Introduction 

The most important processes of forest stand development are growth and disturbance ([43]). Due to the effect of climatic changes, the role of disturbances is becoming more important ([28], [47]). Storms, drought and warm periods, together with temperature breaks in early spring, are very negative factors for Norway spruce forests, in particular allochthonous populations (e.g., [31]). These events will be more frequent according to most of climate change scenarios. The important natural disturbances in spruce stands are wind and beetles. A significant part of European spruce forests is old with frequent disturbances. A change of generation is usually initiated by wind or bark beetles. The process of decline of an old stand may be relatively fast ([18]). Unfortunately, traditional forest monitoring plots (ICP - Forest level I or National Forest Inventories) focus on mature, managed stands in areas with no disturbances. These types of plot are selected according to their position in a net (e.g., 7 x 7 km square net). Only few plots are situated in remnants of semi-natural forests, where the consequences of natural disturbances are not solved by forest management.

The main aim of our research was to understand the mechanisms of I. typographus attack on standing spruce, from habitat and host location to host acceptance ([39]). There are two main hypotheses for host location: random landing ([9]), and primary attraction ([13]). Both methods of host location can be seen as subsequent steps after habitat (stand) selection, a behavior which is likely a balance of a positive input from the host (conifer) kairomone and a negative input from non-host (angiosperm broad-leaves) volatiles, or NHV ([50]). Such “semiochemical diversity” at the habitat level ([49]) may affect both herbivores and predators ([51]). Host acceptance is connected with host recognition, resistance and suitability ([37]), which in turn are connected to tree health ([10]) and ecophysiology ([33]).

Führer et al. ([12]) demonstrated that attacks of I. typographus occur on vigorously growing trees suffering from a sudden stress. This may be explained by a lack of constitutive defense in fast growing trees, combined with a stress-induced failure in the induction of secondary defense mechanisms. In endemic conditions, I. typographus attacks downed trees on sun-exposed slopes with open canopy ([20]). According to Raffa et al. ([37]), the tree-killing bark beetle species display flexible host-selection strategies. When the populations are low, avoiding healthy trees is an adaptive mechanism. Vigorous trees pose a risk to beetles because of their superior defenses. Physiologically compromised trees pose a lower risk, but are sparsely distributed in space, ephemeral in time, and nutritionally suboptimal. In the first stage of the outbreak in mountainous conditions (incipient epidemic population), I. typographus predominantly uses wind-thrown trees, mostly on fresh forest edges (spot initialization), as in endemic conditions. Once populations increase, the discriminating behavior becomes less adaptive, because of the greater likelihood of recruiting enough beetles to overcome healthy trees. Once beetles have successfully killed a tree, because of low tree resistance and/or high beetle population, they may rapidly switch to the closest trees ([2]). Such trees may likely become foci of aggregation and could be killed regardless of their resistance level. Vigorous trees provide a largely vacant resource, and in general are the most suitable for beetles’ nutrition, because of their thick phloem. Beetles are more likely to attack trees adjacent to the already initialized spots ([22]). Sun-exposed slopes or sites are susceptible to I. typographus attack regardless of the gradation phase and stand conditions ([23], [15], [1]). This indicates that questions of sun radiation and shading are important for understanding the mechanisms of I. typographus host selection.

The working hypothesis in the case of standing trees is that the I. typographus pioneer male locates and/or accepts the most susceptible host spruce trees ([32]). The process of attack is initialized by a disturbance, such as wind throw or bark beetle related mortality, which usually results in removal of neighboring trees or their foliage. The remaining trees are suddenly exposed to direct solar radiation. In the case of dense stands with short tree crowns, large parts of the stem will in turn be exposed to the sun, increasing transpiration and water stress. Resistance of a tree to bark beetle would then be diminished. Higher temperatures on the sun-exposed bark would increase emission of bark beetle primary attractants ([6]). The question of host resistance at a different scale is thus important. At the scale of an individual tree, tree physiology ([33]) and secondary chemistry are likely the most important factors addressing host resistance ([46], [52]). At the scale of habitats and landscapes, GIS-based modeling may help in understanding bark beetle damage.

