Attraction of the parasitoid Anisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae) to odors from grain and stored product pests in a Y-tube olfactometer

Biological Control 54 (2010) 29–34

Contents lists available at ScienceDirect

Biological Control journal homepage: www.elsevier.com/locate/ybcon

Attraction of the parasitoid Anisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae) to odors from grain and stored product pests in a Y-tube olfactometer Consuelo Belda *, Jordi Riudavets Entomology, IRTA, Ctra. Cabrils km 2, 08348 Cabrils, Barcelona, Spain

a r t i c l e

i n f o

Article history: Received 15 October 2009 Accepted 11 February 2010 Available online 16 February 2010 Keywords: Preference Sitophilus oryzae Rhyzopertha dominica Tribolium confusum Lasioderma serricorne Host stage Volatiles

a b s t r a c t Pests that affect stored products can be very harmful; they can affect stock, damage products by reducing their weight or by contaminating them, and consequently affect a brand’s reputation. As the range of permitted chemical products is being progressively reduced, biological control is a tool that is being increasingly developed. Anisopteromalus calandrae (Hymenoptera: Pteromalidae) is a well-known ectoparasitoid that attacks late-instar larvae of several stored product pests. The current study evaluates the host preference of female parasitoids, regarding host species, stages and host food products, using a vertical Y-tube olfactometer. Parasitoids were offered late-instar larvae and adults of Sitophilus oryzae (L.) (Coleoptera: Curculionidae), Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae), Tribolium confusum (Jacqueline duVal) (Coleoptera: Tenebrionidae) and Lasioderma serricorne (F.) (Coleoptera: Anobiidae) and host food products (rice and flour). They preferred uninfested host food products (rice or flour) to empty controls and uninfested paddy rice to uninfested brown rice, while wheat flour was clearly more attractive to them than brown rice. For all the host species, larvae-infested products were more attractive than uninfested ones and than adults of the same species, except in the case of T. confusum. When larvae-infested products of different species were compared among themselves, different levels of attractiveness were observed. Adult stages were not attractive in any of the trials. This preference evaluation aimed to assess the potential of using parasitoids as effective biological control agents in stored product companies. Ó 2010 Elsevier Inc. All rights reserved.

1. Introduction Stored product pests can be very damaging to grain and grainbased commodities for a variety of reasons. They can cause direct losses in product weight and also indirect losses: through contamination via their feces; by them acting as vectors for microorganisms; and by them warming the grain, which can lead to problems with moulds (Gorham, 1979). Merely finding live or dead insects in a product can be an important issue. Insect infestations can damage a company’s image by giving its brand a bad reputation. This can negatively affect its custom and income, and also cause legal problems (through non-compliance with legislation) (Benz, 1987). These problems, together with the development of insecticide resistance (Haliscak and Beeman, 1983; Zettler and Cuperus, 1990; Zettler and Beeman, 1991) and the progressive reduction in the number of chemical products permitted for controlling these pests, make biological control an increasingly desirable strategy (Brower et al., 1991). Anisopteromalus calandrae (Howard) is a well-known cosmopolitan parasitoid of Coleoptera which infests stored products (Schöller et al., 2006). A. calandrae was chosen for these experiments due * Corresponding author. Fax: +34 753 39 54. E-mail address: [email protected] (C. Belda). 1049-9644/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2010.02.005

to its natural occurrence, its abundance in the sampled locations (Riudavets et al., 2002), and the fact that it is known to attack a wide variety of hosts, including, amongst others: Sitophilus oryzae (L.) (rice weevil) (Cline et al., 1985; Press and Mullen, 1992; Lucas and Riudavets, 2002), Sitophilus granarius (L.) (granary weevil) (Ghani and Sweetman, 1955), Sitophilus zeamais Motsch (maize weevil) (Wen and Brower, 1994), Rhyzopertha dominica (F.) (lesser grain borer) (Ahmed, 1996; Menon et al., 2002), and Lasioderma serricorne (F.) (Ahmed and Khatun, 1988). This idiobiont, primary ectoparasitoid attacks late-instar larvae (Shin et al., 1994) that grow internally or concealed within the host food (Ghimire and Phillips, 2007). By piercing the host larva with her ovipositor, the female parasitoid paralyzes it and lays one egg outside the integument, which will develop on the body fluids of the host larvae (Ahmed, 1996). Usually only one parasitoid develops from each host larva (Arbogast and Mullen, 1990). Preference studies have been carried out with other parasitoids of the Pteromalidae family, such as Lariophagus distinguendus (Steidle and Schöller, 1997; Steidle et al., 2001, 2003) and Choetosphila elegans (Williams and Floyd, 1971), which are parasitizing different stored product pests. Parasitoid behavior, with respect to searching for a host, is influenced by several factors in a cereal storage ecosystem. These factors range from environmental conditions (Hong and Ryoo, 1991) to host density and food availability (Steidle and Schöller, 2002;

