Daniela Hlávková1,2*
Petr Doležal1,2*- 1Institute of Entomology, Biology Centre Czech Academy of Sciences, České Budějovice, Czechia
- 2Faculty of Science, University of South Bohemia, České Budějovice, Czechia
Climatic extremes have been gathering momentum since the 1880s and are believed to be a long-term factor increasing the mortality of Scots pine trees, Pinus sylvestris (L.) in Europe. Weather monitoring over the past 120 years shows that, in Central Europe, surface air temperatures grow at a rate of 0.18°C per decade. Many changes due to these abiotic stressors are already visible in the forests’ canopy and biodiversity. But the influence of the rise in temperature and in precipitation deficiency brings one more player into this die-back scheme. Bark beetles, and their increasing outbreaks, are further agents acting to accelerate and expand the impacts of weather on trees. While P. sylvestris react to abiotic stressors by decreasing functions of the hydraulic system, mainly the defense system, for bark beetles, warming is a profitable condition. Various bionomy processes are modified: vegetation seasons prolong, larval growth and development rates accelerate, reproductive potential rises, and overwintering success increases. Thus, the insect populations grow, and the infestation pressure on weakened hosts intensifies. Finally, even species of small ecologic importance can cause extensive losses of forest cover. Furthermore, international trade and intercontinental transportation support the potential threat of spreading forest pests far away from their original geographic range. Together with climatic amelioration, pests may adapt to new conditions, establish new prosperous populations, disperse rapidly, and cause prodigious losses. However, detailed information about cambioxylophagous pests on P. sylvestris in Central Europe is still missing. The purpose of our review is to map the bionomy and behavior of six bark beetle species—in particular, the sharp-dentated bark beetle, Ips acuminatus (Gyllenhal, 1827), the six-toothed bark beetle, Ips sexdentatus (Börner, 1767), the common pine shoot beetle, Tomicus piniperda (Linnaeus, 1758), the lesser pine shoot beetle, Tomicus minor (Hartig, 1834), the pine shoot beetle, Tomicus destruens (Wollaston, 1865), the Mediterranean pine engraver, Orthotomicus erosus (Wollaston, 1857) (Coleoptera: Curculionidae: Scolytinae), and the steel-blue jewel beetle, Phaenops cyanea (Fabricius, 1775) (Coleoptera: Buprestidae)—on P. sylvestris in Central Europe, to compare and summarize the available data on European populations, and to try to propose ideas and directions for future research.
Introduction
The negative effects of climate change on forests have increased tree mortality and caused a global decline of forest cover worldwide in the last decade (Logan et al., 2003; Raffa et al., 2008; Allen et al., 2010, 2015; Lindner et al., 2010; Das et al., 2013). Overall global temperatures have increased between 1880 and 2012 by an average of 0.85°C (range 0.65–1.06°C). That means the temperature has risen about 0.08°C per decade since 1880 (Lindsey and Dahlman, 2022; Noaa, 2022). However, in the past 40 years, since 1981, respectively, the warming rate has doubled to 0.18°C per decade (Lindsey and Dahlman, 2022; Noaa, 2022). The IPCC (2007) has projected that total global increases to 2100 will be 1.8–4.0°C, while Walsh et al. (2014) suggest that warming for the same period in the US will be 3.0–9.0°C. Such changes may result in a shift in the hydroclimatic regime and extensive climate variability with intensive weather extremes, including a higher risk of flood, drought, fire, and pest breakouts (Schelhaas et al., 2003; Trenberth et al., 2003; Field and Barros, 2014).
The Scots Pine, Pinus sylvestris (L.)
The distribution area of Pinus sylvestris in Europe spans from Portugal to the Northern Arctic Circle, where this tree species covers an approximate area of 28 million hectares (Mátyás et al., 2004; Houston Durrant et al., 2016). In the United States, Scots pines are cultivated specifically for use as Christmas trees (Houston Durrant et al., 2016), or as erosion control elements (Sullivan, 1993). P. sylvestris is forgiving to the site and water supply, as its drought resistance is high (Cech and Perny, 1998; Vertui and Tagliaferro, 1998; Rigling and Cherubini, 1999; Houston Durrant et al., 2016). Nevertheless, since the 1990s a decline in P. sylvestris cover has been observed throughout its range (Martínez-Vilalta and Piñol, 2002; Hódar et al., 2003; Galiano et al., 2010). The dieback is mainly explained as a complex imbalance between trees and secondary pathogens induced by drought and groundwater shortage (Logan et al., 2003; Dobbertin et al., 2007; Wermelinger et al., 2008; Krams et al., 2012). The seriousness of the situation is evidenced by more than 150 million m3 of pine wood harvested in Austria (Cech and Perny, 1998), Italy (Vertui and Tagliaferro, 1998; Vacchiano et al., 2011), Switzerland (Dobbertin et al., 2005; Bigler et al., 2006; Wermelinger et al., 2008), Southern France (Thabeet et al., 2009), Spain (Galiano et al., 2010), and Czechia (Lubojacký et al., 2019).
The Cambioxylophagous Pest Species Spectrum and Their Aggressivity
Weakened trees are most frequently attacked by species from the family Curculionidae, subfamily Scolytinae, and genera Ips and Tomicus (Lieutier et al., 2004). However, other pests from the family Buprestidae (the steelblue jewel beetle, Phaenops cyanea, Fabricius, 1775) and Cerambycidae may also cause significant damage (Wermelinger et al., 2008; Foit and Čermák, 2014).
The aggressivity potential is characterized by developmental rate, voltinism, fecundity, and host tree defoliation status. Species with an aggregation pheromone and whose above-named parameters are high usually have the capability to attack and kill healthy trees, and thus are considered primary pests. Conversely, species utilizing the products of wood decaying processes will most likely be secondary pests, preferring weakened trees (Escherich, 1914; Lieutier et al., 2004, 2009; Wermelinger et al., 2008; Foit and Čermák, 2014). However, climate warming invigorates the bark beetles’ aggressivity, which means that previously harmless or economically unimportant species are becoming more aggressive and causing serious damage to their hosts (Gaylord et al., 2013; Netherer et al., 2015; Pešková et al., 2016).
The Effect of Temperature and Drought on Trees and Insects
Tree decline is a process during which abiotic and biotic factors cause gradual disintegration of forest cover (Manion, 1981; Thomas et al., 2002; Ostry et al., 2011). Basically, three factors operating progressively play a role at different spatio-temporal scales (Manion, 1981). Firstly, long-term abiotic stressors (e.g., extreme droughts and high temperatures) weaken the trees (Manion, 1981; Dobbertin et al., 2007; Anderegg et al., 2015), which causes cavitation, xylem dysfunction, a limitation of some metabolic processes, and reduces the natural defense of trees against pests through resin channels (Sperry and Tyree, 1988; Hanson and Weltzin, 2000; McDowell et al., 2011; Kelsey et al., 2014; Sangüesa-Barreda et al., 2015). Further decline is influenced by short-term abiotic or biotic factors working synergistically (Anderegg et al., 2015; Gea-Izquierdo et al., 2019). Trees suffering from the action of these stressors accumulate and produce volatile substances, mainly ethanol and terpenoids, which in combination with aggregation pheromones, might attract opportunistic insect species and further weaken host trees (Pitman et al., 1975; Schroeder and Lindelöw, 1989; Gallego et al., 2008; Miller and Rabaglia, 2009; Lingren et al., 2012; Kolb et al., 2016). The third and final contributor to tree mortality is generally some biotic factor (Oliva et al., 2013; Gea-Izquierdo et al., 2019).
Drought also contributes substantially to the link between host and pest. In principle, drought stress actively modulates tree physiology on basic chemical levels. Alterations in trees’ metabolic pathways may take different forms (e.g., regulation of carbon fixation and storage, fatty acid biosynthesis, level and overall composition of secondary metabolites) (Farquhar et al., 1982; Ferrio et al., 2003; Flexas et al., 2007; Moreira et al., 2009; Sampedro et al., 2011; Moreno-Gutiérrez et al., 2012; Fox et al., 2018; López-Goldar et al., 2018; Suárez-Vidal et al., 2019). In addition, alterations might be induced by trees to fight the drought (Carmona et al., 2011; Suárez-Vidal et al., 2019): for example, changes in nutrient content, lignification, thickening of resin canal density, cavitation, hydraulic conductivity (narrowing tracheids or creating pits), or decreases in water content (Gaylord et al., 2013; Hereş et al., 2014; Camarero et al., 2015; Anderegg and HilleRisLambers, 2016; Suárez-Vidal et al., 2019). The water deficit reduces tree plasticity and their ability to respond to pest attacks (Suárez-Vidal et al., 2019). Therefore, host survival is highly dependent on the intensity and duration of the stresses occurring together (Ramegowda and Senthil-Kumar, 2015), as well as species-specific resistance ability (Arango-Velez et al., 2016; Lusebrink et al., 2016).
Insects further profit from climate change as growing season temperatures largely affect all of their life processes, including metabolism and reproduction, developmental rate, mortality of progeny, and voltinism. Temperature also synchronizes spring emergence, and thus the mass attack, which contributes to successful infestation of host trees (Régnière and Bentz, 2007; Powell and Bentz, 2009; Bentz et al., 2010; Weed et al., 2013). The Mediterranean and North-Eastern Europe are considered primary hot spots, where global warming will advance the positive feedback response to pest populations’ behavior (Giorgi, 2006). Moreover, the combination of beneficial conditions with an ample supply of susceptible, and nutritionally optimal food sources often helps to shift the aggressivity of bark beetle species from the endemic to epidemic threshold (Raffa et al., 2008; Gaylord et al., 2013). Based on future climate predictions, an increase in the extent, severity, and frequency of insect outbreaks, as well as the magnitude of tree mortality events, is expected (Allen et al., 2010). Pest range has usually been defined as either “primary-secondary” or “epidemic-endemic,” in connection to aggressivity and ability to multiply (Furniss and Carolin, 1977; Manion, 1981). This type of characterization includes the effect of drought stress only peripherally. A more suitable range definition seems to be the “stress compounders-stress confounders” spectrum (Trugman et al., 2021). This scope better characterizes the interactions between species and biotic agents, as it is based on a wider range of factors (i.e., drought stress, stress physiology, pest activity, and preferences) contributing to tree mortality. While most of the reviewed species act as stress compounders and kill the most stressed trees, Dendroctonus spp. bark beetles act as stress confounders that attack the largest hosts regardless of their physiological conditions (Trugman et al., 2021).
Climate changes may also shift the distribution areas of numerous insect species (Parmesan et al., 2011). Shifting of an area’s characteristic temperature limits and the beetles’ prompt reaction to the climatic amelioration might facilitate their migration to new ecosystems, higher latitudes, and higher elevations (MacLean, 1983; Ayres and Scriber, 1994; Ayres and Lombardero, 2000; Thuiller et al., 2008; Netherer and Schopf, 2010; Parmesan et al., 2011; Buotte et al., 2017; Lantschner et al., 2017).
Studies that have delt with bark beetles in relation to P. sylvestris predominantly include topics like voltinism (e.g., Vité et al., 1974; Hernández Hernández et al., 2004; Pérez and Sierra, 2006; Sarıkaya, 2008; Özcan, 2011; Colombari et al., 2012), development (e.g., Jactel and Lieutier, 1987; Özcan, 2011; Péter, 2014), diapause and cold hardiness (e.g., Bakke, 1968; Gehrken, 1984, 1985, 1989, 1995; Hernández Hernández et al., 2004; Pérez and Sierra, 2006; Colombari et al., 2012), and olfactory communication (e.g., Bakke, 1978; Byers et al., 1985; Lanne et al., 1987; Kohnle, 2004; Romón et al., 2017). Novel methods of forest protection and pest management have been rarely tested (e.g., Colombari et al., 2012, 2013; Faccoli et al., 2012; Chinellato et al., 2014). Unfortunately, our current knowledge of the behavior, migration pathways, and pest status of many species is gradually changing due to global climate changes. Therefore, the aim of this review is to provide an overview of the available information on the most harmful pests of Scots pines with regard to differences between their populations, and to point out the gaps in our knowledge of their bionomy. The above-named species with considerable ecological and economical influence, include the sharp-dentated bark beetle Ips acuminatus (Gyllenhal, 1827), the six-toothed bark beetle, Ips sexdentatus (Börner, 1767), the common pine shoot beetle, Tomicus piniperda (Linnaeus, 1758), the lesser pine shoot beetle, Tomicus minor (Hartig, 1834), the pine shoot beetle, Tomicus destruens (Wollaston, 1865), and the steel-blue jewel beetle, Phaenops cyanea (Fabricius, 1775).
Cambioxylophagous Pests
This group unites pests that can be characterized by feeding on the inner bark, destroying the cambial tissues, or even boring deeply into the sap- and heartwood (Bouget et al., 2005; Sallé et al., 2014). Typical representatives belong in the families Curculionidae (Scolytinae), Buprestidae, and Cerambycidae (Bouget et al., 2005; Sallé et al., 2014).
The Sharp-Dentated Bark Beetle, Ips acuminatus (Gyllenhal, 1827)
According to the BAWBILT (Bark and Wood Boring Insects in Living Trees in Europe) database, I. acuminatus is one of the most aggressive species in Europe, as the damage caused by its outbreaks between 1990–2000 reached almost 13 million m3 of wood (Grégoire and Evans, 2004; Gilbert and Sauvard, 2007; Foit and Čermák, 2014). Beetles develop in the thin bark of the crown or branches of P. sylvestris and other pine species, and transfer blue stain fungi from the genus Opisthostoma, causing growth disorders, crown thinning, and ultimately, death of the host tree (Mathiesen, 1950; Lieutier et al., 1991; Villari, 2012). Consequently, an enormous decline of P. sylvestris monocultures has been recorded throughout Europe (Bakke, 1968; Lieutier et al., 1991; Villari, 2012; Siitonen, 2014).
Distribution. This species extends from Northern Spain through the Fenno-Scandinavian region, from Siberia to China, and through the Korean peninsula to Japan (Wood and Bright, 1992; Bright and Skidmore, 2002; Siitonen, 2014). However, reproductive success is affected by low temperatures, limiting the distribution area (Bakke, 1968). Destructive outbreaks of this species have recently been reported from Slovakia, Germany, Switzerland, Romania, Spain, the Italian and Swiss Alps, Finland, and Czechia (Švestka and Wiesner, 1997; Grégoire and Evans, 2004; Wermelinger et al., 2008; Colombari et al., 2013; Siitonen, 2014). Since this species is well-adapted to cold conditions, the rise in temperature thresholds might enable this beetle to spread northerly. Additionally, survival ability will increase, supporting the growth of hot spots, which will cause extensive damage.
Life Cycle and Reproduction. Ips acuminatus emerges in temperatures above 14°C (Bakke, 1968; Colombari et al., 2012), and the optimum temperature for spring swarming is 18°C (Bakke, 1968; Lekander et al., 1977; Hernández Hernández et al., 2007). Males colonize the upper parts of trunks and branches with thin, smooth bark and phloem thickness about 2-3 mm (Bakke, 1968). After creating a frass-free nuptial chamber, about 0.25 cm2 in size, males produce aggregation pheromone to attract both sexes to the tree (Bakke, 1968). Polygynous males usually mate with 1–7 females, but it can be up to 12 females (Bakke, 1968; Kirkendall, 1990; Løyning and Kirkendall, 1996; Colombari et al., 2012). Unmated females, 10–20% of the population, colonize uninfested trees where they bore maternal galleries. Mated females bore maternal galleries radially from the nuptial chamber and parallel to the trunk (Kirkendall, 1990). Males protect the entrance hole against other males until mid-June (Bakke, 1968). The length of maternal galleries is significantly correlated with population density and reaches 1–11 cm (Colombari et al., 2012). First, eggs are laid at a distance shorter than 1 cm, alternating on either side of the maternal gallery. On average, each female deposits 4-16 eggs (Colombari et al., 2012). Newly hatched larvae bore larval galleries perpendicular to the maternal ones. Colombari et al. (2012) recorded low survival of sub-imaginal stages, and only around 41% of larvae, 21% of pupae, and 65% of young progeny finished the development to adulthood. However, up to 94% of the progeny successfully completed development in Norway (Kirkendall, 1989).
Two types of female genotypes were recorded in the I. acuminatus–sexually mating diploids and pseudogamous triploids. Pseudogamous females reproduce parthenogenetically, but they require mating with males as an initial trigger for embryogenesis. Thus, males’ genetic information isn’t transmitted to the genome of their offspring, and they produce exclusively female progeny. Since triploid offspring have up to 47.3% higher survival than the offspring of sexual mating, pseudogamous females may contribute considerably to the population density in newly colonized areas (Løyning, 2000).
Voltinism. While the Scandinavian populations of I. acuminatus are univoltine (Bakke, 1968), the Central and Southern European ones are bivoltine (Hernández Hernández et al., 2004; Colombari et al., 2012). Although Kirkendall (1990) experiments showed that 23–56% of galleries are nuptial chamber- and male-free, some authors believe that females do not re-emerge to establish sister broods (Pérez and Sierra, 2006). In multivoltine populations, reproductive development continues until the shortening of daylength in late summer induces facultative diapause (Gehrken, 1985).
Diapause and Overwintering. Once the photoperiodic signal is perceived at the edge of the vegetation season, adults start to prepare for overwintering. Flight activity decreases, metabolism slows down, reproduction and ovarian development is ceased, and beetles actively search for a suitable overwintering microhabitat (Gehrken, 1985). The majority of beetles overwinter under the bark of standing trees. Univoltine populations stay in the substrate where they developed; whereas individuals from multivoltine populations may change hosts and infest new trees in the surroundings. However, callow beetles cannot reproduce at the end of the season, as their mating organs are immature (Gehrken, 1985). Overwintering in soil litter under infested trees or in fallen branches has been reported in some Central and Southern European populations (Bakke, 1968; Gehrken, 1985; Hernández Hernández et al., 2004; Pérez and Sierra, 2006; Colombari et al., 2012).
During autumn, facultative diapause intensifies, and ovary development is suspended at the level of germ cells in germarium (Doležal and Sehnal, 2007). In December, previtellogenesis and ovary development is restored. Later, during January, metabolism increases, and diapause is terminated. Post-diapause quiescence gradually terminates with rising spring temperatures and lasts until the end of April (Gehrken, 1985).
