A review of the biology and control of the vine weevil, Otiorhynchus sulcatus (Coleoptera: Curculionidae)

At the turn of the century, damage by Otiorhynchus sulcatus was sporadic and limited to small areas. Increasing horticultural intensification and the adoption of husbandry techniques favourable to the weevil, such as the use of polythene mulches, increased its pest status. The development of the early inorganic pesticides reduced the number of serious outbreaks of this pest and weevil control was further improved by the development of the persistent organochlorine insecticides in the 1940's. The banning of a number of the more persistent insecticides over recent years has now left the horticultural industry in a very vulnerable position. O. sulcatus is now a pest on a range of horticultural crops throughout the temperate regions of the world. Infestations are most common in Europe (where it originated) and the USA, and nearly 150 plants species have been identified as potential hosts to O. sulcatus. Damage is most frequently caused by the root feeding larval stage. Populations as low as one larva plant can kill sensitive species such as Cyclamen. Severe damage by the leaf feeding adults is less common, although low levels of damage or contamination by adults may be unacceptable in certain situations. There is one generation a year. Oviposition by the flightless parthenogenetic females occurs over the summer months with oviposition rates of c. 500 and 1200 eggs adult^-1for outdoor and laboratory populations, respectively. O. sulcatus mainly overwinters as larvae, although significant numbers of adults may survive in areas where winter temperatures are not too severe. A number of natural enemies, such as hedgehogs, frogs and predatory beetles, help to maintain O. sulcatus populations at a low level in natural environments, but they are less successful in intensive horticultural systems where persistent chemicals have been heavily relied on to maintain the population below the economic threshold level. Increasing environmental concern is now forcing growers to consider new pest control strategies. Controlled release formulations of non-persistent products, such as fonofos and chlorpyrifos, have shown potential as control agents for O. sulcatus larvae. Biological control agents, such as insect parasitic nematodes, have been developed commercially and new microbial control agents are in the process of development. Most of the new control products are directed towards control of O. sulcatus larvae. Adult vine weevils are nocturnal and a much more difficult target for the new control agents. It is likely that an integrated approach to pest control will be required to maintain O. sulcatus populations below their economic threshold level.     

Host plant preference and performance of the vine weevil Otiorhynchus sulcatus

Abstract 1 The relationship between reproductive performance and preference for potential host plants of the vine weevil is investigated, as shown in tests on contact (or feeding) preference, presented herein, and tests on olfactory preference, published elsewhere. 2 Assessment of reproductive performance shows that the host‐plant range of the adult vine weevil Otiorhynchus sulcatus in Europe is limited to one gymnosperm genus (Taxus sp.) and a broad range of angiosperm plants in two subclasses of the Dicotyledonae, namely Dilleniidae and Rosidae. The successful reproduction on very distantly related plant taxa suggests that the original weevil‐ and plant‐habitat has mediated the current host‐plant range of the vine weevil. 3 Contact‐preference tests with equally suitable hosts, such as Aronia, Fragaria, Euonymus and Taxus, and one less suitable host, Humulus, indicate a mismatch between contact preference and performance and, as far as olfactory preferences are known, these match neither the contact preferences nor the performance. This mismatch may arise because (i) host plant species offered do not occur in weevil habitat in Europe (e.g. Aronia and the cultivated Fragaria come from North America) and (ii) predation (or disease) risks differ among host plants, thereby altering effective reproductive performance. 4 With respect to performance on novel hosts (Thuja, Prunus) and bad hosts (Rhododendron), some between‐individual variation is found within a single population, suggesting that local populations harbour (possibly genetic) variation for adaptation to new hosts. How this variation is maintained in the face of strong selection pressures on local populations of flightless and thelytokous weevils, is an important question for understanding the broad host plant range in the vine weevil.     

