Physiological and biochemical analysis of overwintering and cold tolerance in two Central European populations of the spruce bark beetle, Ips typographus

Overwintering success is one of the key aspects affecting the development and outbreaks of the spruce bark beetle, Ips typographus (L.) populations. This paper brings detailed analysis of cold tolerance, and its influence on overwintering success, in two Central European populations of I. typographus during two cold seasons. Evidence for a supercooling strategy in overwintering adults is provided. The lower lethal temperature corresponds well to the supercooling point that ranges between −20 and −22 °C during winter months. The supercooled state is stabilized by the absence of internal ice nucleators and by seasonal accumulation of a mixture of sugars and polyols up to the sum concentration of 900 mM. The cryoprotective function of accumulated metabolites is probably based on increasing the osmolality and viscosity of supercooled body fluids and decreasing the relative proportion of water molecules available for lethal formation of ice nuclei. No activity of thermal hysteresis factors (stabilizers of supercooled state) was detected in hemolymph. Lethal times for 50% mortality (Lts50) in the supercooled state at −5, −10 or −15 °C are weeks (autumn, spring) or even months (winter), suggesting relatively little mortality caused by chill injury. Lts50 at −15 °C are significantly shorter in moist (6.9 days) than in dry (>42 days) microenvironment because there is higher probability of external ice nucleation and occurrence of lethal freezing in the moist situation.     

Pathogens of the spruce bark beetles Ips typographus and Ips duplicatus

Pathogens of two important bark beetles, Ips typographus and Ips duplicatus, both in outbreaks connected with infestation of spruces by the fungus Armillaria ostoyae, were compared at four localities in the eastern Czech Republic. Low infestations of Chytridiopsis typographi, Nosema typographi, Menzbieria chalcographi, and Gregarina typographi were detected in I. typographus. In I. duplicatus, only C. typographi and G. typographi were found and with low infection levels. The microsporidium, Larssoniella duplicati, was not detected in I. typographus, but was detected in I. duplicatus at all localities in almost 80% of the samples (a sample consisted of 40–50 beetles collected at one locality in one period) and often with a very high infection level (up to 57% of the beetles infected in a sample). The infection level of L. duplicati did not differ between generations of I. duplicatus. I. duplicatus overwinters mainly in the adult stage, and no decrease in the number of infected overwintering I. duplicatus was observed. The relatively constant infection level of L. duplicati suggests that transmission is unlikely to be horizontal via oral ingestion.     

Effect of temperature and host tree on cold hardiness of hemlock looper eggs along a latitudinal gradient

The hemlock looper, Lambdina fiscellaria, is an economically important insect pest of Canadian forests which overwinters as eggs. Although the hemlock looper causes extensive damages, no information on the mechanisms related to its cold tolerance is known. The objective of this study was to determine the effect of temperature and exposure duration on hemlock looper winter survival but also to identify seasonal supercooling capacity and cryoprotectant levels of three populations along a latitudinal gradient. As host plant may contribute to offspring overwintering success, cold tolerance of hemlock looper eggs from parents whose larvae were fed on three different tree species was also measured. Mean supercooling point (SCP) of hemlock looper eggs was lower than −30 °C from October through the following spring with values being as low as −47 °C in February. Trehalose was the most abundant sugar found in hemlock looper eggs with a peak concentration of 0.3 μg mg⁻¹ DW⁻¹. Glycerol, a polyol, was more often absent in eggs of the different populations and tree species tested in the study. When exposed to different temperature regimes for various periods of time, significant mortality of hemlock looper eggs occurred at higher temperatures than the mean SCP. Thus, hemlock looper could be considered as a chill tolerant species. No clear pattern of population and host plant effects on SCP and cryoprotectants was detected in this study. However, when exposed to different winter temperatures and exposure duration, hemlock looper from higher latitudes survived better (survival rates ranging between 0 and 89% at −20 °C) than those from lower latitudes (survival rates ranging between 0 and 56% at −20 °C). Our results may contribute to a better understanding of hemlock looper winter biology and thus facilitate predictions of outbreaks and range expansion.     

