Associative learning of host presence in non-host environments influences parasitoid foraging (original) (raw)
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Oecologia, 2019
Foraging animals face the difficult task to find resources in complex environments that contain conflicting information. The presence of a non-suitable resource that provides attractive cues can be expected to confuse foraging animals and to reduce their foraging efficiency. We used the parasitoid Cotesia glomerata to study the effect of non-host-infested plants and associative learning on parasitoid foraging efficiency. Inexperienced C. glomerata did not prefer volatiles emitted from host (Pieris brassicae)-infested plants over volatiles from non-host (Mamestra brassicae)-infested plants and parasitoids that had to pass non-host-infested plants needed eight times longer to reach the host-infested plant compared to parasitoids that had to pass undamaged plants. Contrary to our expectations, oviposition experience on a host-infested leaf decreased foraging efficiency due to more frequent visits of non-host-infested plants. Oviposition experience did not only increase the responsiveness of C. glomerata to the host-infested plants, but also the attraction towards herbivore-induced plant volatiles in general. Experience with non-host-infested leaves on the contrary resulted in a reduced attraction towards non-host-infested plants, but did not increase foraging efficiency. Our study shows that HIPVs emitted by non-host-infested plants can confuse foraging parasitoids and reduce their foraging efficiency when non-host-infested plants are abundant. Our results further suggest that the effect of experience on foraging efficiency in the presence of non-host-infested plants depends on the similarity between the rewarding and the non-rewarding cue as well as on the completeness of information that parasitoids have acquired about the rewarding and non-rewarding cues.
foraging efficiency of C. glomerata, it did not reduce the negative influence of natural background vegetation. At the same time, however, females foraging in natural vegetation attacked more host patches on host-plant species on which they previously had a positive oviposition experience. We conclude that, even though the presence of natural vegetation reduces the foraging efficiency of C. glomerata, it does not prevent experienced female wasps from specifically orienting towards the host-plant species from which they had learned the HIPVs.
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,
Adaptive learning of host preference in a herbivorous arthropod
Ecology Letters, 2001
Although many publications deal with the effects of experience on behaviour, adaptive learning (i.e. behavioural change with experience resulting in improved reproductive success) is poorly documented. We present direct evidence that learning of host preference improves fitness in the herbivorous mite, Tetranychus urticae. Individual mites from two strains were repeatedly given a choice between two host plants, tomato and cucumber, and then subjected to a performance test on each. For both strains, food experience affected the subsequent choice: individual mites learned to prefer cucumber over tomato. The performance test showed this effect to be adaptive, as the food plant the mites learned to prefer (cucumber) allowed for increased oviposition, survival and development. These findings have important implications for the interpretation of the preference±performance relationship among herbivorous arthropods. The frequently reported absence of such a relationship may be due to experience-dependent preference and/or performance.
Parasitoids searching for polyphagous herbivores can find their hosts in a variety of habitats. Under this scenario, chemical cues from the host habitat (not related to the host) represent poor indicators of host location. Hence, it is unlikely that naïve females show a strong response to host habitat cues, which would become important only if the parasitoids learn to associate such cues to the host presence. This concept does not consider that habitats can vary in profitability or host nutritional quality, which according to the optimal foraging theory and the preference-performance hypothesis (respectively) could shape the way in which parasitoids make use of chemical cues from the host habitat. We assessed innate preference in the fruit fly parasitoid Diachasmimorpha longicaudata among chemical cues from four host habitats (apple, fig, orange and peach) using a Y-tube olfactometer. Contrary to what was predicted, we found a hierarchic pattern of preference. The parasitism rate realized on these fruit species and the weight of the host correlates positively, to some extent, with the preference pattern, whereas preference did not correlate with survival and fecundity of the progeny. As expected for a parasitoid foraging for generalist hosts, habitat preference changed markedly depending on their previous experience and the abundance of hosts. These findings suggest that the pattern of preference for host habitats is attributable to differences in encounter rate and host quality. Host habitat preference seems to be, however, quite plastic and easily modified according to the information obtained during foraging.
Ecological Entomology, 2008
Abstract 1. In solitary parasitoids, several species can exploit the same host patch and competition could potentially be a strong selective agent as only one individual can emerge from a host. In cereal crops, Aphidius rhopalosiphi and A. ervi share the grain aphid Sitobion avenae as host.2. The present work studied foraging strategies of both species on patches already exploited by the other species. The study analysed larval competition in multi-parasitised hosts and compared the foraging behaviour of females with and without previous experience.3. It was found that A. ervi wins larval competition three times more often than A. rhopalosiphi. Both species spent less time on patches exploited by a heterospecific than on unexploited ones. When they foraged on heterospecifically exploited patches, experienced females induced less mortality in aphids than inexperienced ones.4. Although A. rhopalosiphi is a specialist on cereal aphids and is the most abundant species due to its early appearance in the season, S. avenae is still a profitable host for A. ervi, because: (i) A. rhopalosiphi leaves patches partially exploited, (ii) A. ervi wins larval competition in three out of four multi-parasitised hosts, and (iii) A. ervi is only slightly deterred by the cornicular secretions of the host and can thus easily parasitise hosts.
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...
A variable-response model for parasitoid foraging behavior
Journal of Insect Behavior, 1990
An important factor inducing variability in foraging behavior in parasitic wasps is experience gained by the insect. Together with the insect's 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 parasitoid's responses to stimuli involved in the host-finding 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) host-derived 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 insect's 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.