30

C. Belda, J. Riudavets / Biological Control 54 (2010) 29–34

Shin et al., 1994). In a stored product facility, hosts remain in silos, grain bulks or piles, so they are relatively easy to locate and attack. Temperatures remain constant, which also facilitates parasitoid survival in the storage ecosystem. Among Pteromalidae species, the cues used to find hosts range from chemical stimuli (Ambriz et al., 1996) to visual, vibrational (Meyhöfer and Casas, 1999) and tactile signals (Vinson, 1976; Steidle, 2000). Parasitoids can respond to cues coming from their herbivorous host species or from the different plants on which their hosts feed (Steidle and Schöller, 1997; Steiner et al., 2007). There can be long-distance or short-distance cues (Rojas et al., 2006). On one hand, long-distance or long range cues would tend to be the first cues used by the parasitoid in its orientation towards its host and they are usually emitted by the host food or host plant (Vinson, 1976; Jembere et al., 2003) providing information about the status of the host plant (Vet and Dicke, 1992). Parasitoids can also use short-distance cues. These typically come from the host and are used to locate a specific, or preferred, host stage and attack it (Vet and Dicke, 1992; Ambriz et al., 1996). Different settings can be used to understand how parasitoids locate their hosts. These include: still air olfactometers (Van Tol et al., 2002), one-way olfactometers (Burkholder, 1970), Y-tube olfactometers (Rojas et al., 2006; Wei and Kang, 2006), four arm olfactometers (Giles et al., 1996; Steidle et al., 2001), wind tunnels (Steinberg et al., 1992) and other techniques (Mohan and Fields, 2002). The most appropriate setting to use depends on the insect species and its behavior (Steinberg et al., 1992), and on the type of cues that are to be studied (Vet et al., 1983). The choice of the Y-tube olfactometer for the current set of experiments was mainly determined by the behavior of A. calandrae. The horizontal setting used in many other studies was changed to a vertical setting. The main pest species that occur naturally, abundantly and often together in a grain storage ecosystem are: S. oryzae, R. dominica, L. serricorne (F.) and Tribolium confusum (Jacqueline duVal) (Riudavets et al., 2002). The first three species are known hosts, but T. confusum had not previously been reported as a host for A. calandrae. Determining parasitoid performance in front of this particular range of species can be critical for the use of A. calandrae in biological control. Moreover, assessing the influence of the host on which the parasitoid is reared is also important, because this is known to affect the response towards other species (Steidle and Schöller, 2002; Cournoyer and Boivin, 2004). Many studies can be found on coleopteran pests with other Pteromalidae parasitoid species (Steidle and Schöller, 1997, 2002; Steidle, 2000; Steidle et al., 2003; Steiner et al., 2007), but not on the species tested in this study with A. calandrae or in a Y-tube olfactometer. The main objective was to evaluate whether A. calandrae females could detect specific olfactory cues associated with different host species, life stages, and host food products in the vertical setting of the Y-tube olfactometer. Host species used were S. oryzae, R. dominica, L. serricorne (F.) and T. confusum (Jacqueline duVal). These species were chosen in order to assess whether the parasitoid strain that we were rearing in our laboratory would respond to them in the setting of a vertical Y-tube olfactometer, as all of these species except T. confusum were known hosts for this parasitoid. 2. Materials and methods 2.1. Insect hosts The four stored product pest species used in these trials were obtained from stock cultures maintained in the laboratory. The host stages used in the trials were late-instar larvae, as this was the stage preferred by the parasitoids (Shin et al., 1994; Ahmed, 1996), although adults were also included. Adult stages were tested to evaluate, on one hand, whether the presence of the adult stage would modify the parasitoid response, and on the other, to

