year Leaves 2
CL 1992±1993 1993±1994 1994±1995 1995±1996 1996±1997 1997±1998 1998±1999 1999±1990 Mean Standard deviation CVa (%) CV 1996±1997 1997±1998 1998±1999 1999±1990 Mean Standard deviation CV (%) a
2
Woody parts (g m 2)
Flowers (g m 2)
Fruits (g m 2)
Other (g m 2)
Total (g m 2)
Q. ilex (g m )
Other species (g m )
358 335 235 303 372 255 223 372
143 114 131 204 158 129 144 141
110 95 103 157 145 211 125 120
10 17 3 36 12 23 24 24
19 20 85 44 79 15 119 31
35 37 39 36 37 46 31 28
677 620 598 782 806 681 669 719
307 61 20
145 26 18
133 37 28
19 10 54
52 38 74
36 5 14
694 72 10
156 143 222 116
84 65 87 66
156 150 81 168
10 17 6 3
206 22 15 11
49 49 26 21
664 450 439 387
159 44 28
76 11 15
139 39 28
9 6 67
64 95 148
36 14 40
485 122 25
Standard deviation/mean (coef®cient of variation).
F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285
277
Table 3 Leaf characteristics CL Area of one leaf of Q. ilex LMAa Q. ilex leaves (mg cm 2) Total leaf area shed (m2 m 2) Q. ilex (LAI) Other species (LAI) All species (LAI)
CV
P
6.63 0.59 16.87 1.48
5.97 0.56 17.09 0.83
**
1.80 0.37 1.20 0.23 3.00 0.59
1.06 0.24 0.78 0.12 1.84 0.34
n.s.b *** *** ***
a
Leaf mass per area. Difference not signi®cant. ** P < 0:01. *** P < 0:001. b
element to be determined (Spectrosil, BDH). Concentrations were expressed as percent of DW for macronutrients (N, S, P, Ca, Mg, and K) and in mg g 1 for microelements (Na, Fe, Mn, Zn, Cu, Al, B and Pb). 3. Results 3.1. Litterfall The mean quantity of litter shed yearly in CL was 694 g m 2 (Table 2). The most represented matrix in this litter were the leaves (65% of the total litter production); out of this total, about 307 g m 2 were
Q. ilex leaves (68% of all leaves), followed by those of Q. pubescens (8.5%), Q. crenata (7.5%) and A. unedo (5%). The remaining 11% was the contribution of several deciduous broadleaves (Ostrya carpinifolia Scop., Ulmus minor Mill., Sorbus torminalis (L.) Crantz., Quercus cerris L., F. ornus L.). Among the other matrices of the litter, woody parts made up 19% of the total shed biomass; ¯owers (male catkins from oak species) 2.7%; and fruits (acorns) 7.3%. The remaining 6% consisted of other materials (residues). At CV (Table 2) the yearly litter shed was considerably lower (485 g m 2) and leaves (235 g m 2) represented only 48% of the total. Q. ilex leaves (159 g m 2) were 70% of all leaves, followed by Q.
Fig. 2. Abscission pattern of Q. ilex leaves, represented by the monthly DW for the period 1996±2000 (in percent of year total).
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F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285
Fig. 3. Yearly abscission pattern of Q. ilex leaves, represented by the average monthly DW for the period 1996±2000 (in percent of year total).
Fig. 4. Monthly pattern of (A) crown transparency and (B) crown defoliation (July 1996±December 1998) in the two areas.
pubescens (16%), F. ornus (12%) and A. unedo (2%). Other species were negligible. Wood represented an important fraction (29%); followed by acorns (13%) and ¯owers (2%). Residues were 8%. In both sites
there were considerable variations in the shedding rates, both in total quantities and between different matrices, from one year to the next (Table 2). The most variable matrices were acorns and ¯owers. Table 3
Fig. 5. Correlation between crown transparency and leaf shedding at (A) CL and (B) CV.
Table 4 Element concentrations in the litter matricesa,b Matrice
N (%)
Q. ilex leaves
S (%)
P (%)
Ca (%)
Mg (%)
K (%)
Na (ppm)
Fe (ppm)
Mn (ppm)
Zn (ppm)
Cu (ppm)
Al (ppm)
B (ppm)
1.27 0.22 0.13 0.02 0.05 0.01 0.46 0.07 0.33 0.04 0.40 0.13 212 60.5 99.5 29.2 109 20.4 15.7 2.71 0.96 0.27 0.11 0.02 0.05 0.01 0.89 0.13 0.20 0.02 0.37 0.08 486 181 214 69.9 1708 246 29.0 1.95
Q. pubescens leaves
CL CV
1.35 0.41 0.13 0.02 0.06 0.04 0.65 0.24 0.66 0.14 0.39 0.29 279 134 1.35 0.43 0.13 0.02 0.07 0.05 0.68 0.14 0.29 0.05 0.48 0.23 695 386
98.8 50.9 199 49.7
101 21.3 15.0 4.80 488 117 21.0 3.85
6.53 1.86 91.4 35.3 46.2 14.2 1.18 0.73 5.54 2.39 182 65.2 72.5 23.9 0.77 0.48
A. unedo leaves
CL CV
0.98 0.37 0.10 0.02 0.06 0.02 0.86 0.11 0.50 0.07 0.52 0.14 243 151 0.92 0.31 0.09 0.03 0.06 0.02 1.34 0.12 0.36 0.07 0.39 0.09 366 179
104 42.7 121 41.3
12.1 2.6 33.2 6.85 100 99.6 37.3 5.73
2.44 0.77 3.35 0.63
108 48.8 47.8 11.3 0.94 0.41 103 29.9 44.7 7.0 0.41 0.17
***
***
***
***
***
**
*
***
***
***
*
***
***
***
***
***
**
**
5.76 1.07 73.9 23.3 21.2 7.5 3.92 0.90 232 73.5 39.8 3.1
Pb (ppm)
CL CV
***
***
***
*
***
0.89 0.27 1.12 0.34
**
**
Q. crenata leaves
CL
1.22 0.37 0.13 0.03 0.06 0.02 0.70 0.23 0.56 0.14 0.28 0.15 299 150
135 45.4
217 97.7 16.1 2.05
6.22 1.66
125 31.4 44.4 13.8 1.23 0.32
F. ornus leaves Flowers
CV
1.64 0.14 0.19 0.07 0.08 0.02 1.45 0.43 0.34 0.09 0.71 0.41 276 102
198 86.6
144 65.9 16.4 3.94
4.40 0.96
175 63.4 20.9 5.4
1.09 0.63
CL CV
1.80 0.28 0.16 0.04 0.11 0.03 0.48 0.14 0.33 0.05 0.73 0.38 340 161 1.60 0.53 0.12 0.02 0.09 0.01 0.61 0.09 0.21 0.03 0.50 0.34 415 124
283 212 354 162
78.4 26.1 23.7 7.45 664 89.3 30.5 8.31
13.9 3.98 10.4 0.37
299 247 338 123
21.9 6.0 27.2 2.8
3.17 2.27 1.98 1.19
CL CV
0.66 0.18 0.06 0.02 0.05 0.03 0.23 0.09 0.19 0.06 0.49 0.23 131 134 0.65 0.22 0.06 0.02 0.06 0.02 0.41 0.18 0.15 0.07 0.46 0.27 255 126
68.2 58.4 89.9 65.7
33.7 13.4 9.72 3.66 359 245 11.2 4.21
6.93 1.49 49.7 24.6 11.5 5.3 5.30 2.40 76.3 71.9 15.7 4.5
0.42 0.25 0.34 0.17
CL CV
0.69 0.21 0.08 0.02 0.03 0.01 0.40 0.11 0.25 0.05 0.32 0.32 154 48.4 0.72 0.15 0.08 0.01 0.04 0.01 1.18 0.25 0.17 0.03 0.33 0.04 465 112
121 75.4 278 222
63.0 21.7 17.7 6.68 509 122 24.2 5.11
7.41 1.84 7.86 0.87
3.45 2.02 3.72 2.51
Fruits
Woody parts
a b *
*
***
***
**
***
***
**
**
Asterisk represent the signi®cance of the differences between the two sites (in the same column). Mean values and standard deviation of the years 1997±1998 (no. of samples 8). P > 0:05.
**
P > 0:01.
***
P > 0:001.
***
*
***
***
***
*
*
*
*
*
116 57.6 14.6 4.0 209 123 22.3 2.3 *
***
Table 5 Element concentrations in living leavesa,b
June
August
February
April
c
C1
a b c *
N (%)
S (%)
P (%)
Ca (%)
Mg (%)
K (%)
Na (ppm)
CL CV
2.02 0.21 1.35 0.15
0.14 0.02 0.12 0.01
0.21 0.02 0.07 0.01
0.14 0.06 0.49 0.06
0.26 0.03 0.14 0.03
1.31 0.11 0.49 0.08
56.2 16.7 261 130
66.2 20.0 115 55.8 66.2 30.9 1150 307
21.6 1.3 9.48 2.77 21.1 4.19 4.63 1.13
CL CV
1.39 0.06 1.46 0.12
0.11 0.01 0.12 0.02
0.09 0.01 0.08 0.06
0.27 0.06 0.56 0.11
0.28 0.02 0.20 0.02
0.66 0.06 0.68 0.06
206 25.3 191 50.0
56.9 15.4 219 119 93.0 11.8 1156 430
13.42 2.30 4.28 0.82 19.7 4.5 5.53 0.57
CL CV
1.38 0.05 1.31 0.16
0.11 0.01 0.15 0.02
0.09 0.02 0.08 0.01
0.41 0.09 0.75 0.20
0.35 0.12 0.17 0.05
0.32 0.03 0.45 0.14
CL CV
1.41 0.17 1.59 0.11
0.14 0.02 0.16 0.02
0.10 0.02 0.09 0.02
0.62 0.07 0.80 0.08
0.41 0.08 0.15 0.03
0.52 0.19 0.44 0.05
191 84.4 210 68.2
103.2 43.5 334 72.7 217 58.4 1642 380
CL CV
1.30 0.13 1.22 0.03
0.12 0.01 0.12 0.01
0.07 0.01 0.06 0.02
0.48 0.01 0.86 0.22
0.30 0.07 0.18 0.06
0.52 0.05 0.41 0.06
205 132 310 25.6
114 59.5 668 922 165 46.3 1664 303
***
*
*
*
***
***
***
***
**
***
***
***
***
***
***
***
**
**
***
150 49.6 256 102
*
**
Asterisk represent the signi®cance of the differences between the two sites (in the same column). Mean values and standard deviation of the 1997±1998 and 1998±1999 growing seasons (no. of samples 10). C 1 leaves were collected in August. P > 0:05.