Diapause development is tightly connected with mechanisms that increase cold hardiness. Starting in autumn, I. acuminatus accumulates energetic reserves and cryoprotectants, decreases water content, and empties the guts. Increased amounts of trehalose, and cryoprotective compounds such as ethylene glycol, mannitol, sorbitol, dulcitol, and anti-freeze proteins are synthesized to protect body tissues from ice crystal formation causing lethal injuries (Gehrken, 1984, 1985, 1989, 1992, 1995). Moreover, a sophisticated exoskeleton structure with pores of only about 6.19*10–22 mm in diameter, shields the body from ice crystals penetrating through the body surface (Gehrken, 1992). All these adaptations lower the risk of freezing and increase the chance of successful overwintering. Studies of the supercooling point (SCP—the temperature when body liquids freeze) in I. acuminatus report very low temperatures of −35°C (Gehrken, 1984, 1985, 1995).
The Six-Toothed Bark Beetle, Ips sexdentatus (Börner, 1767)
Ips sexdentatus is an example of a secondary pest that prefers weakened or disturbed pines, even though occurrences of local outbreaks after abiotic disturbances followed by spread to healthy stands have recently increased (Etxebeste et al., 2013).
Their preferred hosts are various species of pines (Pinus spp.) as well as spruces (Picea spp.) in Asia. Some authors have also reported attacks of firs (Abies spp.) and larches (Larix spp.) (Chararas, 1962). In Turkey and Georgia, I. sexdentatus causes extensive dieback of the Caucasian spruce [Picea orientalis (L.)] (Schimitschek, 1944; Lozovoj, 1966; Özcan, 2011).
Distribution. The distribution area of this Eurasian species spans from Portugal through Central and Northern Europe, from the Balkans to Turkey, Russia, China, South-Eastern Asia, and Japan (Jonášová and Prach, 2004; Knížek et al., 2020). Rising temperatures in Europe facilitate the occurrence of natural disturbance and create suitable living conditions for I. sexdentatus, which might lead to an increase in the generation number or extra sister broods.
Life Cycle and Reproduction. Spring swarming starts in late April or early May when temperatures reach 20°C (Özcan, 2011, 2017). Males of I. sexdentatus colonize weakened trees and prefer sections where bark thickness reaches 5–15 mm (Bouhot et al., 1987; Markalas, 1997). Males create a nuptial chamber and produce an aggregational pheromone (ipsdienol) to attract 1–5 females to copulate with (Vité et al., 1974; Francke et al., 1986; Kohnle et al., 1992; Etxebeste and Pajares, 2011). Maternal galleries are oriented parallel to the trunk axis, and their length can reach up to 1 m. Each female deposits ∼40 eggs on both sides of the maternal gallery at a density of around 2 eggs/cm (Jactel and Lieutier, 1987). Infestation density is negatively correlated with the length of maternal galleries (Jactel and Lieutier, 1987). After hatching, larvae feed on the phloem and build galleries perpendicular to the maternal gallery. The sex ratio of offspring is 1:1, and more than 80% of females re-emerge to establish sister broods (Jactel and Lieutier, 1987).
Voltinism. Voltinism of I. sexdentatus is largely temperature dependent (Vité et al., 1974; Sarıkaya, 2008; Özcan, 2011). While populations in Northern Europe are univoltine, Central European populations are bivoltine and in the areas with hot, long summers (e.g., the Mediterranean), 4–6 generations may occur (Chararas, 1962; Vallet, 1981; Sierra and Martín, 2005; Péter, 2014).
Overwintering. Adults of I. sexdentatus overwinter under the bark of standing or fallen trees (Chararas, 1962; Lévieux et al., 1985). Their limits for successful winter survival are relatively high, as the average SCP in adults is −19°C. Sub-adult stages rarely overwinter and suffer higher mortality. The SCP of larvae was −9°C, and the only stage reported to finish development the next spring were pupae (Chararas, 1962; Bakke, 1968; Lévieux et al., 1985).
The Common Pine Shoot Beetle, Tomicus piniperda (Linnaeus, 1758)
Tomicus piniperda is a secondary pest of standing weakened pine trees and a primary pest of annual young shoots, causing substantial disturbance to the photosynthetic apparatus (Långström and Hellqvist, 1991; Långström et al., 2001; Foit and Čermák, 2014). Extensive feeding during outbreaks can lead to disruption or complete cessation of growth, and rarely, even to the host’s death (Långström and Hellqvist, 1991; Långström et al., 2001). Regeneration after defoliation is a long-lasting process accompanied by higher sensitivity to other pathogens (Långström et al., 1990).
Tomicus piniperda prefers the lower parts of trunks, with thicker bark and phloem, of trees stressed by drought or fungal infections (Annila et al., 1999; Långström et al., 2001; Sikström et al., 2011). Its main host tree is P. sylvestris. Their occurrence has also been recorded on other pine species, such as black pine [Pinus nigra (J. F. Arnold)], maritime pine [Pinus pinaster (Aiton)], white pine [Pinus strobus (L.)], red pine [Pinus resinosa (Aiton)], and Jack pine [Pinus banksiana (Lamb.)], as well as Douglas firs [Pseudotsuga menziesii (Mirb.) Franco], spruces (Picea spp.), and larches (Larix spp.) (Browne, 1968; Bright and Skidmore, 1997; Siegert and McCullough, 2001).
Distribution. The distribution range of T. piniperda reaches from Portugal through Europe to Asia and Japan. Its northern border copies the range of P. sylvestris, and in the south, it spans to north Africa (Browne, 1968; Lekander et al., 1977). Climate change not only allowed for continental population mixing and re-colonizations during the postglacial age, resulting in high genetic divergence among European populations, but also allowed for intercontinental moves. The increasing abundance of common shoot pine beetle has been closely monitored in North America, where this species was introduced in the 1990s and became an invasive pest (Czokajlo et al., 1997; Annila et al., 1999; Borkowski, 2001; Öhrn et al., 2018). Moreover, their high adaptability to regional conditions alters the populations’ bionomy (Horn et al., 2009). Based on this information, prediction models of potentially endangered areas have been made (Horn et al., 2012). The enormous versatility and life cycle divergence of this species has strongly influenced opinions on their relationship with Tomicus destruens (Carle, 1973; Gallego and Galián, 2001). The invasive potential of T. piniperda is augmented by its enormous spreading potential and adaptability to new conditions. In future, therefore, this species could become a serious pest worldwide.
Life Cycle and Reproduction. This monogamous bark beetle emerges from overwintering habitats, in thick bark near the base of the trunk, in early spring (Eidmann, 1965, 1974; Bakke, 1968). Adults are active when temperatures exceed 5°C and first flights have been recorded at 10–12°C during early March and April (Långström, 1983). Females initiate the attack and males follow them later (Saarenmaa, 1983). Fertilized females bore maternal galleries about 4–10 cm long (Saarenmaa, 1983) and lay up to 70 eggs on both sides (Šrot, 1968; Schroeder, 1999). Fecundity is positively correlated with female body weight and negatively correlated with infestation density (Schroeder and Weslien, 1994; Schroeder, 1997; Hui and Xue-Song, 1999; Amezaga and Garbisu, 2001). During oviposition, males clean the frass from the galleries (Šrot, 1968), then both sexes emerge and undergo maturation feeding to replenish their energetic reserves (Šrot, 1968). Larval development is temperature dependent (Yvon and Wegensteiner, 2015) and pupation occurs within 7–10 weeks (Šrot, 1968). Young adults emerge from June to mid-July in Sweden (Långström et al., 2002), and from July to August (Knížek, 1998) in Central Europe; they follow parental beetles into the tree crowns to infest 1–3-year-old pine shoots (Långström, 1983; Långström et al., 2002). Feeding starts near the branches whorl and continues apically for a few millimeters up to 7 cm. One tunnel may be occupied by 2–3 individuals (Haack et al., 2001). During outbreaks, intensive regeneration feeding may cause 80–98% defoliation of the crown (Haack et al., 2001).
Voltinism. Tomicus piniperda has so far been considered a univoltine species with hibernation before establishment of a new generation. However, emergence and sister brood occurrence, indicate possible continuous reproduction (Ryall and Smith, 2000) and the potential to become multivoltine (Poland and Haack, 2000).
Overwintering. In Northern Europe, the shoot feeding period is terminated by sub-zero temperatures, usually in the second half of October, when adults migrate to the base of the trunk and bore into the thick bark located 25 cm below the soil litter (Petrice et al., 2002). In China and Southern Europe, populations may overwinter under the bark at higher sections of the trunk or even in shoots on the ground (Masutti, 1969; Långström et al., 2002).
The Pine Shoot Beetle, Tomicus destruens (Wollaston, 1865)
The taxonomic relationship of T. piniperda and T. destruens has long been unclear. In the beginning, these species were considered only diverse ecotypes (Carle, 1973; Schwerdtfeger, 1981; Faccoli et al., 2005b), but gradually doubts about the group’s uniformity have arisen (Lekander, 1971; Wood and Bright, 1992; Pfeffer, 1995). Genetic analyses have revealed divergences typical for distant relatives (Gallego and Galián, 2001; Kerdelhué et al., 2002; Kohlmayr et al., 2002; Faccoli et al., 2005a,b). Subsequently, a sympatric relationship was supported by morphological studies (Faccoli, 2006) and the ecological and climatic requirements based on distribution area (Vasconcelos et al., 2003; Faccoli et al., 2005b).
Tomicus destruens is considered a serious pest of 1-year old pine shoots. The typical hosts are pine species of coastal areas: for example, maritime pine (P. pinaster), stone pine [Pinus pinea (L.)], and Aleppo pine [Pinus halapensis (Mill.)] (Vasconcelos et al., 2003; Faccoli et al., 2005b; Chakali, 2007; Pernek et al., 2012). Infestations have also been recorded on Turkish pine [Pinus brutia (Ten.)], Canary Island pine [Pinus canariensis (C. Smith)], and black pine (Pinus nigra) (Kerdelhué et al., 2002; Gallego et al., 2004, 2008; Faccoli, 2007; Sarıkaya and Avci, 2010). Like T. piniperda, T. destruens colonizes the thick bark in lower sections of the trunk (Chakali, 2007). Its outbreaks frequently turn up in the healthy trees surrounding fire disturbed forests (Branco et al., 2010).
Distribution. Their distribution area includes Macaronesia, the Southern coast of Portugal, Spain, France, the Italian peninsula and Sardinia, Dalmatia, Turkey, Cyprus, and Northern Africa (Chararas, 1962; Lekander, 1971; Mendel et al., 1985; Chakali, 1992, 2007, 2008; Monleón et al., 1996; Ben Jamaa et al., 2000; Kohlmayr et al., 2002; Vasconcelos et al., 2003, 2005; Ciesla, 2004; Gallego et al., 2004; Faccoli et al., 2005b; Horn et al., 2006, 2012; Sarıkaya and Avci, 2010; Pernek et al., 2012; Lentini et al., 2015). Tomicus destruens is a Mediterranean species distributed in lowlands with an elevation maximum of approximately 1,000 m and with a dry, warm climate (Gallego et al., 2004). If the minimum temperature thresholds rise, this bark beetle will be able to spread north of its territory. High adaptability and the ability to develop in P. nigra, which covers the Mediterranean area, could mean immense damage resulting from this species in southern Europe.
Life Cycle. Tomicus destruens adults are active at temperatures around 5°C. The timing of flight activity differs by location and elevation (Sarıkaya and Avci, 2010). Generally, there are two phases, the stronger one, which occurs in October and November, is followed by a second one from mid-November to January (Sabbatini Peverrieri et al., 2008). In Italy, flight starts at 12°C (Faccoli et al., 2005a; Chakali, 2007, 2008; Sabbatini Peverrieri et al., 2008; Lentini et al., 2015), in Sardinia at 14°C (Lentini et al., 2015), and in Algiers, Tunisia and Israel at 6–8°C (Mendel et al., 1985; Ben Jamaa et al., 2000; Chakali, 2008).
Fertilized females bore 3-15 cm long maternal galleries vertically toward the tree crown (Faccoli, 2007, 2009; Chakali, 2008; Gallego et al., 2008; Sarıkaya and Avci, 2010) and oviposit 80–95 eggs on both sides. Every egg chamber is clogged with frass (Chakali, 2008; Lentini et al., 2015). Maternal gallery length, female fertility, and egg hatchability are negatively correlated with attack density (Faccoli, 2007; Sarıkaya and Avci, 2010; Lentini et al., 2015). Larval development is temperature dependent and lasts 50–200 days. Low temperatures substantially increase sub-imaginal mortality (Faccoli et al., 2005a; Horn et al., 2006; Sabbatini Peverrieri et al., 2008; Lentini et al., 2015).
Young adults emerge from the end of May until June (Sabbatini Peverrieri et al., 2008; Pernek et al., 2012) and undergo maturation feeding on young shoots (Chakali, 2007, 2008; Sabbatini Peverrieri et al., 2008; Sarıkaya and Avci, 2010; Lentini et al., 2015). Adults tend to select the same host tree species in which they developed (Tiberi et al., 2009).
Voltinism. Tomicus destruens populations are univoltine or bivoltine (Masutti, 1969; Dajoz, 1980; Mendel et al., 1985; Monleón et al., 1996; Sarıkaya and Avci, 2010; Horn et al., 2012; Lentini et al., 2015). Females continuously replenish energetic reserves, so that they do not need to undergo another cycle of regeneration feeding (Fernández Fernández et al., 1999b; Lentini et al., 2015) and can re-emerge and continue laying eggs up to four times (Lentini et al., 2015).
Overwintering. Tomicus destruens has summer dormancy in all developmental stages including eggs (Nanni and Tiberi, 1997; Pernek et al., 2012). Adults undergo dormancy inside the shoots, where regeneration feeding takes place, or in maternal galleries under the bark of infested trees (Russo, 1940; Masutti, 1969; Triggiani, 1984; Santini and Prestininzi, 1991; Monleón et al., 1996; Nanni and Tiberi, 1997), just like the juvenile stages (Triggiani, 1984; Santini and Prestininzi, 1991; Monleón et al., 1996; Faccoli et al., 2005a).
The Lesser Pine Shoot Beetle, Tomicus minor (Hartig, 1824)
The Tomicus minor beetle is a pest of several pine species (Pinus spp.): most commonly P. sylvestris in Europe, and Yunnan pine [Pinus yunnanensis (Franchet)] in China. These beetles generally prefer weakened hosts (Annila et al., 1999; Fernández Fernández et al., 1999a), but some authors consider this species a secondary aggressive, able to colonize and kill even healthy trees (Fernández Fernández et al., 1999a; Foit and Čermák, 2014).
Distribution. Except for North America, the distribution area of T. minor is similar to that of T. piniperda (Lungren, 2004), i.e., from Portugal through Europe, and copying the North African coast to Asia and Japan (Browne, 1968; Lekander et al., 1977). As its bionomy is not monitored in much detail, it is difficult to predict its future distribution. Due to climate change, a move toward northern territories might be expected. Furthermore, optimal conditions might support an increase in aggressivity, which would probably cause a greater occurrence of hot spots and a larger amount of damage.
Life Cycle. Overwintered T. minor adults first fly at temperatures of about 10°C, and flight peaks at temperatures of about 12°C (Långström, 1983), i.e., March to April in Central Europe and April to May in Scandinavia (Långström, 1983).
Females infest the trees and males follow them. European populations prefer trees with smooth bark or shaded, windthrown, and wind-broken trees (Långström, 1984), while populations in China prefer the thick bark near the trunk base (Ye and Ding, 1999). Fertile females bore “V” shaped maternal galleries transversely with the trunk axis. Usually, galleries are two-armed, with a mating chamber in the middle; however, 10% of the galleries are one-armed (Fernández Fernández et al., 1999a). Females oviposit alternately in both arms (Långström, 1983). Males keep the galleries frass free (Fernández Fernández et al., 1999a) and secure the entrance hole against predators and other males (Långström, 1983). Shortly before the end of ovipositing, males emerge and migrate into the tree crown for regeneration feeding (Långström, 1983), or search for other females to mate with (Fernández Fernández et al., 1999a). In reaction to repeated mating, females extend maternal galleries by about 7 cm and oviposit again. The overall gallery length may reach up to 20 cm and is negatively correlated with attack density. One female oviposits approximately 100 eggs (Fernández Fernández et al., 1999a). Their hatchability is low, with only 26% of progeny reaching maturity (Långström, 1983). Larvae feed on phloem, but low nutrition quality drives feeding into the wooden part, where the fungi inoculated by parental beetles are consumed (Francke-Grosmann, 1951; Fernández Fernández et al., 1999a). Total development lasts about 105 days in Northern Europe (Långström, 1983), 135 days in Southern Europe, and 125 days in China (Lieutier et al., 2015). Re-emergence and sister brood establishment has been observed in Swedish, Spanish and Chinese populations (Långström, 1983; Fernández Fernández et al., 1999a; Långström et al., 2002).
Regeneration Feeding and Overwintering. Regeneration feeding takes place during summer months in the lower part of the tree crown, where beetles feed on 3–4 mm thick young shoots (Långström, 1983). It continues until low autumn temperatures and shortening daylength induces hibernation. The Southern European and Chinese populations hibernate in mined shoots in tree crowns. Conversely, Scandinavian populations migrate to the soil litter and cracks in bark close to the trunk base (Långström, 1983; Fernández Fernández et al., 1999b).
Mediterranean Pine Engraver, Orthotomicus erosus (Wollaston, 1857)
Orthotomicus erosus is considered a secondary pest of recently fallen, windthrown, or fire-injured trees (Mendel and Halperin, 1982; Mendel, 1983; Arias et al., 2005; Lieutier and Paine, 2016; Sarıkaya and Şen, 2017). Although extensive damage to Turkish pine (P. brutia) and Aleppo pine (P. halapensis) has been reported in its natural distribution area of Israel and Iran (Mendel, 1983), these beetles can feed and reproduce in a broad range of coniferous species found in Mediterranean and Aegean coastal regions. The dominant hosts belong to pines and damage has been reported on Turkish pine (P. brutia), Caribbean pine [Pinus caribaea (Morelet)], Canary Island pine (P. canariensis), shortleaf pine [Pinus echinata (Mill.)], Afghan pine [Pinus elderica (Medw)], Aleppo pine (P. halapensis), black pine (P. nigra), stone pine (P. pinea), maritime pine (P. pinaster), Monterey pine [Pinus radiata (D. Don)], red pine (P. resinosa), and Scots pine (P. sylvestris) (Atkinson, 1921; Chararas, 1964; Carle, 1973; Mendel and Halperin, 1982; Walter et al., 2009; Sarıkaya et al., 2013). Less suitable hosts, in which development or maturation feeding has been recorded, include white spruce [Picea glauca ([Moench.] Voss)], Caucasian spruce (P. orientalis), balsam fir [Abies balsamea ([L.] Mill.)], Nordmann fir [Abies nordmanniana (Steven)], Spanish fir [Abies pinsapo (Boiss)], eastern hemlock [Tsuga canadensis ([L.] Carrière)], tamarack [Larix laricina ([Du Roi] K. Koch)], Mediterranean cypress [Cupressus sempervirens (L.)], Arizona cypress [Cupressus arizonica (Greene)], Lebanese cedar [Cedrus libani (A.Rich.)], and Douglas fir (Pseudotsuga menziesii) (Mendel and Halperin, 1982; Gil Sanchéz and Pajares Alonso, 1986; Wood and Bright, 1992; Arias et al., 2005; Walter et al., 2009; Sarıkaya et al., 2013; Pernek et al., 2019). The wide host range of this species and its high mobility (Sarıkaya and Şen, 2017), together with the invasions promoted by international timber transportation (Brockerhoff et al., 2006a; Haack, 2006), have resulted in this species’ recent massive spread into new environments (Sarıkaya et al., 2013; Pernek et al., 2019).
