Tree diversity enhances tree transpiration in a Panamanian forest

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species richness and composition is crucial in the design of plantations to maximize wood produc- tion while ... Both carbon gain and water use are controlled by a variety of physical .... ground using a 5-m-long plastic tube. Crown ... Gap filling for missing sap flux measurements ... determined with a paired Student's t-test.
Journal of Applied Ecology 2012, 49, 135–144

doi: 10.1111/j.1365-2664.2011.02065.x

Tree diversity enhances tree transpiration in a Panamanian forest plantation Norbert Kunert1,*†‡, Luitgard Schwendenmann2,*†, Catherine Potvin3 and Dirk Ho¨lscher1 1

Tropical Silviculture and Forest Ecology, Burckhardt Institute, University of Go¨ttingen, Bu¨sgenweg 1, 37077 Go¨ttingen, Germany; 2School of Environment, The University of Auckland, Private Bag 92019, Auckland 1142, New Zealand; and 3Department of Biology, McGill University, 1205 Dr Penfield, Montreal, QC H3A 1B1, Canada

Summary 1. Tree plantations play an important role in meeting the growing demand for wood, but there is concern about their high rates of water use. Recent approaches to reforestation in the tropics involve the establishment of multispecies plantations, but few studies have compared water use in mixed vs. monospecific stands. 2. We hypothesized that tree species diversity enhances stand transpiration. Tree water use rates were estimated in monocultures (n = 5), two-species mixtures (n = 3), three-species mixtures (n = 3) and five-species mixtures (n = 4). Sap flux densities were monitored with thermal dissipation probes in 60 trees for 1 year in a 7-year-old native tree plantation in Panama. We also estimated changes in the amount of wood produced per unit water transpired (i.e. water use efficiency, WUEwood). 3. Annual stand transpiration rates in two- ⁄ three-species mixtures (464 ± 271 mm year)1) and five-species mixtures (900 ± 76 mm year)1) were 14% and 56% higher than those of monocultures (398 ± 293 mm year)1), respectively. Trees growing in mixtures had larger diameters, conductive sapwood and basal area than those in monocultures, which partly explained the enhanced stand transpiration in mixtures. 4. The five-species mixtures maintained equally high stand transpiration rates during wet (2Æ64 ± 0Æ30 mm day)1) and dry seasons (2Æ51 ± 0Æ21 mm day)1), whereas monocultures and two-species mixtures had significantly lower transpiration rates during the dry season, because of the presence of dry season deciduous species. 5. The WUEwood of the five-species mixtures (2Æ1 g DM kg)1 H2O) was about half that of either monocultures, two- or three-species mixtures. 6. The comparably high stand transpiration rates in the five-species plots may arise from enhanced vegetation-atmosphere-energy exchange through higher canopy roughness and ⁄ or complementary use of soil water. 7. Synthesis and applications. Stand transpiration increased linearly with tree species richness and basal area in monocultures, two- and three-species mixtures, but the ratio of stand transpiration to basal area was larger for five-species mixtures. In conclusion, species selection and consideration of species richness and composition is crucial in the design of plantations to maximize wood production while conserving water resources. Key-words: biodiversity effect, complementarity effect, mixed-species stands, monoculture, native species, selection effect, stand transpiration, water use efficiency

*Correspondence authors. E-mails: [email protected], [email protected] †These authors contributed equally to this manuscript. ‡Present address: Department of Biogeochemical Processes, MaxPlanck-Institute for Biogeochemistry, Hans-Kno¨ll-Straße 10, 07745 Jena, Germany.