determine whether the parasitoid would be able to use adult volatiles as an indirect way of locating larval stages once the host food product had been located. S. oryzae and R. dominica were reared on brown rice, while T. confusum and L. serricorne were reared on a mixture of white wheat flour and yeast (7%). All the colonies were kept under controlled conditions of 25 ± 2 °C and 70 ± 10%RH, with a 16:8 (L:D) photoperiod. 2.2. Parasitoids Anisopteromalus calandrae adult females were obtained from stock cultures maintained in the laboratory, which had originally been collected from grain silos near Barcelona, Spain. A. calandrae were reared at 25 ± 2 °C and 70 ± 10%RH on rice weevils (S. oryzae) in brown rice. The ages of the females used in the test ranged from 1 to 8 days. They were reared on S. oryzae and previous oviposition on this species was supposed for all wasps. Prior to starting the trials, adult A. calandrae females were kept in isolation, i.e. without host for ovipositing, for 10–12 h. This condition could have affected parasitoid starvation. The parasitoids were therefore given sugary water but deprived of hosts. In synovigenic females, responsiveness to hosts or product volatiles may vary according to the time that has passed since their last oviposition (Gauthier and Monge, 1999). As previous oviposition had been impossible for 12 h due to isolation, the predisposition of the females to oviposit was presumed high and it was expected that the parasitoids would be motivated to search for hosts. 2.3. Vertical Y-tube bioassay The intrinsic performance of adult A. calandrae females towards odors coming from host and host food products was assessed in the vertical setting of a Y-tube olfactometer. Preliminary experiments showed that when the olfactometer was placed horizontally, the insects did not respond and often moved round in circles in the same place. Based on these results and on other reports in the literature (Steidle and Schöller, 2002; Press, 1988), we decided to repeat the test with the olfactometer in the vertical position. The results obtained showed that wasps then moved, and moved faster, so the vertical position was used for the trials. The Y-tube olfactometer consisted of a Y-shaped glass tube with arms whose inner diameter was 3.5 cm; each arm was 17 cm long. The angle between the two arms of the olfactometer was 75°, and the angle between each arm and the main body was 145°. Each of the upper arms of the olfactometer was connected to an air pump (Nathura, ECIS, Bessanvido, Italy) which produced a constant air current flowing from the arms of the tube to the base. Air flow was controlled, using a hot wire anemometer (TESTO, Barcelona, Spain), at the ends of both pump tubes prior to the air entering the arms of the olfactometer and was maintained at 2.70 ± 0.10 m/s. The air flow that exited the base of the olfactometer, having passed through the olfactometer, was maintained at 0.20 ± 0.02 m/s. A glass jar was connected to each arm of the olfactometer using plastic tubing (0.5 cm diameter). The lid of each jar contained an air inlet tube, which connected the air pump to the jar, and an outlet tube, which connected the jar to the olfactometer arm. The outlet tubes were covered with gauze (0.3 mm mesh size) inside the jar lid to prevent insects from entering the tubes. Different odor source treatments (four host species, two life stages, and host food: rice or flour) were placed inside the jars for the experiments (Tables 1–3). To start the trial, an A. calandrae female was allowed to walk onto a meshed lid placed at the base of the olfactometer. We then waited until the female had walked off the lid and into the olfactometer arm. The lid was then removed for the rest of the trial and the chronometer was started. Each individual was observed until either it had moved a third of the way up one of the olfac-

31

C. Belda, J. Riudavets / Biological Control 54 (2010) 29–34

Table 1 Response of A. calandrae females when presented with a choice between: (a) an uninfested product and an empty control and (b) two uninfested products in a Y-tube olfactometer. N(A): number of individuals that chose the arm of the olfactometer containing treatment A. N(B): number of individuals that chose the arm of the olfactometer containing treatment B. N(0): number of individuals that did not select either arm of the olfactometer within 5 min. The z and P values relate to a two-sided binomial test of observed and predicted distribution based on a random response. Treatments A vs. B

A

B

N(A)

N(B)

N(0)

z

P

Uninfested product vs. empty control

Brown rice Paddy rice Wheat flour

Empty control Empty control Empty control

35 45 45

15 15 8

10 0 7

2.7 3.9 5.1

<0.01 <0.001 <0.001

Uninfested product vs. uninfested product

Brown rice Brown rice

Paddy rice Wheat flour

19 10

38 40

3 10

2.4 4.1

<0.05 <0.001

Table 2 Response of A. calandrae females when presented with a choice between larvae-infested product and: (a) an uninfested product, (b) another larvae-infested product and (c) adults of the same species, in a Y-tube olfactometer. All the parameters are as in Table 1. Treatments A vs. B

A

B

N(A)

N(B)

z

P

Larvae-infested product vs. uninfested product

S. oryzae in brown rice R. dominica in brown rice L. serricorne in wheat flour T. confusum in wheat flour

Brown rice Brown rice Wheat flour Wheat flour

42 49 43 26

11 3 14 27

N(0) 7 8 3 7

4.3 6.4 3.7 0.14

<0.001 <0.001 <0.001 1.00

Larvae-infested product vs. larvae-infested product

S. oryzae in brown rice R. dominica in brown rice S. oryzae in brown rice

L. serricorne in wheat flour L. serricorne in wheat flour R. dominica in brown rice

9 23 24

40 30 29

11 7 7

4.43 0.95 0.68

<0.001 0.41 0.57

Larvae-infested product vs. adults of the same species alone

S. oryzae R. dominica L. serricorne T. confusum

S. oryzae R. dominica L. serricorne T. confusum

54 38 41 34

4 15 16 14

2 7 3 12

6.5 3.1 3.2 0.3

<0.001 <0.01 <0.01 <0.01

Table 3 Response of A. calandrae females when presented with a choice between adults and an empty control in a Y-tube olfactometer. All the parameters are as in Table 1. Treatments A vs. B

