Foraging Behavior of Egg-Parasitoid Wasps Applied In The. Biological Control of Agricultural Pests
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1 Foraging Behavior of Egg-Parasitoid Wasps Applied In The Biological Control of Agricultural Pests Amanda Caivano Xavier Pereira Colorado State University Fort Collins Abstract Egg-parasitoid wasps have been used in the agriculture as an efficient biological control agent of insect-pests 1. Host searching by egg parasitoids faces a big challenge due to their low ability to find cues from the eggs itself 2. Therefore, these parasitoids had to find another way to look for their host, which made them develop a seek mechanism based in chemical cues from plant volatiles, adult hosts and its products 3. To overcome the problem of low dectability of host eggs, the egg-parasitoid Telenomus podisi seems to use egg volatiles and synthetic sex pheromone of certain bug species in its chemotaxic behavior while searching for the host 4. Moreover, the limited flight capability of many egg parasitoid wasps is also a problem that they have to deal with, being the hitchhiking on the adult host one of the strategies developed for them to find fresh-eggs 3. Some studies have shown the ability developed by the wasps to find their host through the follicular secretion used by the adult-host to glue the eggs on the plant 5 and also through induced synomones, emitted as a consequence of the pest activity on the plant. Those synomones that are adsorbed by the epicuticular waxes of leaves are used as cues and perceived by the egg parasitoid Trissolcus brochymenae 6. Furthermore, the oviposition of some insects on maize leaf surface induces plant synomones that with kairomonal cues also increases the efficiency in the searching by the parasitoid 2. Aiming a more efficient use of these parasitoids in agricultural pest control, the application of certain volatile compounds of bugs on the field have also been studied and showed efficiency to increase recruitment of certain parasitoid wasps in infected soybean fields 7. In this review article, many kinds of cues used by 1
2 many species of egg-parasitoid wasps in their seeking for hosts are discussed, focusing on the biological control of pests. Short-range flight capacity determined by the host Trichogrammatids (Hymenoptera: Trichogrammatidae) are known as an important group of egg parasitoids used in the control of lepidopteran pests in agriculture 8. Trichogrammatoidea annulata De Santis, Trichogramma atopovirilia Oatman and Platner and Trichogramma bruni Nagajara are three Trichogrammatids species used as a biological control in Brazil that had their short-range flight capacity studied and analyzed in three different hosts: Anagasta kuehniella (Zeller), Corcyra cephalonica (Stainton) and Sitotroga cerealella (Olivier) 9. Some parasitoid biological traits are measured in laboratory for evaluating the quality of mass-produced Trichogramma spp. The flight capacity is a new criterion that has been suggested to be incorporated into quality control 10, what makes the study of the flight-range capacity of parasitoid eggs be a great tool for increasing the efficiency in the creation of parasitoids in laboratory, and therefore, on the field. Parasitoid flight capacity was tested on the 10th and 28th generations on the three different hosts, and performed inside a dark chamber. The short-range flying response was determined by the amount of adults found on the bottom and trapped to the sticky top 9. Results shown that the flight capacity of all the trichogrammatids were reduced when emerged from S. cerealella and the highest capacity of T. annulata was showed when reared on C. cephalonica, while for T. atopovirilia was on A. kuehniella and for T. bruni was on both. That way is possible conclude that, according these studies, S. cerealella reflect in a lower short-range flight capacity of these trichogrammatids and it should not be used as a host to mass-produce the egg-parasitoids. Influence of visual cues on host-searching and behavior 2
3 Egg parasitoid wasps use several different cues when foraging for their hosts 11. Among these cues, one that might influence the search for the eggs could be color in association with the presence of hosts. To perform this study, females of two species of Hymenoptera (Scelionidae), Figure 1. Illustration of the experiments (A) Arena used in innate experiment, with five areas and Euschistus heros eggs in the centre. (B) Arena used in training session in multiple-choice experiment. (C) Multiple-choice experiment with training and test sessions. Telenomus podisi Ashmead and Trissolcus basalis Wollaston, had their behavior investigated with colored substrates after associative learning. The host chosen were eggs of Euschistus heros (Fabricius) (Hemiptera: Pentatomidae). The first experiment aimed to examine the innate preference for substrate colors. It was conducted in closed arenas divided