ABSTRACT: By definition, a parasitoid kills the organism it parasitizes. A wasp uses host location cues to aid in finding host organisms. Host location is essential to parasitoid wasp procreation and different species use different location behaviors. Parasitoid wasps locate their hosts in several ways including odor orientation, and infrared detection. Plant volatiles are also made more attractive to parasitoids when oral secretions or anal excretions are left on the damaged plant by the feeding host insects. These airborne semiochemicals lead wasps to microhabitats inhabited by their hosts. This unique form of host location allows the wasp predator to find its prey without visual or chemical cues. Host locating behavior while interesting to the observer is essential to the survival of parasitoid wasp species. Many factors play a role in the host location behavior of parasitoid wasps. Each is a clue aiding in the parasitoid’s search for host insects. A wasp that is searching for a host can recognize landmark cues. Wasps also respond to color. Chemosensory cues or infochemicals utilized by parasitoid wasps can be divided into two groups: non-volatile and volatile. Most prey items of parasitoid wasps are phytophagous, meaning they feed on plants. This characteristic of hosts can be exploited by wasp predators. When host larvae feed on plants they damage the plant and coat the wounds they cause with kairomones. Kairomone chemicals can also be called elicitor chemicals because they ‘elicit’ a chemical response from the host plant. The synomone compounds produced by the plant (sometimes referred to as terpenes and sesquiterpenes) are highly attractive to parasitoid wasps and produced systemically. Different species of host insect elicit different plant responses. Some parasitoid wasps depend on another sensory device in cooperation with photosensory and chemosensory cues. These wasps are called specialized wasps because they only parasitize a particular species of larvae. Wasps use a collection of sensory responses to particular cues as another cue to motivate the wasp to repeat or change particular host locating behaviors. The wasps begin assimilating their sensory cues once they emerge from the cocoon. The wasps link a landmark cue with a particular group of plants, volatile chemical information with non-volatile information, and infrared detection with the host mining beneath the bark surface; they associate one cue with another to locate hosts. Parasitoid wasps display some innate foraging attractions to certain plants. Most parasitoid hosts are crop herbivores. A wasp will recognize particular cues (photosensory, chemosensory, and thermosensory) and associate them with a particular host item. Once the association of cue and host is made, the wasp can initiate other host locating responses. These responses of the wasp can be trained. Host location is a complex and many faceted behavior among parasitoid wasps. Host location behavior is a group of responses to a number of different cues. Parasitoid wasps demonstrate the ability to collect these cues and previous responses to them to make their own cues, (called learned cues in this paper).
KEYWORDS: Parasitoid (Hymenoptera) wasps; host location; sensory cues; learning; biological control.
 

DISCUSSION:

 INTRODUCTION

 A parasitoid is an insect that develops inside another living organisms and in the course of that development kills the host organism. Thus, it is critical to the life cycle of a parasitoid species to have adequate means of finding hosts for parasitism. Many factors play a role in the host location behavior of parasitoid wasps. They contribute to the persistence of the parasitoid insect in its environment. Each is a clue aiding in the parasitoid’s search for host insects. Among these factors or clues are chemosensory, photosensory, and thermosensory cues providing the wasps with information regarding the location of its prey. In addition, the wasps are provided with learning cues. Each of the four factors, the sensory cues and learning, that contribute to host location are described and discussed in this paper. Also discussed is the application of parasitoid wasps as a means of bio-control for crop pests.

CHEMOSENSORY CUES

 Infochemicals work to provide the parasitoid wasp with a trail to follow to host insects. Chemosensory cues, or infochemicals, utilized by parasitoid wasps can be divided into two groups: non-volatile and volatile. Non-volatile chemicals are usually produced by the host insect in oral secretions while feeding and the anal excretions (or frass) left behind. They are sometimes referred to as kairomones because they benefit the receptor of the chemical and not the producer. Non-volatile chemicals are defined as such because they do not disburse well into the atmosphere, and are therefore undetectable to the wasps at long range. (7) Volatile chemicals –those that do disburse well into the atmosphere are produced by the host plants; these infochemicals are detectable over long distances.

