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Keywords:

  • leaf phenology;
  • species composition;
  • tree transpiration;
  • water stable isotopes;
  • Panama

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References

We studied tree water uptake patterns, tested for complementary water use among species and analysed controlling factors in a tropical tree diversity experiment. The water uptake depth of five species was investigated across seasons and diversity levels using the natural abundance of water isotopes (δ2H, δ18O) and modelling. Three distinct water acquisition strategies were found for trees growing in monocultures during the dry season: strong reliance (>70%) on soil water from the upper layer (0–30 cm) (Cedrela odorata), uptake from the upper and deeper layers (>30 cm) in equal proportions (Hura crepitans, Anacardium excelsum and Luehea seemannii) and water uptake predominately from deeper layers (Tabebuia rosea). Seasonal shifts in water uptake were most pronounced for T. rosea. The water uptake pattern of a given species was independent of the diversity level underlining the importance of species identity and species characteristics in spatial and temporal tree water use. Statistics did not show a significant effect of diversity on source water fractions, but we did see some evidence for complementary water resource utilization in mixed species plots, especially in the dry season. Our results also demonstrated that the depth of soil water uptake was related to leaf phenology and tree transpiration rates. A higher proportion of water obtained from deeper soil layers was associated with a high percentage foliage cover in the dry season, which explained the higher transpiration rates. Copyright © 2014 John Wiley & Sons, Ltd.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References

Complementary resource use has been suggested as an explanation for higher productivity observed in mixed plant communities compared with monospecific communities (Haggar and Ewel, 1997; Hooper et al., 2005). Resource use complementarity has been attributed to functional trait and niche differences among species, suggesting that species access resources unavailable to others or differ in spatial and temporal uptake of the same resource (Vandermeer, 1989). For instance, complementary use of light and nitrogen among co-occurring tree species may result in a more effective use of these resources (e.g. Richards and Schmidt, 2010; Zeugin et al., 2010), which may increase plant productivity and retention of nutrients in mixed plant communities (Hooper et al., 2005).

Complementary water use (in our case, partitioning of soil water) due to interspecific belowground and aboveground interactions may result in increased stand transpiration rates, higher soil water depletion and lower runoff in mixed tree stands. Reduced soil water availability limits plant growth, especially in (seasonally) dry regions. Even in the Atlantic lowlands of Costa Rica where annual rain fall is high (approximately 4300 mm per year) and with a dry season of usually more than 100 mm rainfall per month, annual wood productivity in an old-growth forest increased with increasing rainfall in the dry season (Clark et al., 2010).

Sap flux and tree transpiration were investigated in an experimental native tree plantation consisting of monocultural and mixed species plots in Central Panama (Sardinilla biodiversity experiment; Potvin and Gotelli, 2008). Transpiration rates differed among the five tree species (Kunert et al., 2010), and dry season and annual stand transpiration rates in 5-species mixtures were significantly higher compared with monocultures and 2/3-species mixtures at Sardinilla (Kunert et al., 2012). Differences between monocultural and mixed plots were also found in belowground water flows. The seepage rate in 5-species mixtures was significantly lower than below monocultures (Sprenger et al., 2013). Applying the additive partitioning approach (Loreau and Hector, 2001) showed that the enhanced stand transpiration was attributed to complementarity effects (Kunert et al., 2012). However, this approach does not provide information on the underlying mechanisms (e.g. complementary water use), which may explain the observed enhanced transpiration rates in mixed stands.

The application of water stable isotopes is a reliable technique to assess plant water acquisition patterns and complementary water use (White et al., 1985; Ehleringer and Dawson, 1992). Comparing the stable isotope composition of hydrogen in soil and xylem water during the dry season combined with phenological observations in Panamanian lowland forests revealed that soil water partitioning occurs among co-existing trees (Jackson et al., 1995; Meinzer et al., 1999). These studies also showed that trees and shrubs exploiting deeper soil water were able to maintain constant or even elevated transpiration rates during the dry season (Jackson et al., 1995; Meinzer et al., 1999). The observed partitioning of soil water was strongly dependent on tree diameter, but it remained unsolved to which extent the observed water uptake patterns were species related (Meinzer et al., 1999).

The experimental design of the tree plantation in Sardinilla provides a unique opportunity to investigate the effects of species identity and species richness on tree water uptake. Further, ideas about complementary water resource utilization and ecological plasticity in a moist tropical ecosystem subjected to a pronounced dry season can be tested.

The specific objectives of this study were to (i) determine the depth of soil water uptake by five tree species across seasons, (ii) investigate the complementarity in water use among co-occurring species in mixed stands and (iii) examine the interactions between tree water uptake, leaf phenology and tree transpiration. The present study complements earlier studies (Kunert et al., 2010, 2012; Sprenger et al., 2013) and presents quantitative data on soil water utilization of native tree species in the tropics.