**
P > 0:01.
***
P > 0:001.
Fe (ppm)
M (ppm)n
Zn (ppm)
***
**
***
91.1 54.0 233 56.1 224 161 1646 538
***
***
*
***
***
***
Cu (ppm)
**
**
*
*
*
*
15.5 8.3 4.17 0.39 21.1 6.58 4.61 0.8
Al (ppm)
B (ppm)
Pb (ppm)
20.0 5.4 17.63 4.30 0.21 0.09 80.5 28.4 27.8 9.00 0.49 0.20
***
***
*
23.70 6.70 23.82 3.30 0.20 0.12 57.0 12.1 41.64 3.81 0.32 0.29 ***
***
*
99.2 64.6 24.56 10.2 1.09 0.29 238 186 42.8 9.80 1.18 0.64
***
**
14.7 4.1 4.52 0.61 27.4 11.4 4.83 0.41
106.6 45.0 32.30 9.94 1.14 0.27 229 76.5 48.6 7.33 1.05 0.30
18.7 9.6 9.24 13.7 27.4 6.69 5.76 3.19
117.0 88.8 30.0 16.6 1.18 0.39 183.7 72.4 48.90 13.3 0.77 0.32
***
*
**
*
*
Table 6 Yearly total amount of elements in the litter sheda
CL Overall litterfall 67.16 (yearly mean) Singular matrices (yearly mean) Q. ilex leaves 32.81 Q. crenata leaves 3.09 Q. pubescens leaves 4.30 A. unedo leaves 2.05 Other species leaves 7.32 Woody parts 9.10 Flowers 4.57 Fruits 3.92 CV Overall litterfall 33.28 (yearly mean) Singular matrices (yearly mean) Q. ilex leaves 14.57 Q. crenata leaves 4.66 Q. pubescens leaves 4.91 A. unedo leaves 0.15 Woody parts 6.31 Flowers 1.40 Fruits 1.27 a
7.16
2.95
31.59
24.03
29.41
1464
692
604
112
42
583
154
8.5
3.51 0.35 0.44 0.23 0.99 0.96 0.33 0.35
1.18 0.14 0.16 0.11 0.34 0.45 0.25 0.31
13.75 1.92 2.99 1.97 3.79 5.27 0.83 1.07
9.45 1.58 2.86 1.18 3.50 3.53 0.88 1.04
10.88 0.80 0.87 1.14 3.62 6.74 2.11 3.25
649 82 145 49 193 200 95 46
316 36 29 22 88 130 3773 40
352 58 41 2 288 85 21 20
45 448 5 816 16.45 23 4 5
15 1.7 2.1 0.5 4.9 10 2.98 4.69
231 37 36 24 72 127 37 21
52 12 20 11 19 233 6.2 10
2.8 0.35 0.37 0.21 0.83 3.5 0.38 0.14
3.88
1.67
35.54
7.89
13.98
1826
749
3663
87
18
715
133
5.9
1.59 0.74 0.58 0.02 0.70 0.12 0.12
0.60 0.23 0.21 0.01 0.38 0.12 0.13
13.84 5.37 3.46 0.26 11.04 0.66 0.91
3.02 1.21 1.32 0.08 1.67 0.25 0.33
5.35 1.61 1.76 0.07 2.87 1.06 1.26
758 89 439 7 430 39 61
3347 59 85 3 229 21 162
2755 394 2339 230 481 85 65
44 4.6 8.9 0.7 22 2.7 2.1
6.0 1.2 2.0 0.06 6.9 1.2 1.0
353 54 84 2.4 179 25 14
58 6.3 39 0.9 21 3.2 3.2
1.8 0.27 0.21 0.01 3.4 0.15 0.06
F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285
N S P Ca Mg K Na Fe M Zn Cu Al B Pb (kg ha 1) (kg ha 1) (kg ha 1) (kg ha 1) (kg ha 1) (kg ha 1) (g ha 1) (g ha 1) (g ha 1) (g ha 1) (g ha 1) (g ha 1) (g ha 1) (g ha 1)
Mean value of the 1997±1998 and 1998±1999 growing seasons.
281
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shows the leaf area development at the two sites: at CL the surface of a single leaf was greater than at CV; LAI is greater at CL than CV. Figs. 2 and 3 show the pattern of the monthly leaf abscission. At CL there was a very rapid spring defoliation followed by a complete crown renewal. The yearly leaf shedding was concentrated in May (53%), and during the spring (April±June) 75% of leaves fell. Only a small secondary peak (8±9%) was detectable between December and January. At CV, on the other hand, the renewal of the crown occurred more gradually during the growth season. The spring abscission started earlier (15% in April) and remained constant until June (35% of leaves lost in the period April±June). A secondary peak was evident in autumn (October±November) with the 18% of total leaves fallen. After the drop of temperature registered in December 1996, the winter abscission increased dramatically at CL but not at CV. The assessment of crown transparency registered the same pattern as the litterfall (Fig. 4A and B). The correlation between crown transparency and shed foliar biomass in the same month was found to be signi®cant in both sites, with P < 0:001 (Fig. 5A and B). At CL crown transparency reached very marked peaks in May, but recovered quickly with the new foliage; after the frost in December 1996 transparency increased. At CV crown transparency was more or less constant throughout the year, with small peaks in springtime. The transparency values were higher at CL than CV. Defoliation values were higher than transparency values (Fig. 4B), and the differences between the two sites were less marked. At CL defoliation correlated strongly with transparency (P < 0:001; r 0:94), but at CV that correlation was not signi®cant r 0:34. 3.2. Element return The chemical composition of the various litter matrices was different in the two sites (Table 4). Compared to CL, the holm-oak leaves at CV had lower concentrations of N, Mg, K, Cu and a greater amount of Ca, Na and several microelements such as Fe, Mn, Zn, Al, and B. Litter composition differed from that of the living leaves (Table 5). At CV, the N concentration decreased in senescent and dead leaves; the same happened for P and K. The opposite trend was detectable for Ca, Na, Fe, Mn, Al and Pb. At CL,
on the other hand, no signi®cant differences were found in N concentration between living and dead leaves, while P, K and Mn were lower in the litter. Finally Ca, Fe, Al and Cu concentrations increased with age in living leaves, but their concentration remained constant, or was slightly reduced, in the litter. Among the different leaf species, the highest N concentrations were reached in the deciduous trees (F. ornus and Q. pubescens), whereas the lowest were found in A. unedo. Among all the different components of the litter, nitrogen was highest in ¯owers and lowest in fruits and wood. Several differences were site-speci®c, without distinction of matrix: Mg was generally higher at CL, whereas Ca, Na, Fe and Mn were higher at CV. The return of the elements to the soil via litterfall was determined by the yearly amount of litter produced and their concentration values (Table 6). Most of the elements were more abundant at CL because of the greater amount of litter; but the total amount of calcium, sodium, iron, manganese and aluminum was more abundant at CV, because all these elements were present in higher concentrations. 4. Discussion In spite of similar age and basal area, the two sites differed in crown productivity (Table 2). Overall, the litterfall values fell within the range established by other authors (Rapp, 1969; Poli et al., 1970; Rapp and Lossaint, 1981; Arianoutsou, 1989; Bellot et al., 1992; Escudero et al., 1992; Hernandez et al., 1992; Oliveira et al., 1994; MartõÂn et al., 1996; RodaÁ et al., 1999). In particular, behavior at CV was similar to the more xeric stands described by Arianoutsou (1989), whereas the CL values were consistent with those reported by Rapp (1969) for a number of temperate forest ecosystems. At CV the similar basal area is subdivided into a greater number of stems than CL, but has a lower amount of litter production. The differences between CV and CL became more evident when considering only the foliar fraction of the litter. In fact, at CV leaf production was barely more than half the leaf production at CL, whereas woody parts (branches) in the litterfall were more abundant. These differences may be ascribed to the more xeric conditions at CV.
