Journal of
Plant Ecology
Volume 6, Number 4,
Pages 270–276
August 2013
doi:10.1093/jpe/rts042
Advance Access publication
7 December 2012
available online at
www.jpe.oxfordjournals.org
Foliar stoichiometry under different
mycorrhizal types in relation to
temperature and precipitation in
grassland
Zhaoyong Shi1,2,*, Xiaogai Hou1, Yinglong Chen3,4, Fayuan Wang1
and Yanfang Miao1
1
Agricultural College, Henan University of Science and Technology, Luoyang, Henan 471003, China
Laboratory for Earth Surface Processes, Ministry of Education, Peking University, Beijing 100871, China
3
College of Life Sciences, Hebei University, Baoding 071002, China
4
School of Earth and Environment, Faculty of Natural and Agricultural Sciences, The University of Western Australia,
Perth, Australia
*Correspondence address. Agricultural College, Henan University of Science and Technology, Luoyang, Henan
471003, China. Tel: +86-379-64282340; Fax: +86-379-64282340; E-mail: [email protected]
2
Abstract
Aims
Mycorrhizas play key roles in important ecosystem processes and
functions. Carbon (C), nitrogen (N) and phosphorus (P) concentrations and their ratios are very important foliar traits and their cycling
constrains most ecosystem processes. Thus, this study addresses the
influence of mycorrhizal strategies on these foliar nutrients and their
response to climate change.
Methods
A new database was established including mycorrhizal types and
leaf Cmass, Nmass, Pmass, C: N and N: P of each plant species based
on He et al. [(2008) Leaf nitrogen: Phosphorus stoichiometry across
Chinese grassland biomes. Oecologia 155:301–10]. The predominant type of mycorrhizal association of each plant species was
classified according to the published literature and our own observations. We analyzed leaf Cmass, Nmass, Pmass, C: N and N: P among
112 plant species in 316 samples of ascertained mycorrhizal type in
the major grassland biomes of China.
Important Findings
The results show highly significant variation among different mycorrhizal strategy types for foliar Cmass, Nmass and N: P. The highest
Introduction
Numerous studies have indicated that carbon (C), nitrogen
(N) and phosphorus (P) cycling constrain most ecosystem
processes (Aerts and Chapin 2000; Chapin 1980; Tilman
1982). These nutrient elements interact closely in terrestrial
foliar Cmass was observed in ectotrophic mycorrhiza (ECM) type
(469.8 mg g−1) followed by that in arbuscular mycorrhiza (AM)
type (443.884 mg g−1) and nonmycorrhizal (NM) type (434.0 mg
g−1). The foliar N concentration was significantly higher in NM
type (31.0 mg g−1). However, the AM type had the greater C:N
value (19) than the other types although less variation in Cmass
and N:P among abuscular types on AM strategy was observed.
Foliar traits showed significant variation in response to precipitation (mean growing season and annual precipitation (GSP and
MAP)) and temperature (mean growing season and annual temperatures (GST and MAT)) depending on different mycorrhizal
strategies and arbuscular types. When the responses of all folia
parameters to precipitation and temperature were compared, the
influence of GSP on leaf traits was greater than the influence of
GST.
Keywords: mycorrhizal strategy • arbuscular type • foliar
traits • precipitation • temperature
Received: 30 June 2012 Revised: 13 November 2012 Accepted: 13
November 2012
ecosystems, and thus, the dynamics of the cycling of individual elements cannot be examined in isolation (Chapin and
Shaver 1989; Chapin et al. 2002; Vitousek 1982). Ecological
stoichiometry provides new perspectives for studying ecosystem processes at different levels, from leaf physiology to
ecosystem productivity (Dodds et al. 2004; Hessen et al. 2004;
© The Author 2012. Published by Oxford University Press on behalf of the Institute of Botany, Chinese Academy of Sciences and the Botanical Society of China.
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Shi et al. | Foliar stoichiometry under different mycorrhizal types271
Sterner and Elser 2002). Recently, a particular focus of ecological stoichiometry is used to document large-scale patterns of, and the driving factors for, plant C:N:P stoichiometry
(Güsewell 2004; He et al. 2008; Kerkhoff et al. 2006; Moe et al.
