The choice of probing sites by Bracon hebetor Say (Hymenoptera: Braconidae) foraging for Ephestia kuehniella Zeller (Lepidoptera: Pyralidae)

Journal of Stored Products Research 39 (2003) 265–276

The choice of probing sites by Bracon hebetor Say (Hymenoptera: Braconidae) foraging for Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) Essam Darwish, M. El-Shazly*, H. El-Sherif Department of Entomology, Faculty of Science, Cairo University, Giza, Egypt Accepted 16 November 2001

Abstract A direct behavioral assay was conducted to investigate the preferred habitat for host searching by the parasitoid Bracon hebetor (Hymenoptera: Braconidae). The effects of mating, feeding and post-emergence experience on female parasitoid choices of searching sites were also examined. B. hebetor appears to be directed to the habitat of its host through chemical cues originating from the host larvae, frass and adults. These cues elicit a series of directed responses by the female. Generally, the data showed that flour containing 30-day-old larvae was preferred by B. hebetor females. This was followed by the flour containing the frass, then the adult host, and finally the flour containing 10-day-old larvae. It appears that cues produced by young larvae were the weakest whereas cues produced by older ones were the strongest. Feeding seemed to be important in the location of the proper searching site. Although the cues were normally learned by the immature stages of the parasitoid, and were subsequently manifested in their responses as adults, adult experience increased the ability of the parasitoid to locate the suitable habitat for searching. r 2002 Elsevier Science Ltd. All rights reserved. Keywords: Bracon hebetor; Ephestia kuehniella; Foraging; Probing; Feeding; Mating; Experience

1. Introduction The cues that parasitoids use to locate their hosts have important ramifications on their potential for use as biological control agents (Lewis et al., 1990). Indeed, a parasitoid that forages efficiently has more time for feeding, selection of higher quality mates, selection of higher quality hosts and reduces the risk of predation (Mangel, 1987, 1989; Volkl and Mackauer, 1993; *Corresponding author. Tel/fax.: +20-23-83-4243. E-mail address: [email protected] (M. El-Shazly). 0022-474X/02/$ - see front matter r 2002 Elsevier Science Ltd. All rights reserved. PII: S 0 0 2 2 - 4 7 4 X ( 0 2 ) 0 0 0 2 3 - 1

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Heimpel et al., 1997). Foraging efficiency is enhanced through the use of cues associated with the host (Arthur, 1971; Corbet, 1971) and by the parasitoid gaining experience prior to release (Prokopy and Lewis, 1993; Hare et al., 1997; Morgan and Hare, 1998). Much of the older literature suggested that hosts were found through random searching, particularly once a suitable habitat has been located (Cushman, 1926; Clausen, 1940; Sweetman, 1963; Debach, 1964). This idea has been reflected in many ecological models of host location and finding (Royama, 1971; Rogers, 1972). Doutt (1964) divided the process that results in successful parasitism into four steps: (a) host habitat location, (b) host location, (c) host acceptance, and (d) host suitability. Bracon hebetor Say (Hymenoptera: Braconidae) is a cosmopolitan gregarious larval ectoparasite on many lepidopterous pests attacking stored products in Egypt (Awadallah et al., 1985). It is found associated with pyralids including the stored product pest, Anagasta (Ephestia) kuehniella Zeller. E. kuehniella is a common pest of stored products; it is also used as a laboratory host or prey for various parasites and predators reared for release in the biological control of other pests (Farghaly and Ragab, 1985; El-Shazly and El-Sebaey, 1997). Although many investigations have been conducted on the behaviour of this wasp (Fukushima et al., 1989; Strand et al., 1989; Antolin and Strand, 1992; Shonouda and Nasr, 1998), there is a lack of information about the effects of physiological conditions and post-emergence experience on its searching behaviour. Therefore, the specific objective of the present work is to determine the effects of feeding, mating and experience on the choice of probing sites of B. hebetor. 2. Materials and methods The Mediterranean flour moth E. kuehniella and the ectoparasite B. hebetor used in the present study were obtained from the Centre of Agricultural Research, Ministry of Agriculture and Land Reclamation, Giza, Dokki. A laboratory culture of E. kuehniella was reared in glass jars on whole-wheat flour previously heated in order to ensure the absence of any infestation. Every week, females were allowed to oviposit by transferring them to new ovipositional jars for 24 h, so that all larval ages would be available during the experiments. The stock culture of the parasite B. hebetor was reared on 25–30-day-old host larvae in cylindrical glass jars (10 cm  17 cm) containing infested flour. In order to study the effect of the different combinations of feeding, mating and previous experience on the choice of probing sites, newly hatched female parasitoids were divided into 8 categories: Group 1: (a) Mated–fed–na.ıve (b) Mated–fed–experienced (c) Mated–unfed–na.ıve (d) Mated–unfed–experienced Group 2: (a) Unmated–fed–na.ıve (b) Unmated–fed–experienced