Material and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References

Site description

The study was conducted in an experimental tree plantation located close to the village of Sardinilla, Central Panama (9°19′30″N, 79°38′00″W; 70 m a.s.l.). The clay-rich soil is derived from Tertiary limestone and other sedimentary rocks and is classified as Typic and Aquic Tropudalfs (Potvin et al., 2004). Average rainfall measured between April 2007 and December 2009 was 2289 mm per year with 200–350 mm per month during the rainy season (May–November) and less than 30 mm per month during the dry season (January–March) (Wolf et al., 2011). Mean annual temperature was 25·2 °C (Wolf et al., 2011). Photosynthetic photon flux density (35–45 mol m−2 day−1) and vapour pressure deficit (0·8–1.2 kPa) were higher during the dry season compared with the wet season (20–35 mol m−2 day−1 and 0·2–0.8 kPa, respectively) (Wolf et al., 2011). The original tropical moist lowland forest at Sardinilla was logged in 1952/53. After a short period of crop cultivation, the site was converted into a pasture and used to graze cattle.

The experimental plantation was established in July 2001. Six native species were selected: two fast-growing, early successional species [Luehea seemannii Triana & Planch and Cordia alliodora (Ruiz & Pavon) Oken], two light-intermediate species with moderate growth rates [Anacardium excelsum (Bert. & Balb. ex Kunth) Skeels and Hura crepitans L.] and two slow-growing, late successional species [Cedrela odorata L. and Tabebuia rosea (Bertol.) DC.]. The plantation (~9 ha) consists of 24 plots (45 × 45 m). Twelve plots are monocultures (two for each species), six plots have different combinations of three tree species and six plots include all tree species (Scherer-Lorenzen et al., 2005). Saplings were planted at 3-m spacing with an initial tree density of 1111 trees ha−1. At the time of the study, the canopy was closed in most plots. The understory, which varied in density, consisted of grasses, sedges and herbs, and was cut once or twice a year.

Tree selection and sampling

In this study, five species were investigated (L. seemannii, A. excelsum, H. crepitans, C. odorata and T. rosea) (Table 1). C. alliodora was excluded as it did not establish in monoculture and had high mortality rates in mixed plots. Henceforth, we will refer to the actual diversity at the time of the investigation. Three replicate trees were selected per species and diversity level (monocultures, 2/3-species plots and 5-species plots) (45 trees in total). Only six out of 20 possible 3-species combinations were realized at Sardinilla. Among the available six 2/3-species plots, replicates for a given species were selected from different plots. The species composition of the 2/3-species plots is given in Table 1. Plant and soil sampling for isotope analysis was conducted in March 2007 (dry season), July 2007 (wet season), January 2008 (transition period from wet to dry season) and March 2008 (dry season). Xylem samples were obtained by cutting segments (~15 mm in diameter, 50 mm long) from well suberized branches. The bark was removed from the branch samples, as evaporative gas exchange in the bark tissue can result in isotopically enriched water (Dawson and Ehleringer, 1993). Soil samples were obtained within a 1·5 m radius around the trunk at the following depth intervals: 0–10, 10–30, 30–50 and 50–70 cm. We pooled two to three soil cores for a given depth interval. Branch and soil samples were placed in 40-ml borosilicate glass bottles, closed with a Teflon-coated lid, wrapped in Parafilm and kept frozen until analyses.

Table 1. Main characteristics of the trees selected for this study.
SpeciesFamilySpecies codeDiversity level/plotaDiameter (cm)bTree height (m)bFoliage cover March 2008 (%)cLeaf flushing/peak foliage covercLeaf δ18O (‰)Wood δ18O (‰)
MeanSDMeanSDMeanSDMeanSDMeanSD
  1. Values are mean values ± SD (n = 3 trees per species and diversity level). Small letters indicate significant differences among species for a given diversity level (analysis of variance followed by a post-hoc Tukey, p < 0·05).

  2. a

    Species composition in the 2/3-species plots: T2 (Ae, Ls, Tr), T3 (Ae, Co, Ls), T4 (Co, Hc, Ls), T5 (Hc, Tr) and T6 (Ae, Tr).

  3. b

    Diameter and tree height were measured in March 2007. Diameter was measured with a diameter tape. Tree height was determined with a hypsometer (Vertex III, Haglöf, Lensele, Sweden).

  4. c

    Percentage foliage cover was monitored on three branches of each selected tree at least once a month. The number of leaves on each branch was counted and related to the maximum number of leaves observed during the study period (percentage of maximum) (Kunert et al., 2010).

