Getting confused: learning reduces parasitoid foraging efficiency in some environments with non-host-infested plants (original) (raw)
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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.
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,
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.
Biological Invasions, 2017
Invasive insect herbivores have the potential to interfere with native multitrophic interactions by affecting the chemical cues emitted by plants and disrupting the attraction of natural enemies mediated by herbivore-induced plant volatiles (HIPVs). In a previous study, we found that the presence of the exotic herbivore Spodoptera littoralis on Brassica rapa plants infested by the native herbivore Pieris brassicae makes these dually-infested plants unattractive to the main parasitoid of P. brassicae, the braconid wasp Cotesia glomerata. Here we show that this interference by S. littoralis is strongly dependent on the relative densities of the two herbivores. Parasitoids were only deterred by dually-infested plants when there were more S. littoralis larvae than P. brassicae larvae on a plant. Furthermore, the blend of HIPVs emitted by dually-infested plants differed the most from HIPVs emitted by Pieris-infested plants when S. littoralis density exceeded P. brassicae density. We further found that associative learning by the parasitoid affected its preferences: attraction to dually-infested plants increased after parasitoids were presented a P. brassicae caterpillar (rewarding experience) in presence of the odor of a dually-infested plant, but not when presented a S. littoralis caterpillar (non-rewarding experience). A non-rewarding experience prior to the bioassays resulted in a general decrease in parasitoid motivation to respond to plant odors. We conclude that herbivore density and associative learning may play an important role in the foraging behavior of natural enemies in communities, and such effects should not be overlooked when investigating the ecological impact of exotic species on native food webs.
Journal of Chemical Ecology, 2011
Herbivore-induced plant volatiles are important host finding cues for larval parasitoids, and similarly, insect oviposition might elicit the release of plant volatiles functioning as host finding cues for egg parasitoids. We hypothesized that egg parasitoids also might utilize HIPVs of emerging larvae to locate plants with host eggs. We, therefore, assessed the olfactory response of two egg parasitoids, a generalist, Trichogramma pretiosum (Tricogrammatidae), and a specialist, Telenomus remus (Scelionidae) to HIPVs. We used a Y-tube olfactometer to tests the wasps' responses to volatiles released by young maize plants that were treated with regurgitant from caterpillars of the moth Spodoptera frugiperda (Noctuidae) or were directly attacked by the caterpillars. The results show that the generalist egg parasitoid Tr. pretiosum is innately attracted by volatiles from freshly-damaged plants 0-1 and 2-3 h after regurgitant treatment. During this interval, the volatile blend consisted of green leaf volatiles (GLVs) and a blend of aromatic compounds, monoand homoterpenes, respectively. Behavioral assays with synthetic GLVs confirmed their attractiveness to Tr. pretiosum. The generalist learned the more complex volatile blends released 6-7 h after induction, which consisted mainly of sesquiterpenes. The specialist T. remus on the other hand was attracted only to volatiles emitted from fresh and old damage after associating these volatiles with oviposition. Taken together, these results strengthen the emerging pattern that egg and larval parasitoids behave in a similar way in that generalists can respond innately to HIPVs, while specialists seems to rely more on associative learning.
Ecological Entomology, 2001
1. The foraging behaviour of the parasitoid wasp Halticoptera laevigata Thomson (Hymenoptera: Pteromalidae) was studied. This wasp attacks the ®rstinstar larvae of the fruit¯y Myoleja lucida Falle Ân (Diptera: Tephritidae) within honeysuckle Lonicera xylosteum L. (Caprifoliaceae) fruits. It was hypothesised that, to forage ef®ciently, wasps should be able to maintain a systematic or at least nonrandom search pattern on the level of the microhabitat, i.e. branches with fruits, and/or be able to recognise previously searched fruits. 2. Comparisons of observed patch visitation patterns on branches bearing uninfested fruits with expected values for systematic and random visitation patterns indicated that H. laevigata wasps visit patches randomly and do not avoid visiting host-free patches that they have visited previously. 3. While wasps did not alter their search effort on uninfested fruits searched previously by conspeci®cs, they searched for much shorter times and probed less frequently for hosts on uninfested fruits that they had searched previously. 4. The results indicate that H. laevigata wasps engage in partially systematic search and increase their search ef®ciency through the recognition of self-searched fruits. The reasons why partial rather than fully systematic search should be adaptive in this parasitoid are discussed.
Journal of Chemical Ecology, 2012
Insect herbivores often induce plant volatile compounds that can attract natural enemies. Cotesia marginiventris (Hymenoptera: Braconidae) is a generalist parasitoid wasp of noctuid caterpillars and is highly attracted to Spodoptera exigua-induced plant volatiles. The plasticity of C. marginiventris associative learning to volatile blends of various stimuli, such as host presence, also has been shown, but little is known about how this generalist parasitoid distinguishes between host species of varying suitability. Spodoptera exigua is an excellent host that yields high parasitoid emergence, while Trichoplusia ni serves as a sub-optimal host species due to high pre-imaginal wasp mortality. We have found that S. exigua and T. ni induce different volatile blends while feeding on cotton. Here, wind tunnel flight assays were used to determine the importance of differentially induced volatiles in host-finding by C. marginiventris. We found that, while this generalist parasitoid wasp can distinguish between the two discrete volatile blends when presented concurrently, a positive oviposition experience on the preferred host species (S. exigua) is more important than host-specific volatile cues in eliciting flight behavior towards plants damaged by either host species. Furthermore, wasps with oviposition experience on both host species did not exhibit a deterioration in positive flight behavior, suggesting that oviposition in the sub-optimal host species (T. ni) does not cause aversive odor association.
Short- and long-range cues used by ground-dwelling parasitoids to find their host
Naturwissenschaften, 2013
Parasitoids of phytophagous insects face a detectability-reliability dilemma when foraging for hosts. Plantrelated cues are easily detectable, but do not guarantee the presence of the host. Host-related cues are very reliable, but much harder to detect from a distance. Little is known in particular about the way coleopteran parasitoid females use these cues when foraging for a suitable place to lay their eggs. The question is of interest because, unlike hymenopteran larvae, coleopteran parasitoid larvae are highly mobile and able to forage for hosts on their own. We assessed whether females of the parasitoid rove beetle Aleochara bipustulata (L.) (Coleoptera: Staphylinidae) are attracted to plant (Swede roots, Brassica napus) and host-related cues [pupae of the cabbage root fly Delia radicum (L.) (Diptera: Anthomyiidae)]. In the field, A. bipustulata adult females were captured in selective pitfall traps containing pieces of roots damaged by D. radicum larvae, but not in traps containing pieces of healthy roots or D. radicum pupae. However, in the laboratory, the odour of D. radicum pupae attracted A. bipustulata females to mini-pitfalls. Video monitoring in the laboratory showed that foraging A. bipustulata females preferred a zone containing D. radicum pupae and larval tracks rather than one containing an extract of D. radicum-infested roots. Our results suggest a behavioural sequence where A. bipustulata females use plant-related cues at a distance, but then switch their preference to hostrelated cues at a close range. This would be the first observation of this behaviour in coleopteran parasitoids.