L.E.M. Vet

Parasitoid Foraging and Learning

The diminutive size of most parasitoids undoubtedly has limited their choice as subjects for behavioral study, despite their great diversity in lifestyles and reproductive strategies. The present chapter addresses their foraging behavior as influenced by learning. Most of their adult life female parasitoids search for host insects which, in turn, are under selection to avoid being found and devoured. This scenario sets the stage for the evolution of diverse hide-and-seek games played by parasitoids and their victims, most often herbivores. That parasitoids are successful in their quest for hosts is evidenced by the vast number of parasitoid species and their importance in insect management.

An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects

ABSTRACT. A new type of airflow olfactometer is described, and results given of experiments using it to measure behavioural olfactory responses of hymenopterous parasitoids. Compared with Y‐tube olfactometers it shows several advantages. In its exposure chamber four separate abutting odour fields are presented so that the test insect can readily enter and re‐enter them. More than one odour (or different concentrations of one odour) can be tested at the same time, thereby providing complex preference test situations. The various behavioural measures that can be assessed in the apparatus are examined and discussed.

A variable-response model for parasitoid foraging behavior

An important factor inducing variability in foraging behavior in parasitic wasps is experience gained by the insect. Together with the insects genetic constitution and physiological state, experience ultimately defines the behavioral repertoire under specified environmental circumstances. We present a conceptual variable-response model based on several major observations of a foraging parasitoids responses to stimuli involved in the hostfinding process. These major observations are that (1) different stimuli evoke different responses or levels of response, (2) strong responses are less variable than weak ones, (3) learning can change response levels, (4) learning increases originally low responses more than originally high responses, and (5) hostderived stimuli serve as rewards in associative learning of other stimuli. The model specifies how the intrinsic variability of a response will depend on the magnitude of the response and predicts when and how learning will modify the insects behavior. Additional hypotheses related to the model concern how experience with a stimulus modifies behavioral responses to other stimuli, how animals respond in multistimulus situations, which stimuli act to reinforce behavioral responses to other stimuli in the learning process, and finally, how generalist and specialist species differ in their behavioral plasticity. We postulate that insight into behavioral variability in the foraging behavior of natural enemies may be a help, if not a prerequisite, for the efficient application of parasitoids in pest management.

A comparative functional approach to the host detection behaviour of parasitic wasps. 1. A qualitative study on Eucoilidae and Alysiinae

We studied host detection behaviour in Alysiinae (Braconidae; Ichneumonoidea) and Eucoilidae (Cynipoidea), the larvae of which are endoparasitoids of fly larvae and investigated whether this behaviour is determined by their descent or can be considered an adaptation to different environments. We compared the searching behaviour of females of 32 alysiine and 25 eucoilid species from a variety of microhabitats and from different dipteran hosts by using qualitative behavioural variables. Three main modes of searching were detected: vibrotaxis, ovipositor searching and antennal searching, and the species could be classified according to the role these different modes play in the detection of host larvae. The searching modes are largely dependent upon the taxonomic position of the species. In most cases species belonging to one genus show a similar behaviour pattern. However, we also encountered examples of radiation; closely related species that search differently. The function of the three searching modes has not been elucidated so far. Therefore we cannot say that similar searching modes in unrelated species are examples of adaptive convergence. Especially in Drosophila parasitoids we encountered great differences in searching behaviour between different species living in the same microhabitat. We believe differences at all levels of searching, including host detection behaviour may contribute to niche segregation and create possibilites for different parasitoid species to coexist in the same microhabitat, even when they attack the same host species.

The effect of complete versus incomplete information on odour discrimination in a parasitic wasp.

We studied the function of learning in the parasitoid Leptopilina heterotoma by looking at discrimination of odour stimuli used in foraging for a host. To optimize the rate of encounters with hosts, these parasitoids are expected to assess the extent to which variation in host-substrate odours is reliably associated with variation in the presence of hosts, that is, substrate profitability. Where the association is reliable, parasitoids should attend to variation in odours and discriminate between them; where it is not, they should ignore it. We hypothesized that foraging decisions are based on the completeness of information the animal has about differences in substrate profitabilities. Our laboratory studies showed that discrimination and non-discrimination of odour stimuli are dynamic behavioural decisions that can be related to the degree of substrate variation and to an animals informational state. In wind-tunnel studies, females learned to discriminate between odours from substrates that were qualitatively different, for example, between odours from apple and pear substrates or between yeast substrates with different C6 compounds added. They did not discriminate when differences were small (e.g. between odours from two apple varieties or between yeast patches with different concentrations of ethyl acetate), unless unrewarding experiences provided evidence of the absence of hosts in one of the substrates. Hence, we suggest that non-discrimination between odour stimuli in L. heterotoma is not a lack of ability to discriminate but a functional decision by the parasitoid. Copyright 1998 The Association for the Study of Animal Behaviour. Copyright 1998 The Association for the Study of Animal Behaviour.