Cedrela odorataMeliaceaeCoMonoculture11·8a0·612·0c1·1142Jul–Oct21·41·721·80·3
   3-species; T3, T420·0c1·115·7c0·2n.d.     
   5-species14·2a1·811·4a2·1n.d.     
Tabebuia roseaBignoniaceaeTrMonoculture11·5a1·67·4b0·45943Jul–Oct, Feb–Apr24·20·424·51·5
   2/3-species; T2, T5, T69·9a1·57·5a1·9983    
   5-species13·4a4·57·6a0·6100     
Hura crepitansEuphorbiaceaeHcMonoculture18·1b2·35·6a1·13935May–Jul24·51·424·31·1
   2/3-species; T4, T513·5a4·05·9a1·4712    
   5-species19·9a7·16·7a1·711     
Anacardium excelsumAnacardiaceaeAeMonoculture9·9a0·46·4a0·57411Feb–May24·11·323·60·1
   3-species, T2, T313·5a4·010·2b1·179     
   5-species10·4a1·07·1a1·07535    
Luehea seemanniiTiliaceaeLsMonoculture11·1a0·78·3b0·96126Jul–Oct, Feb–Apr23·20·525·80·1
   3-species; T2, T3, T415·1b,c2·010·1b1·483     
   5-species11·9a2·77·4a1·56814    

To evaluate longer-term water use as recorded in structural tissues of the trees, stem cores and sun exposed leaves were collected for cellulose extraction from two to three trees of each species grown in monocultures in August 2007. Core and leaf samples were oven dried (60 °C, 48 h) before conducting further analysis.

Water extraction, isotopic analyses and water source modelling

Water was extracted from plant and soil samples by cryogenic vacuum extraction (Ehleringer and Dawson, 1992). Branch and soil samples were extracted for 90 min based on the results of extraction time curves. Gravimetric water content of all soil samples was determined from sample weight loss by oven drying (105 °C, 48 h). Volumetric soil water content was calculated by multiplying the gravimetric soil water content by the bulk density (0–30 cm: 0·72 g cm−3, below 30 cm: 0·85 g cm−3; Abraham, 2004).

All water samples were analysed for both deuterium (δ2H) and oxygen (δ18O). The isotopic composition was measured by injecting water into a high temperature conversion/elemental analyzer (TC/EA) coupled via a Con-Flo III interface to a Delta V Plus isotope ratio mass spectrometer (Thermo-Electron Cooperation, Bremen, Germany) as described in Gehre et al. (2004). All samples were analysed four times. The value of the first injection was discarded, and the remaining values were averaged. The δ2H and δ18O values are expressed in delta per mil (‰) relative to the Vienna Standard Mean Ocean Water standard. Measurement precision was 2‰ for δ2H and 0·04‰ for δ18O. Water samples were analysed at the Center for Stable Isotope Research and Analysis (KOSI), University of Göttingen, Germany. The δ18O and δ2H values measured from branches and soil material are abbreviated as δxylem and δsoil, respectively.

The outer 5 mm of sapwood (excluding the bark) and leaves were ground in a ball mill and purified to cellulose plus hemicelluloses (Leavitt and Danzer, 1993). The δ18O values were determined after pyrolysis on a ThermoFinnigan TC/EA (Werner et al., 1996), linked to a ThermoFinnigan DeltaPLUS XP stable isotope ratio mass spectrometer, with precision of 0·14‰, at the University of Wyoming Stable Isotope Facility. The δ18O values of leaf and wood cellulose are abbreviated as δleaf and δwood, respectively. The δ18Oleaf and δ18Owood values of all tree species except C. odorata (Table 1) support the assumption of a fairly consistent steady state isotopic enrichment of leaf and wood cellulose 18O in comparison to source water (Roden et al., 2000). The average fractionation factors were 28·5 ± 1·8‰ based on wood cellulose minus source water and 28·0 ± 1·7‰ based on leaf cellulose minus source water.