A

B

Adult vs. empty control

S. oryzae R. dominica L. serricorne T. confusum

Empty Empty Empty Empty

control control control control

tometer arms or for a total of 5 min. Each wasp was then removed, using a mouth aspirator, and discarded. Sixty females were tested in each odor trial. To avoid any possible asymmetries in the experimental set-up due to environmental factors or location effects the olfactometer was cleaned with alcohol (96%) and the arms were switched between the two odor source jars after every five wasps. Jar positions were also rotated after every 10 wasps. The trials were carried out at the same location with uniform light and at the same time of day (between 09:00 and 16:00). We recorded each insect’s final choice after a set time period, following the method proposed by Du et al. (1996) for collecting data and preventing random choices when the insects explored the arms. 2.4. Trials We tested the preference of parasitoids for host food products and for adults and larvae of S. oryzae, T. confusum, R. dominica and L. serricorne. The amount of medium and the number of insects used as odor sources were kept constant: 100 g of medium and 50 insects (adults or larvae depending on the trial) in all replicates. To obtain S. oryzae and R. dominica larvae, we used product that had been infested for more than four weeks in order to provide larvae of the appropriate age. For L. serricorne and T. confusum, the 50 larvae were individually counted and placed in the jars with flour. To

N(A)

N(B)

N(0)

z

P

28 27 26 27

30 21 29 24

2 12 5 9

0.2 0.9 0.4 0.3

0.89 0.47 0.78 0.78

obtain uninfested product, the rice and flour packages were frozen prior to the assays. They were then left inside a chamber under controlled climatic conditions to allow the rice grains to recover an appropriate level of humidity and temperature. Our experiments can be divided into two groups. In the first, we tested whether the parasitoid could detect the host food in different settings, the host food being clean brown rice or clean wheat flour. We evaluated preference for uninfested products as opposed to empty controls and for uninfested product as opposed to another uninfested product. In the second group, we tested whether parasitoids responded differently to different host species and host life stages. We carried out two groups of assays. One group offered the choice between larvae-infested products and: uninfested product; other larvae-infested product; and adults of the same species, while another group of assays offered the choice between adults and empty controls. 2.5. Statistical analysis Significant differences in the proportion of A. calandrae females choosing a particular odor source were tested using a two-sided binomial test (SAS software 2002, SAS Institute, Cary, NC, USA). Insects that did not respond (i.e. insects that stayed on the meshed lid, or that stayed below the third of the olfactometer arm for the whole 5-min period) were not included in the statistical analysis.

32

C. Belda, J. Riudavets / Biological Control 54 (2010) 29–34

A maximum of 12 non-responses were observed per trial (Tables 1–3). 3. Results 3.1. Response of A. calandrae to uninfested products The first group of four trials tested the attractiveness of the uninfested host food product (i.e. rice or flour) vs. the empty control jars, and vs. another uninfested host food product (Table 1). In all the trials conducted, A. calandrae females showed a preference for the air coming from the uninfested host food products rather than the clean air coming from the empty control jars and females were more attracted to odors coming from the arm containing brown rice (70%), the one containing paddy rice (75%) and the one containing white flour (85%) than to those corresponding to the control arm. When the parasitoids were offered a choice between uninfested brown rice and paddy rice, the majority preferred the paddy rice. When uninfested brown rice and wheat flour were offered, the flour proved significantly more attractive. Only 8.6% of all the parasitoids tested showed no response to any odor (30 females of the 300 individuals tested) (Table 1). 3.2. Response of A. calandrae to larvae-infested products This second group of trials focused on testing the attractiveness of odors from larvae-infested products against several different options; we grouped the trials in three sets. First, there were trials testing larvae-infested products against uninfested products, then against another larvae-infested product, and finally against just adults of the same species without any other product (Table 2). In the first set, A. calandrae were significantly more attracted to the odors from the larvae-infested product arm than to the one containing uninfested product when S. oryzae (79%), R. dominica (94%), and L. serricorne (75%) were the host species, but not when the host was T. confusum (49%) (Table 2). In the second set of trials, the choice was between odors from two different larvae-infested products. As T. confusum had not been attractive in the first set of trials, it was excluded. Brown rice infested with R. dominica compared S. oryzae was equally attractive, as was the case for R. dominica compared to L. serricorne. However, L. serricorne-infested flour was more attractive than S. oryzae-infested brown rice (Table 2). In the last trial, which offered R. dominica-infested brown rice as an alternative to L. serricorne-infested wheat flour, no significant differences were observed (Table 2). In the last set of tests, four trials were carried out in which larvae-infested products were offered as an alternative to just adults of the same species. A. calandrae were more attracted to the odors from the arm containing larvae-infested product (71–93%) than to the odors from the arm containing adults (adults without any food product) of all species (Table 2). In the whole group of trials, 74 of the 660 females tested (11.2%) did not respond. 3.3. Response of A. calandrae to adult infested products As we had tested adults against larvae-infested product in the previous group of trials, without observing any preference for the adults at all, we wanted to assess whether the other factor had been too attractive for the adults to be considered. We therefore carried out a further set of trials offering a choice between adults and empty controls (Table 3). A. calandrae females had no significant preference for odors coming from either arm of the olfactometer when adults of any of the four tested species were offered as alternatives to empty controls (Table 3).

