Frankincense tapping reduced photosynthetic carbon gain in Boswellia papyrifera (Burseraceae) trees

Forest Ecology and Management 278 (2012) 1–8

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Frankincense tapping reduced photosynthetic carbon gain in Boswellia papyrifera (Burseraceae) trees Tefera Mengistu a,b,⇑, Frank J. Sterck a, Niels P.R. Anten c, Frans Bongers a a

Wageningen University, Centre for Ecosystem Studies, Forest Ecology and Forest Management, PO Box 47, 6700AA Wageningen, The Netherlands Hawassa University, Wondo Genet College of Forestry and Natural Resources, PO Box 128, Shashemene, Ethiopia c Wageningen University, Centre for Crop Systems Analysis, PO Box 430, 6700AK, The Netherlands b

a r t i c l e

i n f o

Article history: Received 2 March 2012 Received in revised form 24 April 2012 Accepted 25 April 2012 Available online 29 May 2012 Keywords: Boswellia Crown assimilation Ethiopia Frankincense Plant trait Tapping

a b s t r a c t Whole-crown carbon gain depends on environmental variables and functional traits, and in turn sets limits to growth sinks of trees. We estimated the annual whole-crown carbon gain of trees of the species Boswellia papyrifera, which are tapped for frankincense, by integrating leaf photosynthetic rates over the total leaf area and leaf life span. We examined the effect of tapping on total leaf area and leaf photosynthesis and, in turn, on carbon gain and resin yield for trees of a dry highland population and a wetter lowland population. Highland and lowland trees had similar total leaf area, but highland trees had higher photosynthetic rates per unit leaf area than lowland trees since they received more light and had higher photosynthetic capacities. Highland trees therefore achieved a higher annual carbon gain than lowland trees, despite a shorter rainy season and shorter leaf lifespan. Intensive tapping reduced crown leaf area and the carbon gain in the lowland trees, but not in highland trees. These results highlight how the interplay between local conditions and functional traits determine regional variation in tree productivity. However, such differences in productivity and carbon gain did not influence frankincense yield across sites. We conclude that tapping B. papyrifera trees reduces annual carbon gain but the extent differs among different populations. Ó 2012 Elsevier B.V. All rights reserved.

1. Introduction Several tree species in the plant families of the Pinaceae (e.g. pines), Euphorbiaceae (e.g. rubber tree), Mimosaceae (e.g. Acacia) and Burseraceae (e.g. Boswellia) produce gum and resin upon bark wounding or tapping. Boswellia trees of the Burseraceae family dominate large areas of dry woodlands in eastern and central Africa and elsewhere, and produce frankincense which is tapped by local communities for local or international markets (Ogbazghi et al., 2006; Tadesse et al., 2007; Mertens et al., 2009). Tapping creates a carbon sink that may be at the cost of growth sinks, including vegetative growth and reproduction (Cannell and Dewar, 1994; Rijkers et al., 2006; Silpi et al., 2006; Chantuma et al., 2009). Moreover, dry woodland trees may suffer from irregular rainfall patterns, thus creating more limiting growth conditions during some years than others (Murphy and Lugo, 1986; Bullock et al., 1995; Vanacker et al., 2005). Climate change may affect rainfall patterns and re-

⇑ Corresponding author at: Hawassa University, Wondo Genet College of Forestry and Natural Resources, PO Box 128, Shashemene, Ethiopia. Tel.: +251 0912021945; fax: +251 0461191499. E-mail addresses: [email protected] (T. Mengistu), Frank.sterck@ wur.nl (F.J. Sterck), [email protected] (N.P.R. Anten), [email protected] (F. Bongers). 0378-1127/$ - see front matter Ó 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.foreco.2012.04.029