The xylem water isotopic signature reflects the uptake-weighted average of δ2H or δ18O values of potential water sources because roots do not fractionate water during uptake and evaporation from suberized stems is negligible (Ehleringer and Dawson, 1992). Via graphical xylem–soil water isotopic value comparison, the soil water acquisition depth was identified (Brunel et al., 1995). This approach is based on the assumption that soil water is predominantly taken up from the depth where the plant isotopic value matches the soil water isotopic value. This approach has its limitations (Asbjornsen et al., 2007). For example, it does not take into account that xylem water represents a mixture of water from various depths and thus provides only an approximate indication of water uptake depth. The multi-source mixing model SISUS (Stable Isotope Sourcing using Sampling, http://statacumen.com/sisus/) was applied to estimate the proportional contributions of soil water sources to the xylem signature. SISUS identifies exact feasible solutions of source contributions based on a Bayesian model where variability in isotope ratio means vanishes to zero and generates mean proportions and variations for each source (Erhardt, 2009). As δ18Oxylem and δ18Osoil showed the same pattern as deuterium, we run SISUS for δ18H only. SISUS was run for each tree separately using δ2Hxylem and δ2Hsoil of all four soil layers (0–10, 10–30, 30–50 and 50–70 cm) without using prior information on source proportions. All xylem values were within the range of the four potential water sources except for T. rosea during the dry season. Some of the T. rosea δ2H and δ18O xylem values during the dry season were lower than the isotopic signature of soil water. This suggests water uptake from soil layers below 70 cm. Lower soil water δ2H and δ18O values at deeper layers compared with the surface have been measured in several studies (e.g. Bertrand et al., 2012). In these cases, we included an additional deeper water source into the model runs.

Multi-source mixing models offer a more realistic assessment of plant water uptake and allow quantifying and comparing water use of different species (Asbjornsen et al., 2007). However, multi-source mixing models do not provide ‘unique solutions’, as the range of feasible fractional contributions can be large (Phillips and Gregg, 2003; Asbjornsen et al., 2007). In our study, broad ranges were often associated with the lack of strong differences in stable isotope signatures among deeper soil layers (Figure 1). Thus, we averaged the mean proportions for the two upper soil layers (0–10 and 10–30 cm) and the deeper soil layers (>30 cm) for statistical analyses.

image

Figure 1. Stable hydrogen (δ2H) and oxygen (δ18O) isotopic composition of soil and xylem water for C. odorata, T. rosea, H. crepitans, A. excelsum and L. seemannii grown in monocultures. The δ2H and δ18O values are means ± SD (n = 3) measured during the (a) dry season (March 2007) and (b) wet season (July 2007). The grey area indicates the depth of soil water uptake by comparing the xylem isotopic values with the soil water isotopic values. Volumetric soil water content (VSWC) is shown in the right panel.

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Tree water use

Sap flux density in all 45 trees was measured from July 2007 to June 2008 using thermal dissipation sensors (Granier, 1985). The sensors consisted of two 20-mm-long and 2-mm-thick probes. Each tree was equipped with two sensors, one on the southern and one on the northern site of the trunk, at 1·30 m above the ground. The sensors were well insulated and protected. The sensor output was stored every 15 min using data loggers (Campbell Scientific Inc., Logan, UT, USA). Sap flux density was calculated from temperature differences applying the empirical equation determined by Granier (1987) and then summed up over the daylight hours to estimate daily sap flux density (Js, g cm−2 day−1). We scaled measurements from daily sap flux density to whole-tree water use (kg day−1) by relating the measured sap flux density of the outer 2 cm to the whole conductive xylem area. To account for radial patterns in sap flux density, we measured Js at 0–20, 20–40 and 40–60 mm. Tree level transpiration rates (mm day−1) were calculated by dividing daily water use rates (kg day−1) by the unit crown projection area (m2). Further details on the methods are found in Kunert et al. (2010).

Statistical analyses

Mixed-model repeated-measures analyses of variance was used to identify effects of species, diversity and soil depth (where applicable) upon water stable isotopes, source fractions and tree characteristics. A post-hoc, paired t-test (including a Bonferroni correction) was applied to compare all pairs of levels of the independent variables. The δ values were converted into % atom before statistical analyses. Data were first tested for normality using the Shapiro–Wilk test. Pearson product moment correlation was used to test for relationships between water stable isotopes, environmental and tree characteristics. Statistical analyses were conducted using SPSS/PASW Statistics 18 (18.0.2, SPSS Inc., Chicago, IL, USA).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References

Volumetric soil water content and isotopic signatures of soil water and xylem

Volumetric soil water content differed significantly among sampling dates and soil depth (Table IIa). Volumetric soil water content in the top 10 cm was around 30% in the dry season, and soil moisture content increased with depth (Figures 1a and 4). During the wet season, volumetric soil moisture content varied between 52% and 63% (Figure 1b).

Table IIa. Mixed-model repeated-measures analyses of variance carried out on volumetric soil water content, δ2Hsoil and δ18Osoil with sampling date (time) as the repeated effect (within subject effect), and depth, species and tree diversity as fixed effects (between subject effects).
Effectd.f.Volumetric soil water content (%)δ2Hsoil (‰)δ18Osoil (‰)
FpFpFp
  1. a

    Huynth–Feldt adjustment.

