Journal of Integrative Biology http://www.blackwell-synergy.com Formerly Acta Botanica Sinica 2005, 47 (12): 1459−1469 http://www.chineseplantscience.com

Seasonal Variation of δ13C of Four Species: A Biological Integrator of Environmental Variables

Hai-Tao LI1*, Jun XIA1, 2, Le XIANG1, Tao LIANG1 and Qi-Jing LIU1 (1. Institute of Geographic Sciences and Natural Resources Research, the Chinese Academy of Sciences, Beijing 100101, ; 2. Key Laboratory of Water Cycle and Related Land Surface Processes, Institute of Geographic Sciences and Natural Resources Research, the Chinese Academy of Sciences, Beijing 100101, China)

Abstract: Foliar δ13C values, an indicator of long-term intercellular carbon dioxide concentration and, thus, of long-term water use efficiency (WUE) in , were measured for Pinus massoniana Lamb., P. elliottii Engelm., Cunninghamia laceolata (Lamb.) Hook., and Schima superba Gardn. et Champ. in a restored forest ecosystem in the Jiazhu River Basin. Seasonal variation and the relationship between the foliar δ13C values of the four species and environmental factors (monthly total precipitation, monthly average air temperature, relative humidity, atmospheric pressure, and monthly total solar radiation and evaporation) were investigated. The monthly δ13C values and WUE of the four species increased with increasing precipitation, air temperature, solar radiation, and evaporation, whereas δ13C values of the four species decreased with increasing relative humidity and atmospheric pressure. Despite significant differences in δ13C seasonal means for the four species, our results demonstrate a significant convergence in the re- sponses of δ13C values and WUE to seasonal variations in environmental factors among the species inves- tigated and that the δ13C signature for each species gives a strong indication of environmental variables. Key words: δ13C; Cunninghamia laceolata; ; Pinus massoniana; Schima superba; water use efficiency (WUE).

During the past few decades, there has been a grow- between photosynthesis (A) and transpiration (E) of ing awareness of the importance of land-surface hy- vegetation crown in homogeneous models using the drological processes in global climate modeling (US big approach (Friend 2001). Global Change Research Program (USGCRP) 2001). WUE is conventionally determined either as the ra- Models are very sensitive to changes in many surface tio of A/E in the short term or as the ratio of dry matter parameters and, in particular, to the partitioning of en- accumulation to water consumption over a longer time ergy between carbon fixation and water loss (Houghton interval, such as, for example, a growing season. The et al. 2001; IPCC Working Group 1 2004). Therefore, former (A/E) gives instantaneous estimates of WUE an increased understanding of the interactions between and the latter gives a long-term WUE. The long-term the vegetation and the hydrological cycle is of great method cannot be determined easily because it possi- importance. More recently, water use efficiency bly requires a large amount of labor in addition to the (WUE), that is, the amount of carbon biomass pro- actual difficulties involved in the simultaneous and ac- duced per unit water transpired by the plant leaf, has curate measurement of transpiration and biomass in been used as a tool to measure the coupling process the field (Wright et al. 1988). The instantaneous method,