duce the ability of trees to acquire and supply carbon to the different carbon sinks (Lacointe, 2000; Hély et al., 2006; Bolte et al., 2010). It is a major challenge to understand how resin tapping will affect the ability of trees to maintain their vegetative status and photosynthetic capacity and, in turn, their ability to acquire carbon and produce more resin in the future. For resin producing trees, the whole-crown carbon gain depends on a number of functional plant traits, environmental conditions and tapping intensity. Functional traits that affect crown carbon gain include leaf photosynthetic rates, total leaf area and average leaf lifespan (Kikuzawa and Lechowicz, 2006; Selaya and Anten, 2010). However, it is not clear how they scale-up to crown carbon gain in the field (Poorter and Bongers, 2006) and vise versa. This information is especially limited for tropical dry forests and dry woodland trees (Yoshifugi et al., 2006; Kushwaha et al., 2010). In such systems, the seasonality in rainfall is expected to impact the annual carbon gain strongly, particularly when trees lose leaves during a long dry season (Kikuzawa and Lechowicz, 2006). Moreover, the intensive tapping of resin may create a major carbon sink to the system. This carbon drain down tunes the production of seeds (Rijkers et al., 2006), and thus potentially also the production of leaves or the maintenance of proteins that are required for photosynthesis. In turn, such a reduction in growth sink may also impact the future carbon gain and resin yield, as has been

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suggested for the frankincense producing trees (Rijkers et al., 2006). In the present study, we present an experiment that links frankincense tapping and crown functional traits to carbon gain and resin yield for frankincense trees from two populations. One population occurred at a lower altitude (810–900 masl) with a longer and wetter rainy season than the population at higher altitude (1400–1650 masl). These two populations represent the climatic extremes of this species in Ethiopia. The objective of this study was to determine the effects of frankincense tapping on crown carbon gain and resin yield and the underlying functional traits. Our intention, however, is to assess the impact of tapping on leaf and crown traits and on photosynthetic carbon gain, and not to make exact predictions of carbon gain. Moreover, we evaluated how the environmental conditions differed between both populations, and set different constraint on carbon gain and resin yield. Because frankincense, like most resins, is rich in carbon (Hamm et al., 2005; Mertens et al., 2009), tapping is expected to drain carbon reserves limiting the carbon availability for leaf formation. We thus expect a higher tapping intensity to reduce crown leaf area and hence canopy carbon gain. We also expect that trees in the drier highland area, with a shorter rainy season, will be restricted in the crown carbon gain by a limited leaf lifespan, and thus be more affected by tapping compared to lowland trees. To test these hypotheses, we measured leaf and canopy traits of Boswellia papyrifera trees in contrasting sites under different tapping intensities.

2. Materials and methods 2.1. Description of the study sites We studied leaf and crown traits and their impact on carbon gain in B. papyrifera of the family Burseraceae in two contrasting woodlands in northern Ethiopia. Abergelle is at an altitude of 1400–1650 masl (hence referred to as ‘‘highland’’ site) and Metema is at a lower altitude of 810–900 masl (referred to as ‘‘lowland’’ site). The highland site is drier and has erratic rainfall with a short-

Fig. 1. Phenological patterns of Boswellia papyrifera in relation to rainfall and temperature in Metema (lowland, dashed line) and Abergelle (highland, solid line) sites in Ethiopia. The horizontal lines are temperature curves (axis on the right side) and vertical lines are rainfall curves (axis on the left). Codes for successive phenological periods include: FL = flowering, FR = fruiting, BB = leaf bud breaking, CC = pre-leaf fall color change and LS = leaf shedding. Meteorological data is average over a period of 20 years.

