ACTA PHYSIOLOGIAE PLANTARUM Vol. 28. No. 3. 2006: 257-262

The δ13C changes in four plant species of the Loess Plateau over the last 70 years Zheng Shuxia1, Shangguan Zhouping1,2,*, Xue Qingwu3 1 National Laboratory of Soil Erosion and Dryland Agriculture on the Loess Plateau, Institute of Soil and Water

Conservation, Chinese Academy of Sciences, Yangling, Shaanxi, 712100, P.R. China 2 Northwest Sci-Tech University of Agriculture and Forestry, Yangling, Shaanxi, 712100, P.R. China 3 Northwestern Agricultural Research Center, Montana State University, 4570 Montana 35, Kalispell, MT 59901, USA * Corresponding author e-mail: [email protected]

Introduction

Abstract 13

The relative abundance of carbon isotope (δ C) was measured in four C 3 species (Sophora viccifolia, Quercus liaotungensis, Ostryopsis davidiana and Zizyphus jujuba var. spinosa) of the Loess Plateau in China from the 1930’s to 2002. The results showed that the δ13C values in the four species varied from -25.05 ‰ to -29.75 ‰ with their average at -27.04 ‰. A decrease in the δ13C value with time was found in all the four species, which indicating that the water use efficiencies (WUEs) of all the measured species declined during 70 years. However, the decrease in δ13C value differed among the four species with its significant decreases measured in two of the species, Sophora viciifolia and Quercus liaotungensis, its relatively significant decrease found in Ostryopsis davidiana, and its slight decrease appearing in Zizyphus jujuba var. spinosa. in the δ13C values in the four species decreased by 14.65 ‰, 14.46 ‰, 11.99 ‰ and 2.44 ‰, respectively. The different species were shown to have different sensitivities to climatic change, and Zizyphus jujuba var. spinosa was found to be the most drought-tolerant species of the four, which had a high WUE.

Key words: 13C discrimination, C3 plant species, climatic change, WUE

Because

of increased world population, accelerated industrialization and global warming in the past 100 years, climatic changes have had significant influence on continental ecosystems and vegetation distributions. The water use efficiency (WUE) has become an important index to determine plant adaptability to environmental and climatic changes (Ziegler 1995, Shangguan et al. 2000, Saurer et al. 2004). The analysis of stable carbon isotope abundance (δ13C) has been widely adopted in many research fields such as vegetation evolution and paleoclimate reconstruction (Liu et al. 2002, Tu et al. 2004), and photosynthetic pathway determination (Farquhar et al. 1989, Pate and Noble 2000, Tcherkez et al. 2004). The δ13C in plant tissues can also be used to quantify certain aspects of the functional diversity in plant species and is put forward as a substitute for WUE (Farquhar et al. 1989). Generally, there is a positive relationship between δ13C and WUE in plants, and the plants with higher δ13C have higher WUE. With its use for more than 20 years as an analytical technique, δ13C

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has become a generally accepted approach to estimate the long-term plant WUE (Farquhar et al. 1989, Duquesnay et al. 1998, Shangguan et al. 2000, Saurer et al. 2004). Currently, using the technique of stable carbon isotope to measure the long-term WUEs under different environmental conditions and the δ13C responses in plants to climatic variables have been a hot topic in eco-physiological researches (Ziegler 1995). The technique has been used to study the δ13C responses to mineral nutrient availability (Bannister et al. 2002, Hamerlynck et al. 2004), light intensity (Tcherkez et al. 2003), precipitation (Warren et al. 2001, Wang et al. 2003), temperature (Tcherkez 2003), and increased CO2 concentration (Beerling et al. 1998, Zheng et al. 2001, Tu et al. 2004).

WUE is an objective index to evaluate water use and drought-tolerant characteristics of plants and thus capable of providing the theoretical basis for selecting proper plant species for specific environments (Yan et al. 1998). The Loess Plateau is a region with the severest soil erosion in the world and one of the most fragile ecosystems in China. Soil and water conservation is particularly important for the region. As a result, a better understanding of the responses of plant WUE to climatic change will be helpful to set up more sustainable ecosystems (Shangguan et al. 2002). However, little research on the responses of plant WUE to environmental change has been done in the natural ecosystems of the Loess Plateau. This paper presents a study which explored the δ13C changes in four typical species of the Loess Plateau during 70 years from 1930’s to 2002 on purpose of better understanding the relations between WUE and climatic change and thus providing the scientific basis for selecting drought-tolerant species for and reconstructing the forest vegetations in the Loess Plateau.