The aim of this paper is to summarize the main results of our previous work on this issue and synthesize the progress of knowledge.

  Ground-level research and study plots 

We developed a semi-temporary monitoring pair plots approach to understand and model processes of bark beetle-caused spruce mortality at the forest stand scale. Generally, the active plots were located in areas with a high probability of bark beetle or wind caused disturbances, because of proximity to wind destroyed or bark beetle attacked areas. The control plots were situated in undisturbed forest stands (< 50 m from the active plots).

Project Tatry (1999-2001)

The project “Integrated risk assessment and new pest management technology in ecosystems affected by forest decline and bark beetle outbreaks (TATRY)” was conducted in natural spruce forests affected by bark beetle in the Tatra Mountains ([40], [15], [16]).

Plot design

An altitudinal transect was established including 5 pairs of monitoring plots, located between 1000 and 1400 m a.s.l. at a 100 m altitude interval. Each pair consisted of one active plot (60 trees) on the stand edge or bark beetle spot, and one control plot (30 trees) within the forest stand. The plots were visited several times a year in order to identify trees that were attacked by bark beetles ([14]). The measured or monitored variables are shown in Tab. 1. In addition, beetle chemoreception of trees and habitat was studied in the field and laboratory ([50]).

Main results

Main results reported here are from Schlyter ([40]). (1) Relatively healthy trees, i.e., recovering after a damage, with high defoliation of the primary crown and high percentage of secondary shoots, were more susceptible to beetle attack than those with a low defoliation of the primary crown and a low percentage of secondary shoots ([36]). (2) Phenolic predictors of tree resistance against fungal attacks were also good predictors for tree resistance against bark beetle attacks in the field ([29]). Three such phenolic predictors (catechin, taxifolin, and resveratrol) were shown to be anti-feedant semiochemicals for bark beetle ([11]), thus affecting host acceptance. (3) A model for bark beetle development in relation to temperature was developed and tested ([34], [35]). (4) For the first time, information about NHV blends was used for forest protection in the field ([23]).

Project Spiš (2003-2006)

The project “Analysis of causes and possible measures against mass die-back of spruce stands in border regions of north Slovakia” was conducted in planted spruce forests affected by chronic decline and bark beetle attacks ([21]).

Plot design

An altitudinal transect was established, including 3 pairs of monitoring plots located between 740 and 1100 m a.s.l. Each pair consisted of one active plot (30 trees) on the stand edge or bark beetle spot in the forest and one control plot (30 trees) within the forest stand. The plots were visited several times a year in order to identify trees that were attacked by bark beetles. The measured or monitored variables are shown in Tab. 1.

Main results

Main reported here are from Jakuš ([25]). Trunk cooling by transpiration flow is an important mechanism of tree protection against overheating. Our results showed differences in the cooling abilities of sun-exposed parts on sunny days. The level of overheating was higher in trees attacked by bark beetles than healthy trees, because higher defoliation leads to slower transpiration flow.

Project Kysuce (2005-2008)

The project was carried out in planted spruce forests affected by chronic decline and bark beetle attacks.

Plot design

Two mini plots were established, each consisting of three spruce trees. In one plot, drought stress was simulated using a shelter to prevent root access to precipitation. The second plot was used as a control. Sap flow, stem circumference and soil water potential were measured. Air temperature, air relative humidity, global radiation, and precipitation were measured in an open area. Bark beetle boring abilities were tested on the monitored trees ([44]). The measured or monitored variables are shown in Tab. 1.

Main results

Only slight differences in sap flow rates between the plots were recorded, suggesting that only small differences in soil water regime can be achieved by sheltering precipitation to the tree roots. As a result, the bark beetle boring responses were also unclear ([44]).

