Towards an improved understanding of bark beetle and other insect herbivore infestation in conifer forests

Forests are dynamic ecosystems subjected to regenerative, competitive and successional processes over space and time. Catastrophic events, such as storm throw, landslides, avalanches, drought episodes, fungal diseases and large-scale insect outbreaks, are the major forces interrupting these processes and drastically disturbing forest development, composition, structure and function (Attiwil, 1994). Resilient forest ecosystems are able to return to initial or equilibrium states after disturbances (Holling, 1973). While resilience relates to the rate of ecosystem recovery from a distinct disturbance event, resistance is indicated by the degree of disturbance necessary for destabilising an equilibrium state (Attiwil, 1994).

Long-term stability and diversity of forest ecosystems can be positively linked to disturbance events. For example, the recurring infestations of North American mixed hardwood and conifer forests by defoliating insects have led to high compositional and age structural diversity resulting from gap dynamics promoted by herbivore-induced mortality (Reinikainen et al., 2012). Mass outbreaks of mountain pine beetle, Dendroctonus ponderosae, in the pine stands of the USA and Canada have not only caused vast tree mortality, but also stimulated regeneration of species-rich, diversely structured tree cohorts (Amoroso et al., 2013). Similarly, high regenerative potential of Central European Mountain Norway spruce stands after wind and bark beetle disturbances was revealed by dendrochronological studies (Čada et al., 2016).

In anthropogenically strongly altered environments, as characteristic for most parts of Europe, forest management interfering in ecosystem processes might be judged as just another type of (human) disturbance (Attiwil, 1994). However, sustainable, multipurpose forest management is aimed at maintaining the important functions of forests, including a large variety of ecosystem services such as timber production, protection from natural hazards and conservation of species and biodiversity (Bončina et al., 2019; Irauschek et al., 2017). Depending on the geographic location and management objectives, management strategies can, therefore, range from non-intervention or close-to-nature forestry, over combined monetary and ideell objectives, to intensive, even-aged plantation forestry and short-rotation wood biomass production (Jactel et al., 2012).

From a socioeconomic point of view, natural disturbance represents the risk of losing essential goods and services provided by vital forest ecosystems (Hanewinkel et al., 2011; Maroschek et al., 2009). Forestry-related risk can be defined as the probability of disturbance events triggered by specific hazardous factors and leading to damage resulting in monetary and/or ideell costs from a single tree and forest stand to the regional and landscape level (Seidl et al., 2019; Hanewinkel et al., 2011; Shore et al., 2000). The evaluation of all hazards potentially relevant for predicting risk requires a sufficient understanding of the underlying ecological mechanisms and community interactions (Nelson et al., 2008). With respect to biotic risk (specifically, tree disease), Manion (1991) classified potential hazards into predisposing, inciting and contributing factors in a disease spiral, eventually leading to tree death (Figure 1).

Figure 1

Analogous to the definition of disturbance, tree/forest disease can be seen as ‘any deviation in the normal functioning of plants caused by a persistent abiotic or biotic agent’, acting either as short-term, triggering (inciting) factor or as contributing factor (Manion, 1991). Forest trees/stands become particularly susceptible to contributing stressing agents, such as wood and bark boring insects, when already weakened by predisposing and inciting factors which reduce the overall resistance to diseases and insect infestations. Inciting and contributing factors might not only act together, but also have the potential to cause tree mortality directly on their own. Endogenous genotypic disposition is further modified into predisposition of single trees or forests to abiotic and biotic damage by external factors such as climate, site and soil conditions as well as the structural characteristics of the stand (Manion, 1991; Schimitschek, 1969). Predisposing site- and stand-related variables are commonly used as predictors in applied hazard assessment systems for evaluating the current and future probabilities of disturbance events (Berryman, 1986).

The so-called (Award)-Penalty-Point systems, as suggested by Speight and Wainhouse (1989) and Berryman (1986), provide the opportunity to (1) identify the predisposing factors and rank them according to their significance; (2) weigh important predisposing factors (e.g. forest age, stand density) according to their specification (e.g. a particular age class, stand density index); (3) add up several predisposing factors to a total predisposition score under the consideration of (synergistic or antagonistic) interactions between factors; and in this way, (4) indicate the options for prophylactic, silvicultural measures and uncover the knowledge gaps. Such science-based rating systems can be practically applied as checklists (Netherer and Führer, 1999).

