BGBiogeosciencesBGBiogeosciences1726-4189Copernicus PublicationsGöttingen, Germany10.5194/bg-15-693-2018Variations and determinants of carbon content in plants: a global synthesisMaSuhuiHeFengTianDiZouDongtingYanZhengbingYangYulongZhouTianchengHuangKaiyueShenHaihuaFangJingyunjyfang@urban.pku.edu.cnDepartment of Ecology, College of Urban and Environmental Sciences, Peking University, Beijing 100871, ChinaCollege of Life Sciences, University of Chinese Academy of Sciences, Beijing 100049, ChinaCollege of Life Sciences, Capital Normal University, Beijing 100048, ChinaCollege of Earth and Environmental Sciences, Lanzhou University, Lanzhou 730000, ChinaState Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, ChinaJingyun Fang (jyfang@urban.pku.edu.cn)2February201815369370225July20176September20178December201718December2017This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/This article is available from https://bg.copernicus.org/articles/15/693/2018/bg-15-693-2018.htmlThe full text article is available as a PDF file from https://bg.copernicus.org/articles/15/693/2018/bg-15-693-2018.pdf
Plant carbon (C) content is one of the most important plant traits and is
critical to the assessment of global C cycle and ecological stoichiometry;
however, the global variations in plant C content remain poorly understood.
In this study, we conducted a global analysis of the plant C content by
synthesizing data from 4318 species to document specific values and their
variation of the C content across plant organs and life forms. Plant organ C
contents ranged from 45.0 % in reproductive organs to 47.9 % in stems at
global scales, which were significantly lower than the widely employed
canonical value of 50 %. Plant C content in leaves (global mean of
46.9 %) was higher than that in roots (45.6 %). Across life forms, woody
plants exhibited higher C content than herbaceous plants. Conifers, relative
to broad-leaved woody species, had higher C content in roots, leaves, and
stems. Plant C content tended to show a decrease with increasing latitude. The
life form explained more variation of the C content than climate. Our
findings suggest that specific C content values of different organs and life
forms developed in our study should be incorporated into the estimations of
regional and global vegetation biomass C stocks.
Introduction
Carbon (C) is one of the most abundant elements in all living organisms
(Hessen et al., 2004; Dietze et al., 2014). Plant photosynthesis transfers C
from CO2 to the forms of biological compounds to maintain metabolic
functions and build basic structures (Dietze et al., 2014;
Martínez-Vilalta et al., 2016). This process creates a huge organic C
pool in terrestrial vegetation (Schlesinger and Bernhardt, 2013), which is
usually estimated by multiplying total plant biomass by a corresponding
biomass C conversion factor, i.e., the C content (Bert and Danjon, 2006;
Thomas and Martin, 2012). The most widely employed C content in plants is
50 % in the regional and global vegetation C stock estimations (De Vries
et al., 2006; Keith et al., 2009; Lewis et al., 2009; Saatchi et al., 2011;
Zhu et al., 2015, 2017). Originally, this value was calculated from an
average molecular formula CH1.44O0.66, i.e., elemental
composition of about 50 % C, 6 % hydrogen, 44 % oxygen, and trace
amounts of several metal ions in living plant wood (Pettersen, 1984;
Bert and Danjon, 2006).
However, an increasing number of studies have indicated that C content
varied significantly among plant organs (Alriksson and Eriksson, 1998; Bert
and Danjon, 2006; Yao et al., 2015), life forms (Tolunay, 2009; Fang et al.,
2010; Cao and Chen, 2015), biomes (He et al., 2006; Martin and Thomas, 2011;
Martin et al., 2015), and even across individuals (Elias and Potvin, 2003;
Uri et al., 2012; Martin et al., 2013). Using the default value of 50 % as
biomass C conversion factor which ignores the variation of C content may
lead to biases (Zhang et al., 2009; Martin and Thomas, 2011; Rodrigues et
al., 2015). For example, a change of 1 % wood C content from the canonical
value of 50 % can bring up to ∼ 7 Pg C variation in
global vegetation C stocks, which is almost equivalent to half of the
vegetation C stocks of the continental United States (Dixon et al., 1994; Jones and
O'Hara, 2016). Therefore, accurate knowledge of plant C content is crucial
for estimating the potential magnitude of C sequestration in different
biomes and understanding the roles of vegetation in the global C cycle
(Thomas and Martin, 2012).
