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CSIRO PUBLISHING
AUSTRALIANJOURNALOF
PLANTPHYSIOLOGY
Volume 27,2000
©CSIRO 2000
An international journal of plant function
www.publish.csiro.au/journals/ajpp
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Australian Journal of Plant Physiology
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the Australian Academy of Science
Introduction
Since the start of the Industrial Revolution, atmospheric
[CO2] has risen from ~280 µmol mol–1 to ~370 µmol mol–1
(Houghton et al. 1996). This rise in atmospheric [CO2] has
not been linear. Approximately two-thirds of the observed
increase in [CO2] has occurred since the 1950s (Keeling and
Whorf 1994). Although the projected rate of future atmos-
pheric [CO2] increase varies by model, it is generally
acknowledged that atmospheric [CO2] should reach
600 µmol mol–1 sometime during the 21st century (Houghton
et al. 1996).
Because CO2supplies the carbon for all terrestrial
biology, research efforts have focused on determining the
impact of rising atmospheric [CO2] on the growth and repro-
duction of native species and crops (e.g. Kimball et al. 1993;
Poorter 1993; Curtis and Wang 1998). Reproduction is an
especially important parameter since it affects both ecologi-
cal fitness for native species, and economic production for
crops.
The impact of [CO2] on allocation of resources to flower-
ing and changes in reproductive phenology appears to be
highly species-specific (Ackerly and Bazzaz 1995).
Enhanced [CO2] has resulted in earlier flowering (Lawlor
and Mitchell 1991) and increased flower and fruit number
for a number of agronomic plants (Deng and Woodward
1998). In contrast, flowering of some native species has been
unaffected or delayed with increased [CO2] (Garbutt and
Bazzaz 1984; Reekie et al. 1997), but this is by no means a
universal response (e.g. Datura stramonium, Garbutt and
Bazzaz 1984).
While specific attention has been given to aspects of
reproductive biology which could influence seed develop-
ment and yield, almost nothing is known concerning the
impact of [CO2] on pollen production per se. Aside from the
obvious consequences for fertilization, fecundity and eco-
logical fitness, [CO2]-induced changes in pollen production
could have a direct impact on atmospheric pollen concen-
tration, with subsequent effects on human allergic disease
and public health. For example, in a recent survey among the
general population in the US, approximately 70% of respon-
dents indicated pollen as the principal agent producing
symptoms of allergies, with ragweed pollen cited as the indi-
vidual plant species eliciting the greatest response (Meggs
et al. 1996). In addition to ragweed, other weedy species (e.g.
lambsquarters, Chenopodium album L.) and pigweed
(Amaranthus retroflexus L.) as well as native trees
Aust. J. Plant Physiol., 2000, 27, 893–898
10.1071/PP00032 0310-7841/00/100893
Abbreviations used: A, rate of CO2assimilation; Ca, ambient CO2concentration; Ci, internal CO2concentration; DAS, days after sowing;
PPFD, photosynthetic photon flux density; RGR, relative growth rate.
© CSIRO 2000
Rising CO2and pollen production of common ragweed
(Ambrosia artemisiifolia), a known allergy-inducing species:
implications for public health
Lewis H. ZiskaAand Frances A. Caulfield
Climate Stress Laboratory, Bldg 046A, USDA-ARS, Beltsville Agricultural Research Center,
10300 Baltimore Avenue, Beltsville MD 20705, USA.
ACorresponding author: email; ziskal@ba.ars.usda.gov
Abstract. Although environmental factors such as precipitation and temperature are recognized as influencing
pollen production, the impact of rising atmospheric carbon dioxide concentration ([CO2]) on the potential growth
and pollen production of hay-fever-inducing plants is unknown. Here we present measurements of growth and pollen
production of common ragweed (Ambrosia artemisiifolia L.) from pre-industrial [CO2] (280 µmol mol–1) to current
concentrations (370 µmol mol–1) to a projected 21st century concentration (600 µmol mol–1). We found that expo-
sure to current and elevated [CO2] increased ragweed pollen production by 131 and 320%, respectively, compared
to plants grown at pre-industrial [CO2]. The observed stimulations of pollen production from the pre-industrial [CO2]
were due to an increase in the number (at 370 µmol mol–1) and number and size (at 600 µmol mol–1) of floral spikes.
