Ecological Entomology (2006) 31, 155–161
Effects of leaf nitrogen content on oviposition site
selection, offspring performance, and intraspecific
interactions in an omnivorous bug
R O N N Y G R O E N T E M A N 1 , M O S H E G U E R S H O N 2 and M O S H E
C O L L Department of Entomology, The Hebrew University of Jerusalem, Israel
Abstract. 1. Oviposition site preference and its relation to offspring performance have received much attention in studies of herbivorous insects. Although
this relationship is of great ecological significance, its presence in predacious and
omnivorous insects has hardly been explored. When selecting an oviposition site,
omnivores are expected to respond to both prey availability and, even more
strongly, to plant traits that affect both females and their offspring.
2. In this study, females of Orius albidipennis (Heteroptera: Anthocoridae)
showed a strong preference for oviposition at the vein origin site of cotton leaves.
It appears that this site is a limited resource for ovipositing females, because they
defend it against conspecific intruders. This defensive behaviour was significantly
more pronounced on nitrogen-rich than nitrogen-poor plants.
3. The females’ defensive behaviour on nitrogen-rich leaves corresponds with
offspring performance; the nymphs developed faster and enjoyed higher survival
on nitrogen-rich than on nitrogen-poor leaves. At the between-plant level, oviposition preference was not significantly correlated with offspring performance, and
egg hatching rate did not differ significantly between nitrogen treatments.
4. Oviposition site selection by this omnivorous bug appears, however, to be
correlated positively with offspring performance at the within-leaf level. This is
supported by the significantly higher hatching success of eggs deposited at the
preferred vein origin site as compared with those deposited on other parts of
the leaf.
Key words. Omnivore–plant interactions, omnivory, Orius albidipennis, oviposition
preference–offspring performance, resource guarding.
Introduction
The relationship between oviposition site selection by
adults and the performance of their offspring has received
much attention in the ecological literature (Craig et al.,
Correspondence: Ronny Groenteman, School of Biological
Sciences, University of Canterbury, Private Bag 4800, Christchurch,
New Zealand. E-mail: [email protected]
1
Present address: School of Biological Sciences, University of
Canterbury, Private Bag 4800, Christchurch, New Zealand.
2
Present address: Department of Zoology, George S. Wise Faculty
of Life Sciences, Tel Aviv University, Ramat Aviv, Tel Aviv,
69987, Israel.
# 2006 The Authors
Journal compilation # 2006 The Royal Entomological Society
1989; Thompson & Pellmyr, 1991). It has been argued
that eggs should be deposited where optimal conditions
exist for the offspring (Jaenike, 1978). This linkage between
oviposition preference and offspring performance is
expected particularly when parental care is absent and offspring mobility is low. Under such conditions, offspring
fitness should be correlated strongly with characteristics
of the egg deposition site. Indeed, a positive correlation
between female preference for oviposition sites and offspring performance was detected in many studies, primarily
for herbivorous insects (Craig et al., 1989; Stein & Price,
1995; Craig & Ohgushi, 2002). In some cases, however, no
such correlation was detected (some recent examples
include Berdegue et al., 1998; Lamb et al., 2003; Scheirs
et al., 2003, and references therein). One possible
155
156 Ronny Groenteman, Moshe Guershon and Moshe Coll
explanation for this lack of correlation was offered by
Scheirs et al. (2000), who pointed out that females act to
maximise their fitness not only through offspring performance, but through their own performance as well.
Whitham (1978, 1980) found that females of the gall
aphid Pemphigus betae indeed maximise their overall
fitness; stem mothers prefer to establish galls at sites on
the leaves that support more offspring. Adult females
should therefore preferentially inhabit host plants that will
increase their own longevity and fecundity rather than
those that improve offspring performance (Evans, 1976;
Coll & Ridgeway, 1995; Nakashima & Hirose, 1999). A
conflict could result when, for example, the nutritional
needs of ovipositing females and their offspring are not
the same (Evans, 1976).
While much is known about the relationship between
oviposition preference and offspring performance in herbivorous insects (Jaenike, 1978; Thompson, 1988; Craig
et al., 2000; Scheirs et al., 2000; Kanno & Harris, 2002),
relatively little is known about this relationship in predators. Some predators deposit their eggs where prey is concentrated (Hagen et al., 1999). Others oviposit away from
prey (Schellhorn & Andow, 1999), possibly relying on the
high mobility of the hatching young. However, a rigorous
exploration of the relationship between offspring mobility
and oviposition strategy in predators has not yet been
attempted. Even less is known about the oviposition
preference–offspring performance relationship in omnivorous
insects that feed on both prey and plant food sources (but see
Coll, 1996). Omnivory is widespread in nature, and may be
exhibited by most consumers during at least one of their life
stages (Pimm & Lawton, 1978; Whitman et al., 1994; Coll &
Guershon, 2002). These consumers are therefore expected to
respond to both plant characteristics and prey availability
when choosing an oviposition site.