To reduce the uncertainty in estimation of vegetation C stocks, several
studies have used the species-specific organ C content at regional scales
(Jones and O'Hara, 2012; Rodrigues et al., 2015; Wu et al., 2017).
Basically, the weighted mean C content (WMCC) of plants, especially woody
plants, was useful for precise C stock estimation (Zhang et al., 2009).
However, it is hard to obtain available data of C content and biomass
allocation for every species and organ in diverse vegetation. Combining the
phylogenic, taxonomic and environment-dependent traits of species, the
generalized C contents of specific life forms provide an alternative for
realistic estimations (Thomas and Martin, 2012; Wu et al., 2017). For
instance, the Intergovernmental Panel on Climate Change (IPCC, 2006)
provided the wood C content of trees in tropical/subtropical forests
(47 %) and temperate/boreal forests (48 % of broad-leaved trees and 51 %
of conifers). Although the values were more accurate than the
default value of 50 %, errors were still introduced to C stock estimation
in the actual application (Martin and Thomas, 2011), especially when the
uncertainty that resulted from estimation using available plant C contents of
limited specific life forms could not be eliminated (Thomas and Martin,
2012). Thus, the specific C contents of different life form plants require
explicit consideration and application in vegetation C stock evaluations. In
addition, exploring the biogeographic pattern and driving factors of plant C
content will be of benefit for the elucidation of ecological stoichiometry and the
mechanisms of plants' response to global change (Fyllas et al., 2009;
Ordoñez et al., 2009; Zhang et al., 2012).
For the above reasons, we compiled a global dataset of plant organ C content
to provide referable C contents of plant organs in different life forms. We
tried to answer the following two questions: (1) how much C do specific
plant organs contain? (2) What are the biogeographical patterns of plant
C content and the possible driving factors?
Material and methodsData compilation
We searched Google Scholar (https://scholar.google.com/), Web of Science
(http://isiknowledge.com), and CNKI (China National Knowledge Infrastructure)
(http://www.cnki.net/) for literatures reporting the C content of plants
published from 1970 to 2016. We documented 315 publications according to the
following two criteria: (1) the data from natural ecosystems (including
wetland and mangrove) or plantation ecosystems (including grassland and
cropland) were included, while the data from laboratory or field experiments
were excluded; and (2) plant C content detected by two commonly used methods
(i.e., the K2Cr2O7–H2SO4 oxidation and the
combustion methods) was included, while studies that used the default value,
assumed value, or values calculated from the chemical compositions were
excluded from our data compilation. In addition, we also included data of
specific plant organs from the TRY database (https://www.try-db.org) (Kattge
et al., 2011) (Table S1 in the Supplement).
Finally, a total of 24 326 records of 4318 species in 1694 genera and 238
families were included in our global dataset (Fig. 1), in which 36.33
and 63.67 % were from literatures and the TRY database, respectively. For
each data record, we documented the geographical information (latitude,
longitude, and altitude), Latin binomial, genus and family of species, organ
(reproductive organ, root, leaf, and stem), life forms, chemical compounds
(lignin and cellulose), and plant C content. Plant life forms were divided
into five categories: herbaceous species (herb), woody plants, fern, vine,
and bamboo. Data of crops were separately analyzed in the herbaceous
category. The woody plants were further categorized into three groups:
evergreen broad-leaved woody plants, deciduous broad-leaved woody plants, and
conifers. The data with no information on life forms were documented
from Flora of China (http://foc.eflora.cn), Wikipedia
(https://en.wikipedia.org/wiki/Wiki/), Useful Tropical Plants
(http://tropical.theferns.info), or The Plant List
(http://www.theplantlist.org). In order to explore biogeographic patterns and
the driving factors of C content of plant organs, we used the latitude and
longitude of each site to extract data of climatic variables (mean annual
temperature, MAT, ∘C; mean annual precipitation, MAP, mm) from
WorldClim (http://www.worldclim.org/) (Hijmans et al., 2005). Given that
plant C content might vary with the growth stages of individuals (Elias and
Potvin, 2003; Uri et al., 2012; Martin et al., 2013), we recorded the
averaged C content of herbaceous species across different growth stages.