Netherer and Nopp-Mayr (2005) provide an example for PAS application and verification in an area where predisposing factors and actual occurrence of the addressed biotic disturbance factor, an erupting conifer bark beetle species, were concurring. Predisposition to the Eurasian spruce bark beetle, I. typographus, was evaluated for the heavily infested stands of the High Tatra National Parks of Slovakia and Poland using information available from the forest inventory datasets and a digital elevation model. The discriminatory power of site- and stand-related predisposition and of individual predisposing parameters (e.g. proportion of Norway spruce, stand age) was tested by the relative frequencies of attacked and non-attacked management units within the categories of low, medium and high predisposition. Right-skewed frequency curves with increasing predisposition levels for damaged stands and left-skewed curves for undamaged stands showed high explanatory power of the used indicators. Increased forest susceptibility to spruce bark beetle attack was indicated by high levels of solar irradiation, slope position, predisposition to storm damage, proportion of Norway spruce and stand age. Later studies in the same area using statistical approaches underlined these relationships (Mezei et al., 2014a, b).

Although the possibilities of protective forest management and control measures are limited in national parks, PAS can support the identification of high-risk zones, establishment of buffer zones and deduction of management priorities (Netherer and Nopp-Mayr, 2005). In managed stands, forest protection and silvicultural measures will not fully eliminate the risks of abiotic and biotic disturbance, but are suited to balance risks and benefits expected from potential damaging agents and forest products (Jactel et al., 2009). By directly affecting the likelihood of occurrence of damaging agents and forest predisposition to disturbing events, specific silvicultural operations, such as matching of site conditions and tree species composition, site preparation, stand composition, regeneration methods, cleaning and weed control, thinning and pruning, as well as harvesting, significantly modify the risk levels at various points in time. For example, tree species are differently adapted to particular soil structural and nutrient conditions. A mismatch between the choice of tree species composition and site conditions might result in higher risks of fungal diseases and windthrow due to damaged roots and impaired anchorage of trees (Woodward et al., 1998; Nicoll et al., 2006). Soil texture and quality play an important role in survival of herbivore insect species spending parts of their life cycles in the upper soil or humus layer. Considering the various effects of optional silvicultural operations on the ecosystem processes, management measures which strongly influence species composition and stand structure seem to affect abiotic and biotic risks most significantly (Jactel et al., 2009).

Predisposition (susceptibility) of forests to disturbance, the population dynamics of forest insects and the epidemiology of forest diseases are clearly driven by the local microclimate, provision of fuel and resources to biotic and abiotic damage factors, biological control of biotic agents by natural enemies and tree physiology and development (Jactel et al., 2009). These elements are directly linked to global climate and its drastic changes being observed over the last decades, triggering tree mortality (Allen et al., 2009). Based on data for the period 2001–2014, Sommerfeld et al. (2018) demonstrated a strong relationship between warmer and drier than average conditions and increased frequencies and intensities of disturbances in temperate forest ecosystems worldwide. These more recent empirical results substantiate earlier assumptions that forests in European temperate oceanic and continental regions are specifically susceptible to extreme events, such as drought periods and heat waves (Lindner et al., 2010).