Nitrogen content of host plants often limits the development and fecundity of herbivorous insects (McNeill &
Southwood, 1978; Denno & Roderick, 1990) and there is
much evidence to indicate the preference of insects for
nitrogen-rich plants (e.g. Valladares & Lawton, 1991;
Kyto et al., 1996; Jauset et al., 1998; Barros & Zucoloto,
1999). Little is known, however, about the effect of nitrogen content on oviposition site selection in omnivorous
insects. It is not clear, for example, whether omnivorous
consumers that feed on nitrogen-rich prey are responsive to
variations in nitrogen content of their food plants.
Plant chemical composition influences omnivore performance through nutritional and allelochemical effects
(see examples in Naranjo & Gibson, 1996; Coll, 1998; Coll
& Guershon, 2002). Additionally, plant tissue structure
affects the ability of omnivores to feed on and oviposit in
plant materials. Unlike strict predators, omnivorous females
are able to evaluate the nutritional and structural properties
of the oviposition substrate, the plant. Plant characteristics
are especially important to the performance of omnivore
offspring, because many of them feed exclusively on plant
material during the first nymphal stages (Parker, 1981). It
was therefore hypothesised that omnivorous females
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#
strongly prefer to deposit their eggs on plants of high nutritional value for their offspring. This prediction was tested by
manipulating the quality of cotton plants using different
nitrogen fertilisation regimes, and quantifying its effect on
female oviposition and offspring performance in the omnivorous bug Orius albidipennis Reuter (Heteroptera:
Anthocoridae). The relation between omnivore oviposition
preference and offspring performance was tested on two
spatial scales, between plants of different nutritional value,
and between areas within a leaf. Whether preferred oviposition sites are limited was inferred in this study from intraspecific interactions among gravid females at these sites.
Materials and methods
Plants and insects
Cotton plants, Gossypium hirsutum (cv. Acala SJ2),
were grown individually from seeds in an inert rooting
mixture (Vermiculite 2Ò) in 200-ml pots in the greenhouse.
An O. albidipennis culture was established from about 50
females that were collected in the spring of 2000 from
sunflower heads in the Arava valley in southern Israel,
and maintained at 25 1 C, 70 10% RH, and LD
16:8 h following the protocol of Schmidt et al. (1995).
In the culture, the omnivores were fed Ephestia kuehniella
Zeller (Lepidoptera: Pyralidae) eggs. Bean pods were
provided for moisture, to supplement the bugs’ diet, and
to serve as an oviposition substrate.
Female behaviour
To assess the significance of different leaf areas for
O. albidipennis females, their behaviour on leaves was
observed. To that end, we randomly collected seven 6 1-day-old mated females from the colony and placed them
individually on intact cotton leaves, in ventilated Petri dishes.
Four Helicoverpa armigera eggs were offered to the females as
prey on the underside of each leaf and the bugs were then
observed continuously for 8 h. Time allocated by the females
for walking, standing, feeding, and other behaviours (mainly
preening) was recorded. The location of the females, whether
on the upper or lower leaf surface, at the vein origin site, on
the leaf lamina, or on the dish, was also noted. w2 tests (SAS,
2001) were used to compare event frequencies.
Leaf nitrogen content
Cotton plants were irrigated with tap water until the threenode stage, and then assigned randomly to either rich or poor
nitrogen fertilisation regime. The composition of the watering
solutions is provided in Table 1 (following Epstein, 1972).
Leaf nitrogen content was determined for eight randomly
selected leaves from each treatment, following methods
described by Smith (1980).
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2006 The Royal Entomological Society, Ecological Entomology, 31, 155–161
Oviposition site selection by an omnivore
Table 1. Composition of irrigation solutions used to manipulate
nitrogen content of cotton leaves.