Received 9 Dec. 2004 Accepted 12 Jun. 2005 Supported by the Frontier Project (CX10G-E01-08-02) and the Backbone Project (CX10G-E01-02-01) of the Knowledge Innovation Program of the Institute of Geographic Sciences and Natural Resources Research, the Chinese Academy of Sciences. *Author for correspondence. Tel.: +86 (0)10 6488 8996; Fax: +86 (0)10 6485 9781; E-mail: . 1460 Journal of Integrative Plant Biology (Formerly Acta Botanica Sinica) Vol. 47 No. 12 2005 although it can be performed easily, may not necessar- coupling process between carbon assimilation and wa- ily correlate with long-term plant performance (Martin ter transpiration of vegetation in a subtropical watershed, and Thorstenson 1998) and, thus, the WUE calculated we investigated the seasonal changes of foliar δ13C using this method is not suitable to the time scales of values and WUE during the whole growing year, from many hydrological models. Therefore, new and reli- May 2002 to May 2003, and focused on differences in able methods for measuring the WUE of plants need to physiological responses, as indicated by δ13C values be used. and WUE, to meteorological factors for the species A significant positive correlation has been shown investigated under common environmental conditions. between δ13C and WUE both theoretically and empiri- We expect to use monthly integrated data collected from cally (Farquhar et al. 1982a, 1982b, 1989). Since then, the routine weather stations to predict seasonal δ13C δ13C has been gradually developed as an indicator to values and WUE of the species studied to yield useful measure WUE by many authors (Ehleringer and information for the parameterization of WUE for fu- Osmond 1989; Gower and Richards 1990; Smedley et ture modeling considerations. al. 1991; Dawson and Ehleringer 1993; Knight 1994). 13 1 Materials and Methods In part, δ C is partly by Ci/Ca, the ratio of CO2 con- centrations in leaf intercellular spaces (Ci) to that in the 1.1 Study site atmosphere (Ca; Farquhar et al. 1982, 1989; Farquhar The study was performed at the Qianyanzhou Eco- and Richards 1984). This ratio can be used as a proxy logical Research Station, which is located in the Jiazhu of a plant’s long-term WUE because, under water watershed (115°03'01'' E–115°04'22'' E, 26°44'12'' N– 13 stress, plants discriminate less against C during CO2 26°45'28'' N, altitude 80–110 m), Taihe County, Jiangxi uptake, resulting in an increase in integrated WUE. Province. The area is characteristic of a typical sub- Thus, the δ13C value of plant provides an inte- tropical monsoon climate. Annual air temperature av- grated measurement of internal plant physiological and erages 17.8 °C (–5.1 °C in January and 31.3 °C in external environmental traits affecting photosynthetic July). Total solar radiation is 4 349 MJ/m2 and annual gas exchange over the period while the carbon was precipitation amounts to 1 461 mm. Approximately 70% assimilated (Ewe et al. 2003) and it can also be re- of the annual rainfall occurs from March to June and garded as an index of physiological coupling of carbon 30% occurs from July to September. The soil is typi- fixation and water loss in plants. cal red earth generally less than 80 cm in depth. The application of the δ13C method to ecological The Jiazhu watershed belongs to the red soil hilly studies has not been widespread in China (Sun et al. region of subtropical southern China. Originally, there 1993; Lin et al. 1994, 1995;Yan et al. 1998; Liang et was a large area of evergreen broad-leaved forest dis- al. 2000; Su et al. 2000; Qu et al. 2001; Chen 2002). tributed in this region. However, because of anthropo- Most of the research using δ13C in China has focused genic activities or clear-cutting for cultivation, espe- mainly on deciduous forests and grasslands in the tem- cially in the 1950–1960s, the original forest was totally perate zone of northern China, whereas studies on the destroyed at the end of 1970s. Later, the Chinese Acad- and evergreen forests in subtropical zones of emy of Sciences (CAS) established Qianyanzhou Eco- southern China are rare (Lin et al. 1994, 1995). In logical Pilot Station, targeting the restoration of veg- particular, there has been no study investigating the etation and the conservation of soil and water in the seasonal variation of δ13C and the WUE of and area. After nearly 20 years forestation by the CAS, the their responses to changes in environmental factors in present forest patch was constructed mainly by the the subtropical region of China. coniferous species Pinus massoniana Lamb., P. elliottii As part of a larger study seeking to model the Engelm., and Cunninghamia laceolata (Lamb.) Hook., Hai-Tao LI et al.: Seasonal Variation of δ13C of Four Tree Species: A Biological Integrator of Environmental Variables 1461 as well as the evergreen broad-leaved species Schima laboratory for stable isotope analysis. superba Gardn. et Champ. In total, 270 carbon isotopic samples were analyzed 1.2 Species selected on a Finnigan MAT253 gas mass spectrometer (Thermo

All species investigated are C3 plants. They were Electron Corporation, FL, USA) to a precision of ± 0. located in three plots (Table 1). The P. 01‰, in the Stable Isotope Laboratory, Institute of massoniana, P. elliottii, and C. laceolata and the ev- Geology and Geophysics, the Chinese Academy of ergreen broad-leaved species S. superba were all planted Sciences. Carbon isotopic abundance, in per mil units in 1984. Of them, P. elliottii is the most widely planted (‰) was determined using the following equation: 13 exotic species in the subtropical region of southern δ C=((Rsample/Rstandard)–1)×1000 13 12 China. Imported from southeastern America over 50 where Rsample is the C/ C ratio of the sample and 13 12 years ago, this exotic is now the main timber species in Rstandard is the C/ C of the Pee-Dee Belemnite the region because of its high productivity. The other standard. three co-occurring species are all native species. P. 1.4 Meteorological variables massoniana is a typical pioneer species that used to be Routine meteorological data, including precipitation, planted in completely open ground with harsh habitat air temperature, solar radiation, relative humidity, at- conditions. C. laceolata is a widely distributed timber mospheric pressure, and evaporation (Fig. 1), were species with a long history in southern China. The only collected using an AMRS-1 weather station (Changchun, broad-leaved tree species, S. superba, was mixed with Insititute of Changchun Meteorological Instruments, P. massoniana. The occurrence of S. superba and P. China) established in the Jiazhu watershed. Of these massoniana together is a peculiarity of the site. The data, monthly average air temperature, relative humidity, growth characteristics of these species and the site and atmospheric pressure were calculated from daily descriptions are summarized in Table 1. data of averaged hourly records. Monthly total 1.3 Sampling and analysis precipitation, evaporation, and solar radiation were ag- Fully expanded leaves were sampled from May 2002 gregated directly from daily records. Monthly mois- to May 2003. The sampling individuals selected are ture balance was calculated as monthly precipitation representative with mean diameter and height for the minus monthly evaporation. species in the community. In the middle of each month, 1.5 Statistical analysis four replicate samples were obtained from each indi- A two-way ANOVA, using a fixed-factors model tak- vidual from the upper canopy in the four orientations, ing species and time of measurement as factors, and east, west, south, and north. Samples were oven-dried regression analysis were performed using Microsoft at 70 °C, then preserved at below 5 °C in a refrigerator Excel 2000. Multiple comparison for significant mean and ground using a mortar and pestle to 80 mesh in a differences in δ13C values between species, factor

