JOURNAL OF FOREST SCIENCE, 58, 2012 (3): 116–122

Estimation of leaf area index and assessment of its allometric equations in oak forests: Northern Zagros,

S. Khosravi1, M. Namiranian1, H. Ghazanfari2, A. Shirvani1

1Forestry and Forest Economics Department, Faculty of Natural Resources, University of Tehran, Karaj, Iran 2Forestry Department, Faculty of Natural Resources, University of Kurdistan, , Iran

Abstract: The focus of the present study is the estimation of leaf area index (LAI) and the assessment of allometric equations for predicting the leaf area of Lebanon oaks (Quercus libani Oliv.) in Iran’s northern Zagros forests. To that end, 50 oak trees were randomly selected and their biophysical parameters were measured. Then, on the basis of destructive sampling of the oak trees, their specific leaf area (SLA) and leaf area were measured. The results showed that SLA and LAI of the Lebanon oaks were 136.9 cm·g–1 and 1.99, respectively. Among all the parameters we meas- ured, the crown volume exhibited the highest correlation with LAI (r2 = 0.65). The easily measured tree parameters such as diameter at breast height did not show a high correlation with leaf area (r2 = 0.36). Our obtained moderate correlations in the allometric equations could be due to the fact that branches of these trees had been pollarded by the local people when the branches were only 3 or 4 years old; therefore, the natural structure of the crowns in these trees might have been damaged.

Keywords: allometric relationships; destructive sampling; leaf area index; Quercus libani Oliv.; specific leaf area

One of the most commonly used parameters for are generally faster and amendable to automation, the analysis of canopy structures is leaf area index and thereby allow for a larger spatial sample to be (LAI) (Beadle 1997; López-Serrano et al. 2000; obtained (Jonckheere et al. 2004). Unfortunately, Davi et al. 2009) which is defined as the project- the lack of the required equipment for doing such ed one-sided leaf area per unit ground area (De- newly established researches in Iran in the field of blonde et al. 1994). This parameter determines the natural resources has placed obstacles in the way of amount of the plant – atmosphere interface; hence, researchers to estimate LA through using indirect it plays a crucial role in the process of exchanging methods (Adl 2007). To determine LAI, it is essen- energy and mass between the canopy and the at- tial to have an exactly accurate estimation of the to- mosphere (Weiss et al. 2004). Methods for the esti- tal LA of a tree. Though direct methods are of very mation of LAI are mainly categorized as direct and high accuracy, they have the drawback of being ex- indirect methods (Kussner, Mosandl 2000). It is tremely time-consuming; consequently, they make difficult to use direct methods, including harvest- large-scale implementation only marginally feasi- ing, allometry and litter collection (Bréda 2003). ble (Jonckheere et al. 2004). Another important Then, to obtain the LAI of a stand, a destructive aspect of tree researches is the task of figuring out sampling should be done through harvesting the to- an appropriate allometric relationship between LA tal leaf biomass of the trees to generate the total dry and other biophysical parameters of trees such as weight of the foliage (Arias et al. 2007). On the oth- diameter at breast height (DBH), tree height, crown er hand, indirect methods, in which leaf area (LA) surface area, and litter mass (Vyas et al. 2010). is inferred from observations of another variable, These relationships relating to litter mass and DBH

