Anatomical defences against bark beetles relate to degree of historical exposure between species and are allocated independently of chemical defences within trees

Conifers possess chemical and anatomical defences against tree‐killing bark beetles that feed in their phloem. Resins accumulating at attack sites can delay and entomb beetles while toxins reach lethal levels. Trees with high concentrations of metabolites active against bark beetle‐microbial complexes, and more extensive resin ducts, achieve greater survival. It is unknown if and how conifers integrate chemical and anatomical components of defence or how these capabilities vary with historical exposure. We compared linkages between phloem chemistry and tree ring anatomy of two mountain pine beetle hosts. Lodgepole pine, a mid‐elevation species, has had extensive, continual contact with this herbivore, whereas high‐elevation whitebark pines have historically had intermittent exposure that is increasing with warming climate. Lodgepole pine had more and larger resin ducts. In both species, anatomical defences were positively related to tree growth and nutrients. Within‐tree constitutive and induced concentrations of compounds bioactive against bark beetles and symbionts were largely unrelated to resin duct abundance and size. Fewer anatomical defences in the semi‐naïve compared with the continually exposed host concurs with directional differences in chemical defences. Partially uncoupling chemical and morphological antiherbivore traits may enable trees to confront beetles with more diverse defence permutations that interact to resist attack.     

Importance of resin ducts in reducing ponderosa pine mortality from bark beetle attack

The relative importance of growth and defense to tree mortality during drought and bark beetle attacks is poorly understood. We addressed this issue by comparing growth and defense characteristics between 25 pairs of ponderosa pine (Pinus ponderosa) trees that survived and trees that died from drought-associated bark beetle attacks in forests of northern Arizona, USA. The three major findings of our research were: (1) xylem resin ducts in live trees were >10% larger (diameter), >25% denser (no. of resin ducts mm⁻²), and composed >50% more area per unit ring growth than dead trees; (2) measures of defense, such as resin duct production (no. of resin ducts year⁻¹) and the proportion of xylem ring area to resin ducts, not growth, were the best model parameters of ponderosa pine mortality; and (3) most correlations between annual variation in growth and resin duct characteristics were positive suggesting that conditions conducive to growth also increase resin duct production. Our results suggest that trees that survive drought and subsequent bark beetle attacks invest more carbon in resin defense than trees that die, and that carbon allocation to resin ducts is a more important determinant of tree mortality than allocation to radial growth.     

The effect of environmentally induced changes in the bark of young conifers on feeding behaviour and reproductive development of adult Hylobius abietis (Coleoptera: Curculionidae)

Young plants of Sitka spruce, Scots and Corsican pine were subject to high and low light, and high and low nitrogen treatments in a polyhouse experiment. The effect of treatments on resin duct size and nitrogen concentration in stem bark was determined together with feeding by Hylobius abietis Linnaeus on the stems of 'intact' plants and on 'detached' stems cut from the plant. Resin duct size was largest on Corsican pine and smallest on Sitka spruce and inherent variation in duct size between the three conifer species appears to determine the pattern of weevil feeding between species. Resin ducts and the flow of resin from them protect the stems of young conifers from weevil feeding not by affecting the total amount of bark eaten but by limiting the depth of feeding and so protecting the inner phloem and cambium. Shallow feeding may increase the likelihood of effective wound repair. Duct size was positively related to plant growth and in particular increased with bark thickness. Overall, ducts were largest in the high light treatment although species differed in their response to the treatment. It is suggested that the effects of plant size, growing conditions and transplantation on susceptibility to attack by H. abietis, reported in various studies, may be due to underlying variation in resin duct size or flow rate. The effect on weevils of superficial feeding on stems is to increase the time for reproductive maturation by reducing consumption of the inner bark which has a higher nitrogen content.     

White pine weevil performances in relation to budburst phenology and traumatic resin duct formation in Norway spruce

1 As the phenological window hypothesis was reported to be significant in influencing the fitness of many herbivores feeding on tree foliage, could it also explain the performance of an insect such as the white pine weevil Pissodes strobi mainly attacking the bark phloem of conifers? 2 Under field conditions, adult weevils were caged on Norway spruce trees presenting a natural variation in their shoot growth phenology. 3 We evaluated white pine weevil biological performances, including oviposition, the number of emerged insects, survival, adult mean weight and tree defense responses as reflected by the production of induced resin canals. 4 None of the white pine weevil biological parameters was significantly affected by Norway spruce phenology. 5 The number of eggs per hole, the number of oviposition holes per leader, the number of emerged adults and their mean weight were not affected by host phenology. 6 The intensity of the traumatic response observed was variable and not correlated with budburst phenology. 7 Trees with higher traumatic responses, forming two or more layers of traumatic ducts, had lower adult emergence and estimated survival. 8 The distance between the first layer of traumatic resin ducts and the start of the annual ring was not correlated with the number of emerged weevils. 9 Norway spruce, which is an exotic tree in North America and a relatively recent host for the white pine weevil, might not possess the defense mechanisms necessary to fight off the white pine weevil.     