Table 1 Characteristics of the study sites in the Jiazhu River Basin, Qianyanzhou Altitude Stem Height Age Site Species Location (m) diameter (cm) (m) (yr) Cunninghamia laceolata plantation C. laceolata 26°26'4'', 115°2'9'' 72 12.4 14.9 18 (Plot 1) Pinus massoniana and Schima P. massoniana 26°26'34'', 115°2'2'' 89 12.9 10.8 18 superba mixed plantation (Plot 2) S. superba 26°26'34'', 115°2'2'' 89 13.2 10.9 18 P. elliottii plantation (Plot 3) P. elliottii 26°26'36'', 115°2'7'' 83 23.5 13.6 18 Weather station 26°26'40'', 115°2'4'' 75 1462 Journal of Integrative Plant Biology (Formerly Acta Botanica Sinica) Vol. 47 No. 12 2005

Fig. 1. Monthly data of meteorological fac- tors calculated from routine weather records from May 2002 to May 2003. (a) Precipitation, (b) air temperature, (c) relative humidity; (d) solar radiation, (e) atmospheric pressure, (f) evaporation, and (g) moisture balance (=precipitation–evaporation). analysis and hierarchical cluster analysis were con- January. In contrast, relative humidity (Fig. 1c) and ducted using SPSS 12.0 (SPSS, Chicago, IL, USA). atmospheric pressure (Fig. 1e) exhibited lowest values in June or July and reach highest values in December 2 Results or January. Moisture balance (precipitation – potential 2.1 Seasonal variation in meteorological factors evaporation; Fig. 1g) had small negative values in No- All meteorological factors showed clear seasonal vember 2002 and February 2003, during which time patterns. In Fig. 1, precipitation (Fig. 1a), air tempera- the snow depth on the ground was recorded as 10.7 ture (Fig. 1b), solar radiation (Fig. 1d), and evapora- and 16.5 mm in December 2002 and January 2003, tion (Fig. 1f) showed similar variation with a maxi- respectively. At the same time, low values were re- mum in June or July and a minimum in December or corded for global radiation and air temperature, and so Hai-Tao LI et al.: Seasonal Variation of δ13C of Four Tree Species: A Biological Integrator of Environmental Variables 1463 plant metabolism was dormant. Thus, the negative val- order of the mean δ13C values of the four species is as ues of moisture balance do not mean that there was follows: P. elliottii (–29.90) < S. superba (–29.65) < physiological harm to plant life as a result of water C. laceolata (–29.16) < P. massoniana (–29.15). Af- stress. Generally, precipitation, potential evaporation, ter the differences among the δ13C means of species and moisture balance showed approximately similar had been determined (Table 2), multiple comparisons trends, implying that drought did not occur during the by the least significance difference, Bonferroni and Tur- year in which measurements were conducted. key honestly significantly different tests were used to 2.2 Seasonal variation of δ13C in four tree spe- identify which species group means differed (Table 3). cies As given in Table 3, according to differences in the The foliar δ13C values ranged from –30.53 to δ13C means, the four species can be divided into two –28.35‰ and showed significant differences accord- groups: P. massoniana + C. laceolata and P. elliottii + ing to species and the month of measurement over the S. superba. The results of hierarchical cluster analysis course of the entire year (Table 2). further confirmed the above division, particularly when Clearly, the variation between species is more sig- the number of clusters is constrained to 3; then, the nificant than that between seasons. The numerical following three groups were formed: P. massoniana +

Fig. 2. Seasonal variation in δ13C values of four tree species. a. Cunninghamia laceolata. b. Pinus massoniana. c. Pinus elliottii. d. Schima superba.