Project Kyrill (2008-2011)

The project “Study and optimization of real efficiency of control measures against Ips typographus in various gradation phases” investigated the role of drought as a main driving factor of bark beetle outbreaks ([48]).

Plot design

Two large-scale research areas were established. A large roof at 2 m above the ground level and isolation of the root system from side ground water inflow controlled the water regime. Different physiological reactions of the drought stressed trees can be induced by decreasing soil water potential. The first research area “Brdy” was located at 650 m a.s.l., with 6 drought-stressed trees and 12 control trees. Tree response to drought was monitored by dendrometers and soil water potential sensors. A manipulation experiment with adult male beetles, testing the willingness of males to enter the phloem and create a nuptial chamber, was performed in 2008 and 2009. There are two critical factors for such experiments: (i) a large number of male beetles in good health and (ii) suitable weather conditions at the time of the experiment. The second research area ”Kostelec’’ was located at 350 m a.s.l. in a Norway spruce monoculture, with two drought-stressed and two control plots (25 m x 25 m). Physiology of four trees was monitored by dendrometers and sampling needles for proline analysis. The “Kostelec” experiment began in 2010.

Main results

Main results reported here are from Zajickova & Matousek ([48]). (1) Trees exposed to enhanced drought did not show any resin flow when conducting the manipulation experiment with male beetles at the beginning of an enhanced drought in 2008. In 2009, the response level of the defense system of the tree was higher, and flow of resin was recorded in each nuptial chamber. We concluded that the level of drought stress affects pest resistance of the tree. (2) During dry periods, drought-stressed trees showed no changes in stem circumference, while they showed the same values of stem diameter change as control trees during rainy periods.

  Remote sensing and GIS based research 

Project Tatry (1999-2001)

Methods

Vegetation change analysis, digital elevation model, and stand characteristics were integrated in the remote sensing part of this study. Time series of LANDSAT images were used in this study ([22]).

Main results

Main results reported here are from Jakuš et al. ([22]). The spatial pattern of the spread of bark beetle outbreaks was related to the phase of the outbreak and insolation (incoming solar radiation). Progression of the attacks arose mainly from initiation of new bark beetle spots. In the culmination and retrogradation phases, outbreaks spread by further expansion from old spots. The spots spread in all directions except south (forest edge oriented to north). We recorded a time-dependence in the decrease of distances between old and new spots. In the first stage of the outbreak, the beetles migrated over fairly long distances. At later stages, the available resources were more limited, thus the beetles were more likely to attack resources adjacent to old spots even though they were less suitable.

Project SLOVABBO (2003-2004)

The results of project Tatry were used for developing a first version of a GIS and remote sensing based early warning system for bark beetle infestations ([27]). The results were used in the TANABBO model (Tatra National Park Bark Beetle Outbreak - the name of the model is different from the project acronym).

Methods and main results

Main results reported here are from Jakuš et al. ([24]) and Kissiyar et al. ([27]). A rating system for assessing the predisposition of forests to bark beetle attack was developed on the basis of known causal relationships between bark beetle outbreak and environmental parameters. A system of sub models was used. Each sub model produced a certain output that was then used in the model. A one-year prognosis of bark beetle attack was based on modeling of the two processes connected with the spread of a bark beetle outbreak: spot initialization and spot spreading ([22]). The actual risk of beetle attack was estimated by means of a bark beetle development model ([34], [7]), i.e., a vegetation health model derived from MODIS satellite images and a drought index based on soil characteristics, precipitation data, and potential evapotranspiration.

  Discussion 

Semi-temporary monitoring pair plots

The approach of semi-temporary monitoring pair plots was used in several studies and was helpful in investigating the mechanisms of I. typographus attack on spruce. The combination of traditional monitoring plots with semi-temporary monitoring pair plots helped to better understand the mechanism of bark beetle related disturbances. Results showed that I. typographus mostly attacks moderately stressed, “resilient” trees sensu Polák et al. ([36]). The whole sequence of mechanisms is still unclear, in particular about host location and attack (habitat location, host location, host acceptance, overcoming of defenses). Interestingly, while no “primary attraction” sensu strictu ([3]) has been proven, the sensory array of I. typographus includes many receptors for host monoterpenes ([5], [4]). The defense at tree and stand scales may be explained by water stress (project Kyrill).

