There have been debates on the driving factors of C4 plant expansion, such as PCO2 decline in the late Micocene and warmer climate and precipitation at large-scale modern ecosystems. These disputes are mainly due to the lack of direct evidence and extensive data analysis. Here we use mass flora data to explore the driving factors of C4 distribution and divergent patterns for different C4 taxa at continental scale in China. The results display that it is mean annual climate variables driving C4 distribution at present-day vegetation. Mean annual temperature is the critical restriction of total C4 plants and the precipitation gradients seem to have much less impact. Grass and sedge C4 plants are largely restricted to mean annual temperature and precipitation respectively, while Chenopod C4 plants are strongly restricted by aridity in China. Separate regression analysis can succeed to detect divergences of climate distribution patterns of C4 taxa at global scale.
Modern ecosystems, such as tropical savannas, temperate grasslands and semi-deserts, have a significant component of C4 plants1. At global scale, only about 3% of total plant species is characterized by C4 photosynthetic pathway, C4 plants, however, account for roughly 25% of global terrestrial primary production, including important crops, weed plants and potential biofuels2,3. Understanding the occurrence and distribution of C4 biota can yield important information regarding to global primary productivity and to the effects of climate changes on ecosystem structures and functions2,4,5, as well as C4 plant’s past, present and future.
The abundance of C4 species in particular regions and their distribution in relation to climate have been well reported in North America6, Africa7,8, Europe9,10, Australia11, Middle East12,13, but has not been studied details in China and this knowledge is essential for formulating generalization regarding to global C4 occurrence and their relation with climate. The vast area and varied terrain in China with complex ecosystem components (e.g. rain forests, wet lands, temperate grasslands, deserts and tundra) and great climate changes contain more different C4 information. Moreover, the deserts in China and Asia differ markedly from the arid ecosystems of North America, Australia and Europe in the taxonomic groups of C4 species5,14. In China deserts and arid regions, Chenopodiaceae is the leading C4 family, but their distribution in relation to climate has not yet been addressed, this is very important for understanding the effects of climate changes on ecosystem structures and functions, particularly with the increasing of desertification in west China in recent decades15.
Although the occurrence and distribution of C4 plants have been documented at different scales over the past couple of decades, there have been debates on C4 plant expansion at large-scale1,16,17,18,19, for example, (i) what is the driving factor for C4 plant expansion, decrease in atmospheric CO2 concentration in the late Miocene or climate (both ancient and modern) variability19−21? It had been hypothesized that PCO2 decline caused C4 plant expansion rapidly during the late Micocene (~8 to 4 Ma)1,16,17, but some evidences suggested that C4 plant expansion was likely driven by addition factors, such as enhanced low-latitude aridity, seasonal precipitation19 and fire20 in the Miocene. The present-day global distribution of C4 grasses is largely restricted to warmer climate and precipitation, for strong positive relationships between C4 grass abundance and growing season temperature at continental scales5,18. Few found that the restriction of C4 grasses to warmer areas was due largely to their evolutionary history2. (ii) whether the different C4 taxa have similar climate distribution pattern in present-day at large-scale21,22? Indeed, there are few large data sets with which to examine occurrence and climate distribution pattern of different C4 taxa in modern vegetation at continental areas, resulting severely limits the accuracy understanding C4 plant expansion and the ecological implications.
Of the total vascular plants (about 30000 species) in China, 371 species are identified with C4 photosynthesis in 11 families (Table 1; Supplementary Table S1), but 90.83% C4 species occurring in Gramineae (53.64%), Cyperaceae (19.67%) and Chenopodiaceae (17.52%; Chenopod, hereafter). Relative lower C4 plant occurrence is due largely to there is no tropical savannas (with more C4 grasses) in China. In general, total C4 species abundance decreases from south to north and from east to west in China (Fig. 1a,b). The total C4 species abundance in Heilongjiang (most northern territory) is only 1/3 of that in Yunnan (most southern territory), while that in western province of Qinghai is less than 1/3 of that in Taiwan (Fig. 1b). The total C4 species abundance is strongly and positively related with mean annual temperature (Tm) (R2 = 0.56, P < 0.0001) and mean annual precipitation (Pm) (R2 = 0.47, P < 0.0001; Fig. 2a–c). Multiple regression of the total C4 species abundance (YtotalC4) against climate variables shows that there is a strongly and positively correlation between YtotalC4 and Tm, Pm and aridity (AI) as model:
This indicates that these climate factors affect the distribution of total C4 species abundance in China. Stepwise multiple regression analysis exhibits that Tm has highest contributions (61.5%) to total C4 species distribution, while the impacts of Pm (2.0%) and AI (2.6%) are relative less (Table 2).
