Oviposition strategy as a means of local adaptation to plant defence in native and invasive populations of the viburnum leaf beetle

Desurmont, Gaylord A.; Hérard, Franck; Agrawal, Anurag A.

doi:10.1098/rspb.2011.1294

Cited by 14 publications

(13 citation statements)

References 38 publications

(48 reference statements)

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“…Second, the oviposition choices and strategies of VLB appear to be shaped, at least in part, by this wound response. Not only have we shown here that VLB prefers undefended dead twigs, but also we have previously shown that native populations of VLB have locally adapted to plant species with differential twig defensive responses (Desurmont et al 2012). Nonetheless, in the majority of Viburnum species, we observed wound responses that were dramatically lower under natural conditions (i.e., where beetles had a choice for oviposition) as compared to the results of a manipulative study, where VLB females were forced to oviposit on particular branches, especially at high egg density (Fig.…”

Section: Discussionsupporting

confidence: 56%

“…The production of scar tissue in response to oviposition is lower in North American Viburnum species than in Eurasian congeners and this lower response may have contributed to VLB invasion in North America (Desurmont et al , 2012. However, our field observations show that neither variation in twig defense nor insect performance explained VLB defoliation patterns.…”

Section: Discussioncontrasting

confidence: 55%

“…are being readily attacked. The combination of adaptive choices on poorly defended hosts and the relative lack of effective natural enemies in the introduced range together may have created ecological conditions favorable to the VLB as an outbreaking pest in North America (Desurmont et al 2012).…”

Section: Introductionmentioning

confidence: 99%

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Do plant defenses predict damage by an invasive herbivore? A comparative study of the viburnum leaf beetle

Desurmont

Agrawal

2014

Ecological Applications

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The impact of plant defenses on insect herbivores is widely accepted, but their relative effects on oviposition choice, survival, and larval growth in preventing pest damage, especially for invasive insects, is not fully understood. Here, we examined the potential for plant defenses to reduce the economic and environmental impacts of an invasive herbivore, the viburnum leaf beetle, VLB (Pyrrhalta viburni), on Viburnum species in North America. We used a common garden with 15 host Viburnum species of North American, European, and Asian origin and evaluated oviposition preferences, twig defense against oviposition (a reaction that crushes VLB eggs), larval performance in the lab and field, and foliar damage to mature shrubs in two consecutive years. VLB oviposition preference was the strongest predictor of plant damage, with twig defense and larval performance explaining little of the defoliation patterns. In particular, we showed that VLB females evade key defenses by choosing poorly defended twigs for oviposition; assays on the 15 Viburnum species revealed that adults laid over four times more eggs on dead (undefended) twigs than on living twigs. We additionally tested the hypothesis that shrubs with a higher proportion of dead twigs are preferentially chosen for oviposition, leading to more defoliation by larvae and increased dieback in the following year. We term this the infestation feedback hypothesis. Indeed, we report consistent positive correlations between percentage dieback, oviposition, and percentage defoliation across Viburnum species, and among individuals within two species tested separately (V. dentatum and V. opulus). Our results demonstrate that oviposition preference plays a major role in the susceptibility of Viburnum shrubs to the invasive VLB through adults choosing high-quality species for their larvae (a strong preference-performance correlation) and avoiding well-defended twigs among preferred species. More generally, where invasive insects can avoid plant defenses and when preference and performance are positively correlated, an infestation feedback loop can lead to persistent pest problems. Because dieback weakens Viburnum defenses by providing optimal oviposition sites, we recommend that Viburnum growers mechanically remove dead twigs from susceptible shrubs at the end of the growing season, especially in the early stages of VLB colonization.

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Section: Discussionsupporting

confidence: 56%

Section: Discussioncontrasting

confidence: 55%

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Do plant defenses predict damage by an invasive herbivore? A comparative study of the viburnum leaf beetle

Desurmont

Agrawal

2014

Ecological Applications

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“…Heavily infested twigs often die, circumventing their capacity to produce a wound response, and egg survivorship is consequently positively associated with egg mass density. This correlation was consistent across 16 Viburnum species from Europe, Asia, and North America , with the exception of V. tinus, a European species (Desurmont et al, 2012). Here, we explore two potential additional benefits of aggregative oviposition.…”

