Entomologia Experimentalis et Applicata 99: 87–96, 2001.
© 2001 Kluwer Academic Publishers. Printed in the Netherlands.
87
Effects of elevated CO2 on five plant-aphid interactions
Lesley Hughes∗ & Fakhri A. Bazzaz
The Biological Laboratories, Harvard University, Cambridge, MA 02138, USA
∗ Present address: Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia
(E-mail: [email protected]. mq.edu.au)
Accepted: November 7, 2000
Key words: Acyrthosiphon pisum, aphids, Aphis nerii, Aphis oenotherae, Aulacorthum solani, climate change,
CO2 , herbivory, Myzus persicae
Abstract
We investigated interactions between five species of phloem-feeding aphids (Homoptera: Aphididae) and their
host plants at elevated CO2 ; Acyrthosiphon pisum (Harris) on Vicia faba L., Aphis nerii Boyer de Fonscolombe
on Asclepias syriaca L., Aphis oenotherae Oestlund on Oenothera biennis L., Aulacorthum solani (Kaltenbach)
on Nicotiana sylvestris Speg. & Comes and Myzus persicae (Sulzer) on Solanum dulcamara L. Host plants grown
at elevated CO2 generally had greater biomass, leaf area and C:N ratios than those grown at ambient CO2 , while
plants with aphids had lower biomass and leaf area than those without aphids.
The responses of aphid populations to elevated CO2 were species-specific with one species increasing (M. persicae), one decreasing (A. pisum), and the other three being unaffected. CO2 treatment did not affect the
proportion of alate individuals produced. In general, aphid abundance was not significantly related to foliar nitrogen
concentration.
We performed separate analyses to test whether either aphid presence or aphid abundance modified the response
of host plants to elevated CO2 . In terms of aphid presence, only three of the potential 15 interactions (five aphid
species x three plant traits) were significant; A. solani slightly modified the response of the plant biomass to elevated
CO2 and M. persicae affected the response of leaf area and allocation. In terms of aphid abundance, only two of
the potential 15 interactions were significant with A. nerii modifying the plant response to CO2 in terms of total
leaf area and allocation.
We conclude that, in contrast to other insect groups such as leaf chewers, populations of most phloem-feeders
may not be negatively affected by increased CO2 concentrations in the future. The reasons for this difference
include the possibility that aphids may be able to compensate for changes in host plant quality by altering feeding
behaviour or by synthesizing amino acids. In addition, there is little evidence that aphid herbivory, even at high
levels, will substantially modify the response of plants to elevated CO2 .
Introduction
Over the next century, the atmospheric concentration
of CO2 is anticipated to double (Watson et al., 1996).
Profound effects on individual species and communities are expected, both as a direct result of the
‘fertilizing’ effect of CO2 on plant growth, and from
accompanying changes in climate.
The direct physiological effects of enriched CO2
atmospheres for individual plant species are becoming
increasingly well documented (e.g., Curtis & Wang,
1998). Several of these effects may alter the quality
and quantity of food available for insect herbivores.
First, many C3 plants raised in CO2 -enriched atmospheres have higher photosynthetic rates and grow
faster, increasing the biomass of plant material available to herbivorous insects. Second, as a result of
increased photosynthetic rates and faster growth, the
C:N ratio in foliage generally increases, mainly due
to accumulation of non-structural carbohydrates (e.g.,
88
Lindroth et al., 1995). As nitrogen is the single most
important limiting resource for phytophagous insects
(Mattson, 1980), this change alone may be the most
important influence on insect performance. Third, elevated CO2 can alter water content of foliage, leaf
toughness, and concentrations of defensive chemicals
(e.g., Lindroth et al., 1995).