er wet season than the lowland site (Fig. 1). The highland site is dominated by hills, and compared to the lowland and is characterized by soils that are similar in texture, but shallower (on average 15.3 cm versus 27.7 cm) and poorer in cation exchange capacity (CEC 39 versus 48 meq/100 g soil) (Eshete et al., 2011) thus limiting plants to form deep roots. The two sites have similar phosphorus and potassium contents in the soil (Birhane et al., 2010), but the highland site has a higher nitrogen content in the soil (0.29% versus 0.19% soil mass, Eshete et al., 2011). The vegetation at the highland site is categorized as Combretum–Terminalia and Acacia– Commiphora woodlands dominated by B. papyrifera, Acacia etbaica, Terminalia brownii and Lannea fruticosa. The vegetation of the lowland site is categorized as Combretum–Terminalia woodland where Acacia spp., Balanites aegyptiaca, B. papyrifera, Combretum spp., Stereospermum kunthianum and Terminalia brownii are the dominant species. 2.2. Tapping and data collection We selected trees with a DBH of 20 ± 3 cm for the experiment. For each site, the experimental trees were randomly allocated to one of three treatments, i.e. 0 incisions (control), 6 incisions (low tapping intensity) and 12 incisions (high tapping intensity), following traditional tapping techniques. Such tapping starts with a superficial cut of the bark at different locations along the stem. The number of locations is here referred to as the number of incisions. With every resin collection round during the dry season, the incisions are deepened and/or enlarged to open the resin ducts and thus stimulate resin production. The incision on the bark triggers sink stimulation similar to what has been shown in rubber production (Chantuma et al., 2009) and drains the resin (frankincense) to exude (Plate 2). Tapping starts early in October and lasts till the beginning of June and is thus practiced during the dry season (Fig. 1), when trees of this species carry no leaves. While the same locations on the stem are used during a given dry season, different locations are selected in the next dry season. Traditionally, tappers wound the bark with a small hand axe such that the frankincense exudes. Tappers decide the number of cuts usually ranging from 3 to 15 incisions depending on tree size. Six and 12 incisions thus represent the lower and higher tapping intensities, respectively for the selected diameter class in our study area. The tapping treatments were applied over two successive dry seasons, but with seven collection rounds in 2007–2008 and 14 collection rounds in 2008–2009. In the highland, we established one plot and selected 10 trees per tapping treatment for gas exchange out of which five from each tapping treatment were also used for estimating total leaf area. In the lowland, we established four plots with a priori assumption of local variation and five trees were selected per tapping treatment in each plot for both gas exchange and total leaf area. Boswellia is a tree up to 13 m height with leaf and floral buds protruding on the apices along the branches. The tree is monoecious and has compound leaves that contain 9–20 pinnate, veined, leaflets supported by petioles (Plate 1). To estimate the total leaf area of a tree, we counted the total number of apices per tree, the number of leaves per apex (on a sample of three apices per tree), the number of leaflets per leaf (on a sample of three leaves per tree), and measured leaflet area (on five randomly selected leaflets per tree) using ADC model AM 100 leaf area meter (ADC, Bioscientific, Hoddesdon, UK). For each tree, total leaf area was calculated as the product of the number of apices, the number of leaves per apex, the number of leaflets per leaf and the average leaflet area after full expansion. To estimate the leaf lifespan and crown leaf area over the wet season (trees were without leaves during the dry season), we counted leaves and measured leaf size weekly on three apices on

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Plate 1.

Plate 2.

each tree. To determine effective leaf lifespan, leaves were considered ‘‘born’’ when trees had established half of their total crown leaf area at full leaf expansion. Leaves were assumed to be ‘‘dead’’ after they changed color from green to yellow, because this is assumed a critical stage beyond which leaves may no longer achieve a positive daily carbon balance (Reich et al., 2009). We calculated the effective leaf lifespan as the number of days between leaf birth and leaf death.

2.2.1. Gas exchange measurements Gas exchange and environmental conditions were measured on six separate days on highland site trees and 19 days on lowland site trees during the wet season (see also Mengistu et al., 2011). Every day, gas exchange was measured on two fully expanded leaflets of selected trees in the morning (0800–1100 h), and this procedure was repeated around noon (1200–1400 h) and in the afternoon (1500–1700 h), using an open portable gas exchange

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system, LcPro (ADC, Bioscientific, Hoddesdon, UK). To avoid sampling bias, an equal number of trees was randomly selected from each tapping treatments for each measurement day. For all these days, we also measured radiation using LcPro PAR sensor over the same day hours as in the case of the photosynthesis measurements. Moreover, the temperature, relative humidity and leaf water potentials were also measured, but their influence on leaf photosynthesis is presented in Mengistu et al. (2011) and not here. In addition to these in situ measurements under ambient conditions, we measured light responses curves for five leaves in each site. For this purpose, photosynthesis was measured for a range of light values, using a detachable mixed Red/Blue LED light source chamber (2  3 cm) on top of the LcPro leaf chamber. Leaves were enclosed in a leaf chamber without any light for 30 min and, consequently, light levels were increased progressively over a realistic light intensity range, i.e. from 0, 50, 100, 200 to 400 and then up to 2000 using steps of 200 lmol/m2/s. For each measured leaf, a light response curve was established using the non-rectangular hyperbola (Thornley and Johnson, 1990).