2005; Reich and Oleksyn 2004).
There is a growing recognition that plant species and
plant functional types are important controllers of ecosystem
processes and functions (Chapin et al. 1997; Díaz and Cabido
1997; Grime et al. 1997; Hobbie 1992; Tilman et al. 1997;
Wardle et al. 1998), particularly those that link plants with the
soils in which they grow (Berendse 1994; Cornelissen 1999;
Van Breemen 1993; Wardle et al. 1997). There are also some
consensus that mycorrhizal symbioses between plants and
fungi play key roles in important ecosystem processes and
functions (Brundrett 1991; Fitter 1990; Grime et al. 1987; Read
1991; Rygiewicz and Andersen 1994; Smith and Read 2008;
van der Heijden et al. 1998a, 1998b; Wurst and Rillig 2011). We
would therefore expect that classifying plant species according
to their mycorrhizal association may provide a new dimension
to research on functional type classification and application
from which, with a few exceptions (Cornelissen et al. 2001;
Michelsen et al. 1996), mycorrhizas have so far been excluded.
Mycorrhizal strategies are based on the current understanding that different types of mycorrhizal symbiosis
(which also involve different fungal taxa) can promote plant
uptake from different nutrient sources, notably N versus P,
in inorganic versus organic forms (Chapin 1995; Read 1991;
Michelsen et al. 1998; Näsholm et al. 1998; Schulze et al.
1994). Many or most of the ectomycorrhizal fungal associations (Kielland 1994; Michelsen et al. 1996, 1998; Näsholm
et al. 1998; Northup et al. 1995; Read 1991) appear to contrast
with plant species with arbuscular mycorrhizal (AM) fungi,
which generally have no access to complex organic nutrient
sources. Instead, AM plants tend to take up inorganic P more
efficiently (Newsham et al. 1995; Smith and Read 2008; Smith
et al. 2003; van der Heijden 1998b). The role of different types
of mycorrhiza with respect to nutrient uptake and conservation may have important repercussions for the C gains and
losses of ecosystems, and thus, for the C budget at a regional
or global scale (Read 1991). Meantime, researches have suggested that foliar traits were affected by precipitation or temperature whether on area scale or on the global scale (He et al.
2006, 2008; Reich and Oleksyn 2004), the responses of foliar
characteristics to precipitation and temperature varied under
different mycorrhizal strategies on the Tibetan Plateau (Shi
et al. 2012).
Thus, mycorrhizal associations may be an important component of this feedback loop in ecosystem C, N and P and the
dynamics of their relationships with the changes of precipitation and temperature. However, the data to support a link
between mycorrhizal control over C, N, P and their relative
dynamics have been sparse, partly anecdotal and based on
a few species only. Therefore, we hypothesize that different
mycorrhizal strategies of plants affected the stoichiometry
of foliar C, N, P and their ratios and their responses to the
changes of precipitation and temperature. In order to verify
above hypothesis, leaf traits encompassing foliar C, N, P, C:N
and N:P ratios in grassland plants from a wide range of major
grassland types across China were investigated.
Materials and Methods
Data compilation
Data on leaf traits and site-specific precipitation and temperature for this study were drawn from the work reported by He
et al. (2008). The detailed information of the sampling sites
and their distribution can be found in He et al. (2006). The
predominant type of mycorrhizal association of each plant
species was classified according to the published literature
or our own observations (Harley and Harley 1987a, 1987b,
1990; Wang and Qiu 2006; Wang and Shi 2008).
The three mycorrhizal strategies AM, ectotrophic mycorrhiza
(ECM) and nonmycorrhizal (NM) of 112 plant species in 316
plant sampling sites belonging to 64 genera and 23 families were
ascertained and examined in this study (Table 1). Further, the
AM were divided into the three subgroups: Arum, intermediate
and Paris groups according to the type of arbuscules (Table 1).
At least two references from separate studies were involved for
ascertaining the arbuscular types of each plant species, which
are included in this study (Supplementary materials).