Over 40 experimental studies on the effects of
elevated CO2 on plant-insect interactions have been
published to date (reviewed by Watt et al., 1995;
Bezemer & Jones, 1998; Coviella & Trumble, 1999;
Whittaker, 1999). In general, chewing insects fed on
foliage grown at elevated CO2 grow more slowly, take
longer to mature, suffer greater mortality, and have
higher consumption rates. There is good correlative
evidence that both the decline in performance and
increase in consumption are due to a decline in the
nutritional quality of the host plants, with the impact
of elevated CO2 on plant nitrogen explaining much of
the variation in response. Despite these broad generalisations, predictions as to how elevated CO2 will affect
overall rates of herbivory are still difficult to make for
several reasons. Many studies have examined the response of one or a few stages within the life cycle of
an insect species (usually one or two instars in the case
of lepidopterans) and the insects have often been fed
excised foliage, rather than being allowed to feed on
whole plants. In addition, most studies have focused
solely on insect performance in isolation from plant
performance. Questions such as how future increases
in insect consumption rates may be offset by increases
in plant biomass, for example, are largely unexplored.
In this study we focused on the effect of elevated
CO2 on five aphid-host plant combinations. We allowed insects to reproduce for several generations, and
measured both insect and plant performance simultaneously. The impact of elevated CO2 on aphid-plant
interactions is of interest for several reasons. First,
two aphid species, Myzus persicae (Bezemer et al.,
1998, 1999) and Aphis rumicis (Whittaker, 1999) are
the only insects studied so far, in any feeding guild,
whose populations have been positively influenced by
elevated CO2 . Second, aphids are generally considered to be the most important group of insect pests in
temperate regions (Cammell & Knight, 1991), inflicting direct damage by removing large quantities of sap,
and indirect damage by carrying viruses (Risebrow
& Dixon, 1987). The short generation times and immense capacity for increase of these insects give them
the potential for rapid responses to global change,
further enhancing the pest status of some species (Har-
rington et al., 1995). Third, aphid-feeding represents a
continuous carbon sink (Welter, 1989). Sink strength
is considered to be one of the most important influences regulating the acclimation response of plants
to elevated CO2 (Rogers et al., 1995). Herbivory by
aphids therefore, may modify the response of plants
to elevated CO2 . While there have been several studies that have measured the impact of elevated CO2
on aphid performance, only two have also assessed
the effect of aphid herbivory on plant performance at
elevated CO2 (Salt et al., 1996; Diaz et al., 1998).
We addressed the following questions: (1) What
are the direct effects of elevated CO2 on the biomass,
leaf area, allocation patterns and nitrogen content of
the host plants? (2) What are the direct effects of
aphids on the biomass, leaf area, allocation patterns
and nitrogen content of the host plants? (3) What are
the indirect effects of elevated CO2 on aphid populations via changes in plant biomass and composition?
(4) Do aphids modify the response of their host plants
to elevated CO2 ?
Study species
The five aphid-host plant combinations used were
the pea aphid Acyrthosiphon pisum on Vicia faba,
the oleander aphid Aphis nerii on Asclepias syriaca, the evening primrose aphid Aphis oenotherae on
Oenothera biennis, the glasshouse-potato, or foxglove
aphid Aulacorthum solani on Nicotiana sylvestris, and
the peach potato aphid Myzus persicae on Solanum
dulcamara. The effects of elevated CO2 on two of the
species, A. solani (Awmack et al., 1997) and M. persicae (Bezemer et al., 1998, 1999) have been examined
in other studies using different host species, thus allowing us to investigate how consistently these species
respond across different hosts.
Methods
Effect of elevated CO2 on aphid and plant
performance
The following basic experimental design was used
for each aphid-host plant combination. Temperatures
and experiment duration for each combination differed slightly (between 23 and 25 ◦ C) because of
growth requirements of the different aphid species
(Table 1). Optimal conditions for each species were
89
Table 1. Collection source, experimental temperatures, plant ages, and experiment duration for each aphid-host plant combination
Aphid species
(source)
Host plant
(source)
Temperature
◦C
Replicates per
chamber or module
Age of plants
at start (weeks)
Experiment
duration (weeks)
A. pisum
(Berkshire Biological
Southhampton, MA)
V. faba
(Vermont Bean Seed Co.