Behavioural responses of the vine weevil, Otiorhynchus sulcatus, to semiochemicals from conspecifics, Otiorhynchus salicicola, and host plants

The vine weevil Otiorhynchus sulcatus is a parthenogenetic reproducing species which forages for suitable host plants at night, but is found congregated in dark places during the day. Frass of this weevil species is suspected to contain attractive compounds that are host‐plant related. Using a still‐air olfactometer, we tested adult vine weevils at night for their behavioural response to odours from conspecifics, feeding on a mixture of spindle tree (Euonymus fortunei) and yew (Taxus baccata), and to a sexually reproducing related species (Otiorhynchus salicicola), feeding on a mixture of ivy (Hedera helix) and cherry laurel (Prunus laurocerasus). Their attraction to conspecifics and O. salicicola appeared to be related to frass production. Freshly collected frass from O. sulcatus and from O. salicicola males and females was attractive. Prunus laurocerasus and H. helix have not been observed to be hosts of the vine weevil in the field. However, our tests showed that the vine weevil was attracted to mechanically damaged leaves of both plant species, whereas undamaged leaves were not attractive. Only undamaged young unfolding leaves of H. helix were also attractive. The attraction to odours from mechanically damaged host and non‐host plants suggested the involvement of compounds that are commonly found in many plant species. The involvement of plant compounds and/or aggregation pheromones in attraction to frass of the vine weevil and frass of the related weevil species O. salicicola is discussed.     

Susceptibility of strawberry cultivars to the vine weevil Otiorhynchus sulcatus (Coleoptera: Curculionidae)

Abstract 1 The feeding preference of vine weevil, Otiorhynchus sulcatus (Fabricius), adults for foliage from 21 commercial cultivars of strawberries is investigated using binary choice tests with leaf disks, using ‘Honeoye’ as a standard against which all other cultivars are compared. ‘Delmarvel’, ‘Idea’, ‘Lester’, ‘Primetime’ and ‘Seneca’ are not preferred. 2 Variation in leaf nitrogen content is correlated with feeding preference, but does not explain all the variation, because outliers exist for both preferred and nonpreferred cultivars. 3 Removal of leaf hairs with adhesive tape permits their role in deterrence to be evaluated. Eight of the 21 cultivars have deterrent leaf hairs. Paradoxically, some highly preferred cultivars (e.g. ‘Latestar’ and ‘Tristar’) have deterrent leaf hairs, and four of the five nonpreferred cultivars lack significantly deterrent leaf hairs. 4 The 21 tested cultivars do not differ in their suitability for vine weevil larval development. 5 Differences in cultivar susceptibility to vine weevil in the field may involve interactions between the palatability and nutritional value of foliage, which influence fecundity and egg placement, and the tolerance of strawberry plants to larval feeding, determined by root biomass. The nonpreference traits found in the foliage of commercial cultivars of strawberry are present by chance. Accordingly, further selective breeding to enhance strawberry varietal tolerance to vine weevils may be possible.     

Modelling temperature-dependent development and survival of Otiorhynchus sulcatus (Coleoptera: Curculionidae)

Abstract 1 We conducted a laboratory experiment to quantify the stage‐specific effects of temperature on development time and survival of Otiorhynchus sulcatus (Fabricius) (Coleoptera: Curculionidae), a serious economic pest of horticultural crops. Quantification of the relationship between stage development and temperature is required to predict seasonal occurrence of particular life stages and to optimize the timing of monitoring and control tactics. 2 Temperature‐dependent survival rate was quantified using an extreme value function and showed a skewed bell shape, due to the vulnerability of the insect to high temperature in all stages. 3 The development times of O. sulcatus decreased with increasing temperature up to 27 °C for eggs and 24 °C for larvae and pupae. The nonlinear relationship between development rate and temperature was described using the Logan model, and enabled us to estimate the optimum temperature for development. 4 The inherent variation of development time was estimated from the cumulative frequency of stage emergence, which was modelled using the cumulative Weibull function. 5 The stage emergence model, which simulated the transition from one stage to the next in relation to temperature and cohort age, was constructed by incorporating stage‐specific survival and development rate submodels with the Weibull model of stage frequency. 6 Our results show a difference in optimal temperature regime among developmental stages of O. sulcatus.     

