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Flexible use of patch marks in an insect predator: effect
of sex, hunger state, and patch quality
YOSHITAKA NAKASHIMA, MAYUMI TESHIBA and
YOSHIMI HIROSE Institute of Biological Control, Faculty of Agriculture, Kyushu University, Japan
Abstract. 1. Patch marks that allow the subsequent avoidance of marked areas
may be used by small animals to increase foraging efficiency. This study is the
first to demonstrate the presence of a patch-marking system in insect predators.
Furthermore, the marking system is found only in females, and factors such as
hunger state and patch quality play a key role in determining whether a female will
re-investigate a self-marked patch.
2. Females of the insect predator Orius sauteri avoided areas where the female
itself had searched previously but did not avoid areas searched by conspecific
females when deprived of prey for 24 h.There was no evidence that males use such
a patch-marking system, indicating the presence of a sex difference in patch-mark
use.
3. Females did not discriminate between patches visited previously and patches
not visited when they were either well fed or when patches contained abundant prey.
4. The patch mark used by females was effective for 1 h and may be a reliable
indicator of a recently visited area in which prey have been depleted.
5. These results suggest that O. sauteri females have the flexibility to adjust their
behavioural responses to a previously searched area depending on their hunger
state and the availability of prey in their foraging environment.
Key words. Anthocoridae, foraging efficiency, patch mark, patch time, physio-
logical state, prey availability, sex difference.
Introduction
Organisms have a limited amount of time and energy
available to devote to foraging, growth, maintenance, and
reproduction (Stephens & Krebs, 1986; Bell, 1991; Cuthill &
Houston, 1997; Perry & Pianka, 1997). Foraging is one of
the most important activities of animals, and is linked to
their movement (Hassell & Southwood, 1978; Bell, 1990,
1991). Thus, it is important to know how organisms opti-
mise their use of time and energy. The benefits of a high
searching efficiency are that more time and energy can be
allocated to other activities such as reproduction and that
the risk of starvation decreases. The costs of inefficient
searching may include energy and time expended on move-
ment and increased predation risk. Hence, energy and time
may be taken away from other activities, and decrease
fitness.
Insects use several methods to increase resource searching
efficiency. For example, patch marking has been docu-
mented well in insect parasitoids that leave chemical markers
on substrates while searching. These marks allow them to
avoid areas visited previously by themselves or by conspe-
cifics (Price, 1970; Greany & Oatman, 1972; Sugimoto et al.,
1986; van Dijken et al., 1992; Ho
Èller & Ho
Èrmann, 1993;
Sheehan et al., 1993; Bernstein & Driessen, 1996). By avoid-
ing areas visited previously, females can improve their
searching efficiency because an area that has already been
visited by themselves or by other females is likely to contain
fewer unparasitised hosts than areas that have not been
visited. Furthermore, some parasitoid species seem to dis-
criminate between patches marked by themselves and by
conspecifics to avoid self-superparasitism (van Dijken et al.,
1992; Ho
Èller & Ho
Èrmann, 1993; Sheehan et al., 1993;
Bernstein & Driessen, 1996).
Correspondence: Yoshitaka Nakashima, Laboratory of
Entomology, Obihiro University of Agriculture and Veterinary
Medicine, Obihiro 080-8555, Japan. E-mail: nksm@obihiro.ac.jp
Ecological Entomology (2002) 27, 581±587
#2002 The Royal Entomological Society 581
Most insect predators search for prey mainly by walking
after finding prey habitats (i.e. plants). In complex environ-
ments, visiting areas searched previously should be more
time consuming for these insect predators than for other
insects that search by flying. Patch marking may therefore
be an effective system to save time devoted to foraging
activities, and insect predators may use a patch mark.
No study has examined the presence of patch-marking
behaviour in insect predators. The work reported here focused
on patch marking in an insect predator, to test whether a
patch-marking system enhances searching efficiency.