Data analysis
The data were subjected to one-way analysis of variance
using the SPSS software package version 11.0 (SPSS,
Chicago, IL). All leaf traits were normalized by logarithmic
transformation prior to statistical analysis. Group means
for the various leaf traits were compared by multiple comparison tests where more than two groups were compared
Table 1: numbers of plant species, samples (sites), genera, and families in each mycorrhizal and arbuscular type
Mycorrhizal strategy/arbuscular type
Plant species
Plant samples (sites)
Genera
Families
AM
88
262
53
18
ECM
6
20
2
1
NM
18
34
13
8
Arum
33
101
23
8
Intermediate
6
27
6
4
Paris
9
23
6
3
272
Journal of Plant Ecology
Figure 1: effects of mycorrhizal strategy on leaf traits. Mean data + SE are presented. For each trait bars with the same letter are not significantly different at the 5% level.
by least significant difference (LSD) at the 5 or 1% level.
Bivariate correlation analysis was applied to show the
correlation of leaf traits with mean growing season temperature (GST) and mean annual temperature (MAT) and
mean growing season precipitation (GSP) and mean annual
precipitation (MAP) or different mycorrhizal strategies or
arbuscular-type groups.
Results
Analysis of variance revealed that there were significant
differences among different mycorrhizal strategy types in
foliar Cmass, Nmass and N:P. No significant difference in Pmass
and N:P was observed with changing mycorrhizal strategy
(Fig.1). The average foliar Cmass values for all species across
Chinese grasslands were 443.8, 469.8 and 433.9 mg g−1 for
AM, ECM, and NM species, respectively (Fig. 1). The highest
N mass concentration was present in NM groups with 31.0 mg
g−1, which was markedly higher than in AM groups (25.8).
The mass ratio of C and N of NM species was significantly
lower than that of AM groups (Fig. 1).
Furthermore, the influence of arbuscular type of AM
groups on foliar traits was analyzed (Fig. 2). There were no
significant differences in leaf Nmass, Pmass or C:N among Arum,
intermediate and Paris types. Little variation was observed
in Cmass and N:P. The influence of mycorrhizal strategy on
the responses of leaf traits to precipitation and temperature
are shown in Tables 2–5. Both MAP and MAT significantly
affected the C concentration of AM species, but their influence was not notable on ECM or NM species (Table 2). N,
C:N and N:P showed significant correlations with MAP in AM
groups. Only P in ECM groups and N in NM groups were significantly influenced by MAP. Overall, N:P was significantly
correlated with MAT in Arum arbuscular species and in intermediate arbuscular species, P was related to MAP and MAT
and C:N was correlated with MAP (Table 3). In Paris arbuscular species, C, P and C:N were correlated with MAP and N was
associated with MAT.
The effects of GSP and GST on the different mycorrhizal
strategies and arbuscular-type groups are presented in Tables
4 and 5. Generally, the influence of GSP on leaf traits was
greater than the influence of GST.
Figure 2: effects of arbuscular type on leaf traits. Mean + SE are presented. For each trait bars with the same letter are not significantly different at the 5% level.
Shi et al. | Foliar stoichiometry under different mycorrhizal types273
Table 2: correlation between leaf traits and GSP and GST in different mycorrhizal strategy groups
Mycorrhizal
strategy
logC
logN
logP
logC:N
logN:P
GSP
GST
GSP
GST
GSP
GST
GSP
GST
GSP
AM
−0.178a
−0.171a
0.184a
−0.034
−0.022
−0.069
−0.211a
0.064
0.182a
GST
0.053
ECM
0.219
0.132
0.580a
−0.111
0.117
−0.066
0.584a
0.177
0.261
−0.009
NM
0.193
−0.109
0.407b
−0.344b
0.356b
−0.236
−0.343b
0.302
−0.025
−0.052
a) and b) denote significant correlation at the 1 and 5% levels, respectively.