C4/C3 proportion in China flora is about 1.2%, ranging from 0.85% in Tibet to 4.77% in Shandong province (Fig. 3). Most humid southern provinces (e.g. Yunnan, Guangxi and Sichuan) have lower C4/C3, even though the occurrence of C4 species is high in these regions. There are no significant relations between C4/C3 proportions and climate variables in present-day vegetation in China (P > 0.05; Fig. 2d–f), indicating that C4/C3 proportion dose not exhibit certain ecological pattern, even the C4 occurrence dose significantly related with plant abundance at large-scale region.
C4 distribution patterns predicted by total C4 species abundance appear to be insensitive to climate factors known to influence C4 occurrence and expansion because of the different adaptive strategies for C4 taxa to climate variables. Both grass and sedge C4 species abundances are strongly and positively related with Pm (R2 = 0.51, P < 0.001; R2 = 0.58, P < 0.001) and Tm (R2 = 0.50, P < 0.001; R2 = 0.65, P < 0.001), but significantly and negatively with aridity (R2 = 0.23, P < 0.01; R2 = 0.55, P < 0.001) (Fig. 4a–c). Multiple regressions of grass C4 species abundance (YgrassC4) and sedge C4 species abundance (YsedgeC4) against climate variables manifest that YgrassC4 and YsedgeC4 are strong correlated with Tm, Pm and AI as models:
But stepwise multiple regression analysis demonstrates that grass C4 plant distribution is largely restricted to Pm (50.6%), and Tm and AI functions are not significant (P > 0.05). Sedge C4 species is mainly limited to Tm (64.7%) and the impacts of Pm (0.2%) and AI (2.3%) are very less and no significant (P > 0.05; Table 2).
On the contrary, Chenopod C4 plant abundance is strongly and positively related with AI (R2 = 0.88, P < 0.001), and significantly and negatively with both Pm (R2 = 0.92, P < 0.001) and Tm (R2 = 0.25, P < 0.001; Fig. 4a–c). Stepwise regression of Chenopod C4 plant abundance against climate variables shows that there is a strong correlation between YChenopod C4 and Tm, Pm and AI as model:
Stepwise multiple regression analysis exhibits that Chenopod C4 plants is confined to arid index (88.2%) in present-day vegetation at whole China. These suggest the distributions of C4 taxa are restricted to different climate factors at present-day vegetation in China.
There were many studies on the C4 plant expansion and distribution in relation to climate over the past couple of decades1,16,17,18,19, but only few manifested the detail floristic data of C4 occurrence in large regional scale (e.g. Europe9,10, Middle East13, Central Asia14). 371 identified C4 species within China account for roughly 20% of known C4 plants (about 1800 species global) and that is much greater than the percentage (~13%) of China vascular species to worldwide angiosperms, even though China is not a hot spot for C4 photosynthesis (Fig. 1; Supplementary Table S1). The total number of C4 species in China (Table 1), mainly grasses (53.64%), sedges (19.67%) and Chenopods (17.52%), is much greater than that in Europe9 and Middle East13. However, the number of Chenopod C4 species is only 1/3 of that in Middle East and 1.5 times of that in Mongolia14, probably because China arid regions is smaller than Middle East, but larger than Mongolia. This knowledge is essential for building global C4 plant database and formulating generalization regarding their relation to global climate.