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(c) (d)

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Unmated–unfed–na.ıve Unmated–unfed–experienced

In experiments of group 1 (mated females), newly emerged female parasitoids were transferred into assay-cups together with males and they were kept for 48 h under the experimental conditions described at the end of this section. For experiments on fed insects (a and b), females were transferred into assay-cups containing honey droplets for 24 h. In group 1 (a and b) feeding took place before mating. In the test with experienced females, newly hatched female parasitoids were kept with 30-day-old host larvae in assay-cups devoid of flour for 24 h (25 females: 50 host larvae) before being released into the experimental arena. In group 1 (b and d), mating took place before the females were offered their experience with host larvae. In all experiments of group 2 (unmated females) parasitised host larvae were isolated in glass assay-cups (7 cm  7 cm). The assay-cups were continuously monitored for adult parasitoid emergence. Female parasitoids were harvested immediately after their emergence to avoid any mating from taking place. The same steps were followed for tests including na.ıve females to avoid any uncontrolled contact between females and the cadavers of their host. In all tests with unfed females, newly emerged insects were kept in assay-cups devoid of food. In all experiments female parasitoids were released into the experimental arenas on the 5th day after hatching, to ensure that all females in the different experiments were at the same age at the time of the test. The experimental arena consisted of a cylindrical foam container (50 cm  15 cm). Each container was provided with a glass lid furnished with a central hole (7 cm in diameter) covered with muslin gauze for aeration and for manipulation of insects during the tests. In all experiments females were offered 7 assay-cups.

Cup number 0. 1. 2. 3. 4. 5. 6.

Description Empty cups Cups containing Cups containing Cups containing Cups containing Cups containing Cups containing

clean flour flour and host frass flour and host eggs 10-day-old host larvae 30-day-old host larvae adult host

Host larvae in cups 4 and 5 were confined in 25 cm3 plastic vials, tightly covered with muslin gauze to prevent them from escaping and wandering on the lower surface of the cup-cover. All cups were tightly covered with muslin gauze secured with rubber bands, to prevent the infiltration of female parasitoids. The cups were placed into the arena in an anti-clockwise sequence as follows: 0, 6, 2, 3, 4, 1, and 5. This pattern was fixed throughout all tests. After setting up of the different choice cups and introduction of the test insects into experimental arena, the lids were tightly secured over the arena and sealed with odourless white plasticine. The experimental arenas were placed under fluorescent light bulbs (40 W) hanging 50 cm above the glass lid, and fixed to a wooden frame. In order to prevent interference from other light sources, the whole arrangement was covered with black sheets of tissue. The light system was connected to a timer and light was

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set to come on at 0600 h and off at 1800 h. During the light period, the arenas were inspected 5–8 times for 3 consecutive days. In each inspection the number of females performing probing behaviour on the muslin cover of each cup was recorded. Females were then forced to move from the probing sites and were left in the arena for further observations. All experiments were conducted at 28711C while the relative humidity (r.h.) was allowed to fluctuate between 50 and 70% r.h. All experiments were replicated 4 times and each replicate consisted of 50 female parasitoids. The percentage of probing attempts that took place on each cup was calculated from the total number recorded in each group. Because of the irregularities in the number of probing activities between physiological states, we used Fisher’s ‘‘z’’ test at Po0:05 to assess significant differences between the responses on each cup.