Within subject effecta       
Time31127·6060·000137·4730·000157·3590·000
Time × species125·4340·00011·0520·0008·2410·000
Time × tree diversity63·9500·0011·4030·2161·7980·099
Time × depth934·3980·00020·8160·00025·2990·000
Time × species × tree diversity242·0960·0024·0780·0001·1550·282
Time × species × depth361·1440·2681·1530·2571·0680·369
Time × tree diversity × depth181·2840·1951·1760·2781·1370·314
Time × species × tree diversity × depth721·6430·0021·3320·0491·1300·322
Between subject effects       
Species47·5430·00011·1040·0007·6370·000
Tree diversity25·3800·0067·4170·00116·5360·000
Depth314·9750·000509·9800·000724·0220·000
Species × tree diversity85·2290·0001·9170·0632·4770·016
Species × depth121·4390·1570·6700·7771·1480·329
Tree diversity × depth61·9580·0771·7020·1262·9340·011
Species × tree diversity × depth240·8260·6980·9000·6010·9530·533

The δ2Hsoil and δ18Osoil values across sampling dates ranged from −5·5‰ to −57·1‰ and from −0·2‰ to −8·9‰, respectively (Figure 2a). Soil water isotope values in the upper soil layers were higher (Figures 1 and 2a) and plotted below the local meteoric water line (Figure 2a), indicating evaporative fractionation of soil water close to the surface (Hsieh et al., 1996). The δ2Hsoil and δ18Osoil values (averaged over sampling dates, depths and diversity) were affected by species (Table IIa) with highest values under C. odorata (−34·9‰ and −4·5‰, respectively) and lowest under T. rosea (−38·9‰ and −5·7‰, respectively). Further, we found a species × diversity effect upon δ18Osoil (Table IIa). δ18Osoil values under C. odorata and H. crepitans were higher in monocultures (−4·9‰ and −5·3‰, respectively) than in 2/3-species plots (−4·2‰ and −4·9‰, respectively) and 5-species plots (−4·4‰ and −5·1‰, respectively).

image

Figure 2. The δ2H–δ18O relationship for (a) soil water and (b) xylem water collected in March 2007 at Sardinilla, Panama. The local meteoric water line (solid line in Figure 2a and b) was calculated from long-term (1986–1997) monthly composite precipitation δ2H and δ18O values measured at Howard AFB (Panama Canal Zone, 8°55′N, 79°36′W, 13 m a.s.l., rainfall ~1780 mm year−1, http://nds121.iaea.org/wiser/).

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The δ2Hxylem and δ18Oxylem values across sampling dates ranged from −6·2‰ to −48·5‰ and from −1·2‰ to −7·3‰, respectively (Figure 2b). A significant species effect was found upon δ2Hxylem and δ18Oxylem values with highest values in C. odorata (Table IIb, Figure 1a, b). Diversity and species × diversity effects upon δ2Hxylem and δ18Oxylem values were not significant (Table IIb).

Table IIb. Mixed-model repeated-measures analyses of variance conducted on δ2Hxylem, δ18Oxylem and source fractions (0–30 cm depth) with sampling date as the repeated effect (within subject effect), and species and tree diversity as fixed effects (between subject effects).
Effectd.f.δ2Hxylem (‰)δ18Oxylem(‰)Source fraction (%)
FpFpFp
  1. a

    Huynth–Feldt adjustment.

Within subject effecta       
Time326·8710·00026·2470·0003·0740·036
Time × species124·1490·0002·9020·0021·6610·106
Time × diversity61·0470·4010·4800·8220·7430·618
Time × species × diversity241·6190·0540·7520·7840·7190·808
Between subject effects       
Species432·7460·00022·8500·00030·6590·000
Diversity22·1780·1311·9200·1640·5510·587
Species × diversity81·2930·2851·7710·1231·7790·155