Fair Haven, VA)
constant 23 ◦ C
12
2
4
A. nerii (Cambridge,
MA)
A. syriaca
(V & J Seed Farms,
Woodstock, IL)
constant 23 ◦ C
16
3
5
A. oenotherae
(Cambridge, MA)
O. biennis
(Cambridge, MA)
25 ◦ C (day)
20 ◦ C (night)
16
5
4
A. solani (Arlington,
MA)
N. sylvestris
(Arlington, MA)
constant 24 ◦ C
16
5
3
M. persicae
(Cambridge, MA)
S. dulcamara
(Cambridge, MA)
constant 24 ◦ C
16
4
4
determined either from published studies or, when
these were unavailable, from pilot experiments. Our
aim was to maintain each aphid species under conditions that resulted in continuous, parthenogenetic,
reproduction of mainly apterous (wingless) viviparae.
Stock colonies were maintained at ambient CO2 on the
same host plant species and under the same conditions
of temperature, humidity and photoperiod used in the
experiment for the particular aphid species.
During each experiment, plants were grown in
either six glasshouse modules (O. biennis) or six
glass-sided chambers (all other species). Three of the
modules or chambers were assigned randomly to ambient (350 µl−L ) and three to elevated (700 µL−L )
CO2 . The control system for both the modules and
chambers allowed atmospheric CO2 concentrations,
air temperatures and relative humidity to be monitored
independently. CO2 was controlled through an automatic monitoring and injection system using a LiCor
6251 infrared gas analyzer (IRGA, Licor, Lincoln,
NE). Relative humidity was controlled by a Mee Industries Inc. fog injection system and was maintained
at approximately 60–70%. CO2 , temperature, and humidity control for the modules and chambers were
linked to a common software-based control system
(Lander Control Systems Inc. Ontario, Canada). All
experiments were conducted under natural photoperiod with natural illumination supplemented by High
Density Discharge lights suspended over the mod-
ule benches and chambers, providing light levels of
1800 µmol m−2 s−1 at bench level.
Excess plants were germinated for each experiment within the same chambers or modules in which
the experiment would be conducted. Seedlings were
transplanted to individual 1.8 l pots and watered daily.
At the beginning of each experiment a subset of the
most uniform plants was selected and half the plants
(see Table 1 for number of replicates) within each
chamber or module were randomly assigned to receive
aphids. The initial aphid infestation (n = 15) on each
plant was a mixture of adults and final instar nymphs.
All plants were caged individually in lightweight netting supported by stakes and were checked periodically to ensure no aphids had infested the control
plants. Plants were randomly repositioned within each
module or chamber every 3–4 days. Each experiment
was terminated when aphid numbers on each plant
had reached at least 200, but before any plants had
either flowered or died. At the end of each experiment
aphids were removed and counted and the proportion of alate to apterous individuals recorded. Plants
were then separated into above and below ground
parts. Total leaf area was measured for each plant and
then all plant parts were dried at 70 ◦ C and weighed.
Carbon:nitrogen ratios of above ground plant parts
were measured with a Europa CNH Analyzer (Model
ANCA-nt, Europa Elemental Instruments, England).
90
Statistical analysis
Direct effects of CO2 and aphids on plants. The effects of CO2 and aphids on total biomass, total leaf
area, % above ground biomass, % nitrogen and C:N
ratios of the host plants were analyzed by three factor ANOVAs using a split-plot design with CO2 and
block (pair of adjacent modules or chambers) as the
main effects and aphid presence as the sub-plot effect. Biomass data were ln transformed and percentage
data were arcsine transformed to satisfy assumptions
of normality for ANOVA.
Indirect effects of CO2 on aphid populations. The
effects of CO2 treatment on aphid abundance and
proportion of alate individuals were analyzed by two
factor ANOVAs using a randomized complete block
design with CO2 as a fixed and block as a random
factor. Data were ln or arcsine transformed where
appropriate to satisfy assumptions of normality. The
relationship between aphid abundance and nitrogen
content of the plants was analyzed using regressions.
