Host range

Both I. typographus and P. chalcographus can utilize different conifer species of the family Pinaceae. However, they differ in their potential host range, their preference for and their performance on different tree species (table 1, fig. 1) (Postner, Reference Postner and Schwenke1974; Pfeffer, Reference Pfeffer1995; Bertheau et al., Reference Bertheau, Salle, Rossi, Bankhead-Dronnet, Pineau, Roux-Morabito and Lieutier2009b).

Figure 1. Overview on life-histories of Ips typographus (left) and Pityogenes chalcographus (right). Ips typographus: (a) Overwintering usually as an adult. (b) Polygynous reproduction, with a common harem size of three females. (c) Typical breeding system with vertical maternal galleries. (d) Monophagous feeding behaviour with Norway spruce (Picea abies) as the main host. (e) Associated microbes with blue-stain fungi as most relevant symbionts. Pityogenes chalcographus: (f) Overwintering as larva, pupa, and adult. (g) Polygynous reproduction, with a harem size of up to nine females. (h) Typical stellar breeding system. (i) Oligophagous feeding behaviour on various conifer genera with Norway spruce as the main host. (j) Associated microbes with yeasts as most relevant symbionts.

Table 1. Selected life-history traits of Ips typographus and Pityogenes chalcographus

Ips typographus is generally classified as a monophagous bark beetle, whereas P. chalcographus is regarded to be oligophagous (Eidmann, Reference Eidmann1987; Mayer et al., Reference Mayer, Piel, Cassel-Lundhagen, Kirichenko, Grumiau, Okland, Bertheau, Gregoire and Mardulyn2015). The primary host of both beetles is Norway spruce, as it was proven by presence-abundance data under natural conditions or by preference-performance studies in the laboratory (Postner, Reference Postner and Schwenke1974; Pfeffer, Reference Pfeffer1995; Bertheau et al., Reference Bertheau, Salle, Roux-Morabito, Garcia, Certain and Lieutier2009a, Reference Bertheau, Salle, Rossi, Bankhead-Dronnet, Pineau, Roux-Morabito and Lieutier2009b; Cognato, Reference Cognato, Vega and Hofstetter2015; Schroeder and Cocos, Reference Schroeder and Cocos2018). Secondary, less commonly used hosts of both species are from the genera Pinus, Larix, Abies or Pseudotsuga, both native and non-native species (Postner, Reference Postner and Schwenke1974; Bertheau et al., Reference Bertheau, Salle, Rossi, Bankhead-Dronnet, Pineau, Roux-Morabito and Lieutier2009b; Schroeder and Cocos, Reference Schroeder and Cocos2018). Although the two beetles can colonize and breed in similar host species, P. chalcographus is more abundant on all secondary hosts (Bertheau et al., Reference Bertheau, Salle, Rossi, Bankhead-Dronnet, Pineau, Roux-Morabito and Lieutier2009b; Schroeder and Cocos, Reference Schroeder and Cocos2018). The oligophagous behaviour can confer an ecological and evolutionary advantage to P. chalcographus, as it can shift to other plants when primary hosts are scarce or absent, e.g. when new habitats are invaded.

Interspecific competition

Resource partitioning and competition have been described from various bark beetles (Paine et al., Reference Paine, Birch and Svihra1981; Light et al., Reference Light, Birch and Paine1983; Bouhot et al., Reference Bouhot, Lieutier and Debouzie1988; Rankin and Borden, Reference Rankin and Borden1991). Smaller-sized species colonize upper, thin-barked parts of trees, whereas larger-sized beetles are found in lower, thick-barked sections. This separation in ecological niches reduces interspecific competition and is driven by the diameter of the body (Grünwald, Reference Grünwald1986; Schlyter and Anderbrant, Reference Schlyter and Anderbrant1993; Amezaga and Rodriguez, Reference Amezaga and Rodriguez1998). Hence, given the larger body size of I. typographus, it prevails in thicker host material/stem sections than P. chalcographus, although overlaps occur (table 1, fig. 1) (Grünwald, Reference Grünwald1986; Göthlin et al., Reference Göthlin, Schroeder and Lindelöw2000). The latter one can utilize a broader range of bark sections, including those preferred by I. typographus. In these thicker parts, however, P. chalcographus is apparently outcompeted (Grünwald, Reference Grünwald1986).