A¼

/I þ Amax 

qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi fð/I þ Amax Þ2  ð4h/IAmax Þg 2h

 Rd

ð1Þ

In this model, the irradiance (I) is the independent variable and the light saturated photosynthetic rate (Amax), dark respiration rate (Rd), the quantum yield (/), and the curvature factor (h) are estimated by minimizing the sum of squares. 2.2.2. Integrating carbon gain We applied a simple scaling protocol to assess the degree to which tapping or site-related differences in leaf and crown traits affected seasonal carbon gain of trees. We estimated the daily photosynthetic rates per unit leaf area by integrating the three photosynthetic measurements under ambient conditions over the day. Since we took three periodic measurements during the day (each assumed to represent 1/3 of the day), we integrated each measurement for 4 h. Subsequently, we estimated the daily carbon gain and indicated wet season carbon gain (dry season is leafless) of leaves by integrating the daily photosynthetic rates in to the leaf lifespan. We can write this as follows:

Aac ¼ 14; 400ðA1 þ A2 þ A3 ÞTLA  LLS

ð2Þ

Here, Aac stands for the whole crown carbon gain, 14,400 stands for the number of seconds in 4 h; A1, A2 and A3 photosynthetic rate per leaf area averaged over two leaflets for the morning, noon and afternoon, respectively, TLA for the total leaf area and LLS for the effective leaf lifespan. We thus assumed that leaves of the same tree were formed and dropped on the same day. Many studies used vertical integration against radiation gradient to determine total crown carbon gain (Baldocchi, 1993; Bonan, 1995; Nasahara et al., 2008), and distinguished between the sunlit and shaded leaf parts (De Pury and Farquhar, 1997; Wang and Leuning, 1998; Selaya and Anten, 2010). Because frankincense trees exhibit little self-shading, we assumed that the selected leaves represent the light exposure of the total leaf population relatively well, which is a reasonable assumption for the relatively small and open crowns of the study species (Plate 1). Also, six leaflets were selected randomly for gas exchange measurements of one tree on one measurement day (see above) to account for possible shading effects. 2.3. Data analysis A general linear model with univariate analysis and Tukey posthoc multiple comparisons was used to test the effect of tapping intensity on plant traits driving annual carbon gain. The analysis

was done by including the interaction between sites and tapping intensity as a fixed factor. The relationship between crown carbon gain and frankincense yield was tested by linear regression models. Data was analyzed using SPSS (PASW 17.0 for Windows statistical software package).

3. Results 3.1. Phenology Leafing and senescence started earlier in the lowland than in the highland (Fig. 1). Nevertheless, the estimated effective crown leaf lifespan was 81 days in the lowland and only 69 days in the highland. In both sites, leaf bud burst already started before the actual onset of the first rains. Flower and fruit production occurred during the leafless dry period, but sites differed in their timing (Fig. 1). Fruit bud initiation started early during the dry season shortly after leaf shedding in the lowland, whereas it occurred at the end of the dry season in the highland. 3.2. Tapping effects on leaf area and carbon gain Tapping reduced crown leaf area in the lowland, but not in the highland. This reduction in crown leaf area indicated lower crown assimilation for heavily tapped trees in the lowland (Fig. 2; Table 1). The mean leaf photosynthetic rate was higher in the highland (7.1 lmol/m2/s) than in the lowland (4.9 lmol/m2/s) and this was reflected in a higher integrated daily photosynthetic rate (0.35 and 0.23 molCO2/m2/d for the high and lowland site, respectively). Light saturated rates of photosynthesis (Amax) were higher at the highland than at the lowland site (P = 0.008) while the other parameters of the light response of photosynthesis did not differ significantly between sites (Eq. (1); Table 2). The higher photosynthetic capacities as well as a higher light interception (less cloud cover) resulted in higher photosynthetic rates in the highland compared to the lowland (Fig. 2). With a similar average crown leaf area in the two sites, the shorter crown leaf lifespan of trees in the highland apparently was more than compensated by higher daily photosynthetic rates (Fig. 2B, D, and E). Neither crown assimilation nor crown leaf area was significantly correlated with frankincense yield in both sites (Fig. 3).