Over all the trials involving adults, 10.7% of the parasitoids did not respond (28 out of the 240 individuals tested) (Table 3). 4. Discussion Our results show how the searching behavior of A. calandrae can be assessed by means of vertical Y-tube olfactometer assays. The current results show that A. calandrae females are able to find host products and appropriate host stages and consequently attack several host species. These results are therefore consistent with the idea of this parasitoid being able to establish itself and maintain a pest population under a certain level affirmed in other studies (Wen and Brower, 1994). The results for the first set of odors offered to the parasitoid showed that they are able to detect host food product. In other studies, it has been shown that the rice hull of paddy rice may reduce the type and quantity of volatiles emitted from the grain in comparison with dehulled brown rice (Trematerra et al., 1999). However, in our study, females still exhibited a response and even preferred the paddy rice. This could have been because the hull itself emits certain detectable volatiles or because this is how the parasitoids would normally find their target in the field or in stored product facilities. Steidle et al. (2001) stated that undamaged rice odors were not attractive for another Pteromalidae species, L. distinguendus, when it was offered as an alternative to an empty control. However, in our trials with A. calandrae, we found that all forms of uninfested rice tested were preferred to an empty control. Our results may differ from those reported in other studies due to either different environmental conditions or differences in the pest species and parasitoid strains used. Steidle and Schöller (2002) detected that A. calandrae’s ability to find its hosts varied with these and other factors, including geographical strain and grain volume. Our results suggest that in and around rice storage facilities the parasitoid A. calandrae would respond to the presence of host food and would also be able to locate the rice piles by following host food odors. Our second objective was to test which species and stages were preferred by the parasitoid. Two groups of experiments were carried out: the first tested the attractiveness of the larvae-infested products, while the other tested the attractiveness of the adult stages (Table 2). Firstly, A. calandrae females showed their preference for all the larvae-infested products except T. confusum as opposed to the uninfested products (rice or flour). This finding was in line with the results obtained by Steidle (2000) working with L. distinguendus and also with other studies which also reported that herbivore-damaged or infested plants proved more attractive to parasitoids than non-infested plants (Jembere et al., 2003; Steidle and Schöller, 1997; Turlings et al., 1993, 1998). Our results may also be explained by several factors acting together. The rice had been damaged, so the volatiles emitted could have changed and this could have been detected by the parasitoids (Vet and Dicke, 1992; Powell et al., 1998; Turlings et al., 1998). Furthermore, the presence of the larvae inside the kernels, and their feces, could also have contributed to the volatiles emitted (Mattiacci et al., 1999, Steidle, 2000; Rogers and Potter, 2002; Steiner et al., 2007). The attractiveness of the different larval stages was also assessed by means of trials involving larvae-infested products of the different species. In these trials, which were only conducted by offering S. oryzae-infested rice as an alternative to L. serricorne-infested wheat flour, the latter proved the more attractive. The hypothesis that larvae in flour are more accessible than those concealed inside kernels may explain why the parasitoids seemed to prefer flour to rice, though they also seemed to prefer hosts which were concealed in grain. In the case of R. dominica-infested rice against L. serricorne-infested wheat flour, we had expected the odors coming from the cigarette beetle jar to be the more attractive, but this was