Geographic distribution of sample sites used in this
synthesis.
Plant carbon content (%) in four organs across
different life forms. n is the sample size, and SD is the abbreviation of
standard deviation. Samples for stem include the samples from shoot, stem,
twig, and branch. “–” indicates no data.
Histograms of carbon content of (a) reproductive organ,
(b) root, (c) leaf and (d) stem. Abbreviations: SD, standard deviation; CV,
coefficient of variation; n indicates sample size.
Statistical analyses
We first documented statistics of plant organ C content for different life
forms, including arithmetic mean (Mean), median (Median), standard deviation (SD),
and coefficient of variation (CV) (Table 1). The C content of each
organ showed a normal distribution (Fig. 2), and thus the one-sample
Student's t-test was used to determine whether the stem C content of woody
plants significantly differed from the default value of 50 % and the IPCC
values (47, 48, and 51 %), respectively. The two-sample Student's
t-test was used to determine whether statistical differences of plant organ
C content existed between different life forms. Specifically, we compared
the C contents of herbs vs. woody plants, conifers vs. deciduous
broad-leaved woody plants, and conifers vs. evergreen broad-leaved woody
plants.
Trends in the plant carbon contents along latitude and
climate gradients. MAT, mean annual temperature; MAP, mean annual
precipitation. Ordinary least squares (OLS) regression lines are fit to the
data. Solid lines indicate the significant relationships with p < 0.05, and dashed lines denote the insignificant
relationships with p > 0.05. Abbreviations: repr carbon content refers to the reproductive organ carbon content.
Plant carbon content in roots and leaves showed a significant latitudinal
trend.
Variation partitioning (r2) of climate and life forms
to account for the variation in plant carbon contents across different
organs. (a) Reproductive organ, (b) root, (c) leaf, and (d) stem. Life form
independently explained more variation of carbon content in each organ than
climate.
Relationships between plant carbon content and lignin and
cellulose among three organs. Plant carbon content increases significantly
with the increasing lignin in plants (r2= 0.29, p < 0.001),
whereas it is not correlated with the cellulose in plants.
Relationships between plant carbon content and lignin and
cellulose in woody plants and herbaceous plants. Plant carbon content
increases significantly with increasing lignin in plants (r2= 0.29,
p < 0.001), whereas it is not correlated with the cellulose in
plants.
A linear model without accounting for other factors was used to explore
biogeographical patterns of plant organ C content along latitudinal
gradients, MAT and MAP (Han et al., 2011). To evaluate the effects of life
form and climatic factors (i.e., MAT and MAP) on the variations of plant C
contents, a partial generalized linear model was used to calculate the total
explanation, the independent explanation, and the interactive explanation of climatic
factors and life forms for different organs (i.e., reproductive organ, root,
leaf, and stem)(Han et al., 2011). Additionally, a linear
model and an analysis of variance (type III) were performed to test
the variations of C contents explained by climatic factors and life forms. A
linear model was used to explore the relationship of plant C content with
the content of lignin and cellulose. All statistical analyses were performed
in the R 3.3.1 software (R core Team, 2016).
ResultsCarbon content of plant organs
Plant C content varied significantly among organs. Arithmetic means of C
content for reproductive organ, root, leaf, and stem were 45.01,
45.64, 46.85, and 47.88 %, respectively (Fig. 2, Table 1), all of
which were significantly lower than the default value of 50 % (p < 0.05).
Plant organ C content also varied markedly across life forms (Table 1). Among herbaceous plants, C content ranged from 42.41 % in stems to
44.73 % in leaves, and among woody plants, C content changed from
47.43 % in roots to 48.56 % in reproductive organs (Table 1). C contents
in all four organs were significantly higher in the woody species than in
the herbaceous species. Across woody species, C contents in roots, leaves,
and stems of conifers were significantly higher than those of deciduous
broad-leaved and evergreen broad-leaved woody plants. In
addition, the C contents of ferns, vines, and bamboo ranged from 42.98 to
49.20 % (Table 1).