4. Discussion Our results indicate that the effects of tapping on tree carbon gain are site specific, since they had a negative effect on carbon gain in the lowland trees but not in the highland trees. The reduction in carbon gain in the lowland trees was primarily mediated by the tapping impact on crown leaf area. We showed the effects of resin tapping on leaf and crown traits and, subsequently, the degree to which these effects impact the carbon gain of trees. Earlier studies (Rijkers et al., 2006) have documented the impact of resin tapping on reproductive effort but not on crown leaf area. We expected a higher tapping intensity to reduce the crown leaf area and hence crown carbon gain. On the other hand, photosynthesis and sink utilization of carbohydrates are tightly coordinated in some plants (Fujii and Kennedy, 1985; Ainsworth and Bush, 2011). In our study, however, heavy tapping reduced carbon gain, but only in the lowland. Leaf assimilation rate was, however, higher in the highland and unaffected by tapping. This indicated higher crown assimilation rate, despite a shorter leaf lifespan. Moreover, we did not observe any effect of carbon gain or site on the annual resin yield (F-test, F = 1.9, P = 0.2 for site effects on yield).

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Fig. 2. Light capture (A), daily photosynthetic rates (B), light use efficiency (C), effective crown leaf lifespan (D), crown leaf area (E) and estimated crown assimilation (F) in relation to different levels of tapping intensity. Tapping included 6 or 12 incisions, and these treatments were compared with the control (without tapping) across sites. Different letters indicate across site differences after post-hoc test. Bars indicate mean ± SE.

Timing of leaf and flower bud initiation, and crown leaf longevity were important phenological differences between the two areas (Fig. 1). In both study sites, leaf bud burst started before the first rain of the wet season. This phenomenon was earlier recorded for tropical dry forest trees (Rivera et al., 2002; Elliott et al., 2006; Williams et al., 2008), and it has been suggested that such trees either have access to deep soil moisture or have a large stem water storage (Borchert, 1994; Elliott et al., 2006; Williams et al., 2008; Kushwaha et al., 2010). We expected trees in the drier highland area, with a shorter rainy season, to be restricted in crown carbon gain as a result of limited crown leaf lifespan (Suárez, 2010), and also to be more affected by tapping. This was clearly not the case. Despite their shorter leaf lifespan, trees of the drier highland attained substantially higher crown assimilation. This difference was the product of the greater light availability (less cloud cover) and the larger photosynthetic capacities of trees at the highland site. These two factors more than compensated for the shorter leaf lifespan at this site. From Table 2 it was also clear that the photosynthetic capacity was higher in the highland than the lowland (highland = 22.14 ± 1.3 lmol/m2/s and lowland = 14.89 ± 0.98 lmol/ m2/s; P = 0.008). In the lowland, with higher rainfall and a longer wet season, trees achieved a lower annual crown carbon gain.

Surprisingly, rainfall differences alone could not explain the observed difference in annual carbon gain. It seems that a combination of light limitation and shifts in leaf physiological traits have more significant effect on carbon gain differences between these two sites. While the light limitation by clouded weather has been demonstrated for trees of rain forests (Clark and Clark, 1994), studies that demonstrate such strong light limitation by persistent cloudiness for a dry woodland system are limited. Total leaf area and carbon gain of lowland trees were negatively affected by intensive dry season tapping. This suggests a trade-off between tapping and leaf formation: the carbohydrate used for resin production may be at the cost of the carbohydrate invested in leaf area, comparable to the resin production to reproduction trade-off (Rijkers et al., 2006) and rubber production to growth trade-off (Silpi et al., 2006; Chantuma et al., 2009). In a separate study (Mengistu et al., unpublished), we showed that tapping also reduced the reproductive output in the lowland but not in the highland. These results clearly indicate that tapping reduces the leaf area production. This negative effect was, however, site-specific and possibly related to either the lower annual carbon gain in the lowland site or physiological adaptations to specific environmental conditions. In contrast, highland trees possibly buffered the impact