into five coloured zones (yellow, green, brown, black, and white) and E. heros egg masses were placed in the centre of each colored area (Figure 1-A). The second experiment tested the associative learning of substrate color and host presence and it was tested in multiple-choice and dual-choice experiments (Figure 1- B,C). The results shown (Table 1 and 2) that the parasitoid are able to choose for colors, being yellow the preferred one and black the less preferred. The parasitoid females chose the associative learning without yellow substrates, the parasitoids were little influenced by the color of the substrate. In the experiments, the insect went through two different trails of 2 h with 1 h interval between them, that were insufficient to develop either short or long term memory. The preference for the yellow substrate might be related to the region of the visible spectrum in which their receptors respond preferentially 12 and may be connected to the orientation to plant foliage during the search for hosts in the field. 3
4 4
5 Influence of host egg volatiles on chemotaxic behavior The egg parasitoid Telenomus podisi is an important agent of control of two important agricultural pests: Euschistus heros and Tibraca limbativentris 4. Knowing that the success of the parasitism depend upon the parasitoid finding its host, studies were done in order to discover the influence of the original host on T. podisi chemotaxic behavior. The tests were performed both in laboratory and semi-field conditions and mated female of T. podisi that emerged from eggs of T. limbativentris and E. heros were compared. Females emerged from E. heros eggs preferred parasite eggs from their original host, and the same happened with females from T. limbativentris that chose parasite T. limbativentris over T. podisi eggs. It means that T. podisi is more likely to parasite the eggs from which it was developed, then the parasitoids orientation may have a connection with volatile cues associated with the original host, assimilated in some way through learning during the development of the immature stage. Hence, this information can be applied to the mass-creation of T. podisi that if reared on only one host it can become a specialist in parasite a target-pest. Differences in searching behavior of two strains of Telenomus busseolae It is known that among individuals of the same specie exist variability in physiology and behavior of different strains 13. Knowing these differences is very important to select the agent that has the best potential to be used in biological control programs. Telenomus busseolae Gahan (Hymenoptera: Scelionidae) is an egg parasitoid, which has been evaluated to a possible introduction into Italy as a bio-control agent of Corn Stalk Borer, Sesamia nonagrioides (Lefebvre) (Lepidoptera: Noctuidae). There are two parasitoid strains, one from Africa and another from Turkey, which had their walking and host selection behavior tested. The experiments of walking behavior were performed in laboratory in an olfactometer consisted of a round arena where the patterns were recorded for 3 minutes by a computer vision system. After, 5
6 experiments to analyze their host selection behavior mediated by the sex pheromone and body scales of the host were performed. To evaluate the parasitoid response to the synthetic host pheromone, the entrance and the exit of the air of the arena was controlled by a peristaltic pump. To evaluate the response of the parasitoid to host body scales, scales were brushed from ovipositing female moths and put into a circular zone. The results indicated that the African strain walk faster than the Turkish strain, and that it has a slower angular speed and lower turning rate. The African strain exhibited a significant increase in its speed of movement in response to the host s sex pheromone and a more intense local search after encountering host body scales. Both strains responded to the host pheromone, but the African females responded for longer and showed a stronger response under areas with scales. Therefore, it was possible to say that the African strain might be more effective in host searching; however, other experiments have to be performed in field conditions to show with more certain which strain would be more effective in the field to be introduced in Italy. Capacity for learning and memory An innate behavior can be modified by successive exposure to a particular host and can result in learning (memory), which can be retained for different periods of time 14. The egg parasitoid Telenomus podisi Ashmead is an important bio-control agent of stink bugs. As all the parasitoids, its success depends on the location of its host, which may be influenced by learning and memory. To analyze its capacity for learning and memory, a study was performed using lemongrass [Cymbopogon citratus (DC.) Stapf. (Poales, Poaceae)] extract at different developmental stages of the parasitoid immature phase. Eggs of Euschistus heros (Hemiptera, Pentatomidae) parasitized by T. podisi were isolated in glass tubes containing filter paper with lemongrass extract or acetone solvent (control). After emergence, T. podisi females (experienced and inexperienced to the scents) were tested in a Y-tube olfactometer containing both scents. To evaluate memory, females that emerged from eggs that were in contact with lemongrass extract were given a choice between lemongrass extract and acetone when they 6