F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285
Mooney (1981), for example, stated that in a xeric environment the production of supporting organs (as branchlets) is more pronounced than the production of living tissues (leaves). The xeromorphic adaptation of the CV Q. ilex trees was detectable also in the leaf morphology, since the leaves collected at this site were smaller. Their LMA was not higher at all, but in previous research studies signi®cant differences were found between the two sites (Bussotti et al., 2000, 2002). These discrepancies are explained by the different methods of sampling, in fact in the previous works only sun leaves, from the upper part of the crown, were considered. The timing of abscission was also examined in the two areas. Leaf turnover was quicker at CL: abscission occurred practically all at once, at the same time as the ¯ushing, and C leaves were almost completely shed. On the other hand, at CV a large percentage of leaves survived the summer period and were shed in autumn. The scienti®c literature (Rapp, 1969; Poli et al., 1970; Rapp and Lossaint, 1981; Arianoutsou, 1989; Bellot et al., 1992; Escudero et al., 1992; Hernandez et al., 1992; Oliveira et al., 1994; MartõÂn et al., 1996) reports several ®ndings concerning the leaf shedding and phenology of Q. ilex and other Mediterranean evergreen species. It is usually assumed that most of the abscission occurs during the spring months, although a secondary peak during the autumnal and winter months is also detectable. Neither study site was an exception to this trend, but the relative importance of the main peak (spring) and the secondary one (autumn) was very different. This was due to the different ecological conditions of the two stands. In fact, in the xeric stand the leaves displayed a greater longevity than in the mesic one. At CL the availability of water in the soil allows for photosynthetic activity during the summer months (see Bussotti et al., 2002); thus, a complete crown turnover in the spring represents an advantage for the overall effectiveness of the tree. Bussotti et al. (2002) suggested that the phenological behavior in the two sites could be attributed to the different pattern of starch storage and metabolism: the CV holm-oak trees were in fact well-supplied with starch in their branchlets, whereas the CL trees did not present those same reserves. Larcher and ThomaserThin (1988) observed in several Mediterranean sclerophyllous species that large quantities of starch were stored in all the above-ground organs. Starch is utilized
283
during the period of summer drought and during the severest winter cold spells as a source of osmolytes to control the depletion of cellular water. The lack of starch reserves at CL may be explained by the fact that in this site the resources were used mainly for growth (leaf and litter production are clearly greater), whereas at CV they were used as protection against stress factors. This makes the CL Q. ilex more sensitive to winter conditions, explaining also the sudden and marked defoliation which was observed at CL after a sudden temperature drop in December 1996 (Figs. 1 and 2). During the same period at CV, even with similar or colder minimum temperatures, no leaf damage or defoliation occurred. Crown transparency and defoliation trends matched leaf abscission trends fairly closely, with marked variations at times of greater leaf turnover, especially at CL. Transparency and defoliation changes were closely correlated at CL, whereas at CV there were practically no differences between the different dates of observation. This suggests that the two parameters (transparency and defoliation) are mutually compatible and yield the same type of information in relation to variations over time. Defoliation values were always higher than transparency values. The reduction in the number of leaf-years carried by the crown is usually considered the most important parameter in evaluating the vitality of an evergreen tree (UN-ECE, 1994). The ®ndings of this study indicate that the loss of leaves at CL is quickly followed by a complete renewal of the crown and that the canopy has a high productivity, but, on the other hand, the foliage appeared to be more sensitive to climatic stress (frost, in this case). As far as the differences between the two sites are concerned, transparency reached higher values at CL than at CV, whereas differences in defoliation levels were only slight. Comparing data on crown condition (transparency and defoliation) to data on crown productivity and LAI (Tables 2 and 3), it is interesting to note that transparency is lower in conditions of more severe water stress (CV), conditions in which crown productivity is also lower. The explanation probably lies in the different shape of the crowns that trees develop in adapting to different levels of water availability: at CL crowns are broader, although less dense, whereas at CV they are narrower but denser. The elemental composition of the living leaves con®rms the results of Bussotti et al. (2000). Among
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the macronutrients, the differences in Mg (more abundant at CL) and Ca (more abundant in CV) re¯ects the different soil supply in the two study areas. The nutrient supply varies during the year (cf. Robert et al., 1996; Oliveira et al., 1996). Calcium increased in senescent leaves and in the litter according to a behavior consistent with that described by Fink (1991), Bergmann (1992) and Cenni et al. (1998). At CV Ca probably originates from the sea. Calcium carbonate is in fact one of the most important components of sea salt. Sodium concentrations also increased with the leaf age at CV, probably due to the closeness of the site to the sea shore. Other elements such as P and K (and N at CL) showed the opposite trend, being lower in the litter than in the living leaves, thus suggesting the occurrence of translocation processes (Escudero et al., 1992; Gallardo et al., 1999; Escarre et al., 1999) that are more ef®cient in xeric areas (Gallardo et al., 1999). The litter foliar composition of the different species showed that deciduous trees (Q. pubescens, but mostly F. ornus) generally had higher concentrations of many elements than evergreen ones. The composition of the different matrices (acorns, ¯owers, woody parts) was consistent with the ®ndings of MartõÂn et al. (1996), con®rming that ¯owers have the highest element concentrations. With regard to the total bioelement return, the results were consistent with those of other authors (Rapp, 1969; Arianoutsou and Paraskevopoulos, 1992; MartõÂn et al., 1996; Escarre et al., 1999). Their amount depended in most cases on the amount of litterfall, and they were generally more abundant at CL, with the exception of Ca, Na, Fe, Mn and Al. In these latter elements the ``concentration factor'' was more important than the quantity of litter. Leaves were the most important vector for element return. 5. Conclusions In evergreen trees a full loss of leaves may occur as a consequence of severe stress factors, such as drought, frost, attack of defoliator insects or effect of pollutants. During the study period in the two sites the most important stress event we detected was the frost in December 1997, that caused a nearly complete defoliation of holm oak trees at CL but not at CV. The
spring loss of leaves at CL appears to be connected with the ecological adaptation of holm oak in these speci®c site conditions. In this study the parameter that most aptly describes the ecological differences between the two sites is crown productivity, expressed as litterfall (g of dry matter per m2) or as LAI. Crown transparency is determined by the architecture of the crown and the distribution of the foliage, and is a consequence of site-speci®c ecological adaptation processes. It does not necessarily re¯ect conditions of stress or differences in crown productivity between the two sites; but it is a ®nding that can describe the changes occurring over time in the crown condition of a particular site. Defoliation, on the other hand, from a practical point of view provides information that is very similar to that offered by transparency and also describes changes over time in the same way. But it would not be correct to consider the absence of one or more leaf-years in a holm oak as an indicator of reduced or deteriorated tree vitality. Acknowledgements This research was ®nanced by the Regione Toscana (Project ``Studies on Forest Damage'', 92.60.IT.009.0 co-®nanced by the Commission of the European Communities, EC Regulations 3528/86 and 2157/92), Program MONITO (Intensive Monitoring of Forest in Tuscany), Publication no. 22. The authors thank many colleagues who collected samples and carried out morphological measurements. References Anonymous, 1998. Programma MONITO, Monitoraggio intensivo delle foreste toscane. Rapporto Finale 1995±1997. Regione Toscana, Firenze, Italy. Arianoutsou, M., 1989. Timing of litter production in a maquis ecosystem of northeastern Greece. Acta Oecol./Oecol. Plant. 10, 371±378. Arianoutsou, M., Paraskevopoulos, S., 1992. Some aspects of mineral cycling in a maquis (evergreen sclerophyllous) ecosystem of northeastern Greece. Isr. J. Bot. 41, 135±144. Bartolozzi, L., Bussotti, F., De Dominicis, V., Ferretti, M. (Eds.), 1996. Program MONITO, Intensive Monitoring of Forests in Toscana. Concepts, Structure and 1995 Results. Regione Toscana±Giunta Regionale Publishers, Firenze, Italy.
F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285 Bellot, J., SaÂnchez, J.R., LledoÂ, M.J., MartõÂnez, P., EscarreÂ, A., 1992. Litterfall as a measure of primary production in Mediterranean holm-oak forest. Vegetatio 99±100, 69±76. Bergmann, W., 1992. Nutritional Disorder of Plants: Development, Visual and Analytical Diagnosis. Fisher Verlag, Jena, Germany. Bigi, L., Rustici, L., 1984. Regime idrico dei suoli e tipi climatici in Toscana. Regione Toscana, Dipartimento di Agricoltura e Foreste, Firenze, Italy. Bussotti, F., Ferretti, M., Cozzi, A., Grossoni, P., Bottacci, A., Tani, C., 1995. Crown status of holm oak (Quercus ilex L.) trees as related to phenology and environmental stress. Water Air Soil Pollut. 85, 1269±1274. Bussotti, F., Borghini, F., Celesti, C., Leonzio, C., Bruschi, P., 2000. Leaf morphology and macronutrients in broadleaved trees in central Italy. Trees 14, 361±368. Bussotti, F., Bettini, D., Grossoni, P., Mansuino, S., Nibbi, R., Soda, C., Tani, C., 2002. Structural and functional traits of Quercus ilex in response to water availability. Environ. Exp. Bot. 47, 11±23. Cenni, E., Bussotti, F., Galeotti, L., 1998. The decline of Pinus nigra Arn. reforestation stand on a limestone substrate: the role of nutritional factors examined by means of foliar diagnosis. Ann. Sci. For. 55, 567±576. Chenal, F., Depierre, A., Devillers, E., GeÂrard, B., Letz, J.M., Mathieu, Y., 1997. ReÂseau de surveillance de l'eÂtat sanitaire des foreÃts (ReÂseaux EuropeÂen). Protocole pour les observations. DeÂpartment de la Sante des ForeÃts, Of®ce National des ForeÃts, MinisteÁre de l'Agriculture de la PeÃche et de l'Alimentation. Cozzi, A., 1996. Monitoring sites. In: Bartolozzi, L., Bussotti, F., De Dominicis, V., Ferretti, M. (Eds.), Program MONITO, Intensive Monitoting of forests in Toscana. Concepts, Structure and 1995 Results. Regione Toscana±Giunta Regionale Publishers, Firenze, Italy, pp. 9±17. De Lillis, M., Federici, F.M., 1993. Gas exchange and resource-use patterns along a Mediterranean successional gradient. J. Veg. Sci. 4, 269±272. EscarreÂ, A., RodaÁ, F., Terradas, J., Mayor, X., 1999. Nutrient distribution and cycling. In: RodaÁ, F., Retana, J., Gracia, C.A., Bellot, J. (Eds.), Ecology of Mediterranean Evergreen Oak Forests. Ecological Studies, Vol. 137. Springer, Berlin, pp. 253± 269. Escudero, A., Del Arco, J.M., Garrido, M.V., 1992. The ef®ciency of nitrogen retraslocation from leaf biomass in Quercus ilex ecosystems. Vegetatio 99±100, 225±237. Ferretti, M. (Ed.), 1994. Mediterranean Forest Trees. A Guide for Crown Assessment. CEC UN/ECE, Brussels, Geneva. Ferretti, M., Bussotti, F., Cenni, E., Cozzi, A., 1999. Implementation of quality assurance procedures in the Italian programs of forest condition monitoring. Water Air Soil Pollut. 116, 371±376. Fink, S., 1991. The micromorphological distribution of bound calcium in needles of Norway spruce [Picea abies (L.) Karst.]. New Phytol. 119, 33±40. Gallardo, J.F., MartõÂn, A., Moreno, G., 1999. Nutrient use ef®ciency and resorption in Quercus pyrenaica oak coppices under different rainfall regimes of the Sierra de Gata mountains (central western Spain). Ann. For. Sci. 56, 321±331. Gutschick, V.P., 1999. Biotic and abiotic consequences of differences in leaf structure. New Phytol. 144, 3±18.
