Divergent responses of two cereal aphids to previous infestation of their host plant
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Entomologia Experimentalis et Applicata 103: 43–50, 2002.
© 2002 Kluwer Academic Publishers. Printed in the Netherlands.
43
Divergent responses of two cereal aphids to previous infestation of their
host plant
Frank J. Messina, Rodrick Taylor & Margaret E. Karren
Department of Biology, Utah State University, Logan, UT 84322-5305, USA; (E-mail: messina@biology.usu.edu)
Accepted: April 23, 2002
Key words: induced responses, specificity, cereal aphids, feeding preferences, population growth, Diuraphis noxia,
Rhopalosiphum padi, Homoptera, Aphididae
Abstract
We examined the effects of prior infestation by the Russian wheat aphid [Diuraphis noxia (Mordvilko)] and the
bird cherry-oat aphid [Rhopalosiphum padi (L.)] on the subsequent feeding preferences and performance of each
species. Aphid colonies fed and reproduced on wheat seedlings for five days and were then removed. After a period
of plant recovery, we estimated aphid population growth and feeding preferences on control and previously infested
plants. Previous infestation by D. noxia had no effect on the subsequent population growth of either aphid species.
Previous infestation by R. padi reduced its own subsequent growth by 50%, but had little effect on the population
growth of D. noxia. When presented leaves from control plants and D. noxia-infested plants, D. noxia adults
preferred to feed on leaves from control plants; R. padi adults showed no preference. Both aphids preferred leaves
from control plants to those from R. padi-infested plants. In free-flight cages, alates of R. padi settled more often
and produced more progeny on control plants than on plants previously infested by R. padi, but their rates of settling
and reproduction were unaffected by prior D. noxia infestation. Together, our results suggest specificity in both
the plant response to the two aphid species (plant quality for R. padi was lowered by prior R. padi infestation but
not by D. noxia infestation) and in each aphid’s response to the same modification of the host plant (infestation by
R. padi reduced plant quality for itself but not for D. noxia). Effects of prior infestation on the feeding preferences
of R. padi were correlated with effects on performance.
Introduction (Agrawal, 1999) or different stages of the same her-
bivore (van Dam et al., 2001). In this study, we
Plants undergo a wide variety of chemical and mor- examined the specificity of plant and insect responses
phological changes in response to attack by herbivores to feeding by two cereal aphids.
and pathogens (Karban & Baldwin, 1997). Induced Phloem-feeding aphids illustrate the complexity of
responses may serve as a defense by deterring further induced responses in plants. The presence of one aphid
herbivory, but in some cases prior infestation improves can enhance the growth of another (e.g., Kidd et al.,
the performance of later-arriving herbivores (Gange & 1985; Fisher, 1987), particularly if aphid feeding in-
Brown, 1989; Underwood, 1998; Agrawal & Sher- creases nutrient availability by altering the source-sink
riffs, 2001). Increasing evidence suggests that both relationships of leaves (Larson & Whitham, 1991).
induced responses and their consequences are highly On the other hand, feeding by one aphid may reduce
species-specific (Walling, 2000). One type of speci- phloem quality, and hence the performance of later- ar-
ficity, called specificity of elicitation, occurs when a riving species (Petersen & Sandström, 2001). Because
plant shows distinct responses to different herbivore aphids often cause systemic changes in plant chem-
species (Stout et al., 1998). A second type, called istry, feeding by one species can decrease food quality
specificity of effect, arises when the same plant re- for another aphid on a different portion of the plant
sponse has contrasting effects on different herbivores (Moran & Whitham, 1990). Induced plant responses44
can thus lead to asymmetrical competition between produced one unfolded leaf and one emerging leaf.
aphid species (Inbar et al., 1999; Denno et al., 2000). Cages had organdy-cloth windows on the sides and
The Russian wheat aphid [Diuraphis noxia top for ventilation. We used a camelhair brush to add
(Mordvilko)] and the bird cherry-oat aphid [Rhopalosi- 25 adult aphids (apterous D. noxia or alate R. padi)
phum padi (L.)] (Homoptera: Aphididae) commonly to half of the caged plants. Aphids were obtained from
co-occur on wheat (Triticum aestivum L.) and other anholocyclic laboratory colonies maintained on winter
cereals, but may have disparate effects on host plants. wheat (Messina et al., 1993). The R. padi colony was
Russian wheat aphids feed in dense aggregations, usu- derived from a virus-free population at Pennsylvania
ally in curled leaves, and cause extensive chlorosis State University. Voucher specimens were placed in
(Riedell, 1989; Burd & Burton, 1992). Bird cherry- the Utah State University Insect Collection.