Effects of a novel microsporidium on the black vine weevil, Otiorhynchus sulcatus (F.) (Coleoptera: Curculionidae)

A newly discovered microsporidium infecting the black vine weevil, Otiorhynchus sulcatus (F.) (Coleoptera: Curculionidae), provisionally placed in the genus Canningia, was studied to determine its impact on O. sulcatus. O. sulcatus populations from several locations were sampled and evaluated for microsporidiosis. A very low prevalence of the disease was observed in all locations surveyed (<3.0%). Laboratory studies were conducted by orally exposing both larvae and adults of O. sulcatus to varying concentrations of Canningia sp. spores. Larval bioassays at a variety of dosages (0, 10, etc.) were performed to evaluate pathogen infectivity, larval survival and growth. Adult bioassays (dosages: 0, 10, etc.) were performed to evaluate longevity, fecundity and mechanisms of vertical pathogen transmission. Larvae and adults were infected in all spore treatments. Larval growth was significantly reduced at dosages above 10 spores/larva. Adults infected at all dosages experienced high levels of mortality and fecundity was reduced to zero. Greenhouse trials were performed to determine if larvae feeding in soil acquired infections when spores were topically applied as a drench application (0, 10⁵, 10⁶, 10⁷ spores/pot). Established larvae feeding on plant roots in pots developed infections when exposed to drench treatments of 10⁶ and 10⁷ spores/pot after 14-21 days. Canningia sp. is an acute pathogen of O. sulcatus infective to both larvae and adults. Topically applied spores also infected larvae feeding on roots in soilless potting media, suggesting the possibility of using this pathogen in a microbial control program.     

Prior host feeding experience influences ovipositional but not feeding preference in a polyphagous insect herbivore

Black vine weevils, Otiorhynchus sulcatus (Fabricius) (Coleoptera: Curculionidae), are globally‐distributed polyphagous pests of many horticultural crops. We investigated how adult weevils were affected by host switching and, in particular, how host plant species nutritional and defensive chemistry affected subsequent host plant species selection and oviposition. Adults were fed one of three host plant species, blackcurrant [Ribes nigrum L. (Grossulariaceae)], raspberry [Rubus idaeus L. (Rosaceae)], or strawberry [Fragaria x ananassa Duchesne (Rosaceae)], throughout their pre‐reproductive periods and then subjected to behavioral choice assays with these plants. Foliar chemistry differed significantly among the three host plant species. Compared to raspberry and strawberry foliage, blackcurrant foliage was 13% lower in nitrogen, 3% higher in carbon, and 28% higher in phenolic compounds. Initial host plant species had a significant effect on weevil mortality, with more weevils dying when previously fed blackcurrant (12%) than strawberry (3%) or raspberry (0%) regardless of subsequent host. Initial host plant species also affected oviposition, with weevils laying only ca. two eggs per week when previously fed blackcurrant, compared to those on raspberry or strawberry (ca. 11 and 15 eggs per week, respectively). When given a choice, weevils discriminated among host plant species and tended to oviposit on plants on which they had previously fed, even when the plant was nutritionally inferior for egg production and adult survival. In contrast, feeding behavior was only affected by the current host plant species. Feeding and oviposition were related to leaf chemistry only in blackcurrant, as leaf consumption was negatively correlated with foliar carbon and zinc concentrations, and positively correlated with foliar phosphorus and potassium concentrations.     

Application of Metarhizium anisopliae (Metsch.) Sor. conidia to control Otiorhynchus sulcatus (F.) (Coleoptera: Curculionidae) larvae on glasshouse pot plants

The efficacy of the entomogenous fungus Metarhizium anisopliae was assessed against vine weevil (Otiorhynchus sulcatus) larvae in the glasshouse. Prophylactic application of M. anisopliae conidia to begonia resulted in total larval control, but curative applications were less effective with only 65% control when conidial application was delayed until 8 weeks after egg infestation. Prophylactic applications also provided effective larval control on begonia plants which received multiple egg applications over a six week period. Larval mortality was monitored on cyclamen plants which had received a prophylactic drench of M. anisopliae conidia. The population was reduced by 78% within 5 weeks of egg application and control rose to 90% after 17 weeks, although the increase was not significant. Prophylactic conidial drenches were compared with a similar number of compost incorporated conidia on cyclamen, but there was no significant difference between the two spore application strategies. Application of M. anisopliae conidia to impatiens modules before potting-on resulted in over 89% larval control compared to over 97% control when a similar number of conidia were applied to the plants after potting. Larval control was further reduced to 79% when the module drenches were reduced to one quarter of the highest dose (5 × 10⁷ compared to 2 × 10⁸ conidia per module). The persistence of three M. anisopliae strains was examined over a 20 week period on impatiens. There was no overall decline in efficacy over this period, although there was variability in the performance of the different strains and it was suggested that this was linked to temperature. The results of these experiments suggest that M. anisopliae has considerable potential as a microbial control agent for O. sulcatus on glasshouse ornamentals.     