Although many studies have been devoted to the foraging
behaviour of insect predators (e.g. Dixon, 1959; Marks,
1977; Nakamuta, 1982; Murakami & Tubaki, 1984; Ettif-
fouri & Ferran, 1993), differences between the sexes in
foraging have received little attention. Several studies, how-
ever, have revealed that the foraging behaviours of male
and female predators often differ. Honek (1985) showed in
the field that Coccinella septempunctata L. males fly more
frequently between plants than do females and concluded
that this was because males had to spend more time search-
ing for females than for prey. Hemptinne et al. (1996)
demonstrated that females of a coccinellid modified search-
ing patterns in response to aphid density whereas males
did not. In this case, female coccinellids spent more time in
area-restricted searches and less time in extensive searches
when prey density was higher. This difference may result
from the fact that females must search for patches with
abundant prey that ensure high oviposition rates and
offspring survival, whereas male reproductive success is
linked more closely to the rate of encounters with receptive
females. These sex differences in foraging responses to
patch quality suggest differences in possible patch-marking
utilisation. Thus, the hypothesis that patch-marking
systems differ between male and female insect predators
was examined. In addition, it was determined whether insect
predators discriminate between marks left by themselves
and marks left by other individuals in the same manner as
some parasitoids (see above).
Recent theoretical studies have emphasised the impor-
tance of the forager's physiological state and environmental
variables for foraging decisions (Mangel & Clark, 1988;
Mangel, 1989; Mangel & Roitberg, 1989). Hunger is a
physiological factor affecting the foraging behaviour of
insect predators (Dixon, 1959; Mols, 1988; Sabelis, 1990;
Wallin & Ekbom, 1994). In addition, the quality of patches
exploited by insect predators influences their searching
behaviour (Dixon, 1959; Nakamuta, 1982) and is also an
important fitness factor (Evans & Dixon, 1986; Kan,
1988a,b; Hemptinne et al., 1992, 1993, 1996). Thus, it was
hypothesised that both physiological and environmental
factors might affect the patch-marking system of insect
predators, and whether the response to areas searched pre-
viously differed depending on the hunger levels and prey
availability of foraging environments was tested.
An insect predator, Orius sauteri (Poppius) (Hemiptera:
Anthocoridae), was used to explore a patch-marking-based
foraging system. Orius sauteri is a small predatory insect
that locates prey by walking on plants where prey may be
available. This species is an effective biological control
agent of the vegetable pest Thrips palmi Karny (Thysan-
optera: Thripidae) (Nagai, 1993; Ohno & Takemoto, 1997)
and inhabits annual plants and prey on small arthropods,
such as thrips, aphids, mites, and lepidopteran eggs (Yasu-
naga & Kashio, 1993; Yasunaga, 1997). These prey are
usually distributed patchily among host plants and do not
move rapidly between plants. Thus, it was expected that the
ability to avoid areas visited previously would enhance the
efficiency of foraging in O. sauteri.
The existence and function of a patch mark in O. sauteri
were investigated in a series of laboratory experiments. The
following questions were addressed: Do adult females and
males of O. sauteri use a patch mark to avoid areas visited
previously? For how long is the patch mark active? Can an
individual of O. sauteri discriminate between marks left by
itself and marks left by other individuals? Does the quality
of a patch visited (i.e. prey density) affect the use of patch
marks? How does hunger level affect the use of patch
marks? Based on the results, the function of patch mark
use by O. sauteri is discussed.
Materials and methods
Insects
An O. sauteri colony was initiated with adults collected
from eggplant gardens in Hisayama Town, Fukuoka Pre-
fecture, Japan (33380N, 130310E) in summer 1997. A
colony of Thrips palmi Karny as prey for O. sauteri was
established by collecting thrips from an eggplant field in
Sanyo Town, Okayama Prefecture (34460N, 134010E) in
summer 1993. Thrips palmi was reared on kidney bean
plants and O. sauteri was reared on kidney bean plants
infested by T. palmi and kept in plastic boxes
(50 70 46 cm). Both colonies were maintained at
25 1C and a LD 16 : 8 h photoperiod.
Fifth-instar O. sauteri nymphs were drawn from the
laboratory colony and reared individually to the adult
stage in glass vials (2.5 cm diameter, 7.0cm high) containing
30 second-instar larvae of T. palmi, a kidney bean leaflet
(1.5 1.5 cm), and filter paper (1.5 1.5 cm). The prey
larvae, leaflet, and filter paper were changed daily.