116 J. FOR. SCI., 58, 2012 (3): 116–122 can be used to estimate LAI by having the specific ing questions: Can biophysical parameters such as leaf area (SLA) (Gower et al. 1999). Many studies DBH, basal area, tree height, crown length, crown have shown a relationship between LAI and these projected area, and crown volume predict the tree parameters for different species (López-Serrano leaf area? And which of these parameters can be a et al. 2000; Turner et al. 2000; Tobin et al. 2006; better predictor to estimate the leaf area? Arias et al. 2007; Pokorný, Tomášková 2007; Vyas et al. 2010). However, allometric equations have rarely been investigated in oak forests so far Material and methods (Čermák et al. 2008; Babaei-Kafaki et al. 2009). The oak forests of Baneh (a small town in Iran) Study area are among the most important natural ecosys- tems located in the northern Zagros Mountains, Our investigated areas are Armardeh forests lo- and despite their importance, they have not been cated in the southwest of Baneh and northwest of studied comprehensively so far. These forests are , Iran. These forests extend from the richest in the number of oak species in com- 35°51'40" to 35°57'55"N latitude and from 45°44'20" parison with forests of central and southern Za- to 45°49'55"E longitude, with a mean altitude of gros, and Lebanon oak (Quercus libani Oliv.) is about 1,620 m a.s.l. Quercus libani, Quercus infec- one of the dominant tree species in these forests. toria and Quercus brantii are the most dominant Although the policy of Iran’s Forest and Rangeland tree species of our areas of investigation. Gene- Organization is to conserve these forests, due to rally, the watershed of Baneh is a highland region the lack of social acceptance and participation, this with long, snowy, and cold winters and mild sum- policy has not been successfully implemented yet mers. The ombrothermic curve of the monthly sum (Ebrahimi-Rastaghi 2001; Ghazanfari et al. of precipitation and the average temperature for 2004). Consequently, traditional exploitations by 2001–2010 indicate that the dry period may occur local communities living in these regions have still during five months of the year. During this decade, continued. Long-term heavy dependence of forest the mean annual precipitation was 690 mm, most dwellers upon forests resulted in the construction of which was in late autumn to early spring. Fur- of special relationships named traditional forestry thermore, the maximum and minimum tempera- (Valipour et al. 2009). Because of grinding pov- tures in the hottest and coldest months of the year erty of the local people, the villagers cut branches were 29.3°C and 4°C, respectively. off oak trees as fodder supply. This process is as follows: each traditional owner of an area of the forest divides his forest area into 3 or 4 sections; Data collection every year in the late growing season, all branch- es of trees in one of these sections are pollarded; At the beginning of our study, an appropriate thereafter, the leaf-bearing pollarded branches will stand of the abovementioned area was selected, be stored to be used in winter. The principal objec- and the goal of this research was simply explained tive of this traditional forest management pursued to the local owner of that stand in order to get his by forest owners in the region is the production of agreement for participation. In the second stage, fodder for domestic animals, firewood and timber to estimate the density of trees, three parts of (Ghazanfari et al. 2004). In addition, grazing the desired stand were chosen as its representa- prevents natural regeneration of trees (Ebrahimi- tives, and using GPS, the area of these three parts Rastaghi 2001) and leads to old even-aged stands was determined to be approximately 13 hectares. in the forests; hence, the stability of the ecosystem Then, types of species and total trees in this area would be threatened. Under present circumstanc- were evaluated. The results of the inventory for the es, basic information such as biomass, LAI and its identified species of trees showed that the densi- allometric relationships is needed to choose a cor- ties of the total trees, Quercus libani and Quercus rect forest management strategy before the valu- infectoria were 370, 302, and 68 trees·ha–1, respec- able forests of this region are totally destroyed. tively. In the third stage, 50 Lebanon oaks were This article is aimed at estimating LAI and SLA randomly selected, and their biophysical param- with the use of a direct method (destructive sam- eters such as DBH, basal area, tree height, crown pling) and at assessing useful allometric equations length, crown projected area, and crown volume to predict LA of Lebanon oak in Northern Zagros were measured. It should be noted that there are forests in Iran. We do this by addressing the follow- various methods for measuring the LAI of a tree.