Temperature-dependent reproduction of the spruce bark beetle Ips typographus,and analysis of the potential population growth

1. The spruce bark beetle Ips typographus (L.) is one of the most important forest pests in Central Europe, but despite this the effects of temperature on life history and population growth are largely unknown. This study examines the effects of temperature on reproduction and intrinsic demographic statistics. 2. Laboratory experiments on oviposition were carried out at six temperatures in the range 12–33 °C, using the so-called sandwich rearing technique for bark beetles. 3. A linear relationship between oviposition rates and temperatures in the range 15–25 °C was used to estimate the lower temperature threshold for oviposition as 11.4 °C. With a nonlinear model fitted to the data across the whole range of experimental temperatures, the lower and upper limiting temperatures and optimum temperature were found to be 7.9, 33.7, and 28.9 °C, respectively. A model for daily oviposition rate was fitted, which describes the pattern of oviposition over the entire oviposition period. 4. The analysis of life tables, combining developmental rates, reproduction, mortality, and sex ratio, suggests maximum population growth (r_m) at near 30 °C. 5. After generating a first brood, spruce bark beetles often re-emerge from the tree and produce other sister broods. The effects of temperature and number of sister broods on demography were evaluated using age-specific life-table analyses. It is hypothesized that sister broods play an important role in regions where I. typographus is monovoltine, but have only moderate significance where this species has more than one generation per season.     

The role of semiochemicals in tritrophic interactions between the spruce bark beetle Ips typographus, its predators and infested spruce

Abstract:  Semiochemical interactions between the spruce bark beetle Ips typographus , its predators Medetera setiventris , Thanasimus formicarius and Thanasimus femoralis , and the host Norway spruce, Picea abies , were studied in the field. The chemicals S - cis -verbenol, 2-methyl-3-buten-2-ol, ipsdienol, (+)- α -pinene, (−)- α -pinene, (±)- α -pinene, limonene, camphor and their naturally occuring mixtures were used as trap baits in a multiple-choice design that allowed for comparison of their attractivity for the focal species. Medetera was attracted to both the prey aggregation pheromone and its multifunctional component, ipsdienol. On the contrary, both Thanasimus species responded predominantly to ipsdienol and less to the prey aggregation pheromone. In the case of I. typographus , the attractivity of aggregation pheromone seems to be increased by the addition of a mixture of monoterpenic tree volatiles, and by addition of ipsdienol. Bark beetles and predators showed species-specific responses to volatile mixtures representing different stages of tree decay and different stages of bark beetle colony establishment. These responses correlates with the optimal foraging habitat of each species. None of the predator species responded to 2-methyl-3-buten-2-ol, a substantial component of I. typographus pheromonal bouquet, thus it is hypothesized that only substances of monoterpenic origin attract predators.     

Reemergence and second brood in the bark beetle Ips typographus

The knowledge about reemergence of parent spruce bark beetles Ips typographus . their dispersal, and production of a second brood is reviewed. A majority of the beetles reemerge after their first brood. The process is mainly determined by temperature but high breeding density decreases the average time spent in the tree. The difference between males and females in reemergence seems to be small. In the field, a positive relationship between residence time and fat content at reemergence seems to exist, whereas the opposite tendency is found under laboratory conditions. In the laboratory, the survival of beetles reemerging late is on the average lower than that for early reemerging beetles. The time of reemergence and size of the first brood do not, however, seem to influence the production of a second brood. A large proportion of the reemerging beetles are able to establish a new brood in the laboratory, but calculations based on the number of attacked trees and estimated reemergence in forests in South Norway suggest that only about one third of the beetles actually produce a second brood. In northern Europe, successful colonization of new trees by the reemerging beetles seems to require a period of several warm days during the main reemergence period.     