3. Results 3.1. Observations on host perception by B:hebetor A female parasitoid in close contact with a host larva usually stood still for about 15 min, and the antennae were then lowered to touch the body surface of the host. Antennation continued as the parasites mounted their hosts. This attitude lasted 40 min. Finally, females bent their abdomen forward, the ovipositor was unsheathed and probing of the host took place. From 2–3 probes were observed and each one lasted from 1–3 min. On the other hand, when the parasite females were separated from their host larvae, by means of muslin covers on the experimental cups, they started running over the surface and round the edges of the cover. They stopped and remained still with their antennae kept elevated and then started running again. This behaviour lasted about 30 min. When females landed on cups containing suitable hosts in the choice tests, their movements on the cover were slow and the antennae continuously examined the surface. The examination behaviour of the covers, in this case, lasted about 10 min interrupted by periods of quiescence. Examination was then resumed until a particular spot was located, where females started inserting their antennae through the tiny holes of the mesh of muslin covers. The antennae rotated in the cup and were then pulled out. Antennal insertion lasted about 1 h, then the females bent the abdomen forward and inserted the ovipositor at exactly the same spot (probing). This attitude lasted up to 1 h. Groups of up to 4 females probing at the same spot were encountered. 3.2. The choice of searching sites Pooled data obtained from the different tests are presented in Fig. 1. The results showed a higher tendency for females to choose the cups containing older host larvae for probing, as cup (5) received 40.7% of the total number of probes recorded, attracting significantly more female parasitoids than any other cup (Po0:05). Cup (2) containing a mixture of host frass and flour received 28.1% of the total number of probes recorded in all tests. The results also showed that 15.6% of the probes were performed on cup (6) containing adult E. kuehniella. Cup (4) containing 10-day-old host larvae received 10.9% of the total number of probes, while cups (1 and 3)

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Fig. 1. Percentages of probes in the different choices of host or host medium material (cups 0–6, as described in Table 1) obtained from pooled data (total of 1370 probes) from all tests. Sectors marked by (NS) are not significantly different from the control (cup 0).

containing clean flour and flour containing host eggs, respectively, received together less than 5% of the number of probes. On the other hand, cup (0) containing only a white piece of paper was never probed by female parasitoids. 3.3. Effect of feeding Feeding significantly affected the choices of unmated females (experienced/na.ıve) for probing sites (Po0:05), while in case of mated females (experienced/na.ıve), feeding had almost no significant effect. In the case of unmated-na.ıve females, the number of cups probed decreased with feeding. The percentage of probing significantly increased only on cups containing 30-day-old host larvae from 8% to 68% (Po0:05) and it decreased significantly on all the other cups. In experienced females, the percentage of probing on cups containing 30-day-old host larvae also significantly increased from 31% to 61% (Po0:05). In addition, fed females probed only on cups containing 30-day-old host larvae and host frass. 3.4. Effect of mating The effect of mating on the choice of probing sites by female parasitoids is represented in Table 1. In fed-na.ıve females, mating increased the number of cups probed. Unmated females probed on cups containing 30-day-old host larvae, flour and frass, and cups containing host adults. In addition to these cups, mated females significantly increased their probing on cups containing 10-day-old host larvae and on cups containing host frass from 0% to 11% and from 20% to 35% respectively (Po0:05). Likewise, in fed-experienced females, mating increased the

(0) (1) (2) (3) (4) (5) (6)

Sig

Sig

Grp 1a vs Grp 1c

Sig

Grp 1b vs Grp 1d

Effect of feeding

Table 1

Grp Grp Grp Grp

Sig Sig Sig Sig Sig Sig

Grp 2b vs Grp 2d

Sig Sig Sig

Sig Sig Sig Sig Sig

Sig

Grp 1a vs Grp 2a

Sig

Sig

Sig

Grp 1b vs Grp 2b

2a: Unmated–fed–naive. 2b: Unmated–fed–experienced. 2c: Unmated–unfed–naive. 2d: Unmated–unfed–experienced.

Grp 2a vs Grp 2c

Sig Sig Sig

Sig

Grp 1c vs Grp 2c

0.0 2.3 23.0 1.0 24.0 36.0 13.0

Grp 1c 128

Sig Sig

Sig

Grp 1d vs Grp 2d

0.0 3.0 32.0 2.0 5.0 45.0 12.0

Grp 1d 207 0.0 0.0 38.0 0.6 0.6 61.0 0.6

Grp 2b 180

Sig

Sig

Grp 1a vs Grp 1b

Sig

Grp 1c vs Grp 1d

Effect of experience

0.0 0.0 20.0 1.0 0.0 68.0 11.0

Grp 2a 171

Sig

Sig

Grp 2a vs Grp 2b

0.0 9.0 30.0 6.0 11.0 8.0 35.0

Grp 2c 192

Effect of the different physiological parameters on female B. hebetor choices of probing sites

Abbreviations Grp 1a: Mated–fed–na.ıve, Grp 1b: Mated–fed–experienced, Grp 1c: Mated–unfed–na.ıve, Grp 1d: Mated–unfed–experienced, Sig: Significant (Po0.05).