Successful colonization, reproduction, and new generation emergence in live interior hybrid spruce Picea engelmannii×glauca by mountain pine beetle Dendroctonus ponderosae

1 Although mountain pine beetle Dendroctonus ponderosae Hopkins are able to utilize most available Pinus spp. as hosts, successful colonization and reproduction in other hosts within the Pinaceae is rare.
2 We observed successful reproduction of mountain pine beetle and emergence of new generation adults from interior hybrid spruce Picea engelmannii × glauca and compared a number of parameters related to colonization and reproductive success in spruce with nearby lodgepole pine Pinus contorta infested by mountain pine beetle.
3 The results obtained indicate that reduced competition in spruce allowed mountain pine beetle parents that survived the colonization process to produce more offspring per pair than in more heavily-infested nearby pine.
4 We also conducted an experiment in which 20 spruce and 20 lodgepole pines were baited with the aggregation pheromone of mountain pine beetle. Nineteen pines (95%) and eight spruce (40%) were attacked by mountain pine beetle, with eight (40%) and three (15%) mass-attacked, respectively.
5 Successful attacks on nonhost trees during extreme epidemics may be one mechanism by which host shifts and subsequent speciation events have occurred in Dendroctonus spp. bark beetles.     

Resin and the Resistance of Conifers to Fomes annosus

Roots of young trees of different conifer species, Scots pine,Corsican pine, Sitka spruce, and Douglas fir were inoculatedwith Fomes annosus. In the pines, infection was negligible butin the other genera the central wood was extensively invaded.The process of infection was studied further in Sitka spruceby means of a root-severing technique in which an inoculum blockwas forced between the cut ends of a root. In most trees a centralrot developed which in some extended up into the butt: the meanextent of growth recorded was 30 cm in 14 months. In the severedroot portions infection also occurred but F. annosus was subsequentlyreplaced to a considerable extent by other micro-organisms,particularly in trees growing on a peat soil. A similar centralrot developed after inoculations of Norway spruce. The resistance of pine sapwood and the outer wood of spruceand Douglas fir can be explained at least partially by the structureand viability of the resin duct system. Larch, Douglas fir,spruce, and pine form a series showing increasing complexityand activity of the resin system. In addition, studies carriedout on the resin yields of pines growing under different conditionsshowed that the resistance of a tree to F. annosus is correlatedwith its ability to mobilize resin. Site factors, forest management,host age vigour, genetic constitution, and past history mayall influence resin mobilization.     

Nutritional disturbances of young Scots pines caused by pine bark bugs in a dry heath forest

This study deals with the effect of pine bark bugs (Aradus cinnamomeus Panzer) on the nutrition of young Scots pines (Pinus sylvestris L.). Soil and needle samples for analytical purposes were collected from a young pine stand growing on a dry barren mineral soil afflicted by pine bark bugs.The damage to vascular tissues caused by pine bark bugs disturbed the nutrition of the trees, especially in the top part of the crown. The foliar calcium, magnesium, manganese and sulphur concentrations were highly reduced. Scots pines suffered from a lack of calcium, magnesium, nitrogen and phosphorus. These deficiencies were secondary by nature, because no differences were observed between the nutrient concentrations of the underlying soil of the healthy and affected trees. The symptoms of trees damaged by pine bark bugs resembled most of all calcium deficiency symptoms.     

Pinewood Nematode,Bursaphelenchus xylophilus,Associated with Red Pine, Pinus resinosa,in Western Maryland

Red pines Pinus resinosa in Garrett and Allegany counties, Maryland, were examined during 1982-84 to determine distribution of the pinewood nematode, Bursaphelenchus xylophilus, within and among trees. Approximately 25-year-old (younger) and 47-year-old (older) trees were subdivided into the following categories: 1) trees with mostly green needles; 2) trees with mostly reddish-brown needles; 3) trees lacking needles but with bark intact; 4) trees lacking both needles and bark; and 5) trees with chlorotic, bleached-green needles. Bursaphelenchus xylophilus was found infecting 68% of younger red pines and 77% of older red pines. Nematodes were not evenly distributed in trees within any given tree decadence category or in trees of the same age. Nematodes were recovered from 20% of wood samples from trunks and primary and secondary branches in younger pines and from 15 % of older red pines. On the basis of tree decadence category, the highest incidence of infection in younger trees (31%) was in bleached-green needled trees (category 5), whereas in older trees the highest infection (25%) occurred in green needled trees (category 1). At both sites trunks were infected more often than branches.     