The number of prey provided was sufficient to satiate the
predators (Nakashima et al., 1996; Nakashima & Hirose,
1999). Teneral females were divided into two groups: virgin
and mated. Virgin females and males were reared in the
same manner as nymphs. To allow females to mate, 1 day
after emergence, a female was confined in a glass vial for
24 h with a male and 60 prey larvae to allow insemination,
then reared individually as described above. This procedure
ensures successful mating (Nakashima et al., 1996; Honda
et al., 1998). In addition, Orius adults of two hunger states
(well fed and starved) were prepared. Well-fed females were
4±5 days old and fed 30 second-instar T. palmi larvae on the
day before the experiment; starved females were 4±5 days
582 Yoshitaka Nakashima, Mayumi Teshiba and Yoshimi Hirose
#2002 The Royal Entomological Society, Ecological Entomology,27, 581±587
old and had been fed with 30 larvae per day for 3 or 4 days
then starved for 1 day prior to experimentation. All experi-
ments were conducted at 25 1C.
Experimental procedures
All experiments were conducted in an arena consisting of
a covered, glass Petri dish (diameter 6.0 cm, height 1.5 cm),
which was divided into two equal halves by the insertion of
a paper barricade (6.0 1.5 cm). One half served as a treat-
ment area in which a single O. sauteri adult was allowed to
walk for 30 min The barricade prevented the individual
from entering the other half of the arena, which served as
a control. Following the 30-min period, the released adult
and paper barricade were removed and the arena was ready
for a single bioassay.
Three experiments were performed using this arena
design. Experiment 1 sought to determine whether indivi-
duals responded to their own chemical mark and the mark
of a conspecific individual. To test the former, the same
individual removed from the arena with the barricade was
re-introduced immediately into the centre of the arena,
using a fine brush. To test the latter, a different individual
was released immediately into the centre of the arena.
All test individuals were observed for 10 min to determine
the time spent in either the control or treatment half of
the arena. Three categories were examined in both the self-
recognition and conspecific-recognition test: males, virgin
females, and mated females. With respect to the conspecific
test, males were tested with males, virgin females with virgin
females, and mated females with mated females. Addition-
ally, it was sought to determine the period of time during
which a patch mark might be active by withholding mated
females for 1 h before re-introducing the same individuals
into their respective arenas, and observing their movements
for 10 min, as described above. In expt 1, each trial was
replicated 20 times and all individuals were starved for
24 h before testing.
The aim of expt 2 was to investigate whether Orius
females avoid areas searched previously where prey existed.
To determine whether the quality of a patch being searched
by a female predator affects responses to an area visited
previously, second-instar larvae of T. palmi were introduced
into the experimental arena. Prey larvae used in this experi-
ment were killed by freezing at 20 C then maintained at
25 C for a few hours prior to the experiment. Twelve prey
larvae were placed in each side of the experimental arena.
An O. sauteri mated female deprived of prey for 24 h was
released into one side of the arena with the paper barricade
in place. After 30 min, the barricade and all prey were
removed and the same female was released into the centre
of the arena. Female behaviour was observed in the manner
described above, and each trial was replicated 20 times.
The aim of expt 3 was to determine the effect of hunger
state on patch mark utilisation. Mated females that were
provided with 30 prey larvae per day until the experiment
began were used. Experimental procedures were the same as
in expt 1, except for the hunger state of mated females.
Twenty replicates were tested in this experiment.
Statistical analysis
The durations of adult visits to each side of the Petri dish
were analysed using Wilcoxon's signed rank tests, with a
5%level of significance in all tests.
Results
Experiment 1
The residence time of starved females on the control area
was significantly longer than that on the treatment area,
both in mated and virgin females (n20, Wilcoxon's signed
rank test, z2.35, P<0.05 for mated females; z2.35,
P<0.05 for virgin females; Table 1). Residence times of
starved males on the treatment area and the control area
were indistinguishable statistically (n20, Wilcoxon's
signed rank test, z0.28, PNS; Table 1). These results
indicate that starved females of O. sauteri avoided the
area visited previously by themselves while starved males
did not.
Contrary to the responses of females to self-marks,
neither virgin nor mated females avoided the area visited
by other conspecifics (n20, Wilcoxon's signed rank test,
z0.20, PNS for mated females; z0.86, PNS for
virgin females). Males also did not avoid the area visited
by other conspecific males (n20, Wilcoxon's signed rank
test, z0.90, PNS; Table 1).
One hour after removal of a starved mated female
exposed to a treatment area, the residence time of the
same female released again did not differ between treatment
and control area (n20, Wilcoxon's signed rank test,
z0.52, PNS; Table 1).
