Ecology Letters, (2001) 4: 344±347
REPORT
1
Experimental con®rmation of ecosystem model
predictions comparing transient and equilibrium
plant responses to elevated atmospheric CO2
1
P.C.D. Newton, H. Clark,
G.R. Edwards1 and D.J. Ross2
1
Land and Environmental
Management Group,
AgResearch, Private Bag 11008,
Palmerston North, New Zealand.
E-mail:
[email protected]
2
Landcare Research, Private Bag
11052, Palmerston North,
New Zealand.
Present address: TH Huxley
School of Environment, Earth
Abstract
Ecosystem models predict that short-term responses to elevated atmospheric CO2 may
differ substantially from the ``real'' long-term responses expected at equilibrium.
Experimental validation of these model predictions is dif®cult as the data available are
from short-term studies that do not include biogeochemical feedbacks typical of longterm exposure. Using a reciprocal transplant design at a natural CO2 spring, we
generated combinations of atmospheric and soil conditions that represented both shortand long-term elevated CO2 conditions. Plant responses were signi®cantly different
between these treatments, con®rming model predictions that there is not a simple
relationship between transient and equilibrium responses to elevated CO2.
Keywords
CO2 spring, ecosystem models, elevated CO2, transient effects.
Sciences and Engineering,
Imperial College at Wye, Wye,
Ashford, Kent TN25 5AH, U.K.
Ecology Letters (2001) 4: 344±347
INTRODUCTION
Understanding the responses of plants and plant communities to elevated atmospheric CO2 remains an important
issue because of the potential consequences for ecosystem
processes of both natural and agricultural systems (see
references in Walker et al. 1999 and Reddy & Hodges 2000).
Ecosystem models demonstrate that plant/community
responses to elevated CO2 can be modi®ed by biogeochemical feedbacks that change over time (McMurtrie &
Comins 1996; Rastetter et al. 1997; Thornley & Cannell
1997, 2000; Cannell & Thornley 1998; Luo & Reynolds
1999; McMurtrie et al. 2000). As a consequence, short- and
long-term responses to CO2 may be very different, putting
into question the relevance of short-term experiments for
predicting the consequences of elevated CO2 (Luo &
Reynolds 1999; McMurtrie et al. 2000; Thornley & Cannell
2000). To date, ecosystem modelling has been the only tool
by which short- and long-term effects have been evaluated.
As with all modelling, it is important to test the validity of
the predictions by experimentation or observation; while
there are good data for testing the short-term predictions,
testing the long-term equilibrium solutions is problematic
(Thornley & Cannell 2000).
In this paper, we make an experimental comparison of
short-term (transient) and long-term (equilibrium) effects of
Ó2001 Blackwell Science Ltd/CNRS
elevated CO2 on plant growth; the results support model
predictions for grassland responses (Thornley & Cannell
2000). The comparison was achieved in a reciprocal
transplant experiment of soils found at different distances
from a natural CO2 spring. This experiment produced shortterm (transient) combinations of: (i) a soil previously in near
global ambient CO2 concentrations transferred to a high
CO2 concentration (the combination commonly used in
CO2 enrichment experiments); (ii) a soil previously under
elevated CO2 returned to an ambient CO2 atmosphere; and
(iii) ``control'' soils in long-term equilibrium with high and
ambient CO2 concentrations.
MATERIALS AND METHODS
Site
The CO2 spring is situated in the north of New Zealand
(latitude 35°39¢S) where the average rainfall is 1500 mm
and the mean annual temperature is 15.5 °C. The length
of time the spring has been active is uncertain, but
documentary evidence notes strong activity in 1981 (Petty
et al. 1987) and anecdotal evidence indicates activity over
many decades. The spring is cold and the gas emitted is
99.3% CO2 with a very low concentration of H2S (Ross
et al. 2000). The vegetation is a mixture of C3 (principally
Testing CO2 responses predicted by models 345
Holcus lanatus L.) and C4 (principally Pennisetum clandestinum
Hochst. Ex Chiov. and Paspalum dilatatum Poir.) species;
15 further species are variously present, including all the
species used in the experiment (Newton et al. 1996). The
areas selected for the experiment were on a silty clay
loam gley soil (Fluvaquent) (see Ross et al. 2000 for
further details) dominated by Pennisetum clandestinum.