What is the driving factor for C4 plant expansion and distribution remains controversial. The evidences of palaeovegetation and fossil tooth enamel indicated the global expansion of C4 plants may be related to lower PCO2 in the Miocene1,16,17, but some evidences suggested that C4 plant expansion was likely driven by climate variables and fire in both old world and present-day vegetation19,20. Our data clearly demonstrate that C4 plant distributions are restricted to mean annual climate variables (e.g. Tm, Pm and AI) in the present-day vegetation in China (Fig. 2). From the south to the north, Tm governs the vegetation changes, while from the east to the west moisture gradient (Pm) drives plant distributions23,24. Within China, the total C4 species abundance is strongly and positively related with Tm and Pm, this suggests that there is remarkably strong tendency for C4 species to grow in hot and wet conditions, even though the stepwise multiple regression analysis exhibits that the impact of Pm is relative less (Table 2). This is much different with previous observations6,11,25, their evidences manifest that July average daily temperature is a critical factor for C4 distribution and the precipitation gradients seem to have much less impacts. Such significant difference is probably because almost 2/3 identified C4 species are perennial grasses, sedges and some Polygonaceae species, relative higher Pm and Tm are not only favor for their growth in growing seasons, but also for their survival in winters15,23,24. This is also partly supported by the observation of soil organic carbon and present vegetation which indicates that C4 fraction of Inner Mongolia grassland has increased by approximately 10% in the past decades because of increasing of temperature26.
The C4/C3 proportion in China flora is about 1.2% and much lower than 3% estimated at global scale4,18. This is mainly due to complex relief in China, 2/3 of the total area is mountains and plateaus23. More mountains and high moisture in southern provinces lead to vast forest vegetation with relative more tree species and lower fractions of grasses and Chenopod species, even the species abundances for both C3 and C4 plants are much high in the southern regions. In addition, lower C4 plant occurrence in China is for the absence of tropical savannas, which is estimated with more C4 grasses1, but large area of temperate grasslands and deserts (40% of China land) devotes considerable C4 plant resources5,15. There are no significant relations (P > 0.05) between C4/C3 proportions and climate variables in present-day vegetation in China (Fig. 2d–f), indicating that C4/C3 proportions do not show certain ecological pattern (Fig. 3), even though C4 occurrence dose significantly related with plant abundance at large-scale region.
Separate analysis for different C4 taxa succeed in detecting C4 distribution patterns accurately at continental scale, for the separate analysis can eliminate the noise signal from the C4 taxon with different responses to climate variables and adaptive strategies. Previous studies had found that grass and sedge C4 plants were largely restricted to July average daily temperature6,11,18,25. However, it is different in China, separate multiple regression analyses display that the grass and sedge C4 plant abundances are mainly restricted to Pm and Tm respectively (Table 2). Most grass C4 species are terrarium plants and their distributions are mainly restricted to Pm, while almost all sedge C4 species are aquatic plants and the distributions of sedge C4 taxon is governed by Tm in China. This explanation is also supported by the relative higher proportions of perennial C4 grasses and sedges in the floristic data (Supplementary Table S1). Unlike the grass and sedge C4 plants, the distribution of Chenopod C4 taxon is drove by aridity (Table 2; Fig. 4). Chenopod C4 plants are favored arid regions with hot summer and sufficient summer precipitation, because most of Chenopod C4 plants are annual plant species, they can use seasonal precipitation efficiently in dry and hot conditions where the precipitation mainly falls in growing season, and these species can withstand severe droughts as seeds15. Even though there are a few studies on the occurrence of C4 Chenopods in particular regions13,14, but C4 Chenopod distribution in relation to large-scale climate change has remain largely unexplored and this is important for understanding the effects of climate changes on arid ecosystems with the increase of desertification in west China15. In the dry west China (e.g. Xinjiang, Qinghai and Inner Mongolia), 30–45% of the total C4 species is Chenopod plants, while that in the east and south China is less than 1%. Predominant C4 Chenopods in hot and arid ecosystems, as well as strong relations with aridity (Fig. 4), imply that the expansion of C4 Chenopods may be enhanced in China with an increase in hot and aridity worldwide as some climate- change scenarios suggested. Moreover, previous studies proved that the advantage of C4 plants in water-limited deserts are not considered critical for establishing C4 grass distribution pattern, and are commonly invoked to explain the dominance of C4 dicots21,27, even though they did not separate Chenopod C4 species from dicots.
