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(a) Clusters of viburnum leaf beetle (VLB) egg masses along a Viburnum opulus twig. Eggs are laid inside cavities excavated in the twigs and hidden under the protective 'egg cap' secretion. (b) Wound tissue produced by a V. opulus twig encasing four VLB egg masses. Here, egg caps have all fallen off and no viable eggs are visible. Photos by Kent Loeffler.
Source publication
Herbivores have been hypothesized to adapt locally to variation in plant defences and such adaptation could facilitate novel associations in the context of biological invasions. Here, we show that in the native range of the viburnum leaf beetle (VLB, Pyrrhalta viburni), two populations of geographically isolated hosts-Viburnum opulus and Viburnum t...
Contexts in source publication
Context 1
... are laid in round cavities (1-2 mm diameter, 1 mm deep) excavated by the females in the terminal twigs of Viburnum shrubs. Each cavity contains an average of eight eggs [21] and is closed with a cap made of a brown secretion pro- duced by the females (2-4 mm length; figure 1a). In North America, VLB oviposition is typically aggregative, a behaviour characterized by a preference for twigs already infested with egg masses for oviposition, and the positioning of newly laid egg masses adjacent to the existing ones [18]. ...
Context 2
... results of our behavioural experiments were matched by our field observations of egg mass distri- bution for each host: twigs with greater than 10 egg masses were less abundant at the Tinus site (9.9% of the infested twigs) than at the Opulus, Rafinesquianum and Dentatum sites (25.9, 45.0 and 47.7%, respectively; elec- tronic supplementary material, figure S1), suggesting that Tinus beetles do aggregate less than beetles coexisting with the other hosts. However, because of potential differ- ences in beetle abundance between the sampling sites, a direct statistical comparison of egg mass distribution between sites was not possible. ...
Similar publications
1. Gregarious behaviours in phytophagous insects are common, but their adaptive value is rarely well understood. In the present study, we document a novel case of cooperative behaviour, the aggregative oviposition of a leaf beetle, Pyrrhalta viburni Paykull, and the realised fitness benefit of overcoming a plant defensive response (wound tissue pro...
Citations
... Acceptance of flowers as an alternative food may have evolved as an adaptation to the unpredictability of leaf production in mature V. tinus plants in the Mediterranean area. VLB has been shown to locally adapt to its host plants (Desurmont et al., 2012), and comparing the extent of florivory in Mediterranean populations and populations from other parts of its native range would be valuable to explore the evolutionary context of this behaviour. More detailed field observations would help to understand how much larvae rely on flowers in nature and if they also use other strategies to survive in the absence of their preferred food. ...
Flowers can be a valuable food source for primarily leaf‐feeding insects. They may also be an alternative diet when preferred foods are unavailable. Here we explored the value of florivory for the invasive viburnum leaf beetle (VLB). In the field, VLB larvae have been observed to feed on V. tinus inflorescences in the absence of young leaves, their preferred food. Under controlled conditions, we measured VLB larval performance when larvae were fed young V. tinus leaves, old (from the previous year's growth) V. tinus leaves, and V. tinus inflorescences. VLB larvae could complete their development by feeding solely on V. tinus inflorescences, with a negative impact on performance: larval survivorship to adult stage and adult mass decreased and developmental time increased when larvae fed on inflorescences. Survivorship was null when larvae were fed old leaves. Florivory appears to be a suboptimal diet for VLB, which may be used as a last resort when better food sources are absent. These results illustrate the importance of plasticity for the nutritional ecology of herbivorous insects. Dietary flexibility may have facilitated VLB's adoption of novel host plants in its invasive range.