Spatio-temporal impact of climate change on the activity and voltinism of the spruce bark beetle, Ips typographus

The spruce bark beetle Ips typographus is one of the major insect pests of mature Norway spruce forests. In this study, a model describing the temperature-dependent thresholds for swarming activity and temperature requirement for development from egg to adult was driven by transient regional climate scenario data for Sweden, covering the period of 1961–2100 for three future climate change scenarios (SRES A2, A1B and B2). During the 20th century, the weather supported the production of one bark beetle generation per year, except in the north-western mountainous parts of Sweden where the climate conditions were too harsh. A warmer climate may sustain a viable population also in the mountainous part; however, the distributional range of I. typographus may be restricted by the migration speed of Norway spruce. Modelling suggests that an earlier timing of spring swarming and fulfilled development of the first generation will significantly increase the frequency of summer swarming. Model calculations suggest that the spruce bark beetle will be able to initiate a second generation in South Sweden during 50% of the years around the mid century. By the end of the century, when temperatures during the bark beetle activity period are projected to have increased by 2.4–3.8 °C, a second generation will be initiated in South Sweden in 63–81% of the years. The corresponding figures are 16–33% for Mid Sweden, and 1–6% for North Sweden. During the next decades, one to two generations per year are predicted in response to temperature, and the northern distribution limit for the second generation will vary. Our study addresses questions applicable to sustainable forest management, suggesting that adequate countermeasures require monitoring of regional differences in timing of swarming and development of I. typographus , and planning of control operations during summer periods with large populations of bark beetles.     

Characterization of microsatellite loci in the spruce bark beetle Ips typographus (Coleoptera: Scolytinae)

Ips typographus is an economically important pest of Norway spruce stands. We developed five polymorphic microsatellite markers using a biotin enrichment protocol. The number of alleles ranged from three to 11 per locus and no strong evidence for null alleles was found. Heterozygosity ranged from 0.3 to 0.97. These markers could be useful tools to study the population structure and genetic consequences of I. typographus population outbreaks.     

Climate change alters elevational phenology patterns of the European spruce bark beetle (Ips typographus)

The European spruce bark beetle Ips typographus is the most important insect pest in Central European forests. Under climate change, its phenology is presumed to be changing and mass infestations becoming more likely. While several studies have investigated climate effects across a latitudinal gradient, it remains an open question how phenology will change depending on elevation and topology. Knowing how an altered climate is likely to affect bark beetle populations, particularly across diverse topographies and elevations, is essential for adaptive management. We developed a time‐varying distributed delay model to predict the phenology of I. typographus. This approach has the particular advantage of capturing the variability within populations and thus representing its stage structure at any time. The model is applied for three regional climate change scenarios, A1B, A2 and RCP3PD, to the diverse topography of Switzerland, covering a large range of elevations, aspects and slopes. We found a strong negative relationship between voltinism and elevation. Under climate change, the model predicts an increasing number of generations over the whole elevational gradient, which will be more pronounced at low elevations. In contrast, the pre‐shift in spring swarming is expected to be greater at higher elevations. In comparison, the general trend of faster beetle development on steep southern slopes is only of minor importance. Overall, the maximum elevation allowing a complete yearly generation will move upwards. Generally, the predicted increase in number of generations, earlier spring swarming, more aggregated swarming, together with a projected increase in drought and storm events, will result in a higher risk of mass infestations. This will increase the pressure on spruce stands particularly in the lowlands and require intensified management efforts. It calls for adapted long‐term silvicultural strategies to mitigate the loss of ecosystem services such as timber production protection against rockfall and avalanches and carbon storage.     