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Hernandez, I.M., Gallardo, J.F., Santa Regina, I., 1992. Dynamics of organic matter in forests subject to a Mediterranean semiarid climate in the Duero basin (Spain): litter production. Acta Oecol. 13, 55±65. Larcher, W., Thomaser-Thin, W., 1988. Seasonal changes in energy content and storage patterns of mediterranean sclerophylls in a northernmost habitat. Acta Oecol./Oecol. Plant. 90, 271±283. Margaris, N.S., 1981. Adaptative strategies in plants dominating Mediterranean-type ecosystems. In: di Castri, F., Goodall, D.W., Specht, R.L. (Eds.), Ecosystems of the World. 11. Mediterranean-type Shrublands. Elsevier, Amsterdam, pp. 309± 315. MartõÂn, A., Gallardo, J.F., Santa Regina, I., 1996. Aboveground litter production and bioelement potential return in an evergreen oak (Quercus rotundifolia) woodland near Salamanca (Spain). Ann. Sci. For. 53, 811±818. Maurer, S., Matyssek, R., GuÈnthardt-Goerg, M.S., Landolt, W., Einig, W., 1997. Nutrition and the ozone sensitivity of birch (Betula pendula). I. Responses at the leaf level. Trees 12, 1±10. Mooney, H.A., 1981. Primary production in Mediterranean-climate regions. In: di Castri, F., Goodall, D.W., Specht, R.L. (Eds.), Ecosystems of the World. 11. Mediterranean-type Shrublands. Elsevier, Amsterdam, pp. 249±255. Oliveira, G., Correia, O., Martins-LoucËaÄo, M.A., Catarino, F.M., 1994. Phenological and growth patterns of the Mediterranean oak Quercus suber L. Trees 9, 41±46. Oliveira, G., Martins-LoucËaÄo, M.A., Correia, O., Catarino, F., 1996. Nutrient dynamics in crown tissues of cork-oak (Quercus suber L.). Trees 10, 247±254. Poli, E., Leonardi, S., Bella, R., 1970. Produzione di lettiera nella lecceta del M. Minardo (Etna) nel periodo Settembre 1970± Giugno 1974. Arch. Bot. Biogeochem. Ital. 19, 87±106. Rapp, M., 1969. Production de litieÁre et apport au sol d'eÂleÂments mineÂraux dans deux eÂcosysteÁmes meÂditerraneÂens: la foreÃt de Quercus ilex L. et la garrigue de Quercus coccifera L. Oecol. Plant. 4, 377±410. Rapp, M., Lossaint, P., 1981. Some aspects of mineral cycling in the garrigue of southern France. In: di Castri, F., Goodall, D.W., Specht, R.L. (Eds.), Ecosystems of the World. 11. Mediterranean-type Shrublands. Elsevier, Amsterdam, pp. 289±301. Robert, B., Caritat, A., Bertoni, G., Vilar, L., Molinas, M., 1996. Nutrient content and seasonal ¯uctuations in the leaf component of cork-oak (Quercus suber L.) litterfall. Vegetatio 122, 29±35. RodaÁ, F., Mayor, X., SabateÂ, S., Diego, V., 1999. Water and nutrient limitations to primary production. In: RodaÁ, F., Retana, J., Gracia, C.A., Bellot, J. (Eds.), Ecology of Mediterranean Evergreen Oak Forests. Ecological Studies, Vol. 137. Springer, Berlin, pp. 183±194. SabateÂ, S., Sala, A., Gracia, C.A., 1999. Leaf traits and canopy organisation. In: RodaÁ, F., Retana, J., Gracia, C.A., Bellot, J. (Eds.), Ecology of Mediterranean Evergreen Oak Forests. Ecological Studies, Vol. 137. Springer, Berlin, pp. 121±133. UN-ECE, 1994. Manual on Methods and Criteria for Harmonized Sampling, Assessment, Monitoring and Analysis of the Effects of Air Pollution on Forests. Programme Coordinating Centres, Hamburg and Prague. http://www.Icp-Forests.org.
Leaf shedding, crown condition and element return in two mixed holm oak forests in Tuscany, central Italy Filippo Bussottia,*, Francesca Borghinib, Carlo Celestib, Claudio Leonziob, Alberto Cozzic, Davide Bettinic, Marco Ferrettic a
Department of Plant Biology, University of Florence, Piazzale delle Cascine 28, I 50144 Firenze, Italy b Department of Environmental Sciences, University of Siena, Via Mattioli 4, I 53100 Siena, Italy c Linnaea-ambiente srl, Via G. Sirtori 37, I 50137 Firenze, Italy Received 19 September 2001; received in revised form 27 March 2002; accepted 13 May 2002
Abstract Litterfall (leaves, ¯owers, fruits, twigs) was collected every month in two mixed Mediterranean forests of Quercus ilex (holm oak) in central Italy differing for their ecological features: a mesic site (Colognole, CL) and a xeric one (Cala Violina, CV). The survey period lasted 8 years (1992±2000) at CL and 4 years at CV. Chemical analysis of the litterfall was performed in 1997 and 1998. In these 2 years living leaves were also collected for chemical analysis. The main ®ndings were: (i) the litter production was lower and the leaf percentage in the total litterfall was smaller at CV than at CL; (ii) the phenological behavior differed in the two sites and the leaves had greater longevity at CV, whereas at CL trees renewed their crown almost completely each spring; (iii) the chemical composition of the living leaves re¯ected the edaphic differences between the two sites; (iv) the chemical composition of the senescent leaves and the litter in the two sites was very different; (v) crown transparency and defoliation followed the same pattern of the leaf shedding; (vi) transparency was greater at CL, where the litter production was higher, because of the different shape of the crowns. The differences between the two study areas have been discussed in the light of the different ecology of the two sites, since leaf lifespan is greater in dry and infertile soils. # 2002 Elsevier Science B.V. All rights reserved. Keywords: Bioelements; Crown productivity; Crown transparency; Defoliation; Leaf lifespan; Litterfall; Phenology; Mediterranean vegetation; Quercus ilex
1. Introduction Leaf lifespan is in¯uenced by environmental factors: in dry and infertile soils trees maintain their leaves longer than trees growing in more favorable conditions (Mooney, 1981; Gutschick, 1999). In unfavorable environments leaves develop thicker mesophyll and *
Corresponding author. Tel.: 39-055-3288369; fax: 39-055-360137. E-mail address: [email protected] (F. Bussotti).
cuticle (Margaris, 1981) and have high metabolic construction costs (in terms of photosynthetic energy demand) that can be compensated by means of their longevity. Besides, in adverse conditions evergreenness represents the way to exploit also short and sudden periods when photosynthesis is possible. In the Mediterranean environment the most favorable conditions for photosynthesis and metabolic activities are found during the equinoctial periods (spring and autumn), i.e. when in the deciduous broad-leaved trees the vegetative apparatus is lacking (De Lillis and Federici, 1993). On
0378-1127/02/$ ± see front matter # 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 8 - 1 1 2 7 ( 0 2 ) 0 0 2 8 3 - 9
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the other hand, during senescence leaves lose their physiological ef®ciency and the metabolic costs for their maintenance can be high. In favorable edaphic conditions foliar turnover is quicker than in infertile soils (Maurer et al., 1997). In Quercus ilex L. (holm oak) leaf lifespan is currently considered 2±3 years, but may be longer (4±5 years) under worse environmental conditions (Sabate et al., 1999). In Mediterranean stands with Q. ilex L. or other Mediterranean evergreen oaks (Quercus suber L., Quercus coccifera L.) leaf shedding does not occur at a single time during the year: alongside the usual springtime peak, there is normally also a loss of leaves in autumn and winter (Rapp, 1969; Poli et al., 1970; Rapp and Lossaint, 1981; Arianoutsou, 1989; Bellot et al., 1992; Escudero et al., 1992; Hernandez et al., 1992; Oliveira et al., 1994; MartõÂn et al., 1996). Leaf shedding affects the whole mineral nutrient cycle. In the oligotrophic Mediterranean ecosystems, ef®ciency in nutrient use (see Gallardo et al., 1999), i.e. the biomass production by plants (in terms of ®xed C) per unit of nutrient uptake, is presumably a response to decreased soil nutrient availability. Resorption, i.e. the translocation by young tissue of nutrients from senescent tissues such as mature leaves, is a means of re-using the same elements. Within a programme aimed at assessing forest condition in Tuscany (MONITO, Intensive Monitoring of Forest in Tuscany, see Bartolozzi et al., 1996; Ferretti et al., 1999) an apparent anomaly was detected in the phenological pattern of Q. ilex trees in some permanent areas of the regional monitoring network (Bussotti et al., 1995), where the plants renewed their crown completely each year and therefore carried almost exclusively current-year (C) leaves. The aim of the present survey was to ascertain whether such a pattern was determined by natural ecological factors (such as climate, availability of water and nutrients) or was to be considered a pathological stress condition. The selected areas are to be considered as a ``case study'' and do not claim to represent the whole Q. ilex population in Tuscany. 2. Materials and methods 2.1. Study areas The study areas are Colognole (CL) and Cala Violina (CV), both located in Tuscany, near the Tyr-
rhenian coast. The distance between the two plots is about 100 km. In both, the forest vegetation consists of an adult (40±60 years) holm-oak stand mixed with different broad-leaved species (see Table 1); the canopy is fully closed, the soil is deep and the morphology nearly ¯at. CL is characterized by a high water table, spatially irregular trend always in the root zone, guaranteeing a constant water supply even in the warmest and driest months. The CV stand, on the other hand, grows in very xeric conditions, with 5 months of water de®cit in the soil (Bigi and Rustici, 1984). In
Table 1 Characteristics of the study areas (Bigi and Rustici, 1984; Cozzi, 1996; Anonymous, 1998; Bussotti et al., 2000, 2002)a
Physical features UTM X UTM Y Altitude (m a.s.l.) Exposure Slope (%) Bedrock Tree features Main species Other species Age of the dominant trees (years) Stem ha 1 (Q. ilex, %) Basal area, m2 ha 1 (Q. ilex) Mean diameter, cm (Q. ilex) Height of the dominant trees (m) Meteorological data Mean annual rainfall, mm (historical mean 1955±1974) Mean annual temperature, 8C (historical mean 1955±1974) Data on soil (0±20 cm depth) pH N (%) P2O5 (%) K2O (%) Ca (%) Mg (%)
CL
CV
1616000 4818480 250 NE Variable Claiey Schist; Ophiolitic
1645300 4745700 5 N±NW 5 Sandstone
Q. ilex Q. pubescens A. unedo Q. crenata 40±60
Q. ilex Q. pubescens A. unedo F. ornus 40±60
1545 (39) 16.7 (6.2) 16.7 (19.5) 15±18
2080 (69) 13.4 (5.9) 13.4 (14.9) 15±18
978
637
14.7
15.1
5.9 2.0 17.5 0.5 2.5 32.3
5.7 1.3 25.5 1.4 19.3 2.4
a The ®gures exclusively relative to Q. ilex are given in parenthesis.