Experiment 2
Residence times of starved, mated females did not differ
between treatment area and control area when prey were
introduced into the experimental arena during the adult
exposure periods (n20, Wilcoxon's signed rank test,
z0.26, PNS; Table 2).
Experiment 3
Contrary to the responses to self-marked areas of females
in expt 1, the residence time of well-fed females did not
differ significantly between treatment and control areas
(n20, Wilcoxon's signed rank test, z1.68, PNS;
Table 2).
Predator patch-marking 583
#2002 The Royal Entomological Society, Ecological Entomology,27, 581±587
Discussion
This is the first demonstration that an insect predator
deposits a patch mark that is used to avoid areas searched
previously. Furthermore, it is shown that only females use a
patch mark, and that the effectiveness of this mark depends
on two factors: the physiological state of the female and
the quality of the patch being searched. Female predators
deprived of prey spent much less time on a prey-deficient
area where they had searched previously than on newly
encountered areas (Table 1). Thus, females can discriminate
between areas searched previously and areas not searched
previously, and this discrimination is mediated via a patch-
marking chemical laid on the substrate by the female itself.
The chemical composition of the mark was not identified
but it clearly has a short active period (<1 h) (Table 1).
Because of this short active period, the mark deposited by
females is a reliable indicator of a prey-deficient area that
they have visited quite recently.
Sexual selection theory predicts that a female's reproduc-
tive success depends directly on the quality and quantity
of food resources whereas a male's reproductive success
generally increases as it mates with more females (Bateman,
1948; Trivers, 1972; Clutton-Brock & Parker, 1992). Detect-
ing high-quality patches can be advantageous to Orius
females in three ways: increased individual survival, higher
reproductive rates, and increased offspring survival (Naka-
shima, 1998). In contrast, for males, spending time in
patches where prey exist but females are absent will lessen
their chance of locating mates and decrease their fitness.
The use of a patch-marking system may therefore be highly
adaptive. In fact, several studies have shown that female
searching patterns are flexible and dictated by prey avail-
ability while males are not under such constraints (Inoue &
Matsura, 1983; Hemptinne et al., 1996; Nakashima, 1998).
Patch-marking systems will not be effective if prey move
into patches after the first visit of predators; systematic
searching is adaptive when prey are immobile or do not
Table 1. Mean residence times of starved Orius sauteri females and males on areas exposed to different types of O. sauteri females and males
(treatment area) and areas not exposed to O. sauteri (control) in choice situations. After a female or a male was exposed to the treatment area
without prey for 30 min, either the same individual (a, b) or a conspecific individual (c) was released into the experimental arena to measure
residence times. Tested individuals were introduced into the experimental arena immediately after exposure periods in (a) and (c) whereas
mated females were withheld for 1 h before re-introducing them into their respective arenas in (b).
Patch time (s) on
Treatment areas exposed to: treatment area control area SE P-valuey
(a)
Virgin female 215.2 384.9 30.5 0.019
Mated female 241.5 358.6 20.7 0.019
Male 303.0 297.0 20.8 0.778
(b)
Mated female 307.6 313.8 24.7 0.600
(c)
Virgin female 263.9 336.1 28.7 0.391
Mated female 294.9 305.1 23.6 0.841
Male 268.9 331.2 32.1 0.370
yWilcoxon's signed rank test.
Table 2. Mean residence times of mated Orius sauteri females on areas visited previously by themselves (treatment area) and areas not
exposed to females (control) in choice situations. After a mated female was exposed to the treatment area with prey (a) or without prey (b) for
30 min, the same individual was released immediately into the experimental arena to measure residence times. Tested females were starved (a)
or well fed (b).
Patch time (s) on
Hunger state of females exposed to
treatment area and its prey availability treatment area control area SE P-valuey
(a)
Starved female exposed to area 283.5 316.6 23.5 0.79
with prey
(b)
Well-fed female exposed to area 257.5 342.6 25.6 0.10
without prey
yWilcoxon's signed rank test.