oat aphids are less aggregated, do not produce such Aphids fed and reproduced for five days, af-
visible damage, and tend to feed on the lower por- ter which all plants were brought to the labora-
tions of plants (Pettersson et al. 1995; Quiroz et al., tory. Aphids on each infested plant were brushed
1997; Gianoli, 1999). Both species alter leaf protein into a tray containing 50% ethanol. Small camelhair
content (Ni et al., 2001), but feeding by D. noxia brushes were used to reach aphids (especially those
appears to cause a greater enhancement of nutrition of D. noxia) feeding within curled leaves. Aphids
(Sandström et al., 2000; Sandström & Moran, 2001). removed from a subset of infested plants were later
The two aphids may also differ in the tendency to in- counted to provide an estimate of aphid density at the
duce putative plant defenses (Forslund et al., 2000; end of the initial infestation. Because mechanical stim-
Ni et al., 2001). One study suggested that prior ulation alone can induce changes in plant chemistry
feeding by D. noxia increased the fecundity of the (e.g., Cipollini, 1997), uninfested plants were handled
greenbug, Schizaphis graminum (Rondani) (Formusoh in the same way as infested ones, i.e., their leaves were
et al., 1992), but infestation by R. padi seems to reduce brushed over a tray containing 50% ethanol. All plants
plant quality (Gianoli, 2000; Alla et al., 2001). were then transferred to a growth chamber at 24 ◦ C,
Although D. noxia and R. padi appear to elicit dif- 50–60% r.h., and constant light. Plants remained in
ferent plant responses, most studies have considered the chamber for two days, during which time we in-
only one of the two species or have been restricted to spected them and removed the few aphids missed by
chemical assays of particular plant compounds. Even the first brushing. Most plants produced a new leaf
if two herbivores induce different specific changes in during this period. At the start of experiments, plants
plant chemistry, one cannot assume that they will have usually possessed 2–3 unfolded leaves and one tiller.
different effects on overall plant quality (e.g., Under-
wood et al., 2002). We used as a set of experiments Effects on population growth. Four initial experi-
to compare directly the effects of prior infestation by ments compared aphid population growth on control
D. noxia and R. padi on the subsequent feeding pref- plants and previously infested plants. Two experi-
erences and population growth of each species. The ments separately measured the growth of each aphid
experiments were designed to examine both specificity species on control and D. noxia-infested plants; two
of elicitation and specificity of effect. further experiments estimated each aphid’s growth on
control and R. padi-infested plants. Although it would
have been preferable to compare all treatments simul-
Materials and methods taneously, the time required to remove primary in-
festations from a sufficient number of replicate plants
Establishment of control and infested plants. A stan- precluded a full factorial design. In each experiment,
dard protocol was used to produce equal-aged control control and previously-infested plants were returned
and previously infested plants for experiments. Seeds to the greenhouse, inoculated with three adult aphids
of ‘Garland’ winter wheat were germinated in a peat- (apterous D. noxia or alate R. padi) per plant, and
vermiculite mixture in 1450-ml, square pots in a caged as before (N = 20–30 plants per treatment). Af-
greenhouse. Five days after planting, seedlings were ter ten days, plants and aphids were harvested in
thinned to one per pot and fertilized with 50 ml of a 20- jars containing 70% ethanol, and aphids were later
20-20 NPK solution. A cellulose-acetate cage (4.1 cm counted under a dissecting microscope. The 10-day
diameter × 32 cm tall) was placed over each plant duration of the experiment represented approximately
seven days after planting, by which time plants had one and a half aphid generations, so that recovered45
aphids included both the offspring and grandoffspring A second pair of experiments measured the settling
of the original three females per plant. Because all behavior and reproduction of alate R. padi on whole
plants bore at least three leaves and received only three plants (alate D. noxia were not abundant enough to
aphids, any treatment effect on final aphid density will use for this assay). Two control plants and two pre-
reflect variation in food quality rather than variation in viously infested plants were placed into each of ten
food availability (Messina, 1993). cages (dimensions = 32 × 32 × 32 cm). The sides and
Because we were primarily interested in the effects top of the cages consisted of fine-mesh screening, and
of previous infestation on D. noxia populations, a fifth the removable top allowed the introduction of potted
experiment was similar to the previous four but simul- plants. We placed the two plants of the same type at
taneously compared the population growth of D. noxia opposite corners of a cage and alternated which cor-
on control, D. noxia-infested, and R. padi-infested ners received control or previously infested plants in
plants. A final (sixth) experiment examined the pop- successive cages. Cages were arranged under a bank
ulation growth of D. noxia on plants previously in- of fluorescent lights (L16:D8) on a laboratory bench.