Cup Cup Cup Cup Cup Cup Cup

Choices

(B) Statistical analysis

0.0 0.0 22.0 2.0 5.0 49.0 23.0

Grp 1b 123

Effect of mating

0.0 1.0 35.0 0.0 11.0 33.0 20.0

empty (control) contains clean flour contains flour and host frass contains flour and host eggs contains 10-day-old host larvae contains 30-day-old host larvae contains adult host

Cup Cup Cup Cup Cup Cup Cup

(0) (1) (2) (3) (4) (5) (6)

Grp 1a 202

Female conditioning: Total number of probing attempts:

(A) Percentage of probing on the different cups

Table 1 Effect of the different physiological parameters on female B. hebetor choices of probing sites

Sig Sig Sig Sig Sig

Grp 2c vs Grp 2d

0.0 4.0 19.0 1.0 35.0 31.0 10.0

Grp 2d 167

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number of assay-cups probed, to include, in addition to cups containing 30-day-old larvae and cups containing flour mixed with frass, those cups containing an adult host and those containing 10-day-old larvae (from 0.6% to 23% and from 0.6 to 5% respectively, Po0:05). In unfed-na.ıve females, mating significantly increased probing on cups containing host larvae from 8% to 36% on cups containing 30-day-old larvae and from 11% to 24% in cups containing 10-day-old larvae (Po0:05). Meanwhile, mating significantly decreased probing on those cups devoid of host larvae (Po0:05). 3.5. Effect of experience Table 1 shows that in mated-fed females experience significantly increased the percentage of probing from 33% to 49% (Po0:05) on cups containing 30-day-old host larvae. The effect of experience, however, was most obvious in unmated-unfed females. Experience significantly decreased the percentage of probing on the cups devoid of host larvae from 30% to 19% in cups containing frass, from 6% to 1% in cups containing host eggs and flour, and from 35% to 10% in cups containing adults of the host (Po0:05). Meanwhile, experience significantly increased the percentage of probing on cups containing 10-day-old larvae from 11% to 35% and on cups containing 30-day-old larvae from 8% to 31% (Po0:05).

4. Discussion The habit of antennal search and antennal insertion through the muslin covers of the assay cups by B. hebetor could be explained as an attempt to detect specific cues emitted by the host or its habitat that serve in host location. A similar explanation was given by Moran et al. (1969) for the parasitoid Tetrastichus flavigaster Brothers and Moran parasitising psyllid nymphs. This explanation could be supported by studies on the structure of the antennae of some parasitoids that revealed the presence of unique receptors (Slifer, 1969; Weseloh, 1971; Miller, 1972; Borden et al., 1973; Norton and Vinson, 1974). Several chemical cues were related to the searching behaviour of parasitoids that may also explain the searching behaviour of B. hebetor. These cues include the mandibular gland secretions of the host liberated during feeding (Corbet, 1971; Calvert, 1973) and the host’s frass and webbing (Lewis and Jones, 1971; Greany and Oatman, 1972; Hendry et al., 1973). The probing behaviour of B. hebetor was similarly described for other insect species. McGovern and Cross (1974) pointed out that females of B. mellitor Say, a parasitoid of the boll weevil, would pierce the cocoon and wave their ovipositor around in search of a host. A similar description has also been given for the parasitoid Pteromalus venustus Walker, a parasitoid of the alfalfa leafcutter bee (Hobbs and Krunic, 1971). Several stimuli were related to unsheathing of the ovipositor and to probing behaviour. Vinson et al. (1975) pointed out that host odours might result in a reflex action of ovipositor probing. Movement or host vibrations have been considered as important stimuli in the release of ovipositor probing on hosts that are concealed by a covering (Edwards, 1955; Van den Assem and Kuenen, 1958; Ryan and Rudinsky, 1962). Shonouda and Nasr (1998) found that females of B. hebetor responded to the hexane extract of host larvae (containing kairomone) by intensifying their searching and oviposition behaviour.