J. FOR. SCI., 58, 2012 (3): 116–122 117 The direct approaches, not commonly used in such ered to have an approximately oval shape (Fig. 1). studies, are very time-consuming; moreover, for Thus, the volume of the sample trees crown was the case of LA estimation, they are expensive and calculated as follows: destructive to the sample (Vyas et al. 2010). How- 4 dc dc lc ever, in view of the fact that branches and leaves of V = ––– ∏ × –––1 × –––2 × ––– (1) c 3 2 2 2 the oak trees in our study area had been pollarded by local people, we utilized a direct method to es- where: 3 timate LAI. Thus, in the fourth stage, the numbers Vc – volume of the tree crown (m ); d , d in terms of m – two diameters of the crown based of branches of sample trees were determined after c1 c2 they had been totally pollarded by the local owner. on the measurements made along two perpen- From each sample tree, 20 branches were select- dicular directions, ed in different directions, and also from all parts lc – crown length (m). of the crown randomly; then total leaves of these LAI can be calculated using the following branches were counted. To evaluate the percentage equation: of moisture and leaf area, 10–15 leaves from each branch were randomly selected. The samples were n put into paper covers and transferred to the labora- d × ∑ AL i=1 tory. We did not use an area-to-weight relationship LAI = ––––––––––– (2) to estimate projected leaf area, but we preferred to n × 10,000 measure the leaf area of random samples for each tree. In the laboratory, projected leaf areas of the where: fresh leaf samples were determined using a leaf n ∑ AL – total projected one-sided area of leaves for 50 cho- area meter (Delta-T Devices Ltd., Burwell, Cam- i=1 2 bridge, England). After placing them in an oven at sen sample trees (m ), –1 80°C for 48 hours, the dry weight was measured. d – tree density (tree·ha ), To weigh the leaves, a scale with the accuracy of n – number of sample trees (50 trees). 0.01 g was used. Subsequently, the average SLA, de- Subsequently, four regression models were used, fined as the one-sided leaf area per unit of leaf dry and the best models were chosen based on the weight, was calculated. highest determination coefficient (r2) while r2 was also tested for significance:

Data analysis Linear: Y = a + bX (3) Quadratic: Y = a + bX + cX2 (4) When preparing the crown images of sample trees in four directions, the tree crown was consid- Exponential: Y = exp(a + bX) (5) Multiplicative: Y = aXb (6) where: X, Y – independent and dependent variables, respec- tively, a – interception of the line with Y axis, b, c – regression coefficients (Zar 1996).

Independent variables in this paper are DBH, ba- sal area, tree height, crown length, crown projected area, and crown volume, and the dependent vari- able is the projected leaf area for each tree.

Results and Discussion

All the parameters of fifty sample trees are doc- umented in Table 1. The range of SLA is between Fig. 1. The oval shape of the tree crown in the study area 63.6 and 213.4 cm2·g–1. The average projected area

118 J. FOR. SCI., 58, 2012 (3): 116–122 Table 1. The parameters of the sample trees of Lebanon oak (n = 50)

Mean Maximum Minimum SE DBH (cm) 28.10 49.40 13.00 1.20 Basal area (m2) 0.27 0.77 0.05 0.02 Height of tree (m) 9.50 12.90 4.50 0.25 Crown projected area (m2) 6.00 15.10 1.10 0.48 Crown length (m) 6.60 10.60 1.50 0.29 Volume of crown (m3) 28.10 90.10 2.30 2.89 SLA (cm2·g–1) 136.90 213.40 63.60 4.56 Projected leaf area of sample tree (m2) 63.52 226.74 25.47 5.24