fested with varying densities of D. noxia. We included Ambient temperatures were 25–28 ◦ C and relative
this experiment because some studies suggested that humidity was 35–40%.
infestation by D. noxia improved plant quality (For- After plants were added to the cages, we placed
musoh et al., 1992; Sandström et al., 2000), but a 10-cm petri dish containing 20 alate R. padi in the
it seemed likely that a positive effect would occur center of each cage bottom, and removed the lid. Upon
only at intermediate aphid densities. Instead of adding release, aphids often flew to the tops of the cage, but
25 aphids per plant to produce the primary infestation, they usually settled on plants within 12 h. Aphids
we added 0, 5, 10, 25, or 50 aphids per plant (ten were allowed to feed and reproduce for five days,
plants per treatment). Aphids from the primary infes- after which plants and aphids were harvested into
tation were removed as before, and population growth jars with 70% ethanol. The five-day interval between
was estimated ten days after each plant received two aphid release and recovery was less than the time
adults. Greenhouse temperatures during each of the needed to complete a generation, so that all recov-
population-growth experiments fluctuated between 20 ered adults were released individuals and all nymphs
and 30 ◦ C in a daily cycle; relative humidity was 50– were their direct offspring. Paired t tests determined
80%. Analysis of variance was used to assess the effect whether aphid counts differed between control and
of plant history on final population sizes. Counts were previously infested plants. We pooled counts from the
square-root transformed before analysis. two plants of the same type per cage because these
counts were not statistically independent (i.e., the unit
Effects on feeding preferences. The effect of previ- of replication was the cage rather than the individual
ous infestation on feeding preference was measured plant).
in two experiments that used excised leaves. We used
scissors to cut a 6 cm-long section at the base of the
second unfolded leaf on each control or previously Results
infested plant. This leaf was chosen because it usu-
ally bore many aphids during the primary infestation. Effects on population growth. The first experiment
Only one leaf section was obtained from each plant. measured the population growth of D. noxia on control
One control leaf and one previously infested leaf were plants vs. plants previously infested by D. noxia. Mean
placed parallel to each other on moist filter paper in aphid density (± SE) at the end of the primary infes-
each of 50, 10-cm petri dishes. In successive dishes tation was 285.8 ± 14.4 (N = 10). Despite this level
we alternated the left-right orientation of control and of prior infestation, population growth was not sig-
previously infested leaves. We then used a camelhair nificantly different on control and previously infested
brush to place ten adults of either D. noxia or R. padi plants (Figure 1A). In a second experiment, previous
(25 dishes per treatment) in the center of each dish infestation by D. noxia had no effect on the popula-
(midway between the leaves). Dishes were transferred tion growth of R. padi (Figure 1B), even though the
to a growth chamber at 24 ◦ C, and the number of average density of the primary infestation had reached
aphids on each leaf was recorded after 4 h. Paired 359.3 ± 21.6 aphids per plant (N = 10).
t tests examined whether aphid distribution depended Two further experiments used plants previously in-
on leaf type. fested by R. padi. In the first experiment, the average46
Figure 1. (A) Mean number (+ SE) of Russian wheat aphids (D. noxia) on control plants vs. plants previously infested by D. noxia (F = 0.92;
df = 1, 38; P = 0.34). (B) Mean number of bird cherry-oat aphids (R. padi) on control plants vs. plants previously infested by D. noxia
(F = 0.0001; df = 1, 48; P = 0.99). Counts were obtained ten days after each plant received three adults. N = 20–25 plants per treatment.