Lindner et al. (2010) synthesised existing knowledge about the potential effects of climate change on European forest ecosystems, with particular emphasis on regional differences in the degree to which systems might be affected (sensitivity) and their ability to adapt to these changes (adaptive capacity). The study, supported by the European Commission, was thought to provide the scientific basis for the development of options to encourage and support adaptation measures in European forestry in response to global change (Kolström et al., 2011). Such measures are highly needed in view of the manifold goods and services European forests provide to human society (Maroschek et al., 2009) and concern both adaptation of the forest sector itself and the inherent adaptive capacity of the forest ecosystems. The adjustment of tree species to altered environmental conditions by natural selection and gene flow mechanisms may be severely constrained by increased pressure through natural disturbance agents, especially at the margins of species’ distribution. In the European south, forest growth and productivity are increasingly limited by the negative impacts of drought (Ogaya et al., 2003). In regions with harsh climate, such as the boreal zone and mountainous areas, rising temperatures and prolonged growing seasons let expect positive effects such as increased plant growth rates, but also negative consequences such as northward/altitudinal shifts and increased frequency of mass outbreaks of forest insect pests (Veteli et al., 2005). Important examples discussed by Lindner et al. (2010) are the conifer bark beetle species I. typographus and Pityogenes chalcographus and the defoliating moth species gypsy (now renamed to spongy) and nun moth, Lymantria dispar and Lymantria monacha. Spongy and nun moth are polyphagous and have been lately attributed high adaptive phenotypic plasticity, which means that they can adapt their life cycles to diverse climatic conditions and respond quickly to a changing environment (Fält-Nardmann et al., 2018). However, the potential impacts of these and other herbivorous insects on health and multifunctionality of European forests remain uncertain in many respects. While evidence for range extensions of native and invasive alien species is often restricted to model predictions, the mechanisms behind observed distributional changes are better understood for just a few forest herbivore insects (Battisti and Larsson, 2015).

Insects are ectothermic organisms and are thus strongly influenced by environmental parameters in their flight and dispersal behaviour, reproduction, development, performance and mortality. For example, lower mortality rates were observed in warmer winters for the winter moth, Operophtera brumata, the autumnal moth, Epirrita autumnata, and the European pine sawfly, Neodiprion sertifer, in northern Europe. The enhanced survival of hibernating eggs due to the less-frequent occurrence of lower lethal temperatures has recently resulted in the expansion of O. brumata into the north-eastern areas and of E. autumnata into the coldest, most continental areas of Scandinavian mountain birch forests (Battisti and Larsson, 2015). Food availability earlier in the season due to increased spring temperatures might favour insect development; yet, it can also have ambiguous effects on larval performance, as found by Kollberg et al. (2015) for N. sertifer. Potential outbreak risks of this important defoliator in boreal pine forests are influenced by the concentrations of defensive compounds in needles, with decreasing nutritional quality for feeding sawfly larvae (negative toxic effects) but enhanced defence against predators (positive antipredator defence effect) under rising temperatures.

The interactions between climate parameters, such as increased concentrations of tropospheric CO₂ and temperature as well as drought, and host quality and resistance against insect herbivores are diverse and do not follow clear trends among species and feeding guilds (Netherer and Schopf, 2010). While leaf-mining and chewing insects seem to be mainly negatively affected by drier and tougher foliage, elevated levels of defensive compounds and reduced nitrogen contents, some defoliating species such as the PPM, T. pityocampa, have clearly profited from climate change effects (Li et al., 2015). PPM larvae feed and survive on various pine and cedar species as well as Douglas fir in their Mediterranean core and western and central European expansion areas. Rising winter temperatures positively affect larval performance, and thereby support altitudinal and latitudinal range expansion of PPM (Battisti et al, 2005; Hoch et al., 2009).

Adapted to a Mediterranean climate, PPM spends the cold months as third or fourth instar larvae actively feeding on the needles of their (mainly) pine host trees. Distributional range of PPM is limited by those winter temperatures which do not allow the gregarious larvae to leave their protecting silk nests for feeding. Battisti et al. (2005) investigated the causes of range expansion to the north of the Paris Basin and to higher altitudes of the Venosta/Vinschgau Valley in Italy occurring since the 1970s. The observed altitudinal range shift by almost 250 m from 1975 to 2005 in the Vinschgau valley is largely due to increasing winter temperatures allowing for more frequent feeding, reducing the duration of starvation periods and enhancing larval survival. The altitudinal increase was higher on the south-faced slopes of the valley due to the effects of insolation on nest temperatures. Colony survival in the field, as additionally observed by Battisti et al. (2005), was higher at warmer and sunnier site conditions that favour larval growth and larger nest construction and allow for a higher number of feeding hours. There is strong evidence for an ongoing range expansion of PPM. An outbreak of PPM initiated in 2015 (or earlier) was detected in Carinthia in a scattered Pinus nigra and Pinus sylvestris stand growing on a south-exposed boulder field of the Dobratsch mountain at 850–1000 m elevation (Hoch et al., 2017).