Table 3: correlation between leaf traits and GSP and GST in different arbuscular species
logC
logN
logP
logC:N
logN:P
Arbuscular type
GSP
GST
GSP
GST
GSP
GST
GSP
GST
GSP
GST
Arum
−0.007
−0.240*
0.037
0.120
0.047
−0.119
−0.036
−0.149
−0.024
0.251*
Intermediate
−0.053
−0.185
0.386*
0.243
0.443*
0.377
−0.396*
−0.261
−0.027
−0.138
Paris
0.411
−0.253
0.627**
−0.194
0.498*
−0.335
−0.588**
0.169
0.180
0.122
* and ** denote significant correlation at the 5 and 1% levels, respectively.
Table 4: correlation between leaf traits and MAP and MAT in different mycorrhizal strategy groups
Mycorrhizal
strategy
AM
logC
logN
logP
logC:N
logN:P
MAP
MAT
MAP
MAT
MAP
MAT
MAP
MAT
MAP
MAT
−0.164**
0.137*
0.152*
−0.049
−0.019
−0.070
−0.177**
0.073
0.151*
0.041
ECM
0.178
0.262
0.155
−0.156
0.454*
0.037
−0.112
0.276
−0.334
−0.136
NM
0.182
−0.151
0.389*
−0.280
0.317
−0.271
−0.329
0.232
0.002
0.046
* and ** denote significant correlation at the 5 and 1% levels, respectively.
Table 5: correlation between leaf traits and MAP and MAT in different arbuscular types
logC
logN
logP
logC:N
logN:P
Arbuscular type
MAP
MAT
MAP
MAT
MAP
MAT
MAP
MAT
MAP
MAT
Arum
0.002
−0.143
0.012
0.148
0.061
−0.123
−0.012
−0.162
−0.063
0.281**
Inmediated
−0.136
−0.329
0.379
0.102
0.493**
0.390*
−0.396*
−0.130
−0.096
−0.344
Paris
0.424*
−0.502*
0.533**
−0.403
0.545**
−0.364
−0.492**
0.353
0.033
−0.072
* and ** denote significant correlation at the 5 and 1% levels, respectively.
Discussion
The functional importance of mycorrhizal strategy in ecosystems has trigged widespread interest (Vargas et al. 2010; Zhu
and Miller 2003). It is well known that mycorrhizas influence
nutrient cycling. Furthermore, previous studies have shown
that mycorrhizal strategy influenced foliar traits such as foliar
N and P (Cornelissen et al. 2001) and foliar δ15N (Craine et al.
2009; He et al. 2009) at ecosystem or biome level.
Our study on the influence of mycorrhizal strategy on leaf
traits and their responses to precipitation and temperature
is the first to involve the arbuscular type of mycorrhiza. The
foliar C concentrations of AM and ECM mycorrhizal species
were higher than those of NM species, and this may be
related to absorption of carbohydrates by mycorrhizal associations (Smith and Read 2008). As a consequence, photosynthesis by mycorrhizal species (Shi et al. 2011) and their
growth rates (Cornelissen et al. 2001) may be enhanced.
Cornelissen et al. (2001) investigated the leaf traits of 83
British plant species according to mycorrhizal type and they
found no significant difference between ECM species and
AM species in foliar N and P concentrations. Our results support their conclusions (Fig. 1). Two possible explanations for
the higher C: N of AM species than NM species are that AM
have relatively poor N uptake and that AM increase plant
assimilation of C.
274
The factors leading to differences in C concentration and
N:P ratio among different arbuscular types requires future
research because no studies have distinguished between
the functions of the three arbuscular types (Smith and Read
2008) although there have been numerous attempted studies
(Cavagnaro et al. 2003; Dickson et al. 2003; Dickson 2004; van
Aarle et al. 2005).
The influence of precipitation and temperature on leaf
traits has been investigated in previous studies (He et al.
2006a, 2006b; He et al. 2008). To our knowledge, this is the
first study to compare the effects of precipitation or temperature on foliar traits based on arbuscular type. He et al.