Overall, floral weight as a percentage of total plant weight decreased (from 21% to 13%), while investment in pollen
increased (from 3.6 to 6%) between 280 and 600 µmol mol–1 CO2. Our results suggest that the continuing increase
in atmospheric [CO2] could directly influence public health by stimulating the growth and pollen production of
allergy-inducing species such as ragweed.
Keywords: allergens, elevated carbon dioxide, photosynthesis, pollen, relative growth rate.
L. H. Ziska and F. A. Caulfield894
(e.g. Quercus and Acer spp.) and grasses (e.g. Setaria) are
recognized as influencing seasonal allergies through pollen
production (Gergen and Turkeltaub 1992; Emberlin 1994).
In the current experiment, our principal objective was to
test whether the increase in atmospheric [CO2] since the
Industrial Revolution, and projected future increases in
[CO2], may alter growth and pollen production of known
hay-fever-inducing plants using common ragweed
(Ambrosia artemisiifolia L.) as a model species. Pollen pro-
duction of ragweed is generally acknowledged to be a major
source of air-borne allergens and a public health concern in
North America. In general, ragweed production peaks
between late August and November in North America, and is
the principal pollen associated with fall allergies in the US
(Frenz et al. 1995; Meggs et al. 1996). CO2-induced changes
in the life cycle and pollen-producing capacity of aero-aller-
gen plants such as ragweed could have significant implica-
tions for public health.
Materials and methods
Experiments were conducted using a controlled environment chamber
located at the Climate Stress Laboratory, USDA-ARS, Beltsville, MD,
USA. An environmental chamber was used rather than field chambers
or Free-Air CO2Exchange (FACE), in order to maintain constant pre-
industrial [CO2] at a given temperature and consistent light and humid-
ity for 24-h periods.
[CO2] was controlled by flushing the chamber with CO2-free air
using a Ballston 75-60 type CO2scrubber (Ballston Filter Products,
Lexington, MA, USA), then re-injecting CO2to the desired [CO2].
Injection of CO2was controlled by an infrared gas analyser (WMA-2,
PP systems, Haverhill, MA, USA) in absolute mode that sampled
chamber air continuously. The set points for [CO2] control were 280
(pre-industrial), 370 (current) and 600 (future) µmol mol–1 CO2. Actual
CO2concentrations determined at 10-min intervals over 24 h for each
[CO2] treatment were 281.5 ± 23.4, 374 ± 14.1 and 603 ± 12.9 µmol
mol–1, respectively. In all chambers, plants received 14 h of
1.0 mmol m–2 s–1 photosynthetic photon flux density (PPFD) from a
mixture of high-pressure sodium and metal halide lamps for the first
35 days after sowing (DAS). After 35 DAS, PPFD was altered to 12 h
of 1.0 mmol m–2 s–1 PPFD to induce flowering. Day/night temperature
was 28/22°C and average daily humidity exceeded 60%. Temperature,
[CO2] and relative humidity were monitored and recorded at 1-min
intervals by an EGC network data logger (EGC Corp., Chagrin Falls,
OH, USA) in conjunction with a PC.
Seeds of common ragweed (Ambrosia artemisiifolia L.) were broad-
cast in pots of different sizes ranging from 10 to 30 cm in diameter
(1.8–21.2 L in volume). Smaller pots were elevated so that the height of
the plants was uniform. Seed was obtained from the Valley Seed
Company (Fresno, CA, USA). Plants in all pots were thinned to one
plant per pot within 48 h after emergence. Pots were filled with vermi-
culite and watered daily to dripping point with a complete nutrient solu-
tion containing 13.5 mMnitrogen (Robinson 1984). For each
experiment, 32 pots were assigned to a given [CO2], with pots arranged
to avoid mutual shading.