88 ± 6ab 9 ± .38a 17 ± .7a 81 ± 1b 19.5 ± 1.5a 0.018 ± .002a 4.94 ± .14a 0.23 ± .02b 26.9 ± 2.5b 555 ± 82a 16.6 ± 2.5b 370 ± 62a 86 ± 6ab 9 ± .32a 19 ± .5a 79 ± 1b 26.5 ± 1.8ab 0.021 ± .002a 4.79 ± .14a 0.23 ± .02b 40.8 ± 3.9a 777 ± 119ab 23.3 ± 3.6ab 315 ± 62a

Control

75 ± 12a 11 ± .48a 16 ± .8a 67 ± 1a 29.4 ± 4.2b 0.019 ± .002a 7.95 ± .27b 0.38 ± .04a 38.5 ± 7a 944 ± 167ab 28.3 ± 5ab 373 ± 79a 63 ± 7a 11 ± .44a 16 ± .6a 70 ± 1a 42.9 ± 4.7c 0.025 ± .03a 6.30 ± .25b 0.29 ± .03a 47.3 ± 5.8a 1048 ± 198ab 31.5 ± 5.9ab –

Lowland

Highland

Pvalue

Sign.

H (curvature) Amax (max. photosynthesis) / (slope-quantum yield) Rd (respiration rate – dark) C (compensation point)

0.48 ± 0.008 14.89 ± 0.989 0.06 ± 0.013 3.23 ± 0.686 73 ± 5.55

0.47 ± 0.008 22.14 ± 1.291 0.086 ± 0.020 2.17 ± 0.550 55 ± 18.3

0.44 0.008 0.43 0.27 0.39

ns ⁄⁄⁄

ns ns ns

6.3*** 3.6** 2.8* 5.7*** 0.8*** 0.9ns 0.07ns 6.03*** 3.7** 2.6* 2.6* 1.3ns 3.1* 0.6ns 0.1ns 1.4ns 2.6ns 0.9ns 0.26ns 0.6ns 5.8** 1.7ns 1.7ns 1.3ns Number Number Number Days cm2 molCO2/mol lmol/m2/s molCO2/m2/d m2/tree molCO2/tree/yr kg/tree/yr g/tree Apex/tree Leaf/apex Leaflet/leaf Leaf lifespan Leaflet area Light use efficiency Photosynthetic rates Photosynthesis/day Crown leaf area Crown assimilation Carbon gain Incense yield

11.68** 7.13** 6.1* 119.1*** 30.3*** 0.3ns 0.000*** 26.33*** 0.9ns 4.95* 4.95* 1.9 ns

Fig. 3. Frankincense yield predicted from crown leaf area (upper panels) and crown assimilation (lower panels) using linear regression from the two tapping levels. Frankincense yield was unaffected by either of the crown parameters and intensity of tapping.

ns, Non-significant. * 0.01 < P < 0.05. ** 0.001 < P < 0.01. *** P < 0.001.

6 Incision

Parameters

80 ± 11a 10 ± .24a 19 ± .7a 70 ± 1a 31.8 ± 2.5bc 0.018 ± .03a 6.96 ± .26b 0.36 ± .05a 47.1 ± 8.3a 1270 ± 156b 38.0 ± 7.7a 565 ± 50a

Lowland

12 Incision 6 Incision Highland

Control

Site  tapping Tapping Units

Site

Table 2 Photosynthetic light response curve parameter values (mean ± S.E) for B. papyrifera leaves from Abergelle (highland) and Metema (lowland) areas.

118 ± 6b 10 ± .40a 19 ± .6a 82 ± 2b 22.6 ± 1.3a 0.019 ± .001a 5.16 ± .17a 0.22 ± .02b 50.6 ± 4.6a 1005 ± 154ab 30.2 ± 4.6ab –

12 Incision

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Plant traits

Table 1 Leaf and crown traits of B. papyrifera trees in the study sites. The first part shows the effect of site, tapping and the interaction using F-test. Tapping levels are compared for both sites combined. F-values and significant levels are presented. The second part shows mean values with standard errors. Different letters along the row indicate significant differences. We used separate post-hoc, Tukey tests for each parameter.