Microhabitat location and niche segregation in two sibling species of Drosophilid parasitoids: Asobara tabida (Nees) and A. rufescens (Foerster) (Braconidae: Alysiinae)

SummaryOlfactometer tests with Asobara tabida (Nees 1834), a larval endo-parasitoid of frugivorous Drosophilidae showed that females are attracted to the odour of host food: a suspension of living yeast. This attraction decreased as the fermenting medium grew older and became less likely to contain suitable host stages. Olfactometer tests with — what was considered to be — A. tabida from two different microhabitats (fermenting fruits and decaying plants) showed a genetically determined difference in microhabitat odour preference between the two microhabitat ‘strains’. Each ‘strain’ preferred the odour of its own microhabitat. This odour preference was not modified by larval conditioning. Hybridization tests indicated that we were dealing with two sibling species: A. tabida and A. rufescens (Foerster 1862), reproductively isolated by a pre-mating isolation mechanism only. Enforced matings resulted in fertile female offspring. Some small morphological differences were detected. The two species live sympatrically, although each inhabits and is most attracted to its own microhabitat.

Fitness of two sibling species of Asobara (Braconidae: Alysiinae), larval parasitoids of Drosophilidae in different microhabitats

Abstract. 1. Two sibling species of larval endoparasitoids of Drosophilidae: Asobara tabida (Nees) and A.rufescens (Foerster) occur in the same macrohabitat, but inhabit different microhabitats. Each species is most attracted by odours of its own microhabitat.

Comparison of the Behavioural Response of Two Leptopilina Species (Hymenoptera: Eucoilidae), Living in Different Microhabitats, To Kairomone of Their Host (Drosophilidae)

This paper reports on a comparative study on the response of two related parasitoids to kairomone of their hosts. Leptopilina heterotoma (Thomson) attacks larvae of Drosophila in fermenting fruits and Leptopilina fimbriata (Kieffer) attacks larvae of mainly Scaptomyza pallida (Zetterstedt) in decaying plants. In both species the response to water-soluble kairomone involves a reduction in walking speed and an increase in the frequency with which the substrate is probed. However, essential differences in some of the behavioural parameters between the two species were also discovered. Upon encountering a substrate with kairomone L. heterotoma starts to walk more with longer strolls, whereas L. fimbriata is arrested more strongly and starts to walk less with shorter strolls. The differences in response are possibly adaptations to differences in natural host distribution and density as found in the two microhabitats.

Postovipositional Web-Spinning Behavior in a Hyperparasite, Signiphora Coquilletti Ashmead (Hymenoptera: Signiphoridae)

After oviposition the uniparental hyperparasite Signiphora coquilletti Ashmead was observed to spin a web over her host, Trialeurodes vaporariorum (Westwood) previously parasitized by Encarsia formosa Gahan. Signiphora coquilletti was subsequently reared from webbed T. vaporariorum pupae and from webbed pupae of Tetraleurodes mori (Quaintance), T. stanfordi (Bemis), Aleuroplatus coronatus (Quaintance), and A. gelatinosus (Cockerell). Oviposition and web-spinning behavior of S. coquilletti are described, and the ultrastructure of the webs is discussed. We believe that webs may function as a physical barrier to host searching females of competing Encarsia species, or that they may serve as an intraspecific host-marking device. Two additional hypotheses are that webs afford protection against predation of Signiphora immatures in host pupae, or that they reduce mortality of Signiphora by tying host pupae to leaf surfaces.

Variations in natural-enemy foraging behaviour: essential element of a sound biological-control theory

Intraspecific intrinsic variation in foraging behaviour is a common but often overlooked feature of natural enemies. These variations result from adaptations to the variety of foraging circumstances encountered by individuals of the species. We discuss the importance of understanding the mechanisms governing these intrinsic variations and the development of technologies to manage them. Three major sources of variation in foraging behaviour are identified. One source for variation is genotypically fixed differences among individuals that are adapted for different foraging environments. Another source of foraging variation is the phenotypic plasticity that allows individuals to make ongoing modifications of behaviour through learning, which suits them for different host-habitat situations. A third factor in determining variation in foraging behaviour is the natural enemys physiological state relative to other needs, such as food and mating. A conceptual model is presented for comprehensively examining the respective roles of these variables and their interactive net effect on foraging behaviour. We also discuss proposed avenues for managing these variations in applied biological control programmes.