Materials and Methods Location and climatic conditions

The study was conducted in a hilly and loess region of China. The region running from Yan’an in its north to Tongchuan in its south and standing at 35°12′ - 36°36′ N and 109°12′ - 109°42′ E, is covered by forests that consist of deciduous broad leaf

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species. It belongs to the temperate semi-humid and semi-arid climatic zone. Its altitude ranges from 1000 to 1500 m. It has a mean annual temperature of 8.6-13 °C, a mean annual accumulative temperature ≥ 10 °C of 3000-5012 °C, a total annual rainfall of 530-730 mm mainly distributing in July and August, and an aridity index of 1.5. Its soils are mainly grey-brown soil and brown soil. Its major vegetation types are Quercus liaotungensis and Pinus tabulaeformis forests. Besides, there are Populus davidiana, Betula platycladus and Platycladus orientalis forests and some shrubs. Materials

In

accordance with the climatic conditions and vegetation distribution in the Loess Plateau, four represen tative species Quercus liaotungensis, Ostryopsis davidiana, Zizyphus jujuba var. spinosa and Sophora viccifolia were chosen as research materials. All of these species are C3 plants, Quercus liaotungensis is an arbor plant and the other three are shrubs. The specimens of the four species were obtained from the Specimen Museum of the Northwest Institute of Botany, the Chinese Academy of Science. According to the detailed sampling times, locations and site conditions recorded on the labels, the samples of Quercus liaotungensis were mostly collected from the lower canopy (2-3 m above ground) on northward slopes of the hilly loess region, while those of the other three species were taken from the upper canopies (2-3 m above ground) of Ostryopsis davidiana on northward slopes, and Zizyphus jujuba var. spinosa and Sophora viccifolia on southward slopes. The sampling principle was taking the samples from the specimens in each year of the nearly 70 years from 1930’s to 2002. The sampling depended on the available collections of the Specimen Museum in specific years. But there were at least two samples taken in each decade and totally 25 samples were taken from 160 specimens. Each sample consisted of 4-5 leaves in the same year but from different sites. In order to be consistent with local environments and reduce the differences among individual plants, the samples were only collected in places between Yan’an in the North and Tongchuan in the South (Lat. 35°12′ - 36°36′ N, Long. 109°12′ 109°42′ E) standing in the hill regions of the Loess

δ13C CHANGE IN FOUR PLANT SPECIES OVER THE LAST 70 YEARS

Table 1. The foliar δ13 C values in four species of the Loess Plateau in different decades†. Species

Family

Leaf carbon isotope composition δ13C ( ‰) 1930’s

1950’s

1970’s

1980’s

2002

Mean

Decrease from 1930’s to 2002 (%)

Quercus liaotungensis

Fagaceae

-25.51

-27.06

-25.92

-27.62

-29.20

-27.14

14.46

Ostryopsis davidiana

Betulaceae

-26.57

-26.71

-26.99

-26.93

-29.75

-26.99

11.99

Zizyphus jujuba var. spinosa

Rhamnaceae

/

-27.07

-26.69

-28.18

-27.73

-27.49

Sophora viccifolia

Leguminosae

-25.12

-26.40

-26.01

/

-28.80

-26.54

2.44‡ 14.65

†

No plant samples of Zizyphus jujuba var. spinosa in 1930’ and Sophora viccifolia in 1980’ are available due to the limited specimen stored in the Specimen Museum of Northwest Institute of Botany. ‡ The change of leaf δ13 C value in Zizyphus jujuba var. spinosa from 1950’s to 2002 is shown.

Plateau and the sampling time spanned between June and October. Stable Carbon Isotope Analysis carbon isotope δ13C was measured with a MAT-251 mass spectrometer (Finnigan, USA). One or two healthy, mature leaves (big without insect bites) were chosen from each specimen and ground to a uniformly fine powder in a thin agate mortar and then seized with an 80 mesh sieve. 3-5 mg processed samples were put into a vacuum quartz tube, where they were mixed with some Pt powder as activator, and oxidized in an oxygen flux at 850 °C, and then the CO2 thus produced was cryogenically purified with a liquid nitrogen trap after water was trapped with a dry ice-ethanol mix. Then, 13C was measured with a MAT-251 mass spectrometer in comparison with the PDB standard and a precision of <0.02 %. The results are expressed as

The

δ13C(‰)={[(13C/12C) sample-(13C/12C) standard]/(13C/12C) standard}×1000,

where (13C/12C) sample and (13C/12C) standard are the 13C/12C ratios of the sample and the standard (PDB, belemnite from the Pee Dee Formation) (Farquhar et al. 1989).