To determine potential changes in photosynthesis as a function of
the growth [CO2], single leaf photosynthesis (A, the rate of CO2assimi-
lation) was determined as a function of short-term changes in internal
[CO2] (Ci) twice during the vegetative growth at each [CO2] treatment.
Assimilation was determined on the uppermost, fully expanded leaf for
four plants of each [CO2] between 30 and 40 DAS using a differential
infrared CO2analyser (model 6252, Li-Cor Corp., Lincoln, NE, USA)
in an open configuration attached to two single-leaf cuvettes.
Temperature, humidity and [CO2] were set to approximate values main-
tained in the growth chamber. The gas stream was humidified by
bubbling through a temperature-controlled water bath to obtain a given
dew point, and humidity was monitored with a dew point hygrometer
(Hygro M-1, General Eastern Corp., Cambridge, MA, USA). Mass
flow controllers were used to mix dry CO2-free air with 100% CO2to
obtain a desired [CO2] within a cuvette. Supplemental lighting was sup-
plied by a 150-W cool-beam floodlight (GE Corp., Cleveland, OH,
USA) attached to a variable transformer to obtain a desired PPFD.
Photosynthesis was determined initially as the CO2assimilation rate
at the growth [CO2] (Ca) at the growth PPFD (1.0 mmol m–2 s–1), then
re-measured at saturating light intensity (1.6 mmol m–2 s–1). Cawas then
reduced to 90 µmol mol–1 and increased in steps to 180, 360, 720, 1080
and 1450 µmol mol–1. Sufficient time (usually 20–30 min) was given
after Cawas changed, to allow equilibration. At the end of the measure-
ment, leaf laminae contained within a cuvette were cut, and leaf area
determined with a leaf area meter (Li-Cor Corp.).
For each [CO2] treatment, six plants were harvested at 21, 25, 29 and
35 DAS and again at seed maturity. Seed maturity was defined as occur-
ring when seed set exceeded 90%. At each harvest, all plants for a given
[CO2] treatment were cut at ground level and separated into leaf
laminae, stems (including petioles) and roots. Smaller-volume pots
were harvested first to avoid root-binding effects. Total leaf area was
determined photometrically as described previously. Dry weights were
obtained separately for leaves, stems and roots. Material was dried at
65°C for a minimum of 72 h or until dry weight was constant, and then
weighed. For the maturity harvest, leaf area was estimated based on the
regression analysis between leaf area and weight obtained from previ-
ous harvests (R2= 0.99).
Before pollination, 10 terminal staminate floral spikes (catkins)
were selected on each of five plants from each [CO2] treatment, and
labeled. A 5 ×25 cm polyethylene bag was placed over each spike to
collect pollen. Each bag had a 2.5-cm slit cut approximately 2 cm from
the bottom of the bag, into which the floral spike was placed with the
peduncle of the raceme located at the bottom of the slit. After placement
of the bag, the slit was taped so the floral spike was inside the bag with
at least 5 cm of space from the top of the open bag. Tops of bags were
left open for air circulation and ventilation. Floral heads were tapped
gently each day, and pollen was allowed to fall to the bottom of the bag.
After flowers were dehiscent and heads had completed pollen produc-
tion, each bagged floral spike was cut immediately below the first
flower and the floral structure was removed from the bag after tapping
any residual pollen. Each spike was measured for length along with
fresh and dry weights. Total pollen for a given spike was calculated by
subtracting the initial bag weight from the bag and pollen weight. At
maturity, for each plant from each [CO2] treatment, the total number of
floral spikes was recorded, spikes were harvested and the dry weight
(without pollen) recorded. The ratio of pollen collected to dry weight of
the floral structure resulted in a consistent ratio that was used to esti-
mate pollen production per plant.
Because of potential differences in microclimate between chambers,
the same growth chamber was used for all three CO2levels.