Volatile chemicals, sometimes called synomones, are systemically produced only by damaged plants and only in large amounts by plants that are damaged due to insect feeding. (While most plants will produce some synomones when damaged by means other than feeding, only plant damage due to insect infestation will produce large quantities of synomone.) (9, 10, 11, & 12) Most prey items of parasitoid wasps are phytophagous, meaning they feed on plants. This characteristic of hosts can be exploited by wasp predators. When host larvae feed on plants, they damage the plant and coat the wounds they cause with kairomones found in their saliva and frass. Kairomone chemicals can also be called elicitor chemicals because they ‘elicit’ a chemical response from the host plant. In their experiments Turlings et al. demonstrated that plants placed in regurgitate (presumed to contain elicitors) of beet armyworm responded by producing volatile synomone compounds.

Only kairomones elicited the synomone production response (versus water or exposure to another chemical). The synomone compounds produced by the plant (sometimes referred to as terpenes and sesquiterpenes) are highly attractive to parasitoid wasps and produced systemically. Only a wounded plant will produce terpenes and sesquiterpenes and when it does, it produces them en masse. Not only can the synomones be found in damaged leaves, but in undamaged leaves and the stem as well. (9, 10, 11, & 12) In effect, the entire plant sends out a “distress signal”, which can be manipulated by the wasps over long distances as a location cue for probable hosts. (9) The terpenes are good cues for the wasps because they continue to be released even when the host insects pause in their feeding-for up to several hours or even days. (8, 9, & 12) In addition, the plant stands out -chemically speaking- next to healthy (not infested) plants. (9) The plant will also emit a specific amount of a specific synomone for a specific elicitor. (6) Different species of host insect elicit different plant responses. (10 & 11) In this manner, a parasitoid can not only identify which plants are infested, but with which insect they are infested also. The volatile chemosensory cues (synomones) are more strongly attractive to the wasps than the non-volatile cues (kairomones) which exclusively elicit the synomone production response. Thus, neither infochemical is more important than the other is. However, it has been demonstrated that a plant–host complex of infochemicals is more highly attractive than frass-containing kairomones or plants emitting synomone distress signals. (8) Regardless, chemosensory cues emitted by a host insect, a host infested plant or both are key in helping the parasitoid wasp to locate its host. It is difficult for the wasp to find a host without the semiochemical cues left in a sort of trail by the hosts themselves and the plants they are feeding on.

PHOTOSENSORY CUES

   Photosensory cues or visual stimuli are generally represented by landmarks, shapes, and colors. A wasp that is searching for a host can recognize landmark cues. They tell the wasp where it has been, areas it has searched before, and areas that have not been searched previously. Most importantly, they help the wasp when its chemosensory perception is impaired by wind or encountered with conflicting semiochemical information.

In addition, wasps can recognize shapes –taking on an attack posture when encountered with a shape that is not familiar. Wasps also respond to color. For example, aphids darkened by chemical treatment were rejected by host-seeking parasitoids. (6) Some wasps respond to the reflected light from a color. They will attack hosts that appear to be the wrong color to human eyes because the wavelengths of light are similar to those produced by the actual color of the host. (6) In both situations, the wasp is using information communicated to it via visual stimuli. These photosensory cues help the wasp when searching out a host.

Visual stimuli can aid the wasp particularly when wind disrupts olfactory stimuli. (15) However, they have drawbacks that can make them secondary to chemosensory cues. Stimuli that require photoreceptivity can be obstructed from vision or altered by changes in perspective, and they are usually light intensity dependent. Consequently, photosensory cues although important are usually too few, and unreliable to be used independent of other sensory “modalities”, particularly chemosensory.(15)

THERMOSENSORY CUES

 While thermoreceptivity is not widely used among parasitoids, it is as important to the specialized wasps as other sensory reception to generalist wasps. Some parasitoid wasps depend on another sensory device in cooperation with their photosensory and chemosensory cues. These wasps are called specialized wasps because they only parasitize a particular species of wood-boring larvae. These specialized wasps must find their hosts through a layer of bark. They cannot use photosensory or chemosensory cues to locate the hosts (through the bark) only their hosts’ habitat (the tree).