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Fig. 1. Daily pattern of temperatures (minimum and mean) during December 1996.
August, after a prolonged dry period, the pre-dawn water potential (C) was 0.6 MPa at CV and 2.7 MPa at CL (Bussotti et al., 2002). Data on the meteorological behavior during the study period are available in Bussotti et al. (2000). Climate has a regular Mediterranean pattern in both sites, and the most important anomaly occurred in the last days of December 1996 with a sudden drop of temperature (Fig. 1) that was more pronounced at CV than CL. In both sites the mean daily temperature was below 0 8C for four consecutive days. The distance from the sea is about 5000 m for CL and only 200 m for CV. 2.2. Collection and analysis of samples The abscission of leaves, twigs, ¯owers and fruits was monitored from April 1992 to March 2000 at CL and from April 1996 to March 2000 at CV. In each study area nine litter traps were positioned according to a square grid with sides 10 m wide 3 3. Each litter trap had a collecting surface of 0.5 m2. They were emptied monthly and the litter collected was divided according to tree species and biological matrix (leaves, ¯owers, fruits, twigs). Dry weight of samples was determined (DW 72 h at 65 8C). Each time both DW and total surface (using an areameter LI-3100 Licor, Lincoln, NE) were measured on a sub-sample of
100 leaves for each of the main species (Q. ilex L., Quercus pubescens Willd., Quercus crenata Lam. and Arbutus unedo L. at CL; Q. ilex, Q. pubescens, Fraxinus ornus L. and A. unedo at CV). Leaf mass per area (LMA) was calculated as dry weight/leaf area (mg cm 2). This parameter allowed us to calculate the leaf area index (LAI) of the leaf litterfall. A subsample for each matrix was prepared every 3 months in the period 1997±1998. Crown transparency and defoliation were assessed visually both at CL and CV, on the same 30-tree sample in each area, according to the standard criteria used in the transitional network for forest condition assessment (ICP-Forests, see UN-ECE, 1994). Both these parameters are de®ned by a percent scale with 5% steps. Zero indicates an intact crown, whereas the value 100 indicates a crown without leaves. The transparency, de®ned as the percentage of gaps in a tree crown observed against the sky, was assessed monthly during the period July 1996±December 1998 using photographic references for Mediterranean trees (Ferretti, 1994). Defoliation rates were also assessed between July 1996 and April 1998. That assessment was based on the estimation of the number of years of leaves present in the crown. The French protocol (Chenal et al., 1997), in the case of several evergreen species, suggests that the absence of the
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previous-year leaves C 1 be considered as 20± 40% defoliation, and the absence of C 2 leaves as 15±20%. C leaves can be partially lacking because of dead branchlets, insects or other causes. Foliar nutrients were analyzed according to the methods and criteria used in the forest health assessment programmes (UN-ECE, 1994). During the 1997± 1998 and 1998±199 growing seasons, C living leaves were sampled four times: June (just after sprouting), August, February and April. C 1 leaves (senescent leaves) were also collected in August. Five sample trees were selected in each plot according to the standard procedures (UN-ECE, 1994). For each tree, 40 g of leaves were collected (10 g from the four different azimuth orientations) in the upper third of the crown and were pooled to obtain a composite sample for each tree. After collection, the samples were placed in polyethylene bags and stored in a refrigerated box until they reached the laboratory (that same day). About 150 mg of dry matter were mineralized in clean Te¯on vessels with 3 ml of HNO3 at 120 8C for 8 h. Each digestion included at least one blank test.
Analytical determinations were performed by atomic absorption spectrometry (AAS). An air±acetylene ¯ame (2280, Perkin-Elmer) was used for Ca, K and Mg. Pb was determined by electrothermal atomic absorption spectrometry with Zeeman background correction (ZETAAS). Al, B, Cu, Fe, Mn, Na, P and S were assayed by inductively coupled plasma atomic emission spectrometry (ICP/EAS; Plasma 400, Perkin-Elmer). Nitrogen was analyzed according to the Kjeldhal method (UN-ECE, 1994). Each determination was done in three replicates. The accuracy of analytical procedures was checked by simultaneous digestion and analysis of standard reference materials (SRMs). SRMs 1572 ``citrus leaves'' and 1547 ``peach leaves'' from the National Institute of Standards and Technology (NIST, Gaithersburg, MD) were used. Batches with accompanying SRMs outside the certi®ed range were repeated. Element concentrations were determined by the standard methodologies reported by UN-ECE (1994). Standard solutions of inorganic elements were prepared by serial dilution of stock standard solutions containing 1 g l 1 of the
Table 2 Yearly ¯uctuation of the shed biomass, according to the different matrices, from April to March of the following year Leaves 2
CL 1992±1993 1993±1994 1994±1995 1995±1996 1996±1997 1997±1998 1998±1999 1999±1990 Mean Standard deviation CVa (%) CV 1996±1997 1997±1998 1998±1999 1999±1990 Mean Standard deviation CV (%) a
2
Woody parts (g m 2)
Flowers (g m 2)
Fruits (g m 2)
Other (g m 2)
Total (g m 2)
Q. ilex (g m )
Other species (g m )
358 335 235 303 372 255 223 372
143 114 131 204 158 129 144 141
110 95 103 157 145 211 125 120
10 17 3 36 12 23 24 24
19 20 85 44 79 15 119 31
35 37 39 36 37 46 31 28
677 620 598 782 806 681 669 719
307 61 20
145 26 18
133 37 28
19 10 54
52 38 74
36 5 14
694 72 10
156 143 222 116
84 65 87 66
156 150 81 168
10 17 6 3
206 22 15 11
49 49 26 21
664 450 439 387
159 44 28
76 11 15
139 39 28
9 6 67
64 95 148
36 14 40
485 122 25
Standard deviation/mean (coef®cient of variation).
F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285
277
Table 3 Leaf characteristics CL Area of one leaf of Q. ilex LMAa Q. ilex leaves (mg cm 2) Total leaf area shed (m2 m 2) Q. ilex (LAI) Other species (LAI) All species (LAI)
CV
P
6.63 0.59 16.87 1.48
5.97 0.56 17.09 0.83
**
1.80 0.37 1.20 0.23 3.00 0.59
1.06 0.24 0.78 0.12 1.84 0.34
n.s.b *** *** ***
a
Leaf mass per area. Difference not signi®cant. ** P < 0:01. *** P < 0:001. b
element to be determined (Spectrosil, BDH). Concentrations were expressed as percent of DW for macronutrients (N, S, P, Ca, Mg, and K) and in mg g 1 for microelements (Na, Fe, Mn, Zn, Cu, Al, B and Pb). 3. Results 3.1. Litterfall The mean quantity of litter shed yearly in CL was 694 g m 2 (Table 2). The most represented matrix in this litter were the leaves (65% of the total litter production); out of this total, about 307 g m 2 were
Q. ilex leaves (68% of all leaves), followed by those of Q. pubescens (8.5%), Q. crenata (7.5%) and A. unedo (5%). The remaining 11% was the contribution of several deciduous broadleaves (Ostrya carpinifolia Scop., Ulmus minor Mill., Sorbus torminalis (L.) Crantz., Quercus cerris L., F. ornus L.). Among the other matrices of the litter, woody parts made up 19% of the total shed biomass; ¯owers (male catkins from oak species) 2.7%; and fruits (acorns) 7.3%. The remaining 6% consisted of other materials (residues). At CV (Table 2) the yearly litter shed was considerably lower (485 g m 2) and leaves (235 g m 2) represented only 48% of the total. Q. ilex leaves (159 g m 2) were 70% of all leaves, followed by Q.
Fig. 2. Abscission pattern of Q. ilex leaves, represented by the monthly DW for the period 1996±2000 (in percent of year total).
278
F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285
Fig. 3. Yearly abscission pattern of Q. ilex leaves, represented by the average monthly DW for the period 1996±2000 (in percent of year total).
Fig. 4. Monthly pattern of (A) crown transparency and (B) crown defoliation (July 1996±December 1998) in the two areas.
pubescens (16%), F. ornus (12%) and A. unedo (2%). Other species were negligible. Wood represented an important fraction (29%); followed by acorns (13%) and ¯owers (2%). Residues were 8%. In both sites
there were considerable variations in the shedding rates, both in total quantities and between different matrices, from one year to the next (Table 2). The most variable matrices were acorns and ¯owers. Table 3
Fig. 5. Correlation between crown transparency and leaf shedding at (A) CL and (B) CV.