Orthotomicus erosus prefers medium stem parts with thicker bark (diameter up to 90 cm) and main branches (diameter above 5 cm) (Mendel and Halperin, 1982; Seybold and Downing, 2007; Pernek et al., 2019), and often occurs together with I. sexdentatus (Paiva et al., 1988), Hylastes angustatus (Herbst, 1793), Hylurgus ligniperda (Fabricius, 1787), Pissodes nemorensis (Germar, 1824) (Tribe, 1990), Pityogenes calcaratus (Eichhoff, 1878), and T. destruens (Mendel and Halperin, 1982).
Distribution. The native range of O. erosus spans from the Middle East to the Mediterranean countries, Southern and Central Europe, England, Northern Africa, Caucasus and Crimea, as well as to China and Central Asia (Atkinson, 1921; Schimitschek, 1944; Balachowsky, 1949; Chararas, 1964; Lozovoj, 1965; Chararas and M’Sadda, 1970; Carle, 1973; Chararas et al., 1978; Anon, 1981; Mendel and Halperin, 1982; Mendel, 1983, 1988a,b; Yin et al., 1984; Mendel et al., 1986; Wood and Bright, 1992; Paiva, 1994; Pfeffer, 1995; Eglitis, 2000; Lieutier et al., 2002; Haack, 2004, 2006; Henin and Pavia, 2004; Arias et al., 2005; Lee et al., 2005; Brockerhoff et al., 2006a; Ben Jamaa et al., 2007; Seybold and Downing, 2007; Sarıkaya and Avci, 2010; Amini et al., 2013; Gómez and Martínez, 2013). Nonetheless, due to international trade, O. erosus has invaded North and South America (Haack, 2004; Ruiz and Lanfranco, 2008), South Africa, and Fiji (Wood and Bright, 1992; Eglitis, 2000).
Orthotomicus erosus reacts rapidly to changing local temperatures, and within months can switch from endemic to epidemic status in a locality. After an outbreak, the vast range of possible hosts simplifies its spread into near or far surroundings. Taken together, it is possible to assume that the shift in low-temperature limits might enable O. erosus to continue conquering the European continent. On top of that, O. erosus seems to be a perfect candidate for introduction by cargo trade into new niches worldwide.
Life Cycle and Reproduction. The first individuals emerge when temperatures exceed 7–9°C (Tribe, 1990; Sarıkaya et al., 2013), and swarming peaks at temperatures of around 12–15°C (Tribe, 1990; Mendel et al., 1991). Males colonize the substrate and bore into the phloem to excavate a nuptial chamber (Mendel and Halperin, 1982; Giesen et al., 1984). Conspecifics of both sexes are then attracted by an aggregation pheromone. Males usually mate with 1–3 females, but rarely up to even six (Atkinson, 1921; Chararas, 1964; Chararas and M’Sadda, 1970; Carle, 1973; Mendel and Halperin, 1982; Tribe, 1990). Oviposition in the absence of males is not uncommon as a certain percentage of females can be inseminated during the autumnal maturation feeding (Mendel, 1983). Females bore 12–120 mm long maternal tunnels longitudinal to the tree axis in cambium and outer xylem (Mendel and Halperin, 1982), and lay around 75 eggs (maximum 170 eggs) into the egg niches on both sides of the tunnels (Mendel and Halperin, 1982; Eglitis, 2000; Haack, 2004). Perpendicular larval galleries end with a pupation chamber in the inner bark, or more deeply in the sapwood in cases of insufficient bark thickness (Mendel and Halperin, 1982). To reach sexual maturity, young adults undergo maturation feeding and emerge when their cuticle is fully sclerotized (Eglitis, 2000). Total development lasts from 30 to 75 days under optimal temperature conditions (Mendel, 1983).
Orthotomicus erosus has a minimum temperature limitation, as the threshold for oviposition and development of immature stages is 14°C, which supports rapid offspring production and a quick switch from endemic to epidemic status (Mendel and Halperin, 1982; Mendel, 1983; Mendel et al., 1985).
Voltinism. The voltinism in O. erosus depends on temperature and host phloem quality; up to seven generations per year may occur (Mendel, 1983; Mendel et al., 1985; Lieutier and Paine, 2016). European populations are usually bivoltine, while 3–4 generations occur in North and South America and Africa, 4–5 in the Middle East, and up to six in the Mediterranean region (Carle, 1973; Mendel, 1983; Lee et al., 2005; Seybold and Downing, 2007; Sarıkaya, 2008; Sarıkaya et al., 2013; Pernek et al., 2019).
Overwintering. In the fall, O. erosus adults aggregate to overwinter under the bark of host trees (Mendel, 1983; Haack, 2004; Sarıkaya et al., 2013). Generally, dozens of adults penetrate to the phloem through a single entrance hole and then spread in all directions and bore irregular overwintering tunnels (Mendel, 1983).
Adults are the only overwintering stage in populations located close to the northern distribution limit and at high elevations (Mendel, 1983), while immature stages successfully overwinter in regions with mild winters, e.g., Turkey and the United States (Schimitschek, 1944; Seybold and Downing, 2007).
The Steelblue Jewel Beetle, Phaenops cyanea (Fabricius, 1775)
Habitats with sparsely distributed P. sylvestris and a warmer microclimate create optimal conditions for the occurrence of P. cyanea (Sierpiński, 1965; Perz and Ciesielski, 1993). The host tree spectrum also includes white pine (P. strobus), European larch [Larix decidua (Mill.)], European silver fir [Abies alba (Mill.)], and Norway spruce [Picea abies (L.)]. Phaenops cyanea is considered a secondary pest of old, weakened, and damaged trees (Bettag, 1979; Gutowski et al., 1992; Perz and Ciesielski, 1993; Łabêdzki, 1993; Gutowski and Królik, 1996; Luterek, 1996). Under suitable conditions, P. cyanea attack intensity and aggressivity increase, making the species a primary pest that causes damage to healthy forests (Zahradník, 1999; Foit and Čermák, 2014). According to the BAWBILT database, damage to eight million hectares and 12 million m3 were recorded in Slovakia and Poland during the 1990s (Grégoire and Evans, 2004). Vast losses have also been recorded in Germany, Czechia, Hungary, and Romania (Templin, 1962; Hellrigl, 1978; Apel, 1988; Wiegard and Amarell, 1994; Majunke, 1995; Apel et al., 1999; Knížek et al., 2020).
Distribution. Phaenops cyanea occurs almost throughout the Palearctic region, except in the extreme northern and Atlantic areas—i.e., Northern Africa, the Caucasus, Siberia, and Northern Mongolia (Gutowski et al., 1992; Mühle, 1993; Gutowski and Królik, 1996). In Central Europe, their distribution area predominantly includes lowlands up to 800 m.a.s.l. (Templin, 1962; Gabryel, 1967; Gfeller, 1985; Gutowski et al., 1992; Szujecki, 1995), although their ability to cope with temperature fluctuations allows them to spread into mountains at around 1,400 m.a.s.l., where sudden species abundance has been recorded (Gfeller, 1985; Del Pozo et al., 1995; Sowińska, 2006). Their abundance is lower in Southern Europe and in the north-western part of the continent (Templin, 1962; Hellrigl, 1978; Apel, 1988; Wiegard and Amarell, 1994; Majunke, 1995; Apel et al., 1999). In future, increases in the low-temperature thresholds might mean the distribution area will extend into highlands or even into the mountains. Also, areas with low abundance could suffer from significant damage as the life cycle might speed up.
Life Cycle. In Central Europe, flight activity starts in May and June, peaking 1 month later when temperatures reach 20°C (Stumpf, 1999; Zahradník, 1999). Mating takes place on the trunk surface and males repeatedly mate with females. Fertilized females then search for sunlit cracks in the bark to lay their eggs (Dengler, 1975; Gutowski et al., 1992; Zahradník, 1999; Bílý, 2002; Sowińska, 2006). Larvae hatch 3–4 days later and bore through the bark to the phloem (Filippenkova, 1971; Apel, 1991). Larval tunnels are irregular, flat or oval in the transverse cross-section, and 15–30 cm long (Gutowski et al., 1992; Zahradník, 1999; Bílý, 2002; Sowińska, 2006). Larval development lasts approximately 3 months, but detailed information about the factors influencing larval maturation, number of instars, and pupation are missing (Zahradník, 1999; Bílý, 2002). Larval abundance is significantly impacted by natural enemies and other species of cambioxylophagous insects (Gutowski et al., 1992; Szujecki, 1995). Another important factor in larval mortality are host tree defensive mechanisms, especially resin ducts (Gutowski et al., 1992) and the ability to avoid them (Weissbecker et al., 2006). The pupation process takes place in pupal chambers in the bark (Sierpiński, 1965; Bílý, 2002) or in the sapwood of trees with thin bark (Sierpiński, 1965). The length of the life cycle varies from a typical annual to an extended biennial or an exceptional 3-years cycle (Sierpiński, 1965; Szujecki, 1995; Apel et al., 1999; Zahradník, 1999).
Maturation Feeding and Overwintering. Adults undergo regeneration and maturation feeding on pine needles throughout the vegetation season from May to September (Gutowski et al., 1992; Zahradník, 1999; Bílý, 2002; Sowińska, 2006), which may lead to a considerable loss of the photosynthetic apparatus (Bílý, 2002).
Phaenops cyanea adults are short-living beetles. Males die within 3 or 4 days after copulation (Filippenkova, 1971; Apel, 1991), while females live up to 36 days (Bílý, 2002). During September and October, mature larvae and prepupae bore overwintering chambers 2–3 cm deep under the bark, or in the case of thin bark, 1–1.5 cm deep in the sapwood (Bílý, 2002). Pupation occurs in April and May and adults emerge 2–3 weeks later (Bílý, 2002). Young instar larvae overwinter in their tunnels and continue development the following spring (Gutowski et al., 1992; Zahradník, 1999; Bílý, 2002).
Discussion
The global climate is continuously warming (Field and Barros, 2014), and weather models predict significant changes in temperature conditions by the end of the twenty first century (IPCC, 2007; Kolb et al., 2016). Even though temperature fluctuations represent an ordinary phenomenon in the world’s climate millennia, the current unprecedented warming is likely to act as a powerful agent affecting the relationship between trees and subcortical insects. While forest ecosystems possess a long restoration time and their flexibility to react to climate changes is a little bit slow (Lindner et al., 2010), the cambioxylophagous insects rapidly react to any temperature increase, which ultimately results in the pest having higher fitness and reproductive success (Bakke, 1968).
Insects respond to climate warming in multiple ways, according to Lehmann et al. (2020); the monitored modifications are 55% related to voltinism and phenology and 62% to population dynamics. As ectotherms, active and post-diapause insects are primarily sensitive to environmental temperatures (Forrest, 2016), and thus optimal weather conditions early in spring result in an immediate response (Bartolomeus et al., 2011; Roy et al., 2015; Sato and Sato, 2015; Thomsen et al., 2016), for example, the earlier onset of spring swarming in bark beetles (Faccoli, 2009). A warm and dry vegetation season supports a shortening of the developmental period for all immature insect stages and shifts univoltine populations to multivoltine or adds one more generation in bivoltine populations (Jönsson et al., 2009; Mitton and Ferrenberg, 2012; Hlásny et al., 2021). Temperature influences such as these were recently confirmed in species causing several infestations of spruce and larch in Central Europe—e.g., European spruce bark beetle Ips typographus (Linnaeus, 1758), double-spined bark beetle Ips duplicatus (Sahlberg, 1836), and large larch bark beetle Ips cembrae (Heer, 1836)—either in laboratory experiments (Wermelinger and Seifert, 1998; Schebeck and Schopf, 2017; Davídková and Doležal, 2019), in laboratory cultures (Pfeffer and Knížek, 1995), or under field conditions (Mrkva, 1995; Wermelinger et al., 2012). A similar trend can also be observed in several bark beetle pests of P. sylvestris—e.g., I. sexdentatus, T. piniperda, and T. destruens (Šrot, 1968; Jactel and Lieutier, 1987; Horn et al., 2006; Sabbatini Peverrieri et al., 2008; Özcan, 2011; Péter, 2014; Yvon and Wegensteiner, 2015). Furthermore, increasing autumn temperatures bring a significant prolongation of the vegetation season (Bartolomeus et al., 2011; Diamond et al., 2011; Karlsson, 2014; Kharouba et al., 2014; Roy et al., 2015), which enables completion of development to most chilling tolerant stage prior to the onset of the harsh winter season and increases the probability of successful overwintering (e.g., Gallinat et al., 2015; Raffa et al., 2015; Rosenberger et al., 2017a; Schebeck and Schopf, 2017; Štefková et al., 2017). Together, these factors result in an enormous increase in pest population density (Wermelinger et al., 2008), an extensive dieback of host trees (e.g., Allen et al., 2010; IPCC, 2014; Senf et al., 2018; Hlásny et al., 2021; Marqués et al., 2022), and a shift in pest aggressivity. Under the influence of a changing climate, several species with minor economic importance in the past—e.g., I. acuminatus, T. piniperda, T. destruens, T. minor, and P. cyanea—have recently become more aggressive, causing severe environmental and economic losses (Gaylord et al., 2013; Netherer et al., 2015; Pešková et al., 2016).
An insects’ response to a warming environment may include shortening of its life cycle, and thus reaching epidemic levels in a shorter time (Bradshaw and Holzapfel, 2006). However, different life traits were recorded in two species of North American bark beetles, Dendroctonus ponderosae (Hopkins, 1902) and Dendroctonus rufipennis (Kirby, 1837). In the semivoltine species D. rufipennis, rising temperatures together with a longer growing season may result in finishing the development of callow adults in 1 year (Hansen et al., 2001; Hansen and Bentz, 2003; Schebeck et al., 2017). This shift from semi- to univoltinism has been predicted and recently also observed in some parts of D. rufipennis range (Régnière and Bentz, 2007; Schebeck et al., 2017; Bentz et al., 2019). A further shift to bivoltinism is highly improbable due to the occurrence of obligatory diapause that conditions the sexual maturation of progeny (Schebeck et al., 2017; Bentz et al., 2019). In the case of univoltine D. ponderosae, the shift to bivoltinism is conditioned by extreme temperature increases (Bentz et al., 2019), and thus only extreme climate change scenarios would be powerful enough to initiate a shift toward bivoltinism in its natural range (Bentz et al., 2019). However, expansion to Mexico and the southeast United States as well as lower latitudes in Europe might result in bivoltinism (Bentz et al., 2019). The species’ survival in a changing climate will depend on its physiological plasticity and possible mechanisms that might result in bivoltine populations of Dendroctonus bark beetles in future cannot be excluded completely (Bentz et al., 1991, 2019; Powell and Bentz, 2014; Bentz and Hansen, 2017).
The above-mentioned immediate responses of insects to high temperatures predominantly include short-term changes. Long-term effects of a changing climate can be demonstrated by shifts in the distribution area of species, regardless of the latitude and altitude (Gallego et al., 2004; Thuiller et al., 2008; Netherer and Schopf, 2010), as numerous species pioneer previously uncolonized territories (Buotte et al., 2017; Lantschner et al., 2017). It was estimated that up to 90% of insect species react to temperature changes by widening their geographic range (Lehmann et al., 2020). That has already been monitored for different kinds of pests like the larch bud moth, Zeiraphera diniana (Hübner, 1799), gypsy moth, Lymantria dispar (Linnaeus, 1758), pine processionary moth, Thaumetopoea pityocampa (Denis and Schiffermüller, 1775), emerald ash borer, Agrilus planipennis (Fairmaire, 1888), orpine bark beetles O. erosus, H. ligniperda, Hylurgus micklitzi (Wachtl, 1881), and Hylastes linearis (Erichson, 1836), etc. (Turchin et al., 2003; Toffolo et al., 2006; Liebhold et al., 2013; Faccoli et al., 2020). Thus, it can be assumed that sooner or later pine pests may spread their territories. Species expansions are a natural phenomenon and a dynamic process shaped by variations in climatic conditions that have occurred constantly for millions of years (Liebhold et al., 1995). Usually, the distribution range of species is determined by suitable ecological conditions, which support population viability (Liebhold et al., 1995). Therefore, the essential factors controlling species spread are climate, as well as the natural biological and geographical barriers (Bentz et al., 2010; Lantschner et al., 2017). At first, climate change promotes species dominance and spread within a domestic area (Bradley et al., 2012). Later, the former insurmountability of the natural barriers is dwindled due to extreme climatic deviations. Further spread into new, unexploited areas is supported by growing international trade (Mayr, 1963; Liebhold et al., 1995; Seebens et al., 2017), and new migration pathways into untapped food resources are loosed (Allee et al., 1949; Odum, 1971; Fox and Fox, 1986; Williamson and Brown, 1986; van Lenteren et al., 1987; Pimentel, 1993; Erbilgin et al., 2014; Cooke and Carroll, 2017; Rosenberger et al., 2017b). The introduction of forest pests is usually unnoticeable, but over time, some of them become a threat to the forest (Liebhold et al., 1995; Niemelä and Mattson, 1996). Typical prominent invasive representatives are the wood borers and bark beetles (Brockerhoff et al., 2006b; Liebhold et al., 2017). Even though pest density and distribution in the invaded area might be low, the seriousness of the damage inflicted could be economically high, as documented for the white pine weevil, Pissodes strobi (Say, 1831) on P. strobus in North America (Pimentel, 1993).
It seems that the phenotypic plasticity of bark beetles is elevated due to their ability to assimilate to new conditions. So, in time, there is a possibility that the selection pressure triggered by climate changes will play a role in reinforcing pre-adapted features or provoking genetic changes for preferential features, which would allow the native insects to be faster and more successful in their expansions. On top of that, the ability to utilize non-native tree species, causing damage or even their death, might also be positively affected (Carroll et al., 2004; Bentz et al., 2010; Wingfield et al., 2010; Paine et al., 2011; Branco et al., 2015; Lantschner et al., 2017; Liebhold et al., 2017). An example case might be the possible dispersion of T. destruens, which typically attacks coastal pine species, with an ability to evolve in inland species like P. nigra (Faccoli, 2007). The threat lies in the fact that P. nigra refuges are scattered around Southern Europe and cover Mediterranean mountains (Vidaković, 1991). If bark beetle populations from contact zones successfully breed in a new host, enormous devastation of southern European pine forests would occur.