Methyl jasmonate induces traumatic resin ducts,terpenoid resin biosynthesis,and terpenoid accumulation in developing xylem of Norway spruce stems

Norway spruce (Picea abies L. Karst) produces an oleoresin characterized by a diverse array of terpenoids, monoterpenoids, sesquiterpenoids, and diterpene resin acids that can protect conifers against potential herbivores and pathogens. Oleoresin accumulates constitutively in resin ducts in the cortex and phloem (bark) of Norway spruce stems. De novo formation of traumatic resin ducts (TDs) is observed in the developing secondary xylem (wood) after insect attack, fungal elicitation, and mechanical wounding. Here, we characterize the methyl jasmonate-induced formation of TDs in Norway spruce by microscopy, chemical analyses of resin composition, and assays of terpenoid biosynthetic enzymes. The response involves tissue-specific differentiation of TDs, terpenoid accumulation, and induction of enzyme activities of both prenyltransferases and terpene synthases in the developing xylem, a tissue that constitutively lacks axial resin ducts in spruce. The induction of a complex defense response in Norway spruce by methyl jasmonate application provides new avenues to evaluate the role of resin defenses for protection of conifers against destructive pests such as white pine weevils (Pissodes strobi), bark beetles (Coleoptera, Scolytidae), and insect-associated tree pathogens.     

Effects of nitrogen fertilization on pine needle chemistry and sawfly performance

Summary Changes in needle nitrogen and resin acid concentrations in young Scots pine trees fertilized with ammonium nitrate were followed over 3 years. Sawfly larvae (Neodiprion sertifer) were reared on fertilized and control trees the year after fertilization. Both nitrogen and resin acid concentrations increased in fertilized trees. The fact that resin acid concentrations increased contradicts predictions of the carbon/nutrient balance hypothesis. We suggest that needle resin-acid concentrations are limited more by the size of the resin ducts than by the availability of substrate for resin acid synthesis, and that the formation of resin ducts is limited by the availability of nitrogen. A modification of the carbon/nutrient balance hypothesis, relating compartment formation to allelochemical synthesis, is discussed. Performance of sawfly larvae was not affected by fertilization treatment, probably because concentrations of nitrogen (positively affecting performance) and resin acids (adversely affecting performance) increased simultaneously in fertilized trees. Thus, the results of this study do not support the notion that fertilization increases the resistance of trees to needle-eating insects.     

Performance of the tree‐killing bark beetles Ips typographus and Pityogenes chalcographus in non‐indigenous lodgepole pine and their historical host Norway spruce

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The effect of larval aggregation behaviour on larval growth of the spruce bark beetle Dendroctonus micans

1. The great spruce bark beetle Dendroctonus micans is a primary pest of spruce in Europe. It is unusual among Eurasian scolytids in that apparently healthy trees are attacked by solitary adults, but larvae feed en masse , in response to a larval aggregation pheromone.
2. The effect of brood size on larval growth was determined in experiments on detached bark, logs and living trees. A positive relationship was found between brood size and larval growth in experiments started with either eggs or larvae up to fifth instar. The relationship appeared to be independent of the effects of both preformed and induced defences in bark.
3. No evidence was found to support the hypothesis that larvae feeding in groups spend a greater proportion of time feeding. Addition of resin to egg chambers in detached bark pieces resulted in high mortality of first-instar larvae. A possible role for larval aggregation in minimizing the effects of host defences is discussed.     