Introduction The world-wide increase in the number and area of tree plantations is especially pronounced in the tropics. The main factor driving the expansion of plantation forestry is the growing regional and global demand for wood. Currently, most

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136 N. Kunert et al. plantations in the tropics are monocultures of pine, eucalyptus, teak and acacia species (FAO 2005; Lamb, Erskine & Parrotta 2005). Such monospecific and intensively managed plantations produce high yields, but have made only minor contributions to the restoration of ecosystem health (Lamb, Erskine & Parrotta 2005). To improve ecosystem function and biodiversity, several authors advocate the establishment of mixed-species plantations (e.g. Montagnini & Jordan 2005; Paquette & Messier 2010). In addition to their improved ecological value, there are some indications that mixed-species plantations are more productive than monospecific stands (Forrester, Bauhus & Khanna 2004; Bristow et al. 2006). Enhanced productivity is often associated with increased tree water use (Law et al. 2002). For example, significantly higher transpiration rates have been measured in a very productive eucalyptus plantation in comparison to a natural forest in Ethiopia (Fritzsche et al. 2006). However, whether the increase in water consumption is proportional to biomass increase and whether this relationship changes with increasing tree diversity is unclear (Forrester et al. 2010). The measure linking the amount of stem biomass (or carbon) produced with the amount of water transpired to the atmosphere is defined as water use efficiency per amount wood production (WUEwood, Hubbard et al. 2010). WUE of tree plantations is relevant for water management but to date has mainly been studied in eucalyptus plantations (Whitehead & Beadle 2004; Forrester et al. 2010). Both carbon gain and water use are controlled by a variety of physical, biological and chemical factors. Carbon uptake and tree growth are mainly influenced by nutrient and water availability (Kozlowski, Kramer & Pallardy 1991; Rennenberg et al. 2009), light conditions (Binkley et al. 2010) and silvicultural treatments (Hubbard et al. 2010). Higher productivity of species-rich plant communities compared with monospecific communities is often explained by two mechanisms: complementarity and selection (Hooper et al. 2005). The complementarity mechanism implies that mixtures are able to access and use resources more efficiently because they consist of species with a variety of functional traits that may complement each other (Tilman, Lehman & Thomson 1997; Firn, Erskine & Lamb 2007). The selection (or sampling) effect suggests that with increasing number of species, it is more likely to have one or several highly productive species present in the mixture (Tilman, Lehman & Thomson 1997). Tree water use and transpiration are controlled by stomatal and boundary layer conductance (Jarvis & McNaughton 1986). Tree water use is also influenced by canopy structure, conductive sap wood area and diameter (Meinzer, Goldstein & Andrade 2001). Mixed-species stands differ from monocultures in their structural characteristics, such as canopy architecture and leaf traits (Menalled, Kelty & Ewel 1998; Bauhus, van Winden & Nicotra 2004) as well as in the spatial and temporal stratification of roots (da Silva et al. 2009). Mixtures of plants with diverse stature and traits may use the available resources more efficiently and thus enhance plant growth and most probably water consumption (Law et al. 2002). Comparing water use in mixed eucalyptus–acacia plantations with monocultures revealed higher rates of stand transpiration in

the mixed plantation (Forrester et al. 2010). Enhanced rates of water use in mixed stands may involve complementarity or selection mechanisms. Distinguishing between these two mechanisms has implications for the selection of species mixtures to maximize plantation productivity given a certain level of resource availability. The focus of our study was to (i) estimate transpiration rates and WUE in monocultural and mixed-species plots, (ii) assess the effect of tree diversity on tree water use rates and (iii) assess the complementarity and selection effect upon basal area and stand transpiration using the additive partitioning approach developed by Loreau & Hector (2001). We hypothesized that higher tree diversity enhances tree water use and stand transpiration rates.

Materials and methods STUDY SITE

The study was conducted in an experimental plantation close to the village of Sardinilla, Central Panama (919¢N, 7938¢W), 50 km north of Panama City. The elevation of the site is approximately 70 m above sea level. Mean annual precipitation of the nearby meteorological station in Salamanca is 2300 mm (1977–2007), with a pronounced dry season from January to March (STRI 2010). The mean annual temperature in the region is 26Æ2 C. The clay-rich soils in Sardinilla are classified as Typic and Aquic Tropudalfs and are derived from limestone (Potvin, Whidden & Moore 2004). Most of the area was clear-cut in the 1950s, but the original vegetation in the area around Sardinilla was most probably a tropical moist forest similar to that on Barro Colorado Island (Holdridge & Budowski 1956).