In mountain areas, occurrence of and damage by forest insect pests are expected to be substantially affected by climate change (Lindner et al., 2010). The Eurasian spruce bark beetle, I. typographus, is a prominent example for a forest pest insect with frequent mass outbreaks and multiple generation development in the forest stands of the European mountain regions, even at sites of higher elevations (Netherer and Schopf, 2010; Økland et al., 2015). Bark beetle development is limited by the induction of a (facultative) reproductive diapause in multivoltine populations in late summer (Schebeck et al., 2022). The freeze-intolerant adult beetles adapt to the winter period by accumulating cryoprotective sugars and polyols, which strongly lower lethal temperature thresholds during hibernation to minimum values of −25°C and below (Annila, 1969). As a consequence, cold winter conditions do not significantly enhance the mortality rates among adult I. typographus, while this might, in fact, be the case in mild winters due to increased energy demands of overwintering individuals at higher temperatures (Økland et al., 2015). Beetle emergence from overwintering sites and spring swarming, as key elements in the spruce bark beetle life cycle, requires the accumulation of a certain thermal sum in combination with minimum air temperatures of 16°C–18°C (Wermelinger, 2004). Brood establishment and development of offspring are particularly dependent on the microclimatic conditions of Norway spruce phloem, and potential numbers of completed spruce bark beetle generations increase with rising spring and summer temperatures (Baier et al., 2007). The thermal sums required for termination of development stages of I. typographus are well-established and essential input parameters in models for predicting the phenology of this important bark beetle species.

Models can be particularly useful for analysing the causalities of disturbance in forest ecosystems, evaluating insect population dynamics or transferring scientific knowledge into practical forest management. The review by Seidl et al. (2011) addresses different modelling concepts and approaches with regard to the abiotic and biotic disturbance agents wind, drought, fire, ungulate browsing and insect pests. Science-based expert models for practical decision support in forestry provide a more generalised picture of causalities, which is gained from existing knowledge, expert experience and case studies. Although geographically limited, empirical studies at a local level can yield essential insights into the causal relationships of disturbance, commonly derived from statistical analyses such as tree-based classification, logistic regression models to predict the likelihood of attack and multiple regression.

Mechanistic models parametrised with experimental and/or literature data are of great value for the investigation of insect–host plant interactions and their potential effects at a population level (e.g. mass outbreaks). An example presented by Seidl et al. (2011) is the scenario analysis regarding possible responses of the European pine sawfly N. sertifer to different concentrations of resin acids in the needles of P. sylvestris. Model scenarios showed that only slight changes in one of these parameters can significantly change the risk of sawfly outbreaks (Larsson et al., 2000). The model output is in accordance with the later empirical observations of Kollberg et al. (2015) that increased resin acid concentrations had negative effects on larval survival and sawfly fecundity, but enhanced larval defence against predators in case of increasing temperatures, as described in section 2.2.

A more comprehensive and advanced modelling concept is to take up simulations of how the defence or physiological status of trees might influence outbreak risks in an ecosystem modelling approach. Jönsson et al. (2012) ‘guessed’ the impact of I. typographus on Norway spruce stands by amplifying a vegetation dynamic modelling framework with a population dynamic and a phenology model. The model combination allowed to jointly predict the availability of stressed host trees, bark beetle migration between patches and I. typographus reproductive success and development. Phenological models simulate insect life cycle events, such as swarming times and development rates, under the consideration of species and instar-specific temperature requirements (Seidl et al., 2011). Several phenology models were established for the spruce bark beetle based on Central and Northern European climate conditions (Jönsson et al., 2009, 2007; Baier et al., 2007; Wermelinger and Seifert, 1998).