To test whether the relationship between aphid abundance and nitrogen content was different between CO2
treatments we used ANCOVA with nitrogen content
as the co-variate; a significant interaction between
the co-variate and CO2 level indicated that CO2 level
modified the response of aphids to nitrogen content.
Modification of plant response to CO2 by aphids. We
performed separate analyses to test if either the (i)
presence or (ii) abundance of aphids modified the response of plants to elevated CO2 . The effect of aphid
presence on total biomass, total leaf area, and % above
ground biomass was tested by ANOVA (split-plot design with CO2 and blocks as the main plot effects and
aphid presence as the sub-plot effect). The effect of
aphid abundance was tested by ANCOVA using aphid
numbers on each plant as the co-variate. A significant
interaction between the co-variate and CO2 treatment
indicated that aphids modified plant responses to CO2 .
Results
Direct effects of elevated CO2 on the host plants. Total biomass of A. syriaca, S. dulcamara, N. sylvestris,
and O. biennis was significantly greater under elevated
CO2 with increases ranging from 22% in O. biennis to
207% in S. dulcamara (Figure 1). Total leaf area under
elevated CO2 increased signficantly only in A. syriaca
and S. dulcamara (Figure 2). The percentage of aboveground biomass decreased significantly in A. syriaca
and O. biennis at elevated CO2 (Figure 3). Percentage foliar nitrogen was signficantly decreased, and
C:N ratios signficantly increased, in all species except
O. biennis (Figure 4).
Direct effects of aphids on host plants. Aphids had
significant negative effects on the biomass and leaf
area of all host plant species at both ambient and elevated CO2 (Figures 1 and 2). A. nerii was the only
aphid species to significantly affect (increase) the %
allocation to above ground biomass (Figure 3). Aphids
did not significantly affect nitrogen concentration or
C:N ratios in any of the plant species.
Indirect effects of elevated CO2 on aphid populations.
The responses of aphid populations to elevated CO2
were highly species-specific (Figure 5). Populations of
A. pisum were reduced by over 60% at elevated CO2 .
In contrast, populations of M. persicae increased by
120% at elevated CO2 . CO2 treatment did not significantly affect the populations of the remaining three
species. Some winged adults were produced by all
the aphid species except M. persicae, but the proportion of winged to wingless was not affected by CO2
treatment.
Aphid numbers were significantly related to % nitrogen in the plant tissues only in A. pisum (ambient
CO2 : P = 0.0401, r 2 = 0.19), and in A. solani (elevated CO2 : P < 0.0001, r 2 = 0.572; both CO2 levels
combined: P = 0.0008, r 2 = 0.205). A. solani was
the only species for which the relationship between
aphid numbers and % nitrogen differed between CO2
treatments, with the slope at elevated CO2 being significantly steeper (slope at ambient CO2 ± 95% c.l.
= 1.23 ± 4.29, elevated CO2 = 18.23 ± 6.71).
Modification of plant response to elevated CO2 by
aphids. We performed separate analyses to test
whether the (i) presence and (ii) abundance of aphids
modified the response of plants to elevated CO2 . The
interaction between CO2 and aphid presence on total
biomass was significant only for A. solani, (Figure 1);
in this pair the presence of aphids slightly dampened
the response of plant biomass to elevated CO2 . M. persicae was the only aphid for which there was a significant interaction between CO2 and aphid presence on
leaf area and % above ground biomass (Figures 2 and
3).
91
Figure 1. Effects of aphids and CO2 on total plant biomass (means ± s.e.). (a) A. pisum on V. faba, (b) A. nerii on A. syriaca, (c) A. oenotherae
on O. biennis, (d) A. solani on N. sylvestris, (e) M. persicae on S. dulcamara.
We used aphid abundance as a co-variate in ANCOVAs testing the effect of CO2 level on plant responses. A. nerii was the only aphid species whose
abundance significantly modified the plant response to
CO2 in terms of total leaf area and % above ground
biomass (Figures 2 and 3). Aphid abundance did not
modify the response of total biomass to CO2 treatment
for any species.