Nitrogen poor
Component
Nitrogen rich
(concentration in M) (ml l–1 distilled water) (ml l–1 distilled water)
2.0 KNO3
1.0 Ca(NO3)2
1.0 MgSO4
1.0 (NH4)H2PO4
1.0 KCl
1.0 CaCl2
1.0 NaH2PO4
KoratineÒa
3.0
4.0
1.0
2.0
–
–
–
0.1
–
–
1.0
–
3.0
4.0
2.0
0.1
a
Contains the following microelements (g l–1): Fe, 5.5; Mn, 2.7;
Zn, 1.35; Cu, 0.2 and Mo, 0.5.
Oviposition site selection
To evaluate the effect of leaf nitrogen content on the
within-leaf oviposition site selection, we randomly collected
20, 6 1-day-old mated O. albidipennis females from the
culture and placed them individually in Petri dishes
containing an intact nitrogen-rich cotton leaf or a nitrogenpoor leaf. The females were supplied with E. kuehniella eggs
ad libitum and were allowed to oviposit for 6 days.
To prevent cannibalism on newly hatched nymphs by
adult females, the leaves were replaced on the third day of
the experiment. At the end of the experiment, the number
of eggs and their location on the leaves were recorded. Two
zones were recognised on each leaf: the vein origin within a
0.5 cm radius from the petiole, and the rest of the leaf
lamina. The area of each leaf zone was measured and
used to calculate egg density per cm2 per day per female.
Cumulative number of eggs deposited per female per day at
the two leaf zones was also calculated. Data were analysed
using ANOVA with a split-plot model (SAS, 2001), with
nitrogen treatment as the whole plot effect, and leaf zone
as the subplot level. Egg-bearing leaves were observed for
an additional 5 days to determine hatching rate. These
results were then analysed together with results of the egg
hatching experiment below.
Egg hatching success
To determine differences in hatching rate between eggs
deposited at the two leaf zones, single O. albidipennis
females were placed together with intact leaves from either
one of the two nitrogen treatments (seven nitrogen-rich and
nine nitrogen-poor leaves) in Petri dishes. The females were
allowed to oviposit for 3 days. The number of eggs deposited in the two leaf areas (vein origin and leaf lamina) was
determined for each female. The eggs were allowed to hatch
for five additional days, after which the hatching success
(proportion of hatched eggs) in different zones of nitrogenrich and nitrogen-poor leaves was determined. To assess
the effects of nitrogen fertilisation regime and oviposition
157
site on hatching success, data were arcsine of square root
transformed to homogenise variances and then subjected to
ANOVA with a split-plot model (nitrogen treatment as the
whole plot and leaf zone as the subplot) (SAS, 2001).
Nymph performance
In this experiment, the effect of leaf nitrogen content on
offspring performance was evaluated. Nymph performance
at the vein origin site and the leaf lamina were not compared, because this comparison is not likely to be of biological importance in view of the high mobility of the
nymphs. Bean pods bearing 2 1-day-old eggs were
collected from the O. albidipennis culture and held at
25 1 C until nymphs emerged. The pods were inspected
every 2 h, and newly hatched nymphs were used in the
experiment. Intact nitrogen-rich and nitrogen-poor leaves
were enclosed singly in Petri dishes at 25 1 C. On each
leaf, four first-instar nymphs were enclosed individually in
plastic tubes (0.12 cm diameter 0.7 cm height) attached
to the underside of the leaf with modelling clay. This way,
the nymphs were held individually to prevent cannibalism.
The nymphs were inspected every 4–10 h over the course
of 2 days. At each inspection, survival (alive or dead) and
developmental stage (first or second stadium) were
recorded for each nymph. The observations were terminated when a nymph reached the second stage, which was
recognised by a change in body shape and transparency,
and the presence of exuvium. The experiment was replicated three times for a total of 12 nymphs for each nitrogen
fertilisation treatment. Per cent mortality on nitrogen-rich
and nitrogen-poor leaves was analysed using ANOVA with
nymphs nested within leaves. Duration in hours of the first
instar on the two nitrogen treatments were compared with a
Student t-test (SAS, 2001).
Female survival
Female survival on nitrogen-rich and nitrogen-poor
leaves was recorded daily during the oviposition site selection experiment above. As stated, the 20, 6 1-day-old
females were provided with E. kuehniella eggs ad libitum
and were held individually for 6 days on either nitrogenrich or nitrogen-poor cotton leaves. The females had no
opportunity to cannibalise nymphs because leaves were
replaced before egg hatching. Female Orius do not feed on
conspecific eggs that are imbedded in leaf tissue (Collyer,
1953; Askari & Stern, 1972; R. Groenteman, pers. obs.).