Next, they use thermosensory cues detected by special sensillum on their antennae to detect infrared radiation and locate hosts. (7) Wood-boring larvae produce heat metabolically as they grow and mine their way to the outer surface of the tree for emergence. (7) Wasps that alight on the bark use their antennae like a divining rod, but instead of searching for water, they are searching for infrared radiation produced by the larvae. The wasps are able to detect heat and thereby locate hosts for oviposition in a way otherwise impossible with only photo and chemoreceptors.

LEARNED CUES

 Wasps to learn and retain cues to aid in the location of host organisms for future use. (1) D.R. Papaj said, “learning is…a mechanism by which an organism copes with the capricious nature of its environment…any change in behavior with experience.” (5,6, & 13) Wasps use this “mechanism” to sort the many cues they receive while looking for hosts. In the same way, they also make a collection of cues to use again on new foraging endeavors. In fact, Papaj et al. observed parasitoids that “…were actually receiving and storing information about their semiochemical environment and adopting behavior consistent with that information.” (5) Wasps are able to learn (usually by association); they can collect a positive oviposition experience with one or more multi-sensory cues and store it for future use. This collection of sensory responses to particular cues can be called a learning cue motivating the wasp to repeat or change particular host locating behaviors when encountered with cues already stored in their cue collection. (6) The wasps begin assimilating their sensory cues once they emerge from the cocoon. (There is some evidence that the collection of cues starts even earlier while the wasp is still in the egg, but that is not discussed in this paper). (14) The wasps link a landmark cue with a particular group of plants, volatile chemical information with non-volatile information, and infrared detection with the host mining beneath the bark surface; they associate one cue with another to locate hosts. (9)

Parasitoid wasps display some innate foraging attractions to certain plants; demonstrating a preference for some chemosensory cues upon emergence. (3) However, a wasp’s innate knowledge is often insufficient in light of the enhancements that come with learning. (6) For example, a wasp that is allowed to oviposit on a host that she has used sensory cues to find will store the cues, recall them, and use them again for up to seven days after the initial oviposition experience. Therefore, an experienced parasitoid (one with a greater amount of learned cues stored) can locate a host’s habitat in a shorter amount of time and consequently find more hosts than a “naïve”, (inexperienced) wasp. (5) These abilities to associate cues one with another and use them to make host location more efficient show how wasps employ learned cues.

APPLICATION

 Information regarding parasitoid wasps use of cues is helpful to learn about their behavior, but it can also be exploited as a bio-control agent. Biological control is the manipulating of an organism to exploit its predation on another organism leading to reduction or elimination of the prey population.
Most parasitoid hosts are crop herbivores. This means that they feed on plants of economical importance to humans. Plants of economical value include crop plants, like corn, wheat, and cotton, garden plants like tomatoes and cabbage, and orchard plants like grape vines and apple trees. Each of these plants may be fed upon by one or more insect species and in the process the insects damage the plant and lower its economic value.

Agriculturists and horticulturists are trying to find ways to effectively manage phytophagous insects that can severely damage plants and decrease profits. There are many ways of preventing heavy losses due to insect infestation. The idea for using parasitoid wasps as a means of control versus insecticide application provides an alternative to spraying toxic chemicals on all the inhabitants of a particular plant complex. A parasitoid usually has a narrow target range (it only parasitizes a relatively few insects). While chemicals usually effect most all insects, including those that are beneficial (like the wasps) and those that are harmful. Since the wasp is a living organism it will stay in an area and continue to procreate and provide control for as long as it is near a population of host insects. Whereas, insecticides evaporate into the atmosphere and leach into the soil. More important than either of these characteristics for bio-control is the wasp’s ability to learn. A wasp will recognize particular cues (photosensory, chemosensory, thermosensory, and learned cues) that associate them with a particular host item. Once the association of cue and host is made, the wasp can initiate other host locating responses. These responses of the wasp can be trained. This training, or “conditioning” provides a reward for a particular response. This means a wasp can be trained to seek out something as unfamiliar as the odor of vanilla if the appropriate infochemicals (kairomones and synomones) are associated with the vanilla compounds. In this way, generalist wasp can be made into specialized wasps parasitizing specific crop garden, and orchard pests.