Discussion
Direct effects of CO2 and aphids on plants. As separate treatments, both CO2 level and aphid presence
had the expected effects on plant growth. Elevated
CO2 generally enhanced biomass and leaf area, but
had variable effects on root/shoot allocation, consistent with most other studies (e.g., Curtis & Wang,
1998). The negative effects of aphids on plant growth
were generally greater than the positive effects of CO2
under the experimental conditions used, with all plant
species suffering substantial reductions in total biomass and leaf area. The magnitude of aphid damage
in these experiments was not surprising, given that the
aphids were kept under constant optimal conditions
and were not subject to natural enemies. Nonetheless, comparable aphid densities in the field have been
found (e.g., Dixon et al., 1993), indicating that future
effects of elevated CO2 on some plant species may
be relatively small compared to the effects of insect
herbivores.
None of the aphid species significantly affected
either % N or C:N ratios in the host plants. This is
consistent with the findings of most other studies (e.g.,
Hawkins et al., 1986), that aphids do not preferentially
remove nitrogen from the phloem sap.
Indirect effects of CO2 on aphid performance. The
effects of elevated CO2 on aphid populations varied
substantially among the five species tested, with one
being negatively affected, another positively affected,
and with no significant effects found for the remaining
92
Figure 2. Effects of aphids and CO2 on total leaf area (means ± s.e.). (a) A. pisum on V. faba, (b) A. nerii on A. syriaca, (c) A. oenotherae on
O. biennis, (d) A. solani on N. sylvestris, (e) M. persicae on S. dulcamara.
three. Production of alate forms was not signficantly
affected by CO2 treatment. It should be noted here that
this study measured only final aphid populations at
harvest, rather than estimating short-term indicators of
performance such as daily reproductive rate. Several
studies that have measured both short- and longer-term
aspects of aphid performance have found inconsistencies in the direction of reponse at elevated CO2 (e.g.,
Docherty et al., 1997). Given these inconsistencies,
the longer term measurement of population size after several generations, which integrates the effect of
CO2 on many life history processes, will be a better
predictor of future effects than shorter term estimates.
This study brings the number of identified aphid
species investigated for responses to elevated CO2 to a
total of 14. Our main conclusion is that, at a population
level, elevated CO2 has not had substantial effects on
the majority of aphid species tested. In the 12 species
for which population measurements have been made,
elevated CO2 has not had a significant effect on eight:
A. nerii, A. oenotherae, A. solani (this study), Aphis
fabae fabae, Pemphigus populitransversus (Salt et al.,
1996), Brevicoryne brassicae (Smith, 1996; Bezemer et al., 1999), Phyllaphis fagi (Docherty et al.,
1997), and Sitobion avenae (Diaz et al., 1998). Two
species have been negatively affected, A. pisum in
the present study, and Rhopalosiphum padi (Newman
et al., 1999), plus an unidentified species infecting
wheat in a study by Thompson et al. (1993). M. persicae (this study, Bezemer et al., 1998, 1999) and Aphis
rumicis (Whittaker, 1999) are the only species found
to be significantly advantaged at elevated CO2 .
Given that elevated CO2 consistently reduces foliar
N content and increases C:N ratios, and that foliar N
is usually correlated with both the nitrogen content
of phloem sap and aphid performance (e.g., Dixon
et al., 1993), why have the majority of aphid species
tested not been negatively affected by elevated CO2 in
the same way as most leaf chewers? Three possible
explanations, acting singly, or in combination, seem
plausible.
93
Figure 3. Effects of aphids and CO2 on % above ground biomass (means ± s.e.). (a) A. pisum on V. faba, (b) A. nerii on A. syriaca, (c)
A. oenotherae on O. biennis, (d) A. solani on N. sylvestris, (e) M. persicae on S. dulcamara.
First, the negative effects of elevated CO2 on plant
nitrogen may be outweighed by positive effects on
some other plant characteristic(s). Any factor that
affects nitrogen content will also affect the concentrations of other nutrients, pH, phloem pressure, leaf
toughness and defensive chemicals. Salt et al. (1996)
and Docherty et al. (1997), have also speculated that
aphids may be affected by an increase in leaf surface
temperature at elevated CO2 (Idso et al., 1993), or by
changes in partitioning and sap flow rates in the plant
(Girousse & Bournoville, 1994).