Latitudinal trends of carbon content and possible driving
factors
Plant C contents in roots and leaves decreased with increasing latitude and
decreasing MAT and MAP (r2= 0.05, p < 0.001 in all cases),
while reproductive and stem C content displayed no significant latitudinal
trends (r2= 0.02, p > 0.05; r2 < 0.01, p > 0.05; Fig. 3, Table S2).
The C content of plant organs was significantly affected by climatic factors
(p < 0.05 in stem), life form, and their interaction (p < 0.05
in all cases, except for reproductive organs) (Tables S3–S6).
The effects of climatic factors and life forms on plant C content varied
largely across the plant organs (Fig. 4). The independent explanations of
climatic factors on the variation in the C contents of the reproductive
organs, roots, leaves, and stems were 8.4, 0.2, 3.8, and 0.5 %,
respectively. The variation of C content in the reproductive organs, roots,
leaves, and stems explained independently by life forms were 19.8,
21.5, 7.2, and 10.0 %, respectively. The interactive explanations
of climatic factors and life form on the variation of C content of the
reproductive organs, roots, leaves, and stems were 15.7, 3.6,
5.2, and 0.7 %, respectively. These results demonstrated that the
variation of plant C content was explained more by life form than by
climatic factors (Fig. 4; Tables S3–S6).
Discussion
We evaluated plant C content across plant organs and life forms by
establishing a global plant C content dataset. Our results showed that plant
C content varied remarkably among organs, which was consistent with previous
studies (Alriksson and Eriksson, 1998; Northup et al., 2005; Tolunay, 2009).
Notably, we found that the global average C contents of four organs were
significantly lower than the canonical value of 50 %, which was widely used
to convert vegetation biomass to C stock at large scales, such as in
temperate forests (De Vries et al., 2006), tropical forests (Lewis et al.,
2009; Saatchi et al., 2011), and global forests (Keith et al., 2009). In
addition, C contents of stems and leaves were significantly higher than
another default value of 45.45 % proposed by Whittaker (1975), although
the C contents of roots and reproductive organs showed no significantly
statistical difference. Furthermore, our results showed that plant C
contents varied significantly among life forms (Table 1). Among woody
plants, the stem C contents of broad-leaved woody species (i.e., 47.69 % in
deciduous and 47.78 % in evergreen) and conifers (51.48 %) were
comparable with those (47.7 and 50.8 %, respectively) reported by
Thomas and Martin (2012). However, these data were significantly lower than
the values of temperate broad-leaved woody species (48 %; p < 0.001
and p= 0.018) and conifers (51 %; p < 0.001), though higher than
those of tropical broad-leaved woody species (47 %; p < 0.001 and
p < 0.001) proposed by IPCC (2006). This suggested that these values
from IPCC may underestimate or overestimate the stem C content for
broad-leaved trees and conifers at global scales.
The variation of plant C content among organs and life forms was associated
with differences in their chemical compositions (Figs. 5–6). Plant organs
are composed of several organic compounds with different C content, such as
lignin (with C content of 63–66 %), cellulose (with C content of
about 44 %), and nonstructural carbohydrates (NSC) (e.g., sugar or starch
with C content of about 44 %) (Adler, 1977; Poorter and Bergkotte, 1992).
Our result was consistent with previous findings that plant organs with
higher lignin (e.g., stems) tend to have a higher C content than organs with lower
lignin content (e.g., leaves, roots, and reproductive organs; Fig. 5a)
(Savidge, 2000; Lamlom and Savidge, 2003; Bert and Danjon, 2006; Martin and
Thomas, 2011). Despite the high lignin in roots, the C content in roots
was lower than that in leaves, probably because of the high proportions of
protein and other C-rich compounds in leaves (Rouwenhorst et al., 1991;
Niinemets et al., 2002) and high content of starch in roots (Bert and
Danjon, 2006). The lowest C content in reproductive organs was consistent
with its high quantities of NSC and low content of lignin (Barros et al.,
1996). Across life forms, woody plants generally require proportionally
greater investments of C at the cellular level to synthesize lignin to
support structures with relatively low growth rate, which result in high
lignin and C content (Fig. 6a). In contrast, the high relative growth rate
of herbs is accordant with their low lignin and C content (Armstrong et al.,
1950; Johnson et al., 2007). Furthermore, the difference in stem C contents
of broad-leaved woody plants (i.e., 47.69 and 47.78 % for deciduous and
evergreen species, respectively) and conifers (50.48 %) could also be
explained by their corresponding differences in chemical compositions
(Lamlom and Savidge, 2003; Thomas and Martin, 2012).