Adjustments to PPFD, humidity and temperature control were made
prior to the start of each [CO2] treatment to maintain consistency in
microclimate. In addition, the entire experiment (i.e. all three [CO2]
treatments) was repeated. A two-way ANOVA (SuperANOVA, Abacus
Concepts, Berkeley, CA, USA) was used to test for differences between
the two runs and between treatments. Because no significant run effect
was detected, treatment effects were compared with a one-way analysis
of variance on the combined data. Final biomass for a given [CO2] treat-
ment differed by <10% between runs. Three separate post-hoc tests
(Student–Newman–Keuls, Duncan New Multiple Range and Fisher’s
895
protected LSD) determined differences at the 0.05 significance level as
a function of [CO2] treatment.
Results
Pollen production increased significantly with rising [CO2].
The observed increase was 132% from pre-industrial to
current CO2levels, and ~90% from current to future CO2
levels of 600 µmol mol–1 (Fig. 1). Sensitivity of pollen pro-
duction to increasing [CO2] was greater from pre-industrial
to current CO2levels (0.7 g of pollen per 10 µmol mol–1
increase in [CO2]), diminishing as CO2increased to
600 µmol mol–1 (0.4 g of pollen per 10 µmol mol–1 increase
in [CO2]). Floral spike number did not change from pre-
industrial to current [CO2], but pollen production per
spikelet increased significantly (Fig. 1). From 370 to
600 µmol mol–1 CO2, no further change in pollen production
per spikelet was noted, but the number of floral spikes
approximately doubled (Fig. 1). Analysis of the diameter of
200 individual pollen grains for each [CO2] using a SEM
(15 kV, ×1.5k) indicated no change in average pollen size
(data not shown).
Small (non-significant) changes in total biomass (i.e.
roots, stems and leaves) were observed by 21 DAS, and sig-
nificant differences were observed by 29 DAS (Fig. 2).
Significant differences in relative growth rate (RGR) also
occurred by 29 DAS among [CO2] treatments (0.174, 0.209
and 0.220 g g–1 day–1 for the 280, 370 and 600 µmol mol–1
[CO2] treatments, respectively).
At seed maturity, total plant biomass was directly propor-
tional to [CO2]. From pre-industrial to current atmospheric
[CO2], leaf weight and stem weight increased by 36 and 49%,
respectively, with no significant change in root or floral
weight (Table 1). Leaf area, however, almost doubled in size
for this same increase in [CO2] (Table 1). At 600 µmol mol–1,
significant increases in all growth parameters at maturity
were observed relative to the 370 and 280 µmol mol–1 treat-
ments. The largest relative increase was observed for root
weight which increased ~ 4-fold from 280 to 600 µmol mol–1
[CO2]. No significant changes in stem to root ratio or
specific leaf area occurred among [CO2] treatments (data not
shown).
Leaf photosynthesis, measured at the growth [CO2],
increased significantly with [CO2], rising 170 and 250%
from pre-industrial to current and future [CO2], respectively,
and 30% from current to future [CO2] (Table 2). Values of
assimilation at a measurement [CO2] of 280 µmol mol–1 did
not differ among [CO2] treatments. However, at higher mea-
surement CO2levels, leaves grown at 280 µmol mol–1 [CO2]
had significantly lower photosynthetic rates — an indication
of down-regulation (Table 2). Acclimation was not observed
between the 370 and 600 µmol mol–1 [CO2] treatments.
Analysis of the response of assimilation to internal CO2indi-
cated no significant change in the initial slope of the
response curve as a function of [CO2] treatment. However,
the internal CO2concentration where leaf assimilation is
equal to zero (Γ*, the CO2compensation point), and the
maximum observed assimilation rate was lower for the 280
than the 370 and 600 µmol mol–1 treatments (data not
shown).
Discussion
For many years, both botanists and health workers have been
interested in those climatic and/or meteorological factors
that influence atmospheric pollen concentration (e.g.
Gregory 1973; Buck and Levetin 1982). Abiotic factors that
influence pollen productivity such as rainfall, temperature
and light also determine pollen amounts and severity of
Rising CO2and pollen production of common ragweed
Pollen production (g plant–1)
0
5
10
15
20
25 280 µmol mol–1
370 µmol mol–1
7
600 µmol mol–1
Pollen spike–1 (mg)
0
10
20
30
40
Floral spikes (plant–1)
0
200
400
600
800
1000
b
a
a
a
a
c
b
bb
1890 2000 2050?