Use of a nematode, Heterorhabditis heliothidis, to control black vine weevil, Otiorhynchus sulcatus, in potted plants

Application of aqueous suspensions of infective juvenile Heterorhabditis heliothidis, isolate T327, to the soil resulted in up to 100% parasitisation of larvae of the black vine weevil, Otiorhynchus sulcatus, in potted yew, raspberries and grapes in nurseries, and over 87% parasitisation on potted cyclamens and strawberries. Pupae and newly emerged adults on grapevines were also parasitised. Another isolate, T310, produced 92.5 to 98.5% parasitism of O. sulcatus larvae on potted cyclamens in glasshouse, but was less effective on strawberries. Neoaplectana bibionis was found to be less effective than H. heliothidis T327 strain. The use of these nematodes provides an economical and effective method for controlling O. sulcatus on potted plants in glasshouses and nurseries.     

The effect of the CpTi gene in strawberry against attack by vine weevil (Otiorhynchus sulcatus F. Coleoptera: Curculionidae)

The degree of protection against insect feeding conferred upon transgenic strawberry lines expressing the Cowpea trypsin inhibitor was evaluated under glasshouse conditions. Insect bioassays were carried out using vine weevil (Otiorhynchus sulcatus) in two experiments and in both experiments there was a highly significant reduction in damage by weevil larvae on the transgenic lines.     

Association of Beauveria bassiana with grapevine plants deters adult black vine weevils,Otiorhynchus sulcatus

Fungal entomopathogens are known as microbial pathogens of insects, colonising multiple habitats and ecosystems. Besides being an entomopathogen, the fungus Beauveria bassiana can also establish as an endophyte in plants. Limited knowledge is so far available on the ability of plant-associated B. bassiana to influence plant-feeding insects. Here, we assessed the capability of adult black vine weevils Otiorhynchus sulcatus to select grapevine as a host plant in the presence of plant-associated B. bassiana after foliar application of a commercially available mycoinsecticide (product Naturalis®) on young potted grapevine plants. Three pairwise comparisons of weevil behaviour were conducted when weevils were released in a two-choice olfactometer and were given the choice between (i) control plants and plants treated with Naturalis®, (ii) control plants and plants treated with the formulation of Naturalis® without fungal propagules, and (iii) plants treated with Naturalis® and plants treated with the formulation. Adult O. sulcatus were significantly deterred by plants treated with Naturalis® or the formulation in comparison to control plants. In a direct comparison between plants treated either with Naturalis® or the formulation weevils significantly preferred plants treated with the formulation and avoided Naturalis® treated plants, where B. bassiana putatively had established as an endophyte. These results suggest that adult black vine weevils are able to detect and subsequently avoid plants treated with B. bassiana and indicate a new mode of action of plant-associated entomopathogenic fungi when integrated in pest management programmes.     

Biological control of the black vine weevil, Otiorhynchus sulcatus (Coleoptera: Curculionidae) with entomopathogenic nematodes (Nematoda: Rhabditida)

Trials conducted under glasshouse conditions showed that control of Otiorhynchus sulcatus larvae in strawberry plants can be effective using Steinernema carpocapsae and Heterorhabditis megidis, given that temperature and moisture extremes are avoided. In field experiments, the double line T-Tape® drip irrigation system performed better than the single line T-Tape® system, effectively distributing the nematodes along and across strawberry raised beds, and placing them close to the root zone where O. sulcatus larvae feed. As soil temperatures are satisfactory for nematode infectivity from late spring to early autumn, nematode applications were aimed at late instar larvae during spring, and early instar larvae during summer. Late summer field treatment with S. carpocapsae induced 49.5% reduction of the early instar larvae, and field application of the same nematode species in late spring resulted in 65% control of late instar larvae. In the same trial, spring application of H. megidis caused 26% mortality of late instar larvae of O. sulcatus.     