7 were 24, 48, 72, and 96 hours old. The results showed that the inexperienced females chose acetone over lemongrass extract. It can be explained because the lemongrass extract has a substance called citral that is known as an insect repellent. However, the experienced females chose the lemongrass extract over the solvent, showing that the parasitoid probably related the odor, even being an insect repellent, to the presence of the plant or the host related to it. The presence of lemongrass during the immature developmental stage altered the chemotaxic orientation of T. podisi and stimulated learning in these organisms that lasted for up to 72 hours. These results may be applied to increase the efficiency of parasitism once parasitized postures could be exposed to eggs odors or even to the hosts pheromone, enabling learning and maximizing the success of parasitism. The use of pheromone cues as a mechanism to seek the host A series of stimuli, being chemical, physical or morphological, are used as strategies to parasitoid seek their hosts 4. It is known that parasitoids use semiochemicals to increase the efficiency to find their hosts, that are different from specie to specie. Telenomus podisi is an important parasitoid wasp of stink bug eggs, being T. limbativentris and E. heros two pests highly controlled by it. To analyze the attraction and chemotaxic response to a specific sexpheromone of T. limbativentris, studies were done placing a filter paper treated with zingiberenol solution (synthetic sex pheromone) and hexane (control) in an olfactomer. T. podisi females from E. heros hosts moved more (69.04%) in the direction of zingiberenol rather than to the control and the same occurred with the parasitoids from eggs of T. limbativentris that showed more preference to the sex pheromone (75%). Parasitoid wasps of the genus Trichogramma are also efficient in the control of many agricultural pests by parasitizing their eggs 15. It is known as an agent of control of the noctuid moth Heliothis virescens that has a nocturnal behavior. Nevertheless, in some way, their pheromone may be adsorbe onto host plants, so that wasps can use these cues during the day to 7
8 find the moth eggs. In one study, Trichogramma pretiosum (Hymenoptera, Trichogrammatidae) showed a combination of chemical espionage on a host sex pheromone with phoretic behaviour. T. pretiosum seemed to be less attached to high-hv (females with high ratio of the saturated 16:Ald to the unsaturated Z11-16:Ald in their sex pheromone) than to low-hv ( low ratio of these saturated to unsaturated compounds). The wasp also did not show a preference for separate sex pheromone compounds of H. virescens, but when pre-exposed to the major sex pheromone component they did show a preference, indicating learning behavior. It was also found that hitchhiking is a strategy used by these wasps to find moth eggs, one time that mated females were mounted significantly more than virgin females or males. It suggests that T. pretiosum could actually use the moth sex pheromone adhered to plants for close-range location of female moths, and then the location of their eggs. Knowing that wasps have the ability to find their hosts using chemical cues, the use of certain pheromones in field could be a good method to attract parasitoid wasps aiming the bio-control of a pest 7. To prove the efficacy of this method, one of the major components of metathoracic glands secretions of stink bugs, (E)-2-hexenal, was applied in soybean aiming the increase the abundance of Telenominaes to enhance stink bug egg parasitism in infested areas. The areas of soybean were treated with (E)-2-hexenal in a shortterm (one week) and in long-term (seven weeks) experiments. The abundance of Trissolcus spp. (Hymenoptera: Platygastridae: Telenominae) was evaluated with yellow sticky traps and the incidence and intensity of parasitism with sentinel eggs of Euschistus heros. In short-term experiments, there was an increase in abundance of Trissolcus spp. in treated areas, associated with greater intensity of parasitism. In long-term experiments, the treatment did not influence the abundance of Telenominae or parasitism levels. Therefore, applications of (E)-2-hexenal could be used to increase recruitment of Trissolcus spp. in the early flowering stages of soybean, also showing to be efficient to attract other natural enemies, which resulted in a significant increase on egg predation. The egg parasitoid Trissolcus brochymenae also shows response to kairomones from several stages of its host, Murgantia histrionica 5. Parasitoid females respond by increasing residence 8