Table 2 Two-way analysis of variance of δ13C values for species and time of measurement

Source of variation Sum of squares d.f. Mean square FPFcritical Month of measurement 6.686 9 12 0.557 2 7.360 3 1.393×10–6 2.032 7 Species 5.459 9 3 1.820 0 24.038 8 1.023×10–8 2.866 3 Error 2.725 5 36 0.075 7 Total 14.872 3 51 1464 Journal of Integrative Plant Biology (Formerly Acta Botanica Sinica) Vol. 47 No. 12 2005

C. laceolata, S. superba, and P. elliottii. The exotic increases in precipitation, potential evaporation, air species P. elliottii was singled out from its original temperature, and solar radiation. However, the other group with S. superba. two meteorological factors, namely relative humidity We then applied factor analysis to explore the ca- and atmospheric pressure, were negatively correlated sual mechanism underlying the δ13C pattern (Table 4). with the δ13C values of the four species investigated. According to the correlation coefficients between This implies that the WUE decreased with increases in variables and common factors in Table 3, we found relative humidity and atmospheric pressure, which are that δ13C values of C. laceolata, P. massoniana, and positively correlated with each other based on their P. elliottii were determined by factor 1, whereas that definitions that ambient atmospheric pressure is the sum of S. superba was determined by factor 2. This may of the partial pressure of vapor and that of the other indicate different adaptation strategies of the different components. species to environmental changes. For P. massoniana and C. laceolata, a higher R2 2.3 Relationship between δ13C and WUE and me- was found between δ13C and moisture balance than teorological factors for P. elliottii and S. superba, which indicates that A significant correlation was found between the moisture balance accounts for a greater proportion of meteorological variables and δ13C values for the four the δ13C value for the former two species than for the species (Table 5). latter two. For all species, a significant positive correlation ex- isted between δ13C and the four meteorological factors 3 Discussion 13 (i.e. precipitation, evaporation, air temperature, and solar The δ C values of terrestrial C3 plants growing un- radiation). Because leaf δ13C is generally considered an der natural conditions range from –22‰ to –34‰ (Vogel indicator of the WUE of plants, the WUE of the four 1993). The range of δ13C values reported in the present species was also positively correlated with these four study, varying from –28.35‰ to –30.53‰, is consis- meteorological factors. That is, the WUE increased with tent with previously published results. Published val- ues of δ13C in extreme arid-zone plants range from –20‰ to –26‰ (Ehleringer and Cooper 1988; DeLucia Table 3 Results of multiple comparisons for mean δ13C and Schlesinger 1991; Ehleringer 1993). In sites expe- values for the four species δ13 Pinus Cunninghamia P. Schima riencing high rainfall, C values have been measured massoniana laceolata elliottii superba in the range –27‰ to –34‰ (Francey et al. 1985; P. massoniana. ** Garten and Taylor 1992; Ehleringer et al. 1993). Such C. laceolata ** values correspond with the range of values measured P. elliottii ** for the four species in the present study for all the Schima superba ** Asterisks indicate a significant difference between the pairs. months recorded. In forest sites, especially those in which canopy cover is high, vertical stratification in

the isotopic composition of the source of CO2 may Table 4 Rotated factor matrix for δ13C complicate analysis of foliar δ13C patterns (Farquhar Factor Species 12 et al. 1989; Ehleringer et al. 1993). Previous measure- Cunninghamia laceolata 0.857 0.300 ments in rainforest systems in south-east Queensland, Pinus massoniana 0.935 0.219 Australia, indicate that stratification occurs over a range P. elliottii 0.855 0.319 of 2‰ or less (Stewart et al. 1995). In the present Schima superba 0.293 0.955 study, this variability has been reduced by sampling Extraction method: principal component analysis. Rotation method: varimax with Kaiser normalization. only exposed and sunlit leaves and by avoiding Hai-Tao LI et al.: Seasonal Variation of δ13C of Four Tree Species: A Biological Integrator of Environmental Variables 1465

