Time scales of associating food and odor by predator communities in the field

Janssen, Arne; Fonseca, Juliana Oliveira; Colares, Felipe; Silva, Lidiane Gomes da; Pedrosa, Aline Rodrigues Porto; Lima, Eraldo; Wijk, Michiel P. van; Pallini, Ângelo; Oliveira, Cyntia Meireles de; Sabelis, Maurice W.; Lesna, I.K.A.

doi:10.1093/beheco/aru094

Cited by 11 publications

(14 citation statements)

References 68 publications

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“…The innate preference of inexperienced parasitoids for hostplus non-host caterpillar-damaged plants could be caused by a quantitative difference in emitted volatiles related to caterpillar feeding, as a result of unequal numbers of caterpillars on the two plant infestation types (Geervliet et al, 1998a). Only very few previous studies have shown that insects that can learn to associate cues with the presence of their host/food in the laboratory also accordingly show altered behaviour in (semi-)field situations (Lewis & Martin, 1990;Hare et al, 1997;Raine & Chittka, 2008;Zrelec et al, 2013;Janssen et al, 2014;Kruidhof et al, 2015). Quantitative differences could also have occurred because of changed emission rates of caterpillar-related volatile compounds due to co-infestation by phloem-feeding insects such as aphids (Rodriguez-Saona et al, 2003;Zhang et al, 2013;Ponzio et al, 2016;Li et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…This new experience levelled out the preference for plants induced by only host caterpillars in the wind-tunnel experiment. Only very few previous studies have shown that insects that can learn to associate cues with the presence of their host/food in the laboratory also accordingly show altered behaviour in (semi-)field situations (Lewis & Martin, 1990;Hare et al, 1997;Raine & Chittka, 2008;Zrelec et al, 2013;Janssen et al, 2014;Kruidhof et al, 2015). Cotesia glomerata is well known for its ability to learn in the laboratory (Geervliet et al, 1998a,b;Bleeker et al, 2006;Smid et al, 2007;Kruidhof et al, 2012a,b).…”

Section: Discussionmentioning

confidence: 99%

“…Although thorough laboratory studies have identified the potential of learning by parasitoids as well as some of the underlying mechanisms Turlings et al, 1993;Vet et al, 1995;Hoedjes et al, 2011;Wäschke et al, 2013), the significance of learning in foraging under complex field conditions has seldom been studied (Lewis & Martin, 1990;Mery, 2013, but see Papaj & Vet, 1990Hare et al, 1997;Kruidhof et al, 2015). The few field studies show that both predators and herbivores have enhanced foraging success under field conditions when they associated the presence of their food with a distinct odour (Zrelec et al, 2013;Janssen et al, 2014). In parasitoids, oviposition experience on a host-infested plant enhanced the number of host patches visited per time unit in a field-tent setup.…”

Section: Introductionmentioning

confidence: 99%

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Associative learning of host presence in non‐host environments influences parasitoid foraging

Rijk

Sánchez

Smid

et al. 2018

Ecological Entomology

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Associative learning of host presence in non‐host environments influences parasitoid foraging

Rijk

Sánchez

Smid

et al. 2018

Ecological Entomology

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“…First, the localisation of prey on novel host plants may not be easy because foraging efficiency may be compromised: the blends of volatiles produced by novel host plants in response to attack by the herbivore may not be recognised as cues by the natural enemy complex. Yet, selection for attraction of predators by volatiles can be rapid (Margolies et al., ) and predators can learn to respond to volatiles of novel host plants (Papaj & Lewis, ; Turlings et al., ; Vet et al., ; Drukker et al., ; Takabayashi et al., ; Janssen et al., ). Second, natural enemies may have difficulties in consuming prey on a novel host plant because herbivores use toxins from their host plants for their own protection (Smiley et al., ; Denno et al., ; Rank, ; Nishida, ; Singer et al., ,b; Zvereva & Rank, ).…”

Section: Introductionmentioning

confidence: 99%

Parasitoids follow herbivorous insects to a novel host plant, generalist predators less so