Tree water uptake patterns

C. odorata, the only deciduous species at Sardinilla, obtained a significantly higher amount of water from upper soil layers compared with the other species except for January and March 08 in 3-species plots (Figure 3a–c). Grown in monocultures and 5-species plots, C. odorata extracted between 65% and 90% of its water from the upper 30 cm (Figure 3a, c). Only 56–72% was taken up from 0 to 30 cm when C. odoratoa was grown in 3-species mixtures (Figure 3b). Across all sampling dates, H. crepitans obtained most of its water from 0 to 30 cm depth ranging from 61% to 74% in monocultures (Figure 3a), 59% to 70% in 2/3-species plots (Figure 3b) and 59% to 71% in 5-species plots (Figure 3c). Independent of tree diversity, T. rosea utilized only a small proportion of water (11–24%) from the top 30 cm during the dry season (Figure 3a–c). Season had a significant effect on T. rosea's water acquisition pattern. During the wetter months, T. rosea acquired more water from 0 to 30 cm: 41–49% (monocultures), 50–54% (2/3-species plots) and 32–55% (5-species plots) (Figure 3a–c). Differences in water uptake pattern between dry and wet season were also observed for A. excelsum and L. seemannii. On average, both species obtained 52–60% of their water from below 30 cm depths during the dry season. Uptake of water from deeper layers was most pronounced in 3-species mixtures in March 2007 (A. excelsum: 68%; L. seemannii: 66%; Figure 3b). The upper soil profile was the main source of water in July 2007 and January 2008 for A. excelsum and L. seemannii across all diversity levels (Figure 3a–c). It is interesting to note that all species (except for C. odorada in July 2007 and H. crepitans in January 2008) growing in 2/3-species plots hardly differed in their water uptake pattern during the wetter months (July 2007, January 2008): 46–57% of their water was extracted from 0 to 30 cm depth (Figure 3b).

image

Figure 3. Per cent water uptake from the upper soil layer (0–30 cm depth) for the different tree species grown in (a) monocultures, (b) 2/3-species plots and (c) 5-species plots throughout an entire dry–wet–dry cycle, Sardinilla, Panama. The values are means (n = 3) based on the mean model solution calculated from the multi-source mixing model SISUS (Erhardt, 2009). The average SD was 15% (4–35%).

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A graphical synthesis, presenting the water uptake by depth interval (0–10, 10–30, 30–50 and 50–70 cm) in 5-species mixtures during the dry season (March 08), shows that there is a strong complementarity of water use between C. odorata and T. rosea (Figure 4a). In contrast, the differences in water uptake among H. crepitans, A. excelsum and L. seemannii are less pronounced (Figure 4a). However, H. crepitans, A. excelsum and L. seemannii extract a considerable proportion of water from 10–30 and 30–50 cm depths for which C. odorata and T. rosea obtain a small fraction (Figure 4a). A similar pattern was observed for all species in 5-species plots in March 2007 (data not shown) and for T. rosea, A. excelsum and L. seemannii in 2/3-species plots in March 2007 (Figure 4b) and March 2008 (data not shown). The water uptake depth for C. odorata and H. crepitans grown in 2/3-species plots varied considerably among replicates. C. odorata in 3-species plots took up less water from 0 to 10 cm depth (26–48%) compared with C. odorata in 5-species plots (62–82%), whereas H. crepitans in 3-species plots took up more water from 0 to 10 cm depth (42–47%) compared with H. crepitans in 5-species plots (28–32%) (Figure 4). Complementary water use among species in 2/3-species and 5-species plots was less pronounced in July 2007 with T. rosea, H. crepitans, A. excelsum and L. seemannii taking up 30–45% water from 0 to 10 cm, 18–24% from 10 to 30 cm, 14–20% from 50 to 70 cm and 22–28% from 50 to 70 cm. C. odorata obtained 60%, 12%, 13% and 15% at 0–10, 10–30, 30–50 and 50–70 cm, respectively.

image

Figure 4. Tree transpiration rates, per cent water uptake and volumetric soil water content of species (VSWC, mean ± SD, n = 45) grown in (a) 5-species plots and (b) 2/3-species plots during the dry season (March 2008). The values are means (n = 3) based on the mean model solution calculated from the multi-source mixing model SISUS (Erhardt, 2009). The average SD was 7% (4–24%). Mean tree transpiration rates are for the period from 15 January 2008 to 15 April 2008. Note: Tree size is not to scale. For tree height and diameter, see Table 1.

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The depth of soil water uptake by trees, inferred from δ2Hxylem values (and δ18Oxylem values, data not shown), was negatively correlated with percentage foliage cover (r2 = 0·770, p = 0·000, Figure 5a) and tree transpiration rates (r2 = 0·388, p = 0·010, Figure 5b) during the dry season. This implies that species able to tap into deeper soil water sources as indicated by lower δ2Hxylem were able to sustain more transpiring leaves over the course of the dry season, which in turn resulted in higher tree transpiration rates. Despite a significant species effect on diameter and height (Table 1), we did not find a significant correlation between diameter or tree height and δ2Hxylem and δ18Oxylem values for a given species (data not shown).

image

Figure 5. Relationship between xylem water δ2H values, and (a) percentage foliage cover (r2 = 0·770, p = 0·000) and (b) tree transpiration rates (r2 = 0·388, p = 0·010). The values are means ± SD (n = 3) measured during the dry season (March 2008).