Effect of different semiochemicals blends on spruce bark beetle,Ips typographus (Coleoptera: Scolytidae)

The spruce bark beetle, Ips typographus, is a recent new introduction to the Qilian Mountains of China. An outbreak of these beetles has infested over 0.03 million hectares of spruce forests in this area. Although primary attraction to volatiles has been clearly demonstrated for I. typographus, the existence and role of attraction to insect‐produced pheromones have been widely debated. Currently, commercial lures for I. typographus include only the volatiles ipsdienol, cis‐verbenol, trans‐verbenol, 2‐methyl‐3‐buten‐2‐ol and 2‐phenylethanol in Europe. Several potential pheromone candidates have been identified for I. typographus. Our GC–MS and GC–FID analyses volatiles from hindgut extracts of I. typographus in different attack phases demonstrated that the 2‐methyl‐3‐buten‐2‐ol, ipsdienol, cis‐verbenol and trans‐verbenol as major hindgut components, and ipsenol, 2‐phenylethanol, trans‐ myrtenol and verbenone as minor components. We tested various combinations of semiochemical candidates, to determine an optimal blend. Our results suggest that addition of 2‐methyl‐3‐buten‐2‐ol to either ipsenol alone, or to blends of ipsenol and other semiochemical candidates, significantly enhanced attraction of I. typographus. Therefore, a simple lure consisting of ipsenol and 2‐methyl‐3‐buten‐2‐ol would be an optimal blend of I. typographus in the Qilian Mountains, China. We conclude that this optimal semiochemical blend may provide an effective biological pest control method for use in forest ecosystem against I. typographus.     

Host resistance elicited by methyl jasmonate reduces emission of aggregation pheromones by the spruce bark beetle, Ips typographus

We treated Norway spruce (Picea abies) stems with methyl jasmonate (MeJA) to determine possible quantitative and qualitative effects of induced tree defenses on pheromone emission by the spruce bark beetle Ips typographus. We measured the amounts of 2-methyl-3-buten-2-ol and (S)-cis-verbenol, the two main components of the beetle's aggregation pheromone, released from beetle entrance holes, along with phloem terpene content and beetle performance in MeJA-treated and untreated Norway spruce logs. As expected, phloem terpene levels were higher and beetle tunnel length was shorter (an indication of poor performance) in MeJA-treated logs relative to untreated logs. Parallel to the higher phloem terpene content and poorer beetle performance, beetles in MeJA-treated logs released significantly less 2-methyl-3-buten-2-ol and (S)-cis-verbenol, and the ratio between the two pheromone components was significantly altered. These results suggest that host resistance elicited by MeJA application reduces pheromone emission by I. typographus and alters the critical ratio between the two main pheromone components needed to elicit aggregation. The results also provide a mechanistic explanation for the reduced performance and attractivity observed in earlier studies when bark beetles colonize trees with elicited host defenses, and extend our understanding of the ecological functions of conifer resistance against bark beetles.     

Quantification of different yeasts associated with the bark beetle,Ips typographus,during its attack on a spruce tree

There were different amounts and types of yeasts associated with individuals ofIps typographus spruce bark beetles during different phases of their attack on a healthy spruce tree. The yeasts were isolated on Sabouraud agar medium in order to identify them and estimate their numbers.Hansenula holstii andCandida diddensii type yeasts were most frequently isolated. The increase in number of these two yeast types probably accounted for most of the total yeast increase found during the later attack phases of the bark beetles. Lesser amounts ofHansenula capsulata, Pichia pinus, Candida nitratophila, and twoCryptococcus type yeasts were also found.     

Characteristics of Norway spruce trees (Picea abies) surviving a spruce bark beetle (Ips typographus L.) outbreak

The characteristics of spruce individuals, which survived a massive bark beetle outbreak, were compared with the characteristics of neighbouring attacked trees in Šumava National Park (Czech Republic). Selected parameters related to crown geometry, stand conditions and distances between trees were measured or estimated. Significant differences were found between the surviving trees and the neighbouring trees attacked by I. typographus. Trees with a higher level of stem shading (longer crown length) tended to survive. The attacked trees were usually located in areas with larger basal area, especially southwards from them. A shorter distance to a previously attacked tree increased the probability of additional attack. Spruce trees with more progressive crown structure transformation (primary structure defoliation) were significantly more frequently attacked by spruce bark beetle. Superior and taller trees had a clearly longer life expectancy than dominant ones. These results show that the attack of trees by bark beetle can be predicted to a certain degree, which can be used in management of endangered spruce forests.     