... The field experiment was limited by the number of available PDB and PAP trees so we could only make evaluations under single-choice conditions and were unable to determine which species the ALB adults would choose from a distance in the field (even though we know from the 'short-range' laboratory study that females prefer to oviposit on PDB). Evaluation under field conditions is important given that wind direction, wind speed, beetle density, plant density and plant height during the active season would influence host selection by adults (Elkin & Reid, 2010;Marshall et al., 2012;Nam et al., 2013;Wang et al., 2000;Yee et al., 2009); the beetles might also adapt to host tree defence systems by changing their behaviour (Desurmont et al., 2012). We plan to plant more PDB and PAP trees in the field to test the behaviour and choices made by ALB adults in future research. ...
Forests in north-western China are comprised mainly of poplar trees, predominantly Populus alba var. pyramidalis (PAP). Both Populus deltoides cl. Beikang (PDB) and PAP are attacked by the Asian long-horned beetle (ALB), but vary in their resistance to attack. To investigate performance of ALB on PDB and PAP, we evaluated: host-locating time, feeding and oviposition; and larval survival rate and weight in single-choice and two-choice bioassays; and undertook a field single-choice test. Results showed that there was no significant difference in the time that female ALB took to locate PDB and PAP in a cage bioassay, but males located PDB faster than PAP. Although not statistically significant, the mean weight of frass produced by adults feeding on PDB was less than on PAP in both the two-choice and single-choice experiments. The mean numbers of oviposition notch grooves on PDB and PAP in the single-choice experiment were similar, but there were more oviposition notch grooves on PDB than on PAP in the two-choice experiment. Survival rates of young larvae on PDB were significantly lower than on PAP. The average weights of larvae on PAP were significantly higher than on PDB in both two-choice and single-choice experiments. In the field experiment, mean numbers of oviposition notch grooves were significantly higher on PDB than on PAP, but mean weights and survival rates of larvae were significantly lower on PDB than on PAP, which suggested that PDB attracted ALB oviposition but showed strong resistant to developing ALB offspring. In conclusion, although PDB was more attractive for oviposition by ALB, it was still more resistant than PAP, providing a useful reference for selection of resistant varieties.
... Plant defences are thought to have played a major role in the evolution of VLB ovipositional ecology (Desurmont et al., , 2012, but information on the relative impacts of plant defences and natural enemies on egg survivorship in its native range is still lacking. The impact of natural enemies may be density-dependent, which may increase or decrease the benefit of aggregating egg masses (Prokopy & Roitberg, 2001). ...
... The result that parasitism is seemingly positively density-dependent suggests a trade-off between aggregating egg masses to overcome plant defences and dispersing egg masses to escape parasitoids. However, the documented facts that native and invasive VLB populations strongly prefer to aggregate their egg masses and that native VLB populations adapt their ovipositional strategy to local variation in plant defences (Desurmont et al., 2012) strongly suggest that the benefit of overcoming plant defences has been the main driver of VLB's oviposition behaviour over evolutionary time. ...
1. The viburnum leaf beetle (VLB) is native to Eurasia and invasive in North America. It lays eggs inside young Viburnum twigs; eggs can be crushed by plant defences (wounding response) and attacked by natural enemies (parasitoids).
2. We evaluated plant defences and parasitism rates in 42 field sites in 11 European countries, on three host plants (V. opulus, V. lantana, and V. tinus), and under two main climatic conditions (Mediterranean, oceanic/continental).
3. Plant defences killed six times more eggs than natural enemies overall (25.4% vs. 4.1%). This effect was consistent for all host plants and climatic conditions. Egg survivorship and parasitism were lower in Mediterranean sites.
4. Parasitism was positively density‐dependent, indicating a higher risk of parasitism on heavily infested twigs, but this effect was confounded with host plant species.
5. These results suggest that plant defences have been the dominant selection force driving the evolution of VLB oviposition behaviour.
... For example, several plant species form necrotic tissue at the site of egg deposition; this response may result in desiccation of the eggs and/or their detachment from leaves (13,14). Egg-induced growth of novel plant tissue can squeeze and thus kill the eggs (15). Plants can also produce ovicidal compounds in response to egg deposition (16). ...