EXPERIMENTAL DESIGN OF THE PLANTATION

The experimental tree plantation was set up with plots of varying tree species richness and species combinations (Fig. 1). In total, 24 plots were established between June and July 2001. Each plot was 45 · 45 m and was further divided into four subplots of 22Æ5 · 22Æ5 m. Six native tree species were planted based on their range of relative growth rates (Scherer-Lorenzen et al. 2005): the fastgrowing species Luehea seemannii (Triana & Planch, Tiliaceae) and Cordia alliodora [(Ruiz & Pavon) Oken, Boraginaceae]; the intermediate species Anacardium excelsum [(Bertero & Balb. ex Kunth) Skeels, Anacardiaceae] and Hura crepitans (Linne´, Euphorbiaceae) and the slow growing species Tabebuia rosea [(Bertol.) DC, Bignoniaceae] and Cedrela odorata (Line´, Meliaceae). The relative growth rates measured in the 50-ha permanent plot on Barro Colorado Island are 9Æ1%, 7Æ0%, 5Æ9%, 4Æ9%, 3Æ4% and 2Æ3% per year, respectively. Cedrela odorata is deciduous, whereas the other species were classified as semi-deciduous. Seedlings were planted with 3-m spacing that is the standard commercial planting density in Central America, equating to 1111 stems per ha. The planting design included two monoculture plots for each species (12 monoculture plots in total), six-three-species mixture plots with different species combinations and six-six-plots containing all six species (Fig. 2). However, all C. alliodora trees grown in monocultures and the majority of C. alliodora in the three-species and six-species mixtures died within the first year probably due to undrained and compacted soil (Potvin & Gotelli 2008). Consequently, we did not include C. alliodora in this study. Measurements and analyses were carried out using the actual

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Tree transpiration in a tropical plantation 137 AM416 multiplexer). Sap flux density (Js in g cm)2 h)1) was calculated from differences in voltage using the calibration equation determined by Granier (1987) and averaged for the two sensors per tree prior to further calculations. Changes of sap flux density with increasing xylem depth were assessed for each tree in the last 2 weeks of the experiment. Js was measured at 20–40 mm depth below the cambium and was also determined at a third depth (40–60 mm) in trees with a diameter >8 cm. Sap flux was measured from July 2007 to June 2008 (365 days). Sap flux sensors were changed when necessary to ensure that sap flux was measured in the outermost part of the sapwood. The estimation of water use (Q) for individual trees was based upon the sapwood area of the tree and the radial changes in Js present in the sapwood. Species-specific xylem depth was estimated by dye injection for three trees per species, showing that sapwood depth of all species was greater than sensor length. Sap flux density was extrapolated to tree water use (Q, kg day)1) by summing up the water flow in a given number of ring-shaped stem cross sections corresponding to the respective installation depth, Js as measured at the reference depth and the normalized profile of Js for the species considered (Edwards, Becker & Cerma´k 1996): Q¼

i¼n X i¼1

Fig. 1. Plot layout and description of plot species composition, Sardinilla, Panama. Quadrats highlighted in grey indicate subplots where selected trees were located. diversity at the time of study, consisting of three-two-species mixtures, three-three-species mixtures and four-five-species mixtures.

MICROMETEOROLOGICAL AND SOIL MOISTURE MEASUREMENTS

Micrometeorological data including photosynthetic photon flux density (PPFD, mol m)2 s)1), air temperature (C), relative humidity (%) and precipitation (mm) were provided by ETH Zu¨rich. Vapour pressure deficit (VPD, kPa) was calculated from air temperature and relative humidity. Soil moisture content was measured with time domain reflectometry sensors (TDR, CS610; Campbell Scientific Inc., Logan, UT, USA) at four locations within the plantation at three depths (10, 35 and 60 cm) and stored on data loggers (CR800 and CR1000; Campbell Scientific Inc.).