Table 4 Element concentrations in the litter matricesa,b Matrice
N (%)
Q. ilex leaves
S (%)
P (%)
Ca (%)
Mg (%)
K (%)
Na (ppm)
Fe (ppm)
Mn (ppm)
Zn (ppm)
Cu (ppm)
Al (ppm)
B (ppm)
1.27 0.22 0.13 0.02 0.05 0.01 0.46 0.07 0.33 0.04 0.40 0.13 212 60.5 99.5 29.2 109 20.4 15.7 2.71 0.96 0.27 0.11 0.02 0.05 0.01 0.89 0.13 0.20 0.02 0.37 0.08 486 181 214 69.9 1708 246 29.0 1.95
Q. pubescens leaves
CL CV
1.35 0.41 0.13 0.02 0.06 0.04 0.65 0.24 0.66 0.14 0.39 0.29 279 134 1.35 0.43 0.13 0.02 0.07 0.05 0.68 0.14 0.29 0.05 0.48 0.23 695 386
98.8 50.9 199 49.7
101 21.3 15.0 4.80 488 117 21.0 3.85
6.53 1.86 91.4 35.3 46.2 14.2 1.18 0.73 5.54 2.39 182 65.2 72.5 23.9 0.77 0.48
A. unedo leaves
CL CV
0.98 0.37 0.10 0.02 0.06 0.02 0.86 0.11 0.50 0.07 0.52 0.14 243 151 0.92 0.31 0.09 0.03 0.06 0.02 1.34 0.12 0.36 0.07 0.39 0.09 366 179
104 42.7 121 41.3
12.1 2.6 33.2 6.85 100 99.6 37.3 5.73
2.44 0.77 3.35 0.63
108 48.8 47.8 11.3 0.94 0.41 103 29.9 44.7 7.0 0.41 0.17
***
***
***
***
***
**
*
***
***
***
*
***
***
***
***
***
**
**
5.76 1.07 73.9 23.3 21.2 7.5 3.92 0.90 232 73.5 39.8 3.1
Pb (ppm)
CL CV
***
***
***
*
***
0.89 0.27 1.12 0.34
**
**
Q. crenata leaves
CL
1.22 0.37 0.13 0.03 0.06 0.02 0.70 0.23 0.56 0.14 0.28 0.15 299 150
135 45.4
217 97.7 16.1 2.05
6.22 1.66
125 31.4 44.4 13.8 1.23 0.32
F. ornus leaves Flowers
CV
1.64 0.14 0.19 0.07 0.08 0.02 1.45 0.43 0.34 0.09 0.71 0.41 276 102
198 86.6
144 65.9 16.4 3.94
4.40 0.96
175 63.4 20.9 5.4
1.09 0.63
CL CV
1.80 0.28 0.16 0.04 0.11 0.03 0.48 0.14 0.33 0.05 0.73 0.38 340 161 1.60 0.53 0.12 0.02 0.09 0.01 0.61 0.09 0.21 0.03 0.50 0.34 415 124
283 212 354 162
78.4 26.1 23.7 7.45 664 89.3 30.5 8.31
13.9 3.98 10.4 0.37
299 247 338 123
21.9 6.0 27.2 2.8
3.17 2.27 1.98 1.19
CL CV
0.66 0.18 0.06 0.02 0.05 0.03 0.23 0.09 0.19 0.06 0.49 0.23 131 134 0.65 0.22 0.06 0.02 0.06 0.02 0.41 0.18 0.15 0.07 0.46 0.27 255 126
68.2 58.4 89.9 65.7
33.7 13.4 9.72 3.66 359 245 11.2 4.21
6.93 1.49 49.7 24.6 11.5 5.3 5.30 2.40 76.3 71.9 15.7 4.5
0.42 0.25 0.34 0.17
CL CV
0.69 0.21 0.08 0.02 0.03 0.01 0.40 0.11 0.25 0.05 0.32 0.32 154 48.4 0.72 0.15 0.08 0.01 0.04 0.01 1.18 0.25 0.17 0.03 0.33 0.04 465 112
121 75.4 278 222
63.0 21.7 17.7 6.68 509 122 24.2 5.11
7.41 1.84 7.86 0.87
3.45 2.02 3.72 2.51
Fruits
Woody parts
a b *
*
***
***
**
***
***
**
**
Asterisk represent the signi®cance of the differences between the two sites (in the same column). Mean values and standard deviation of the years 1997±1998 (no. of samples 8). P > 0:05.
**
P > 0:01.
***
P > 0:001.
***
*
***
***
***
*
*
*
*
*
116 57.6 14.6 4.0 209 123 22.3 2.3 *
***
Table 5 Element concentrations in living leavesa,b
June
August
February
April
c
C1
a b c *
N (%)
S (%)
P (%)
Ca (%)
Mg (%)
K (%)
Na (ppm)
CL CV
2.02 0.21 1.35 0.15
0.14 0.02 0.12 0.01
0.21 0.02 0.07 0.01
0.14 0.06 0.49 0.06
0.26 0.03 0.14 0.03
1.31 0.11 0.49 0.08
56.2 16.7 261 130
66.2 20.0 115 55.8 66.2 30.9 1150 307
21.6 1.3 9.48 2.77 21.1 4.19 4.63 1.13
CL CV
1.39 0.06 1.46 0.12
0.11 0.01 0.12 0.02
0.09 0.01 0.08 0.06
0.27 0.06 0.56 0.11
0.28 0.02 0.20 0.02
0.66 0.06 0.68 0.06
206 25.3 191 50.0
56.9 15.4 219 119 93.0 11.8 1156 430
13.42 2.30 4.28 0.82 19.7 4.5 5.53 0.57
CL CV
1.38 0.05 1.31 0.16
0.11 0.01 0.15 0.02
0.09 0.02 0.08 0.01
0.41 0.09 0.75 0.20
0.35 0.12 0.17 0.05
0.32 0.03 0.45 0.14
CL CV
1.41 0.17 1.59 0.11
0.14 0.02 0.16 0.02
0.10 0.02 0.09 0.02
0.62 0.07 0.80 0.08
0.41 0.08 0.15 0.03
0.52 0.19 0.44 0.05
191 84.4 210 68.2
103.2 43.5 334 72.7 217 58.4 1642 380
CL CV
1.30 0.13 1.22 0.03
0.12 0.01 0.12 0.01
0.07 0.01 0.06 0.02
0.48 0.01 0.86 0.22
0.30 0.07 0.18 0.06
0.52 0.05 0.41 0.06
205 132 310 25.6
114 59.5 668 922 165 46.3 1664 303
***
*
*
*
***
***
***
***
**
***
***
***
***
***
***
***
**
**
***
150 49.6 256 102
*
**
Asterisk represent the signi®cance of the differences between the two sites (in the same column). Mean values and standard deviation of the 1997±1998 and 1998±1999 growing seasons (no. of samples 10). C 1 leaves were collected in August. P > 0:05.
**
P > 0:01.
***
P > 0:001.
Fe (ppm)
M (ppm)n
Zn (ppm)
***
**
***
91.1 54.0 233 56.1 224 161 1646 538
***
***
*
***
***
***
Cu (ppm)
**
**
*
*
*
*
15.5 8.3 4.17 0.39 21.1 6.58 4.61 0.8
Al (ppm)
B (ppm)
Pb (ppm)
20.0 5.4 17.63 4.30 0.21 0.09 80.5 28.4 27.8 9.00 0.49 0.20
***
***
*
23.70 6.70 23.82 3.30 0.20 0.12 57.0 12.1 41.64 3.81 0.32 0.29 ***
***
*
99.2 64.6 24.56 10.2 1.09 0.29 238 186 42.8 9.80 1.18 0.64
***
**
14.7 4.1 4.52 0.61 27.4 11.4 4.83 0.41
106.6 45.0 32.30 9.94 1.14 0.27 229 76.5 48.6 7.33 1.05 0.30
18.7 9.6 9.24 13.7 27.4 6.69 5.76 3.19
117.0 88.8 30.0 16.6 1.18 0.39 183.7 72.4 48.90 13.3 0.77 0.32
***
*
**
*
*
Table 6 Yearly total amount of elements in the litter sheda
CL Overall litterfall 67.16 (yearly mean) Singular matrices (yearly mean) Q. ilex leaves 32.81 Q. crenata leaves 3.09 Q. pubescens leaves 4.30 A. unedo leaves 2.05 Other species leaves 7.32 Woody parts 9.10 Flowers 4.57 Fruits 3.92 CV Overall litterfall 33.28 (yearly mean) Singular matrices (yearly mean) Q. ilex leaves 14.57 Q. crenata leaves 4.66 Q. pubescens leaves 4.91 A. unedo leaves 0.15 Woody parts 6.31 Flowers 1.40 Fruits 1.27 a
7.16
2.95
31.59
24.03
29.41
1464
692
604
112
42
583
154
8.5
3.51 0.35 0.44 0.23 0.99 0.96 0.33 0.35
1.18 0.14 0.16 0.11 0.34 0.45 0.25 0.31
13.75 1.92 2.99 1.97 3.79 5.27 0.83 1.07
9.45 1.58 2.86 1.18 3.50 3.53 0.88 1.04
10.88 0.80 0.87 1.14 3.62 6.74 2.11 3.25
649 82 145 49 193 200 95 46
316 36 29 22 88 130 3773 40
352 58 41 2 288 85 21 20
45 448 5 816 16.45 23 4 5
15 1.7 2.1 0.5 4.9 10 2.98 4.69
231 37 36 24 72 127 37 21
52 12 20 11 19 233 6.2 10
2.8 0.35 0.37 0.21 0.83 3.5 0.38 0.14
3.88
1.67
35.54
7.89
13.98
1826
749
3663
87
18
715
133
5.9
1.59 0.74 0.58 0.02 0.70 0.12 0.12
0.60 0.23 0.21 0.01 0.38 0.12 0.13
13.84 5.37 3.46 0.26 11.04 0.66 0.91
3.02 1.21 1.32 0.08 1.67 0.25 0.33
5.35 1.61 1.76 0.07 2.87 1.06 1.26
758 89 439 7 430 39 61
3347 59 85 3 229 21 162
2755 394 2339 230 481 85 65
44 4.6 8.9 0.7 22 2.7 2.1
6.0 1.2 2.0 0.06 6.9 1.2 1.0
353 54 84 2.4 179 25 14
58 6.3 39 0.9 21 3.2 3.2
1.8 0.27 0.21 0.01 3.4 0.15 0.06
F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285
N S P Ca Mg K Na Fe M Zn Cu Al B Pb (kg ha 1) (kg ha 1) (kg ha 1) (kg ha 1) (kg ha 1) (kg ha 1) (g ha 1) (g ha 1) (g ha 1) (g ha 1) (g ha 1) (g ha 1) (g ha 1) (g ha 1)
Mean value of the 1997±1998 and 1998±1999 growing seasons.