Behavioural response of Heterorhabditis megidis towards plant roots and insect larvae

The behavioural response of infective juveniles (IJs) of Heterorhabditis megidis (strain NLH-E87.3) to cues from roots of strawberry (Fragaria x ananassa Duch.), thuja (Thuja occidentalis L.) and to larvae of the black vine weevil, Otiorhynchus sulcatus, was studied. Choice assays were conducted in an Y-tube olfactometer filled with moist sand. Infective juveniles were activated by the presence of intact roots of both strawberry and thuja plants. Some nematodes aggregated in the compartments with roots but most moved away from the roots to the opposite side. Given a choice, IJs showed a preference for strawberry roots above O. sulcatus larvae. No difference in preference was observed between thuja roots and O. sulcatus larvae. The combination of strawberry roots with vine weevil larvae was preferred above roots alone. In the assays with thuja roots and larvae versus thuja roots alone, however, IJs were stimulated to move but showed preference for the opposite compartment away from the arms with roots and larvae. Nematodes responded differently to mechanically damaged roots as opposed to roots damaged by vine weevil larvae. In assays with damaged thuja roots, IJs were most attracted by the roots damaged by larvae, whereas in the strawberry assays IJs showed a clear preference for the mechanically damaged roots. When challenged with a choice between strawberry and thuja roots, IJs moved preferentially to strawberry than to thuja roots. A preference for the combination of strawberry roots plus larvae over the thuja roots plus larvae was also observed.     

Efficacy of Beauveria bassiana against the strawberry pests, Lygus lineolaris, Anthonomus signatus and Otiorhynchus ovatus

There are several insect species causing serious economic losses in strawberry, Fragaria vesca L., productions. In Quebec, Canada, the tarnished plant bug, Lygus lineolaris (Palisot de Beauvois), the strawberry bud weevil clipper, Anthonomus signatus (Say) and the strawberry root weevil, Otiorhynchus ovatus (L.) are the most important pests. We tested the susceptibility of these pests to the entomopathogenic fungus Beauveria bassiana under laboratory conditions. Sixteen isolates were evaluated for their insecticide potential against these insects. Adults of each species were infected by the immersion method. All isolates were pathogenic to adults of all three species, causing mortality rates between 23.3% and 100% at a concentration of 1 × 10⁷ conidia/ml. Based on the screening results, isolate INRS‐CFL was selected for its insecticide potential and then used for further analyses against L. lineolaris, A. signatus and O. ovatus adults. Bioassays were performed to evaluate the lethal concentration (LC₅₀) and the average survival time (AST) of this isolate against both insect species. Results of dose–response mortality bioassays using four concentrations – 1 × 10⁴, 1 × 10⁶, 1 × 10⁸ and 1 × 10⁹ conidia/ml – indicated a LC₅₀ values of 5.3 × 10⁵, 1.8 × 10⁷ and 9.9 × 10⁷ conidia/ml at 7 days after inoculation for L. lineolaris, A. signatus and O. ovatus respectively. Using a dose of 1 × 10⁸ conidia/ml, the AST values were estimated at 4.41, 7.56 and 8.29 days, respectively, at a concentration of 1 × 10⁸ conidia/ml. This study demonstrated the potential of B. bassiana for the management of L. lineolaris, A. signatus and O. ovatus. Results also suggest that the heteropteran species is more susceptible than coleopteran species to B. bassiana.     

Efficacy of the entomopathogenic nematodes Steinernema kraussei and Heterorhabditis megidis against the black vine weevil Otiorhynchus sulcatus in open field‐grown strawberry plants