Female survival on nitrogen-rich and nitrogen-poor leaves
were compared using a Student t-test (SAS, 2001).
Intraspecific interactions
Interactions between O. albidipennis females were recorded
to assess whether preferred leaf settling sites constitute a
# 2006 The Authors
Journal compilation # 2006 The Royal Entomological Society, Ecological Entomology, 31, 155–161
158 Ronny Groenteman, Moshe Guershon and Moshe Coll
limited resource for the females. Mated, 6 1-day-old
female bugs (n ¼ 20) were randomly collected from the
culture and placed individually in Petri dishes (9 cm
in diameter) containing an intact either nitrogen-rich or nitrogen-poor cotton leaf. After a 20-min acclimation period,
during which most females settled on the leaves, a second
female, labelled as the intruder, was introduced into each
dish. Interactions between the two females were observed
and the outcome was recorded. The female that remained
at the interaction site was declared the ‘winner’, while the
one that left the site was designated the ‘loser’. When both
females remained or both left the site, a draw was declared.
The proportion of spontaneous settling at the vein origin
site and the proportion of victories achieved by owners and
intruders on nitrogen-rich and nitrogen-poor leaves were
analysed using w2 tests (SAS, 2001). Relative size of the
interacting females, expressed as head and prothoracic
widths and the length of the fore tibia, was recorded, and
the correlation of these parameters with interaction outcome was w2 tested (SAS, 2001) for the effect of size on the
likelihood of winning the interaction.
Results
Egg hatching success
Hatching success was significantly higher at the vein
origin site than on the leaf lamina in both nitrogen regimes.
Whereas 59.9 8.6% and 60.8 8.7% of the eggs in the
vein origin site hatched on nitrogen-rich and on nitrogenpoor leaves respectively, only 29.7 8.6% and
30.2 8.7% of the eggs hatched on the leaf lamina of
nitrogen-rich and nitrogen-poor leaves respectively
(F1,36 ¼ 15.83, P < 0.001). Nitrogen fertilisation regime
did not affect hatching success significantly (F1,32 ¼ 1.88,
P ¼ 0.18) and there was no significant interactive effect
between nitrogen regime and leaf site (F1,36 ¼ 0.159,
P ¼ 0.69).
Nymph performance
Duration of the first instar was significantly shorter on
nitrogen-rich than on nitrogen-poor leaves (20.7 2.7 and
38.9 4.3 h
respectively;
t5 ¼ 3.59,
P ¼ 0.016).
Although nymphs survived longer on nitrogen-rich than
on nitrogen-poor leaves (41.39 4.7 and 31.52 4.44 h
respectively), this difference was not statistically significant
(F1,20 ¼ 2.57, P ¼ 0.137).
Female behaviour
Standing on the underside of the leaf was the most
frequent behaviour exhibited by the females; it occurred in
73% of the events (w23 ¼ 42.97, P < 0.001). In 40% of the
cases where females stood on the underside of the leaves,
they did so at the vein origin. These results indicate that
females occupy the vein origin site over 30 times
more frequently than would be expected based on the differences in size between the vein origin and leaf lamina sites.
Female survival and behaviour
Female survival time did not differ significantly on leaves
from the two nitrogen regimes (4.2 0.39 and
3.2 0.39 days on nitrogen-rich and nitrogen-poor leaves
respectively; t39 ¼ 1.59, P ¼ 0.12).
Intraspecific interactions
Leaf nitrogen content
Fertilisation regime had a significant effect on leaf nitrogen
content (t14 ¼ 11.31, P < 0.001). Leaves of plants grown
under a poor regime had a significantly lower nitrogen level
than those that received nitrogen-rich fertilisation
(mean SE: 1.49 0.08% and 2.59 0.077% nitrogen of
dry weight respectively).
Mated O. albidipennis females displayed a tendency to
settle spontaneously at the vein origin site. This tendency
(measured as frequency of settling events) was stronger
on nitrogen-rich leaves than it was on nitrogen-poor
ones (w219 ¼ 3.2, P ¼ 0.07 and w219 ¼ 1.8, P ¼ 0.18
Table 2. Density (means 1 SE) of Orius albidipennis eggs deposited in two areas of cotton leaves grown under two nitrogen fertilisation regimes.