Plant defenses against herbivorous insects can target the feeding stages and the egg stage. Feeding-induced plant defenses are known to be primed by cues indicating imminent infestation, including sex pheromones. However, priming of egg-induced plant defenses has been unknown so far. Therefore, we studied whether a plant’s response to insect sex pheromones, which might indicate imminent egg depositions, primes defenses against the eggs. Indeed, exposure of pine to the sex pheromones of an herbivorous sawfly primes the tree’s defense against sawfly eggs. The priming effect results in enhanced egg mortality, enhanced accumulation of hydrogen peroxide in egg-laden needles, and differential expression of several defense-related pine genes. These findings open up exciting research perspectives in plant protection from insect infestation.
... High densities of egg masses often kill infested twigs, preventing further wound tissue production and thus enhancing egg survivorship (Desurmont et al. 2009;Desurmont and Weston 2011). These two factors, aggregative oviposition and plant wound response, are assumed to play a key role in P. viburni invasion success in North America Desurmont et al. 2012). The role of enemy release on invasion success remains to be elucidated, and the impact of natural enemies of P. viburni in its native range is still poorly known. ...
The viburnum leaf beetle Pyrrhalta viburni (Coleoptera: Chrysomelidae) is a specialist Viburnum leaf-feeder that is native to Eurasia and invasive in North America. Eggs of P. viburni are laid in round cavities excavated by the ovipositing female beetle and covered with a protective secretion. We document in this paper the mite fauna associated withP. viburni egg masses on Viburnum tinus in southern France. We then report the results of experiments investigating the seasonal patterns of mite infestation and the effects of the most
common mite found within egg masses, Trichoribates trimaculatus (Oribatida: Ceratozetidae), on P. viburni egg survivorship. A diverse mite fauna of 18 species was found on V. tinus twigs, often living within P. viburni egg masses, including predaceous, phytophagous, and detritivorous species.
Mite abundance and diversity were higher on Viburnum twigs containing at least one intact egg mass and were positively correlated with the number of intact egg masses per twig. Detritivorous mites were more abundant on twigs nine months after oviposition than one and four months after oviposition. Finally, we found no evidence that T. trimaculatus impacts P. viburni egg survivorship and overwintering success. These findings show that P. viburni egg masses and their associated cavities form a icrohabitat favorable for the establishment of several mite species. It seems likely that these associations are cases of commensalism where mites benefit from the presence of food and shelter in these protected cavities, with no direct negative impact on P. viburni eggs.
... 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). ...
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 whose fabricator 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. This article is protected by copyright. All rights reserved
... Recently, viburnum leaf beetle (Pyrrhalta viburni), a species native to Eurasia, has become established in North America (Weston et al. 2007). This species threatens the integrity of many remaining early successional shrublands, because it has transitioned to using several native Viburnum spp. as host plants (Desurmont et al. 2012), many of which have historically been important components of these transitional habitats. Viburnum leaf beetle was first detected in northwestern Pennsylvania (Erie County) in 2001. ...
... Adults emerge from mid-June (Weston et al. 2007) to late July and continue feeding on viburnum foliage. Plants that are defoliated for !2 consecutive years typically die (Desurmont et al. 2012;RJS and MIH, pers. obs.). ...
Over the last two centuries, a large and increasing number of non-native phytophagous insect species have become established in North America. In addition to the direct effects these insects have on their new host plants, indirect effects such as changes in community composition, community structure, and resource abundance have been reported. We investigated the indirect effects of viburnum leaf beetle (Pyrrhalta viburni), a Eurasian native, on a landbird community using shrubland habitat during spring migration. We compared avian community composition and bird mass before and after viburnum leaf beetles invaded our site. Before invasion, southern arrowwoods (Viburnum dentatum) were a prominent native component of the vegetation community. Not only was the avian community more diverse prior to infestation, our estimates from this period also suggest seven of nine species examined gained mass, and most did so at high rates. The avian community was less diverse after beetle infestation, and capture rates for seven of 69 species dropped significantly while capture rate of one species increased significantly. Finally, after infestation we found that no bird species showed evidence of mass gain. Given the decline of early successional habitats in eastern North America and the significance of early successional habitats to both birds that breed in these habitats as well as forest breeding birds during nonbreeding phases of the annual cycle, degradation of these habitats by invasive insects may have a larger effect than previously realized.