281
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F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285
shows the leaf area development at the two sites: at CL the surface of a single leaf was greater than at CV; LAI is greater at CL than CV. Figs. 2 and 3 show the pattern of the monthly leaf abscission. At CL there was a very rapid spring defoliation followed by a complete crown renewal. The yearly leaf shedding was concentrated in May (53%), and during the spring (April±June) 75% of leaves fell. Only a small secondary peak (8±9%) was detectable between December and January. At CV, on the other hand, the renewal of the crown occurred more gradually during the growth season. The spring abscission started earlier (15% in April) and remained constant until June (35% of leaves lost in the period April±June). A secondary peak was evident in autumn (October±November) with the 18% of total leaves fallen. After the drop of temperature registered in December 1996, the winter abscission increased dramatically at CL but not at CV. The assessment of crown transparency registered the same pattern as the litterfall (Fig. 4A and B). The correlation between crown transparency and shed foliar biomass in the same month was found to be signi®cant in both sites, with P < 0:001 (Fig. 5A and B). At CL crown transparency reached very marked peaks in May, but recovered quickly with the new foliage; after the frost in December 1996 transparency increased. At CV crown transparency was more or less constant throughout the year, with small peaks in springtime. The transparency values were higher at CL than CV. Defoliation values were higher than transparency values (Fig. 4B), and the differences between the two sites were less marked. At CL defoliation correlated strongly with transparency (P < 0:001; r 0:94), but at CV that correlation was not signi®cant r 0:34. 3.2. Element return The chemical composition of the various litter matrices was different in the two sites (Table 4). Compared to CL, the holm-oak leaves at CV had lower concentrations of N, Mg, K, Cu and a greater amount of Ca, Na and several microelements such as Fe, Mn, Zn, Al, and B. Litter composition differed from that of the living leaves (Table 5). At CV, the N concentration decreased in senescent and dead leaves; the same happened for P and K. The opposite trend was detectable for Ca, Na, Fe, Mn, Al and Pb. At CL,
on the other hand, no signi®cant differences were found in N concentration between living and dead leaves, while P, K and Mn were lower in the litter. Finally Ca, Fe, Al and Cu concentrations increased with age in living leaves, but their concentration remained constant, or was slightly reduced, in the litter. Among the different leaf species, the highest N concentrations were reached in the deciduous trees (F. ornus and Q. pubescens), whereas the lowest were found in A. unedo. Among all the different components of the litter, nitrogen was highest in ¯owers and lowest in fruits and wood. Several differences were site-speci®c, without distinction of matrix: Mg was generally higher at CL, whereas Ca, Na, Fe and Mn were higher at CV. The return of the elements to the soil via litterfall was determined by the yearly amount of litter produced and their concentration values (Table 6). Most of the elements were more abundant at CL because of the greater amount of litter; but the total amount of calcium, sodium, iron, manganese and aluminum was more abundant at CV, because all these elements were present in higher concentrations. 4. Discussion In spite of similar age and basal area, the two sites differed in crown productivity (Table 2). Overall, the litterfall values fell within the range established by other authors (Rapp, 1969; Poli et al., 1970; Rapp and Lossaint, 1981; Arianoutsou, 1989; Bellot et al., 1992; Escudero et al., 1992; Hernandez et al., 1992; Oliveira et al., 1994; MartõÂn et al., 1996; RodaÁ et al., 1999). In particular, behavior at CV was similar to the more xeric stands described by Arianoutsou (1989), whereas the CL values were consistent with those reported by Rapp (1969) for a number of temperate forest ecosystems. At CV the similar basal area is subdivided into a greater number of stems than CL, but has a lower amount of litter production. The differences between CV and CL became more evident when considering only the foliar fraction of the litter. In fact, at CV leaf production was barely more than half the leaf production at CL, whereas woody parts (branches) in the litterfall were more abundant. These differences may be ascribed to the more xeric conditions at CV.
F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285
Mooney (1981), for example, stated that in a xeric environment the production of supporting organs (as branchlets) is more pronounced than the production of living tissues (leaves). The xeromorphic adaptation of the CV Q. ilex trees was detectable also in the leaf morphology, since the leaves collected at this site were smaller. Their LMA was not higher at all, but in previous research studies signi®cant differences were found between the two sites (Bussotti et al., 2000, 2002). These discrepancies are explained by the different methods of sampling, in fact in the previous works only sun leaves, from the upper part of the crown, were considered. The timing of abscission was also examined in the two areas. Leaf turnover was quicker at CL: abscission occurred practically all at once, at the same time as the ¯ushing, and C leaves were almost completely shed. On the other hand, at CV a large percentage of leaves survived the summer period and were shed in autumn. The scienti®c literature (Rapp, 1969; Poli et al., 1970; Rapp and Lossaint, 1981; Arianoutsou, 1989; Bellot et al., 1992; Escudero et al., 1992; Hernandez et al., 1992; Oliveira et al., 1994; MartõÂn et al., 1996) reports several ®ndings concerning the leaf shedding and phenology of Q. ilex and other Mediterranean evergreen species. It is usually assumed that most of the abscission occurs during the spring months, although a secondary peak during the autumnal and winter months is also detectable. Neither study site was an exception to this trend, but the relative importance of the main peak (spring) and the secondary one (autumn) was very different. This was due to the different ecological conditions of the two stands. In fact, in the xeric stand the leaves displayed a greater longevity than in the mesic one. At CL the availability of water in the soil allows for photosynthetic activity during the summer months (see Bussotti et al., 2002); thus, a complete crown turnover in the spring represents an advantage for the overall effectiveness of the tree. Bussotti et al. (2002) suggested that the phenological behavior in the two sites could be attributed to the different pattern of starch storage and metabolism: the CV holm-oak trees were in fact well-supplied with starch in their branchlets, whereas the CL trees did not present those same reserves. Larcher and ThomaserThin (1988) observed in several Mediterranean sclerophyllous species that large quantities of starch were stored in all the above-ground organs. Starch is utilized
283
during the period of summer drought and during the severest winter cold spells as a source of osmolytes to control the depletion of cellular water. The lack of starch reserves at CL may be explained by the fact that in this site the resources were used mainly for growth (leaf and litter production are clearly greater), whereas at CV they were used as protection against stress factors. This makes the CL Q. ilex more sensitive to winter conditions, explaining also the sudden and marked defoliation which was observed at CL after a sudden temperature drop in December 1996 (Figs. 1 and 2). During the same period at CV, even with similar or colder minimum temperatures, no leaf damage or defoliation occurred. Crown transparency and defoliation trends matched leaf abscission trends fairly closely, with marked variations at times of greater leaf turnover, especially at CL. Transparency and defoliation changes were closely correlated at CL, whereas at CV there were practically no differences between the different dates of observation. This suggests that the two parameters (transparency and defoliation) are mutually compatible and yield the same type of information in relation to variations over time. Defoliation values were always higher than transparency values. The reduction in the number of leaf-years carried by the crown is usually considered the most important parameter in evaluating the vitality of an evergreen tree (UN-ECE, 1994). The ®ndings of this study indicate that the loss of leaves at CL is quickly followed by a complete renewal of the crown and that the canopy has a high productivity, but, on the other hand, the foliage appeared to be more sensitive to climatic stress (frost, in this case). As far as the differences between the two sites are concerned, transparency reached higher values at CL than at CV, whereas differences in defoliation levels were only slight. Comparing data on crown condition (transparency and defoliation) to data on crown productivity and LAI (Tables 2 and 3), it is interesting to note that transparency is lower in conditions of more severe water stress (CV), conditions in which crown productivity is also lower. The explanation probably lies in the different shape of the crowns that trees develop in adapting to different levels of water availability: at CL crowns are broader, although less dense, whereas at CV they are narrower but denser. The elemental composition of the living leaves con®rms the results of Bussotti et al. (2000). Among
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the macronutrients, the differences in Mg (more abundant at CL) and Ca (more abundant in CV) re¯ects the different soil supply in the two study areas. The nutrient supply varies during the year (cf. Robert et al., 1996; Oliveira et al., 1996). Calcium increased in senescent leaves and in the litter according to a behavior consistent with that described by Fink (1991), Bergmann (1992) and Cenni et al. (1998). At CV Ca probably originates from the sea. Calcium carbonate is in fact one of the most important components of sea salt. Sodium concentrations also increased with the leaf age at CV, probably due to the closeness of the site to the sea shore. Other elements such as P and K (and N at CL) showed the opposite trend, being lower in the litter than in the living leaves, thus suggesting the occurrence of translocation processes (Escudero et al., 1992; Gallardo et al., 1999; Escarre et al., 1999) that are more ef®cient in xeric areas (Gallardo et al., 1999). The litter foliar composition of the different species showed that deciduous trees (Q. pubescens, but mostly F. ornus) generally had higher concentrations of many elements than evergreen ones. The composition of the different matrices (acorns, ¯owers, woody parts) was consistent with the ®ndings of MartõÂn et al. (1996), con®rming that ¯owers have the highest element concentrations. With regard to the total bioelement return, the results were consistent with those of other authors (Rapp, 1969; Arianoutsou and Paraskevopoulos, 1992; MartõÂn et al., 1996; Escarre et al., 1999). Their amount depended in most cases on the amount of litterfall, and they were generally more abundant at CL, with the exception of Ca, Na, Fe, Mn and Al. In these latter elements the ``concentration factor'' was more important than the quantity of litter. Leaves were the most important vector for element return. 5. Conclusions In evergreen trees a full loss of leaves may occur as a consequence of severe stress factors, such as drought, frost, attack of defoliator insects or effect of pollutants. During the study period in the two sites the most important stress event we detected was the frost in December 1997, that caused a nearly complete defoliation of holm oak trees at CL but not at CV. The
spring loss of leaves at CL appears to be connected with the ecological adaptation of holm oak in these speci®c site conditions. In this study the parameter that most aptly describes the ecological differences between the two sites is crown productivity, expressed as litterfall (g of dry matter per m2) or as LAI. Crown transparency is determined by the architecture of the crown and the distribution of the foliage, and is a consequence of site-speci®c ecological adaptation processes. It does not necessarily re¯ect conditions of stress or differences in crown productivity between the two sites; but it is a ®nding that can describe the changes occurring over time in the crown condition of a particular site. Defoliation, on the other hand, from a practical point of view provides information that is very similar to that offered by transparency and also describes changes over time in the same way. But it would not be correct to consider the absence of one or more leaf-years in a holm oak as an indicator of reduced or deteriorated tree vitality. Acknowledgements This research was ®nanced by the Regione Toscana (Project ``Studies on Forest Damage'', 92.60.IT.009.0 co-®nanced by the Commission of the European Communities, EC Regulations 3528/86 and 2157/92), Program MONITO (Intensive Monitoring of Forest in Tuscany), Publication no. 22. The authors thank many colleagues who collected samples and carried out morphological measurements. References Anonymous, 1998. Programma MONITO, Monitoraggio intensivo delle foreste toscane. Rapporto Finale 1995±1997. Regione Toscana, Firenze, Italy. Arianoutsou, M., 1989. Timing of litter production in a maquis ecosystem of northeastern Greece. Acta Oecol./Oecol. Plant. 10, 371±378. Arianoutsou, M., Paraskevopoulos, S., 1992. Some aspects of mineral cycling in a maquis (evergreen sclerophyllous) ecosystem of northeastern Greece. Isr. J. Bot. 41, 135±144. Bartolozzi, L., Bussotti, F., De Dominicis, V., Ferretti, M. (Eds.), 1996. Program MONITO, Intensive Monitoring of Forests in Toscana. Concepts, Structure and 1995 Results. Regione Toscana±Giunta Regionale Publishers, Firenze, Italy.