Table 5 Regression equations and the related parameters between δ13C and meteorological factors (n = 13 samples) Cunninghamia laceolata Pinus massoniana Pinus elliottii Schima superba Precipitation y = –29.51+0.001 97x, y = –29.57+0.002 062x, y = –30.23+0.001 644x, y = –30.15+0.002 457x, R2 = 0.581 5, P < 0.01 R2 = 0.597 2, P < 0.01 R2 = 0.360 4, P < 0.05 R2 = 0.440 2, P < 0.05 Potential evaporation y = –29.61+0.004 592x, y = –29.71+0.006 035x, y = –30.39+0.005 354x, y = –30.41+0.008 217x, R2 = 0.349, P < 0.05 R2 = 0.483 8, P < 0.01 R2 = 0.361 5, P < 0.05 R2 = 0.465 4, P < 0.05 Air temperature y = –29.68+0.028 8x, y = –29.85+0.038 2x, y = –30.46+0.030 50x, y = –30.60+0.051 87x, R2 = 0.3101, P < 0.05 R2 = 0.508 8, P < 0.01 R2 = 0.308 3, P < 0.05 R2 = 0.487 2, P < 0.01 Relative humidity y = –20.68–0.093 95x, y = –21.27–0.087 36x, y = –20.55–0.103 65x, y = –16.03–0.151x, R2 = 0.386 6, P < 0.05 R2 = 0.312, P < 0.05 R2 = 0.417 0, P < 0.05 R2 = 0.483 6, P < 0.01 Solar radiation y = –29.85+0.001 876x, y = –30.02+0.002 36x, y = –30.71+0.002 202x, y = –30.82+0.003 173x, R2 = 0.379 8, P < 0.05 R2 = 0.553 8, P < 0.01 R2 = 0.456 6, P < 0.05 R2 = 0.518 1, P < 0.01 Atmospheric pressure y = 0.312 0–0.029 33x, y = 8.520 9–0.037 49x, y = 5.194 6–0.034 93x, y = 23.709 0–0.053 11x, R2 = 0.330 9, P < 0.05 R2 = 0.504 8, P < 0.01 R2 = 0.416 0, P < 0.05 R2 = 0.525 6, P < 0.01 Moisture balance y = –29.45+0.002 65x, y = –29.44+0.002 639x, y = –30.12+0.002 013x, y = –29.98+0.002 974x, R2 = 0.597 2, P < 0.01 R2 = 0.552 8, P < 0.01 R2 = 0.305 5, P < 0.05 R2 = 0.364 4, P < 0.05