During the last century, Central Europe experienced many epidemic outbreaks and migrations of the bark beetle pests. These have had a significant impact on an extensive area of boreal and temperate forests (Raffa et al., 2008; Økland et al., 2011). Spruce, pine, and larch stands were affected. Climate change brings many alterations to forest ecosystems, and the mechanisms and stimuli that trigger pest expansion beyond range borders are still not well-comprehended (Økland et al., 2019). The main problem is the complexity of interactions between beetles’ bionomy, climate, and environment dispositions (Økland et al., 2019). Therefore, in the near future, a higher expansion rate of forest pests like I. typographus, I. cembrae, I. duplicatus, Ips mannsfeldi (Wachtl, 1879), I. acuminatus, and Ips aminitus (Eichhoff, 1871) is to be expected (Lekander et al., 1977; Grodzki, 2003; Vakula et al., 2007; Holuša et al., 2010; Olenici et al., 2010; Aakala et al., 2011; Økland et al., 2011; Lindelöw et al., 2015; EFSA PLH, 2017).
Even though rising thermic limits and extension of the growing season support changes in voltinism, multivoltinism persists until beetles perceive the shortening daylength (Annila, 1969; Schopf, 1985, 1989; Doležal and Sehnal, 2007; Schroeder and Dalin, 2017). Therefore, after the summer solstice, the shortening of day length accompanied by the drop in night temperature induce diapause development in many temperate-zone species (Doležal and Sehnal, 2007; Saunders, 2014). Based on the latitude and altitude, a slow adjustment of reproduction, development, and stress resistance to local conditions occurs (Schebeck et al., 2021). This evolutionary adaptation reduces pre-imaginal mortality during the harsh season, and thus reduces population losses (Baier et al., 2007). Diapause is terminated during the period of low mid-winter temperatures (Doležal and Sehnal, 2007) and the following post-diapause quiescence is solely temperature dependent (DeWilde, 1970; Gehrken, 1985), which shifts insect emergence from hibernation sites until favorable conditions occur in the following spring (Dobart, 2006; Doležal and Sehnal, 2007). However, intraspecific differences in photoperiodic threshold have been recorded in several species of bark beetles, including I. typographus (Schopf, 1985, 1989; Doležal and Sehnal, 2003, 2007; Baier et al., 2007; Faccoli, 2009; Schroeder and Dalin, 2017; Schebeck et al., 2021). In northern populations of this species, diapause development occurred even during long day conditions (Schroeder and Dalin, 2017; Schebeck et al., 2021). Thus, it seems that the photoperiod threshold is, at least for now, an important driver influencing the voltinism of local populations. Nevertheless, the hidden danger of climate change might be a general increase in night temperatures. Long-lasting constant temperature below 5°C (at least 2 months) induces diapause development in I. typographus (Doležal and Sehnal, 2007), but these conditions in Central Europe and Southern Scandinavia have already stagnated. Additionally, climate models predict that the frequency of years with chill conditions will decrease by more than 50% by the end of this century (Jönsson et al., 2011). Consequently, long and warm periods at the end of the vegetation season may eventually cease diapause development, as was confirmed by laboratory research of D. rufipennis. In a recent study, lack of cold stimulation produced active non-diapausing adults that laid viable eggs (Davenport, 2020). Such a situation may result in prompt temperature-mediated emergence in early spring followed by rapid population growth (Jönsson et al., 2011; Davenport, 2020). Therefore, studies of photoperiodic response and its temperature modifications in populations of bark beetles across their geographic range represent a crucial area of investigation for understanding changes in bionomy, predicting future trends, and finally, for adjusting forest management (Jönsson et al., 2011).
Conclusion
In summary, climate change, especially temperature increases, significantly impacts insect pests of P. sylvestris in multiple ways, including behavioral details, population dynamics, voltinism, distribution, and epigenetic features such as diapause development and overwintering strategies. Unfortunately, empirical data on relationships between temperature conditions and phenological traits in those bark beetle species are still scarce, which complicates effective management of pest species. Detailed research on species and population levels are crucial to evolve new, and improve existing, methods of forest protection and pest management.
Author Contributions
DH contributed to the content of the study and wrote the first draft of the manuscript. PD contributed to the content and wrote and controlled sections of the manuscript. Both authors contributed to manuscript revision, read, and approved the submitted version.
Funding
This study was supported by Forests of the Czech Republic, state enterprises, project 05/2019.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Acknowledgments
We thank two reviewers and the editor for their comments that considerably improved the quality of this manuscript. Many thanks come to Rachel Nadine Kolisko, M.Sc., for the English language revision.
References
Aakala, T., Kuuluvainen, T., Wallenius, T., and Kauhanen, H. (2011). Tree mortality episodes in the intact Picea abies-dominated taiga in the Arkhangelsk region of northern European Russia. J. Veg. Sci. 22, 322–333. doi: 10.1111/j.1654-1103.2010.01253.x
Allee, W. C., Park, O., Emerson, A. E., Park, T., and Schmidt, K. P. (1949). Principles of animal ecology. Philadelphia: Saunders Company.
Allen, C. D., Breshears, D. D., and McDowell, N. G. (2015). On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6:art129. doi: 10.1890/ES15-00203.1
Allen, D. C., Macalady, A. K., Chenchouni, H., Bachelet, D., McDowell, N., Vennetier, M., et al. (2010). A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For. Ecol. Manage. 259, 660–684. doi: 10.1016/j.foreco.2009.09.001
Amezaga, I., and Garbisu, C. (2001). Effect of maturation feeding period on survival of Tomicus piniperda (Coleoptera: Scolytidae). Can. Entomol. 133, 131–137. doi: 10.4039/Ent133131-1
Amini, S., Hosseini, R., and Sohani, M. M. (2013). A faunal study of bark beetles (Coleoptera: Curculionidae: Scolytinae) in Guilan province in North of Iran. Entomofauna 34, 169–176.
Anderegg, L. D., and HilleRisLambers, J. (2016). Drought stress limits the geographic ranges of two tree species via different physiological mechanisms. Glob. Chang. Biol. 22, 1029–1045. doi: 10.1111/gcb.13148
Anderegg, W. R. L., Hicke, J. A., Fisher, R. A., Allen, C. D., Aukema, J., Bentz, B., et al. (2015). Tree mortality from drought, insects, and their interactions in a changing climate. New Phytol. 208, 674–683. doi: 10.1111/nph.13477
Annila, E. (1969). Influence of temperature upon the development and voltinism of Ips typographus L. (Coleoptera, Scolytidae). Ann. Zool. Fenn 1969:6.
Annila, E., Långström, B., Varama, M., Hiukka, R., and Niemelä, P. (1999). Susceptibility of defoliated Scots pine to spontaneous and induced attack by Tomicus piniperda and Tomicus minor. Silva Fenn. 33, 93–106. doi: 10.14214/sf.660
Anon. (1981). Pest interception of quarantine significance at port of entry. Agric. Pl. Pest News. 1:3.
Apel, K. H. (1988). Befallsverteilung von Melanophila acuminata Deg., Phaenops cyanea F. und Ph. formaneki Jacob. (Col., Buprestidae) auf Waldbrandflachen. Beiträge Für Die Forstwirtschaft. 22, 45–48.
Apel, K. H., Wenk, M., and Klaiber, C. (1999). Status Kolloquium zum Massenwechsel und zur Wirtsfindung des Blauen Kiefernprachtkäfers in Eberswalde. Brandenburgische Forstnachrichten. 8, 13–15.
Arango-Velez, A., ElKayal, W., Copeland, C. C., Zaharia, L. I, Lusebrink, I., and Cooke, J. E. (2016). Differences in defence responses of Pinus contorta and Pinus banksiana to the mountain pine beetle fungal associate Grosmannia clavigera are affected by water deficit. Plant. Cell. Environ. 39, 726–744. doi: 10.1111/pce.12615
Arias, M., Robertson, L., GarciaAlvarez, A., Arcos, S. C., Escuer, M., Sanz, R., et al. (2005). Bursaphelenchus fungivorus (Nematoda: Aphelenchida) associated with Orthotomicus erosus (Coleoptera: Scolitydae) in Spain. For. Pathol. 35, 375–383. doi: 10.1111/j.1439-0329.2005.00422.x
Ayres, M. P., and Lombardero, M. J. (2000). Assessing the consequences of global change for forest disturbance from herbivores and pathogens. Sci. Total. Environ. 262, 263–286. doi: 10.1016/S0048-9697(00)00528-3
Ayres, M. P., and Scriber, J. M. (1994). Local adaptation to regional climates in Papilio canadensis (Lepidoptera: Papilionidae). Ecol. Monogr. 64, 465–482. doi: 10.2307/2937146
Baier, P., Pennerstorfer, J., and Schopf, A. (2007). PHENIPS—A comprehensive phenology model of Ips typographus (L.) (Col., Scolytinae) as a tool for hazard rating of bark beetle infestation. For. Ecol. Manage. 249, 171–186. doi: 10.1016/j.foreco.2007.05.020
Bakke, A. (1968). Ecological studies on bark beetles (Coleoptera: Scolytidae) associated with Scots pine (Pinus sylvestris L.) in Norway with particular reference to the influence of temperature. Meddr. Norske. SkogsforsVes. 21, 443–602.
Bakke, A. (1978). Aggregation pheromone components of the bark beetle Ips acuminatus. Oikos 31, 184–188. doi: 10.2307/3543561
Bartolomeus, I., Ascher, J. S., Wagner, D., Danforth, B. N., Colla, S., Kornbluth, S., et al. (2011). Climate-associated phenological advances in bee pollinators and bee-pollinated plants. Proc. Natl. Acad. Sci. USA 108, 20654–20659. doi: 10.1073/pnas.1115559108
Ben Jamaa, M. L., Lieutier, F., Yart, A., Jerraya, A., and Khouja, M. L. (2007). The virulence of phytopathogenic fungi associated with the bark beetles Tomicus piniperda and Orthotomicus erosus in Tunisia. Forest Pathol. 37, 51–63. doi: 10.1111/j.1439-0329.2007.00478.x
Ben Jamaa, M., Jerraya, A., and Lieutier, F. (2000). Les scolytes ravageurs de pins en Tunisie. Annales de L’Inrgref. 4, 27–39.
Bentz, B. J., and Hansen, E. M. (2017). Evidence for a prepupal diapause in the mountain pine beetle (Dendroctonus ponderosae). Environ. Entomol. 47, 175-183. doi: 10.1093/ee/nvx192
Bentz, B. J., Jönsson, A. M., Schroeder, M., Weed, A., Wilcke, R. A. I., and Larsson, K. (2019). Ips typographus and Dendroctonus ponderosae models project thermal suitability for intra- and inter-continental establishment in a changing climate. Front. For. Glob. Chan. 2:1. doi: 10.3389/ffgc.2019.00001
Bentz, B. J., Logan, J. A., and Amman, G. D. (1991). Temperature-dependent development of the mountain pine beetle (Coleoptera: Scolytidae) and simulation of its phenology. Can. Entomol. 123, 1083–1094. doi: 10.4039/Ent1231083-5
Bentz, B. J., Régnière, J., Fettig, C. J., Hansen, E. M., Hayes, J. L., Hicke, J. A., et al. (2010). Climate change and bark beetles of the western United States and Canada: direct and indirect effects. BioScience 60, 602–613. doi: 10.1525/bio.2010.60.8.6
Bettag, E. (1979). Zur Biologie einiger Prachtköfer aus der Pfalz. Pfälzer. Heimat. Speyer. 30, 129–132.
Bigler, C., Bräker, O. U., Bugmann, H., Dobbertin, M., and Rigling, A. (2006). Drought as an inciting mortality factor in Scots pine stands of the Valais, Switzerland. Ecosystems 9, 330–343. doi: 10.1007/s10021-005-0126-2
Bílý, S. (2002). Summary of the bionomy of the buprestid beetles of Central Europe (Coleoptera: Buprestidae). Acta Entomol. Mus. Natl. Pragae. 10, 1–104.
Borkowski, A. (2001). Threats to pine stands by the pine shoot beetles Tomicus piniperda (L.) and Tomicus minor (Hart.) (Col., Scolytidae) around a sawmill in Southern Poland. J. Appl. Entomol. 125, 489–492. doi: 10.1046/j.1439-0418.2001.00580.x
Bouget, C., Brustel, H., and Nageleisen, L.-M. (2005). Nomenclature des groupes écologiques d’insectes liés au bois: synthèse et mise au point sématique. C. R. Biologies. 328, 936–948. doi: 10.1016/j.crvi.2005.08.003
Bouhot, L., Lieutier, F., and Debouzie, D. (1987). Spatial and temporal distribution of attacks by Tomicus piniperda L. and Ips sexdentatus Boern. (Col., Scolytidae) on Pinus sylvestris. J. Appl. Entomol. 106, 356–371. doi: 10.1111/j.1439-0418.1988.tb00604.x
Bradley, B. A., Blumenthal, D. M., Early, R., Grosholz, E. D., Lawler, J. J., Miller, L. P., et al. (2012). Global change, global trade, and the next wave of plant invasions. Front. Ecol. Environ. 10:20–28. doi: 10.1890/110145
Bradshaw, W. E., and Holzapfel, C. M. (2006). Evolutionary response to rapid climate change. Science 312, 1477-1478. doi: 10.1126/science.1127000
Branco, M., Brockerhoff, E. G., Castagneyrol, B., Orazio, C., and Jactel, H. (2015). Host range expansion of native insects to exotic trees increases with area of introduction and the presence of congeneric native trees. J. Appl. Ecol. 52, 69–77. doi: 10.1111/1365-2664.12362
Branco, M., Pereira, J. S., Mateus, E., Tavares, C., and Paiva, M. R. (2010). Water stress affects Tomicus destruens host pine preference and performance during the shoot feeding phase. Ann. For. Sci. 67, 608–608. doi: 10.1051/forest/201021
Bright, D. E., and Skidmore, R. E. (1997). A catalog of Scolytidae and Platypodidae (Coleoptera). Supplement 1 (1990-1994). Ottawa: NRCResearch Press.
Bright, D. E., and Skidmore, R. E. (2002). A catalog of Scolytidae and Platypodidae (Coleoptera). Supplement 2 (1995-1999). Ottawa: NRCResearch Press.
Brockerhoff, E. G., Bain, J., Kimberley, M., and Knizek, M. (2006a). Interception frequency of exotic bark and ambrosia beetles (Coleoptera: Scolytinae) and relationship with establishment in New Zealand and worldwide. Can. J. For. Res. 36, 289–298. doi: 10.1139/x05-250
Brockerhoff, E. G., Liebhold, A. M., and Jactel, H. (2006b). The ecology of forest insect invasions and advances in their management. Can. J. For. Res. 36, 263–268. doi: 10.1139/x06-013
Browne, F. G. (1968). Pests and diseases of forest plantation trees: an annotated list of the principal species occurring in the British Commonwealth. Oxford: Clarendon Press.
Buotte, P. C., Hicke, J. A., Preisler, H. K., Abatzoglou, J. T., Raffa, K. F., and Logan, J. A. (2017). Recent and future climate suitability for whitebark pine mortality from mountain pine beetles varies across the western US. For. Ecol. Manage. 399, 132–142. doi: 10.1016/j.foreco.2017.05.032
Byers, J. A., Lanne, B. S., Löfqvist, J., Schlyter, F., and Bergström, G. (1985). Olfactory recognition of host-tree susceptibility by pine shoot beetles. Naturwissenschaften 72, 324–326. doi: 10.1007/BF00454776
Camarero, J. J., Gazol, A., SangüesaBarreda, G., Oliva, J., and VicenteSerrano, S. M. (2015). To die or not to die: early warnings of tree dieback in response to a severe drought. J. Ecol. 103, 44–57. doi: 10.1111/1365-2745.12295
Carle, P. (1973). Le dépérissment du pin mesogeen en Provence. Rôle des insectes dans les modifications d’équilibre biologiquedes forêts envahies par Matsucoccus feytadui Duc. (Coccoides, Margarodidae). [dissertation thesis]. France: University of Bordeaux. doi: 10.1051/forest/19740101
Carmona, D., Lajeunesse, M. J., and Johnson, M. T. (2011). Plant traits that predict resistance to herbivores. Funct. Ecol. 25, 358–367. doi: 10.1111/j.1365-2435.2010.01794.x
Carroll, A. L., Taylor, S. W., Regniere, J., and Safranyik, L. (2004). “Effects of climate change on range expansion by the mountain pine beetle in British Columbia,” in Mountain pine beetle symposium: challenges and solutions, eds T. L. Shore, J. E. Brooks, and J. E. Stone (Ottawa: Natural Resources Canada, Canadian Forest Service), 223–232.
Chakali, G. (1992). Les insectes ravageurs du Pin d’Alep, Pinus halepensis Mill., en Algérie. Memoires de La Société Royale Belge D’entomologie 35, 505–509.
Chakali, G. (2007). Stratégie d’attaque de l’hylésine Tomicus destruens (Wollaston 1865) (Coleoptera: Scolytidae) sur le pin d’Alep en zone semi-aride (Algérie, Djelfa). Annales de La Société Entomologique de France 43, 129–137. doi: 10.1080/00379271.2007.10697502
Chakali, G. (2008). Biology and behaviour of the bark beetle, Tomicus destruens (Wollaston, 1865) (Coleoptera: Scolytidae) in Alepo pine of Algeria. Boletim Do Museu Municipal Do Funchal 14, 35–42.
Chararas, C., and M’Sadda, K. (1970). Attraction chimique et attraction sexuelle chez Orthotomicus erosus Woll. (Coléoptère, Scolytidae). C.R. Acad. Sci. 271, 1904–1907.
Chararas, C., Ducauze, C., and Revolon, C. (1978). Etude comparative du pouvoir attractif de certains coniféres sur divers Scolytidae (Insectes, Coléoptères). C.R. Acad. Sci. 286:346.
Chinellato, F., Battisti, A., Finozzi, V., and Faccoli, M. (2014). Better today but worse tomorrow: how warm summers affect breeding performance of a Scots pine pest. Agrochimica 58, 133–145.