584 Yoshitaka Nakashima, Mayumi Teshiba and Yoshimi Hirose
#2002 The Royal Entomological Society, Ecological Entomology,27, 581±587
move rapidly (Bernstein & Driessen, 1996). This is the case
for prey resources exploited by O. sauteri, such as thrips,
mites, and lepidopteran eggs. Compared with the prey
resources, however, O. sauteri females, which are resources
for males, have much greater mobility. Thus, male search-
ing in areas searched previously may not necessarily be
inefficient because Orius females may move into a patch
immediately after males have left the patch. Nakashima
(1998) demonstrated that O. sauteri females usually move
by walking among plants when they search for prey while
males appear to fly more frequently than females. Flying
behaviour of males may be more effective for searching for
females, which are relatively active. Flying also means that
males are less likely to re-encounter a recently searched
patch.
Orius sauteri females responded to areas searched pre-
viously depending on their hunger state and the availability
of prey in areas to which they were exposed, and only
starved females searching in areas without prey use the
patch-marking system (Tables 1 and 2). Environmental
and physiological factors are important sources of varia-
bility affecting search behaviours (Bell, 1991). Dynamic state
variable models predict that prey availability in patches
and nutrient or energetic budgets will reflect the forager's
condition relative to its various needs, and accordingly
foragers behave to maximise their lifetime reproductive
success (Mangel & Clark, 1988). This theory seems to hold
true for patch mark use of O. sauteri. The work reported
here shows that prey availability and hunger state can act as
factors determining whether O. sauteri females use their
patch-marking system. The flexible switching according to
physiological and environmental conditions is likely to be
favoured by the need to search for prey; starved females
that are searching in an unprofitable environment face the
difficult situation under which they may starve to death or
suffer reduced reproduction if they are unable to find prey.
The flexible system may be adaptive for O. sauteri females
to search efficiently for prey because their natural habitats
(annual plants) have complex structures, and prey resources
are usually distributed patchily.
The mechanism underlying avoidance behaviours of
O. sauteri females depending on their hunger state and
availability of prey is not clear, however possible mechan-
isms may be that hunger states and/or the presence of prey
affect the deposition of patch marks, the response to patch
marks, or both. To reveal the mechanism of flexible use of
patch marks, it will be necessary to identify the chemical
substance involved and to determine whether the deposition
of marks depends on hunger state and prey availability.
In the present study, there was an inherent problem in
manipulating hunger states: partitioning the separate effects
of prey deprivation (i.e. hunger state, experience with prey,
egg load, and life expectancy) on foraging behaviour is
difficult experimentally in the similar context of studies
of parasitoids and fruit flies (Rosenheim & Rosen, 1991;
Minkenberg et al., 1992; Heimpel & Rosenheim, 1995).
Although other internal states covarying with hunger levels
may influence behaviour, it can be concluded that prey
deprivation clearly affects the individual's response to a
patch mark. This is the first demonstration that prey depri-
vation and patch quality influence the use of patch marking.
Parasitoid females avoid severe offspring competition
caused by self or conspecific superparasitism via the use
of a marking pheromone (Godfray, 1994). Patch-marking
behaviour is thought to be a response to the potential
profitability of a patch or host: rewards in terms of repro-
ductive success are higher on unexploited patches than
on exploited patches. Contrary to most parasitoids that
respond to areas exploited by conspecifics, the results of
expts 1 and 3 show that O. sauteri females avoid only self-
marked areas and do not avoid the area marked by con-
specifics (Table 1). It is difficult to draw conclusions from
such limited data about individual specificity of the mark,
however two hypotheses may explain the use of individual-
specific marks. (1) It may not be advantageous for a female
searching a patch without prey to inform conspecific
females (potential competitors) about the status of patches,
as suggested by Ho
Èller and Ho
Èrmann (1993). (2) The patch
mark left by a female may include only individual-specific
information to increase foraging efficiency because marking
decisions are influenced by prey deprivation and patch
quality (foraging history of each female) as described
above. Thus, conspecific marks may be less valuable as
information other than to the female that deposited them.
Although this remains to be determined, it can be concluded
that the patch mark should be an effective system for
searching for prey.
Acknowledgements
We thank Drs J. A. Rosenheim, J. Y. Honda and T. Ueno
for their valuable comments. We are grateful to Naomi
Nakamuta for her assistance in carrying out experiments.
This work was partly supported by a Research Fellowship
(to Y.N.) through the Japan Society for the Promotion of
Science.
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Accepted 12 January 2002
Predator patch-marking 587
#2002 The Royal Entomological Society, Ecological Entomology,27, 581±587
