Parasitoid Learning Research Articles

Integrating Parasitoid Olfactory Conditioning in Augmentative Biological Control: Potential Impact, Possibilities, and Challenges

Despite of the vast body of theoretical and empirical literature dealing with parasitoid learning, this knowledge has thus far rarely been exploited for manipulating the efficacy of augmentative biological pest control. This may be due to the fact that most studies on learning behavior were performed under laboratory conditions, whereas field trials remain scarce. However, the few studies that did investigate parasitoid foraging success under (semi-)field conditions show strong learning effects. Using so-called ‘parasitoid olfactory conditioning’ (POC), parasitoids can be trained to become more efficient in the different phases involved in the process of host searching and host acceptance. POC can thus result in a ‘foraging efficacy gain’, defined as the difference between the number of naive and conditioned parasitoids that need to be released to reach a certain parasitization level of the target-pest in the crop environment. This ‘gain’ increases with an improved parasitoid learning ability and depends on the interplay between the parasitoid, crop, target-pest species and parasitoid rearing method. Moreover, the ‘foraging efficacy gain’ depends on the technical implementation of POC, as this will determine the strength, duration and stability of the learning-induced behavioral change. In this perspective paper we will discuss a) the conditions that can enhance the ‘foraging efficacy gain’, b) the possible approaches to implementation of POC and their costs and benefits, and c) a stepwise approach to develop appropriate POC methods for the optimization of biological pest control.

Effect of fruit and host fly species on the associative learning by Fopius arisanus.

Parasitoids, released in augmentative biological control programmes, which display a rapid host-location capacity, have a higher likelihood of successfully controlling target pest species. By learning to associate sensory cues to a suitable oviposition site, might parasitoids used as biological control agents, locate hosts more rapidly, and perhaps increase the efficacity of e.g. Tephritidae fruit fly management. We studied associative learning of Fopius arisanus (Hymenoptera: Braconidae) and tested its range of learning in natural and conditional hosts and host fruits, i.e. Bactrocera dorsalis, Zeugodacus cucurbitae, Ceratitis capitata and Ceratitis cosyra (Diptera: Tephritidae) and on fruits (papaya, tomato, banana). Naïve female F. arisanus were compared with experienced wasps, which had been offered infested and non-infested fruit, and been allowed to oviposit. Preferences for olfactory cues from infested fruits were thereafter assessed in a two-choice olfactometer. Naïve and trained parasitoids preference differed in general and non-responders to infested fruits were higher among naïve parasitoids. The trained wasps preferred the fruit infested in the training more than the control fruit, for all combination, except when C. cosyra infested the fruits, hence avoidance behavioural response was observed towards the odour of the infested fruit. Fopius arisanus was capable of behaviourally respond to the learned information, e.g. associative odour learning was achieved, yet limited depending on interaction level, fruit fly and fruit combination. To create F. arisanus preference of an associated odour, it might hence be needed to ensure oviposition in perceived suitable host and host fruit, for the parasitoid learning to become favourable in a biological control setup.

Invasive insect herbivores as disrupters of chemically-mediated tritrophic interactions: effects of herbivore density and parasitoid learning

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.

Learning predator promotes coexistence of prey species in host-parasitoid systems.

Ecological theory suggests that frequency-dependent predation, in which more common prey types are disproportionately favored, promotes the coexistence of competing prey species. However, many of the earlier empirical studies that investigated the effect of frequency-dependent predation were short-term and ignored predator-prey dynamics and system persistence. Therefore, we used long-term observation of population dynamics to test how frequency-dependent predation influences the dynamics and coexistence of competing prey species using insect laboratory populations. We established two-host-one-parasitoid populations with two bruchid beetles, Callosobruchus chinensis and C. maculatus, as the hosts and the pteromalid wasp Anisopteromalus calandrae as their common parasitoid. When the parasitoid was absent, C. chinensis was competitively excluded in ∼20 wk. Introducing the parasitoid greatly enhanced the coexistence time to a maximum of 118 wk. In the replicates of long-lasting coexistence, the two host species C. maculatus and C. chinensis exhibited periodic antiphase oscillations. Behavioral experiments showed frequency-dependent predation of A. calandrae that was caused by learning. Females of A. calandrae learned host-related olfactory cues during oviposition and increased their preference for the common host species. Numerical simulations showed that parasitoid learning was the essential mechanism that promoted persistence in this host-parasitoid system. Our study is an empirical demonstration that frequency-dependent predation has an important role in greatly enhancing the coexistence of prey populations, suggesting that predator learning affects predator-prey population dynamics and shapes biological communities in nature.

Associative odour learning affects mating behaviour in Aphidius ervi males (Hymenoptera: Braconidae)

We used the aphid parasitoid Aphidius ervi reared in its host Acyrthosiphon pisum to examine if male sexual attractive responses can be conditioned to an odour (vanilla) that is not present in the natural environment. We used prior mating experience (exposure to females) as a non-conditioning stimulus and vanilla odour as a conditioning stimulus. The behavioural responses were tested in a glass Y-olfactometer just after eclosion (i.e., initial response) and after a training experience (i.e., trained response). During the 10-min training period individual males were allowed to copulate with a virgin female with or without vanilla odour present, or were exposed only to vanilla odour. Wing fanning was a recurrent behaviour which denoted increased sexual attraction to a volatile stimulus. Total time and time doing wing fanning in each olfactometer arm were determined. Vanilla odour, which initially did not elicit sexual-related behaviours, triggered strong sexual attractive responses when males were trained to females plus vanilla odour. Neither copulation only nor vanilla odour only treatments elicited such behaviours in trained males. The results are discussed in terms of parasitoid learning ability and its ecological consequences.