Ciesla, W. (2004). Forests and forest protection in Cyprus. For. Chron. 80, 107–113. doi: 10.5558/tfc80107-1
Colombari, F., Battisti, A., Schroeder, L. M., and Faccoli, M. (2012). Life-history traits promoting outbreaks of the pine bark beetle Ips acuminatus (Coleoptera: Curculionidae, Scolytinae) in the south-eastern Alps. Eur. J. For. Res. 131, 553–561. doi: 10.1007/s10342-011-0528-y
Colombari, F., Schroeder, M. L., Battisti, A., and Faccoli, M. (2013). Spatio-temporal dynamics of an Ips acuminatus outbreak and implications for management. Agric. For. Entomol. 15, 34–42. doi: 10.1111/j.1461-9563.2012.00589.x
Cooke, B. J., and Carroll, A. L. (2017). Predicting the risk of mountain pine beetle spread to eastern pine forests: considering uncertainty in uncertain times. For. Ecol. Manage. 396, 11–25. doi: 10.1016/j.foreco.2017.04.008
Czokajlo, D., Wink, R. A., Warren, J. C., and Teale, S. A. (1997). Growth reduction of Scots pine, Pinus sylvestris, caused by the larger pine shoot beetle, Tomicus piniperda (Coleoptera, Scolytidae) in New York State. Can. J. For. Res. 27, 1394–1397. doi: 10.1139/x97-111
Das, A. J., Stephenson, N. L., Flint, A., Das, T., and van Mantgem, P. J. (2013). Climatic correlates of tree mortality in water- and energy-limited forests. PLoS One 8:e69917. doi: 10.1371/journal.pone.0069917
Davenport, M. E. (2020). Variability in adult reproductive diapause of the spruce beetle, Dendroctonus rufipennis. [dissertation thesis]. Denver: University of Colorado at Denver.
Davídková, M., and Doležal, P. (2019). Temperature-dependent development of the double-spined spruce bark beetle Ips duplicatus (Sahlberg, 1836) (Coleoptera; Curculionidae). Agric. For. Entomol. 21, 388–395. doi: 10.1111/afe.12345
Del Pozo, E., García, F., and Monreal, J. A. (1995). Nota sobre un fuerte ataque de bupréstido Phaenops cyanea (F.) en un monte de Pinus nigra Arnold en la Sierra del Segura. Albacete. Bol. Sanid. Veg. Plagas. 21, 475–479.
Dengler, K. (1975). Zur Bekämpfung des Blauen Kiefernprachtkäfers Phaenops cyanea F1. Zeitschrift für Angewandte Entomologie. 78, 5–9. doi: 10.1111/j.1439-0418.1975.tb04143.x
Diamond, S. E., Frame, A. M., Martin, R. A., and Buckley, L. B. (2011). Species’ traits predict phenological responses to climate change in butterflies. Ecology 92, 1005–1012. doi: 10.1890/10-1594.1
Dobart, N. (2006). Studies on the emergence of Ips typographus L. (Col., Scolytidae) from hibernating sites. [dissertation thesis]. Wien: Universität für Bodenkultur.
Dobbertin, M., Mayer, P., Wohlgemuth, T., Feldmeyer-Christe, E., Graf, U., Zimmermann, N. E., et al. (2005). The Decline of Pinus sylvestris L. forests in the Swiss Rhone valley - a result of drought stress? Phyton. 45, 153–156.
Dobbertin, M., Wermelinger, B., Bigler, C., Bürgi, M., Carron, M., Forster, B., et al. (2007). Linking increasing drought stress to Scots pine mortality and bark beetle infestations. Sci. World. J. 7, 231–239. doi: 10.1100/tsw.2007.58
Doležal, P., and Sehnal, F. (2003). “Imaginal diapause in the bark beetle Ips typographus,” in Proceedings: Ecology, Survey and Management of Forest Insects, eds M. L. McManus and A. M. Liebhold (Newtown Square, PA: U.S. Dept. of Agriculture), 127.
Doležal, P., and Sehnal, F. (2007). Effects of photoperiod and temperature on the development and diapause of the bark beetle Ips typographus. J. Appl. Entomol. 131, 165–173. doi: 10.1111/j.1439-0418.2006.01123.x
Eglitis, A. (2000). EXFOR Database pest reports: Orthotomicus erosus. Washington, DC: USDA Forest Service.
Eidmann, H. H. (1965). Untersuchungen über die Verteilung und den Verlauf von Insektenbefall an berindetem Kiefern- und Fichtenholz. Skogshögskolan, Institutionen För Skogsentomologi, Rapporter Och Uppsatser. 3, 1–59.
Eidmann, H. H. (1974). Versuche über den Verlauf des Schwärmens von Borkenkäfern und des Insektenbefalls an Kiefernholz in Mittelschweden. Studia Forestalia Suecica 113, 1–26.
Erbilgin, N., Ma, C., Whitehouse, C., Shan, B., Najar, A., and Evenden, M. (2014). Chemical similarity between historical and novel host plants promotes range and host expansion of the mountain pine beetle in a naïve host ecosystem. New Phytol. 201, 940–950. doi: 10.1111/nph.12573
Escherich, K. (1914). Die Forstinsekten Mitteleuropas, Band I. Berlin: Paul Parley Verlag. doi: 10.5962/bhl.title.45237
Etxebeste, I., and Pajares, J. A. (2011). Verbenone protects pine trees from colonization by the six-toothed pine bark beetle, Ips sexdentatus Boern. (Col.: Scolytinae). J. Appl. Entomol. 135, 258–268. doi: 10.1111/j.1439-0418.2010.01531.x
Etxebeste, I., Lencina, J. L., and Pajares, J. (2013). Saproxylic community, guild and species responses to varying pheromone components of a pine bark beetle. Bull. Entomol. Res. 103, 497–510. doi: 10.1017/S0007485312000879
Faccoli, M. (2006). Morphological separation of Tomicus piniperda and T. destruens (Coleoptera: Curculionidae: Scolytinae): new and old characters. Eur. J. Entomol. 103, 433–442. doi: 10.14411/eje.2006.057
Faccoli, M. (2007). Breeding performance and longevity of Tomicus destruens on Mediterranean and continental pine species. Entomol. Exp. Appl. 123, 263–269. doi: 10.1111/j.1570-7458.2007.00557.x
Faccoli, M. (2009). Breeding performance of Tomicus destruens at different densities: the effect of intraspecific competition. Entomol. Exp. Appl. 132, 191–199. doi: 10.1111/j.1570-7458.2009.00883.x
Faccoli, M., Battisti, A., and Masutti, L. (2005a). “Phenology of Tomicus destruens (Wollaston) in northern Italian pine stand,” in Entomological research in Mediterranean forest ecosystems, eds F. Lieutier and D. Ghaioule (Paris: INFRA Editions), 185–193.
Faccoli, M., Finozzi, V., and Colombari, F. (2012). Effectiveness of different trapping protocols for outbreak management of the engraver pine beetle Ips acuminatus (Curculionidae. Scolytinae). Int. J. Pest. Manag. 58, 267–273. doi: 10.1080/09670874.2011.642824
Faccoli, M., Gallego, D., Branco, M., Brockerhoff, E. G., Corley, J., Coyle, D. R., et al. (2020). A first worldwide multispecies survey of invasive Mediterranean pine bark beetles (Coleoptera: Curculionidae, Scolytinae). Biol. Invas. 22:2219. doi: 10.1007/s10530-020-02219-3
Faccoli, M., Piscedda, A., Salvato, P., MauroSimonato, Masutti, L., and Battisti, A. (2005b). Genetic structure and phylogeography of pine shoot beetle populations (Tomicus destruens and T. piniperda, Coleoptera Scolytidae) in Italy. Ann. For. Sci. 62, 361–368. doi: 10.1051/forest:2005031
Farquhar, G. D., O’Leary, M. H., and Berry, J. A. (1982). On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Funct. Plant Biol. 9, 121–137. doi: 10.1071/PP9820121
Fernández Fernández, M. M., Pajares Alonso, J. A., and Salgado Costas, J. M. (1999a). Oviposition and development of the immature stages of Tomicus minor (Coleoptera, Scolytidae). Agric. For. Entomol. 1, 97–102. doi: 10.1046/j.1461-9563.1999.00012.x
Fernández Fernández, M. M., Pajares Alonso, J. A., and Salgado Costas, J. M. (1999b). Shoot feeding and overwintering in the lesser pine shoot beetle Tomicus minor (Col., Scolytidae) in north-west Spain. J. Appl. Entomol. 123, 321–327. doi: 10.1046/j.1439-0418.1999.00082.x
Ferrio, J. P., Florit, A., Vega, A., Serrano, L., and Voltas, J. (2003). Δ13C and tree-ring width reflect different drought responses in Quercus ilex and Pinus halepensis. Oecologia 137, 512–518. doi: 10.1007/s00442-003-1372-7
Field, C. B., and Barros, V. R. (2014). Climate Change 2014 - Impacts, Adaptation and Vulnerability: Regional Aspects. Cambridge: Cambridge University Press. doi: 10.1017/CBO9781107415379
Filippenkova, V. V. (1971). Parazity stvolovych vreditelei sosny v lesach Srednego Zavozhia. [Parazites of timber pests of pines in the forests of the Middle Volga river]. Entomol. Rev. 50, 763–769.
Flexas, J., DiazEspejo, A., Galmes, J., Kaldenhoff, R., Medrano, H., and RibasCarbo, M. (2007). Rapid variations of mesophyll conductance in response to changes in CO2 concentration around leaves. Plant. Cell. Environ. 30, 1284–1298. doi: 10.1111/j.1365-3040.2007.01700.x
Foit, J., and Čermák, V. (2014). Colonization of disturbed Scots pine trees by bark- and wood-boring beetles. Agric. For. Entomol. 16, 184–195. doi: 10.1111/afe.12048
Forrest, J. R. K. (2016). Complex responses of insect phenology to climate change. Curr. Opin. Insect Sci. 17, 49–54. doi: 10.1016/j.cois.2016.07.002
Fox, H., DoronFaigenboim, A., Kelly, G., Bourstein, R., Attia, Z., Zhou, J., et al. (2018). Transcriptome analysis of Pinus halepensis under drought stress and during recovery. Tree Physiol. 38, 423–441. doi: 10.1093/treephys/tpx137
Fox, M. D., and Fox, B. J. (1986). “The susceptibility of natural communities to invasion,” in Ecology of Biol Invasions, eds R. H. Groves and J. J. Burdon (Cambridge: Cambridge Univ. Press), 57–66.
Francke, W., Pan, M.-L., Bartels, J., König, W. A., Vité, J. P., Krawielitzki, S., et al. (1986). The odour bouquet of three pine engraver beetles (Ips spp.). J. Appl. Entomol. 101, 453–461. doi: 10.1111/j.1439-0418.1986.tb00879.x
Francke-Grosmann, H. (1951). Über die Ambrosiazucht der beiden Kiefernborkenkafer Mylophilus minor Htg. und Ips acuminatus Gyll. Meddelanden Fran Statens Skogsforskningsinstitut 41, 1–52.
Furniss, R. L., and Carolin, V. M. (1977). Western forest insects. Portland: USA Pacific NW F&RES. doi: 10.5962/bhl.title.131875
Galiano, L., Martínez-Vilalta, J., and Lloret, F. (2010). Drought-induced multifactor decline of Scots pine in the Pyrenees and potential vegetation change by the expansion of co-occurring oak species. Ecosystems 13, 978–991. doi: 10.1007/s10021-010-9368-8
Gallego, D., and Galián, J. (2001). The internal transcribed spacers (ITS1 and ITS2) of the rDNA differentiates the bark beetle forest pests Tomicus destruens and T. piniperda. Insect. Mol. Biol. 10, 415–420. doi: 10.1046/j.0962-1075.2001.00279.x
Gallego, D., Canovas, F., Esteve, M. A., and Galian, J. (2004). Descriptive biogeography of Tomicus (Coleoptera: Scolytidae) species in Spain. J. Biogeogr. 31, 2011–2024. doi: 10.1111/j.1365-2699.2004.01131.x
Gallego, D., Galián, J., Diez, J. J., and Pajares, J. A. (2008). Kairomonal responses of Tomicus destruens (Col., Scolytidae) to host volatiles α-pinene and ethanol. J. Appl. Entomol. 132, 654–662. doi: 10.1111/j.1439-0418.2008.01304.x
Gallinat, A. S., Primack, R. B., and Wagner, D. L. (2015). Autumn, the neglected season in climate change research. Trends Ecol. Evol. 30, 169–176. doi: 10.1016/j.tree.2015.01.004
Gaylord, M. L., Kolb, T. E., Pockman, W. T., Plaut, J. A., Yepez, E. A., Macalady, A. K., et al. (2013). Drought predisposes piñon-juniper woodlands to insect attacks and mortality. New Phytol. 198, 567–578. doi: 10.1111/nph.12174
Gea-Izquierdo, G., Férriz, M., García-Garrido, S., Aguín, O., Elvira-Recuenco, M., Hernandez-Escribano, L., et al. (2019). Synergistic abiotic and biotic stressors explain widespread decline of Pinus pinaster in a mixed forest. Sci. Total. Environ. 685, 963–975. doi: 10.1016/j.scitotenv.2019.05.378
Gehrken, U. (1984). Winter survival of an adult bark beetle Ips acuminatus Gyll. J. Insect. Physiol. 30:421429. doi: 10.1016/0022-1910(84)90100-8
Gehrken, U. (1985). Physiology of diapause in the adult bark beetle, Ips acuminatus Gyll., studied in relation to cold hardiness. J. Insect. Physiol. 31, 909–916. doi: 10.1016/0022-1910(85)90024-1
Gehrken, U. (1989). Supercooling and thermal hysteresis in the adult bark beetle, Ips acuminatus Gyll. J. Insect. Physiol. 35, 347–352. doi: 10.1016/0022-1910(89)90084-X
Gehrken, U. (1992). Inoculative freezing and thermal hysteresis in the adult beetles Ips acuminatus and Rhagium inquisitor. J. Insect. Physiol. 38, 519–524. doi: 10.1016/0022-1910(92)90077-Q
Gehrken, U. (1995). Correlative influence of gut appearance, water content and thermal hysteresis on whole body supercooling point of adult bark beetles, Ips acuminatus Gy11. Comp. Biochem. Physiol. Part A: Physiol. 112, 207–214. doi: 10.1016/0300-9629(95)00068-I
Gfeller, W. (1985). Bemerkenswerte Käferfunde im Wallis, Sommer 1984. Mitt. Entomol. Ges. Basel. 35, 69–73.
Giesen, H., Kohnle, U., Vité, J. P., Pan, M. L., and Francke, W. (1984). Das aggregationspheromon des mediterranen Kiefernborkenkäfers Ips (Orthotomicus) erosus. Zeitschrift für angewandte Entomologie 98, 95–97. doi: 10.1111/j.1439-0418.1984.tb02688.x
Gil Sanchéz, L. A., and Pajares Alonso, R. (1986). Los escolítidos de las coníferas en la Peninsula Ibérica. Madrid: INIA, Ministerio de Agricultura, Pesca y Alimentacíon.
Gilbert, M., and Sauvard, D. (2007). “The Bawbilt Database,” in Bark and Wood Boring Insects in Living Trees in Europe, a Synthesis, eds F. Lieutier, K. R. Day, A. Battisti, J. C. Grégoire, and H. F. Evans (Dordrecht: Springer), 15–18. doi: 10.1007/978-1-4020-2241-8_3
Gómez, D., and Martínez, G. (2013). Bark beetles in pine tree plantations in Uruguay: First record of Orthotomicus erosus Wollaston (Coleoptera: Curculionidae: Scolytinae). Coleopt. Bull. 67, 470–472. doi: 10.1649/0010-065X-67.4.470
Grégoire, J. C., and Evans, H. F. (2004). “Damage and control of BAWBILT organism, an overview,” in Bark and Wood Boring Insects in Living Trees in Europe, a Synthesis, eds F. Lieutier, A. Battisit, J. C. Grégoire, and H. F. Evans (Dordrecht: Springer), 19–37. doi: 10.1007/978-1-4020-2241-8_4
Grodzki, W. (2003). Distribution range of the double spined bark beetle Ips duplicatus C.R. Sahlb. (Col.: Scolytidae) in the mountain areas of Southern Poland. Sylwan 147, 29–36.
Gutowski, J. M., and Królik, R. (1996). A review of the morphology, distribution and biology of Palearctic species of the genus Phaenops Dej. (Coleoptera: Buprestidae). Crystal. Series Zool. 3, 3–88.
Gutowski, J. M., Królik, R., and Partyka, M. (1992). Studia nad biologia, wystêpowaniem i znaczeniem gospodarczym w Polsce bogatków z rodzaju Phaenops Dejan (Coleoptera: Buprestidae). Prace Instytutu Badawczego Leśnictwa. 736, 1–79.
Haack, R. A. (2004). Orthotomicus erosus: A new pine-infesting bark beetle in the United States. Newsletter of the Michigan entomological society 49, 3–4.
Haack, R. A. (2006). Exotic bark- and wood-boring Coleoptera in the United States: recent establishments and interceptions. Can. J. For. Res. 36, 269–288. doi: 10.1139/x05-249
Haack, R. A., Lawrence, R. K., and Heaton, G. C. (2001). Tomicus piniperda (Coleoptera: Scolytidae) shoot-feeding characteristics and overwintering behavior in Scotch pine Christmas trees. J. Econ. Entomol. 94, 422-429. doi: 10.1603/0022-0493-94.2.422
Hansen, E. M., and Bentz, B. J. (2003). Comparison of reproductive capacity among univoltine, semivoltine, and re-emerged parent spruce beetles (Coleoptera?: Scolytidae). Can. Entomol. 135, 697–712. doi: 10.4039/n02-109
Hansen, E. M., Bentz, B. J., and Turner, D. L. (2001). Temperature-based model for predicting univoltine brood proportions in spruce beetle (Coleoptera: Scolytidae). Can. Entomol. 133, 827–841. doi: 10.4039/Ent133827-6
Hanson, P. J., and Weltzin, J. F. (2000). Drought disturbance from climate change: response of United States forests. Sci. Total. Environ. 262, 205–220. doi: 10.1016/S0048-9697(00)00523-4
Hellrigl, K. G. (1978). Ökologie und Brutpflanzen europäischer Prachtkäfer (Col., Buprestidae). Zeitschrift Für Angewandte Entomologie. 85, 167–191. doi: 10.1111/j.1439-0418.1978.tb04028.x
Henin, J. M., and Pavia, M. R. (2004). Interactions between Orthotomicus erosus (Woll.) (Col., Scolytidae) and the Argentine ant Linepithema humile (Mayr) (Hym., Formicidae). J. Pest. Sci. 77, 113–117. doi: 10.1007/s10340-003-0045-y
Hereş, A. M., Camarero, J. J., López, B. C., and Martínez-Vilalta, J. (2014). Declining hydraulic performances and low carbon investments in tree rings predate Scots pine drought-induced mortality. Trees 28, 1737-1750. doi: 10.1007/s00468-014-1081-3
Hernández Hernández, R., Pérez, V., Sanchez, G., Castella, J., and Palencia, J. (2004). Ensayos de atracción captura de Ips acuminatus (Coleoptera: Scolytidae). Ecología 18, 35–52.