Second, changes in the ratio of soluble nitrogen to
sugars or the partitioning of the soluble nitrogen pool
into different fractions may be as, or more, important
than changes in total nitrogen. Evidence from both
field studies and laboratory experiments using artificial diets indicates that different aphid species have
specific requirements for certain amino acids (e.g.,
Risebrow & Dixon, 1987). Aphids also respond to the
ratio between sugars and soluble nitrogen in their diet
(Braun and Flückiger, 1989). The effect of elevated
CO2 on phloem composition will therefore be important for the performance of individual aphid species
though unfortunately there are scant data available. In
general, amino acids in phloem sap have been found
to decline at elevated CO2 (Wang & Nobel, 1995;
Docherty et al., 1997), but data on a wider range of
plant species will be needed to understand speciesspecific differences in response of aphids to elevated
CO2 .
A third possible reason why most aphid species are
not negatively affected at high CO2 is that they may
be able to compensate adequately for CO2 -induced
changes in nutritional quality by altering the position on the plant where they feed, the rate of uptake,
or post-ingestive metabolism (Abisgold et al., 1994).
Such compensatory responses may serve as a future
buffer against variation in host plant quality as a result
of changes in atmospheric CO2 concentration.
94
Figure 4. Effect of CO2 on % nitrogen (L.H. axis) and C:N ratios (R.H. axis), (means ± s.e.). (a) V. faba, (b) A. syriaca, (c) O. biennis, (d)
N. sylvestris, (e) S. dulcamara.
Interaction of aphids and CO2
Will the response of plants to elevated CO2 in the
future be modified by the presence of herbivores?
Laboratory feeding studies in which insects increased
consumption rates when fed excised foliage from
plants grown at elevated CO2 have led to speculation
that damage by herbivores may increase in the future. When insect and plant performance at elevated
CO2 has been assessed simultaneously, however, the
general conclusion has been that increases in plant
biomass at elevated CO2 more than compensate for increased insect consumption (Caulfield & Bunce 1994;
Salt et al., 1995; Hughes & Bazzaz, 1997).
There is little evidence from this study that aphids
substantially modified the response of their host plants
to elevated CO2 . When the effect of aphid presence is
considered, only three of the 15 possible interactions
between aphids and plant characteristics (five aphid
species × three plant traits) were significant. When
aphid abundance was taken into account, only two of
the possible 15 interactions were significant. These results are consistent with those of the two other studies
in which both aphid and plant performance has been
measured simultaneously under elevated CO2 (Salt
et al., 1996; Diaz et al., 1998).
Conclusions
Simultaneous measurements of both insect and plant
responses to elevated CO2 are important to generate
predictions as to how levels of insect herbivory may
change in the future. As separate treatments, we found
that elevated CO2 had the expected positive effect, and
aphids the expected negative effect, on plant biomass
and leaf area. There were substantial differences between the performance of different aphid species at
elevated CO2 but, taken together with results from
other studies, our overall conclusion is that elevated
CO2 may not have substantial effects on most aphid
populations in the future. The already serious pest,
M. persicae, appears to be an exception to this generalisation. The reasons for the lack of effects under
elevated CO2 for most species include the possibility
that phloem-feeders can compensate for changes in ni-
95
Figure 5. Effect of CO2 on aphid abundance (means ± s.e.). (a) A. pisum on V. faba, (b) A. nerii on A. syriaca, (c) A. oenotherae on O. biennis,
(d) A. solani on N. sylvestris (e) M. persicae on S. dulcamara.
trogen concentrations by altering feeding behaviour or
by synthesizing amino acids with the aid of symbionts,
at least on the scale at which elevated CO2 affects plant
quality. In addition, there is little evidence from this
and other studies that aphids will substantially modify
the response of plants to elevated CO2 .