F. Bussotti et al. / Forest Ecology and Management 176 (2003) 273±285 Bellot, J., SaÂnchez, J.R., LledoÂ, M.J., MartõÂnez, P., EscarreÂ, A., 1992. Litterfall as a measure of primary production in Mediterranean holm-oak forest. Vegetatio 99±100, 69±76. Bergmann, W., 1992. Nutritional Disorder of Plants: Development, Visual and Analytical Diagnosis. Fisher Verlag, Jena, Germany. Bigi, L., Rustici, L., 1984. Regime idrico dei suoli e tipi climatici in Toscana. Regione Toscana, Dipartimento di Agricoltura e Foreste, Firenze, Italy. Bussotti, F., Ferretti, M., Cozzi, A., Grossoni, P., Bottacci, A., Tani, C., 1995. Crown status of holm oak (Quercus ilex L.) trees as related to phenology and environmental stress. Water Air Soil Pollut. 85, 1269±1274. Bussotti, F., Borghini, F., Celesti, C., Leonzio, C., Bruschi, P., 2000. Leaf morphology and macronutrients in broadleaved trees in central Italy. Trees 14, 361±368. Bussotti, F., Bettini, D., Grossoni, P., Mansuino, S., Nibbi, R., Soda, C., Tani, C., 2002. Structural and functional traits of Quercus ilex in response to water availability. Environ. Exp. Bot. 47, 11±23. Cenni, E., Bussotti, F., Galeotti, L., 1998. The decline of Pinus nigra Arn. reforestation stand on a limestone substrate: the role of nutritional factors examined by means of foliar diagnosis. Ann. Sci. For. 55, 567±576. Chenal, F., Depierre, A., Devillers, E., GeÂrard, B., Letz, J.M., Mathieu, Y., 1997. ReÂseau de surveillance de l'eÂtat sanitaire des foreÃts (ReÂseaux EuropeÂen). Protocole pour les observations. DeÂpartment de la Sante des ForeÃts, Of®ce National des ForeÃts, MinisteÁre de l'Agriculture de la PeÃche et de l'Alimentation. Cozzi, A., 1996. Monitoring sites. In: Bartolozzi, L., Bussotti, F., De Dominicis, V., Ferretti, M. (Eds.), Program MONITO, Intensive Monitoting of forests in Toscana. Concepts, Structure and 1995 Results. Regione Toscana±Giunta Regionale Publishers, Firenze, Italy, pp. 9±17. De Lillis, M., Federici, F.M., 1993. Gas exchange and resource-use patterns along a Mediterranean successional gradient. J. Veg. Sci. 4, 269±272. EscarreÂ, A., RodaÁ, F., Terradas, J., Mayor, X., 1999. Nutrient distribution and cycling. In: RodaÁ, F., Retana, J., Gracia, C.A., Bellot, J. (Eds.), Ecology of Mediterranean Evergreen Oak Forests. Ecological Studies, Vol. 137. Springer, Berlin, pp. 253± 269. Escudero, A., Del Arco, J.M., Garrido, M.V., 1992. The ef®ciency of nitrogen retraslocation from leaf biomass in Quercus ilex ecosystems. Vegetatio 99±100, 225±237. Ferretti, M. (Ed.), 1994. Mediterranean Forest Trees. A Guide for Crown Assessment. CEC UN/ECE, Brussels, Geneva. Ferretti, M., Bussotti, F., Cenni, E., Cozzi, A., 1999. Implementation of quality assurance procedures in the Italian programs of forest condition monitoring. Water Air Soil Pollut. 116, 371±376. Fink, S., 1991. The micromorphological distribution of bound calcium in needles of Norway spruce [Picea abies (L.) Karst.]. New Phytol. 119, 33±40. Gallardo, J.F., MartõÂn, A., Moreno, G., 1999. Nutrient use ef®ciency and resorption in Quercus pyrenaica oak coppices under different rainfall regimes of the Sierra de Gata mountains (central western Spain). Ann. For. Sci. 56, 321±331. Gutschick, V.P., 1999. Biotic and abiotic consequences of differences in leaf structure. New Phytol. 144, 3±18.
285
Hernandez, I.M., Gallardo, J.F., Santa Regina, I., 1992. Dynamics of organic matter in forests subject to a Mediterranean semiarid climate in the Duero basin (Spain): litter production. Acta Oecol. 13, 55±65. Larcher, W., Thomaser-Thin, W., 1988. Seasonal changes in energy content and storage patterns of mediterranean sclerophylls in a northernmost habitat. Acta Oecol./Oecol. Plant. 90, 271±283. Margaris, N.S., 1981. Adaptative strategies in plants dominating Mediterranean-type ecosystems. In: di Castri, F., Goodall, D.W., Specht, R.L. (Eds.), Ecosystems of the World. 11. Mediterranean-type Shrublands. Elsevier, Amsterdam, pp. 309± 315. MartõÂn, A., Gallardo, J.F., Santa Regina, I., 1996. Aboveground litter production and bioelement potential return in an evergreen oak (Quercus rotundifolia) woodland near Salamanca (Spain). Ann. Sci. For. 53, 811±818. Maurer, S., Matyssek, R., GuÈnthardt-Goerg, M.S., Landolt, W., Einig, W., 1997. Nutrition and the ozone sensitivity of birch (Betula pendula). I. Responses at the leaf level. Trees 12, 1±10. Mooney, H.A., 1981. Primary production in Mediterranean-climate regions. In: di Castri, F., Goodall, D.W., Specht, R.L. (Eds.), Ecosystems of the World. 11. Mediterranean-type Shrublands. Elsevier, Amsterdam, pp. 249±255. Oliveira, G., Correia, O., Martins-LoucËaÄo, M.A., Catarino, F.M., 1994. Phenological and growth patterns of the Mediterranean oak Quercus suber L. Trees 9, 41±46. Oliveira, G., Martins-LoucËaÄo, M.A., Correia, O., Catarino, F., 1996. Nutrient dynamics in crown tissues of cork-oak (Quercus suber L.). Trees 10, 247±254. Poli, E., Leonardi, S., Bella, R., 1970. Produzione di lettiera nella lecceta del M. Minardo (Etna) nel periodo Settembre 1970± Giugno 1974. Arch. Bot. Biogeochem. Ital. 19, 87±106. Rapp, M., 1969. Production de litieÁre et apport au sol d'eÂleÂments mineÂraux dans deux eÂcosysteÁmes meÂditerraneÂens: la foreÃt de Quercus ilex L. et la garrigue de Quercus coccifera L. Oecol. Plant. 4, 377±410. Rapp, M., Lossaint, P., 1981. Some aspects of mineral cycling in the garrigue of southern France. In: di Castri, F., Goodall, D.W., Specht, R.L. (Eds.), Ecosystems of the World. 11. Mediterranean-type Shrublands. Elsevier, Amsterdam, pp. 289±301. Robert, B., Caritat, A., Bertoni, G., Vilar, L., Molinas, M., 1996. Nutrient content and seasonal ¯uctuations in the leaf component of cork-oak (Quercus suber L.) litterfall. Vegetatio 122, 29±35. RodaÁ, F., Mayor, X., SabateÂ, S., Diego, V., 1999. Water and nutrient limitations to primary production. In: RodaÁ, F., Retana, J., Gracia, C.A., Bellot, J. (Eds.), Ecology of Mediterranean Evergreen Oak Forests. Ecological Studies, Vol. 137. Springer, Berlin, pp. 183±194. SabateÂ, S., Sala, A., Gracia, C.A., 1999. Leaf traits and canopy organisation. In: RodaÁ, F., Retana, J., Gracia, C.A., Bellot, J. (Eds.), Ecology of Mediterranean Evergreen Oak Forests. Ecological Studies, Vol. 137. Springer, Berlin, pp. 121±133. UN-ECE, 1994. Manual on Methods and Criteria for Harmonized Sampling, Assessment, Monitoring and Analysis of the Effects of Air Pollution on Forests. Programme Coordinating Centres, Hamburg and Prague. http://www.Icp-Forests.org.