SAP FLUX DENSITY, TREE WATER USE AND STAND TRANSPIRATION

Sap flux measurements were conducted in the five surviving tree species. Sample trees were chosen in five monoculture plots (one plot for each of the five investigated species, with four sample trees per plot); three plots of two-species mixtures (four sample trees per species), three plots of three-species mixtures (four sample trees per species) and four replicate plots of the five-species mixture (one sample tree of each species in every five-species mixture plot, Fig. 1). Sap flux density was measured with thermal dissipation sensors (Granier 1985). Every tree was equipped with two sensors, placed on the southern and northern sides of the trunk at 130 cm above the ground. Probe output voltage was recorded every 30 s, and the average value stored every 15 min (CR800 and CR1000 datalogger; AM16 ⁄ 32 and

Qi with Qi ¼

Jsci Ai 1000

eqn 1

where Qi is the water flow through ring i, Jsci (g cm)2 day)1) is the cumulative sap flux density and Ai (cm2) is the ring-shaped area of sapwood that extends between the tip and the end of each probe for a given depth interval i. Tree water use was up scaled to stand transpiration rate (Tstand mm day)1) as follows: Pi¼n QDBH Tstand ¼ i¼1 eqn 2 Aplot where QDBH is the water use rate of a given tree and Aplot (m2) is plot area. QDBH was estimated by deriving relationships between measured tree water use rates and tree diameters for each day and species. We excluded the outer tree row of each plot from the analysis to reduce edge effects on tree development.

TREE AND STAND STRUCTURE, LEAF AREA INDEX, BIOMASS INCREMENT AND WATER USE EFFICIENCY

Diameter at breast height (DBH) of all sample trees was measured with a girth tape. Tree height and crown base height of each sample tree were determined with a hypsometer (Vertex III; Haglo¨f, Lensele, Sweden). The crown extension in each of eight cardinal directions was estimated by projecting the edges of the crown vertically to ground using a 5-m-long plastic tube. Crown projection area was calculated as the sum of eight pitch circles. Hemispherical photographs were taken vertically with a digital camera (Minolta Dimage Xt, Chuo-Ku, Osaka, Japan). The camera was equipped with a 185 fish-eye lens and was placed in a levelling device (Regent Instruments, Sainte-Foy, Quebec, Canada). Five pictures were taken per plot, and measurements were repeated five times during the study period. Images were analysed for leaf area index with Gap Light Analyzer Version 2.0 (GLA, Simon Fraser University, Burnaby, BC, Canada). An inventory of all plots was conducted every year at the onset of the dry season, and individual tree height and DBH were measured as explained above. Above-ground biomass (kg) was calculated using species-specific allometric equations derived in 2006 ⁄ 07 by harvesting 10 trees per species per diversity treatment (Oelmann et al. 2010). Above-ground biomass increment for the subplots was estimated by

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138 N. Kunert et al.

Fig. 2. Left: Normalized daily sap flux density shown as annual course (weekly means for each species, n = 4). Right: Scatter plots show the relationships between sap flux in mixtures and monoculture. Straight line represents the 1 : 1 relation. Photosynthetic photon flux density (PPFD), vapour pressure deficit (VPD), weekly rainfall (annual total 2260 mm) and soil moisture (mean of n = 4 sensors per soil depth ± SD) over the course of the study period. No VPD data were available for June 2008 because of sensor failure. Mean PPFD and VPD were significantly higher during the dry season than during the wet season (P < 0Æ001). subtracting the above-ground biomass calculated from inventory data for 2007 from the 2008 biomass. Water use efficiency of wood production [WUEwood, g dry matter (DM) kg)1 H2O] was calculated as the ratio between annual increment in above-ground biomass and the annual water use of all trees of a given plot.

yield stands for any measurable variable in an ecosystem (stand transpiration and basal area in this case) and is expected to be zero under the null hypothesis of no biodiversity effects. These various effects can be related by additive partitioning as follows: DY ¼ Y0 YE ¼

ADDITIVE PARTITIONING OF BIODIVERSITY EFFECTS

We used the approach developed by Loreau & Hector (2001) to measure the net biodiversity effect (DY) on stand transpiration and basal area by additive partitioning of the selection vs. the complementarity effect. The net biodiversity effect has the dimension of yield, where

¼

X Xi

RY0;i Mi 

X i

RYE;i Mi

DRYi Mi ¼ NDRYMþNcovðDRY;MÞ i

eqn 3

where N is the number of species in the mixture, Mi is the yield of species i in monoculture, Y0,i is the observed yield of species i P in mixture, Y0 = i Y0,i is the total observed yield of the mixP ture and YE = i YE,i is the total expected yield of the mixture.

