Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness

The pine weevil (Hylobius abietis), a major pest of conifer forests throughout Europe, feeds on the bark and cambium, tissues rich in terpenoid resins that are toxic to many insect herbivores. Here, we report the ability of the pine weevil gut microbiota to degrade the diterpene acids of Norway spruce. The diterpene acid levels present in ingested bark were substantially reduced on passage through the pine weevil gut. This reduction was significantly less upon antibiotic treatment, and supplementing the diet with gut suspensions from untreated insects restored the ability to degrade diterpenes. In addition, cultured bacteria isolated from pine weevil guts were shown to degrade a Norway spruce diterpene acid. In a metagenomic survey of the insect's bacterial community, we were able to annotate several genes of a previously described diterpene degradation (dit) gene cluster. Antibiotic treatment disrupted the core bacterial community of H. abietis guts and eliminated nearly all dit genes concordant with its reduction in diterpene degradation. Pine weevils reared on an artificial diet spiked with diterpenes, but without antibiotics, were found to lay more eggs with a higher hatching rate than weevils raised on diets with antibiotics or without diterpenes. These results suggest that gut symbionts contribute towards host fitness, but not by detoxification of diterpenes, as these compounds do not show toxic effects with or without antibiotics. Rather the ability to thrive in a terpene‐rich environment appears to allow gut microbes to benefit the weevil in other ways, such as increasing the nutritional properties of their diet.     

The large pine weevil Hylobius abietis (L.) as a potential vector of the pathogenic fungus Diplodia sapinea (Fr.) Fuckel

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Resistance and response of <Emphasis Type="Italic">Pinus pinaster</Emphasis> seedlings to <Emphasis Type="Italic">Hylobius abietis</Emphasis> after induction with methyl jasmonate

Experimental induction of plant chemical defences with methyl jasmonate (MeJa) is a valuable tool for understanding the ecology of plant defensive responses. However, few studies have examined whether MeJa-induced defences in conifers are effective against insect herbivores. We studied, in 17 half-sib Pinus pinaster families, (i) the effect of MeJa application on plant growth and on the induction of diterpenoid resin in different sections of the stem; (ii) whether MeJa-induced defences increase the resistance of living pine juveniles against the large pine weevil Hylobius abietis in an in vivo bioassay and (iii) the induction of resin content after weevil wounding. Resin concentration was greater in the upper section of the stem compared with basal sections in both MeJa-induced and non-induced seedlings. Sixty days after MeJa application, treated plants showed 40% greater resin content all along the stem, but reduced height growth compared to control plants. MeJa-induction was effective against the pine weevil, as induced seedlings were 21% less damaged than control plants. Wounding activity by H. abietis produced a strong local defensive response after 48 h, where resin concentration was double that observed in the basal and apical sections not exposed to the insects.     

The effect of red wood ant abundance on feeding damage by the pine weevil Hylobius abietis

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Growth and nutritional response of Pinus pinaster after a large pine weevil (Hylobius abietis) attack

Hylobius abietis is an important pest of coniferous plantations in Europe, to which high mortality, stem deformities, and growth loss are typically attributed. In pine trees, as in other long-lived organisms, there is uncertainty regarding the long-term costs of short-term resistance against invading organisms. We examined the nutritional status of Pinus pinaster after a 2-year long H. abietis attack, measuring needle and phloem N and P concentrations, and the impact of the damage on subsequent growth, survival, and stem deformities over a period of 5 years. The study sites were a P. pinaster family × fertilization trial, and a neighbouring twin trial with similar climate and soil characteristics that was not attacked. Growth losses after the H. abietis attack were important (up to 40%), but restricted to the first years after the attack. Five years after the attack, the annual height increment of pines in the attacked stand was not related to the initial damage suffered, and plants showed regular stems, normal leader dominance, and regular height after 5 years. These findings suggest strong compensatory growth in P. pinaster and indicate relatively high tolerance to the large pine weevil. Needle nutrient concentrations in the healthy stand were, as expected, significantly greater in experimentally fertilized plants, and they were linearly related to those in phloem showing equilibrated stoichiometry both for nitrogen (r = 0.86; P < 0.01; N = 25) and phosphorus (r = 0.84; P < 0.01; N = 25). However, at the attacked stand, nutrient concentrations in the needles did not follow the experimentally manipulated nutrient availability in soils, and phosphorus concentration in the needles was unexpectedly not related to those in the phloem. The pine seedlings attacked by H. abietis showed altered potential of allocating nutrients to their tissues according to the nutrient availability existing in the soil, as well as altered stoichiometry in N and P concentrations among phloem and leaves. Maritime pine seems to be tolerant to the pine weevil attack, at least in the conditions of this study, where pine weevil damage caused a deep alteration of nutrient allocation and nutritional status. Further research is needed to elucidate to what extent altered nutrient allocation may be part of an induced response to the attack or just derived from the vascular injury caused by the weevil wounding in the phloem.     