Figure 2. (A) Mean number (+ SE) of Russian wheat aphids (D. noxia) on control plants vs. plants previously infested by the bird cherry-oat
aphid (R. padi) (F = 2.55; df = 1, 48; P = 0.12). (B) Mean number of R. padi on control plants vs. plants previously infested by R. padi
(F = 73.01; df = 1, 59; P < 0.001). Counts were obtained ten days after each plant received three adults. N = 25–30 plants per treatment.
density of R. padi was 268.0±11.2 at the time of aphid ined D. noxia growth on control, D. noxia-infested,
removal (N = 14). The subsequent population growth and R. padi-infested plants. Average densities of the
of D. noxia was approximately 12% higher on control primary infestation were 286 ± 20.5 and 256.7 ± 23.1
plants than on plants previously infested by R. padi aphids per plant for D. noxia- and R. padi-infested
(Figure 2A), but this difference was not significant plants, respectively (N = 10 sampled plants per treat-
(P = 0.12). In a second experiment, prior infestation ment). Ten days after all plants received three adults,
by R. padi had a strong negative effect on its own pop- population sizes of D. noxia were virtually identical
ulation growth; aphid density on previously infested on control plants (209.7 ± 16.5) and those previ-
plants was nearly 50% lower than it was on control ously infested by D. noxia (205.5 ± 13.5). Populations
plants (Figure 2B). The density of the primary infes- were slightly smaller on plants previously infested by
tation in this experiment was 269.8 ± 19.3 aphids per R. padi (180.4 ± 10.9), but the effect of previous in-
plant (N = 12). festation on the population growth of D. noxia was
The above experiments suggested that the popula- again non-significant (F = 1.19; df = 2, 70; P = 0.31;
tion growth of D. noxia was unaffected by previous N = 23–25 plants per treatment).
infestation. To confirm this, we simultaneously exam-47
Table 1. Mean number (± SE) of Russian wheat aphids
(D. noxia) on plants previously infested by different densi-
When alates of R. padi were presented control plants
ties of D. noxia. Counts from the secondary infestation were and plants previously infested by R. padi, they were
obtained ten days after each plant received two adults significantly more likely to settle on control plants
(Table 3). The density of nymphs also reflected this
Primary infestation
preference for control plants (Table 3).
Initial density Final density Secondary infestationa
0 0 68.9 ± 7.4
Discussion
5 39.5 ± 7.2 69.8 ± 6.4
10 108.0 ± 9.2 56.2 ± 6.0
Effects of aphid infestation on wheat seedlings were
25 287.5 ± 42.4 48.6 ± 5.6
species-specific. Specificity of elicitation (Stout et al.,
50 553.5 ± 41.8 55.4 ± 6.3
1998) was suggested by the contrasting responses of
a Analysis of variance; F = 2.11; df = 4, 44, P = 0.10, N = 9–
R. padi to plants that had been infested with simi-
10 replicate plants per treatment.
lar densities of either D. noxia or R. padi. Popula-
tion growth was reduced by previous R. padi infes-
The final population-growth experiment examined tation, and adults avoided both excised leaves and
whether the performance of D. noxia on previously in- whole plants that had been fed upon by R. padi. In
fested plants depended on the density of the previous contrast, the population growth of R. padi was un-
infestation. Adding 0, 5, 10, 25, or 50 Russian wheat affected by D. noxia infestation, and adults readily
aphids per plant produced wide variation in aphid den- colonized leaves and plants that had been fed upon
sity at the end of the primary infestation (Table 1). by D. noxia. Among aphids, specificity of elicitation
Subsequent population growth tended to be higher on could be mediated by differences in the composition of
plants that experienced the two lowest levels of pre- saliva (Prado & Tjallingii, 1997; Felton & Eichenseer,
vious infestation, but the effect of previous infestation 1999), which may generate different profiles of plant
on the population growth was not significant (Table 1). allelochemicals (Forslund et al., 2000; Ni et al., 2001).