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Pooled data in Fig. 1 showed that B. hebetor females were preferentially attracted to cups containing 30-day-old host larvae. Parasitoid preference for older host larvae has also been recorded for other host-parasitoid relationships. Thus, Wang (1991) reported the same preference for B. hebetor parasitising the larvae of Plodia interpunctella (Hubner). . Similarly, when given a choice of second and fifth instar larvae, the endoparasitoid Venturia canescens (Gravenhorst), parasitised the smaller instar at a much lower rate than when wasps had no choice (Sait et al., 1997). The attraction of B. hebetor females to host frass for probing is in agreement with the finding of van Alphen and Vet (1986). They found that many parasitoids respond to chemicals emitted from the intact or contaminated habitat of their host and from various host larval products, such as frass, during their search for oviposition sites. Fukushima et al. (1989) found that kairomone from the frass of Cadra cautella Walker was responsible for the stinging behaviour of B. hebetor. On other hand, probing of B. hebetor on cups containing adults of E. kuehniella could be due either to some unidentified chemical cues emitted by the adults of the host, or to a combination of such cues with flour. The possibility that female parasitoids were attracted to the cups containing adults by means of visual or acoustic cues would give another explanation of these results. Host adults were left free in their cups during all the tests and tended to rest on the lower surface of the cup-cover, where they were located by female parasitoids and probed. Our results (Fig. 1) showed that the number of probes recorded on the assay-cups containing non-infested flour (cups 1 and 3) was not statistically different from the number recorded on the empty cups. Analysis of variance indicated that the eggs of the host did not play a role in the attraction of the parasitoid to the searching site. Vinson (1976) stated that plant volatiles emanating from the host’s food or food plant are the first cues in the chain of events that lead to host location by many hymenopterous parasitoids. This statement may reflect the fact that the parasitoid is attracted to the habitat of the host irrespective of its presence. The effect of feeding on the choice of probing sites by B. hebetor depended to a large extent on the other physiological states of the females as shown in Table 1. The significant increase in the percentage of probing only on the cups containing 30-day-old host larvae with feeding may be attributed to the fact that unfed females may face a trade-off between searching for food and an oviposition site. This is in agreement with the finding of Smith (1993) that unfed females are under time-limited sub-optimal conditions, and that in such cases error costs for finding less suitable hosts are low. Theoretical optimisation models predict a fitness pay-off for lower selectivity under sub-optimal conditions and hence females should accept less suitable hosts for oviposition. Therefore, the nutritional state may be important in that the intake of food increases longevity which consequently extends the time available for host location (Vet et al., 1995). The results in Table 1 also indicate that mating significantly increased the percentage of probing on cups containing host larvae. This is in agreement with the results of Guertin et al. (1996) who showed that, in laboratory as well as in field studies, unmated B. hebetor females were more reluctant to move into stored maize in their search for hosts than were mated females. Moreover, the significant increase of probing on cups containing host larvae, especially on 30-day-old larvae, may be attributed to the tendency of females to produce female-biased progeny, as the host size significantly affects the sex ratio of B. hebetor in favour of females. Our results showed that experience significantly affected the incidence of probing of female parasitoids on all cups. Probing increased only on cups containing host larvae, and decreased on

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the other cups. The innate response of newly hatched ‘‘na.ıve’’ parasitoids was generally enhanced by experience, and this improvement was more obvious when parasitoids were unfed. Host cues learned in previous experience, upon contact with the host, seemed to play an important role in subsequent host habitat recognition. Likewise, Vet (1983) demonstrated that adult experience affected responses of the parasitoid Leptopilina clavipes (Hartig). Our results are also in agreement with Turlings et al. (1989, 1990) who found that contacting host faeces was sufficient experience for the wasp Cotesia marginiventris (Cresson) to dramatically increase their responses to odour experienced during contact. C. marginiventris recognised specific semiochemicals in the faeces of suitable hosts, and associated surrounding odours with the possible presence of host, and subsequently used these odours as cues in host searching. Similarly, Lewis and Tumlinson (1988) found that non-volatile contact kairomones in the frass of host larvae served as a key stimulant in learning by the parasitoid wasp Microplitis croceipes (Cresson) after contact with these kairomones. The wasp was found to be attracted to odours that were present during contact experience, even if these odours were not normally associated with the host. Vet and Groenewold (1990) obtained similar results with the hymenopterous parasitoid, Leptopilina heterotoma (Thomson). Working with B. hebetor, Amelia (1995) reported that post-emergence experience influenced the response of the parasitoid females to volatiles emanating from the host habitat complex, and that na.ıve and experienced females differed qualitatively and quantitatively in their behavioural responses to host-associated volatiles. The results obtained in the present work showed that the interactions between external cues emitted by the host and internal factors generated from physiological conditions influenced female choices of probing sites (Fig. 2). No single physiological state was solely responsible for the choice

Fig. 2. Effect of the different physiological states on the percentage of probing on different choices. Key for physiological states as in Table 1.