Carbon dioxide concentration was measured at canopy
height (c. 20 cm above soil level) on ®ve occasions
between February 1995 and March 1998 using an infrared gas analyser (Ross et al. 2000). Two sites with
contrasting CO2 concentrations were selected for the
experiment; the mean concentration at the ambient (or
low) CO2 site was 372 p.p.m. (range, 346±409 p.p.m.) and
at the high CO2 site 574 p.p.m. (range, 483±724 p.p.m.).
The shorthand notation used subsequently is La and Ha
for low and high atmospheric CO2 sites, and Ls and Hs
for sites which had soils that developed under low and
high atmospheric CO2 conditions, respectively.
Design
Three plant species Ð Lotus uliginosus L. (legume), Paspalum
dilatatum (C4 grass) and Plantago lanceolata L. (C3 forb) Ð
were used in a full reciprocal transfer involving all
combinations of species, atmospheric CO2 concentration
(Ha, La) and soil origin (Hs, Ls). Plants were grown from
commercial seed lines in an unheated glasshouse in small
plastic pipes (internal diameter, 23 mm; length, 60 mm)
®lled with sterile peat-based seed (i.e. low nutrient) compost.
Vegetation was cleared from the high and low CO2 sites and
lengths of plastic pipe (internal diameter, 105 mm; length,
200 mm) were driven into the ground at each location. All
the pipes were lifted and then reinstalled at the appropriate
site and the plants transplanted into the centre of the large
pipes. The design was completely randomized with three
replications of each species per CO2 and soil treatment, i.e.
18 plants at each CO2 site.
Plants
At the end of the experiment, plants were divided into leaf,
stem and root material. Stem material included the stems of
Lotus uliginosus, the rhizomes of Paspalum dilatatum and the
basal leaf midribs of Plantago lanceolata.
Soils
Soil properties were measured at each site on three samples
each containing ®ve 2.5 cm diameter cores taken to a depth
of 20 cm at the start of the experiment. Soil moisture, pH
(in water), organic C, Olsen P, total N and microbial C
and N were measured according to Blakemore et al. (1987)
and Ross et al. (2000). CO2-C production and net N
mineralization were determined from a laboratory incubation at 25 °C in soil maintained at 60% of water-holding
capacity, with mineral N (NH+4 -N + NO)3 -N) in 2 MKCl
extracts being determined by auto-analyser procedures (Ross
et al. 2000).
Analysis
Soil properties at the high and low sites had nonhomogeneous variances and were compared using the
non-parametric Mann±Whitney U-test. Plant data were
analysed by analysis of variance (ANOVA) and heterogeneous
variances were managed by data transformation. For ANOVA,
each pot was considered as an experimental unit with the
factors being species, atmospheric CO2 concentration and
origin of the soil.
RESULTS
Organic C, total N concentrations, CO2-C and net mineralN production (14±56 days) were higher in soil from the
high than the low CO2 area; NO)3 -N was the predominant
form of mineral-N in both soils (Table 1).
There were signi®cant interactions between soil and
atmosphere in relation to plant mass and its allocation, but
no difference between the species responses (Fig. 1). Plants
growing in the elevated equilibrium combination HaHs had
greater total mass than any other treatment (Fig. 1a) and
also had the lowest allocation to leaves (Fig. 1b). The
transient treatment combination (HaLs) had a signi®cantly
lower allocation to stem (Fig. 1c) and a greater allocation to
root (Fig. 1d) than any other treatment. The second
transient treatment (LaHs) had the lowest allocation to root
(Fig. 1d).
DISCUSSION
The difference in properties between the high and low CO2
soils are consistent with those established from a comprehensive sampling of topsoil (0±5 cm) across this site (Ross
et al. 2000), which found positive relationships between
atmospheric CO2 concentration and organic C, total N and
rates of net N mineralization. Our soil differences are also
consistent with equilibrium predictions for grassland systems exposed to a doubling of CO2 (Thornley & Cannell