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We found a relationship between the water source signal during the growth period and the δ18O signature in cellulose for C. odorata, H. crepitans and A. excelsum. The cellulose (δ18Owood = 28‰) of C. odorata resembled the δ18Oxylem values measured in July 2007, indicating that most wood was formed during the time of major leaf flushing early in the wet season (Table 1). The H. crepitans δ18Owood values were closest to the δ18Oxylem signature measured at the end of the wet season, in January 2008. Cellulose formation of A. excelsum, as inferred from δ18Owood values, coincided with the time of major leaf production at the onset and during the dry season (Table 1).

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References

Tree species identity and soil water uptake

Despite a large range of feasible source contributions for a given soil layer and considerable variation among replicates, three distinct water uptake strategies were identified for trees grown in monocultures: strong reliance on upper soil layer water sources (C. odorata), uptake from all soil layers in equal proportions (H. crepitans, A. excelsum and L. seemannii) and reliance mainly on deep soil water (T. rosea). The differences among species in their depth of water uptake were most pronounced during the dry season.

The depth of soil water uptake by plants has been linked to rooting patterns and active root area (Ogle et al., 2004). The species C. odorata and H. crepitans are reported to have most of their root biomass located in the upper horizon (Cintron, 1990; Coll et al., 2008; Jefferson Hall, personal communication 2010), which may explain their reliance on upper soil water sources. H. crepitans might have been able to cope with drier conditions by storing water in its particularly large trunk, which, at Sardinilla, is shaped like an elephant's foot, providing a buffer during periods of limited water availability (Delagrange et al., 2008). T. rosea has both lateral roots and deeply penetrating taproots as observed during root excavations at Sardinilla (Jefferson Hall, personal communication 2010), which enables T. rosea to extract water from deeper soil layers. Water uptake from deeper layers by L. seemannii during the dry season was also reported from a natural forest on Barro Colorado Island, Panama (Meinzer et al., 1999).

Plasticity in their patterns of water uptake was observed in T. rosea and to a lesser degree in A. excelsum and L. seemannii (Figure 3a–c). The ability to switch between soil water sources depending on water availability has been reported for a number of species in arid/semiarid regions (e.g. Dawson and Pate, 1996; Eggemeyer et al., 2009) and tropical rainforests subjected to seasonal droughts (e.g. Oliveira et al., 2005; Markewitz et al., 2010). A recent study conducted during the dry season in a tropical rainforest in French Guiana found changes in water uptake depth of up to 50 cm within a few days (Stahl et al., 2013). Plasticity in water uptake depth may put plants at an advantage if competition occurs within the ecosystem or water becomes extremely limited (Ehleringer and Dawson, 1992). Strong vertical gradients in nutrient levels are often found in tropical ecosystems (Jobbagy and Jackson, 2001). Accessing nutrient-rich water from the upper layer during the wet season suggests a dynamic water and nutrient use strategy and has implications on the stand nutrient and water budget as discussed later.

In summary, we found interspecific differences in soil water uptake patterns, although all species were exposed to the same environmental conditions. This contrasts with the view that belowground plant functional traits such as root distribution and water uptake depth will be similar among species, as these traits are closely related and governed by soil water availability (Dawson et al., 1998; Meinzer et al., 2001). Our findings also suggest that the observed differences in water acquisition strategies are species-specific traits, as we did not find a correlation between xylem water isotopic composition and tree size for a given species. No strong correlation between tree height and water uptake depth was found by Stahl et al. (2013) investigating trees of varying size in a tropical rainforest in French Guiana. The authors reported that the water uptake depth of shorter trees (less than 25 m) was highly variable ranging from 10 to 200 cm depth (Stahl et al., 2013). In contrast, a strong dependence between tree diameter and water uptake depth was reported by Meinzer et al. (1999) with larger trees extracting water mainly from the upper soil profile.

Phenology, tree transpiration and complementary water use

Our results demonstrated that water acquisition strategies were closely linked to leaf phenology especially during the dry season. Species able to tap into deeper soil water sources were able to produce and sustain transpiring leaves over the course of the dry season (Figure 5a, b). On Barro Colorado Island, Central Panama, the sap flux of A. excelsum increased, whereas xylem δ2H values became more depleted over the course of the dry season (Meinzer et al., 1999), indicating that A. excelsum was able to tap into deeper soil water sources during this period.

In monocultures, stand transpiration rates mediated by species-specific water uptake strategies had in turn an effect on seepage rates. Seepage rates calculated for the wet season 2008 were inversely correlated with stand transpiration rates with the highest seepage rate in H. crepitans (−6·13 mm day−1, Sprenger et al., 2013; stand transpiration rate = 0·69 mm day−1, Kunert et al., 2012) and the lowest seepage rate in L. seemannii (−5·18 mm day−1, Sprenger et al., 2013; stand transpiration rate = 2·62 mm day−1, Kunert et al., 2012). This suggests that species-specific water uptake patterns have implications on stand water budgets.