(2006a) showed that the effect of MAT was significant for
leaf traits; the effect of MAP was not significant for any of
the leaf functional traits if the role of mycorrhiza was not
taken into consideration. In this study, the influence of MAT
or GST and MAP or GSP on foliar traits was in accordance
with those of He et al. (2006b, 2008). The influence of mycorrhiza on plant response to precipitation (MAP and GSP) and
temperature (MAT and GSP) was different among the three
arbuscular types, which may relate to the species of plants
and mycorrhizal fungi involved. The detailed mechanisms
require further elucidation because the functional differences among the three arbuscular types are unclear (Smith
and Read 2008).
The different responses of foliar traits to precipitation and
temperature based on different mycorrhizal strategies have
important implications for understanding plant responses
to global climate change and the ecology of mycorrhizas.
The plant community or ecosystem may respond differently
to climate change depending on the role of mycorrhizal
associations. Vargas et al. (2010) indicated that ecosystem
CO2 fluxes of arbuscular- and ECM-dominated vegetation
types are differentially influenced by precipitation and
temperature. Moreover, in terrestrial ecosystems, symbiotic
associations between plant roots and mycorrhizal fungi are
nearly ubiquitous, with 90% of all plant species forming
mycorrhizas (Smith and Read 2008). Their prevalence has led
to the assertion that ‘the majority of plants, strictly speaking,
do not have roots; they have mycorrhizas’ (http://www.ibeg.eu/englishhomepage.htm). The potentially symbiotic
association is well known to function as an exchange of
plant carbohydrate for fungal P and mycorrhizal colonization
has also been shown to increase plant N acquisition (PerezMoreno and Read 2001) and enhance host plant resistance
to drought and pathogens (Smith and Read 2008). Clearly,
considerable research effort is required in the future to allow
fully quantitative investigation of the function of mycorrhizal
associations on a global ecosystem scale.
Conclusion
Our study showed that there was highly significant variation among different mycorrhizal strategy types for foliar
Cmass, Nmass and N: P. No significant differences in Pmass or
Journal of Plant Ecology
N:P ratio were observed with changing mycorrhizal strategy. The variation of leaf Nmass, Pmass or C:N was not significant with the changes of arbuscular types in AMs. The
responses of foliar traits to precipitation and temperature
were varied depending on different mycorrhizal strategies
and arbuscular types.
Supplementary material
Supplementary material is available at Journal of Plant Ecology
online.
Funding
National Natural Science Foundation of China (grant
40971150); the Chinese Postdoctoral Science Foundation
(20090450004, 20103018); the open fund of Laboratory for
Earth Surface Processes, Ministry of Education (2011004);
the Science Foundation Fostering Innovative Ability of Henan
University of Science and Technology (2009CZ0006).
Acknowledgment
The authors thank Dr Peter Christies of Queen’s University Belfast for
his comments on this article.
References
Aerts R, Chapin FS III (2000) The mineral nutrition of wild plants revisited: A re-evaluation of processes and patterns. Adv Ecol Res 30:1–67.
Berendse F (1994) Litter decomposability—a neglected component of
plant fitness. J Ecol 82:87–190.
Brundrett M (1991) Mycorrhizas in natural ecosystems. Adv Ecol Res
21:171–313.
Cavagnaro TR, Smith FA, Ayling SM, Smith SE (2003) Growth and
phosphorus nutrition of a Paris-type arbuscular mycorrhizal symbiosis. New Phytol 157:127–34.
Chapin FS III (1980) The mineral nutrition of wild plants. Ann Rev
Ecol Syst 11:233–60.
Chapin FS III (1995) New cog in the nitrogen cycle. Nature 377:199–200.
Chapin FS III, Shaver GR (1989) Differences in growth and nutrient
use among arctic plant growth forms. Funct Ecol 3:73–80.
Chapin FS III, Matson PA, Mooney H (2002) Principles of Terrestrial
Ecosystem Ecology. New York: Springer.
Chapin FS III, Walker BH, Hobbs RJ, et al. (1997) Biotic control over
the functioning of ecosystems. Science 277:500–04.
Cornelissen JHC (1999) A triangular relationship between leaf size
and seed size among woody species: Allometry, ontogeny, ecology
and taxonomy. Oecologia 118:248–55.