1997, 2000). The greater rates of C and N mineralization in
the high soil over the second period of incubation are
indicative of qualitative differences between the soils in
substrate and/or decomposer communities. Changes in soil
fauna and ¯ora with atmospheric CO2 have been identi®ed
in this soil, including positive relationships between CO2
and microbial biomass (Ross et al. 2000), mycorrhizal
Ó2001 Blackwell Science Ltd/CNRS
346 P.C.D. Newton et al.
Table 1 Properties (0±20 cm depth) of a gley soil from areas
exposed to either a low or high atmospheric CO2 concentration at
a naturally occurring CO2 spring
Property
Low CO2
soil (Ls)
High CO2
soil (Hs)
Moisture (g/kg)
pH
Organic C* (g/kg)
Total N* (g/kg)
``Olsen'' P (mg/kg)
Microbial C (mg/kg)
Microbial N (mg/kg)
CO2-C* (mg/kg/h; 7±14 days)
746 4.83
88
6.5
14
1890
323
0.76
708
4.76
97
7.2
16
1729
326
1.08
37
31
23
51
28
99
79
97
97
72
93
96
Mineral-N (mg/kg; 0 days)
D Mineral-N (mg/kg)
0±14 days
14±56 days*
% Mineral-N as NO)3 -N
0 days
14 days*
56 days*
*Variables are signi®cantly different between soils as identi®ed by a
Mann±Whitney U-test.
Equivalent to approximately 60% of water-holding capacity.
infection rates (Rillig et al. 2000) and the abundance of
bacterial-feeding nematodes (Yeates et al. 1999).
The response of plant growth to the treatments con®rms
model predictions of large differences between short- and
long-term responses to elevated atmospheric CO2 (McMurtrie & Comins 1996; Rastetter et al. 1997; Cannell &
Thornley 1998; Luo & Reynolds 1999; Thornley & Cannell
2000). The long-term (equilibrium) response to elevated
CO2 was positive (HaHs vs. LaLs). In contrast, the shortterm comparison (HaLs vs. LaLs) Ð typical of most CO2
enrichment studies Ð showed no effect (and even a slight
suppression) of plant growth at elevated atmospheric CO2.
Nil or negative effects of elevated CO2 are not frequently
reported, but they can occur across all functional groups
including legumes (Diaz et al. 1993; Ackerly & Bazzaz 1995;
StoÈcklin et al. 1997) and could occur due to sequestration of
N in the micro¯ora (Diaz et al. 1993; but see Hungate et al.
1996). Immobilization of N occurs in many elevated CO2
studies (50% of those summarized by Zak et al. 2000) and is
a key driver of the short-term responses suggested by
ecosystem models (McMurtrie et al. 2000). We have no
direct evidence for N sequestration in the transient HaLs
combination, but the increased allocation to roots in this
treatment is indicative of nutrient limitation (Brouwer 1962).
It is clear that transient treatments can lead to responses
that are not related in a simple way to the equilibrium
responses that we need to understand. Ecosystem models
show that transient effects can arise from a temporary
imbalance in energy and nutrient supply and such a
response is consistent with the data presented here;
however, many other possible factors (e.g. pathogens,
changes in population genetic structure) are not considered
by ecosystem models, but may modify the long-term
response of ecosystems to elevated CO2. Despite these
Figure 1 Mean values of three plant species
for total mass (a) and plant fractions (b,c,d)
after 147 days of exposure to combinations
of a high (Ha) and low (La) CO2 atmosphere and a soil developed under high (Hs)
or low (Ls) CO2 atmosphere at a natural
CO2 spring. Treatments were applied in a
complete reciprocal transplant design. There
were no interactions with species and in all
cases there was a signi®cant soil ´ atmosphere interaction. Different letters signify
means that differ by more than the LSD
calculated for the soil ´ atmosphere term
for P ˆ 0.05.
Ó2001 Blackwell Science Ltd/CNRS
Testing CO2 responses predicted by models 347
limitations, modelling is an essential tool for extrapolating
from our current data sets, and efforts such as this study
to validate model predictions are an important part of this
process.
ACKNOWLEDGEMENTS
We thank Fred Potter for statistical advice. Financial
support from the New Zealand Foundation for Research
Science and Technology (contract C10X0007) is gratefully
acknowledged. This work contributes at the core research
level to the Global Change and Terrestrial Ecosystems
(GCTE) Core Project of the International Geosphere
Biosphere Programme (IGBP).
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BIOSKETCH
Paul Newton is a pasture ecologist interested in the consequences of global change for grazed pasture systems. His main
area of research involves the understanding of how mechanisms determining species abundance are modi®ed by grazing
and elevated CO2.
Editor, F.I. Woodward
Manuscript received 12 January 2001
First decision made 19 February 2001
Manuscript accepted 5 April 2001
Ó2001 Blackwell Science Ltd/CNRS