Dynamics of odour learning in Leptopilina boulardi, a hymenopterous parasitoid (original) (raw)
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Odor learning and foraging success in the parasitoid,Leptopilina heterotoma
Journal of Chemical Ecology, 1990
A brief 2-hr experience with host Drosophila larvae in artificial apple-yeast or mushroom microhabitats had three effects on the foraging behavior of female Leptopilina heterotoma (Hyrnenoptera: Eucoilidae) parasitoids under field conditions. First, experienced females released at the center of circular arrays of apple-yeast and mushroom baits were more likely to find a microhabitat over the course of a daily census than naive ones. Second, for those females that found a microhabitat, experienced ones found it faster than naive ones (i.e., experience reduced travel times). Third, females experienced with a particular microhabitat were more likely to find that microhabitat than an alternative one. Learned preferences were retained for at least one day and possibly as many as seven. Results generally did not depend on the host species (D. melanogaster or D. simulans) with which females were given experience. Females tended to arrive at baits upwind of the point of release, suggesting that odor is involved in finding host microhabitats and, in particular, in learning to find them more effectively. The implications of these results for the application of serniochemicals in biological control are discussed briefly.
Parasitoid Foraging and Learning
Chemical Ecology of Insects 2, 1995
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 tum, 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. 1.1. The Fixed Response Perspective The study of parasitoid foraging behavior entered a new era around the time of publication of Vinson's review (Vinson, 1984) on parasitoid-host relationships in the first edition of Chemical Ecology of 1nsects (Bell and Carde, 1984). Prior to that time, students of parasitoid foraging behavior mainly were involved in identifying and describing the steps of how an insect parasitoid finds a potential host in which to lay its eggs (e.g., Lewis et al. 1976). Although a major emphasis was placed on the importance of chemical stimuli in guiding this process, an impressive array of stimuli was revealed. In spite of this diversity in stimuli and behaviors involved, some generalizations were possible. For example, different searching phases, such as habitat location, host location, host examination, were distinguished. The importance of host-derived cues including frass, webbing, mandibular secretions, and scales of adult moths, in attracting and arresting parasitoids at a short distance also seemed a general phenomenon (Weseloh,
Biological Control, 1998
In many parasitoid species, behaviors leading to host selection are triggered by the perception of mostly chemical cues, which often depends on learning processes. Among the latter, associative learning, where a neutral stimulus (e.g., an odor) is perceived as associated with a reward (e.g., oviposition or contact with host products), ensures a higher probability of locating a host. In this work we investigated the effect of two physiological factors, mating and oviposition experience, on odor learning involved in the ovipositor search in the parasitoid Leptopilina boulardi (Barbotin et al.). We developed a bioassay to quantify individual learning performances based on the observation of an odor-conditioned probing response, characterized by several parameters such as the latency (i.e., the time elapsed between the onset of the conditioned odor and the start of the conditioned probing behavior), the duration of the first probing, and the total probing duration. The percentage of females that learned a fruit odor (banana) associated to an oviposition reward did not depend on mating or prior oviposition experience. However, both factors influenced the parameters of the learned response: oviposition experience could induce a higher latency and a shorter probing duration, whereas the opposite changes could result from mating. These results were discussed with regard to physiological changes known to influence host-searching activity. We concluded on the possible consequences of these variabilities at the individual level. The evaluation of how such physiological events affect traits correlated to parasitization efficiency is important for improving biocontrol strategies. 1998 Academic Press
1993
Parasitoids that forage for herbivorous hosts by using infochemicals may have a problem concerning the reliability and detectability of these stimuli: host stimuli are highly reliable but not very detectable at a distance, while stimuli from the host's food are very detectable but generally not very reliable in indicating host presence. One solution to this problem is to learn to link highly detectable stimuli to reliable but not very detectable stimuli. Ample knowledge is available on how associative learning aids foraging parasitoids in the location of suitable microhabitats. However, in this paper we report on another solution to the reliability-detectability problem and present evidence for an essential, but as yet overlooked, aspect of Drosophila parasitoid ecology. For the first time it is shown that a parasitoid of Drosophila larvae spies on the communication system of adult Drosophila flies to locate potential host sites: naive parasitoids strongly respond to a volatile aggregation pheromone that is deposited in the oviposition site by recently mated female flies. Thus, the parasitoids resort to using highly detectable information from a host stage different from the one under attack (i.e. infochemical detour). The function and ecological implications of these findings are discussed.
Testing the habituation assumption underlying models of parasitoid foraging behavior
PeerJ, 2017
Habituation, a form of non-associative learning, has several well-defined characteristics that apply to a wide range of physiological and behavioral responses in many organisms. In classic patch time allocation models, habituation is considered to be a major mechanistic component of parasitoid behavioral strategies. However, parasitoid behavioral responses to host cues have not previously been tested for the known, specific characteristics of habituation. In the laboratory, we tested whether the foraging behavior of the egg parasitoid Trissolcus basalis shows specific characteristics of habituation in response to consecutive encounters with patches of host (Nezara viridula) chemical contact cues (footprints), in particular: (i) a training interval-dependent decline in response intensity, and (ii) a training interval-dependent recovery of the response. As would be expected of a habituated response, wasps trained at higher frequencies decreased their behavioral response to host footpr...