Eggs (no. cm2)a
Oviposition site selection
Females deposited significantly more eggs per leaf area at
the vein origin site than on the lamina (F1,18 ¼ 45.19,
P < 0.001, Table 2). Nitrogen fertilisation regime did not
significantly affect the overall number of eggs deposited per
female per day (1.68 0.27 and 1.46 0.27 on nitrogenrich and nitrogen-poor leaves respectively; F1,18 ¼ 0.501,
P ¼ 0.488), and no significant interaction was detected in
the effects of nitrogen level and leaf site on oviposition rate
(F1,18 ¼ 0.33, P ¼ 0.575).
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#
Site on leaf
Area (cm2)
Nitrogen rich
Nitrogen poor
Vein originb
Leaf laminac
0.196
12.37
4.58 0.99a
0.04 0.01b
5.12 0.96a
0.03 0.01b
a
Values within columns followed by the same letter do not differ
significantly (Student t-test, P < 0.001). Values within rows do not
differ significantly.
b
An area of 0.5 cm diameter tangent to the petiole.
c
An area 4 cm diameter tangent to the petiole, excluding the vein
origin site.
# 2006 The Authors
2006 The Royal Entomological Society, Ecological Entomology, 31, 155–161
Oviposition site selection by an omnivore
respectively). Moreover, females that settled at the vein
origin site on nitrogen-rich leaves prevailed in conspecific
contests significantly more often than did the invading
females. This, however, was not the case on nitrogen-poor
leaves; on these leaves, settled and invading females had a
similar chance of winning conflicts (w219 ¼ 6.25, P ¼ 0.01
and w219 ¼ 2.57, P ¼ 0.1 on nitrogen-rich and nitrogenpoor leaves respectively). The relative size of the interacting
females did not correlate with their chance of winning.
Larger females were not more likely to win the interaction
on both nitrogen-rich and nitrogen-poor leaves. w2 values
for differences in prothoracic size are given; head and fore
tibia sizes act in the same manner (w21 ¼ 2.2, P ¼ 0.14 and
w21 ¼ 0.03, P ¼ 0.88, on nitrogen-rich and nitrogen-poor
leaves respectively).
Discussion
In this study, O. albidipennis females showed a strong
preference for oviposition at the vein origin sites of cotton
leaves. Results indicate that oviposition site selection by
this omnivorous bug is correlated positively with offspring
performance at the within-leaf level.
Nitrogen content of cotton leaves did not affect oviposition rate by O. albidipennis; a similar number of eggs were
deposited per female on nitrogen-poor and nitrogen-rich
plants. In another omnivorous anthocorid, Anthocoris confusus, however, young bean pods were preferred over old
pods for oviposition (Evans, 1976), perhaps in response to
a difference in nitrogen content in old vs. young plant
tissues (Mattson, 1980). Although no significant effect of
leaf nitrogen content on egg deposition was detected in the
present study, first-instar O. albidipennis nymphs developed
more rapidly and survived longer on nitrogen-rich leaves
than on nitrogen-deficient ones. Several studies on omnivorous Heteroptera have shown that the quality of the food
plant greatly affects the performance of young nymphs.
For example, Naranjo and Stimac (1985) showed that low
quality food plants (foliage) enabled Geocoris punctipes to
develop only to the second instar, while higher quality
plants (bean pods) allowed the development up to the
third instar.
Contrary to its effect on the young nymphs, leaf nitrogen
content did not have a significant effect on female longevity
or egg deposition. This result may be attributed to the free
access the females had before the experiment to prey, a
high nitrogen food source. Evans (1976) suggested that
A. confusus females insert their rostrum into plant tissue to
determine the suitability of the plant for oviposition. In Orius
insidiosus, which feeds mostly in the xylem with some
evidence of mesophyll feeding (Armer et al., 1998), both
moisture and nutrient levels could be detected by the females.
Data show that significantly more eggs were deposited
per cm2 at the vein origin site than on the leaf lamina. The
ability of O. albidipennis females to distinguish between
structures within the leaf and preferentially deposit their
eggs at particular sites appears to be correlated with egg
159
hatching success. It seems that the eggs are inserted into the
most succulent part of the leaf to reduce risk of desiccation
(Richards & Schmidt, 1996). A similar preference for
petioles and main leaf veins as oviposition sites has been
reported for other Orius species (Askari & Stern, 1972;
Tawfik & Ata, 1973a, b; Richards & Schmidt, 1996).