9 time and reducing linear speed to chemical cues from gravid females, virgin females and males, fifth and third instars, and eggs. The parasitoid displayed arrestment behavior, increased residence time, changed walking pattern, and intense substrate examination. Influence of volatile compounds of plants Herbivore-induced plant volatiles are important host finding cues for egg parasitoids 19. The plant epicuticular crystalline waxes play an essential ecological function mediating interactions between the pest and the parasitoid 6. The footprints, oviposition and attack of Murgantia histrionica on cabbage plants induce synomones that are adsorbed by the epicuticular waxes of leaves and then perceived by the egg parasitoid T. brochymenae. Leaf portions with the abaxial lamina previously dewaxed and then contaminated by footprints of M. histrionica did not play a role in the parasitoid response, thus it might not be directly involved in the chemicals induced by M. histrionica footprints. Another study evaluated the influence of volatile organic compounds (VOCs) of soybean induced after attack of Euschistus heros on the searching behavior of the egg parasitoid Telenomus podisi 18. The results suggested that (E,E)-a-farnesene and methyl salicylatemight help T. podisi to determine the presence of stink bugs on a plant. Other bioassays were conducted to compare (E,E)-a-farnesene with the volatiles emitted by undamaged and damaged plants, to evaluate if this compound was the main cue used by T. podisi or if other minor compounds could also be used to locate its host. The results showed that other minor volatiles also play a hole in the host-searching behavior of T. podisi. The oviposition of Sesamia nonagrioides also induces changes in the cues present on maize leaf surface, which arrest females of T. busseolae ². The induction appears to be systemic as the parasitoid also responds to leaves and leaf portions that are not directly affected by ovipositing females. These plant-synomones, acting with the kairomonal cues from scales left on the plant by the ovipositing of S. nonagrioides, significantly increases parasitoid efficiency during host finding. 9
10 Two egg parasitoids, a generalist, Trichogramma pretiosum and a specialist, Telenomus remus also showed response to volatiles released by young maize plants that were treated with regurgitant from caterpillars of the moth Spodoptera frugiperda (Noctuidae) 19. The generalist egg parasitoid, T. pretiosum was innately attracted by volatiles from freshlydamaged while the specialist T. remus was attracted only to volatiles emitted from fresh and old damage after associating these volatiles with oviposition, seeming to be relied more in associative learning. The wasp Trichogramma brassicae also uses oviposition-induced cues from Brussels sprouts to locate eggs of the cabbage white butterflies Pieris brassicae and Pieris rapae that differ in their egg-laying behaviour 20. These plant cues are stimulated by the anti-aphrodisiac pheromones, compounds that are passed from males to females during mating. One studied showed that the feeding damage in rice made by the rice stem bug Tibraca limbativentris induces the release of 16 volatiles compounds of this plant 21. The main compounds induced were (E)-2-hexenal, (E)-2-octen-1-ol, methyl salicylate and α-muurolene, that significantly attracted Telenomus podisi females to the rice plants. The generalist egg parasitoid Ooencyrtus telenomicida, when exposed to volatiles from tomato plants in different conditions, were attracted only to volatiles produced by N. viridula adult-infested plants 17. It is well-known that when hosts move on a substrate, they can leave chemical trails that have a kairomonal effect on parasitoids 16. Epicuticularwaxes of plant foliage influence parasitoids random and trail-following searching by adsorbing substrate-borne kairomones (released by Figure 2. Random searching behavior of Trissolcus basalis elicited by substrate- borne kairomones of Nezara viridula Figure 3. Trail following behavior displayed by males of the parasitoid Metaphycus luteolus and elicited by substrate-borne pheromone by conspecific females. 10