Results

During the nearly 70 years from 1930’s to 2002, the δ13C values in four species varied from -25.05

‰ to -29.75 ‰ with an average of -27.04 ‰. The δ13C value varied from -25.51 ‰ in 1939 to -29.20 ‰ in 2002 for Quercus liaotungensis, from -25.12 ‰ in 1933 to -28.80 ‰ in 2002 for Sophora viccifolia, from -25.05 ‰ - -29.75 ‰ for Ostryopsis davidiana, and from -26.69 ‰ - -28.69 ‰ for Zizyphus jujuba var. spinosa (Figure). The ranges of changes in δ 13 C was 4.70 ‰ in Ostryopsis davidian, 3.69 ‰ in Quercus liaotungensis, 3.68 ‰ in Sophora viccifolia, and 2.00 ‰ in Zizyphus jujuba var. spinosa. The δ13C values in four species appeared to significantly decrease as the climate and environment changed over the last century. However, the downtrend of δ13C in the four species was different (Figure). The δ 13 C val ues of Sophora viccifolia, Quercus liaotungensis and Ostryopsis davidiana significantly de creased. While, the δ 13 C value in Zizyphus jujuba var. spinosa slightly decreased compared to other three species. mean δ13C values of the four species in 1930’s, 1950’s, 1970’s, 1980’s and 2002 are shown in Table 1. In the nearly a century, the ranking of the average δ13C of the four species in different decades goes in the increasing order of Sophora viccifolia (-26.54 ‰)> Ostryopsis davidiana (-26.99 ‰)> Quercus liaotungensis (-27.14 ‰)> Zizyphus jujuba var. spinosa (-27.49 ‰). From 1930’s to 2002, the decrease of δ13C value in Sophora viccifolia and Quercus liaotungensis were significant, reaching 14.65 % and 14.46 %, respectively. The decrease of δ 13 C in Ostryopsis

The

259

Z. SHUXIA, S. ZHOUPING & X. QINGWU

Table 2. Annual precipitation and evaporation of the semi-arid region in different decades (unit: mm). Meteorological parameter

1950’s

1960’s

1970’s

1980’s

Precipitation

526.2

532.2

508.6

513.5

518.1

Evaporation

1632.4

1678.3

1647.2

1562.1

1629.2

davidiana was relatively obvious, reaching 11.99 %. While, the decrease of δ13C in Zizyphus jujuba var. spinosa was only 2.44 %. The maximum δ13C value occurred in 1930’s for Quercus liaotungensis and Sophora viccifolia, and occurred in 1970’s for Ostryopsis davidiana and Zizyphus jujuba var. spinosa. While the minimum δ13C value occurred in 2002 for all the three species but Zizyphus jujuba var. spinosa whose minimum δ13C value occurred in 1980’s.

from -21.7 ‰ to -30.0 ‰, averaging at -26.7 ‰. In this experiment, Quercus liaotungensis, Ostryopsis davidiana, Zizyphus jujuba var. spinosa and Sophora viccifolia chosen from the Loess Plateau were all C3 plants and their δ13C values varied from -25.05 ‰ to -29.75 ‰, averaging at -27.04 ‰, which is consistent with what Wang et al. (2003) reported.

Many research results have shown that there is a

positive correlation between δ13C and WUE in plants leaves (O’Leary 1988, Farquhar et al. 1989), and the changes of δ13C values may be used to evaluate long-term plant WUE (Ziegler 1995, Duquesnay et al. 1998, Saurer et al. 2004, Tu et al. 2004). Duquesnay et al. (1998) determined the δ13C value in the tree-rings of beeches growing in northwest France and found a 44 % increase in WUE over the last 100 years. Beerling et al. (1998) found that Ginkgo trees growing at high CO2 concentrations in the Mesozoic period presented a much higher WUE than those growing at regular CO2 level.