Pine weevil damage to Norway spruce seedlings: effects of nutrient‐loading,soil inversion and physical protection during seedling establishment

• 1 The pine weevil Hylobius abietis (L.) feeds on the bark of young conifer seedlings and is one of the most economically important forest pests in Europe.
• 2 In a field experiment, we examined the combined effects of the treatments: nutrient‐loading of seedlings, planting in scarified plots and protection of seedlings against pine weevil damage for either half a season or a full season.
• 3 Nutrient loading had no significant effect on the amount of pine weevil feeding.
• 4 Seedling mortality was significantly reduced when seedlings were protected from pine weevil feeding during establishment. This occurred even though the debarked area of protected seedlings 5 weeks after the shields had been removed was similar to that of the unprotected seedlings. This indicates that initial protection rendered the seedlings more tolerant to later wounding by pine weevil.
• 5 Planting in soil inversion significantly reduced feeding compared with planting in humus.
• 6 We conclude that nutrient‐loading of seedlings in the autumn before planting would not increase pine weevil feeding after planting. Mortality could be reduced by treatments that postpone the start of pine weevil feeding on seedlings. Such treatments, combined with planting in soil inversion, would result in increased seedling growth, vitality and tolerance to pine weevil attack.

     

Feeding on roots in the humus layer by adult pine weevil, Hylobius abietis

1 The consumption by adult pine weevil, Hylobius abietis, of the bark of roots present in the humus layer was assessed in a field study conducted in southern Sweden during two years (1998 and 2002). The study sites were divided into two areas: (i) a shelterwood where 80–100 mature Scots pine trees per hectare remained after cutting and (ii) a clearcut where no trees were left. 2 On average, 3741 m² per hectare of root bark was present in the humus layer, of which 135 m² was not coniferous but comprised species such as bilberry and broadleaved trees. 3 The mean area debarked by pine weevils was 2.9 m² per hectare; 2.6 m² of conifer roots and 0.3 m² of bilberry roots. Roots of broadleaved trees were almost never consumed. No clear preferences for roots of a specific level of vitality were observed. 4 No consistent difference between the shelterwood and clearcut was found, either in the amount of root bark area available or in the extent of root feeding by pine weevil. 5 A weak negative correlation between debarked areas on roots and seedlings was found, indicating that root feeding may have reduced damage to seedlings. 6 It is concluded that conifer roots in the humus layer constitute a major food source for the pine weevil and can be utilized for a considerable period in both clearcuts and shelterwoods.     

Chemical composition and antifeedant activity of some aromatic plants against pine weevil (Hylobius abietis)

The pine weevil Hylobius abietis is an important pest causing severe damage to conifer seedlings in reforestation areas in Europe and Asia. Plants that have no evolutionary history with the pine weevil are of special interest in the search for compounds with a strong antifeedant activity. Thus, the essential oils of nine aromatic plants, viz Amomum subulatum, Cinnamomum tamala, Curcuma longa, Laurus nobilis, Ocimum basilicum, Origanum majorana, Origanum vulgare, Syzygium aromaticum and Trachyspermum ammi were extracted by hydrodistillation. The essential oil constituents were identified by gas chromatography–mass spectrometry, and antifeedant properties towards the pine weevil were assessed using choice feeding bioassay. The essential oils of C. longa, O. majorana, S. aromaticum and T. ammi showed an excellent antifeedant activity towards the pine weevil for 24 hr, whereas the essential oil of other plants showed the activity for 6 hr. There was a positive correlation between the amount of benzenoid compounds and the antifeedant activity of the essential oils. This study suggests that pine weevil non-host plant compounds have potential to be used for the protection of seedlings against pine weevil feeding. However, further study will be needed to explore the antifeedant activity of individual components and oils in the laboratory as well as in the field.     