Driving factor for C4 plant expansion at spatial and temporal large-scale is controversial. The palaeosol carbonate and fossil tooth enamel data implicated that the C4 plant expansion may have been due to decreasing of PCO2 in late Miocene1, but other evidences suggested that the development of low-latitude season aridity and changes in growing conditions led to the expansion of C4 plants at ~7 Ma19. These different explanations are mainly due to the lack of direct evidences and extensive data analysis. Our mass flora data analysis partly supports Pagain’s perspective19, but their evidences also can not explain the divergence distribution pattern of different C4 taxa. The divergence in C4 climate pattern implicates these C4 taxa may be with different area of origins, evolutionary histories2,21, expansion mechanism and adaptive strategies, because the Chenopod C4 taxon has a diametrically opposed distribution pattern with grass and sedge C4 taxa (Fig. 4). In the previous studies6,18,25, it had been found that grass and sedge C4 plants are governed by July average daily temperature, but the distribution of grass, sedge and Chenopod C4 species in China are largely restricted to Pm, Tm and AI respectively, for the mean annual climate variables (especially Pm and Tm) can accurately describe the climate restrictions of plant distributions in China23,24. Edwards and Still also proved that the restriction of C4 grasses to warmer areas was due largely to their evolutionary history2.
Comparing with most previous researches1,16–19 this work provides detail floristic data of C4 occurrence in large regional scale based on China flora sources, which is essential for building worldwide C4 plant database, and also contributes direct evidence formulating generalization regarding the driving factors of C4 plant expansion. We suggest that the restriction of C4 distributions at continental scale is due to largely the annual climate variables (e.g. Pm, Tm and AI) in present-day ecosystems in China. Different C4 taxa may exhibit diametrically opposite pattern in relation to climate at large-scale likely due to their differences in adaptations, area of origins and evolutionary histories2,21. Our findings suggest that the expansion of C4 Chenopods will increase with the increasing of aridity in western and central China as climate- change scenarios expected, on the contrary, that for grass and sedge C4 species may decrease in the future. This may have huge impacts on vegetation dynamics and primary plant production for the C4 plants accounts for roughly 1/4 of global terrestrial primary production2,3.
China topography and climate
China, occupied a large area, about 9.6 million km2 (3°51′–53°33.5′N; 73°33′–135°05′E), stretches 5,026 km across the East Asian landmass. It is primarily mountains, plateaus and plains country, 2/3 of the total area is mountains and plateaus23. Land elevation in the east plains is about 100–200 m above sea level (as l), while that in the southwest mountains and plateaus are as high as 4000–8000 m as l. The relief is very complicated with both latitudinal and longitudinal climate zones, mixed with steep altitudinal gradients in the northwest and southwest parts, leading great changes in climate.
The climate in China is extremely diverse due to its wide coverage, assortment of terrains and distances to the sea for different locations. Most of China lies in the temperate belt, with its south in subtropical belt and north in subarctic belt. In general, the average temperature in China is 11.8 °C, varying from 31 °C in July to −10 °C in January. Because of the Influences of both latitude and monsoon activities, temperatures vary a great deal, low temperature in winter is −40°C in Mohe, the northernmost of China, while in hot summer temperature can be as high as 50 °C in Turpan basin, Xinjiang. The average annual precipitation is about 620 mm, ranging from 150–400 mm in the western deserts and semi-deserts to 500–800 mm in the central region and vast flat plains, and 800–1000 mm in the eastern and coastal areas. The main nature vegetation types include tropical rain forest, wet land, grassland, desert and tundra23.
Obtaining C4 taxon data and analysis
Local C4 taxon data of 32 provinces and municipalities (Fig. 1a) were collected from the C4 plant database of Plant Adaptation Strategy and Mechanism Group, Institute of Botany, CAS, Reipublicae Popularis Sinicae23, Catalogue of Life China and local flora sources28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60. Long-term (1950–2010) climate data were provided by the National Meteorological Information Center of China Meteorological Administration. C4/C3 proportion refers to the ratio of C4 species number to C3 species number in local flora. Regressions of C4 taxon (e.g. total C4 species abundance, grass and sedge C4 species abundances) against climate variables (e.g. temperature, precipitation and aridity) were performed using SPSS 17.0 in order to explain the distribution patterns of C4 taxa accurately at global scale. Stepwise multiple regression analyses between C4 taxon and climatic variables were used to quantify the critical restriction of C4 taxon. All statistical analyses were performed using SPSS 17.0 (SPSS for Windows, Chicago, IL, USA).
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This research was funded by grants from National Scientific Foundation of China (31070228, 31170304). We are grateful for the free climate data provided by National Meteorological Information Center of China Meteorological Administration and Worldclim-Global Climate Data (http: //www. worldclim.org/).
The authors declare no competing financial interests.
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Wang, R., Ma, L. Climate-driven C4 plant distributions in China: divergence in C4 taxa. Sci Rep 6, 27977 (2016). https://doi.org/10.1038/srep27977
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