C. Belda, J. Riudavets / Biological Control 54 (2010) 29–34

not the case. Secondly, we decided to do trials with adults because there are other parasitoids that use cues coming from adult stages, detecting kairomones emitted by the integument, or pheromones (Cournoyer and Boivin, 2004). This was not, however, the case for the parasitoid that we studied, as adult stages were never preferred alone, in any of the trials, even against larvae-infested products of the same species and empty controls. The host on which a generalist parasitoid is reared can influence its preference and fitness, and adapting to a new host takes several generations (Steidle and Schöller, 2002; Cournoyer and Boivin, 2004). Nonetheless, in the trials conducted, we found that there were no significant differences between the host on which the parasitoids had been reared (S. oryzae) and other hosts offered when the reference host was R. dominica. Moreover, when the other host was L. serricorne-infested flour, it was preferred to the rice weevil. This shows that the parasitoid was probably more attracted to the flour in the first stage. Then, once flour or rice has been found, the parasitoid has to detect and parasitize either of the hosts if they are suitable. Host detection would define the intrinsic performance of the parasitoid. From our study, we can conclude that uninfested product was attractive to A. calandrae females either as rice or flour. If presented at the same time, flour was more attractive than brown rice, and paddy rice was preferred to brown rice. With the exception of T. confusum, larvae-infested products were more attractive than uninfested products or adults; adult stages were not attractive. As the larvae were not tested alone without rice or flour (Steidle and Schöller, 1997), we do not know if they emit attractive volatiles when alone. Although larvae are unlikely to be found alone in natural environments, this would be an interesting avenue for future research aimed at determining the specific cues involved. As host feces can also be an important attractant for parasitoids, additional trials could be conducted with isolated feces in order to see how parasitoids respond to them. Acknowledgments Special thanks to Dr. James Campbell and Dr. Frank Arthur for their help reviewing this manuscript. This work was supported by grants from the ‘‘Instituto Nacional de Investigación Agraria y Alimentaria: Subprograma Nacional de Recursos y Tecnologías Agrarias en Cooperación con las Comunidades Autónomas” and ‘‘INIA RTA 2008-00002-CO2-01 (FEDER)”; and Grant No. 64 from the ‘‘Programa de Becas Predoctorales para la formación de personal investigador” of the ‘‘Instituto Nacional de Investigación Agraria y Alimentaria (INIA)”. References Ahmed, K.S., 1996. Studies on the ectoparasitoid, Anisopteromalus calandrae How. (Hymenoptera: Pteromalidae) as a biocontrol agent against the lesser grain borer, Rhyzopertha dominica (Fab.) in Saudi Arabia. Journal of Stored Products Research 32, 137–140. Ahmed, K.N., Khatun, M., 1988. Lasioderma serricorne (F.), a possible alternate host of Anisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae) in Bangladesh. Bangladesh Journal of Zoology 16, 165–166. Ambriz, S.J., Strand, M.R., Burkholder, W.E., 1996. Behavioral response of the parasitoid Lariophagus distinguendus (Forst) (Hymenoptera: Pteromalidae) to extracts from cocoons of Lasioderma serricorne Fab. (Coleoptera: Anobiidae) and their effects on subsequent oviposition responses. Biological Control 6, 51–56. Arbogast, R.T., Mullen, M.A., 1990. Interaction of maize weevil (Coleoptera: Curculionidae) and parasitoid Anisopteromalus calandrae (Hymenoptera: Pteromalidae) in a small bulk of stored corn. Journal of Economic Entomology 83, 2462–2468. Benz, G., 1987. Integrated Pest Management in material protection, storage and food industry. In: Delucchi, V. (Ed.), Protection Integrée Quo vadis?, vol 86. Springer, pp. 31–69. Brower, J.H., Parker, R., Cogburn, R., 1991. Biologicals: insect diseases, insect parasites and predators. In: Krischik, V., Cuperus, G., Galliart, D. (Eds.), Management of Grain, Bulk Commodities and Bagged Products. U.S. Dep. Agric. Coop. Ext. Serv. Circ. E-912, pp. 219–225.