In Austria, efforts to simulate I. typographus phenology were initiated in the 1990s by the investigation of its thermal requirements, leading to a model prototype (Führer and Coeln, 1998; Coeln et al., 1996). The parameters relevant for modelling bark beetle phenology, as described by Netherer and Pennerstorfer (2003), include correlations between air and phloem temperatures and thermal values for spring swarming, development of instars and maturation feeding of callow beetles. Development time in days and development rates for terminating egg, larval and pupal stage and for complete pre-imaginal development, respectively, were determined at four different constant temperature regimes in the laboratory. As the next important step towards practical implementation of the phenology model, the experimentally derived thermal values needed to be verified under field conditions. Observed brood development at felled or standing living trees under the fluctuating temperature conditions of the forest environment may differ significantly from the development rates found at constant laboratory temperatures. Moreover, the assumption made by Netherer and Pennerstorfer (2003) of a solely linear relationship between temperature and development time did not hold true under natural conditions. In fact, bark beetle development slows down above the optimal temperature threshold (30.4°C) until an upper developmental temperature threshold (38.9°C), which was considered later in the improved phenology model PHENIPS (Baier et al., 2007).

PHENIPS predicts the potential number of generations per season depending on temperature and photoperiodic limits. Simulations, therefore, consider facultative diapause induction at a certain daylength (Baier et al., 2007) or obligate diapause for predominantly univoltine populations (Annila, 1969; Schebeck et al., 2022). Furthermore, re-emergence of parental beetles from the initially established breeding systems and initiation of sister broods are included in model procedures. Parental beetles commonly leave the breeding systems at the time of advanced larval stage to establish further (sister) broods at less-densely colonised parts of the trunk or at new host trees (Schopf et al., 2019; Anderbrant, 1989).

PHENIPS was repeatedly validated for Central European spruce bark beetle populations (Fleischer et al., 2016; Berec et al., 2013). Moreover, the phenology model was used for investigating the causalities behind extensive tree mortality incited by bark beetle infestation in the forest stands of the High Tatra National Park in Slovakia (Mezei et al., 2017). The outbreaks extended to the timberline in the protected, core areas of the national park (Figure 2) and peaked in the 1990s and again, from 2005 onwards, triggered by a large windthrow event in 2004. The subalpine climate conditions in the area commonly restrict bark beetle development to one generation per year, which raised the question whether attack pressure on Norway spruce stands was enhanced in years warm enough to allow for the development of sister broods. Sister broods can significantly increase the population growth of I. typographus at high elevation sites (Wermelinger and Seifert, 1999) and were shown to produce offspring numbers as high as those of first-generation broods (Netherer et al., 2001).

Figure 2

The timing and completion of filial and sister generations and onset of spring swarming was calculated retrospectively with PHENIPS for each year of the period 1987–2012 for the forest sites of Tatranská Javorina district of the High Tatra National Park (Mezei et al., 2017). Effective seasonal temperature sums (air and bark temperature above the developmental zero of 8.3°C necessary for complete generation development) (Baier et al., 2007; Wermelinger and Seifert, 1998) were included as predictive variables in nonlinear regression models to explain changes in tree mortality. Annual tree mortality was expressed as timber volume of spruce trees killed by bark beetles. Except for 2012, in no year of the study period, the temperature requirements for the termination of a second bark beetle generation were met, which emphasised the predominantly univoltine character of the Tatra beetle population (Netherer and Pennerstorfer, 2003). However, yearly maximum air temperature sums were continuously increasing over the study period and I. typographus outbreaks were repeatedly initiated in years thermally favouring complete sister brood development. In coincidence with wind disturbance, weather conditions allowing for full generation and sister brood development were identified as the most important triggers of bark beetle-induced mortality in the autochthonous mountain Norway spruce area of the High Tatras. Measures of precipitation, such as the amount of rainfall from July to August and year-round snowfall, proved as less significant but still relevant predictors of tree mortality in alternative explanatory models (Mezei et al., 2017).