Influence of handling and conditioning protocol on learning and memory of Microplitis croceipes

Abstract Microplitis croceipes (Cresson) (Hymenoptera: Braconidae) learns odors in association with both hosts and food. The food‐associated ‘seeking’ behavior of M. croceipes was investigated under various training protocols utilizing the conditioning odor, 3‐octanone. We investigated the effects of odor training, or its lack, training duration, training frequency, time elapsed after training, wasp hunger state, and training reinforcement, on the food‐seeking responses of M. croceipes females. We found that odor‐trained females show strong food seeking responses, whereas non‐odor‐trained females do not respond to the odor, and that a single 10 s association with the odor whilst feeding on sugar water subsequently conditioned the wasps to exhibiting significant responses to it. Increases in training time to more than 10 s did not improve their responses. Repetition of the food–odor associations increased a wasp's recall, as well as its response over time, compared to a single exposure. Repeated exposure to the learned odor in the absence of a food reward decreased the responses of less hungry individuals. However, the level of response increased significantly following a single reinforcement with the food–odor association. Understanding the factors that influence learning in parasitoids can enhance our ability to predict their foraging behavior, and opens up avenues for the development of effective biological detectors.

Parasitoid learning during interactions with ants: how to deal with an aggressive antagonist

Pauesia picta, P. pinicollis and P. silvestris (Hymenoptera: Aphidiidae) are common parasitoids of the conifer aphid Cinara pinea, which is regularly attended by red wood ants (Formica spp.). In this study, I tested whether females of these parasitoid species learned during interactions with honeydew-collecting Formica polyctena workers that caution is not necessary if searching behaviour is adapted, and whether parasitoids benefit from being able to learn. When searching on Scots pines, naive females of P. picta and P. pinicollis generally retreated to a pine needle when making contact with a honeydew-collecting ant, did not approach ants from the side or from the front and kept a ”safe distance” from ants when sitting on needles. After some non- aggressive ant encounters, experienced female parasitoids changed their behaviour: they reduced their searching speed, approached ants from the side and even from the front, retreated less often in response to an approaching ant and reduced the ”safe distance”. These experienced females had a significantly higher rate of oviposition than naive females or females foraging for an unattended host. Thus, the ability of the parasitoid to learn during interactions with an antagonist led to a prolonged retention time and a higher oviposition rate. By contrast, there was no evidence of learning in P. silvestris. Females of this species showed no behavioural change in response to ant encounters, and there was no difference in the foraging success of naive and experienced female parasitoids.

Learning, Host Fidelity, and the Stability of Host-Parasitoid Communities.

Simple models of host-parasitoid interactions show that a polyphagous parasitoid tends to drive extinct all but the most fecund of its hosts. Coexistence requires a mechanism by which hosts with lower fecundity can increase when rare. We explore how recently discovered parasitoid learning behavior can contribute to species coexistence. On emergence as adults, parasitoids learn chemical cues associated with their natal host and hence are more likely to locate and to oviposit in hosts of the same species. For two models incorporating different assumptions about parasitoid searching, we derive conditions for the strength of host fidelity that permits a feasible multihost equilibrium and argue that this equilibrium is stable whenever the corresponding single-host equilibria are stable.

Learning, Host Fidelity, and the Stability of Host-Parasitoid Communities

Simple models of host‐parasitoid interactions show that a polyphagous parasitoid tends to drive extinct all but the most fecund of its hosts. Coexistence requires a mechanism by which hosts with lower fecundity can increase when rare. We explore how recently discovered parasitoid learning behavior can contribute to species coexistence. On emergence as adults, parasitoids learn chemical cues associated with their natal host and hence are more likely to locate and to oviposit in hosts of the same species. For two models incorporating different assumptions about parasitoid searching, we derive conditions for the strength of host fidelity that permits a feasible multihost equilibrium and argue that this equilibrium is stable whenever the corresponding single‐host equilibria are stable.

Persistence of experience effects in the parasitoid Trichogramma nr. brassicae

1. The importance of learning in parasitoids is likely to depend on how long learning effects persist, the number of learned stimuli that can be retained, and whether learning effects are confined to low ranked hosts.2. The duration of learning of host‐specific stimuli was tested in four strains of Trichogramma nr. brassicae (Hymenoptera: Trichogrammatidae). Both the persistence of learning of the rearing host and oviposition experience were tested in separate experiments.3. The response to a non‐preferred host, Sitotroga cerealella, was measured at different times following experience on that host or an alternative host, Heliothis punctigera. Both types of experience persisted for at least 5 days in all four strains.4. The effect of oviposition in a highly preferred host, H. punctigera, following oviposition in S. cerealella was also tested. The increased acceptance of S. cerealella following oviposition on this host persisted despite a subsequent oviposition on H. punctigera.5. The implications for host range at both individual and population levels are discussed.

Semiochemicals and learning in parasitoids

There is increasing evidence that parasitoid responses to semiochemicals, important stimuli in the host location process, are influenced by experience. This paper focuses on the role of learning, in particular associative learning, in responses to odors. Emphasis is placed on associative learning during the adult stage, the influence of preadult experience is discussed briefly. New data on learning in the speciesLeptopilina heterotoma are given. It is demonstrated that females can learn to respond to a novel odor, which they subsequently use in microhabitat selection. Learning was shown to be associative whereby host products (contact kairomone) or an oviposition experience could function as the reinforcers (reward). The effect of learning seemed stronger when parasitoids were rewarded with an oviposition experience. The paper concludes with a discussion on the application of parasitoid learning in pest management.