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of tapping by their higher annual carbon gain. For both sites, we did not observe a significant difference in the resin yield between the low (6 incisions) and high (12 incisions) tapping intensities (Table 1). For the tree size considered here, we therefore recommend relatively low tapping intensities, because it limits the damage to the bark of the tree while the annual resin yield is approximately maintained. Better comparisons across trees of different size and wider range of tapping regimes are, however, recommended to provide more specific guidelines for tapping intensity and frequency (see also Eshete et al., 2011). Despite the variation in environmental conditions between sites, trees achieved similar resin yields. Given that leaf lifespan varies systematically with climate (Wright et al., 2004), the drier highland has short leaf lifespan compared to the lowland. However, none of the considered functional traits (crown leaf area, leaf lifespan and assimilation) had immediate impacts on resin

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yield. This is remarkable, given the large difference in carbon gain across trees. The resin, as a compound rich in carbon (Hamm et al., 2005; Mertens et al., 2009) and nitrogen, its yield was not affected by differences in carbon gain or site nutrient conditions. However, the impact of site nutrient status with frankincense production may require further investigation. Since the measured trees had a similar stem diameter, we propose that the size of bark and the amount of resin secretary structures and canals could be a stronger driver for frankincense yield than the constraints set by carbon gain or nutrient status. Moreover, maximum yield of resins from plants depends on the kind of duct, the location of ducts in plants and how ducts are influenced by wounding (Langenheim, 2003). Another reason could be that frankincense production is primarily to defend damage (Langenheim, 2003) and that allocating resources to this function might have preference over other sinks even when trees have reduced carbon gain. We note that our analysis is based on a number of simplifying assumptions. First, we measured light conditions during 10–25% of the growing season and we therefore do not fully account for variation in weather conditions during the season. However, there is a clear trend for the weather during the rainy season to be more cloudy at the lowland than at highland site, which is consistent with the tendency for more precipitation to be associated with more cloudy weather. Second we measured gas exchange at two moments during the wet season. However, leaf gas exchange may vary in relation to dry spells or temperature changes within the wet season. Our intention, however, was to assess the impact of tapping related changes in leaf and crown traits on photosynthetic carbon gain, and not to make detailed and very precise predictions of carbon gain. B. papyrifera trees thus seem acclimated or adapted to local conditions through changes in functional crown traits. Moreover, carbon gain of trees responded strongly to the variation in light intensity associated with the degree of cloudiness during the rainy season. Because rain is another important climatic factor, setting limits to leaf lifespan, the possible consequences of increased drought and associated weather conditions under climate change (Vanacker et al., 2005; Hély et al., 2006; WWF, 2006; Butterfield, 2009) suggest difficulty of predicting future sustainability of B. papyrifera trees, both for their annual carbon gain and resin productivity. 5. Conclusion These results clearly indicate that tapping B. papyrifera trees reduces leaf area production but its impact on annual carbon gain was site specific. Heavy tapping negatively affected leaf area production and annual crown assimilation in the lowland. In the highland, trees are less affected by tapping due to better light conditions and larger photosynthetic capacities that enable a greater carbon gain. Thus, the combined effect of higher photosynthetic rate and shorter leaf lifespan resulted in more carbon gain than the combined effect of long leaf lifespan and lower photosynthetic rate. We conclude that B. papyrifera trees are differentially acclimated to their local environmental conditions within the tropical woodland systems they live in. However, the impact of future climate change may alter the length of the leaf bearing period with a possible effect on crown carbon gain and resin productivity of the species. Acknowledgments We thank Dr. Lourens Poorter for comments on an earlier manuscript draft. We are grateful for the support provided by Prof. Masresha Fetene during data collection. We thank field assistants

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in Abergelle and Metema for the collaboration during data collection. This study is largely funded by the Netherlands Foundation for the Advancement of Scientific Research in the Tropics (NWOWOTRO) as part of the integrated research program FRAME (Frankincense, myrrh and gum arabic: sustainable use of dry woodlands resources in Ethiopia, Grant Number W01.65.220.00).

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