Rainfall deficit, increased summer temperatures and availability of wind-thrown trees were identified as the main parameters explaining cross-regional temporal fluctuations in the volumes of standing trees killed by I. typographus attack (Marini et al., 2017). This analysis of a pan-European database clearly showed that drought and temperature warming trigger bark beetle infestation even in the absence of storm events, a result that was also found at a regional scale based on data of the Austrian Federal Forests (Netherer et al., 2019). In the analyses, the combined phenology and transpiration deficit model PHENIPS-TDEF, which can provide parallel simulations of potential bark beetle development and tree/forest stand drought stress (Matthews et al., 2018) was used. At the Rosalia Roof study plots (see section 2.4), ensemble hydrological simulations (collective of models) explained up to 80% of daily seasonal variation in empirical hydrological data. These results were regarded sufficiently reliable in predicting periods of drought stress, which potentially coincide with the swarming times of I. typographus, host selection and attack of vigorous trees at times of high population densities and attack pressure. PHENIPS-TDEF in combination with the large forest inventory dataset of the Austrian Federal Forests, comprising site- and stand-related information as well as records of salvaged timber for forest management units located from high montane to lowland areas, served to study the main drivers of recent bark beetle disturbance events in Austria (Netherer et al., 2019). Statistical approaches such as classification trees and binary logistic regression were used to investigate the significance of predisposing stand characteristics (proportion of Norway spruce, stand age, stand density), temperature conditions for bark beetle development and chronic or acute drought episodes for stand susceptibility to I. typographus infestations. As expected, I. typographus infestation was more likely in forest areas with increased stand-related predisposition indices. A lower proportion of infested stands was found at chronically dry soil conditions (shallow, xeric, low-moisture soils according to forest inventory data), corroborating preferential spruce bark beetle attack of well water supplied but acutely stressed Norway spruce. Furthermore, attacks already present in the previous year pointing to high population density and attack pressure, effective thermal sums allowing for at least two bark beetle generations and sister broods and summer/(previous) year transpiration deficits proved as important predictors of bark beetle-induced amounts of salvaged timber in the models (Netherer et al., 2019).

While model outcomes have strongly corroborated the relevance of increased temperature and precipitation deficits for I. typographus mass outbreaks, we are far from fully understanding the causalities of bark beetle infestations and the complex interactions of Norway spruce, bark beetles and their associated micro-organisms such as bacteria and fungi. The review by Netherer et al. (2021) highlights these relationships from the perspectives of drought-stressed host trees, bark beetle host selection, host acceptance and colonisation behaviour, as well as symbiotic fungi.

Heat and drought stress cause the closure of stomata in the needles of Norway spruce, which limits photosynthesis and initiates a cascade of biochemical reactions, involving the synthesis of antioxidants and specialised metabolites for quenching reactive oxygen species and enhancing tree defence (Tausz et al., 2001). On the other hand, the concentrations of secondary metabolites in tree bark, volatile fractions of monoterpenes and other defence compounds, and pheromone components produced in the gut of beetles from specific monoterpenes and de novo serve as gustatory and olfactory signals in host selection and host acceptance by I. typographus (Blomquist et al., 2010). The role of ophiostomatoid fungi, which are commonly associated with bark beetles, has been hypothesised to range from detoxification of defence compounds and production of pheromone components for the attraction of beetles to the defeat of tree defences (Netherer et al., 2021; Netherer and Hammerbacher, 2021). Beetles serve as vectors for fungi into the phloem, but less is known about the benefits provided to bark beetles by the various fungal species (Schopf et al., 2019; Six and Wingfield, 2011). Furthermore, among the multitude of specialised metabolites present in Norway spruce, such as monoterpene hydrocarbons, oxygenated monoterpenes and phenolics, their ecological relevance in the Norway spruce–I. typographus system and impact on ophiostomatoid fungi is understood for only a couple of bark compounds (Netherer et al., 2021). To what extent drought stress affects the concentrations and blends of these substances is in large part still unclear.