Hernández Hernández, R., Pérez, V., Sánchez, G., Castella, J., Palencia, J., Gil, J. M., et al. (2007). Ensayos de trampeo de escolítidos perforadores subcorticales en pinares mediante el uso de feromonas 2002-2005. Ecología 21, 43–56.
Hlásny, T., Zimová, S., Merganičová, K., Štěpánek, P., Modlinger, R., and Turčáni, M. (2021). Devastating outbreak of bark beetles in the Czech Republic: drivers, impacts, and management implications. For. Ecol. Manage. 490, 1–13. doi: 10.1016/j.foreco.2021.119075
Hódar, J. A., Castro, J., and Zamora, R. (2003). Pine processionary caterpillar Thaumetopoea pityocampa as a new threat for relict Mediterranean Scots pine forests under climatic warming. Biol. Conserv. 110, 123–129. doi: 10.1016/S0006-3207(02)00183-0
Holuša, J., Lubojacký, J., and Knížek, M. (2010). Distribution of double-spined spruce bark beetle Ips duplicatus in the Czech Republic: spreading in 1997-2009. Phytoparasitica 38, 435–443. 0121-9 doi: 10.1007/s12600-010-0121-9
Horn, A., Kerdelhué, C., Lieutier, F., and Rossi, J.-P. (2012). Predicting the distribution of the two bark beetles Tomicus destruens and Tomicus piniperda in Europe and the Mediterranean region. Agric. For. Entomol. 14, 358–366. doi: 10.1111/j.1461-9563.2012.00576.x
Horn, A., Roux-Morabito, G., Lieutier, F., and Kerdelhué, C. (2006). Phylogeographic structure and past history of the circum-Mediterranean species Tomicus destruens Woll. (Coleoptera: Scolytinae). Mol. Ecol. 15, 1603–1615. doi: 10.1111/j.1365-294X.2006.02872.x
Horn, A., Stauffer, C., Lieutier, F., and Kerdelhué, C. (2009). Complex postglacial history of the temperate bark beetle Tomicus piniperda L. (Coleoptera, Scolytinae). Heredity 103, 238–247. doi: 10.1038/hdy.2009.48
Houston Durrant, T., de Rigo, D., and Caudullo, G. (2016). “Pinus sylvestris in Europe: distribution, habitat, usage and threats,” in European Atlas of Forest Tree Species, eds J. San-Miguel-Ayanz, D. de Rigo, G. Caudullo, T. Houston Durrant, and A. Mauri (Luxembourg: Publication Office of the European Union).
Hui, Y., and Xue-Song, D. (1999). Impacts of Tomicus minor on distribution and reproduction of Tomicus piniperda (Col., Scolytidae) on the trunk of the living Pinus yunnanensis trees. J. Appl. Entomol. 123, 329–333. doi: 10.1046/j.1439-0418.1999.00353.x
IPCC. (2007). “Climate Change 2007: The Physical Science Basis,” in Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, eds S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, et al. (New York, NY: Cambridge University Press).
IPCC. (2014). “Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects,” in Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, eds V. R. Barros, C. B. Field, D. J. Dokken, and M. D. Mastrandre (New York, NY: Cambridge University Press).
Jactel, H., and Lieutier, F. (1987). Effects of attack density on fecundity of the Scots pine beetle Ips sexdentatus Boern (Col.; Scolytidae). J. Appl. Entomol. 104, 190–204. doi: 10.1111/j.1439-0418.1987.tb00515.x
Jonášová, M., and Prach, K. (2004). Central-European Mountain spruce (Picea abies (L.) Karst.) forests: regeneration of tree species after a bark beetle outbreak. Ecol. Eng. 23, 15–27. doi: 10.1016/j.ecoleng.2004.06.010
Jönsson, A. M., Appelberg, G., Harding, S., and Bärring, L. (2009). Spatio-temporal impact of climate change on the activity and voltinism of the spruce bark beetle, Ips typographus. Glob. Chang. Biol. 15, 486–499. doi: 10.1111/j.1365-2486.2008.01742.x
Jönsson, A. M., Harding, S., Krokene, P., Lange, H., Lindelow, A., Okland, B., et al. (2011). Modelling the potential impact of global warming on Ips typographus voltinism and reproductive diapause. Clim. Chang. 109, 695–718. doi: 10.1007/s10584-011-0038-4
Karlsson, B. (2014). Extended season for northern butterflies. Int. J. Biometeorol. 58, 691-701. doi: 10.1007/s00484-013-0649-8
Kelsey, R. G., Gallego, D., Sánchez-García, F. J., and Pajares, J. A. (2014). Ethanol accumulation during severe drought may signal tree vulnerability to detection and attack by bark beetles. Can. J. For. Res. 44, 554-561. doi: 10.1139/cjfr-2013-0428
Kerdelhué, C., Roux-Morabito, G., Forichon, J., Chambon, J.-M., Robert, A., and Lieutier, F. (2002). Population genetic structure of Tomicus piniperda L. (Curculionidae: Scolytinae) on different pine species and validation of T. destruens (Woll.). Mol. Ecol. 11, 483–494. doi: 10.1046/j.0962-1083.2002.01460.x
Kharouba, H. M., Paquette, S. R., Kerr, J. T., and Vellend, M. (2014). Predicting the sensitivity of butterfly phenology to temperature over the past century. Glob. Chang. Biol. 20, 504–514. doi: 10.1111/gcb.12429
Kirkendall, L. R. (1989). Within-harem competition among Ips females, an overlooked component of density-dependent larval mortality. Ecography 12, 477–487. doi: 10.1111/j.1600-0587.1989.tb00925.x
Kirkendall, L. R. (1990). Sperm is a limiting resource in the pseudogamous bark beetle Ips acuminatus (Scolytidae). Oikos 57:80. doi: 10.2307/3565740
Knížek, M. (1998). Lýkohub sosnový. Tomicus piniperda (L.). Lýkohub menší. Tomicus minor (Hartig). Lesnická práce 77, 1–4.
Knížek, M., Liška, J., Lubojacký, F., Véle, A., and Zahradník, P. (2020). Význam biotických škodlivých činitelů borovice lesní,” in Škodliví Činitelé v Lesích Česka 2019/2020 - Krize Zdravotního Stavu Borovice Lesní. Sborník Referátů Z Celostátního Semináře S Mezinárodní Účastí. Czech Republic: Zpravodaj ochrany lesa, 16–21.
Kohlmayr, B., Riegler, M., Wegensteiner, R., and Stauffer, C. (2002). Morphological and genetic identification of the three pine pests of the genus Tomicus (Coleoptera, Scolytidae) in Europe. Agric. For. Entomol. 4, 151–157. doi: 10.1046/j.1461-9563.2002.00139.x
Kohnle, U. (2004). Host and non-host odour signals governing host selection by the pine shoot beetle, Tomicus piniperda and the spruce bark beetle, Hylurgops palliatus (Col., Scolytidae). J. Appl. Entomol. 128, 588–592. doi: 10.1111/j.1439-0418.2004.00898.x
Kohnle, U., Meyer, M., and Kluber, J. (1992). Formulation of population attractant for the pine bark beetle, Ips sexdentatus (Col, Scolytidae). Allgemeine Forst Und Jagdzeitung. 163, 81–87.
Kolb, T. E., Fettig, C. J., Ayres, M. P., Bentz, B. J., Hicke, J. A., Mathiasen, R., et al. (2016). Observed and anticipated impacts of drought on forest insects and diseases in the United States. For. Ecol. Manage. 380, 321–334. doi: 10.1016/j.foreco.2016.04.051
Krams, I., Daukšte, J., Kivleniece, I., Brūmelis, G., Cibuļskis, R., Āboliņš-Ābols, M., et al. (2012). Drought-induced positive feedback in xylophagous insects: Easier invasion of Scots pine leading to greater investment in immunity of emerging individuals. For. Ecol. Manage. 270, 147–152. doi: 10.1016/j.foreco.2012.01.012
Łabêdzki, A. (1993). Nowa plaga naszych lasów. Przypłaszczek granatek. Przegląd Leoeniczy. 2, 14–15.
Långström, B. (1983). Life cycles and shoot-feeding of pine shoot beetles. Stud. For. Suec. 163, 1–29.
Långström, B. (1984). Windthrown Scots pines as brood material for Tomicus piniperda and T. minor. Silva Fenn. 18, 187–198. doi: 10.14214/sf.a15392
Långström, B., and Hellqvist, C. (1991). Shoot damage and growth losses following three years of Tomicus-attacks in Scots pine stands close to a timber storage site. Silva Fenn. 25:604. doi: 10.14214/sf.a15604
Långström, B., Annila, E., Hellqvist, C., Varama, M., and Niemelä, P. (2001). Tree mortality, needle biomass recovery and growth losses in Scots pine following defoliation by Diprion pini (L.) and subsequent attack by Tomicus piniperda (L.). Scand. J. For. Res. 16, 342–353. doi: 10.1080/02827580118325
Långström, B., Lisha, L., Hongpin, L., Peng, C., Haoran, L., Hellqvist, C., et al. (2002). Shoot feeding ecology of Tomicus piniperda and T. minor (Col., Scolytidae) in Southern China. J. Appl. Entomol. 126, 333–342. doi: 10.1046/j.1439-0418.2002.00651.x
Långström, B., Tenow, O., Ericsson, A., Hellqvist, C., and Larsson, S. (1990). Effects of shoot pruning on stem growth, needle biomass, and dynamics of carbohydrates and nitrogen in Scots pine as related to season and tree age. Can. J. For. Res. 20, 514–523. doi: 10.1139/x90-068
Lanne, B. S., Schlyter, F., Byers, J. A., Löfqvist, J., Leufvén, A., Bergström, G., et al. (1987). Differences in attraction to semiochemicals present in sympatric pine shoot beetles, Tomicus minor and T. piniperda. J. Chem. Ecol. 13, 1045–1067. doi: 10.1007/BF01020537
Lantschner, M. V., Atkinson, T. H., Corley, J. C., and Liebhold, A. M. (2017). Predicting North American Scolytinae invasions in the Southern Hemisphere. Ecol. Appl. 27, 66–77. doi: 10.1002/eap.1451
Lee, J. C., Smith, S. L., and Seybold, S. J. (2005). Mediterranean Pine Engraver.” in Pest Alert R5-PR-016. Berkeley, CA: US Department of Agriculture, 1–4.
Lehmann, P., Ammunét, T., Barton, M., Battisti, A., Eigenbrode, S. D., Jepsen, J. U., et al. (2020). Complex responses of global insect pests to climate warming. Front. Ecol. Environ. 18:141–150. doi: 10.1002/fee.2160
Lekander, B. (1971). On Blastophagus destruens Woll. and a description of its larva (Col. Scolytidae). Entomol. Tidskr. 92, 271–276.
Lekander, B., Bejer-Petersen, B., Kangas, E., and Bakke, A. (1977). The distribution of bark beetles in the Nordic Countries. Entomol. Fenn. 32, 1–36.
Lentini, A., Coinu, M., and Luciano, P. (2015). Biological studies on Tomicus destruens (Wollaston) (Coleoptera Curculionidae Scolytinae): Phenology, voltinism and sister broods. Redia 108, 37–47.
Lévieux, J., Lieutier, F., and Delplanque, A. (1985). Les scolytes ravageurs du pin sylvestre. R.F.F. 6, 431–440. doi: 10.4267/2042/21835
Liebhold, A. M., Brockerhoff, E. G., Kalisz, S., Nuñez, M. A., Warde, D. A., and Wingfield, M. J. (2017). Biological Invasions in forest ecosystems. Biol. Invas. 19, 3437–3458. doi: 10.1007/s10530-017-1458-5
Liebhold, A. M., MacDonald, W. L., Bergdahl, D., and Mastro, V. C. (1995). Invasion by exotic forest pests: a threat to forest ecosystems. For. Sci. 41:a0001. doi: 10.1093/forestscience/41.s1.a0001
Liebhold, A. M., McCullough, D. G., Blackburn, L. M., Frankel, S. J., Von Holle, B., and Aukema, J. E. (2013). A highly aggregated geographical distribution of forest pest invasions in the USA. Dive. Distrib. 19, 1208–1216. doi: 10.1111/ddi.12112
Lieutier, F., and Paine, T. D. (2016). “Responses of Mediterranean forest phytophagous insects to climate change,” in Insects and Diseases of Mediterranean Forest Systems, eds D. T. Paine and F. Lieutier (Berlin: Springer), 801–858. doi: 10.1007/978-3-319-24744-1_28
Lieutier, F., Day, K. R., Battisti, A., Grégoire, J. C., and Evans, H. F. (2004). Bark and Wood Boring Insects in Living Trees in Europe, a Synthesis. Dordecht: Springer. doi: 10.1007/978-1-4020-2241-8
Lieutier, F., Garcia, J., Yart, A., Vouland, G., Pettinetti, M., and Morelet, M. (1991). Ophiostomatales (Ascomycètes) associées à Ips acuminatus Gyll (Coleoptera: Scolytidae) sur le pin sylvestre (Pinus sylvestris L) dans le Sud-Est de la France et comparaison avec Ips sexdentatus Boern. Agronomie 11, 807–817. doi: 10.1051/agro:19910911
Lieutier, F., Ghaioule, D., Yart, A., and Sauvard, D. (2002). Attack behavior of pine bark beetles in Morocco and association with phytopathogenic fungi. Ann. Rech. For. Maroc. 35, 96–109.
Lieutier, F., Långström, B., and Faccoli, M. (2015). “Chapter 10. The Genus Tomicus,” in Bark Beetles: Biology and ecology of native and invasive species, eds F. E. Vega and R. W. Hofstetter (Amsterdam: Elsevier Academic Press), 371–426. doi: 10.1016/B978-0-12-417156-5.00010-1
Lieutier, F., Yart, A., and Salle, A. (2009). Stimulation of tree defenses by Ophiostomatoid fungi can explain attack success of bark beetles on conifers. Ann. For. Sci. 66, 801–801. doi: 10.1051/forest/2009066
Lindelöw, A., Isacsson, G., Ravn, H. P., and Schroeder, M. (2015). Tetropium gabrieli and Ips cembrae (Coleoptera; Cerambycidae and Curculionidae) - invasion of two potential pest species on larch in Sweden. Entomol. Tidskr. 136, 103–112.
Lindner, M., Maroschek, M., Netherer, S., Kremer, A., Barbati, A., Garcia-Gonzalo, J., et al. (2010). Climate change impacts, adaptive capacity, and vulnerability of European forest ecosystems. For. Ecol. Manage. 259, 698–709. doi: 10.1016/j.foreco.2009.09.023
Lindsey, R., and Dahlman, L. (2022). Climate Change: Global Temperature. https://www.climate.gov/news-features/understanding-climate/climate-change-global-temperature (accessed May 17, 2022).
Lingren, B. S., Miller, D. R., and LaFontaine, J. P. (2012). MCOL, frontalin and ethanol: a potential operational trap lure for Douglas-fir beetle in British Columbia. Entomol. Soc. Br. Columb. 109, 71–73.
Logan, J. A., Régnière, J., and Powell, J. A. (2003). Assessing the impacts of global warming on forest pest dynamics. Front. Ecol. Environ. 1:130–137. doi: 10.1890/1540-9295(2003)001[0130:ATIOGW]2.0.CO;2
López-Goldar, X., Villari, C., Bonello, P., Borg-Karlson, A. K., Grivet, D., Zas, R., et al. (2018). Inducibility of plant secondary metabolites in the stem predicts genetic variation in resistance against a key insect herbivore in maritime pine. Front. Plant Sci. 9:1651. doi: 10.3389/fpls.2018.01651
Løyning, M. K. (2000). Reproductive performance of clonal and sexual bark beetles (Coleoptera: Scolytidae) in the field. J. Evol. Biol. 13, 743–748. doi: 10.1046/j.1420-9101.2000.00227.x
Løyning, M. K., and Kirkendall, L. R. (1996). Mate discrimination in a pseudogamous bark beetle (Coleoptera: Scolytidae): Male Ips acuminatus prefer sexual to clonal females. Oikos 77:336. doi: 10.2307/3546074
Lozovoj, D. I. (1965). Insect pests of park and forest plantations in Georgia SSR. Tbilisi: Izd-vo Akademii nauk Gruzinskoi SSR.
Lozovoj, D. I. (1966). Hozjajstvenno vaznye vidy koroedov hvojnyh (elovyh) nasazdenij Gruzii i mery bor’by s nimi. [Economically important species of bark beetles in the conifer (Spruce) stands of Soviet Georgia, and their control]. Tbilisi: USSR.
Lubojacký, J., Lorenc, F., Liška, J., and Knížek, M. (2019). “Hlavní problémy v ochranë lesa v Česku v roce 2018 a prognóza na rok 2019,” in Škodliví činitelé v lesích Česka 2018/2019 - Historie a současnost kůrovcových kalamit ve střední Evropë. Sborník referátů z celostátního semináře s mezinárodní účastí. Průhonice, ed. M. Knížek (Czech Republic: Zpravodaj ochrany lesa).
Lungren, J. G. (2004). Exotic forest pest information system for North America: Tomicus minor. https://www.invasive.org/species/list.cfm?id=5 (accessed November 10, 2021).
Lusebrink, I., Erbilgin, N., and Evenden, M. L. (2016). The effect of water limitation on volatile emission, tree defense response, and brood success of Dendroctonus ponderosae in two pine hosts, lodgepole, and jack pine. Front. Ecol. Evol. 4:2. doi: 10.3389/fevo.2016.00002
Luterek, R. (1996). Podstawowe szkodniki owadzie drzewostanów popoźarowych Puszczy Noteckiej. Prace Komisji Nauk Rolniczych I Leoenych. Poznañ. PTN. 82, 103–110.
MacLean, S. F. (1983). Life cycles and the distribution of Psyllids (Homoptera) in Arctic and Subarctic Alaska. Oikos 40:445. doi: 10.2307/3544317
Majunke, C. (1995). Zur Bedeutung nadelfressender und stammbrütender Forstinsekten im nordostdeutschen Tiefland. Mitt. Dtsch. Ges. allg. angew. Entomol. 10, 71–77.