Cornelissen JHC, Aerts R, Cerabolini B, et al. (2001) Carbon cycling
traits of plant species are linked with mycorrhizal strategy. Oecologia
129:611–9.
Craine JM, Elmore AJ, Aidar MP, et al. (2009) Global patterns of foliar
nitrogen isotopes and their relationships with climate, mycorrhizal
fungi, foliar nutrient concentrations, and nitrogen availability. New
Phytol 183:980–92.
Shi et al. | Foliar stoichiometry under different mycorrhizal types275
Díaz S, Cabido M (1997) Plant functional types and ecosystem function in relation to global change. J Vegetat Sci 8:463–74.
Näsholm T, Ekblad A, Nordin A, et al. (1998) Boreal forest plants take
up organic nitrogen. Nature 392:914–6.
Dickson S (2004) The Arum-Paris continuum of mycorrhizal symbioses. New Phytol 161:187–200.
Newsham KK, Fitter AH, Watkinson AR (1995) Multi-functionality
and biodiversity in arbuscular mycorrhizas. Trends Ecol Evol (Amst)
10:407–11.
Dickson S, Schweiger PF, Smith FA, et al. (2003) Paired arbuscules in
the Arum-type arbuscular mycorrhizal symbiosis with Linum usitatissimum L. Canada J Bot 81:457–63.
Northup RR, Yu Z, Dahlgren RA, Vogt KA (1995) Polyphenol control
of nitrogen release from pine litter. Nature 377:227–9.
Dodds WK, Marti E, Tank JL, et al. (2004) Carbon and nitrogen
stoichiometry and nitrogen cycling rates in streams. Oecologia
140:458–67.
Perez-Moreno J, Read DJ (2001) Nutrient transfer from soil nematodes to plants: a direct pathway provided by the mycorrhizal
mycelial network. Plant Cell Environ 24:1219–26.
Fitter AH (1990) The role and ecological significance of vesiculararbuscular mycorrhizas in temperate ecosystems. Agric Ecosyst
Environ 29:257–65.
Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47: 376–91.
Grime JP, Mackey JML, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature
328:420–2.
Grime JP, Thompson K, Hunt R, et al. (1997) Integrated screening
validates primary axes of specialization in plants. Oikos 79:259–81.
Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–66.
Harley JL, Harley EL (1987a) A check-list of mycorrhiza in the British
flora. New Phytol 105:1–102.
Harley JL, Harley EL (1987b) A check-list of mycorrhiza in the British
flora—addenda, errata and index. New Phytol 107:741–9.
Harley JL, Harley EL (1990) A check-list of mycorrhiza in the British
flora—second addenda and errata. New Phytol 115:699–711.
He JS, Fang J, Wang Z, et al. (2006a) Stoichiometry and large-scale
patterns of leaf carbon and nitrogen in the grassland biomes of
China. Oecologia 149:115–22.
He JS, Wang L, Flynn DF, et al. (2008) Leaf nitrogen: Phosphorus stoichiometry across Chinese grassland biomes. Oecologia 155:301–10.
He JS, Wang Z, Wang X, et al. (2006b) A test of the generality of leaf
trait relationships on the Tibetan Plateau. New Phytol 170:835–48.
He XH, Xu MG, Qiu GY, Zhou JB (2009) Use of 15N stable isotope
to quantify nitrogen transfer between mycorrhizal plants. J Plant
Ecol 2:107–18.
Hessen DO, Agren GI, Anderson TR, et al. (2004) Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85:1179–92.
Hobbie SE (1992) Effects of plant species on nutrient cycling. Trends
Ecol Evol 7:336–9.
Kerkhoff AJ, Fagan WF, Elser JJ, et al. (2006) Phylogenetic and
growth form variation in the scaling of nitrogen and phosphorus
in the seed plants. Am Nat 168:E103–22.
Kielland K (1994) Amino acid absorption by arctic plants: Implications
for plant nutrition and nitrogen cycling. Ecology 75:2373–83.
Michelsen A, Quarmby C, Sleep D, Jonasson S (1998) Vascular plant
15N natural abundance in heath and forest tundra ecosystems is
closely correlated with presence and type of mycorrhizal fungi in
roots. Oecologia 115:406–18.