understorey individuals in the closed forest system used. evergreen conifers (Garten and Taylor 1992; Marshall It appears that foliar δ13C values are usually nega- and Zhang 1994). tively correlated with water availability. Ehleringer et However, the δ13C values reported in the present al. (1988) surveyed 30 perennial species within a desert study show a positive correlation with monthly total community and found that the δ13C values increased precipitation, evaporation, and moisture balance, and a with decreasing water availability. Stewart et al. (1995) negative correlation with monthly average relative hu- observed an increase in δ13C values with decreasing midity and atmospheric pressure, which deserves fur- rainfall in southern Queensland, Australia. Similar re- ther examination. sults were also documented by Schluze et al. (1998). Physiological studies have identified the importance Su et al. (2000) found that δ13C values decreased of relative humidity in controlling stomatal conductance with increasing annual average precipitation and air tem- (Aphalo and Javis 1993; Zang and Nobel 1996). When perature along the grassland zone of the Northeast China atmospheric moisture content is low, leaves decrease Transect. In a more recent study in the warm temper- their stomatal conductance to reduce water loss. This ate zone of northern China, Yan et al. (2001) reported reduces the exchange of CO2 between the substomatal 13 that the δ C values of six woody species in a broad- cavity and the surrounding atmosphere, Ci drops ow- leaved deciduous forest with an average annual rainfall ing to CO2 fixation by photosynthesis, leading to a re- 13 of 611.9 mm, varied from –28.11‰ to –24.72‰. The duced Ci/Ca ratio, and, therefore, high δ C values δ13C values reported in the present study are more nega- (Farquhar et al. 1982b). Conversely, with high relative tive than those reported by Yan et al. (2001), which humidity, stomatal conductance will be high, maintain- 13 can be attributed to the high annual rainfall and air tem- ing high Ci/Ca ratios and, hence, low foliar δ C values. perature as a consequence of the subtropical monsoon The three factors obtained from routine weather sta- climate in the area investigated in the present study. tion data, namely monthly total precipitation, The results of the present study also provide support- evaporation, and moisture balance, which apparently ive evidence of previous finding that deciduous broad- varied inversely with relative humidity and atmospheric leaved tree species have lower δ13C values than do pressure (Fig. 1), are not efficient indicators of water 1466 Journal of Integrative Plant Biology (Formerly Acta Botanica Sinica) Vol. 47 No. 12 2005 stress or water availability to trees because precipita- slowly than plants with a low WUE under periods of tion as water input and evaporation as water loss in high soil moisture availability because a high WUE may this case show a nearly simultaneous change as sea- mean a greater stomatal limitation on photosynthesis sons progress, as does moisture balance. The fact that and, therefore, a lower rate of carbon gain. Ehleringer precipitation was inversely associated with humidity in et al. (1988) further pointed out that, if limiting but this context could partly, and indirectly, explain our relatively high amounts of soil moisture are equally avail- observation of an increase in δ13C with increasing able to both high and low WUE plants, the lower WUE precipitation, which is inconsistent with many previ- plant should be the better competitor if both plants have ous reports (Ehleringer et al. 1988; Stewart et al. 1995; equal access to the same soil moisture. Such a pattern Schluze et al. 1998). is consist with our present case. The four species The absolute range of seasonal δ13C values found investigated, distributed in three plots but very close to for each species is quite small, the numerical order being each other (Table 1), commonly had a high annual pre- 1.172‰ in C. laceolata, 1.248‰ in P. massoniana, cipitation input of 1 461 mm and so maintained a high 1.406‰ in P. elliottii, and 1.738‰ in S. superba. The soil moisture content. Further evidence is that P. same order was found in the standard deviations and elliottii, in the present study with the lower δ13C value, coefficients of variation for the four species. This is in has higher productivity than P. massoniana in the wa- agreement with the grouping results by multiple com- tershed (Chen et al. 1998). Therefore, it is concluded parisons of differences in δ13C means. Passioura (1982) that P. elliottii and S. superba will be more competi- proposed two contrasting strategies of plants, conser- tive species than P. massoniana and C. laceolata in vative and prodigal, which represent plant populations succession. A succession pathway from coniferous with higher or lower WUE, respectively. Cohen (1970) species (P. massoniana) to pioneer heliophilous broa- predicted that the water use pattern should become more dleaf trees (i.e. S. superba, Michelia figo) to meso- conservative during a drought. A more positive δ13C philous broad-leaf trees in subtropical China has been value indicates a more conservative water use pattern. identified (Peng et al. 1996), which partly supports Our statistical results show that P. massoniana and C. our conclusion. From the view of succession, the pio- laceolata have a more conservative WUE pattern, neer species have the lower δ13C values than do later- whereas P. elliottii and S. superba have a more prodi- stage species (Huc et al. 1994). Such a viewpoint con- gal WUE pattern, which can be attributed to the spe- forms with the results of the present study. cies characteristics and habitat conditions. Pinus Over the range of individuals sampled in the present massoniana and C. laceolata are widely distributed study, for each species there is a strong relationship conifers used as pioneer tree species to restore degraded between δ13C and each one of the six meteorological ecosystems with harsh habitats, which are usually ac- factors of precipitation, potential evaporation, air companied by low water availability and atmospheric temperature, relative humidity, solar radiation, and at- humidity. P. elliottii is the exotic species introduced mospheric pressure. This demonstrates that the foliar from southeast America and S. superba is the native δ13C of each species here is a successful empirical in- evergreen broad-leaved species; both are usually found dictor of the six meteorological factors within the usual 13 in wet soil conditions. range of C3 whole-leaf δ C values. In this context, P. massoniana and C. laceolata have more positive the δ13C signature of the four species can be used as foliar δ13C than P. elliottii and S. superba. More posi- an indicator of environmental influences over plant 13 tive foliar δ C indicates high WUE and low Ci/Ca ra- function, especially at the individual species level. This tios (Farquhar et al. 1989). Ehleringer et al. (1988) contrasts with previous uses of this parameter only as suggested that plants with a high WUE grow more an indicator of WUE, a parameter of plant function. Hai-Tao LI et al.: Seasonal Variation of δ13C of Four Tree Species: A Biological Integrator of Environmental Variables 1467