More research is, therefore, needed to uncover the impact of stress intensity on tree resistance, the synergisms and tradeoffs among environmental stress factors, and final effects on the performance and outbreak risks of biotic invaders. At the same time, the wealth of knowledge available demonstrates for how long and how intensively this model system has already been studied (Netherer and Hammerbacher, 2021). From dendrochronological and palaeoecological records, we know that spruce bark beetle outbreaks are not at all a new phenomenon but have been recurring on a regular basis since centuries (Kuosmanen et al., 2020). Norway spruce forest ecosystems are, in fact, well adapted to bark beetle infestation and show high regenerative capacity and resilience to disturbance events, as observed after large-scale I. typographus outbreaks in mountain national parks (Winter et al., 2015). However, especially in climate-sensitive montane areas, the short- to medium-term consequences of wind and bark beetle-caused forest dieback involve the loss of forest carbon stocks and shifts from forest carbon sinks to sources (Seidl et al., 2014). The speed of population build-up and increased frequency of mass outbreaks in a warming climate render this bark beetle species one of the most important forest insect pests of European conifer forests.

Among the most intriguing questions are whether pioneer beetles are attracted by susceptible Norway spruce trees and if yes, how beetles recognise and deliberately choose stressed trees with weakened defences (Netherer et al., 2021; Netherer and Hammerbacher, 2021). It is more precisely stated thus: Is drought-stressed Norway spruce more susceptible to spruce bark beetle attack and if yes, due to which physiological and biochemical processes taking place in the host tree? These were the central research questions tackled in the Rosalia Roof Project, a comprehensive rainfall exclusion experiment setup in a mature Norway spruce stand in the Forest Demonstration Centre (Lehrforst) of BOKU. The idea behind this interdisciplinary, in situ study was to jointly investigate soil hydrological and physiological parameters of drought-stressed and non-stressed control trees as well as bark beetle behaviour at these target trees. Main aims of the comprehensive study were to describe the relationships between soil and tree water deficits and the identification of thresholds regarding stress-related tree attractiveness to and defence capability against attacking spruce bark beetles (Figure 3).

Figure 3

The study setup comprised an area of about 1400 m² polyester roofs beneath canopy, 1.20 m above the ground level, to install three different treatments – two fully covered (roofed) and two partially covered plots with an average size of 20 × 20 m, as well as two uncovered control plots (Figure 3). The roof treatment caused strong decreases in the volumetric soil water content and soil water potential, and in the osmotic potential at full saturation of the phloem, pre-dawn twig water potential, sap flow, and resin flow rates of the target trees (Netherer et al., 2015; Matthews et al., 2018) in the course of two study seasons. A distinct period of heat and drought in July of season 2 (2013) significantly stressed target trees of all treatments (Netherer et al., 2015). Roofed trees were most drought stressed and less able to defend attacks by resin flow over the whole season (spring to late summer) in 2013; yet, treatment alone did not fully explain tree individual stress states over time.

To relate drought stress of the study trees to the incidence and success of spruce bark beetle attack, a novel experimental approach, the ‘attack box’ method, was applied (Netherer et al., 2015). Such boxes allow bark beetles to move around freely without being forced to attack the tree. Instead, an attack box offers opportunities for the beetles of staying in the entrance bottle, enter and move around in the main body of the box, crawl on the bark, taste the bark tissue or attack the tree, or leave the box into an exit device. Temperature conditions inside the boxes did not differ significantly from those of the forest environment, as tested by use of dataloggers. However, maximum temperature conditions during the attack experiments positively affected the proportion of beetles leaving the entrance bottles and entering the exit device (Netherer et al., 2015), as well as the number of attack attempts (unpublished data). Most significantly, individual stress states of trees played a role in bark beetle attack success, especially in spring (Netherer et al., 2015; Matthews et al., 2018). While more than 90% of attacks were successful at fully covered trees about 1 year after the establishment of roofs, the well water supplied control trees were able to defend more than 70% of attacks by repelling beetles with resin. This relationship became less clear 2 months later, in the middle of the hot and dry summer 2013, when control trees were similarly stressed and successfully attacked as roofed trees.