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10Æ9a 21Æ8b 5Æ8a 16Æ2b 12Æ4a 24Æ1a 12Æ5a 20Æ9a 7Æ5a 19Æ1b 35 27 24 29 30 32 29 27 30 38 202a 186a 73a 72a 86a 83a 183a 184a 93a 125a

Mean SD Mean

3Æ8 2Æ2 4Æ6 9Æ7 4Æ5 23Æ1 1Æ7 9Æ8 4Æ6 8Æ4 10Æ6 11Æ2 9Æ4 22Æ2 21Æ5 29Æ0 11Æ8 19Æ0 18Æ6 17Æ1 Co

Hc

Ls

Tr

Cedrela odorata

Hura crepitans

Luehea seemannii

Tabebuia rosea

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Small letters indicate significant differences between monocultures and mixtures for a given species.

0Æ4 2Æ0 1Æ1 2Æ5 1Æ0 1Æ7 1Æ0 1Æ9 0Æ3 2Æ3 6Æ4 8Æ3 11Æ7 13Æ0 5Æ4 6Æ8 8Æ7 9Æ3 7Æ4 7Æ6 0Æ6 2Æ8 0Æ6 2Æ5 1Æ9 7Æ2 1Æ6 2Æ5 1Æ3 3Æ2 10Æ1 12Æ9 12Æ0 18Æ1 18Æ0 19Æ3 11Æ8 13Æ3 11Æ5 12Æ2 4 8 4 8 4 8 4 8 4 8

Mean SD Mean

daily

Js Crown area (m ) Tree height (m)

daily) and tree water use rates (Q)

2

SD Mean

monoculture mixtures monoculture mixtures monoculture mixtures monoculture mixtures monoculture mixtures Ae

Mean daily integrated sap flux densities (Js daily) ranged from 72 to 202 g cm)2 day)1 (Table 1). No statistically significant difference in Js daily was found between monocultures and mixtures for a given species (Table 1). The seasonal patterns of normalized Js daily varied strongly among species and also among diversity levels for a given species (Fig. 2, left panels). Plotting weekly averages of normalized Js daily in monocultures vs. mixtures revealed that differences between monocultures and mixtures were most obvious during the dry season (Fig. 2, right panels). This was most pronounced for T. rosea. Throughout the whole dry season (January–April 2008), T. rosea trees grown in mixed stands appeared to the left of the 1 : 1 line indicating higher normalized Js daily compared with monocultures. Anacardium excelsum trees grown in mixtures sustained higher sap flux density rates towards the end of the dry season (April, May 2008) compared with monocultures. Luehea seemannii in mixtures had lower sap flux density rates at the onset of the dry season (January 2008) but

Anacardium excelsum

USE RATES

N

SAP FLUX DENSITY, SEASONALITY AND TREE WATER

DBH (cm)

Results

Table 1. Structural characteristics of the study trees (mean values ± SD) and mean daily integrated sap flux densities (Js

Normalized daily Js was calculated by dividing daily integrated Js by the highest observed daily integrated Js during the study period (percentage of maximum). Gap filling for missing sap flux measurements (35 days in H. crepitans, all other species 30 cm) (L. Schwendenmann & R. Sa´nchez-Bragado, unpublished data). Access to water from different depths in the soil profile makes available a larger total volume of soil water, which in turn may explain the higher leaf cover and enhanced transpiration in mixed-species plots during the dry season.