Given that δ13C is a biological expression of environ- ed. Study on the Restoration of Red Soil Hilly Ecosystem and mental conditions integrated over time, it may, indeed, its Sustainable Development of Agriculture (II). Series from provide us with a more meaningful measure of envi- Chinese Ecosystem Research Network. Meteorology Press, ronmental variables. In this respect, we reason that the Beijing. pp. 99–107 (in Chinese with an English abstract). δ13 C signature of plants may be used as an indicator of Cohen D (1970). The expected efficiency of water utilization in environmental influences on plant function, in contrast plants under different competition and selection regimes. Isr with its more common use as a descriptor of plant J Bot 19, 50–54. function itself. Dawson TE, Ehleringer JR (1993). Isotopic enrichment of water Furthermore, perhaps more striking are the results in the woody tissue of plants: Implications for plant water presented here that the δ13C signature of leaf tissue source. Geochim Cosmochim Acta 57, 3487–3492. from plants that are dominated by common meteoro- Delucia EH, Schlesinger WH (1991). Resource-use efficiency logical conditions can be used not only as a indicator and drought tolerance in adjacent Great Basin and Sierran of water availability factors, such as precipitation, po- tential evaporation, and moisture balance, but also as a plants. Ecology 72, 51–58. indicator of other variables, such as air temperature, Ehleringer JR (1993). Carbon and water relations in desert plants: relative humidity, solar radiation, and atmospheric An isotopic perspective. In: Ehleringer JR, Hall AE, Farquhar pressure. All four species unexceptionably show a clear GD, eds. Stable Isotopes and Plant Carbon-Water Relations. convergence on the significant correlation between their Academic Press, San Diego. pp. 155–172. δ13C values and each of the meteorological factors. Ehleringer JR, Cooper TA (1988). Correlations between carbon Assuming that the δ13C of the species investigated in isotope ratio and microhabitat in desert plants. Oecologia the present study is a reasonably good indicator of their 76, 562–566. respective WUE, from a modeling point of view our Ehleringer JR, Osmond CB (1989). Stable isotopes. In: Pearcy results shed light on this feasibility, that the integrated RW, Ehleringer J, Mooney HA, Rundel PW, eds. Plant Physi- WUE across the whole crown in the watershed can be ological Ecology: Field Methods and Instrumentation. parameterized from routine meteorological records at Chapman & Hall, London. pp. 281–330. a very high confidence level. Ewe SML, Sternberga LSL (2003). Seasonal gas exchange char- Acknowledgements The authors thank Professors acteristics of Schinus terebinthifolius in a native and disturbed Yao-Ming LIN, Yun-Fen LIU, and Yong-Rui CHEN for upland community in Everglades National Park, Florida. Fort their assistance with the field work. Ecol Manage 179, 27–36. References Farquhar GD, Richards RA (1984). Isotopic composition of

Aphalo PJ, Jarvis PG (1993). An analysis of Ball’s empirical plant carbon correlates with water-use efficiency of wheat model of stomatal conductance. Ann Bot 72, 321–327. genotypes. Aust J Plant Physiol 11, 539–552. Chen SP, Bai YF, Han XG (2002). Variation of water-use effi- Farquhar GD, Ball MC, Von Caemmerer S, Roksandic Z (1982a). δ13 ciency of Leymus chinensis and Cleistogenes squarrosa in Effect of salinity and humidity on C value of halophytes: different plant communities in Xilin River Basin, Nei Mongol. Evidence for diffusional isotope fractionation determined by Acta Bot Sin 44, 1484–1490 (in Chinese with an English the ratio of intercellular/atmospheric partial pressure of CO2 abstract). under different environmental conditions. Oecologia 58, 121– Chen YR, Wang YF, Li F, Xu GL (1998). Growth analysis of 124. Pinus massoniana and Pinus elliottii forest in the experimen- Farquhar GD, O’Leary MH, Berry JA (1982b). On the relation- tal region of the middle part of Jiangxi province. In: Chen T, ship between carbon isotope discrimination and the intercel- lular carbon dioxide concentration in leaves. Aust J Plant 1468 Journal of Integrative Plant Biology (Formerly Acta Botanica Sinica) Vol. 47 No. 12 2005

Physiol 9, 121–137. irradiance on stable carbon isotope ratio, intercellular CO2 Farquhar GD, Ehleringer JR, Hubick KT (1989). Carbon iso- concentration and water-use efficiency of two woody plants tope discrimination and photosynthesis. Annu Rev Plant in subtropical natural forest. J Trop Subtrop Bot 3, 77–82 (in Physiol Plant Mol Biol 40, 503–537. Chinese with an English abstract). Francey RJ, Gifford RM, Sharkey TD, Weir B (1985). Physi- Marshall JD, Zhang J (1994). Carbon isotope discrimination ological influences on carbon isotope discrimination in huon and water-use efficiency in native plants of the north-central (Lagarostrobus franklinii). Oecologia 66, 211–218. Rockies. Ecology 75, 1887–1895.