Markalas, S. (1997). Frequency and distribution of insect species on trunks in burnt pine forests of Greece. J. Swiss Entomol. Soc. 70, 57–61. doi: 10.1007/BF01996922
Marqués, L., Ogle, K., Peltier, D. M. P., and Camarero, J. J. (2022). Altered climate memory characterizes tree growth during forest dieback. Agric. For. Meteorol. 314, 1–12. doi: 10.1016/j.agrformet.2021.108787
Martínez-Vilalta, J., and Piñol, J. (2002). Drought-induced mortality and hydraulic architecture in pine populations of the NE Iberian Peninsula. For. Ecol. Manage. 161, 247–256. doi: 10.1016/S0378-1127(01)00495-9
Masutti, L. (1969). Pinete dei litorali e Blastophagus piniperda L. una difficile convivenza [Pine stands of the [Adriatic] coast and Blastophagus [Myelophilus] piniperda: a bad combination.]. Monte E. Boschi. 20, 15–27.
Mathiesen, A. (1950). Über einige Borkenkäfern assoziierte Bläuepilze in Schweden. Oikos 2, 275–308. doi: 10.2307/3564798
Mátyás, C., Ackzell, L., and Samuel, C. J. A. (2004). EUFROGEN Technical guidelines for genetic conservation and use for Scots pine (Pinus sylvestris). Rome: International Plant Genetic Resources Institute.
Mayr, E. (1963). Animal species and evolution. Cambridge, MA: Harvard Univiversity Press. doi: 10.4159/harvard.9780674865327
McDowell, N. G., Beerling, D. J., Breshears, D. D., Fisher, R. A., Raffa, K. F., and Stitt, M. (2011). The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends. Ecol. Evol. 26, 523–532. doi: 10.1016/j.tree.2011.06.003
Mendel, Z. (1983). Seasonal history of Orthotomicus erosus (Coleoptera:Scolytidae) in Israel. Phytoparasitica 11, 13–24. doi: 10.1007/BF02980707
Mendel, Z. (1988a). “The relation of bast scale and bark beetle outbreaks to management of pine plantations in Israel,” in XVII International Congress of Entomology, Proceedings of the IUFRO working party, eds T. L. Payne and H. Saarenmaa (Vancouver, BC), 329–335.
Mendel, Z. (1988b). Attraction of Orthotomicus erosus and Pityogenes calcaratus to a synthetic aggregation pheromone of Ips typographus. Phytoparasitica 16, 109–117. doi: 10.1007/BF02980465
Mendel, Z., and Halperin, J. (1982). The biology and behaviour of Orthotomicus erosus in Israel. Phytoparasitica 10, 169–181. doi: 10.1007/BF02994526
Mendel, Z., Boneh, O., Shenhar, Y., and Riov, J. (1991). Diurnal flight patterns of Orthotomicus erosus and Pityogenes calcaratus in Israel. Phytoparasitica 19, 23–31. doi: 10.1007/BF02981008
Mendel, Z., Madar, Z., and Golan, Y. (1985). Comparison of the seasonal occurrence and behavior of seven pine bark beetles (Coleoptera. Scolytidae) in Israel. Phytoparasitica 13, 21–32. doi: 10.1007/BF02994434
Mendel, Z., Madar, Z., and Golan, Y. (1986). Hymenopterous parasitoids of pine bark beetles in Israel. Hasadeh 66, 1899–1901.
Miller, D. R., and Rabaglia, R. J. (2009). Ethanol and (-)-α-pinene: Attractant kairomones for bark and ambrosia beetles in the southeastern US. J. Chem. Ecol. 35, 435–448. doi: 10.1007/s10886-009-9613-9
Mitton, J. B., and Ferrenberg, S. M. (2012). Mountain pine beetle develops an unprecedented summer generation in response to climate warming. Am. Nat. 179, E163–E171. doi: 10.1086/665007
Monleón, A., Blas, M., and Riba, J. M. (1996). Biology of Tomicus destruens (Wollaston, 1865) (Coleoptera: Scolytidae) in the Mediterranean forest. Elytron 10, 161–167.
Moreira, X., Sampedro, L., and Zas, R. (2009). Defensive responses of Pinus pinaster seedlings to exogenous application of methyl jasmonate: concentration effect and systemic response. Environ. Exp. Bot. 67, 94–100. doi: 10.1016/j.envexpbot.2009.05.015
Moreno-Gutiérrez, C., Dawson, T. E., Nicolás, E., and Querejeta, J. I (2012). Isotopes reveal contrasting water use strategies among coexisting plant species in a Mediterranean ecosystem. New Phytol. 196, 489–496. doi: 10.1111/j.1469-8137.2012.04276.x
Mrkva, R. (1995). Nové poznatky o bionomii, ekologii a hubení lýkožrouta severského. Lesnická práce. 74, 5–7.
Mühle, H. (1993). Melanophila Eschscholtz, 1829 and Phaenops Dejean, 1833 (Insecta, Coleoptera): proposed conservation of usage by the designation of Buprestis acuminata De Geer, 1774 as the type species of Melanophila. Bull. Zool. Nomencl. 50, 31–34. doi: 10.5962/bhl.part.1786
Nanni, C., and Tiberi, R. (1997). “Integrating cultural tactics into the management of bark beetle and reforestation pests,” in (ed). A.M. Liebhold, F.M. Stephen, K.R. Day, and S.M. Salom (Radnor, PA: US Department of Agriculture), 131–134.
Netherer, S., and Schopf, A. (2010). Potential effects of climate change on insect herbivores in European forests - General aspects and the pine processionary moth as specific example. For. Ecol. Manage. 259, 831-838. doi: 10.1016/j.foreco.2009.07.034
Netherer, S., Matthews, B., Katzensteiner, K., Blackwell, E., Henschke, P., Hietz, P., et al. (2015). Do water-limiting conditions predispose Norway spruce to bark beetle attack? New Phytol. 205, 1128–1141. doi: 10.1111/nph.13166
Niemelä, P., and Mattson, W. J. (1996). Invasion of North American forests by European phytophagous insects. BioScience 46, 741–753. doi: 10.2307/1312850
Noaa. (2022). National Centers for Environmental Information, State of the Climate: Monthly Global Climate Report for April 2022. https://www.ncei.noaa.gov/access/monitoring/monthly-report/global/202204/supplemental/page-1. (accessed May 17, 2022).
Öhrn, P., Björklund, N., and Långström, B. (2018). Occurrence, performance and shoot damage of Tomicus piniperda in pine stands in Southern Sweden after storm-felling. J. Appl. Entomol. 142, 854–862. doi: 10.1111/jen.12533
Økland, B., Erbilgin, N., Skarpaas, O., Christiansen, E., and Långström, B. (2011). Inter-species interactions and ecosystem effects of non-indigenous invasive and native tree-killing bark beetles. Biol. Invasions. 13, 1151–1164. doi: 10.1007/s10530-011-9957-2
Økland, B., Flo, D., Schroeder, M., Zach, P., Cocos, D., Martikainen, P., et al. (2019). Range expansion of the small spruce bark beetle Ips amitinus: a newcomer in northern Europe. Agr. Forest Entomol. 21, 286–298. doi: 10.1111/afe.12331
Olenici, N., Duduman, M.-L., Olenici, V., Bouriaud, O., Tomescu, R., and Rotariu, C. (2010). “The first outbreak of Ips duplicatus (Coleoptera, Curculionidae, Scolytinae) in Romania. Methodology of Forest Insect and Disease Survey in Central Europe,” in Proceedings of the 10th IUFRO Workshop of WP 7.03.10 September 20-23, 2010), eds H. Delb and S. Pontuali (Freiburg: Fakultät für Forst- und Umweltwissenschaften der Albert-Ludwigs-Universität and Forstliche Versuchs- und Forschungsanstalt (FVA)), 135–140.
Oliva, J., Boberg, J. B., Hopkins, A. J. M., and Stenlid, J. (2013). “Concepts of epidemiology of forest diseases,” in Infectious forest diseases, eds P. Gonthier and G. Nicolotti (Oxfordshire: CABI International), 1–28. doi: 10.1079/9781780640402.0001
Ostry, M. E., Venette, R. C., and Juzwik, J. (2011). Decline as a disease category: Is it helpful? Phytopathology 101, 404–409. doi: 10.1094/PHYTO-06-10-0153
Özcan, G. E. (2011). Use of pheromone-baited traps for monitoring Ips sexdentatus (Boerner) (Coleoptera: Curculionidae) in oriental spruce stands. Afr. J. Biotechnol. 10:1709. doi: 10.5897/AJB11.1709
Özcan, G. E. (2017). Assessment of Ips sexdentatus population considering the capture in pheromone traps and their damages under non-epidemic conditions. Šumarski List 141, 47–56. doi: 10.31298/sl.141.1-2.5
Paine, T. D., Steinbauer, M. J., and Lawson, S. A. (2011). Native and exotic pests of Eucalyptus: a worldwide perspective. Annu. Rev. Entomol. 56, 181–201. doi: 10.1146/annurev-ento-120709-144817
Paiva, M. R. (1994). “Population trends and olfactory responses of Scolytid species and their predators on Pinus pinaster Ait. Behaviour, population dynamics and control of forest insects,” in Proceedings of the IUFRO Joint Conference, eds F. P. Hain, S. M. Salom, W. R. Ravlin, T. L. Payne, and K. F. Raffa (Hawaii: Maui), 45–58.
Paiva, M. R., Pessoa, M., and Vité, J. P. (1988). Reduction in the pheromone attractant response of Orthotomicus erosus (Woll.) and Ips sexdentatus Boern. (Col., Scolytidae). J. Appl. Ent. 106, 198–200. doi: 10.1111/j.1439-0418.1988.tb00583.x
Parmesan, C., Duarte, C., Poloczanska, E., Richardson, A. J., and Singer, M. C. (2011). Overstretching attribution. Nat. Clim. Chan. 1, 2–4. doi: 10.1038/nclimate1056
Pérez, G., and Sierra, J. M. (2006). Efficacia de cebos atrayentes y trapas en el controlo de Ips acuminatus (Coleoptera: Scolytidae). Bol. Sanid. Veg. Plagas. 32, 259–266.
Pernek, M., Lacković, N., Lukić, I., Zorić, N., and Matošević, D. (2019). Outbreak of Orthotomicus erosus (Coleoptera, Curculionidae) on Aleppo pine in the Mediterranean region in Croatia. Southeast Eur. For. 10, 19–27. doi: 10.15177/seefor.19-05
Pernek, M., Novak Agbaba, S., Lacković, N., Dod, N., Lukić, I., and Wirth, S. (2012). The role of biotic factors on pine (Pinus spp.) decline in north Dalmatia. Šumarski List. 136, 343–354.
Perz, S., and Ciesielski, S. (1993). Kontrola wystêpowania przypłaszczka granatka (Phaenops cyanea Fabr.). Przegląd Leoeniczy 3, 6–7.
Pešková, V., Soukup, F., and Knížek, M. (2016). Biotičtí škodliví činitelé na borovici a sucho. Lesnická Práce 4, 1–8.
Péter, S. (2014). Effect of climate change on population dynamics of bark beetles: relationships between temperature and development rate of Ips sexdentatus (Boern.). [dissertation thesis]. Metz: Biology and Ecology for Forest.
Petrice, T. R., Haack, R. A., and Poland, T. M. (2002). Selection of overwintering sites by Tomicus piniperda (Coleoptera: Scolytidae) during fall shoot departure. J. Entomol. Sci. 37, 48–59. doi: 10.18474/0749-8004-37.1.48
Pfeffer, A. (1995). Zentral- und westpaläarktische Borken- und Kernkäfer (Coleoptera: Scolytidae, Platypodidae). Entomologia: Naturhistorisches Museum Basel.
Pfeffer, A., and Knížek, M. (1995). Expanze lýkožrouta Ips duplicatus (Sahlb.) ze severské tajgy. Zpravodaj ochrany lesa, 1995, 8–11.
Pimentel, D. (1993). “Habitat factors in new pest invasions,” in Evolution of insect pests: patterns of variation, eds K. C. Kim and B. A. McPheron (New York, NY: John Wiley and Sons, INC).
Pitman, G. B., Hedden, R. L., and Gara, R. I. (1975). Synergistic effects of ethyl alcohol on the aggregation of Dendroctonus pseudotsugae (Col., Scolytidae) in response to pheromones. Zeitschrift Für Angewandte Entomologie 78, 203–208. doi: 10.1111/j.1439-0418.1975.tb04172.x
Poland, T. M., and Haack, R. A. (2000). Tomicus piniperda (Coleoptera: Scolytidae): Is shoot-feeding required for reproductive maturation? Great Lakes Entomol. 33, 9–15.
Powell, J. A., and Bentz, B. J. (2009). Connecting phenological predictions with population growth rates for mountain pine beetle, an outbreak insect. Landsc. Ecol. 24, 657–672. doi: 10.1007/s10980-009-9340-1
Powell, J. A., and Bentz, B. J. (2014). Phenology and density-dependent dispersal predict patterns of mountain pine beetle (Dendroctonus ponderosae) impact. Ecol. Modell. 273, 173–185. doi: 10.1016/j.ecolmodel.2013.10.034
Raffa, K. F., Aukema, B. H., Bentz, B. J., Carroll, A. L., Hicke, J. A., Turner, M. G., et al. (2008). Cross-scale drivers of natural disturbances prone to anthropogenic amplification: dynamics of biome-wide bark beetle eruptions. Bioscience 58, 501–517. doi: 10.1641/B580607
Raffa, K. F., Aukema, B. H., Bentz, B. J., Carroll, A. L., Hicke, J. A., and Kobl, T. E. (2015). “Responses of tree-killing bark beetles to a changing climate,” in Climate change and insect pests, eds C. Björkman and P. Niemel (Madison, WI: University of Wisconsin), 173–201. doi: 10.1079/9781780643786.0173
Ramegowda, V., and Senthil-Kumar, M. (2015). The interactive effects of simultaneous biotic and abiotic stresses on plants: mechanistic understanding from drought and pathogen combination. J. Plant Physiol. 176, 47-54. doi: 10.1016/j.jplph.2014.11.008
Régnière, J., and Bentz, B. (2007). Modeling cold tolerance in the mountain pine beetle, Dendroctonus ponderosae. J. Insect. Physiol. 53, 559–572. doi: 10.1016/j.jinsphys.2007.02.007
Rigling, A., and Cherubini, P. (1999). Wieso sterben die Waldföhren im “TeIwald” bei Visp? Eine Zusammenfassung bisheriger Studien und eine dendroökologische Untersuchung [What is the Cause of the High Mortality Rates of the Scots Pines in the “Telwald” near Visp (Switzerland)? A Summary of Previous Studies and a Dendroecological Study]. Schweiz. Z. Forstwes. 150, 113–131. doi: 10.3188/szf.1999.0113
Romón, P., Aparicio, D., Palacios, F., Iturrondobeitia, J. C., Hance, T., and Goldarazena, A. (2017). Seasonal terpene variation in needles of Pinus radiata (Pinales: Pinaceae) trees attacked by Tomicus piniperda (Coleoptera: Scolytinae) and the effect of limonene on beetle aggregation. J. Insect. Sci. 17:66. doi: 10.1093/jisesa/iex066
Rosenberger, D. W., Aukema, B. H., and Venette, R. C. (2017a). Cold tolerance of mountain pine beetle among novel eastern pines: a potential for trade-offs in an invaded range? For. Ecol. Manage. 400, 28–37. doi: 10.1016/j.foreco.2017.05.031
Rosenberger, D. W., Venette, R. C., Maddox, M. P., and Aukema, B. H. (2017b). Colonization behaviors of mountain pine beetle on novel hosts: Implications for range expansion into northeastern North America. PLoS One 12:e0176269. doi: 10.1371/journal.pone.0176269
Roy, D. B., Oliver, T. H., Botham, M. S., Beckmann, B., Brereton, T., Dennis, R. L. H., et al. (2015). Similarities in butterfly emergence dates among populations suggest local adaptation to climate. Glob. Chang. Biol. 21, 3313–3322. doi: 10.1111/gcb.12920
Ruiz, C., and Lanfranco, D. M. (2008). Los escarabajos de corteza en Chile: Una revision de la situaciôn actual e implicancias en el comercio intemacional. Bosque 29, 109–114. doi: 10.4067/S0717-92002008000200002
Russo, G. (1940). Il blastofago del pino (Blasophagus (Myelophilus) piniperda L. var. rubripennis Reitter). R. Laboratorio di Entomologia Agraria 19, 1–13.
Ryall, K. L., and Smith, S. M. (2000). Brood production and shoot feeding by Tomicus piniperda (Coleoptera: Scolytidae). Can. Entomol. 132, 939–949. doi: 10.4039/Ent132939-6
Saarenmaa, H. (1983). Modeling the spatial pattern and intra- specific competition in Tomicus piniperda (Coleoptera, Scolytidae). Commun. Inst. For. Fenn. 1983:40.
Sabbatini Peverrieri, G., Faggi, M., Marziali, L., and Tiberi, R. (2008). Life cycle of Tomicus destruens in a pine forest of central Italy. Bull. Insectol. 61, 337–342.
Sallé, A., Nageleisen, L.-M., and Lieutier, F. (2014). Bark and wood boring insects involved in oak declines in Europe: current knowledge and future prospects in a context of climate change. For. Ecol. Manage. 328, 79–93. doi: 10.1016/j.foreco.2014.05.027
Sampedro, L., Moreira, X., and Zas, R. (2011). Resistance and response of Pinus pinaster seedlings to Hylobius abietis after induction with methyl jasmonate. Plant Ecol. 212, 397–401. doi: 10.1007/s11258-010-9830-x
Sangüesa-Barreda, G., Linares, J. C., and Camarero, J. J. (2015). Reduced growth sensitivity to climate in bark-beetle infested Aleppo pines: connecting climatic and biotic drivers of forest dieback. For. Ecol. Manage. 357, 126–137. doi: 10.1016/j.foreco.2015.08.017
Santini, L., and Prestininzi, M. (1991). Il Tomicus destruensnelle Pinete tosco-laziali: biologia e possibilità dicontrollo,” in Giornate di studio sulle avversità del pino. Bologna: Tipografia Moderna, 232–241.
Sarıkaya, O. (2008). Batı Akdeniz Bölgesi İğneyapraklı Ormanlarının Scolytidae (Coleoptera) Faunası. [dissertation thesis]. Isparta: Süleyman Demirel Üniversitesi, Fen Bilimleri Enstitüsü.
Sarıkaya, O., and Avci, M. (2010). Distribution and biology of the Mediterranean pine shoot beetle Tomicus destruens (Wollaston, 1865) in the western Mediterranean region of Turky. Türk. Entomol. Derg. 34, 289–298.