Evaluation of attractants and traps for monitoring small banded pine weevil Pissodes castaneus

This study aimed to develop a semiochemical‐baited trapping system to monitor the populations of small banded pine weevil, Pissodes castaneus, a serious pest in Pinus sylvestris young stands that are weakened by biotic and abiotic factors. The scope of the work included the development of a dispenser for compounds (ethanol and α‐pinene) emitted by P. sylvestris and the pheromones of P. castaneus: grandisol and grandisal. Additionally, the effectiveness of beetle catches in different types of traps (unitrap, cross‐unitrap and long and short pipe traps) baited with a dispenser was assessed. The olfactometric studies showed that most of the newly hatched beetles that had not fed were attracted by a mixture of grandisol and grandisal. However, in the group of feeding beetles, half were attracted by a mixture of ethanol and α‐pinene. These results indicated that both pheromones and α‐pinene plus ethanol should be useful for capturing P. castaneus beetles. In the field trials, the highest efficiency was found in baited unitraps that caught up to several hundred P. castaneus beetles, while the baited cross‐unitraps caught up to a few dozen beetles. No insects were found in either type of baited pipe trap or in any of the unbaited control traps. The baited unitraps and cross‐unitraps also collected, with varied intensity, Hylobius abietis beetles, a serious pest of reforestations. These results indicate the possibility of using a unitrap baited with a 4‐component attractant for monitoring P. castaneus in integrated pest management for the protection of young forests.     

Hylobius abietis L. feeding on the novel host Pinus brutia Ten. increases emission of volatile organic compounds

Plants respond to feeding by herbivorous insects by producing volatile organic chemicals, which mediate interactions between herbivores and plants. Yet, few studies investigated whether such plant responses to herbivory differ between historical host and novel plants. Here, we investigated whether herbivory by the pine weevil Hylobius abietis causes a release of volatile organic chemicals from a novel tree Pinus brutia and compared the relative amounts of volatiles released from herbivore's historical hosts and P. brutia. We collected volatiles emitted from P. brutia seedlings that were either subjected to feeding by H. abietis or no feeding. Our results indicated that feeding increased emission of volatile compounds, composed of monoterpenes and sesquiterpenes, and that the emission was several fold higher in the damaged seedlings than in undamaged seedlings. In particular, emission of monoterpenes and sesquiterpenes increased by 4.4‐and 10‐fold in the damaged plants, respectively. Strikingly, individual monoterpenes and sesquiterpenes showed much greater dissimilarity between damaged and undamaged seedlings. Furthermore, several minor monoterpenes showed negative relationships with the weevil gnawed area. We discussed these results with the results of previous studies focused on historical host plants of H. abietis and hypothesized the ecological relevance and importance of our results pertaining relevance to the plant–herbivory interactions.     

Soil type and microtopography influencing feeding above and below ground by the pine weevil Hylobius abietis

Abstract 1 The influence of soil type and microtopography on above and below ground feeding by adult pine weevils Hylobius abietis (L.) (Coleoptera: Curculionidae) was evaluated in a field experiment with enclosed weevil populations of known size. 2 Four soil treatments, each with a food source at the centre, were presented within each enclosure: (i) a flat surface with fine‐grained, cultivated humus; (ii) a flat surface with sand; (iii) a conical mound of sand; and (iv) a conical pit in sand. The food source consisted of a stem section of Scots pine Pinus sylvestris L. extending both above and below ground. 3 The majority of feeding on the half buried stem sections occurred below ground; only 2.7% of the total bark area consumed was situated above ground. The variation over time in bark area consumed was not significantly associated with any of the tested weather factors. 4 The amount of feeding was 10‐fold higher on food sources placed in fine‐grained humus than those in areas of flat sand. 5 Less pine bark was consumed on mounds of sand than flat sand surfaces, and there was more feeding in sandy pits than on flat sand. These effects on feeding are explained by the observation that the weevils had difficulties climbing the sandy slopes (27° gradient). 6 We conclude that pine weevil damage to conifer seedlings can be considerably reduced by planting on mounds of pure mineral soil and that planting deeply in the soil increases the risk of damage.     