Tree thermal properties and water stress

Hais & Kučera ([17]) showed that surface temperature in a spruce forest is strongly influenced by topography; slope and aspect influence potential radiation and heat load. Higher surface temperatures can be expected at forest edges during clear sky conditions in summer. Part of the I. typographus attack mechanism is connected with the effects of solar radiation and surface temperatures on individual trees (project Spiš) and forest stands ([23], [15], [1]). This is also in agreement with Schopf & Köhler ([41]).

Drought predisposes spruce to bark beetle attack. Questions related to water stress were studied in projects Spis and Kysuce in mountain conditions. We did not obtain clear results due to the variability of the natural conditions. In contrast, project Kyrill provided evidence in support of the role of water stress in predisposing spruce to I. typographus attack.

Thermal sensing is a proxy of insolation and water stress effects on trees. According to Jones & Schofield ([26]), it is primarily used to study plant water relations and specifically stomatal conductance, because a major determinant of leaf temperature is the rate of evaporation or transpiration from the leaf. The cooling effect of transpiration arises because a substantial amount of energy is required to convert liquid water to water vapor.

Tree health and host resistance

The results of project Tatry also showed the importance of parameters related to spruce crown transformation and host resistance, in accordance with Moravec et al. ([32]). Malenovský et al. ([30]) suggested the use of remote sensing for mapping crown transformation. One type of markers of spruce host resistance are phenolic compounds ([8]), which may affect host colonization ([40]) and are active as antifeedant semiochemicals ([11]). According to Soukupová et al. ([42]), it is possible to assess the content of phenolic compounds in spruce needles with the use of remote sensing techniques.

Key variables

Our research suggests that several variables related to I. typographus attack can be measured in ground plots and used for modeling bark beetle disturbances via GIS. The main variables are indicators of water stress (sap flow, stem diameter) and the surface temperature of trees or stands. In addition, crown transformation and phenolic content are also recommended as possible variables to be measured.

Practical applications

The knowledge gained during project Tatry on the anti-attractant and semiochemical diversity effects of NHV ([49], [50]) is now being put into practice for forest protection ([23], [19], [38]). The results from GIS and remote sensing application were used for decision making in NP Tatry ([40], [15]) and NP Sumava ([45]).

  Conclusions 

1. Our observations and experiments confirmed the hypotheses of habitat selection (non-host volatiles and semiochemical diversity) and location of moderately-stressed host trees, although further work about olfactory orientation (to habitat cues and host odor) and host resistance is needed.
2. Reactions of trees to bark beetle attack can be predicted by monitoring several parameters, e.g., air temperature and tree physiology.
3. Data from ground monitoring can be integrated with GIS and remote sensing systems for bark beetle prognosis and management at the habitat and landscape levels.

  Acknowledgements  

We thank C. Schiebe, Alnarp, for comments on an earlier draft. The Slovak participation was supported by the project implementation: Centrum of excellence of biological methods of forest protection (ITMS: 26220120008), supported by the Research & Development Operational Programme funded by the ERDF. Experimental work during the Tatry project was supported by grants from the Swedish Council for Forestry and Agricultural Research (SJFR: #23.0521:96 and #24.0293:98) and an EU-INCO project (CT 98-0151). FS was funded by FORMAS project #230-2005-1778 “Semiochemical diversity and insect dynamics”, the Linnaeus program “Insect chemical ecology, ethology, and evolution (ICE³), and by the Department of Plant Protection Biology, SLU, Alnarp. Joint publication of the COST Action FP0903 Climate Change and Forest Mitigation and Adaptation in a Polluted Environment. Keith Edwards improved the English.

  References