CONLUDING REMARKS

 Host location is a complex and many faceted behavior among parasitoid wasps. Host location behavior is a group of responses to a number of different cues. Each cue provides the parasitoid with important information by means of stimuli. Each sensory stimulus is received in a different way, but all provide information critical to the survival of the species. Parasitoid wasps demonstrate the ability to collect these cues and previous responses to them to make their own cues, (called learned cues in this paper). Learned cues can be manipulated by humans in order to magnify the benefits of parasitoid-crop pest interactions for bio-control. In this way, studies of parasitoid wasps and their means of host location are extremely beneficial.

ACKNOWLEDGEMENTS: The author is grateful for thought provoking discussions with her peers, but claims responsibility for the research of this paper and the assimilation of the ideas collected therein. Special thanks to Sandra Molitoris, for her constructive criticisms and editing.

REFERENCE CITATIONS:

1. Alcock, J. 1998. Chapter 1. An evolutionary approach to animal behavior. Animal behavior. Sinauers Associates, Inc. Publishers. Sunderland, Massachusetts.

2. Bjostad, L. 1998.Personal communication. Colorado State University. Fort Collins, Colorado.

3. Grasswitz, T.R. 1998. Effect of the adult experience on the host  location behavior of the aphid parasitoid. Biological Control. 12: 177-181.

4. Lewis, W.J., J.H. Tumlinson. 1988. Host detection by chemically  mediated associative learning in a parasitic wasp. Nature. 331: 257-259.

5. Papaj, D.R. and L.E.M. Vet, 1990. Odor learning and foraging success  in the parasitoid Leptopilina heterotoma. Journal of Chemical Ecology. 16: 3137-3150.

6. Powell, W., F. Pennacchio, G.M. Poppy, and E. Tremblay. 1998. Strategies involved in the location of hosts by the parasitoid  Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae). Biological Control. 11(2): 104-112.

7. Richerson, J.V. and J.H. Borden.1972. Host finding by heat  perception in Coeloides brunneri (Hymenoptera: Braconidae). Canadian Entomologist. 104: 1877-1881.

6. Steinberg, S., M. Dicke, and L.E.M. Vet. 1993. Relative  importance of infochemicals from first and second trophic level  in long range host location by the larval parasitoid Cotesia  glomerata. Journal of Chemical Ecology. 19(1): 47-59.

7. Tumlinson, J.H., W.J. Lewis, and L.E.M. Vet. How parasitic wasps  find their hosts. Scientific American. 268(3): 100-106.

8. Tumlinson, J.H., T.C.J. Turlings, and W.J. Lewis. Semiochemically  mediated foraging behavior in beneficial parasitic insects. 1993. Archives of Insect Biochemistry and Physiology. 22(3-4): 385-391

9. Turlings, T.C.J., P.J. McCall, H.T. Alborn, and J.H. Tumlinson. An  elicitor in caterpillar oral secretions that induces corn seedlings to emit chemical signals attractive to parasitic wasps. Journal of Chemical Ecology. 19(3): 411-425.

10. Turlings, T.C.J., J.H. Tumlinson, and W.J. Lewis. 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250: 1251-1254

11. Vet, L.E.M., W.J. Lewis, D.R. Papaj, and J.C. van Lenteren. 1990. A variable-response model for parasitoid foraging behavior. Journal of Insect Behavior 3(4): 471-490.

12. Vinson, S.B. and J.H. Williams. 1991. Host selection behavior of  Campoletis sonorensis: a model system. Biological Control 1: 107-117.

13. Wackers, F.L., and W.J. Lewis. 1994. Olfactory and visual learning and their combined influence on host site location by the parasitoid Microplitis croceipes (Cresson). Biological Control. 4(2): 105-112.