Non-pesticide alternatives for reducing feeding damage caused by the large pine weevil (Hylobius abietis L.)

The large pine weevil (Hylobius abietis L.) is an important pest of young forest stands in Europe. Larvae develop under the bark of freshly cut pine and spruce stumps, but maturing weevils feed on the bark of coniferous seedlings. Such seedlings frequently die because of bark consumption near the root collar. We tested the effect of three treatments (the insecticide alpha cypermethrin, a wax coating and a glue coating) on the feeding damage caused by H. abietis on Douglas fir (Pseudotsuga menziesii) and Norway spruce (Picea abies) seedlings under semi-natural conditions. In two experiments (one in 2016 and another in 2017) seedlings in cages were subjected to pine weevil feeding for 16 weeks under shaded outdoor conditions. The experiment in 2016 compared insecticide and wax treatments and an untreated control on Douglas fir and Norway spruce, and the experiment in 2017 compared insecticide, wax and glue treatments and an untreated control on Norway spruce. In both experiments, all treatments significantly reduced H. abietis feeding damage at week 8 at the end of both experiments (week 16); the effect of treatments was significant only on spruce seedlings. The damages on Douglas fir seedlings was less on treated seedlings than on untreated control seedlings but differences were not significant. Coating stems with glue and especially with wax was generally effective at reducing weevil damage and in most cases provided control that was not significantly different from that provided by insecticide treatment. Our results suggest that a wax coating has the potential to replace the protection of seedlings provided by insecticides.     

Olfactory and visual stimuli used in orientation to conifer seedlings by the pine weevil, Hylobius abietis

Abstract. The influence of noncontact plant cues is investigated on the likelihood that individual conifer seedlings will be found by walking adults of the pine weevil, Hylobius abietis, in the field. Traps with solely odour or solely visual stimuli catch significantly more weevils than stimulus-free traps, and traps with the combination of odour and visual stimuli catch more weevils than traps with odour or visual stimuli alone. There is essentially an additive effect between odour and visual stimuli. The reactions to odour and visual stimuli are similar for three phases of the pine weevil's life cycle associated with three ages of clear-cuttings (i.e. sites where all trees have been harvested). Visual stimuli appear to be at least as important as odour for the pine weevil in finding an undamaged conifer seedling.     

Phenotyping tree resistance to a bark‐chewing insect,the pine weevil Hylobius abietis

Breeding for resistance to forest pests and pathogens is emerging as a promising tool for minimising the impact of the increasing biotic threats that our forests are experiencing as a consequence of global change. Efficient phenotyping protocols of resistance are urgently needed. Here we present the results of two experiments aimed to determine whether the variation in resistance to the pine weevil Hylobius abietis, a harmful pest of European conifers, can be inferred by nondestructive bioassays using excised plant material collected in forest genetic trials. Weevil damage and amount of nonvolatile resin induced by weevil feeding were assessed in young trees and in branches of adult trees using several phenotyping procedures (bioassays using either living trees, excised plant material and cut stem twigs) on four pine species (Pinus pinaster, P. radiata, P. sylvestris and P. pinea). Half of the plants were previously induced with methyl jasmonate (MJ), a treatment that is known to affect resistance to the pine weevil. In Experiment 1, living and excised plants showed parallel results: MJ treatment significantly reduced weevil damage, and saplings responded to weevil damage locally increasing the nonvolatile resin (NVR) in the stems proportionally to the damage suffered. This response was, however, slightly lower in excised than in living saplings. On the contrary, patterns of weevil feeding on stem twigs completely departed from those observed in living and excised seedlings. Moreover, cut stem twigs were unable to respond to weevil feeding increasing NVR according to the weevil damage. In Experiment 2, assessment of weevil damage on excised branches explained around 50% of variation in damage on living branches. This relationship became much more pronounced (R² = 0.81) when explored at the mean treatment level; branch manipulation did not alter the patterns of variation in resistance across pine species or MJ treatments. Irrespective of the assessment procedure, MJ consistently decreased weevil damage in all pine species, with larger reduction in weevil damage in stone and maritime pine than in radiata and Scots pine. Radiata pine was the most resistant while Scots pine was the most susceptible to the pine weevil. Overall, results suggest that using excised plant material is an operative alternative for phenotyping weevil resistance whenever care is taken to maintain the functionality of the excised plant material. This will allow taking advantage of multiple available conifer genetic trials to deepen the ecological genetics of resistance to the pine weevil and to screen for resistance without compromising the long‐term utility of those genetic trials.     