TREE DIVERSITY EFFECT ON WATER USE EFFICIENCY

The WUEwood values estimated at Sardinilla are within the range of values (3Æ3–9Æ4 g DM kg)1 H2O) reported from a 15-year mixed and monospecific acacia–eucalypt plantation in Australia (Forrester et al. 2010). The same study revealed that the acacia–eucalypt mixtures had higher WUE than monocultures because of a significant increase in the WUE of eucalypts in the mixed stand (Forrester et al. 2010). At Sardinilla, the average WUEwood of two-species mixtures was significantly higher compared with all other diversity levels, which is in accordance with the findings of Forrester et al. (2010). It should be noted that the high WUEwood in the two-species plots might also be an artefact of the die-off of C. alliodora, which resulted in a 30% reduction in biomass of these plots. In contrast to the results of Forrester et al. (2010), the five-species plots had a much lower WUEwood compared with the monocultures, which can be explained by the considerably higher transpiration rates; still, the reasons for the lack of a proportional increase in productivity are discussed below. There are four factors that potentially limit productivity in the five-species plots: silvicultural treatments, water availability, light conditions and nutrients. Silvicultural treatments were consistent amongst plots, and water was most likely not limiting (as explained above); thus, these two factors can be omitted for the comparison between monocultures and five-species mixtures. The third factor, light conditions were seasonally variable because of cloud cover during the wet season, indicating that the influence of diffuse solar radiation may have a role in differences between WUEwood of monocultures and mixtures. During the dry season, increased evaporative demand enhances transpiration rates (O’Grady, Eamus & Hutley 1999). However, in the five-species plots, the more complex crown structure of the mixtures may lead to more self-shading, thereby preventing an associated increase in productivity during this time. Furthermore, light use efficiencies tend to be lower in direct solar radiation in comparison to diffuse solar radiation (Alton, North & Los 2007), and thus, the dry season was the period of highest water use but also potentially the per-

iod of lowest productivity, resulting in lower WUEwood at the annual time-scale. Unfortunately, this assumption of lower productivity during the dry season could not be confirmed by biomass measurements because inventory was only carried out at an annual intervals. The fourth factor that governs productivity is nutrient availability. Limitation by N and ⁄ or P as well as species- and diversity-related differences in N and P nutrient use efficiency may limit increases in productivity in the five-species mixtures (Richards et al. 2010). Hura crepitans and T. rosea had a lower N- and P-nutrient use efficiency compared with A. excelsum and L. seemannii (Zeugin et al. 2010). Further, tree species at Sardinilla tended to have lower P use efficiency in two- and three-species mixtures compared with monocultures and fivespecies mixtures (Zeugin et al. 2010). Regardless of the mechanism of limitation of productivity in five-species mixtures that changed the proportionality between water use and growth, mixed stands are clearly not able to make the most efficient use of water resources. Low resource-use efficiency is also indicated by highly diverse old-growth stands in the Amazon forest respiring 70% of the assimilated carbon (Chambers et al. 2004).

MANAGEMENT CONSIDERATIONS AND CONCLUSIONS

In tropical tree plantations, site-specific management plans need to define the goal of the enterprise (e.g. high yields, land cover protection, water resource restoration or a combination thereof). Our study showed that water use in mixtures was enhanced, and stand transpiration was highest in the five-species plots while WUEwood was lowest in the species-richest plots. Enhanced water use may not be problematic when water is plentiful (e.g. in non-seasonal climates or during the wet season). However, managers need to be aware of the potential impact of higher transpiration rates on water resources in drier climates or during periods of limited water availability. We recommend the establishment of species mixtures containing a low number of species. Such plantations should achieve high growth rates through complementary resource use while keeping water use rates at a modest level.

Acknowledgements We thank Sebastian Wolf for providing the micrometeorological data and Jose Monteza for collecting data on tree growth. We thank Klaus Winter for advice and Milton Garcia for technical support. We would also like to thank Cate Macinnis-Ng and three reviewers for their valuable comments on an earlier version of the manuscript. This study benefited from the logistical support provided by Smithsonian Tropical Research Institute and Panama’s National Authority for the Environment (ANAM) and was funded by the German Research Foundation (DFG, Ho-2119 ⁄ 3) and a Natural Sciences and Engineering Research Council of Canada (NSERC) operating grant.

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 2011 The Authors. Journal of Applied Ecology  2011 British Ecological Society, Journal of Applied Ecology, 49, 135–144