• 1 Entomopathogenic nematodes are commercially available for inundative biological control of many insects, including the black vine weevil Otiorhynchus sulcatus (F.) (Coleoptera: Curculionidae). Currently, there is a lack of commercial application tests in field‐grown crops comparing the efficacy of different species of entomopathogenic nematodes.
• 2 Field trials were carried out under different growing conditions in Ireland and Norway to evaluate the efficacy of two commercially available nematode species on the market for control of the black vine weevil Heterorhabditis megidis and Steinernema kraussei.
• 3 Heterorhabditis megidis was evaluated not only at temperatures ideal for this species (soil temperatures above 10 °C), but also in the low temperature trials with S. kraussei as a ‘positive control’. Steinernema kraussei is sold as a cold active product and was therefore evaluated at low soil temperatures (below 10 °C).
• 4 The overall results indicated that H. megidis was effective as long as temperatures were optimum (not dropping below 10 °C). For S. kraussei, the results obtained were rather disappointing, where control barely reached 50% in the trial with the coldest temperature. Temperature and soil type appeared to be a major limiting factor for the efficacy of both nematode species.
• 5 On the basis of the results and experience obtained in these trials, the future implications for biological control of O. sulcatus with entomopathogenic nematodes in commercial field‐grown strawberry production are discussed.

     

The entomopathogenic nematode Steinernema kraussei and Metarhizium anisopliae work synergistically in controlling overwintering larvae of the black vine weevil,Otiorhynchus sulcatus,in strawberry growbags

Previously, the combination of reduced rate of entomopathogenic nematodes (EPN) and fungus caused additive or synergistic mortality to third-instar black vine weevil (BVW), Otiorhynchus sulcatus. In this study, we examined this interaction in unheated glasshouses during winter and compared a combination of commercial formulation of a cold-tolerant EPN, S. kraussei (Nemasys L?) and fungus Metarhizium anisopliae strain V275 against overwintering third-instar BVW. The combination of M. anisopliae with S. kraussei at a rate of 1×10¹⁰ conidia+250,000 nematodes/growbag resulted in additive or synergistic effects, providing 100% control of overwintering larvae.     

Orientation of Heterorhabditis megidis to insect hosts and plant roots in a Y-tube sand olfactometer

The host-searching behaviour of Heterorhabditis megidis strain NLH-E 87.3 in the presence of insect hosts and plant roots, offered individually and in combination, was studied using a newly developed Y-tube olfactometer filled with sand. Within a period of 24 hours infective juveniles (IJs) were significantly attracted to living G. mellonella larvae and caused 100% larval mortality. Otiorhynchus sulcatus larvae, however, did not elicit host-oriented movement of IJs and no larval mortality was observed. Roots of strawberry plants induced a negative response in IJs. The combination of strawberry roots and O. sulcatus larvae, however, strongly attracted IJs leading to 37% host mortality. It was shown that this type of Y-tube choice arena is a useful tool in studying the searching behaviour of entomopathogenic nematodes in a semi-natural habitat.     

Influences of host size and host species on theinfectivity and development of Heterorhabditismegidis (strain NLH-E87.3)

The infectivity, time to first emergence of infective juveniles (IJs), total number of IJs per insect and IJs body length of the entomopathogenic nematode Heterorhabditis megidis (strain NLH-E87.3) after development in larvae of two insect hosts, Galleria mellonella (greater wax moth) and Otiorhynchus sulcatus (vine weevil) was studied. At a dose of 30 IJs, larvae of G. mellonella show to be significantly more susceptible than O. sulcatus larvae. At a dose of one IJ, vine weevil larvae were more susceptible. The number of invading infective juveniles (IJs) increased with host size while the host mortality at a dose of one IJ decreased with the increase of host size. Time to first emergence was longer at a dose of one IJ per larva and increased with the increase of host size in both insect species. Reproduction of IJs differed between host species, host sizes and doses of nematodes. Generally, the IJs body size increased with an increasing host size. The longest infective juveniles were produced at the lowest IJ doses. Results are discussed in relation to the influence of different host species and their different sizes on the performance of H. megidis (strain NLH-E87.3) as a biological control agent.     

Sustainable control of black vine weevil larvae,Otiorhynchus sulcatus (Coleoptera: Curculionidae) with Heterorhabditis bacteriophora in strawberry

Efficacy, persistence and recovery of the nematode Heterorhabditis bacteriophora was tested in the laboratory after application of the nematode to strawberry roots by dipping. To mitigate nematode sedimentation and improve attachment to strawberry roots, carboxy-methyl-cellulose was added to the nematode solution. Mortality of black vine weevil Otiorhynchus sulcatus varied between 90 and 96% in the pot trials.