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of probing sites. Rather, it was a combination of all physiological states that caused females to restrict their searching behaviour to a particular assay-cup, or to increase the searching range to cover different choices. In other words, it is possible to conclude that the effects of different cues emitted by the host are only functional as guiding trails for the parasite whose physiological state determines the response elicited. This conclusion is in agreement with the findings of Takasu and Lewis (1993, 1995) who recognised that both the information from host-related cues and the nutritional state of the parasitoid determined foraging behaviour. Our conclusion also agrees with the statement of Vet et al. (1995). They reported that the patterns of parasitoid foraging are determined by the interactions of genetic, physiological, environmental and experiential factors. Accordingly, we recommend that females of B. hebetor should be experienced and fed before release to obtain the highest rates of successful attacks by the parasitoids, if they are to be used in biological control or Integrated Pest Management programs.

References Amelia, F.R., 1995. Behavior, patterns of seasonal field activity and cold tolerance in B. hebetor Say (Hymenoptera: Braconidae). Ph.D. Thesis, University of Wisconsin, Madison, USA, 158pp. Antolin, M.F., Strand, M.R., 1992. Mating system of Bracon hebetor Hymenoptera: Braconidae. Ecological Entomology 17, 1–7. Arthur, A.P., 1971. Associative learning by Nemeritis canescens (Hymenoptera, Ichneumonidae). Canadian Entomologist 103, 1137–1141. Awadallah, K.T., Tawfik, M.F.S., Abdella, M.M.H., 1985. Biocycle of Bracon hebetor Say (Hymenoptera: Braconidae) on the wax moth Galleria mellonella, L. (Lepidoptera: Galleridae). Annals of Agriculture Science of Moshtohor 23, 343–350. Borden, J.H., Miller, G.E., Richerson, J.V., 1973. A possible new sensillum on the antennae of Itoplectis conquisitor. Canadian Entomologist 105, 1363–1367. Calvert, D., 1973. Experimental host preferences of Monoctonus paulensis, including a hypothetical scheme of host selection. Annals of the Entomological Society of America 66, 28–33. Clausen, S.A. (Ed.), 1940. Entomophagous Insects. McGraw-Hill, New York, 688pp. Corbet, S.A., 1971. Mandibular gland secretion of larvae of the flour moth, Anagasta kuehniella, contains an epideictic pheromone and elicits oviposition movements in a hymenopteran parasite. Nature 232, 481–484. Cushman, R.A., 1926. Location of individual hosts versus systematic relation of host species as a determining factor in parasite attack. Proceedings of the Entomological Society of Washington 28, 5–6. Debach, P., 1964. Biological Control of Insect Pests and Weeds. Reinhold, New York, 844pp. Doutt, R.L., 1964. Biological characteristics of entomophagous adults. In: DeBach, P. (Ed.), Biological Control of Insect, Pests and Weeds. Chapman & Hall, London, pp. 145–167 (Chapter 6). Edwards, R.L., 1955. How the hymenopteran parasite Mormoniella vitripennis Walker finds its host. British Journal of Animal Behaviour 3, 37–38. El-Shazly, M.M., El-Sebaey, I.I.A., 1997. Development and predation rates of Coranus aegyptius F. and Vachiria natolica St.al (Hemiptera: Reduviidae: Harpactorinae). Egyptian Journal of Biological Pest Control 7, 47–51. Farghaly, H.T.H., Ragab, Z.A., 1985. Relationship between relative humidity and adult biology of Bracon hebetor Say. Bulletin de la Soci!et!e Entomologique d’Egypt 65, 131–135. Fukushima, J., Yasumasa, K., Takahisa, S., 1989. Isolation and identification of a kairomone responsible for the stinging behavior of Bracon hebetor Say (Hymenoptera: Braconidae) from frass of the almond moth Cadra cautella Walker. Agricultural and Biological Chemistry 53, 3057–3059. Greany, P.D., Oatman, E.R., 1972. Oviposition by an isolated parasite abdomen. Annals of the Entomological Society of America 65, 991–992.