These results suggest therefore that oviposition site selection is influenced primarily by water balance rather than
nutritional requirements, because leaf nitrogen level did not
have a significant influence on the number of deposited
eggs or on their hatch rate. That the females select oviposition sites that maximise the hatch rate of deposited eggs
rather than to optimise nymph performance may be related
to the high mobility of the neonates and their ability to
search for food away from the egg hatching site. Nymphal
food may include not only prey items but also plant material, such as pollen (Kiman & Yeargan, 1985; Cocuzza
et al., 1997; Vacante et al., 1997). In the gall aphid
Pemphigus betae, in contrast, nymphs are totally restricted
to their gall and cannot alter their feeding site until adulthood. In a classic study, Whitham (1978, 1980) demonstrated that females show strong preference for
oviposition (gall forming) sites on the leaf most suitable
for the nymphs. Aggregated aphid nymphs often exhibit
mutual facilitation to increase the quality of their food
source (Freese & Zwölfer, 1996). In strict predators and
in omnivores, however, preference for optimal oviposition
sites may be counteracted by potential aggressive and
cannibalistic behaviours.
The preference of O. albidipennis for the vein origin site
of the leaf was also apparent from the behaviour of
females. Mated females were frequently observed standing
at the vein origin site on the lower surface of cotton leaves.
Orius tristicolor has also been reported to prefer this resting
site (Shields & Watson, 1980). The bugs actively seek the
vein origin site, and once it is found they remain there,
inactive, for extended periods. Furthermore, mated
O. albidipennis females that spontaneously settled at the
vein origin site of cotton leaves actively defended it against
other females. These antagonistic interactions were significantly stronger on the nitrogen-rich leaves. That the
females primarily defend the vein origin site as an oviposition site rather than a resting site is strongly suggested by
preliminary data that indicate that males and unmated
females do not settle spontaneously at this site and are
not likely to defend it successfully (R. Groenteman and
M. Guershon, unpublished data). Aggressive interactions
for preferred reproduction sites on the leaves were also
recorded for the gall aphid P. betae (Whitham, 1980).
Unlike the current study, however, female size mediated
contest outcome, with larger stem mothers usually taking
over the preferred site on the leaf. In the current study,
variation in size between gravid females appears to be less
important for contest outcome, maybe because of their
predatory habits.
The insertion of the eggs in plant tissue may protect them
not only from desiccation, but from predation as well. In
Anthocoris confuses, another family member with a similar
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Journal compilation # 2006 The Royal Entomological Society, Ecological Entomology, 31, 155–161
160 Ronny Groenteman, Moshe Guershon and Moshe Coll
oviposition strategy, eggs that were deposited loosely on
the plant surface were preyed upon by the ovipositing
females themselves (Evans, 1976). In this species, which is
apparently more prey-dependent than Orius sp., more loose
eggs are deposited and higher egg predation occurs when
prey is scarce. In a companion study, it was observed that
female O. albidipennis deposit more loose eggs on the leaf
surface when more females compete for the preferred oviposition site, the vein origin (R. Groenteman, pers. obs.).
These eggs may then be more vulnerable to predation. The
guarding behaviour exhibited by females at the vein origin
site is likely to reduce the number of loose eggs and result in
clustered deposition of sibling eggs. It would be interesting
to investigate the impact of egg clustering, either sibling or
conspecific, on female reproductive success.
Strict predators rely on a nitrogen-rich prey diet, and
ovipositing females may therefore respond to prey availability. In many cases, however, prey availability varies greatly
in space and time, making it difficult for ovipositing females
to predict prey availability for their offspring. Omnivores,
however, feeding on both plants and prey, may capitalise on
their ability to assess the quality of plant resources, as these
often change more slowly than does prey availability.
Omnivores may therefore respond primarily to variations
in host-plant quality, which may be a better predictor of
nymph performance. Further, omnivores and their herbivorous prey may respond in similar ways to variations in
plant quality, resulting in a spatial or temporal overlap in
their distributions. A similar oviposition strategy is probably exhibited by at least some of the strict predators and the
omnivores that were found to oviposit near prey aggregations; they may actually be responding to variations in plant
quality, be it by taste (in omnivores) or smell, in a way
similar to that of their herbivorous prey. Oviposition site
selection that enhances offspring performance in omnivores
and strict predators is likely to greatly influence their ability
to suppress prey populations on various host plants.
Acknowledgements
We thank T. Yuval and A. Yigael for technical assistance,
R. Yonah for help with manuscript preparation, and R.
Yonah, B. Yuval and two anonymous reviewers for valuable comments on its drafts.
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Accepted 18 August 2005
# 2006 The Authors
Journal compilation # 2006 The Royal Entomological Society, Ecological Entomology, 31, 155–161