Information gleaned and former patch quality determine foraging behavior of parasitic wasps
Behavioral Ecology, 2011
A good estimate of patch quality is of prime importance for a randomly searching forager with limited longevity or fecundity. The forager can perceive cues related to the presence of resource on arrival in a patch and estimates its quality relatively to previous patches. This prior estimate can then be updated through sampling in the patch. However, these 3 sources of information have never been manipulated independently in the same experiment to quantify the effect of each one on foraging behavior. Here, we report experiments highlighting the mechanism by which the braconid Asobara tabida, a parasitoid wasp laying eggs in Drosophila larvae, uses information both gleaned from the previous patch visited and obtained on arrival in the next one, to estimate the quality of the latter and to behave accordingly. We disentangled the effects of the prior estimate of patch quality made on arrival in the patch and the effect of sampling in the patch on the foraging behavior of the parasitoid. We show that information gleaned by A. tabida from a previously visited patch plays a strong role in the response to both chemical cues and oviposition events by parasitoid when exploiting a patch. The information process highlighted in the present study is consistent with the Bayesian-like decision-making, which is suspected in parasitoids, bumblebees, and humans. Moreover, motivation to stay in the patch is likely to be tuned to the forager's experience.
Journal of Insect Behavior, 1996
Wind tunnel experiments were conducted to determine roles of odor learning in food foraging of the larval parasitoid, Microplitis croceipes (Hymenoptera: Braconidae). Females that had neither fed on sucrose water nor experienced any odor and females that had experienced an odor without feeding failed to respond to any odors in a wind tunnel. Most of the females that had fed without an odor also did not respond to odors. However, most of the females that had experienced an odor during feeding on sucrose water flew to the odor. These results indicate that when females experience an odor during feeding, they learn to associate the odor with food and subsequently respond to the odor. As age of females increased, their response to an experienced odor increased, peaked 2 to 5 days after emergence, and then decreased. With an increasing number of odor experiences while feeding, accuracy of females choosing the experienced odor increased. Females that experienced an odor while feeding three to five times chose the experienced odor 90% of the time. When females experienced an odor while feeding five times, the memory of food associated odor lasted at least 2 days. When they experienced food with two odors successively, they could memorize both odors, and multiple experiences did not cause memory interference. Even when females had learned a food-associated odor, their response to the learned odor ceased after several visits on patches containing the odor but no food. Such "negative experience" may cause switching of food searching to new odors by females.
Associative learning of host presence in non-host environments influences parasitoid foraging
Ecological Entomology
1. Parasitoids are known to utilise learning of herbivore-induced plant volatiles (HIPVs) when foraging for their herbivorous host. In natural situations these hosts share food plants with other, non-suitable herbivores (non-hosts). Simultaneous infestation of plants by hosts and non-hosts has been found to result in induction of HIPVs that differ from host-infested plants. Each non-host herbivore may have different effects on HIPVs when sharing the food plant with hosts, and thus parasitoids may learn that plants with a specific non-host herbivore also contain the host. 2. This study investigated the adaptive nature of learning by a foraging parasitoid that had acquired oviposition experience on a plant infested with both hosts and different non-hosts in the laboratory and in semi-field experiments. 3. In two-choice preference tests, the parasitoid Cotesia glomerata shifted its preference towards HIPVs of a plant-host-non-host complex previously associated with an oviposition experience. It could, indeed, learn that the presence of its host is associated with HIPVs induced by simultaneous feeding of its host Pieris brassicae and either the non-host caterpillar Mamestra brassicae or the non-host aphid Myzus persicae. However, the learned preference found in the laboratory did not translate into parasitisation preferences for hosts accompanying non-host caterpillars or aphids in a semi-field situation. 4. This paper discusses the importance of learning in parasitoid foraging, and debates why observed learned preferences for HIPVs in the laboratory may cancel out under some field experimental conditions.
Animal Behaviour, 2008
Parasitoids of herbivorous larvae are well known to be able to associatively learn a response to feedinginduced plant volatiles. However, little is known of the abilities of egg parasitoids to learn a response to herbivore oviposition-induced plant volatiles (OVIV). The eulophid wasp Chrysonotomyia ruforum is known to be attracted by OVIV from Scots pine released 3 days after host egg deposition. This study aimed to elucidate (1) the impact of the nutritional state of the parasitoid on its response to OVIV and (2) the effect of learning and response to the temporal change of OVIV. Supply of food as a reward during associative learning trials inevitably influences the nutritional state and thus leads to an experimental constraint. Nevertheless, the results indicate that the parasitoids have to associate OVIV with host presence and that they need to be supplied with food to learn and to respond to OVIV. Furthermore, the parasitoids' positive response to OVIV from pine twigs laden with eggs for 3 days was independent of the induction time of pine twigs experienced. However, a positive response was given only to OVIV from pine twigs with 3-day-old eggs, while OVIV from twigs with other induction times (1, 2, 4 days) were not attractive. Thus, our findings indicate an unusual learning process in this specialized egg parasitoid. We suggest that the parasitoid is using a learning strategy by which common information is filtered out of similar odour blends (here: 1-to 4-day-long induced pine twigs), but a behavioural response to this learned information becomes evident only in a specific odour context (here: 3-day-long induced twigs).
The effect of complete versus incomplete information on odour discrimination in a parasitic wasp
Animal Behaviour, 1998
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 animal's informational state.