33

Burkholder, W.E., 1970. Pheromone research with stored product coleopteran. In: Wood, D.L., Silverstein, R.M., Nakajima, M. (Eds.), Control of Insect Behavior by Natural Products. Academic Press, New York, USA, pp. 1–20. Cournoyer, M., Boivin, G., 2004. Infochemical-mediated preference behavior of the parasitoid Microctonus hyperodae when searching for its adult weevil hosts. Entomologia Experimentalis et Applicata 112, 117–124. Cline, L.D., Press, J.W., Flaherty, B.R., 1985. Suppression of the rice weevil, Sitophilus oryzae (Coleoptera: Curculionidae) inside and outside of burlap, woven polypropylene, and cotton bags by the parasitic wasp Anisopteromalus calandrae (Hymenoptera: Pteromalidae). Journal of Economic Entomology 78, 835–838. Du, Y.J., Poppy, G.M., Powell, W., 1996. Relative importance of semiochemicals from first and second trophic levels in host foraging behaviour of Aphidius ervi. Journal of Chemical Ecology 22, 1591–1605. Gauthier, N., Monge, J.P., 1999. Behavioral and physiological responses to conflicting oviposition stimuli in a synovigenic parasitoid. Physiological Entomology 24, 303–310. Ghani, M.A., Sweetman, H.L., 1955. Ecological studies on the granary weevil parasite Aplastomorpha calandrae (Howard). Biologia 1, 115–139. Ghimire, M.N., Phillips, T.W., 2007. Suitability of five species of stored product insects as hosts for development and reproduction of the parasitoid Anisopteromalus calandrae (Hymenoptera: Pteromalidae). Journal of Economic Entomology 100, 1732–1739. Giles, D.K., Heinz, K.M., Parrella, M.P., 1996. Quantitative assessment of insect olfactometer performance by experimental flow analysis. Biological Control 7, 44–47. Gorham, J.R., 1979. The significance for human health of insects in food. Annual Review of Entomology 24, 209–224. Haliscak, J.P., Beeman, R.W., 1983. Status of malathion resistance in five genera of beetles infesting farm-stored corn, wheat and oats in the United States. Journal of Economic Entomology 76, 717–722. Hong, Y.S., Ryoo, M.I., 1991. Effect of temperature on the functional and numerical responses of Lariophagus distinguendus (Hymenoptera: Pteromalidae) to various densities of the host Sitophilus oryzae (Coleoptera: Curculionidae). Journal of Economic Entomology 84, 837–840. Jembere, B., Ngi-Song, A.J., Overholt, W., 2003. Olfactory responses of Cotesia flavipes (Hymenoptera: Braconidae) to target and non-target Lepidoptera and their host plants. Biological Control 28, 360–367. Lucas, E., Riudavets, J., 2002. Biological and mechanical control of Sitophilus oryzae (Coleoptera: Curculionidae) in rice. Journal of Stored Product Research 38, 293– 304. Mattiacci, L., Hütter, E., Dorn, S., 1999. Host location of Hyssopus pallidus, a larval parasitoid of the codling moth, Cydia pomonella. Biological Control 15, 241–251. Menon, A., Flinn, P.W., Barry, A., Dover, B.A., 2002. Influence of temperature on the functional response of Anisopteromalus calandrae (Hymenoptera: Pteromalidae), a parasitoid of Rhyzopertha dominica (Coleoptera: Bostrichidae). Journal of Stored Product Research 38, 463–469. Meyhöfer, R., Casas, J., 1999. Vibratory stimuli in host location by parasitic wasps. Journal of Insect Physiology 45, 967–971. Mohan, S., Fields, P.G., 2002. A simple technique to assess compounds that are repellent or attractive to stored product insects. Journal of Stored Products Research 38, 23–31. Powell, W., Pennachio, F., Poppy, G.M., Tremblay, E., 1998. Strategies involved in the location of hosts by the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae). Biological Control 11, 104–112. Press, J.W., 1988. Movement of a weevil parasitoid Anisopteromalus calandrae (Howard), within a column of wheat in relation to host location. Journal of Agricultural Entomology 5, 205–208. Press, J.W., Mullen, M.A., 1992. Potential of the weevil parasitoid Anisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae), for protecting commercially packaged wheat from infestation by the rice weevil Sitophilus oryzae (L.) (Coleoptera: Curculionidae). Journal of the Kansas Entomological Society 65, 348–351. Riudavets, J., Lucas, E., Pons, M.J., 2002. Insect and mites of stored products in the northeast of Spain. Integrated protection in stored products. IOBC WPRS Bulletin 25, 41–44. Rogers, M.E., Potter, D.A., 2002. Kairomones from scarabaeid grubs and their frass as cues in below-ground host location by the parasitoids Tiphia vernalis and Tiphia pygidialis. Entomologia Experimentalis et Applicata 102, 307–314. Rojas, J.C., Castillo, A., Virgen, A., 2006. Chemical cues used in host location by Phymastichus coffea, a parasitoid of coffee berry borer adults, Hypothenemus hampei. Biological Control 37, 141–147. SAS Institute, 2002. Enterprise Guide v2.0. SAS Institute, Cary, NC. Schöller, M.E., Flinn, P.W., Grieshop, M.J., Zd’árková, E., 2006. Biological control of stored product pests. In: Heaps, J.W. (Ed.), Insect Management for Food Storage and Processing, second ed. AACC International, Minnesota, USA, pp. 67–87. Shin, S.S., Chun, Y.S., Ryoo, M.I., 1994. Functional and numerical responses of Anisopteromalus calandrae and Lariophagus distinguendus (Hymenoptera: Pteromalidae) to the various densities of an alternative host, Callosobruchus chinensis. Korean Journal of Entomology 24, 199–206. Steidle, J.L.M., 2000. Host recognition cues of the granary weevil parasitoid Lariophagus distinguendus. Entomologia Experimentalis et Applicata 95, 185– 192. Steidle, J.L.M., Schöller, M., 1997. Olfactory host location and learning in the granary weevil parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). Journal of Insect Behaviour 10, 331–342.