Discussion

In the researches about

260

2

R = 0. 6565

- 26 - 27 - 28 - 29 - 30 1920 1940

- 25

1960 1980 Year

2000 2020

2

R = 0. 3124

- 26 - 27 - 28 - 29 - 30 1920 1940

1960 1980 Year

y = - 0. 0396x + 51. 089

- 25

2

R = 0. 3911

1B - 26 - 27 - 28 - 29 - 30 1920

1940

1960

1980

2000

2020

Year

y = - 0. 0217x + 15. 395 1C

eaf carisotope bon isotcomposition ope compositio(n¡ (‰ LeafLcarbon ë) )

y = - 0. 0475x + 66. 405 1A

2000 2020

Leacarbon f carboisotope n isotopcomposition e composition ((¡‰ë )) Leaf

Leaf Leacarbon f carboisotope n isotopcomposition e composition ((¡‰ë ))

LeafLcarbon ë) ) eaf carisotope bon isotcomposition ope compositio(n¡ (‰

paleoecology and paleoclimate, the stable isotope analysis was conducted for pollen, plant residuals and silicate in the Loess Plateau to reveal the relations between vegetation and climatic change (Liu et al. 2002). Wang et al. (2003) analyzed carbon isotopes of 367 C3 herbaceous species growing in the loess region of northern China and found that the δ13C value ranged

- 25

1961-1990

- 25

y = - 0. 0526x + 76. 64 2

R = 0. 8762

1D

- 26 - 27 - 28 - 29 - 30 1920

1940

1960

1980

Year

2000

2020

Figure. Leaf carbon isotope compositions of Quercus liaotungensis (1A), Ostryopsis davidiana (1B), Zizyphus jujuba var. spinosa (1C) and Sophora viccifolia (1D) in different years from 1930’s to 2002. Every point shown is a value available from the measurement of a mixed sample consisted of 4-5 leaves in the same year but from different sites distributed in the areas between Yan’an in the North and Tongchuan in the South in the hilly regions of the Loess Plateau.

δ13C CHANGE IN FOUR PLANT SPECIES OVER THE LAST 70 YEARS

Zheng et al. (2001) an a lyzed the δ 13 C in wax-coated leaf specimen of Trema angustifolia BL. and Trema cannabina Lour. grow ing in Guangdong Province, China and stated that their WUEs increased by 19.5 % and 40.0 % over the last century, respectively. The above research results all showed that the elevated CO2 concentration is favorable for the improvement of plant WUE. Theoretically, the high CO2 can improve the photosynthetic capacity and then accelerate plant growth and biomass accumulation but restrain plant transpiration and then decrease its water loss, it thus contributes to an increase in plant WUE.

In this experiment, the foliar δ13C of four species decreased from the 1930’s to 2002, indicating that the plant WUE decreased over years. The result is not con sis tent with what Duquesnay (1998), Beerling et al. (1998) and Zheng et al. (2001) found. This is mainly related to plant species and specific environment conditions. Under typical semi-arid climatic conditions of the Loess Plateau, low precipitation, high evaporation and high soil water deficit are the dominant influential factors affecting δ13C values and resulting in significant decrease in WUE. Recently, based on the annual precipitation and evaporation data during 1951-1999 in the arid and semi-arid areas of China, Yang et al. (2003) found that the annual evaporation was about three times as high as the annual precipitation in the 1950’s, 1960’s, 1970’s and 1980’s (Table 2). The precipitation and evaporation were all reduced over the last 40 years; moreover, the decrease in precipitation was greater than that in evaporation. Therefore, the climate in the Loess Plateau became droughty. In the Loess Plateau, water deficit is the key limiting factor for plant growth. For a long time, plants responded morphologically and physiologically to adapt to the environment characterized by limited soil water and high evaporation, i.e. stomata closure, leaf area reduction and dwarfed plants. In recent years, there have been large areas of dwarf old trees and herbages in the Loess Plateau (Shangguan et al. 2002). Though atmospheric CO2 has increased significantly over the last century, the accumulation of photosynthetic production due to the elevated CO2 was far less than the amount of water loss due to high evapo-transpiration, and this resulted in the decreases in long-term plant WUE.

The minimum δ13C value of all the three species but Zizyphus jujuba var. spinosa occurred in 2002, which indicated that plant WUE decreased drastically in recent years. During nearly a century, the decreases in foliar δ13C values of the four species differed. The δ13C values of Sophora viccifolia and Quercus liaotungensis decreased more significantly than those of Ostryopsis davidiana and Zizyphus jujuba var. spinosa, which indicated that the different species showed different sensitivities to climatic change. The δ13C of Zizyphus jujuba var. spinosa decreased much less than did those of the other three species, which indicated that the WUE of Zizyphus jujuba var. spinosa decreased less than the other three species, indicating that Zizyphus jujuba var. spinosa was more drought-tolerant and had higher WUE than the other three species.

Acknowledgements

This study was funded by the National Natural Science Foundation of China (Project No: 30370230) and the United Scholar's Item of Talent Training Program in West China of Chinese Academy of Sciences.

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Received May 09, 2005; accepted October 12, 2005 edited by Z. Krupa

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