The impact of host plant species on the larval development of the large pine weevil Hylobius abietis L.

• 1 The developmental performance of the large pine weevil Hylobius abietis was studied in the laboratory on four species of conifer, Corsican pine Pinus nigra var. maritima, Sitka spruce Picea sitchensis, Douglas‐fir Pseudotsuga menziesii and Japanese larch Larix kaempferi.
• 2 All species supported development, but, there was considerable variation in larval mortality, development time and weight of adults on emergence between host species.
• 3 Levels of mortality were highest in Japanese larch (77%) and lowest in Corsican pine (8.2%), and the heaviest adults emerged from Corsican pine (130 mg) and the smallest from Douglas‐fir (74 mg).
• 4 A constitutive plant defence chemical, lignin, found to vary within a northern provenance of Sitka spruce, also strongly affected larval development.
• 5 The significance of these findings is discussed in relation to the management of H. abietis.

     

Whitebark pine facilitation at treeline: potential interactions for disruption by an invasive pathogen

In stressful environments, facilitation often aids plant establishment, but invasive plant pathogens may potentially disrupt these interactions. In many treeline communities in the northern Rocky Mountains of the U.S. and Canada, Pinus albicaulis, a stress‐tolerant pine, initiates tree islands at higher frequencies than other conifers – that is, leads to leeward tree establishment more frequently. The facilitation provided by a solitary (isolated) P. albicaulis leading to tree island initiation may be important for different life‐history stages for leeward conifers, but it is not known which life‐history stages are influenced and protection provided. However, P. albicaulis mortality from the non‐native pathogen Cronartium ribicola potentially disrupts these facilitative interactions, reducing tree island initiation. In two Rocky Mountain eastern slope study areas, we experimentally examined fundamental plant–plant interactions which might facilitate tree island formation: the protection offered by P. albicaulis to leeward seed and seedling life‐history stages, and to leeward krummholz conifers. In the latter case, we simulated mortality from C. ribicola for windward P. albicaulis to determine whether loss of P. albicaulis from C. ribicola impacts leeward conifers. Relative to other common solitary conifers at treeline, solitary P. albicaulis had higher abundance. More seeds germinated in leeward rock microsites than in conifer or exposed microsites, but the odds of cotyledon seedling survival during the growing season were highest in P. albicaulis microsites. Planted seedling survival was low among all microsites examined. Simulating death of windward P. albicaulis by C. ribicola reduced shoot growth of leeward trees. Loss of P. albicaulis to exotic disease may limit facilitation interactions and conifer community development at treeline and potentially impede upward movement as climate warms.     

Ants protect conifer seedlings from feeding damage by the pine weevil Hylobius abietis

• 1 Ants that protect food resources on plants may prey on (or deter) herbivores and thereby reduce damage. Red wood ants (of the Formica rufa group) are dominant ants in boreal forests of Eurasia and affect the local abundance of several herbivorous species.
• 2 The pine weevil Hylobius abietis (L.) is a herbivore that causes severe damage by feeding on the bark of coniferous seedlings within areas of forest regeneration.
• 3 We investigated whether ants can protect conifer seedlings from pine weevil feeding. In a manipulative experiment, ants were attracted to sugar baits attached to spruce seedlings and the damage caused by pine weevils was compared with control seedlings without ant‐baits.
• 4 The feeding‐scar area was approximately one‐third lower on the seedlings with ant‐baits compared with the controls. Besides red wood ants, Myrmica ants were also attracted in high numbers to the ant baits and the relative effects of these species are discussed.
• 5 The results obtained in the present study support the trophic cascade hypothesis (i.e. damage to herbivores is suppressed in the presence of predators). The decreased pine weevil feeding on the baited seedlings was probably a result of nonconsumptive interactions [i.e. the presence of (or harassment by) ants distracting pine weevils from feeding].
• 6 Understanding the role of ants may have important implications for future strategies aiming to control pine weevil damage. For example, maintaining suitable conditions for ants after harvesting stands may be an environmentally friendly but currently unexploited method of for decreasing weevil damage.