Sarıkaya, O., and Şen, I. (2017). Population genetic structure of Orthotomicus erosus (Wollaston, 1857) (Coleoptera: Curculionidae, Scolytinae) in pine forests of the Mediterranean Region of Turkey. Appl. Ecol. Env. Res. 15, 915–928. doi: 10.15666/aeer/1504_915928
Sarıkaya, O., Ibis, H. M., and Toprak, O. (2013). The flight activity and population density of Orthotomicus erosus (Wollaston, 1857) in the Brutian pine (Pinus brutia Ten.) forests of Ízmir Province, Turkey. Int. J. Sci. Basic Appl. 12, 208–219.
Sato, Y., and Sato, S. (2015). Spring temperature predicts the long-term molting phenology of two cicadas, Cryptotympana facialis and Graptopsaltria nigrofuscata (Hemiptera: Cicadidae). Ann. Entomol. Soc. Am. 108, 494–500. doi: 10.1093/aesa/sav036
Saunders, D. S. (2014). Insect photoperiodism: effects of temperature on the induction of insect diapause and diverse roles for the circadian system in the photoperiodic response. Entomol. Sci. 17, 25–40. doi: 10.1111/ens.12059
Schebeck, M., and Schopf, A. (2017). Temperature-dependent development of the European larch bark beetle, Ips cembrae. J. Appl. Entomol. 141, 322–328. doi: 10.1111/jen.12351
Schebeck, M., Dobart, N., Ragland, G. J., Schopf, A., and Stauffer, C. (2021). Facultative and obligate diapause phenotypes in populations of the European spruce bark beetle Ips typographus. J. Pest. Sci. 2021, 1–11. doi: 10.1007/s10340-021-01416-w
Schebeck, M., Matthew Hansen, E., Schopf, A., Ragland, G. J., Stauffer, C., and Bentz, B. J. (2017). Diapause and overwintering of two spruce bark beetle species. Phisiol. Entomol. 42, 200–210. doi: 10.1111/phen.12200
Schelhaas, M.-J., Nabuurs, G.-J., and Schuck, A. (2003). Natural disturbances in the European forests in the 19th and 20th centuries. Glob. Chang. Biol. 9, 1620–1633. doi: 10.1046/j.1365-2486.2003.00684.x
Schopf, A. (1985). Zum Einfluss der Photoperiode auf die Entwicklung und Kältresistenz des Buchdruckers, Ips typographus (L.) (Coleoptera: Scolytidae). Anz. Schädlingskde, Pflanzensch Umweltsch. 58, 73–75. doi: 10.1007/BF01903228
Schopf, A. (1989). Die Wirkung der Photoperiode auf die Induktion der Imaginaldiapause von Ips typographus (L.) (Coleoptera: Scolytidae). J. Appl. Ent. 107, 275–288. doi: 10.1111/j.1439-0418.1989.tb00257.x
Schroeder, L. M. (1997). Oviposition behavior and reproductive success of the cerambycid Acanthocinus aedilis in the presence and absence of the bark beetle Tomicus piniperda. Entomol Exp. Appl. 82, 9–17. doi: 10.1046/j.1570-7458.1997.00108.x
Schroeder, L. M. (1999). Population levels and flight phenology of bark beetle predators in stands with and without previous infestations of the bark beetle Tomicus piniperda. For. Ecol. Manage. 123, 31–40. doi: 10.1016/S0378-1127(99)00014-6
Schroeder, L. M., and Dalin, P. (2017). Differences in photoperiod-induced diapause plasticity among different populations of the bark beetle Ips typographus and its predator Thanasimus formicarius. Agric. For. Entomol. 19, 146–153. doi: 10.1111/afe.12189
Schroeder, L. M., and Lindelöw, A. (1989). Attraction of scolytids and associated beetles by different absolute amounts and proportions of α-pinene and ethanol. J. Chem. Ecol. 15, 807–817. doi: 10.1007/BF01015179
Schroeder, L. M., and Weslien, J. (1994). Interactions between the phloem-feeding species Tomicus piniperda (Col.: Scolytidae) and Acanthocinus aedilis (Col.: Cerambycidae), and the predator Thanasimus formicarius (Col.: Cleridae) with special reference to brood production. Entomophaga. 39, 149–157. doi: 10.1007/BF02372353
Seebens, H., Blackburn, T. M., Dyer, E. E., Genovesi, P., Hulme, P. E., Jeschke, J. M., et al. (2017). No saturation in the accumulation of alien species worldwide. Nat. Commun. 8, 1–9. doi: 10.1038/ncomms14435
Senf, C., Pflugmacher, D., Zhiqiang, Y., Sebald, J., Knorn, J., Neumann, M., et al. (2018). Canopy mortality has doubled in Europe’s temperate forests over the last three decades. Nat. Commun. 9, 1–8. doi: 10.1038/s41467-018-07539-6
Seybold, S. J., and Downing, M. (2007). “What risks do invasive bark beetles and woodborers pose to forest of the Western United States? A case study of the Mediterranean Pine Engraver, Orthotomicus erosus,” in Proceedings of a Symposium at the 2007 Society of American Foresters Conference. The Western bark beetle research group: A unique collaboration with forest health protection, eds J. L. Hayes and J. E. Lundquist (Portland, OR: U.S. Department of Agriculture, Forest Service, Pacific Northwest Research Station), 111–134.
Siegert, N. W., and McCullough, D. G. (2001). Preference of Tomicus piniperda (Coleoptera: Scolytidae) parent adults and shoot-feeding progeny adults for three pine species. Can. Entomol. 133, 343–353. doi: 10.4039/Ent133343-3
Sierpiński, Z. (1965). Nowe dane dotyczace biologii przyplaszzka granatka (Phaenops cyanea F.). Sylwan. 109, 65–70.
Sierra, J. M., and Martín, A. B. (2005). Efectividad de trampas de feromona en la captura masiva de Ips sexdentatus Boern. (Coleoptera: Scolytidae), escolítido perforador de los pinos. Bol. Sanid. Veg. Plagas. 30, 745–752.
Siitonen, J. (2014). Ips acuminatus kills pines in Southern Finland. Silva Fenn. 48:1145. doi: 10.14214/sf.1145
Sikström, U., Jacobson, S., Pettersson, F., and Weslien, J. (2011). Crown transparency, tree mortality and stem growth of Pinus sylvestris, and colonization of Tomicus piniperda after an outbreak of Gremmeniella abietina. For. Ecol. Manage. 262, 2108–2119. doi: 10.1016/j.foreco.2011.07.034
Sowińska, A. (2006). Biologia i ekologia przypłaszczka granatnika Phaenops cyanea (F.) (Col., Buprestidae) - aktualny stan wiedzy. Leśne Práce Badawce. 3, 233–240.
Sperry, J. S., and Tyree, M. T. (1988). Mechanism of water stress-induced xylem embolism. Plant Physiol. 88, 581–587. doi: 10.1104/pp.88.3.581
Šrot, M. (1968). Příspëvek k bionomii lýkohuba sosnového (Myelophilus piniperda L.) a novým metodám chemického hubení škůdce. [The bionomics of Myelophilus piniperda, a new methods of chemical pest control]. Lesnický Časopis. 14, 375–390.
Štefková, K., Okrouhlik, J., and Doležal, P. (2017). Development and survival of the spruce bark beetle, Ips typographus (Coleoptera: Curculionidae: Scolytinae) at low temperatures in the laboratory and the field. Eur. J. Entomol. 114, 1–6. doi: 10.14411/eje.2017.001
Stumpf, W. (1999). Zur Biologie und Verbreitung von Prachtkäferarten der Gatutungen Poecilonota, Scintillatrix, Buprestis und Phaenops in Thüringen (Coleoptera, Buprestidae). Thüringer Faunistische Abhandlungen. 6, 169–176.
Suárez-Vidal, E., Sampedro, L., Voltas, J., Serrano, L., Notivol, E., and Zas, R. (2019). Drought stress modifies early effective resistance and induced chemical defences of Aleppo pine against a chewing insect herbivore. Environ. Exp. Bot. 162, 550–559. doi: 10.1016/j.envexpbot.2019.04.002
Sullivan, J. (1993). Pinus sylvestris in Fire Effects Information System. Washington, DC: U.S. Department of Agriculture.
Švestka, M., and Wiesner, C. (1997). Vývoj a využití feromonu lýkožrouta vrcholkového - Ips acuminatus. Thayensia 4, 153–159.
Templin, E. (1962). Animal pests as a factor in the death of pine trees. Germany: Tierische Schädlinge als Faktor des Kiefernsterbens.
Thabeet, A., Vennetier, M., Gadbin-Henry, C., Denelle, N., Roux, M., Caraglio, Y., et al. (2009). Response of Pinus sylvestris L. to recent climatic events in the French Mediterranean region. Trees 23, 843–853. doi: 10.1007/s00468-009-0326-z
Thomas, F. M., Blank, R., and Hartmann, G. (2002). Abiotic and biotic factors and their interactions as causes of oak decline in Central Europe. For. Pathol. 32, 277–307. doi: 10.1046/j.1439-0329.2002.00291.x
Thomsen, P. F., Jørgensen, P. S., Bruun, H. H., Pedersen, J., Riis-Nielsen, T., Jonko, K., et al. (2016). Resource specialists lead local insect community turnover associated with temperature - analysis of an 18-year full-seasonal record of moths and beetles. J. Anim. Ecol. 85, 251-261. doi: 10.1111/1365-2656.12452
Thuiller, W., Albert, C., Araújo, M. B., Berry, P. M., Cabeza, M., Guisan, A., et al. (2008). Predicting global change impacts on plant species’ distributions: future challenges. Perspect. Plant Ecol. Evol. Syst. 9, 137–152. doi: 10.1016/j.ppees.2007.09.004
Tiberi, R., Faggi, M., Sabbatini Perevieri, G., Marziali, L., and Niccoli, A. (2009). Feeding preference of Tomicus destruens progeny adults on shoots of five pine species. Bull. Insectol. 62, 261–266.
Toffolo, E. P., Bernardinelli, I., Stergulc, F., and Battisti, A. (2006). “Climate change and expansion of the pine processionary moth, Thaumetopoea pityocampa, in northern Italy,” in Proceedings of the Workshop 2006 IUFRO Party 7.03.10, (Vienna: Gmunden), 331–340.
Trenberth, K. E., Dai, A., Rasmussen, R. M., and Parsons, D. B. (2003). The Changing character of precipitation. Bull. Am. Meteorol. Soc. 84, 1205–1218. doi: 10.1175/BAMS-84-9-1205
Tribe, G. D. (1990). Phenology of Pinus radiata log colonization and reproduction by the European bark beetle Orthotomicus erosus (Wollaston) (Coleoptera: Scolytidae) in the south-western Cape Province. J. Ent. Soc. Sth. Afr. 53, 117–126.
Triggiani, O. (1984). Tomicus (Blastophagus) piniperda (Coleoptera, Scolytidae Hylesininae): biologia, danni e controllo nel litorale ionico. Entomologica 19, 5–21.
Trugman, A. T., Anderegg, L. D., Anderegg, W. R., Das, A. J., and Stephenson, N. L. (2021). Why is tree drought mortality so hard to predict? Trends Ecol. Evol. 36, 520–532. doi: 10.1016/j.tree.2021.02.001
Turchin, P., Wood, S. N., Ellner, S. P., Kendall, B. E., Murdoch, W. W., Fischlin, A., et al. (2003). Dynamical effects of plant quality and parasitism on population cycles of larch budmoth. Ecology 84, 1207–1214. doi: 10.1890/0012-9658(2003)084[1207:DEOPQA]2.0.CO;2
Vacchiano, G., Garbarino, M., Borgogno Mondino, E., and Motta, R. (2011). Evidences of drought stress as a predisposing factor to Scots pine decline in Valle d’Aosta (Italy). Eur. J. For. Res. 131, 989–1000. doi: 10.1007/s10342-011-0570-9
Vakula, J., Kunca, A., Zúbrik, M., Leontovyč, R., Longauerová, V., and Gubka, A. (2007). “Distribution of two invasive pests in Slovakia since 1996. Alien, Invasive Species and International Trade,” in Proceedings of the IUFRO Unit 7.03.12, Jedlnia, eds H. Evans and T. Oszako (Poland: Forest Research Institute), 105–113.
Vallet, E. (1981). Etude du dépérissement du Pin sylvestre enrégion Centre et des principaux avageurs scolytides associes: Tomicus piniperda, Ips sexdentatus et Ips acumunatus (col. Scolytidae). [dissertation thesis]. Paris: Biologievégétale, Université d’Orléans.
van Lenteren, J. C., Woets, J., Grijpma, P., Ulenberg, S. A., and Minkenberg, O. P. J. M. (1987). Invasions of pest and beneficial insects in the Netherlands. Proc. K. Ned. Akad. Wet. Ser. C. Biol. Med. Sci. 90, 51–80.
Vasconcelos, T., Branco, M., Goncalyes, M., and Cabral, M. T. (2005). “Periods of flying activity of Tomicus spp,” in Portugal,” in Entomological Research in Mediterranean Forest Ecosystems, eds F. Lieutier and D. Ghaioule (Paris: INRA Editions), 177–184.
Vasconcelos, T., Nazaré, N., Branco, M., Kerdelhue, C., Sauvard, D., and Lieutier, F. (2003). “Host preference of Tomicus piniperda and Tomicus destruens for three pine species,” in Proceedings IUFRO Kanazawa 2003 “Forest Insect Danamics and Host Influences“, eds N. Kamata, A. M. Liebhold, D. T. Quiring, and K. M. Clancy (Kanazawa: Kanazawa University), 19–21.
Vertui, F., and Tagliaferro, F. (1998). Scots pine (Pinus sylvestris L.) die-back by unknown causes in the Aosta Valley. Italy. Chemos. 36, 1061–1065. doi: 10.1016/S0045-6535(97)10172-2
Vidaković, M. (1991). Conifers: morphology and Variation. Tree Physiol. 12, 319–319. doi: 10.1093/treephys/12.4.319a
Villari, C. (2012). Fungi associated with the pine engraver beetle Ips acuminatus and their interactions with the host tree. [dissertation thesis]. Padova: University of Padova.
Vité, J. P., Bakke, A., and Hughes, P. R. (1974). A population attractant of Ips sexdentatus. Naturwissenschaften 61, 365–366. doi: 10.1007/BF00600309
Walsh, J., Wuebbles, D., Hayhoe, K., Kossin, J., Kunkel, K., Stephens, G., et al. (2014). “Climate science supplement,” in Climate change impacts in the United States: The third national climate assessment, U.S. Global Change Research Program, eds J. M. Melillo, T. C. Richmond, and G. W. Yohe (Washington, D.C: U.S. Global Change Research Program, GlobalChange.gov), doi: 10.7930/J0KS6PHH
Walter, A. J., Venette, R. C., and Kells, S. A. (2009). Acceptance and suitability of novel trees for Orthotomicus erosus, an exotic bark beetle in North America. Biol. Invas. 12, 1133–1144. doi: 10.1007/s10530-009-9531-3
Weed, A. S., Ayres, M. P., and Hicke, J. A. (2013). Consequences of climate change for biotic disturbances in North American forests. Ecol. Monogr. 83, 441–470. doi: 10.1890/13-0160.1
Weissbecker, B., Schröder, T., Apel, K. H., and Schütz, S. A. (2006). Perception of odours by forest pests: comparison of a wood breeding beetle (Monochamus galloprovincialis) and a bark breeding beetle (Phaenops cyanea). Mitt. Dtsch. Ges. allg. angew. Entomol. 15, 235–238.
Wermelinger, B., and Seifert, M. (1998). Analysis of the temperature dependent development of the spruce bark beetle Ips typographus (L) (Col., Scolytidae). J. Appl. Entomol. 122, 185–191. doi: 10.1111/j.1439-0418.1998.tb01482.x
Wermelinger, B., Epper, C., Kenis, M., Ghosh, S., and Holdenrieder, O. (2012). Emergence patterns of univoltine and bivoltine Ips typographus (L.) populations and associated natural enemies. J. Appl. Entomol. 136, 212–224. doi: 10.1111/j.1439-0418.2011.01629.x
Wermelinger, B., Rigling, A., Schneider Mathis, D., and Dobbertin, M. (2008). Assessing the role of bark- and wood-boring insects in the decline of Scots pine (Pinus sylvestris) in the Swiss Rhone valley. Ecol. Entomol. 33, 239–249. doi: 10.1111/j.1365-2311.2007.00960.x
Wiegard, S., and Amarell, U. (1994). Ecological studies in a pollution gradient: do plant and animal communities respond differently? Arch. Nat. Conserv. Landscape Res. 33, 271–286.
Williamson, M. H., and Brown, K. C. (1986). The analysis and modelling of British invasions. Philos. Trans. R. Soc. Lond. Ser. B. Biol. Sci. 3114, 505–522. doi: 10.1098/rstb.1986.0070
Wingfield, M. J., Slippers, B., and Wingfield, B. D. (2010). Novel associations between pathogens, insects and tree species threaten world forests. N. Z. J. For. Sci. 40, S95–S103.
Wood, S. L., and Bright, D. E. (1992). A catalog of Scolytidaeand Platypodidae (Coleoptera), Part 2: Taxonomic Index. Provo: Great Basin Naturalist Memoirs, Brigham Young University.
Ye, H., and Ding, X. S. (1999). Impacts of Tomicus minor on distribution and reproduction of Tomicus piniperda (Col.,Scolytidae) on the trunk of the living Pinus yunnanensis trees. J. Appl. Entomol. 123, 329–333.
Yin, H. F., Huang, S. H., and Li, Z. H. (1984). Economic insect fauna of China, Coleoptera, Scolytidae. Beijing: Science Press.
Yvon, A., and Wegensteiner, R. (2015). Studies on the development of Tomicus piniperda and Tomicus minor (Coleoptera, Curculionidae) depending on temperature. Mitt. Dtsch. Ges. Allg. Angew. Entomol. 20, 275–278.
Keywords: Scots pine, bark beetles, bionomy, ecological physiology, climate change
Citation: Hlávková D and Doležal P (2022) Cambioxylophagous Pests of Scots Pine: Ecological Physiology of European Populations—A Review. Front. For. Glob. Change 5:864651. doi: 10.3389/ffgc.2022.864651
Received: 28 January 2022; Accepted: 17 May 2022;
Published: 09 June 2022.
Edited by:
Sigrid Netherer, University of Natural Resources and Life Sciences Vienna, AustriaReviewed by:
Milan Pernek, Croatian Forest Research Institute, CroatiaAllan L. Carroll, University of British Columbia, Canada
Copyright © 2022 Hlávková and Doležal. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Daniela Hlávková, hlavkova.daniela@entu.cas.cz; Petr Doležal, dolezal@entu.cas.cz