Diapause and overwintering of two spruce bark beetle species

Diapause, a strategy to endure unfavourable conditions (e.g. cold winters) is commonly found in ectothermic organisms and is characterized by an arrest of development and reproduction, a reduction of metabolic rate, and an increased resistance to adversity. Diapause, in addition to adaptations for surviving low winter temperatures, significantly influences phenology, voltinism and ultimately population growth. We review the literature on diapause and overwintering behaviour of two bark beetle species that affect spruce‐dominated forests in the northern hemisphere, and describe and compare how these strategies can influence population dynamics. The European spruce bark beetle Ips typographus (L.) (Coleoptera, Curculionidae) is the most important forest pest of Norway spruce in Europe. It enters an adult reproductive diapause that might be either facultative or obligate. Obligate diapausing beetles are considered strictly univoltine, entering this dormancy type regardless of environmental cues. Facultative diapausing individuals enter diapause induced by photoperiod, modified by temperature, thus being potentially multivoltine. The spruce beetle Dendroctonus rufipennis (Kirby) (Coleoptera: Curculionidae) infests all spruce species in its natural range in North America. A facultative prepupal diapause is averted by relatively warm temperatures, resulting in a univoltine life cycle, whereas cool temperatures induce prepupal diapause leading to a semivoltine cycle. An adult obligate diapause in D. rufipennis could limit bi‐ or multivoltinism. We discuss and compare the influence of diapause and overwinter survival on voltinism and population dynamics of these two species in a changing climate and provide an outlook on future research.     

Redundancy, synergism, and active inhibitory range of non-host volatiles in reducing pheromone attraction in European spruce bark beetle Ips typographus

Brandt's voles ( Microtus brandti ) are small native mammals that inhabit the grasslands of Inner Mongolia, China. The species is considered a pest, particularly during population outbreaks, which have increased in frequency since 1970 from 1 every 7 years to 1 every 3 to 5 years. Using historical records taken between 1948 and 1998, we found that there was significant correlation between years for which the monthly averages of the Southern Oscillation Index (SOI) were consistently high, and years in which outbreaks occurred. Also there was a tendency for outbreaks not to occur in years with precipitation above or below average. For some years at some sites, annual or biannual estimates are available for the density of Brandt's vole populations. We found that the seasonal rate of increase over the non-breeding season from autumn to spring was negatively correlated with the density in autumn. The rate of increase over the breeding season from spring to autumn was independent of the density in spring but instead, reflects the species' preference for habitat with short, sparse grass; populations do not persist in highly degraded grasslands or in tall, dense grassland. The link between outbreaks and climatic indices, and the numerical response of Brandt's voles to particular habitat characteristics, suggest that current grazing intensity tends to maintain grass at low height in years with average precipitation. The substantial increase in livestock numbers over the last 50 years appears to have increased the number of years when the balance of grazing and plant growth favours high rates of increase in Brandt's vole populations, and hence, there has been an increase in the frequency of outbreaks.     

Behavioural and electrophysiological responses of the bark beetle, Ips typographus, to potential pheromone components

ABSTRACT. Field tests showed ( S )-(-)- cis -verbenol and ( R )-(+)- trans -verbenol in combination with a second pheromonal component, 2-methyl-3-buten-2-ol, more attractive than the combination with their optical antipodes. Inhibition of response to the attractant component, ( S )-(-)- cis -verbenol, by high concentrations of its optical antipode did not occur. No significant differences were noted for response to the attractant, ( S )-(-)- cis -verbenol and 2-methyl-3-buten-2-ol, with the addition of either ipsdienol enantiomer or a racemic mixture of ipsdienol enantiomers. Electroantennogram (EAG) studies correlated well with the behavioural studies. EAGs recorded from male and female beetles revealed both sexes to have a lower threshold for the pheromone, ( S )-(-)- cis -verbenol, than its host terpene precursor, (-)- alpha -pinene. EAGs showed a greater number of acceptors for (-)- alpha-pinene in males than in females. EAGs at acceptor saturation to the enantiomers of alpha -pinene and the verbenol isomers showed males more responsive to (-)- alpha -pinene, (±)- cis -verbenol, and ( R )-(+)- trans -verbenol. Significantly greater EAGs were elicited in females than in males to (-)- alpha -pinene, and (±)- and ( S )-(-)- cis -verbenol. No significant differences in EAGs of females to the enantiomers of trans -verbenol were noted. EAGs showed similar thresholds in males and females to the pheromone component, 2-methyl-3-buten-2-ol; however, female response at threshold was significantly greater than male response. The results are discussed with regard to olfactory acceptor evolution.     