Acknowledgements
We are grateful to Richard Stomberg for valuable
horticultural advice and general assistance with the experiments, John Nevins and Glenn Berntson for their
generous help with the C:N analysis, and Jenny Lin
for assistance in the glasshouse. This work greatly
benefited from interaction and discussion with Glenn
Berntson, Michal Jasienski, Alison Li, Peter Wayne
and Mark Westoby. We also thank Caroline Awmack
for commenting on the manuscript. This research was
supported by an International Fellowship from the
American Association of University Women (to L.H)
and a NIGEC Grant (No. 901214-HAR) (to F.A.B).
References
Abisgold, J. D., S. J. Simpson & A. E. Douglas, 1994. Nutrient regulation in the pea aphid Acyrthosiphon pisum: application of a novel geometric framework to sugar and amino acid
composition. Physiological Entomology 19: 95–102.
Awmack, C. S., R. Harrington & S. R. Leather, 1997. Host plant effects on the performance of the aphid Aulacorthum solani (Kalt.)
(Homoptera: Aphididae) at ambient and elevated CO2 . Global
Change Biology 3: 545–549.
Bezemer, T. M & T. H. Jones, 1998. Plant-insect herbivore interactions in elevated atmospheric CO2 : quantitative analyses and
guild effects. Oikos 82: 212–222.
Bezemer, T. M, T. H. Jones & K. Knight, 1998. Long-term effects of
elevated CO2 and temperature on populations of the peach potato
aphid Myzus persicae and its parasitoid Aphidius matricariae.
Oecologia 116: 128–135.
Bezemer, T. M., K. J. Knight, J. E. Newington & T. H. Jones, 1999.
How general are aphid responses to elevated atmospheric CO2 ?
Annals of the Entomological Society of America 92: 724–730.
Braun, S. & W. Flückiger, 1989. Effect of ambient ozone and acid
mist on aphid development. Environmental Pollution 56: 177–
187.
Cammell, M. E. & J. D. Knight, 1991. Effects of climate change on
the population dynamics of crop pests. Advances in Ecological
Research 22: 117–162.
Caulfield, F. & J. A. Bunce, 1994. Elevated atmospheric carbon
dioxide concentration affects interactions between Spodoptera
exigua (Lepidoptera: Noctuidae) larvae and two host plant
species outdoors. Environmental Entomology 23: 999–1005.
96
Coviella, C. E. & J. T. Trumble, 1999. Effects of elevated atmospheric carbon dioxide on insect-plant interactions. Conservation Biology 13: 700–712.
Curtis, P. S. & X. Wang, 1998. A meta-analysis of elevated CO2
effects on woody plant mass, form, and physiology. Oecologia
113: 299–313.
Diaz, S., L. H. Fraser, J. P. Grime & V. Falczuk, 1998. The impact of
elevated CO2 on plant-herbivore interactions: experimental evidence of moderating effects at the community level. Oecologia
117: 177–186.
Dixon, A. F. G., P. W. Wellings, C. Carter & J. F. A. Nichols,
1993. The role of food quality and competition in shaping the
seasonal cycle in the reproductive activity of the sycamore aphid.
Oecologia 95: 89–92.
Docherty, M., F. A. Wade, D. K. Hurst, J. B. Whittaker & P. J. Lea,
1997. Responses of tree sap-feeding herbivores to elevated CO2 .
Global Change Biology 3: 51–59.
Girousse, C. & R. Bournoville, 1994. Role of phloem sap quality
and exudation characteristics on performance of pea aphid grown
on lucerne genotypes. Entomologia Experimentalis et Applicata
70: 227–235.
Harrington, R., J. S. Bale & G. M. Tatchell, 1995. Aphids in a
changing climate. In: R. Harrington & N. E. Stork (eds), Insects in a Changing Environment. Academic Press, London,
pp. 126–157.