Alterations of the resin canal system of <Emphasis Type="Italic">Pinus pinaster</Emphasis> seedlings after fertilization of a healthy and of a <Emphasis Type="Italic">Hylobius abietis</Emphasis> attacked stand

Changes in resource availability and biotic and abiotic stress may alter the defensive mechanisms of pine trees. The effect of fertilisation on the resin canal structure of Pinus pinaster seedlings established in two trials in NW Spain, one attacked by Hylobius abietis and the other non-attacked, was studied. The leaders of 50 plants were destructively sampled and the resin canal density, the canal area and its relative conductive area in the phloem and xylem were assessed. Experimentally increased nutrient availability significantly decreased resin canal density in the phloem of the seedlings in the two analysed trials, where unfertilised seedlings presented up to 30% more resin canal density than the fertilised seedlings (mean value ± SEM = 0.32 ± 0.02 resin canals mm⁻² in the fertilised plants versus 0.45 ± 0.04 resin canals mm⁻² in the control plants). Fertilisation had no effect on the resin canal system in the xylem, but significantly increased tracheid size. Significant differences of resin canals among sites were observed mainly in the xylem; the resin canal density was 1.7-fold greater in the attacked site than in the non-attacked site. The similar structure of phloem resin canals in both sites supports that phloem resin canals are constitutive mechanisms of defence in P. pinaster, whereas xylem resin canals would be constitutive mechanisms but also inducible mechanisms of resistance following the attack of pine weevils or bark beetles. XM and LS equally contributed to this paper.     

Function of Sitka spruce stone cells as a physical defence against white pine weevil

Stone cells are a physical defence of conifers against stem feeding insects such as weevils and bark beetles. In Sitka spruce, abundance of stone cells in the cortex of apical shoot tips is associated with resistance to white pine weevil. However, the mode of action by which stone cells interfere with growth and development of weevil larvae is unknown. We developed a bioassay system for testing potential effects of stone cells, which were isolated from resistant trees, on weevil larvae. Bioassays using artificial diet and controlled amounts of stone cells focused on physical defence. We evaluated the effects of stone cells on establishment of neonate larvae, mandible wear and changes in relative growth rates of third instar larvae. Establishment of neonates and relative growth rates of third instars were significantly reduced by stone cells. Stone cells appeared to be indigestible by weevil larvae. Our results suggest that stone cells affect weevil establishment and development by forming a physical feeding barrier against neonate larvae at the site of oviposition, and by reducing access to nutrients in the cortex of resistant trees, which contain an abundance of stone cells in place of a more nutrient rich tissue in susceptible trees.     

Induced defence reaction in Scots pine following stem attacks by Tomicus piniperda

The induced defence reaction of Scots pine Pinus sylvestris to stem attacks by the common pine shoot beetle, Tomicus piniperda (Col, Scolytidae), was studied by inducing natural attacks on young Scots pine trees of different vigour Pruned trees were more heavily attacked by T piniperda than unpruned ones Vigorous trees successfully contained the attacking beetles within resinous lesions, whereas less vigorous trees failed to defend themselves The content of resin acids increased dramatically in the lesions on all trees, and the resin acid composition differed somewhat between some treatments Starch accumulation in the inner bark of the main stem was lower in pruned trees than in unpruned ones, and starch reserves were depleted in the most heavily attacked trees All but one of the unpruned trees survived the attack, whereas most of the severely pruned ones died following attack by beetles at densities exceeding c 300 egg galleries m⁻²     

Application of methyl jasmonate reduces growth but increases chemical defence and resistance against Hylobius abietis in Scots pine seedlings

Scots pine (Pinus sylvestris L., Pinaceae) produces a terpenoid resin which consists of monoterpenes and resin acids that offer protection against herbivores and pathogen attacks. Methyl jasmonate (MJ) is a potential plant elicitor which induces a wide range of chemical and anatomical defence reactions in conifers and might be used to increase resistance against biotic damage. Different amounts of MJ (control, 10 mm , and 100 mm ) were applied to Scots pine to examine the vigour, physiology, herbivory performance, and induction of secondary compound production in needles, bark, and xylem of 2‐year‐old Scots pine seedlings. Growth decreased significantly in both MJ treated plants, and photosynthesis decreased in the 100 mm MJ treated plants, when compared to 10 mm MJ or control plants. The large pine weevil (Hylobius abietis L.) (Coleoptera: Curculionidae) gnawed a significantly smaller area of stem bark in the 100 mm treated plants than in the control or 10 mm treated plants. The 100 mm MJ treatment increased the resin acid concentration in the needles and xylem but not in the bark. Furthermore, both MJ treatments increased the number of resin ducts in newly developing xylem. The changes in plant growth and chemical parameters after the MJ treatments indicate shifts in carbon allocation, but MJ also affects plant physiology and xylem development. Terpenoid resin production was tissue‐specific, but generally increased after MJ treatments, which means that this compound may offer potential protection of conifers against herbivores.     