Behavioural sequence in the attraction of the bark beetle Ips typographus to pheromone sources

ABSTRACT. The functions of the two synergistic pheromone components, (4S)- cis -verbenol (cV) and 2-methyl-3-buten-2-01 (MB), and the role of ipsdienol in the attraction of Ips typographus (L.) (Scolytidae) to pheromone sources were studied in the field. Absolute and relative beetle catches were compared between several traps placed at and nearby a central pheromone source: a pipe trap containing the source, a surrounding sticky trap, a nearby window trap, and four distant window traps. A higher catch in the outer down-wind distant traps indicated an up-wind anemotaxis to the source. Increased MB release, with cV constant, increased the proportion caught in the central pipe trap, indicating MB as a landing stimulus. Release of MB alone gave a very small catch. Ipsdienol could not substitute for cV in the synergism with MB. An increase of cV, with MB constant, increased the number of beetles caught, but not the proportion caught in the pipe trap. The sex ratio was equal in the window traps, but fell to 30% males in both sticky and pipe traps, showing that a large proportion of the males attracted to the source did not land. The proportion of males in the pipe trap was reduced at the highest cV dose. The results support the idea of each pheromone component having a different relative importance in releasing different steps in the behavioural chain.     

Change in overwintering mechanism of the Cucujid beetle, Cucujus clavipes

Overwintering larvae of the Cucujid beetle, Cucujus clavipes, were freeze tolerant, able to survive the freezing of their extracellular body fluids, during the winter of 1978–1979. These larvae had high levels of polyols (glycerol and sorbitol), thermal hysteresis proteins and haemolymph ice nucleators that prevented extensive supercooling (the supercooling points of the larvae were ? 10°C), thus preventing lethal intracellular ice formation. In contrast, C. clavipes larvae were freeze suspectible, died if frozen, during the winter of 1982–1983, but supercooled to ～ ? 30°C. The absence of the ice nucleators in the 1982–1983 larvae, obviously essential in the now freeze-susceptible insects, was the major detected difference in the larvae from the 2 years. However, experiments in which the larvae were artifically seeded at ? 10°C (the temperature at which the natural haemolymph ice nucleators produced spontaneous nucleation in the 1978–1979 freeze tolerant larvae) demonstrated that the absence of the ice nucleators was not the critical factor, or at least not the only critical factor, responsible for the loss of freeze tolerance in the 1982–1983 larvae. The lower lethal temperatures for the larvae were approximately the same during the 2 winters in spite of the change in overwintering strategy.     

Behavior of male and female spruce bark beetles,Ips typographus,on the bark of host trees during mass attack

The behavior of 118 spruce bark beetles, Ips typographus,was observed on trees under colonization. Most individuals were followed from when they landed until they entered or left the tree. Both males and females spent most time inspecting crevices and searching for a place to start boring or for a hole to enter. These behaviors accounted for 87 and 70% of all behavioral acts recorded for males and females, respectively. Females entered galleries with males only after a period of pushing at the gallery entrance. Males spent on average 3 min and females 4 min on the bark before entering or leaving the tree. Thirty-three percent of the beetles eventually entered the tree, 31% flew away, 35% dropped from the host, and one beetle was eaten by a predator. The results are discussed in relation to the question of mate choice in bark beetles and to studies on attack dynamics of spruce bark beetle populations.