     

Symbiont‐mediated chemical defense in the invasive ladybird Harmonia axyridis

The volatile alkylpyrazines methyl‐ and methoxypyrazines (MPs) present in the reflex bleeds of coccinellid beetles such as the harlequin ladybird beetle Harmonia axyridis are important semiochemicals that function in antipredatory defense behavior. Pyrazines have also been coadapted from a primarily defensive role into pheromones that function in intraspecific communication, attraction, and aggregation behavior. However, the biosynthesis of MPs in ladybird beetles is poorly understood. Here, we tested the hypothesis that MPs could be produced by microbial symbionts in H. axyridis, which generates four different MPs. The evaluation of tissue‐specific MP production showed that MP concentrations were highest in the gut tissue and hemolymph of the beetles rather than the fat body tissue as the presumed site of MP biosynthesis. Furthermore, manipulation of gut microbiota by antibiotic‐containing diets resulted in a lower MP content in adult beetles. The analysis of the bacterial community of the digestive tract revealed the presence of bacteria of the genera Serratia and Lactococcus which are reportedly able to produce MPs. In line with the known diet‐dependent production of MP in H. axyridis, we determined that the presence or relative abundance of some of the potential MP producers (Enterococcus and Staphylococcus) is also diet‐dependent. We hypothesize a potential role of the microbiota in MP production in H. axyridis as a possible example for outsourcing the synthesis of ecologically important semiochemicals to its gut bacteria.     

Beauveria caledonica is a naturally occurring pathogen of forest beetles

In New Zealand, two introduced scolytid beetles, Hylastes ater and Hylurgus ligniperda (Curculionidae: Scolytinae) are pests in pine plantations. Investigation of the naturally occurring pathogens of these exotic pests revealed that both are attacked by Beauveria caledonica, a species originally isolated and described from soil in Scotland. The isolates in New Zealand were identical in morphology and conserved DNA region (rDNA, elongation factor α) sequence to isolates held in the USDA-ARS insect pathogens culture collection. In bioassay, the B. caledonica isolates were highly pathogenic to adults of H. ligniperda and larvae of Tenebrio molitor. Sporulation was observed on cadavers, confirming the species can utilise the cadavers. As both species were likely to have been introduced to New Zealand from Europe, a search was made for B. caledonica in the northern UK and Ireland. The fungus was found as a naturally-occurring pathogen of the weevil pest, Hylobius abietis (Curculionidae: Scolytinae), developing in spruce and other beetles in forests in both regions.     

Host-plant acceptance on mineral soil and humus by the pine weevil Hylobius abietis (L.)

1 The pine weevil Hylobius abietis (L.) (Coleoptera, Curculionidae) is an economically important pest of conifer forest regeneration in Europe and Asia. 2 Soil scarification, which usually exposes mineral soil, is widely used to protect seedlings from weevil attack. However, the mechanism behind this protective effect is not yet fully understood. 3 Field experiments were conducted to determine the pine weevil's responses to visual and odour stimuli from seedlings when moving on mineral soil and on undisturbed humus surface. 4 One experiment measured the number of pine weevils approaching seedlings, with and without added host odour, on mineral soil and undisturbed humus. Seedlings with added host odour attracted more weevils on both soil types. Unexpectedly, somewhat more weevils approached seedlings surrounded by mineral soil. 5 In a similar experiment, feeding attacks on seedlings planted directly in the soil were recorded. Only half as many seedlings were attacked on mineral soil as on undisturbed humus. 6 In the first experiment, the weevils were trapped 2.5 cm from the bases of the seedlings' stems, whereas they could reach the seedlings in the experiment where seedlings were planted directly in the soil. We conclude that the pine weevils' decision on whether or not to feed on a seedling is strongly influenced by the surrounding soil type and that this decision is taken in the close vicinity of the seedling. The presence of pure mineral soil around the seedling strongly reduces the likelihood that an approaching pine weevil will feed on it.