Novel forest decline triggered by multiple interactions among climate,an introduced pathogen and bark beetles

Novel forest decline is increasing due to global environmental change, yet the causal factors and their interactions remain poorly understood. Using tree ring analyses, we show how climate and multiple biotic factors caused the decline of whitebark pine (Pinus albicaulis) in 16 stands in the southern Canadian Rockies. In our study area, 72% of whitebark pines were dead and 18% had partially dead crowns. Tree mortality peaked in the 1970s; however, the annual basal area increment of disturbed trees began to decline significantly in the late 1940s. Growth decline persisted up to 30 years before trees died from mountain pine beetle (Dendroctonus ponderosae), Ips spp. bark beetles or non‐native blister rust pathogen (Cronartium ribicola). Climate–growth relations varied over time and differed among the healthy and disturbed subpopulations of whitebark pine. Prior to the 1940s, cool temperatures limited the growth of all subpopulations. Growth of live, healthy trees became limited by drought during the cool phase (1947 –1976) of the Pacific Decadal Oscillation (PDO) and then reverted to positive correlations with temperature during the subsequent warm PDO phase. In the 1940s, the climate–growth relations of the disturbed subpopulations diverged from the live, healthy trees with trees ultimately killed by mountain pine beetle diverging the most. We propose that multiple factors interacted over several decades to cause unprecedented rates of whitebark pine mortality. Climatic variation during the cool PDO phase caused drought stress that may have predisposed trees to blister rust. Subsequent decline in snowpack and warming temperatures likely incited further climatic stress and with blister rust reduced tree resistance to bark beetles. Ultimately, bark beetles and blister rust contributed to tree death. Our findings suggest the complexity of whitebark pine decline and the importance of considering multiway drought–disease–insect interactions over various timescales when interpreting forest decline.     

Dependence of the cellulosolytic activity in the lichen <Emphasis Type="Italic">Hypogymnia physodes</Emphasis> (L.) Nyl. on the substrate

Samples of the lichen H. physodes were collected from bark of living trees (pine, spruce, birch, alder, rowan, and willow); from the wood of these trees and of juniper; from bark of dead spruce, alder, and rowan trees; and from the moss Hypnum pallescens. Thalli of this lichen were placed onto medium with carboxylmethyl cellulose (CMC) (water being used as a control). Output of sugars was determined using the Nelson-Somogyi technique. Cellulosolytic activity of samples from the bark of pine and birch was higher than that of samples from the bark of spruce. In thalli of the lichen from wood, from moss, and from bark of living alder and rowan trees, the output of sugars on the medium with CMC was similar to that in the control. The cellulosolytic activity was revealed in samples from the lichen from bark of dead rowan and alder trees. In the lichen from spruce bark, the output of sugars on the medium with CMC was higher in samples from dead trees in comparison with living trees. The results are discussed.     

Ethylene in induced conifer defense: cDNA cloning, protein expression, and cellular and subcellular localization of 1-aminocyclopropane-1-carboxylate oxidase in resin duct and phenolic parenchyma cells

Members of the Pinaceae family have complex chemical defense strategies. Conifer defenses associated with specialized cell types of the bark involve constitutive and inducible accumulation of phenolic compounds in polyphenolic phloem parenchyma cells and oleoresin terpenoids in resin ducts. These defenses can protect trees against insect herbivory and fungal colonization. The phytohormone ethylene has been shown to induce the same anatomical and cellular defense responses that occur following insect feeding, mechanical wounding, or fungal inoculation in Douglas fir (Pseudotsuga menziesii) stems (Hudgins and Franceschi in Plant Physiol 135:2134–2149, 2004). However, very little is known about the genes involved in ethylene formation in conifer defense or about the temporal and spatial patterns of their protein expression. The enzyme 1-aminocyclopropane-1-carboxylate oxidase (ACO) catalyzes the final step in ethylene biosynthesis. We cloned full-length and near full-length ACO cDNAs from three conifer species, Sitka spruce (Picea sitchensis), white spruce (P. glauca), and Douglas fir, each with high similarity to Arabidopsis thaliana ACO proteins. Using an Arabidopsis anti-ACO antibody we determined that ACO is constitutively expressed in Douglas fir stem tissues and is up-regulated by mechanical wounding, consistent with the wound-induced increase of ethylene levels. Immunolocalization showed cytosolic ACO is predominantly present in specialized cell types of the wound-induced bark, specifically in epithelial cells of terpenoid-producing cortical resin ducts, in polyphenolic phloem parenchyma cells, and in ray parenchyma cells.J.W. Hudgins and Steven G. Ralph contributed equally to this work.