Fig. 1. Pollen production, pollen per floral spike and number of floral
spikes in common ragweed grown at pre-industrial CO2concentrations
(280 µmol mol–1), current concentrations (370 µmol mol–1) and a pro-
jected 21st century concentration (600 µmol mol–1). Bars are ± s.e.
Student–Newman–Keuls was used to determine differences among the
[CO2] treatments at the 0.05 significance level (a, b or c).
L. H. Ziska and F. A. Caulfield896
allergies among susceptible populations during a given
allergy season. Consequently, there has been a great deal of
interest in modeling changes in pollen type and abundance
associated with global climate change (Emberlin 1994).
However, less is known concerning the direct stimulation of
growth and pollen production of allergy-inducing species by
rising [CO2], one of the principal ‘greenhouse’ gases.
The observed stimulation in growth and photosynthesis
observed here for ragweed is consistent with results seen
elsewhere for C3species grown with enhanced [CO2]
(Kimball et al. 1993). Increasing the [CO2] to 600 µmol mol–1
increased ragweed RGR within 4 weeks following emer-
gence, and stimulated biomass at maturity almost 3-fold
above pre-industrial [CO2] values. Final vegetative biomass
values obtained in the current experiment at ambient [CO2]
are consistent with those observed for single ragweed plants
in abandoned agricultural fields at maturity (D. Patterson,
pers. comm.). In the current study, both leaf area and weight
were particularly sensitive to [CO2]. The continued stimula-
tion of single-leaf photosynthesis (at least through anthesis)
and the observed increase in leaf area have obvious implica-
tions for maintaining a continued stimulation of photo-
synthesis and growth at the whole plant level with future CO2
levels.
If growth of ragweed is indeed stimulated by increasing
[CO2], how does this alter subsequent reproductive effort?
Floral spikes of ragweed contain both staminate and pistil-
late flowers. Pollen is wind-directed from numerous stami-
nate flowers to pistillate heads, which are fewer in number
and occur at the base of the floral spike (Bianchi et al. 1959).
Because wind is the primary means of transport, large
amounts of pollen are necessary to achieve seed set.
Increasing vegetative growth provides both a structural plat-
form for floral production and the carbon assimilate needed
to produce flowers. In the current experiment, floral weight
increased 70%, but floral weight as a percentage of total
plant weight decreased (from 21% to 13%) from 280 to
600 µmol mol–1 CO2. However, investment in pollen
increased (from 3.6 to 6%) from 280 to 600 µmol mol–1 CO2.
Because of the role of ragweed pollen in inducing aller-
gies, the reproductive response of ragweed to rising atmos-
pheric [CO2] is of obvious interest. In the current study, the
response of ragweed pollen production to rising [CO2] was
2-fold. Increasing [CO2] from pre-industrial to current levels
increased the amount of pollen produced by an individual
floral spike. As [CO2] increased further to 600 µmol mol–1,
no additional increase in pollen per floral spike was
observed, but the number of floral spikes rose significantly.
The net result was an approximate doubling of pollen
production capacity from pre-industrial to present day [CO2]
and a further doubling to a projected [CO2] of
600 µmol mol–1.
Interestingly, interpolation of the potential pollen
response of ragweed to [CO2] from the 1950s
(~315 µmol mol–1) to current levels shows a percentage
Days after sowing
20 22 24 26 28 30 32 34 36
Total biomass (g plant–1)
0
4
8
12
16
20
24
280 µmol mol–1
370 µmol mol–1
600 µmol mol–1
CO
2
growth concentration
*
*
Fig. 2. Change in total plant biomass (g plant–1) as a function of days
after sowing (DAS) for ragweed grown at pre-industrial, current and
future atmospheric [CO2]. Bars are ± s.e. Relative growth rate (RGR)
was determined between 21 and 29 DAS. No further change in RGR as
a function of [CO2] was observed after 35 DAS. * indicates a signifi-
cant increase in total biomass relative to the 280 µmol mol–1 [CO2]
control.