Section: Introductionmentioning

confidence: 55%

Reduction of oviposition time and enhanced larval feeding: two potential benefits of aggregative oviposition for the viburnum leaf beetle

Desurmont

Weston

Agrawal

2013

Ecological Entomology

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1. Although aggregation in non-social arthropods is common, its adaptive value is not always clear. Oviposition behaviour of the viburnum leaf beetle (Pyrrhalta viburni ) is aggregative, with females preferring to lay eggs on twigs already infested by conspecifics. We previously showed that aggregative oviposition aided in overcoming host plant defences. Here we explore two additional benefits of this behaviour: reduction of time investment in oviposition; and improvement of host use by larval group feeding.2. In video-recorded trials, the presence of conspecific egg masses did not have an impact on the time associated with oviposition, but it did affect females' preoviposition behaviour: the length of foraging movements was 21% shorter on infested than on non-infested twigs, and was concentrated near the infested area.3. In two separate studies of insect performance, larvae were reared to maturity in groups of different densities (five or 10, and five or 20, respectively) on several hosts (four and 17 Viburnum spp., respectively). Independent of host species, adults were > 13% heavier (groups of 10 vs. five), and pupation success was 27% higher (groups of 20 vs. five) at higher larval density.4. Two additional effects were dependent on host species: larval survivorship (groups of 10 vs. five), and adult mass (groups of 20 vs. five). These effects were not associated with plant defensive traits (i.e. trichomes or leaf toughness), but adult mass was associated with host nutritional quality (i.e. foliar nitrogen content).5. These results show that several traits of P. viburni larval performance are positively density-dependent, and suggest that benefits of group feeding could have played a role in the evolution of oviposition behaviour in P. viburni . Our results also demonstrate that plant quality can mediate benefits of aggregation, underscoring the importance of ecological context in understanding the feeding strategies of insects.

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“…These studies include the deposition of eggs either on or in plant tissues of closely related taxa (Müller & Rosenberger, 2006;Gültekin, 2007), the triggering of gall induction at oviposition sites (Formiga et al, 2011), and the ovipositor probing of egg-insertion sites to assess plant-tissue suitability by agromyzid leaf miners (Sehgal, 1971;Winkler et al, 2010). In addition, insect oviposition frequently activates counterdefenses by the host plant that include chemical defenses such as the generation of plant-host volatile chemicals as a response from oviposition lesions that attract egg parasitoids (Colazza et al, 2004;Moraes et al, 2008), and structural defenses such as egg-crushing wound response tissue from the plant hosts of certain leaf beetles (Desurmont et al, 2012). The natural history of insect oviposition in plants has provided a major source of data and inferences as to how plants and insects interact on modern ecological and evolutionary time scales (Renwick, 1989;Childers, 1997).…”

Section: Introductionmentioning

confidence: 99%

The natural history of oviposition on a ginkgophyte fruit from the Middle Jurassic of northeastern China

et al. 2017

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A distinctive pattern of oviposition lesions occurs on a ginkgoalean seed, Yimaia capituliformis, which likely was inflicted by a kalligrammatid lacewing with a long, sword-like, plant-piercing ovipositor. This newly recorded oviposition type, DT272, occurs in the 165 million-year-old Jiulongshan Formation, of Middle Jurassic age, in Northeastern China. DT272 consists from three to seven, approximately equally spaced lesions with surrounding callus tissue, the fabricator of which targeted fleshy outer and inner tissues of a ginkgophyte fruit. This distinctive damage also is known from the fleshy attachment pad surfaces of basal bennettitalean bracts. Examination of the life history of this probable ginkgoalean-kalligrammatid oviposition interaction indicates that the spacing of the eggs in substrate tissues disfavored inter-larval contact, but little can be said of defense and counterdefense strategies between the plant host and the newly hatched immatures.

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Oviposition strategy as a means of local adaptation to plant defence in native and invasive populations of the viburnum leaf beetle

Cited by 14 publications

References 38 publications

Do plant defenses predict damage by an invasive herbivore? A comparative study of the viburnum leaf beetle

Do plant defenses predict damage by an invasive herbivore? A comparative study of the viburnum leaf beetle

Reduction of oviposition time and enhanced larval feeding: two potential benefits of aggregative oviposition for the viburnum leaf beetle

The natural history of oviposition on a ginkgophyte fruit from the Middle Jurassic of northeastern China

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