E. Darwish et al. / Journal of Stored Products Research 39 (2003) 265–276

275

Guertin, D.S., Ode, P.J., Strand, M.R., Antolin, M.F., 1996. Host-searching and mating in an outbreeding parasitoid wasp. Ecological Entomology 1, 27–33. Hare, J.D., Morgan, D.J.W., Nguyun, T., 1997. Increased parasitization of California red scale in the field after exposing its parasitoid, Aphytis melinus, to a synthetic kairomone. Entomologia Experimentalis et Applicata 82, 73–81. Heimpel, G.E., Rosenheim, J.A., Mangel, M., 1997. Predation on adult Aphytis parasitoids in the field. Oecologia 110, 346–352. Hendry, L.B., Greany, .P.D., Gill, R.J., 1973. Kairomone mediated host-finding behavior in the parasitic wasp Orgilus lepidus. Entomologia Experimentalis et Applicata 16, 471–477. Hobbs, G.A., Krunic, G.A., 1971. Comparative behavior of three chalcidoid parasites of the alfalfa leafcutter bee, Megachile rotundata, in the laboratory. Canadian Entomologist 103, 674–685. Lewis, W.J., Jones, R.L., 1971. Substance that stimulates host-seeking by Microplitis croceipes, a parasite of Heliothis species. Annals of the Entomological Society of America 64, 471–473. Lewis, W.J., Tumlinson, J.H., 1988. Host detection by chemically mediated associative learning in a parasitic wasp. Nature 331, 257–259. Lewis, W.J., Vet, L.E.M., Tumlinson, J.H., van Lenteren, J.C., Papaj, D.R., 1990. Variations in parasitoid foraging behaviour: essential element of a sound biological control theory. Environmental Entomology 19, 1183–1193. Mangel, M., 1987. Oviposition site selection and clutch size in insects. Journal of Mathematical Biology 25, 1–22. Mangel, M., 1989. Evolution of host selection in parasitoids: does the state of the parasitoid matter? American Naturalist 133, 688–705. McGovern, W.L., Cross, W.H., 1974. Oviposition of a parasite Bracon mellitor attacking larvae of the boll weevil inside the cotton square. Annals of the Entomological Society of America 67, 520–521. Miller, M.C., 1972. Scanning electron microscope studies of the flagellar sense receptors of Paridesmia discus and Nasonia vitripennis. Annals of the Entomological Society of America 65, 1119–1123. Morgan, D.J.W., Hare, J.D., 1998. Volatile cues used by the parasitoid, Aphytis melinus, for host location: California red scale revisited. Entomologia Experimentalis et Applicata 88, 235–245. Moran, V.C., Brothers, D.J., Case, J.J., 1969. Observations on the biology of Tetrastichus flavigaster Brothers and Moran parasitic on psyllid nymphs. Transactions of the Royal Entomological Society of London 121, 41–58. Norton, W.N., Vinson, S.B., 1974. A comparative ultrastructural and behavioral study of the antennal sensory sensilla of the parasitoid, Cardiochiles nigriceps. Journal of Morphology 142, 329–350. Prokopy, R.J., Lewis, W.J., 1993. Application of learning to pest management. In: Papaj, D.R., Lewis, A.C. (Eds.), Insect Learning: Ecological and Evolutionary Perspectives. Chapman & Hall, New York, pp. 308–342. Rogers, D., 1972. Random search and insect population models. Journal of Animal Ecology 41, 369–383. Royama, T., 1971. A comparative study of models for predation and parasitism. Researches in Population Ecology Kyoto, Supplement 1, 1–91. Ryan, R.E., Rudinsky, J.A., 1962. Biology and habits of the Douglas fir beetle parasite, Coeloides brunneri Viereck. Canadian Entomologist 94, 748–763. Sait, S.M., Begon, M., Thompson, D.J., Harvey, J.A., Hails, R.S., 1997. Factors affecting host selection in an insect host–parasitoid interaction. Ecological Entomology 22, 225–230. Shonouda, M.L., Nasr, F.N., 1998. Impact of larval-extract kairomone of Ephestia kuehniella Zell. (Lep., Pyralidae), on the behavior of the parasitoid Bracon hebetor Say (Hym., Braconidae). Journal of Applied Entomology 122, 33–35. Slifer, E.H., 1969. Sense organs on the antenna of a parasitic wasp, Nasonia vitripennis. Biological Bulletin 136, 223–263. Smith, B.H., 1993. Merging mechanism and adaptation: an ethological approach to learning and generalization. In: Papaj, D.R., Lewis, A.C. (Eds.), Insect Learning. Ecological and Evolutionary Aspects. Chapman & Hall, New York, pp. 126–157. Strand, M.R., Williams, H.J., Vinson, S.B., Mudd, A., 1989. Kairomonal activities of 2-acylcyclohexane-1,3-diones produced by Ephestia kuehniella Zeller in eliciting searching behaviour by the parasitoid Bracon hebetor Say. Journal of Chemical Ecology 15, 1491–1500. Sweetman, H.L., 1963. Principles of Biological Control. Dubridge, Wm. C. Brown Co, Iowa, 560pp.