Table 1. Changes in measured (leaf area, leaf, stem and root dry
weights) vegetative parameters at maturity for common ragweed
(Ambrosia artemisiifolia L.) grown at pre-industrial, current and
future levels of atmospheric [CO2]
Different letters within a column indicate statistical differences between
[CO2] treatments at the 0.05 level according to Student–Newman–
Keuls. Data are given on a per-plant basis
[CO2] Area Weight (g) Total
(µmol mol–1)(m
2) Leaf Stem Root Floral weight (g)
280 1.15 c 65.1 c 30.7 c 11.3 b 28.9 b 135.1 c
370 2.17 b 88.7 b 45.7 b 13.5 b 35.7 b 183.6 b
600 3.41 a 178.9 a 97.1 a 50.3 a 49.2 a 372.4 a
Table 2. Photosynthesis (as CO2assimilation rate, µmol CO2
m–2 s–1) for ragweed (Ambrosia artemisiifolia L.) grown and
measured at pre-industrial, current and future atmospheric [CO2]
Different letters within a column indicate statistical differences between
[CO2] treatments at the 0.05 level according to Student–Newman–
Keuls. Additional details are given in ‘Materials and methods’
Growth [CO2] Measurement [CO2] (µmol mol–1)
(µmol mol–1) 280 370 600
280 15.1 23.3 b 33.1 b
370 19.6 40.7 a 53.0 a
600 14.8 35.6 a 52.9 a
897
increase in ragweed pollen consistent with the recent
reported percentage increase in allergies and allergy-induced
asthma among the general population (Platt-Mills and Carter
1997; Woolcock and Peat 1997). However, has the actual
amount of ragweed pollen in the environment increased
within the last 40 years? Because the rise in atmospheric
[CO2] has been so rapid, traditional 14C dating techniques to
determine in situ increases in pollen production since the
mid-1950s are not applicable. The earliest pollen studies are
based on some 13 000 gravity slide samples from 22
American cities summarized from 1916 to 1928 (Durham
1929). Unfortunately, direct comparisons between gravi-
metric and volumetric devices (e.g. Rotorod sampler) are dif-
ficult to perform. Differences in pollen recovery cannot be
quantified, even roughly (see Frenz 1999a). Even if different
sampling techniques were comparable, changes in land use
and nitrogen deposition in industrial areas could not be sep-
arated from any direct atmospheric CO2effect. Current
regional, on-site estimates of ragweed pollen production do
not date back more than a few years (Frenz et al. 1995, Frenz
1999b), although it is hoped that these data could be used to
verify potential increases in ragweed pollen with future
increases in atmospheric [CO2].
Will similar increases in pollen with enhanced [CO2] be
observed for other known allergy-inducing species?
Projected increases in [CO2] have been shown to stimulate
the photosynthesis and growth of C3species such as lambs-
quarters (Carlson and Bazzaz 1982) and oak (Bunce 1992),
as well as some C4species such as pigweed (Tremmel and
Patterson 1993) and foxtail (Ziska and Bunce 1997).
However, the reproductive response to [CO2] cannot always
be elucidated from observed increases in vegetative biomass
(Jablonski 1997).
Critics of the role of CO2in climate change correctly
point out that rising [CO2] could result in a lush plant
environment (Idso and Idso 1994). However, it should also
be emphasized that the rise in [CO2] is indiscriminatory with
respect to the stimulation of both useful and noxious plant
species. Furthermore, elimination of noxious weedy species
by chemical means cannot always be assumed as atmos-
pheric [CO2] increases (Ziska et al. 1999). Consequently, the
role of rising atmospheric [CO2] with respect to distribution,
growth and pollen production of weeds impacting human
health should be of growing concern.
Acknowledgments
The authors thank Dr JA Bunce of the Climate Stress
Laboratory for his suggestions to the manuscript, Dr Dave
Patterson, weed specialist at North Carolina State University
for his advice and Dr Linda Ford of the National Allergy
Bureau for her insightful comments.
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Manuscript received 25 February 2000, accepted 3 July 2000
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