DBH – diameter at breast height, SLA – specific leaf area, SE – standard error of leaves is 63.52 m2·tree–1. Therefore, consider- height was investigated (López-Serrano et al. ing the tree density of Lebanon oak in the study 2000; Turner et al. 2000; Law et al. 2001; Adl area, which is 302 trees·ha–1, LAI of Lebanon oak 2007; Arias et al. 2007; Pokorný, Tomášková would be 1.99. When conducting a similar study 2007; Calvo-Alvarado et al. 2008; Babaei-Ka- on forests of southern Zagros, the trees of which faki et al. 2009), and less attention was devoted to were not pollarded by the local people, Adl (2007) the tree’s crown-related parameters (Laubhann et found the value of 171.2 cm2·g–1 for two-sided al. 2010; Vyas et al. 2010). But, with the considera- SLA of Quercus brantii. Moreover, his results also tion of specific conditions of our investigated area, showed that LAI for this species, with a density of which is under traditional management, besides 90 trees·ha–1, is equal to 1.1, which is less than the investigating other parameters, we also directed value we calculated for Quercus libani Oliv. It is a our attention to the crown-related parameters, point of note that, in view of the fact that the local particularly the crown volume. Our results indicate residents cut the branches off oak trees in a period that the easily-measurable tree parameters such of 3 or 4 years, the estimated value of LAI for the as DBH do not show a high correlation with leaf explored forests is only for the growth of branches area. This point was also confirmed by some previ- within this time period. ous reports (Gower et al. 1999; Khan et al. 2005; In Fig. 2, allometric relationships were developed Babaei-Kafaki et al. 2009). For instance, though between the leaf area and the biophysical param- Vyas et al. (2010) introduced a low r2 in the rela- eters such as DBH (a), basal area (b), height of the tion between DBH and LA, estimated an excellent tree (c), crown length (d), crown projected area (e), correlation between LA and the crown spread area. and crown volume (f). They were highly significant In another study on Quercus macranthera affected (P < 0.001). As shown dotted in a model of Fig. 2, by traditional pollarding of the tree, Babaei-Kafa- the distribution of the leaf area increases at di- ki et al. (2009) reported weak allometric equations ameters of about 25 cm or more; this observation between LAI, DBH and tree height (r2 = 0.28 and is also clearly true of the other models. It should 0.26, respectively). Since Armardeh forests can be be pointed out that replacing the basal area with considered as a traditional silvopastoral system, DBH did not increase the determination coefficient the moderate correlations of allometric equations (model b). According to model (f) of Fig. 2, the found in this study could be explained in light of value of r2 in a bivariate regression model between the fact that the branches had been pollarded for the crown volume and the leaf area was 0.65, which a period of 3 or 4 years; hence, the natural struc- was the highest coefficient of determination among ture of the tree crown could be damaged. In fact, the abovementioned models. It is worth mention- all branches of the old or young trees were only 3 or ing that models (a) and (b) are multiplicative ones; 4 years old. Branches and leaves do not have an op- models (c), (e) and (f) are quadratic equations; and portunity for continuous and simultaneous growth model (d) is exponential. along with the trunk of the tree growing both in In most of the previous studies, the correlation diameter and height. Therefore, in any stage of the between the leaf area and the diameter at breast tree growth, branches remain very young. While

J. FOR. SCI., 58, 2012 (3): 116–122 119 (a) 250 0.9383 (b) 250 0.4691 LALA = 2.5543 = 2.5543 DBH0.9383 DBH LA =LA 112.35 = 112.35 BA0.4691 BA 2 2 200 rr² = = 0.36 0.36 200 r² =r 0.36 = 0.36 ) ) 2 2 150 150 LA (m2) LA (m LA (m 100 LA (m2) 100

50 50

0 0 10 20 30 40 50 0 0.2 0.4 0.6 0.8 DBH (cm) BA (m2)

2 0.15CL (c) 250 LALA = 2.7378= 2.7378 TH TH2–37.191 - 37.191 TH TH + 161.12 + 161.12 (d) 250 LALA = 20.86= 20.86 e 0.15CH e 2 2 r²r = = 0.45 0.45 r²r == 0.400.40 200 200

) 150 ) 150 2 2 LA (m2) 100 LA (m2) 100 LA (m LA (m 50 50

0 0 4 6 8 10 12 14 1357911 TH (m) CLCH (m) (m)

(e) 2 (f) 2 250 LA =LA 0.6515 = 0.6515 CPA CSA2 – 1.112 - 1.115 CPA CSA + 39.517 + 39.517 250 LALA = =0.0139 0.0139 CV2 CV + + 0.3687 0.3687 CV CV + + 36.512 36.512 2 2 200 r = 0.62r² = 0.62 200 r²r = = 0.65 0.65 ) )

2 150 2 150

LA (m2) 100 LA (m2) 100 LA (m LA (m 50 50

0 0 0 4 8 12 16 0 20 40 60 80 100 CPACSA (m (m2)2) CV (m3)