Grosman

Holtz

Pallini

et al. 2017

Entomologia Exp Applicata

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The ‘enemy‐free space’ hypothesis predicts that herbivorous insects can escape their natural enemies by switching to a novel host plant, with consequences for the evolution of host plant specialisation. However, if natural enemies follow herbivores to their novel host plants, enemy‐free space may only be temporary. We tested this by studying the colonisation of the introduced tree Eucalyptus grandis (Hill) Maiden (Myrtaceae) by insects in Brazil, where various species of herbivores have added eucalyptus to their host plant range, which consists of native myrtaceous species such as guava. Some herbivores, for example, Thyrinteina leucoceraea Ringe (Lepidoptera: Geometridae), cause outbreaks in eucalyptus plantations but not on guava, possibly because eucalyptus offers enemy‐free space. We sampled herbivores (mainly Lepidoptera species) and natural enemies on eucalyptus and guava and assessed parasitism of Lepidoptera larvae on both host plant species during ca. 2 years. Overall, predators were encountered more frequently on guava than on eucalyptus. In contrast, parasitoids were encountered equally and parasitism rates of Lepidoptera larvae were similar on both host plants. This indicates that herbivores may escape some enemies by moving to a novel host plant. However, this escape may be temporary and may vary with time. We argue that studying temporal and spatial patterns of enemy‐free space and the response of natural enemies to host use changes of their herbivorous prey is essential for understanding the role of natural enemies in the evolution of host plant use by herbivorous arthropods.

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“…as CPs, whose VOCs have been categorized into three distinct types, namely, cool-pungent, cool-sweet, and cool-fruity, respectively 29 . In addition, in this study we explored the importance of plastic experiences of exposure to mint odors on predators' attractivity, because we are aware that olfactory preference of herbivores' natural enemies can be elevated through associative experiences 30 . The natural enemies come to prefer VOCs released from the herbivore-infested host plant in some cases when they have previously experienced the conspecific herbivore prey on the conspecific host species with the same genotype 31,32 .…”

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confidence: 99%

Mint companion plants enhance the attraction of the generalist predator Nesidiocoris tenuis according to its experiences of conspecific mint volatiles

Rim

Hattori

Arimura

2020

Sci Rep

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Mint plants enable improvement of pest management by attracting herbivore enemies to constitutively released mint volatiles. The generalist predator Nesidiocoris tenuis is used worldwide to control agricultural pests, but little is known about whether mint can serve as a companion plant that attracts this predator. To examine this, olfactory responses of N. tenuis were assessed using apple mint, candy mint, and spearmint as odor sources. Of the volatiles released by these mint species, candy mint volatiles alone were more attractive than those from undamaged eggplant, and were as attractive as volatiles from eggplant damaged with Spodoptera litura larvae. However, no prominent preference for particular volatile(s) among the mint volatiles was shown by O. strigicollis. When N. tenuis had been previously exposed to candy mint, the predator showed a stronger preference for candy mint volatiles than damaged eggplant volatiles. It was, however, irrelevant whether the predator received benefit or not by predating animal prey during the mint-experience period. In contrast, spearmint-experience increased the preference for spearmint volatiles only when the predator acquired prey during the mintexperience period. These findings suggest that previous exposure of N. tenuis to some particular mint species can increase its preference for volatiles from the conspecific mints. Plants produce and emit volatile organic chemicals (VOCs) in order to resist environment stresses such as heat and light 1 , to deter herbivores and pathogenesis 2-4 , and to attract beneficial organisms, including natural enemies of herbivores 5-7 and pollinators 8. The pivotal roles of plant VOCs in the tritrophic system consisting of plant, herbivore, and predator have been intensively researched in a large array of cultivated crops 7 to be applied for use of biological control of herbivores 9. Among such applications, "companion planting" is one successful example of polyculture in which target plants (TPs) are cultivated with companion plants (CPs) to assist TP growth or protection against pests by attracting beneficial insects or repelling pests 10. For example, CPs such as mint, basil and marigold work as attractants for herbivore enemies 11,12. Moreover, an aphid predator, Cycloneda sanguinea L. (Coccinellidae), has been shown to be attracted to corianders owing to their pollen and nectar serving as supplementary foods 13. Recently, Togashi et al. showed that candy mint (Mentha x piperita L. cv. Candy) and spearmint (M. spicata L.) attract Phytoseiulus persimilis Athias-Henriot (Phytoseiidae), a specialized predatory mite of Tetranychidae, but not Neoseiulus californicus McGregor (Phytoseiidae) 14 , a generalized predator that consumes not only mites but also pollen, thrips, and other tiny arthropods 15. These results were certainly unexpected because it was initially expected that the generalist N. californicus rather than the specialist P. persimilis would be responsive to mint VOCs. To the best of our knowledge about companion plants attracting...

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Time scales of associating food and odor by predator communities in the field

Cited by 11 publications

References 68 publications

Associative learning of host presence in non‐host environments influences parasitoid foraging

Associative learning of host presence in non‐host environments influences parasitoid foraging

Parasitoids follow herbivorous insects to a novel host plant, generalist predators less so

Mint companion plants enhance the attraction of the generalist predator Nesidiocoris tenuis according to its experiences of conspecific mint volatiles

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