Hawkins, C. D. B., M. I. Whitecross & M. J. Aston, 1986. Interactions between aphid infestation and plant growth and uptake
of nitrogen and phosphorus by three leguminous host plants.
Canadian Journal of Botany 64: 2362–2367.
Hughes, L. & F. A. Bazzaz, 1997. Effect of elevated CO2 on
interactions between the western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae) and the common milkweed,
Asclepias syriaca. Oecologia 109: 286–290.
Idso, S. B., B. A. Kimball, D. E. Akin & J. Kridler, 1993. A general relationship between CO2 -induced reductions in stomatal
conductance and concomitant increases in foliage temperature.
Environmental and Experimental Botany 33: 443–446.
Lindroth, R. L., G. E. Arteel & K. K. Kinney, 1995. Responses of
three saturniid species to Paper Birch grown under enriched CO2
atmospheres. Functional Ecology 9: 306–311.
Mattson, W. J., 1980. Herbivory in relation to plant nitrogen content.
Annual Review of Ecology and Systematics 11: 119–161.
Newman, J. A., D. J. Gibson, E. Hickam, M. Lorenz, E. Adams, L.
Bybee & R. Thompson, 1999. Elevated carbon dioxide results in
smaller populations of the bird cherry-oat aphid Rhopalosiphum
padi. Ecological Entomology 24: 486–489.
Risebrow, A. & A. F. G. Dixon, 1987. Nutritional ecology of
phloem-feeding insects. In: F. Slansky & J. G. Rodriguez (eds),
Nutritional Ecology of Insects, Mites, Spiders, and Related
Invertebrates. John Wiley and Sons, New York, pp. 421–448.
Rogers, A., J. B. Bryant, C. A. Raines, S. P. Long, H. Blum & M.
Frehner, 1995. Acclimation of photosynthesis to rising CO2 concentration in the field. Is it determined by source sink balance?
In: P. Mathis (ed), Photosynthesis: From Light to Biosphere, Vol.
I. Kluwer Academic Publishers, Dordrecht, pp. 1001–1004.
Salt, D. T., G. L. Brooks & J. B. Whittaker, 1995. Elevated carbon
dioxide affects leaf-miner performance and plant growth in docks
(Rumex spp.). Global Change Biology 1: 153–156.
Salt, D. T., P. Fenwick & J. B. Whittaker, 1996. Interspecific herbivore interactions in a high CO2 environment: root and shoot
aphids feeding on Cardamine. Oikos 77: 326–339.
Smith, P. H. D., 1996. The effects of elevated CO2 on aphids.
Antenna 20: 109–111.
Thompson, G. B., J. K. M. Brown & F. I. Woodward, 1993. The
effects of host carbon dioxide, nitrogen and water supply on the
infection of wheat by powdery mildew and aphids. Plant, Cell
and Environment 16: 687–694.
Wang, N. & P. S. Nobel, 1995. Phloem exudate collected via scale
insect stylets for the CAM species Opuntia ficus-indica under
current and doubled CO2 concentrations. Annals of Botany 75:
525–532.
Watson, R. T., M. C. Zinyowera & R. H. Moss, 1996. Climate
Change 1995: Impacts, Adaptations and Mitigation of Climate
Change: Scientific-Technical Analyses. Cambridge University
Press, Cambridge.
Watt, A. D., J. B. Whittaker, M. Docherty, G. Brooks, E. Lindsay
& D. T. Salt, 1995. The impact of elevated atmospheric CO2 on
insect herbivores. In: R. Harrington & N. E. Stork (eds), Insects
in a Changing Environment. Academic Press, London, pp. 198–
217.
Welter, S. C., 1989. Arthropod impact on plant gas exchange. In:
E. A. Bernays (ed), Insect-Plant Interactions, Vol. 1. CRC Press,
Boca Raton, pp. 135–150.
Whittaker, J. B., 1999. Impacts and responses at population level
of herbivorous insects to elevated CO2 . European Journal of
Entomology 96: 149–156.