... and leatherleaf varieties (Viburnum spp. Resistance to VLB is attributed to a number of traits (Desurmont et al. 2012 ) including plant chemistry and plantinduced defenses. A list of the most susceptible or resistant species of viburnum can be found at Viburnum Leaf Beetle Citizen Science, Susceptibility to Infestation (Weston 2015). ...
... A list of the most susceptible or resistant species of viburnum can be found at Viburnum Leaf Beetle Citizen Science, Susceptibility to Infestation (Weston 2015). In North America, VLB have overcome some defenses by coordinating aggregated oviposition attacks and overwhelming the plant's ability to crush or push out eggs (Weston and Desurmont 2011; Desurmont et al. 2012). As VLB spreads into new areas, consider planting resistant cultivars and species. ...
... These results complement previous research showing that VLB oviposition is a highly plastic behaviour, depending on several factors and environmental conditions including: twig and leaf traits (Weston et al., 2008;Desurmont & Weston, 2011;, presence and quality of conspecifics (Desurmont & Weston, 2010), and presence of dead twigs on the infested shrub Desurmont & Agrawal, 2014). Adaptive plasticity certainly played a role in shaping the interactions between VLB and its host plants in its native range: previous research showed that VLB populations coexisting with different Eurasian Viburnum species have adapted their oviposition strategy (aggregative vs. non-aggregative) in accordance with the defensive capacity of their host plant, and are able to adjust their strategy when transferred on a different host plant (Desurmont et al., 2012). In its invasive range, owing to the generally lower defences of evolutionarily naive North American Viburnum species , VLB's offensive arsenal is even more efficient than in its native range, which probably contributed to the success of its invasion. ...
1. Plant defence of Viburnum shrubs against oviposition by its specialist herbivore, the viburnum leaf beetle [ VLB Pyrrhalta viburni ( P aykull)], involves an egg‐crushing wound response in twigs. Although the response is variable among Viburnum species, it can have a strong impact on egg survivorship. Beetles typically aggregate egg masses with conspecifics along infested twigs, forming clusters that can overwhelm the twig response. It was investigated whether twig responses and beetle oviposition behaviour vary seasonally.
2. In a field experiment, twig defences decreased towards the end of the VLB oviposition period: wound response of the N orth A merican Viburnum dentatum L. and the E uropean V. opulus L. was reduced by 100% and 54%, respectively, in S eptember compared with the J uly to A ugust period.
3. Oviposition trials demonstrated a corresponding behavioural change: VLB females displayed aggregative oviposition in A ugust, but not in S eptember.
4. Further tests revealed that late‐season VLB females reverted to aggregative oviposition after being kept on uninfested twigs, whereas females kept on heavily infested twigs did not. This behavioural change suggests that relaxation of aggregative oviposition originates from cues associated with high densities of egg masses.
5. Relaxation of aggregative oviposition may be adaptive (and beneficial for invasion) on shrubs with low levels of defences by reducing intra‐specific competition.
... For example, aggregative oviposition in the invasive viburnum leaf beetle has evolved to overcome egg-crushing defenses of viburnum hosts in its native range [23]. In its introduced range, the efficiency of this 'offensive' behavior is increased due to reduced egg-crushing defense in novel host plants, providing a coevolutionary mismatch facilitating the herbivore's invasion [21 ]. This scenario is likely prevalent in the case of herbivores that exert strong selection on their hosts, such as herbivores that often kill their host [24]. ...