11 their hosts or by producing oviposition), inducing contact synomones. Contact chemicals can generate two main searching behaviors: biased random search, and trail following search. Biased random search behavior (Figure 2) is characterized by ortho- and klino-kinetic reactions. The trail-following search (Figure 3) is a positive taxis response in which chemicals deposited on a substrate are followed by another organism that maintains contact with the substrate as it moves. Random searching behavior is more likely induced by cues indirectly associated with the target organism. Therefore, random research may be more profitable than trail following behavior in the case of indirect cues, such as substrate-borne indirect cues. Conclusion This paper summarizes the researches that have been conducted to discover more about how parasitoid wasps of eggs seek for their host. The parasitoids wasps seem to use many kinds of methods to find their hosts. Among them are phoresy, chemical cues from adults, eggs and even from attacked plants, which make these wasps so successful as bio control agents. Knowing the foraging dynamic of these wasps is very important because the efficiency of parasitism can be increased, laboratorial practices can be improved and the use of pesticides can become a second method of control of agricultural pests. 11
12 References 1 Carneiro, Tatiana R.; Fernandes, Odair A.. (2012) Interspecific interaction between Telenomus remus (Hymenoptera: Platygastridae) and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) on Spodoptera frugiperda (Lepidoptera: Noctuidae) eggs. An. Acad. Bras. Ciênc Salerno G, De Santis F, Iacovone A, Bin F, Conti E (2013) Short-range cues mediate parasitoid searching behavior on maize: the role of oviposition-induced plant synomones. Biol Control 64: Fatouros, N.E., Dicke, M., Mumm, R., Meiners, T. & Hilker, M. (2008) Foraging behavior of egg parasitoids exploiting chemical information. Behavioral Ecology 19, Tognon R., Sant Ana J. and Jahnke, S.M. (2014) Influence of original host on chemotaxic behaviour and parasitism in Telenomus podisi Ashmead (Hymenoptera: Platygastridae). BULLETIN OF ENTOMOLOGICAL RESEARCH 104, Conti, E., Salerno, G., Bin, F., Williams, H.J. & Vinson, B. (2003) Chemical cues from Murgantia histrionica eliciting host location and recognition in the egg parasitoid Trissolcus brochymenae. Journal of Chemical Ecology 29, Frati F, Salerno G, Conti E (2013) Cabbage waxes affect Trissolcus brochymenae response to shortrange synomones. Insect Sci. doi: /j x 7 Vieira, Cecilia Rodrigues; Blassioli-Moraes, Maria Carolina; Borges, Miguel; et al. (2014) Field evaluation of (E)-2-hexenal efficacy for behavioral manipulation of egg parasitoids in soybean. BIOCONTROL 59, Sithanantham S, Chandish RB, Jalali SK, Bakthavatsalam N, Biological control of insect pests using egg parasitoids. Springer, New Delhi. 9 Dias-Pini, N. S.; DaSilva, C. S. B.; Penaflor, M. F. G. V.; et al., Does host determine short-range flight capacity of trichogrammatids. JOURNAL OF APPLIED ENTOMOLOGY 138, Edição: 9, van Lenteren JC, Need for quality control of massproduced biological control agents. In: Quality control and production of biological control agents: theory and testing procedures. Ed. by van Lenteren JC, CABI Publishing, Wallingford, de Aquino MFS, Dias AM, Borges M, Moraes MCB, Laumann RA (2012) Influence of visual cues on host-searching and learning behaviour of the egg parasitoids Telenomus podisi and Trissolcus basalis. Entomol Exp Appl 145: Brown PE, Frank CP, Groves HL & Anderson M (1998) Spectral sensitivity and visual conditioning in the parasitoid wasp Trybliographa rapae (Hymenoptera: Cynipidae). Bulletin of Entomological Research 88:
13 13 Colazza, S., Rosi, M.C., Differences in the searching behaviour of two strains of the egg parasitoid Telenomus busseolae (Hymenoptera: Scelionidae). European Journal of Entomology 98, Tognon, R., Sant Ana, J. & Jahnke, S.M. (2013) Learning and memory in Telenomus podisi (Hymenoptera, Platygastridae). Iheringia Série Zoologia 103, Xu, Jinzhu; Huigens, Martinus E.; Orr, David; et al.(2014). Differential response of Trichogramma wasps to extreme sex pheromone types of the noctuid moth Heliothis virescens. XECOLOGICAL ENTOMOLOGY, 39 p: Colazza S, Cusumano A, Lo Giudice D, Peri E (2014) Chemoorientation responses in hymenopteran parasitoids induced by substrate-borne semiochemicals. BioControl 59: Peri, E.; Cusumano, A.; Agro, A.; et al. (2011) Behavioral response of the egg parasitoid Ooencyrtus telenomicida to host-related chemical cues in a tritrophic perspective. BIOCONTROL, p Michereff, Mirian F. F.; Borges, M.; Laumann, R..; et al. (2013) Influence of volatile compounds from herbivore-damaged soybean plants on searching behavior of the egg parasitoid Telenomus podisi. ENTOMOLOGIA EXPERIMENTALIS ET APPLICATA, 147 p Penaflor, M. F. G. V.; Erb, M.; Miranda, L. A.; et al. (2011) Herbivore-Induced Plant Volatiles Can Serve as Host Location Cues for a Generalist and a Specialist Egg Parasitoid. JOURNAL OF CHEMICAL ECOLOGY, 37 p Pashalidou, F.G., Huigens, M.E., Dicke, M. & Fatouros, N.E. (2010) The use of oviposition-induced plant cues by Trichogramma egg parasitoids. Ecological Entomology, 35, Melo M., R. C.; St'Ana, J.; Blassioli-Moraes, M. C.; et al. (2014) Herbivory-induced plant volatiles from Oryza sativa and their influence on chemotaxis behaviour of Tibraca limbativentris stal. (Hemiptera: Pentatomidae) and egg parasitoids. BULLETIN OF ENTOMOLOGICAL RESEARCH, 104 p
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