The population growth of D. noxia was in fact sim- Specificity of effects can be detected by comparing
ilar on plants whose primary infestations differed by the responses of two or more herbivores to the same
five-fold (compare the 10- vs. 50-aphid treatments in change in the host plant (Tran et al., 1997). In our
Table 1). experiments, prior infestation by R. padi reduced its
own subsequent growth, but did not have a significant
Effects on feeding preferences. Adults of D. noxia effect on the growth of D. noxia. It is unclear why
were about two times more likely to settle and feed Russian wheat aphids were less sensitive to previous
on leaves from control plants than on leaves from R. padi infestation, but our results are consistent with
plants previously infested by D. noxia (Table 2). In field and greenhouse experiments in which the two
contrast, adults of R. padi were distributed equally aphid species were added to grasses simultaneously
on the two kinds of leaves. When presented control (Bergeson & Messina, 1997). In that study, the pres-
leaves vs. leaves previously infested by R. padi, adults ence of R. padi lowered the rate of increase of D. noxia
of both aphid species strongly preferred control leaves only when the former species reached extremely high
(Table 2). densities (a few thousand individuals per seedling).
The settling and reproduction of R. padi alates Perhaps the modification of leaf chemistry caused by
on whole plants mirrored their responses to excised D. noxia feeding renders this aphid less susceptible to
leaves. In each experiment, about half of the 20 alates induced defenses of cereals (Telang et al., 1999). In
per cage were recovered five days after they were particular, D. noxia appears to be less sensitive than
released. In the first experiment, alates showed no R. padi to hydroxamic acids, which are known to be
avoidance of plants previously infested by D. noxia; induced by R. padi infestation (Givovich & Niemeyer,
they were in fact slightly more common on previously 1995; Mayoral et al., 1996; Ni & Quisenberry, 2000).
infested plants (Table 3). As a consequence, nymphal Our experiments cannot exclude the possibility
densities were about 20% higher on plants previously that D. noxia is negatively affected by local R. padi
infested by D. noxia than on control plants, but this feeding, but does not respond to systemic effects. In
difference was only marginally significant (Table 3). the preference test, D. noxia adults avoided leaves
from R. padi-infested plants (Table 2), and some of48
Table 2. Mean number (± SE) of aphids settling on control leaves vs. leaves pre-
viously infested by the Russian wheat aphid (D. noxia) or the bird cherry-oat aphid
(R. padi). Counts were obtained 4 h after the release of ten adults per dish
Number of aphids / leaf
Primary Test species Control leaves Infested leaves ta P
infestation
D. noxia D. noxia 4.7 ± 0.5 2.4 ± 0.4 2.75 0.01
R. padi 5.1 ± 0.4 4.6 ± 0.4 0.61 0.55
R. padi D. noxia 3.5 ± 0.3 1.8 ± 0.4 2.58 0.02
R. padi 5.0 ± 0.5 2.6 ± 0.4 3.02 0.01
a Paired t test, N = 25 replicate dishes per test.
Table 3. Mean number (± SE) of bird cherry-oat aphids (R. padi) on control plants vs.
plants previously infested by the Russian wheat aphid (D. noxia) or R. padi. Counts
were obtained five days after the release of 20 alate adults per cage
Number of aphids / cage
Primary
infestation Aphid stage Control plants Infested plants ta P
D. noxia Adults 5.1 ± 1.0 6.4 ± 0.7 1.30 0.23
Nymphs 71.2 ± 13.7 92.6 ± 6.3 1.86 0.10
R. padi Adults 7.5 ± 0.9 3.4 ± 0.8 2.58 0.002
Nymphs 99.7 ± 11.0 51.1 ± 7.5 5.7049
induced responses has implications for the exogenous Felton, G. W. & H. Eichenseer, 1999. Herbivore saliva and its
application of plant elicitors (such as jasmonic acid) effects on plant defense against herbivores and pathogens. In:
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deter feeding by R. padi (Slesak et al., 2001); it would Fisher, M., 1987. The effect of previously infested spruce needles
not be surprising to find that the same exposure has on the growth of the green spruce aphid, Elatobium abietinum,
and the effect of the aphid on the amino acid balance of the host
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