34

C. Belda, J. Riudavets / Biological Control 54 (2010) 29–34

Steidle, J.L.M., Schöller, M., 2002. Fecundity and ability of the parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae) to find larvae of the granary weevil Sitophilus granarius (Coleoptera: Curculionidae) in bulk grain. Journal of Stored Product Research 38, 43–53. Steidle, J.L.M., Steppuhn, A., Reinhard, J., 2001. Volatile cues from different host complexes used for host location by the generalist parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). Basic and Applied Ecology 2, 45– 51. Steidle, J.L.M., Steppuhn, A., Ruther, J., 2003. Specific foraging kairomones used by a generalist parasitoid. Journal of Chemical Ecology 29, 131–143. Steinberg, S., Dicke, M., Vet, L.E.M., Wanningen, R., 1992. Response of the braconid parasitoid Cotesia (=Apanteles) glomerata to volatile infochemicals: effects of bioassay set-up, parasitoid age and experience and barometric flux. Entomologia Experimentalis et Applicata 63, 163–175. Steiner, S., Steidle, J.L.M., Ruther, J., 2007. Host-associated kairomones used for habitat orientation in the parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). Journal of Stored Product Research 43, 587–593. Trematerra, P., Fontana, F., Mancini, M., Sciarretta, A., 1999. Influence of intact and damaged cereal kernels on the behaviour of the rice weevil, Sitophilus oryzae (L.) (Coleoptera: Curculionidae). Journal of Stored Product Research 35, 265–276. Turlings, T.C.J., Wäkers, F.L., Vet, L.E.M., Lewis, J., Tumlinson, H., 1993. Learning of host-finding cues by hymenopterous parasitoids. In: Papaj, D.R., Lewis, A.C. (Eds.), Insect Learning. Chapman and Hall, New York, USA, pp. 51–78. Turlings, T.C.J., Bernasconi, M., Bertossa, R., Bigler, F., Caloz, G., Dorn, S., 1998. The induction of volatile emissions in maize by three herbivore species with different feeding habits: possible consequences for their natural enemies. Biological Control 11, 122–129.

Van Tol, R.W.H.M., Visser, J.H., Sabelis, M.W., 2002. Olfactory responses of the vine weevil, Otiorynchus sulcatus, to tree odors. Physiological Entomology 27, 213– 222. Vet, L.E.M., Dicke, M., 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37, 141–172. Vet, L.E.M., Van Lenteren, J.C., Heymans, M., Meelis, E., 1983. An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects. Physiological Entomology 8, 97–106. Vinson, S.B., 1976. Host selection by insect parasitoids. Annual Review of Entomology 21, 109–133. Wei, L., Kang, L., 2006. Electrophysiological and behavioral responses of a parasitic wasp to plant volatiles induced by two leaf miner species. Chemical Senses 31, 467–477. Wen, B., Brower, J.H., 1994. Suppression of maize weevil, Sitophilus zeamais (Coleoptera: Curculionidae), populations in drums of corn by single and multiple releases of Anisopteromalus calandrae (Hymenoptera: Pteromalidae). Journal of the Kansas Entomological Society 67, 331–339. Williams, R.N., Floyd, E.H., 1971. Effect of two parasites Anisopteromalus calandrae and Choetosphila elegans, upon populations of the maize weevil under laboratory and natural conditions. Journal of Economic Entomology 64, 1407– 1408. Zettler, L., Beeman, R., 1991. Resistance to chemicals. In: Krischik, V., Cuperus, G., Galliart, D. (Eds.), Management of Grain, Bulk Commodities and Bagged Products. U.S. Dep. Agric. Coop. Ext. Serv. Circ. E-912, pp. 163–166. Zettler, J.L., Cuperus, G.W., 1990. Pesticide resistance in Tribolium castaneum (Coleoptera: Tenebrionidae) and Rhyzoperta dominica (Coleoptera: Bostrichidae) in wheat. Journal of Economic Entomology 83, 1667–1681.