Fig. 2. Allometric relationships between leaf area (LA) and biophysical parameters such as diameter at breast height (DBH – a), basal area (BA – b), height of the tree (TH – c), crown length (CL – d), crown projected area (CPA – e), and crown volume (CV– f)

effects of traditional forest management have not area and biophysical parameters were highly sig- been fully identified yet, it is evident that these nificant, however, the r2 values were not very high practices have influenced the forest structure and (r2 = 0.36–0.65). As compared with easily measur- tree characteristics (Valipour et al. 2009). able variables such as DBH and basal area, related variables to the crown of trees such as crown pro- jected area and crown volume had better capability Conclusion to predict the leaf area at an individual tree level. The proposed allometric relationships in this re- The leaf area index (LAI) was estimated and the search are most likely affected by pollarding of the useful allometric equations for predicting the leaf tree. Therefore, the results of this study should be area of Lebanon oak grown in Iran’s Northern considered with caution, as the data correspond Zagros forests were also assessed. All regression only to one stand within the range covered by the models describing the relationship between leaf habitat of the pollarded oak. For this reason, fur-

120 J. FOR. SCI., 58, 2012 (3): 116–122 ther experiments, particularly those with the aim in predicting LAI and carbon allocation in forests. Agri- of making a comparison between LAI of trees in cultural and Forest Meteorology, 149: 349–361. virgin, natural and disturbed forests of the study Deblonde G., Penner M., Royer A. (1994): Measuring area, might be of significant scientific and practical leaf area index with the Li-Cor LAI-2000 in pine stands. interest. Ecology, 75: 1507–1511. Ebrahimi-Rastaghi M. (2001): The Rule of Baneh (Pistacia atlantica) in Management of Beyond Northern Iranian Acknowledgements Forests. Technical Report. Forest and Rangeland Organiza- tion, Tehran: 23. (in Persian) The authors would like to thank the Centre for Ghazanfari H., Namiranian M., Sobhani H., Mohajer Research & Development of Northern Zagros For- R.M. (2004): Traditional forest management and its ap- ests and University of Tehran for providing an op- plication to encourage public participation for sustainable portunity for participating in the this project. We forest management in the Northern Zagros Mountains of also wish to thank G. Khosravi, A. Khosravi, Kurdistan province, Iran. Scandinavian Journal of Forest S. Babaei and inhabitants of Armardeh village for Research, 19: 65–71. their assistance during the experiments, and A. Sa- Gower S.T., Kucharik C.J., Norman J.M. (1999): Direct faei for revising the language. We would also like and indirect estimation of leaf area index, FAPAR, and net to acknowledge the thoughtful comments of two primary production of terrestrial ecosystems. Remote anonymous reviewers. Sensing Environment, 70: 29–51. Jonckheere I., Fleck S., Nackaerts K., Muys B., Coppin P., Weiss M., Baret F. (2004): Review of methods for in situ References leaf area index determination – Part I. Theories, sensors and hemispherical photography. Agricultural and Forest Adl H.R. (2007): Estimation of leaf biomass and leaf area Meteorology, 121: 19–35. index of two major species in Yasuj forests. Iranian Journal Khan M.N.I., Suwa R., Hagihara A. (2005): Allometric of Forest and Poplar Research, 15: 417–426. (in Persian) relationships for estimating the aboveground phytomass Arias D., Calvo-Alvarado J., Dohrenbusch A. (2007): and leaf area of mangrove Kandelia candel (L.) Druce trees Calibration of LAI-2000 to estimate leaf area index (LAI) in the Manko Wetland, Okinawa Island, Japan. Trees, 19: and assessment of its relationship with stand productivity 266–272. in six native and introduced tree species in Costa Rica. Kussner R., Mosandl R. (2000): Comparison of direct and Forest Ecology and Management, 247: 185–193. indirect estimation of leaf area index in mature Norway Babaei-Kafaki S., Khademi A., Mataji A. (2009): Rela- spruce stands of eastern Germany. Canadian Journal tionship between leaf area index and physiographical and of Forest Research, 30: 440–447. edaphical condition in a Quercus macranthera stand (Case Laubhann D., Eckmüllner O., Sterba H. (2010): Applica- study: Andebil’s forest, Khalkhal). Iranian Journal of Forest bility of non-destructive substitutes for leaf area in different and Poplar Research, 17: 280–289. (in Persian) stands of Norway spruce (Picea abies [L.] Karst.) focusing Beadle C.L. (1997): Dynamics of leaf and canopy develop- on traditional forest crown measures. Forest Ecology and ment. In: Nambiar E.K.S., Brown A. (eds): Management Management, 260: 1498–1506. of Soil, Nutrient Water in Tropical Plantation Forests. Law B.E., Van Tuyl S., Cescatti A., Baldocchi D.D. Australia, ACIAR Monograph 43: 169–211. (2001): Estimation of leaf area index in open-canopy Pon- Bréda J.J.N. (2003): Ground-based measurements of leaf area derosa pine forests at different successional stages and index: a review of methods, instruments and current con- management regimes in Oregon. Agricultural and Forest troversies. Journal of Experimental Botany, 54: 2403−2417. Meteorology, 108: 1–14. Calvo-Alvarado J.C., McDowell N.G., Waring R.H. López-Serrano F.R., Landete-Castillejos T., Martínez- (2008): Allometric relationships predicting foliar biomass Millán J., Del Cerro-Barja A. (2000): LAI estimation of and leaf area: sapwood area ratio from tree height in natural pine forest using a non-standard sampling technique. five Costa Rican rain forest species. Tree Physiology,28 : Agricultural and Forest Meteorology, 101: 95–111. 1601–1608. Pokorný R., Tomášková I. (2007): Allometric relation- Čermák J., Tognetti R., Nadezhdina N., Raschi A. ships for surface area and dry mass of young Norway (2008): Stand structure and foliage distribution in Quercus spruce aboveground organs. Journal of Forest Science, pubescens and Quercus cerris forests in Tuscany (central 53: 548–554. Italy). Forest Ecology and Management, 255: 1810–1819. Tobin B., Black K., Osborne B., Reidy B., Bolger T., Davi H., Barbaroux C., Francois C., Dufrêne E. (2009): Nieuwenhuis M. (2006): Assessment of allometric al- The fundamental role of reserves and hydraulic constraints gorithms for estimating leaf biomass, leaf area index and