Friend AD (2001). Modelling canopy CO2 fluxes: are “big-leaf” Martin B, Thorstenson YR (1998). Stable carbon isotope simplifications justified? Global Ecol Biogeogr 10, 603–619. composition, water use efficiency, and biomass productiv- Garten CT, Taylor GE (1992). Foliar δ13C within a temperate ity of Lycoperson esculentum, Lycopersicon pennelii, and

deciduous forest: Spatial, temporal, and species sources of the F1 hybrid. Plant Physiol 88, 213–217. variation. Oecologia 90, 1–7. Passioura JB (1982). Water in the soil-plant-atmosphere Gower ST, Richards JH (1990). Larches: Deciduous conifers in continuum. In: Lange OL, Nobel PS, Osmond CB, Ziegler H, an evergreen world. Bioscience 40, 818–826. eds. Encyclopedia of Plant Physiology, New Series, Vol. 12B. Houghton JT, Ding Y, Griggs DJ et al. (2001). Climate Change: Physiological Plant Ecology 2. Water Relations and Carbon The Scientific Basis. Cambridge University Press, Cambridge, Assimilation. Springer-Verlag, Berlin. pp. 5–33. UK. Peng S (1996). Southern Subtropical Forest Community Huc R, Ferhi A, Guehl JM (1994). Pioneer and late stage tropi- Dynamics. Science Press China, Beijing. pp. 444 (in Chinese cal rainforest tree species (French Guiana) growing under with an English abstract). common conditions differ in leaf gas exchange regulation, Qu CM, Han XG, Su B, Huang JH, Jiang GM (2001). Edge carbon isotope discrimination and leaf water potential. effects of plant water use efficiency indicated by foliar δ13C Oecologia 99, 297–305. value in a fragmented seasonal rainforest in Xishuangbanna. IPCC Working Group 1 (2004). Working Group I Workshop on Acta Phytoecol Sin 25, 1–5 (in Chinese with an English Climate Sensitivity. (Workshop Report). IPCC Working Group abstract). 1 Technical Support Unit, Boulder, Colorado, USA. Schulze ED, Williams RJ, Farquhar GD, Schulze W, Langridge Knight JD, Livington NJ, Kessel CV (1994). Carbon isotope J, Miller JM, Walker BH (1998). Carbon and nitrogen iso- discrimination and water use efficiency of six crops grown tope discrimination and nitrogen nutrition of trees along a under wet and dry land conditions. Plant Cell Environ 17, rainfall gradient in northern Australia. Aust J Plant Physiol 173–179. 25, 413–425. Liang YL, Kang SZ, Shan L (2000). The effects of soil moisture Smedley MP, Dawson TE, Comstock JP et al. (1991). Seasonal and nitrogen and phosphorus addition on carbon isotope carbon isotope discrimination in a grassland community. discrimination and water use efficiency in wheat. Acta Oecologia 85, 314–320. Phytoecol Sin 24, 289–292 (in Chinese with an English Stewart GR, Turnbull MH, Schmidt S, Erskine PD (1995). 13C abstract). natural abundance in plant communities along a rainfall Lin ZF, Peng CL, Lin GZ, Li SS (1994). Stable carbon isotope gradient: A biological integrator of water availability. Aust J ratio and activities of PEP carboxylase and PEP Plant Physiol 22, 51–55. carboxykinase in pineapple leaves. Acta Bot Sin 36, 534–538 Su B, Han XG, Li LH, Huang JH, Bai YF, Qu CM (2000). (in Chinese with an English abstract). Responses of δ13C value and water use efficiency of plant Lin ZF, Lin GZ, Kong GH, Zhang HB (1995). Effect of growth species to environmental gradients along the grassland zone Hai-Tao LI et al.: Seasonal Variation of δ13C of Four Tree Species: A Biological Integrator of Environmental Variables 1469

of Northeast China Transect. Acta Phytoecol Sin 24, 648– ing photosynthesis. In: Ehleringer JR, Hall AE, Farquhar 655 (in Chinese with an English abstract). GD, eds. Stable Isotope and Plant Carbon-Water Relations. Sun GC, Lin ZF, Lin GZ, Li SS (1993). 13C/12C ratio and water Academic Press, San Diego. pp. 43. use efficiency of Pinus massoniana in subtropical artificial Wright GC, Hubick KT, Farquhar GD (1988). Discrimination in forest. Chin J Appl Ecol 4, 325–327 (in Chinese with an carbon isotope of leaves correlated with water use efficiency English abstract). of field-grown peanuts cultivars. Aust J Plant Physiol 15, US Global Change Research Program (2001). A Plan for a New 815–825.

Science Initiative on the Global Water Cycle. USGCRP, Zhang H, Nobel PS (1996). Dependency of Ci/Ca and leaf tran- Washington, DC. pp. 118. spiration efficiency on the vapour pressure deficit. Aust J Vogel JC (1993). Variability of carbon isotope fractionation dur- Plant Physiol 23, 561–568.

(Managing editor: Ping HE)