Our results showed that C contents in roots and leaves decreased
significantly with increasing latitude (Fig. 3). This was inconsistent with
previous studies reporting that C content of global plant fine root showed
no latitudinal trend (Yuan et al., 2011) but was consistent with the
latitudinal trends of plant C contents of roots and leaves in China's
forests (Zhao et al., 2016). Generally, climatic factors (i.e., temperature
and precipitation) regulate elemental contents in plant organs by
influencing the associated plant metabolism and functioning (Reich and
Oleksyn, 2004; Reich, 2005; Zhang et al., 2012). In our study, climatic
factors explained independently less variation of plant C contents of four
organs (0.2–8.4 %, see Fig. 4) than other factors. The climatic
factors and life form together explained higher proportion of the variation
in C contents of roots and leaves (25.3 and 16.2 % in Fig. 4), while
both the independent effect of climatic factors and the interactive effect
of climate and life form on the C content of stem were lower (0.5 and
0.7 %, respectively) than those of other organs. This may be
one reason for the lack of significant latitudinal trend for C content in
stems.
Our data showed that the life form independently explained more variation of
plant C content of four organs (7.2–21.5 %, Fig. 4), which was
consistent with the results of Fyllas et al. (2009) and other studies about
plant nutrient stoichiometry at global scales (Han et al., 2011; Zhao et
al., 2016; Tian et al., 2017). Further, the interactive effects of climatic
factors with life forms were higher than the independent explanations of
climate (0.7–15.7 %, Fig. 4). These results conjointly revealed the
important role of plant life form in shaping plant C content, which implied
that the shift of species composition in regional vegetation along the
latitudinal gradients influenced by climate could partly explain the
biogeographic pattern of plant C content. Generally, the proportion of woody
plants tends to a decrease while that of herbs increases with increasing
latitude and decreasing MAT and MAP (Fig. S1 in the Supplement). Hence, the variation in life
forms grouping in different biomes further corroborates our results of the
biogeographic pattern of plant C content.
Conclusions
Plant C content varied with organs and life forms at global scales.
Specifically, plant C content in leaves was higher than that in roots.
Across life forms, woody plants exhibited higher C content than herbaceous
plants. Using the canonical values of 50 % may underestimate and
overestimate the C content in stems and leaves of conifers and in all organs
of other life forms, respectively. Thus, specific plant C contents given in
Table 1 provided an alternative to IPCC for their guidelines to update the
plant C fractions and could improve the accuracy of vegetation C stock
estimations. Furthermore, plant C content showed significant latitudinal
trends induced by climatic factors and life forms. This suggests that these
latitudinal trends and driving factors should be incorporated into the
research of plant ecological stoichiometry and biogeochemical modeling.
Data used in this study can be found in the Supplement.
The Supplement related to this article is available online at https://doi.org/10.5194/bg-15-693-2018-supplement.
The authors declare that they have no conflict of
interest.
Acknowledgements
This work was supported by the National Natural
Science Foundation of China (31330012, 31621091). We thank Peng Li, Chengjun Ji, and Zhiyao Tang for their helpful suggestions
for data collection and analysis. We thank Aaron Hogan, Anwar Eziz, Jianxiao
Zhu, Qiong Cai, and Ming Ouyang for a friendly review of the manuscript. We
also thank the TRY initiative on plant traits (http://www.try-db.org). The
TRY database is hosted at the Max Planck Institute for Biogeochemistry (Jena,
Germany) and supported by DIVERSITAS/Future Earth, the German Centre for
Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, and EU project
BACI (grant ID 640176).
Edited by: Akihiko Ito
Reviewed by: two anonymous referees
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