J. FOR. SCI., 58, 2012 (3): 116–122 121 litter fall in different-aged Sitka spruce forests. Forestry, (LAI) of two important tropical species (Tectona grandis 79: 453–465. and Dendrocalamus strictus). Journal of Forestry Research, Turner D.P., Acker S.A., Means J.E., Garman S.L. (2000): 21: 197–200. Assessing alternative allometric algorithms for estimating Weiss M., Baret F., Smith G.J., Jonckheere I., Coppin P. leaf area of Douglas-fir trees and stands. Forest Ecology (2004): Review of methods for in situ leaf area index (LAI) and Management, 126: 61–76. determination – Part II. Estimation of LAI, errors and sam- Valipour A., Namiranian M., Etemad V., Ghazanfari pling. Agricultural and Forest Meteorology, 121: 37–53. H. (2009): Relationship between diameter, height and Zar J.H. (1996): Biostatistical Analysis. 3rd Ed. Upper Saddle geographical aspects with bark thickness of Lebanon oak River, Prentice Hall: 662. tree (Quercus libani Oliv.) in Armardeh, Baneh (Northern Zagros of Iran). Research Journal of Forestry, 3: 1–7. Received for publication Ferbruary 13, 2011 Vyas D., Mehta N., Dinakaran J., Krishnayya N.S.R. Accepted after corrections January 2, 2012 (2010): Allometric equations for estimating leaf area index

Corresponding author: Ing. Sheyda Khosravi, M.Sc., University of Tehran, Faculty of Natural Resources,Forestry and Forest Economics Department, Shahid Chamran Blvd., P. O. Box 31585-4314, Karaj, Iran e-mail: [email protected]

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