No significant differences were found in the soil water uptake pattern between trees grown in monoculture and mixtures. This suggests that for the species studied, the species-specific water acquisition pattern was invariant. One may argue that the investigated 7-year-old trees were too young or the tree density too low for trees to interact. Measuring the vertical and horizontal extension of the rooting system (roots > 2 mm) revealed that lateral expansion of roots exceeded the 3-m spacing of planting, suggesting belowground interaction among trees (Jefferson Hall, personal communication 2010).

We did find some evidence of complementary water use among co-occurring species, especially between C. odorata and T. rosea in 5-species plots in the dry season (Figure 4a). Further, any of the other three species is unlikely to strongly compete with C. odorata or T. rosea for water, as their water uptake depth differs at 10–30 and 30–50 cm depth (Figure 4a). In contrast, if H. crepitans, A. excelsum and L. seemannii occurred together in a mixture, there would be a considerable overlap in soil water uptake depths. In 2/3-species plots, these strategies remain the same for T. rosea, A. excelsum and L. seemannii (Figure 4b). Neighbourhood effects may explain the high variability and differences found for C. odorata and H. crepitans in 2/3-species plots compared with 5-species plots. Both species rely predominantly on water from the upper 30 cm, and when grown next to each other, as in plot T4, they may compete for water especially in the dry season (Figure 4b). In the 5-species plots, C. odorata and H. crepitans are not planted next to each other. H. crepitans did not grow well in mixtures with C. odorata and L. seemannii (T4) as indicated by the lower diameter (Table 1). Investigating the variation in tree diameter and height at Sardinilla, Potvin and Dutilleul (2009) found that the size of neighbours was the largest source of variation, and suggested that neighbourhood plays a central role in determining productivity. Thus, 2/3-species mixtures most likely vary in their degree of complementarity depending on species composition. Considerable differences in basal area, aboveground carbon pool, stand transpiration and nutrient stocks were found among the existing six 2/3-species plots (Oelmann et al., 2010; Zeugin et al., 2010; Povin et al., 2011; Kunert et al., 2012), highlighting the importance of species composition. However, not all possible 3-species combinations were established at Sardinilla and thus could not be tested.

In summary, we did find some evidence of complementary water use among co-occurring species, which may partly explain the twofold higher annual transpiration rates of trees growing in the 5-species mixtures (Kunert et al., 2012) and lower seepage rates (Sprenger et al., 2013).

It is important to note that our sampling approach only assessed the spatial partitioning of soil water sources along a vertical axis. Uptake along the vertical axis is mainly influenced by species-specific differences in root activity (Stratton et al., 2000). However, spatial partitioning can also occur along a horizontal axis (laterally) defined by the pattern of species distribution and spacing (Hinckley et al., 1991).

Conclusion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References

Despite a wide range of feasible water source contributions for each soil layer, our results showed interspecific differences in soil water uptake in monocultures and some evidence for complementary soil water use among co-occurring species in mixed plots. Even though annual rainfall at Sardinilla is high, seasonal changes in the depth of water uptake were observed for three of the five species, suggesting that seasonal shifts are likely to be a common feature of tree species in moist tropical forests. In general, a higher proportion of deep water uptake was associated with a higher percentage foliage cover in the dry season, higher sap flux densities and water use rates. Species also differed in their leaf phenology and physiological characteristics, which may reduce competition and facilitate resource acquisition and thus influence productivity and stand water use. Differences in productivity among 2/3-species mixtures indicate the importance of species characteristics and species composition but not necessarily of species diversity. Further research may look more closely into physiological and morphological traits and neighbourhood effects linked to resource complementarity to better predict the importance of species diversity in maintaining ecosystem functions such as carbon and water cycling.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References

We are grateful to Catherine Potvin, the PI of the Sardinilla experiment, for the permission to use the Sardinilla experimental tree plantation for this study. We thank Felipe Rodriguez for field assistance, Lilian Waczyk for helping with the cryogenic water extractions and Reinhard Langel for conducting the water stable isotope analyses. Special thanks to Mareike Röder for the tree illustrations in Figure 4. We thank Guillaume Bertrand and an anonymous reviewer for their comments on a previous version of this manuscript. Logistical support was provided by Smithsonian Tropical Research Institute. The research was conducted under a permit from the Panamanian National Authority for the Environment (ANAM). This study was funded by the German Research Foundation (DFG, Ho-2119/3), with partial support from the US National Science Foundation ARC-0902180 to EP.

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  4. Material and Methods
  5. Results
  6. Discussion
  7. Conclusion
  8. Acknowledgements
  9. References
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