Michelsen A, Schmidt IK, Jonasson S, et al. (1996) Leaf 15N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non- and arbuscular mycorrhizal species access
different sources of soil nitrogen. Oecologia 105:53–63.
Moe SJ, Stelzer RS, Forman MR, et al. (2005) Recent advances in
ecological stoichiometry: insights for population and community
ecology. Oikos 109:29–39.
Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P
in relation to temperature and latitude. Proc Natl Acad Sci USA
101:11001–6.
Rygiewicz PT, Andersen CP (1994) Mycorrhizae alter quality and
quantity of carbon allocated below ground. Nature 369:58–60.
Schulze ED, Kelliher FM, Korner C, et al. (1994) Relationships among
maximum stomatal conductance, ecosystem surface conductance,
carbon assimilation rate and plant nitrogen nutrition: a global ecology scaling exercise. Ann Rev Ecol Syst 25:629–60.
Shi ZY, Wang FY, Zhang C, Yang ZB (2011) Exploitation of phosphorus patches with different phosphorus enrichment by three arbuscular mycorrhizal fungi. J Plant Nutrit 34:1096–106.
Shi ZY, Liu YY, Wang FY, Chen YL (2012) Influence of mycorrhizal
strategy on the foliar traits of the plants on the Tibetan Plateau
in response to precipitation and temperature. Turkish J Bot
36:392–400.
Smith SE, Read DJ (2008) Mycorrhizal Symbiosis (3rd edn). London:
Elsevier Ltd.
Smith SE, Smith FA, Jakobsen I. (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses.
Plant Physiol 133:16–20.
Sterner RW, Elser JJ (2002) Ecological Stoichiometry: the Biology of Elements
from Molecules to the Biosphere. Princeton: Princeton University Press.
Tilman D (1982) Resource Competition and Community Structure.
Princeton: Princeton University Press.
Tilman D, Knops J, Wedin JD, et al. (1997) The influence of functional diversity and composition on ecosystem processes. Science
277:494–9.
van Aarle IM, Cavagnaro TR, Smith SE, et al. (2005) Metabolic activity of Glomus intraradices in Arum- and Paris-type arbuscular mycorrhizal colonization. New Phytol 166:611–8.
van Breemen N (1993) Soils as biotic constructs favouring net primary productivity. Geoderma 57:183–211.
van der Heijden MG, Klironomos JN, Ursic M, et al. (1998b)
Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72.
van der Heijden MGA, Boller T, Wiemken TA, Sanders IR (1998a)
Different arbuscular mycorrhizal fungal species are potential determinants of plant community structure. Ecology 79:2082–91.
Vargas R, Baldocchi DD, Querejeta JI, et al. (2010) Ecosystem CO2
fluxes of arbuscular and ectomycorrhizal dominated vegetation
types are differentially influenced by precipitation and temperature. New Phytol 185:226–36.
Vitousek PM (1982) Nutrient cycling and nutrient use efficiency. Am
Naturalist 119:553–72.
276
Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of
mycorrhizas in land plants. Mycorrhiza 16:299–363.
Wang FY, Shi ZY (2008) Biodiversity of arbuscular mycorrhizal fungi
in China: a review. Adv Environ Biol 2:31–9.
Wardle DA, Barker GM, Bonner KI, Nicholson KS (1998) Can comparative approaches based on plant ecophysiological traits predict
the nature of biotic interactions and individual plant species effects
in ecosystems? J Ecol 86:405–20.
Journal of Plant Ecology
Wardle DA, Bonner KI, Nicholson KS (1997) Biodiversity and plant litter:
experimental evidence which does not support the view that enhanced
species richness improves ecosystem function. Oikos 79: 247–58.
Wurst S, Rillig MC (2011) Additive effects of functionally dissimilar
above- and belowground organisms on a grassland plant community. J Plant Ecol 4:221–7.
Zhu YG, Miller RM (2003) Carbon cycling by arbuscular mycorrhizal
fungi in soil-plant systems. Trends Plant Sci 8:407–9.