276

E. Darwish et al. / Journal of Stored Products Research 39 (2003) 265–276

Takasu, K., Lewis, W.J., 1993. Host- and food-foraging of the parasitoid Microplitis croceipes: learning and physiological state effects. Biological Control 3, 70–74. Takasu, K., Lewis, W.J., 1995. Importance of adult food sources to host searching of the larval parasitoid Microplitis croceipes. Biological Control 5, 25–30. Turlings, T.C., Tumlinson, J.H., Lewis, W.J., Vet, L.E.M., 1989. Beneficial arthropod behavior mediated by airborne semiochemicals. VIII. Learning of host-related odours induced by a brief contact experience with host by-products in Cotesia marginiventris Cresson, a generalist larval parasitoid. Journal of Insect Behaviour 2, 217–225. Turlings, T.C.J., Scheepmaker, J.W.A., Vet, L.E.M., Tumlinson, J.H., Lewis, W.J., 1990. How contact foraging experiences affect preferences for host—related odours in the larval parasitoid Cotesia marginiventris Cresson (Hymenoptera: Braconidae). Journal of Chemical Ecology 16, 1577–1589. van Alphen, J.J.M., Vet, L.E.M., 1986. An evolutionary approach to host finding and selection. In: Waage, J., Greathead, D. (Eds.), Insect Parasitoids. Academic Press, London, pp. 23–61. van Den Assem, J., Kuenen, D.J., 1958. Host finding of Choetospila elegans Westwood, a parasite of Sitophilus granarius. Entomologia Experimentalis et Applicata 1, 174–180. Vet, L.E.M., 1983. Host habitat location through olfactory cues by Leptopilina clavipes Hartig (Hym. Eucoilidae), a parasitoid of fungivorous Drosophila: the influence of conditioning. Netherlands Journal of Zoology 33, 225–249. Vet, L.E.M., Groenewold, A.W., 1990. Semiochemicals and learning in parasitoids. Journal of Chemical Ecology 16, 3119–3135. Vet, L.E.M., Lewis, W.J., Carde! , R.T., 1995. Parasitoid foraging and learning. In: Carde, R.T., Bell, W.J. (Eds.), Chemical Ecology of Insects 2. Chapman & Hall, New York, pp. 65–101. Vinson, S.B., 1976. Host selection by insect parasitoids. Annual Review of Entomology 21, 109–133. Vinson, S.B., Jones, R.L., Sonnet, P., Beirl, B.A., Beroza, M., 1975. Isolation, identification and synthesis of hostseeking stimulants for Cardiochiles nigriceps, a parasitoid of the tobacco bud-worm. Entomologia Experimentalis et Applicata 18, 443–450. Volkl, W., Mackauer, M., 1993. Interactions between ants attending Aphis fabae spp. cirsiiacanthoidis on thistles and foraging parasitoid wasps. Journal of Insect Behaviour 6, 301–312. Wang, W.X., 1991. Studies on the relationship between host size and sex ratio of Bracon hebetor (Hym: Braconidae). Chinese Journal of Biological Control 71, 16–18. Weseloh, R.M., 1971. Influence of primary (parasite) hosts on host selection of the hyperparasite Cheiloneurus noxius. Annals of the Entomological Society of America 64, 1233–1236.