The overall proportion of beetles trying to attack the trees indicating host attractiveness was comparably high for all study trees any time in the study season. As concluded by Netherer and Hammerbacher (2021), both vital and stressed Norway spruce trees appear to be highly attractive to I. typographus post landing, but acute stress can lead to an abrupt deterioration of tree defence capability, enhancing bark beetle attack success. The complex and non-monotonic character of this relationship is further corroborated by the observed trend of decreasing attractiveness of trees at severe stress states (Netherer et al., 2015). These results match with earlier findings that I. typographus clearly prefers vigorous trees subjected to sudden, recent stress, while dying or strongly weakened Norway spruce trees are preferentially colonised by more secondary Scolytinae such as the small spruce bark beetle, Polygraphus poligraphus (Führer et al., 1997). Whether I. typographus has to compete with other phloem-feeding beetles in the niche of heavily stressed or recently fallen trees or can successfully mass attack fairly vital trees is a function of the insect's population density and stress states of forest tree populations (Figure 4). From a practical forest management point of view, these findings underline the economic meaning and necessity of monitoring forest drought stress for evaluating the risk of spruce bark beetle outbreaks.

Figure 4

Still, knowledge is lacking about the intrinsic causalities of mass outbreaks on biochemical, chemo-ecological and behavioural, and molecular level of multipartite relationships between Norway spruce, I. typographus and its associated microbial organisms (Netherer et al., 2021). A clear identification of environmental and tree parameters essential for bark beetle host choice requires the study of attraction, host selection and acceptance from landscape to bark tissue level by use of (semi)field and laboratory bioassays. To follow this approach, the preferences of male spruce bark beetles in choosing bark cores sampled from differentially drought-stressed trees of the Rosalia Roof study were tested via Petri-dish arena choice experiments (Morgante, 2021; Netherer et al., 2022). Petri-dish arena approaches can also be used to examine nutritional and detoxification roles of fungal associates in artificial diets enriched with terpenoid or phenolic compounds (Kandasamy et al., 2019; Netherer et al., 2021).

Experimental inoculations of ophiostomatoid (blue-stain) fungi, such as Endoconidiophora polonica and Grosmannia penicillata, associated with I. typographus can help to investigate important mechanisms of tree resistance, such as induced defence reactions and immune response (Krokene, 2015). The growth of ophiostomatoid fungi into tree phloem stimulates hypersensitive wound reaction by the host tree to prevent a further spreading of the microorganisms via the formation of necrotic areas and impregnation of tissues with resinous and phenolic compounds (Schopf et al., 2019; Christiansen et al., 1987). The overall size of wound reaction zones can point to the stress status and defence capability of trees, with mild drought stress hypothesised to increase tree resistance (shorter lesions due to faster limitation of fungal growth) and severe stress hypothesised to render trees more vulnerable to biotic attack (Christiansen and Glosli, 1996). Norway spruce trees at the Rosalia Roof Project I study plots were inoculated with E. polonica in July 2014 and the size of hypersensitive wound reaction zones around the inoculation holes was checked 6 weeks later (Netherer et al., 2016). Mean necrotic and resinous areas tended to be larger at the roofed trees, pointing to slightly reduced capacity of defending the fungus. On the contrary, completely and partially roofed trees responded to fungal inoculations with increased resin flow rates, while the control trees did not (Netherer et al., 2016). Stimulation of tree resistance can help to control further biotic invasion, but might also speed up the exhaustion of tree defences (Lieutier et al., 2009).

The study was repeated at new test trees of the Rosalia Roof Project II in summer 2020 (Morgante, 2021). At that time, wound reaction zones in response to G. penicillata were significantly longer and overall larger at the roofed trees, while this was not the case for the evidently less virulent strain of E. polonica used in the experiments. Interestingly, the size of wound reaction zones was positively correlated with preferences of beetles for bark cores sampled from the trees observed in Petri-dish arena studies (Netherer et al., 2022) and the number of attacks found in attack box experiments (unpublished data). Tree defence capability against fungal attack likely reflects susceptibility to bark beetle attack, both of which depend on the concentrations of terpenoid and phenolic compounds in the bark. The impact of drought stress and fungal inoculations on the content of secondary metabolites in the bark/phloem of Norway spruce is one of the main questions that remain to be elucidated.