Mating system, reproductive performance and gallery morphology

Ips typographus and P. chalcographus are polygynous bark beetles, however, they differ markedly in the number of females attracted per male (table 1, fig. 1). After building a mating chamber in the phloem, P. chalcographus males can mate with up to nine females (Schwerdtfeger, Reference Schwerdtfeger1929), whereas I. typographus has harem sizes of generally two or three, sometimes four, females (Wermelinger, Reference Wermelinger2004).

The two beetles also differ in their fecundity. One female of I. typographus can deposit up to 80, or even 100, eggs per gallery (Anderbrant and Lofqvist, Reference Anderbrant and Lofqvist1988; Anderbrant, Reference Anderbrant1990; Wermelinger, Reference Wermelinger2004), whereas one P. chalcographus female can lay up to 40 eggs (Schwerdtfeger, Reference Schwerdtfeger1929; Führer and Mühlenbrock, Reference Führer and Mühlenbrock1983). The average reproductive output per female, however, is much lower and highly variable under natural conditions (Thalenhorst, Reference Thalenhorst1958), depending on various factors, like the quality of the breeding material and inter- and intraspecific competition (Anderbrant and Lofqvist, Reference Anderbrant and Lofqvist1988; Anderbrant, Reference Anderbrant1990; Faccoli and Bernardinelli, Reference Faccoli and Bernardinelli2011). About 30 eggs per female likely reflect the average reproductive potential per gallery of P. chalcographus (Schwerdtfeger, Reference Schwerdtfeger1929) and 25 to 60 eggs for I. typographus (Thalenhorst, Reference Thalenhorst1958; Anderbrant and Lofqvist, Reference Anderbrant and Lofqvist1988; Anderbrant, Reference Anderbrant1990).

Both species differ in the architecture of their galleries (table 1, fig. 1). After mating I. typographus females build their mother tunnels in a vertical direction, following the fibre direction of the host. In contrast, females of P. chalcographus construct their mother tunnels in different directions starting from a central mating chamber, resulting in a stellar breeding system (Postner, Reference Postner and Schwenke1974). Obviously, these galleries are shaped by the number of females per male but underlying evolutionary drivers for these differences in the reproductive biology are unknown. It is also unclear if there is an optimal direction for maternal or larval tunnels, which might be influenced by factors, like the spatial structure of nutrients and tree defences as well as growth properties of associated fungi.

Pityogenes chalcographus usually shows higher attack densities and higher egg gallery densities on hosts and tends to be more ubiquitous than I. typographus (Hedgren et al., Reference Hedgren, Weslien and Schroeder2003; Hedgren, Reference Hedgren2004). The latter one, however, has a much higher tree-killing ability on living hosts (Hedgren, Reference Hedgren2004). Moreover, P. chalcographus is often found on trees that have already been attacked by I. typographus (Hedgren, Reference Hedgren2004). In habitats with plenty of suitable breeding material, e.g. storm-felled trees, P. chalcographus is more abundant in later phases of a post-storm period (Hedgren, Reference Hedgren2004; Schroeder and Cocos, Reference Schroeder and Cocos2018), underlining different preferences for host quality.

Fungal symbionts

Bark beetles are generally associated with a wide variety of filamentous fungi and yeasts (Six, Reference Six2013; Biedermann and Vega, Reference Biedermann and Vega2020) and more than 30 different fungus species have been isolated from the galleries of I. typographus and P. chalcographus (table 1, fig. 1) (Kirschner, Reference Kirschner1998; Kirisits, Reference Kirisits, Lieutier, Day, Gregoire and Evans2004; Giordano et al., Reference Giordano, Garbelotto, Nicolotti and Gonthier2013; Jankowiak et al., Reference Jankowiak, Kolarik and Bilanski2014). Most of these species are likely commensals or antagonists, however, bark beetles usually also have a few beneficial fungal associates. These mutualistic species provide nutritional benefits, aid in detoxification of tree defensive compounds and pheromone production and/or protect their hosts against antagonistic microbes (Francke-Grosmann, Reference Francke-Grosmann and Henry1967; Birkemoe et al., Reference Birkemoe, Jacobsen, Sverdrup-Thygeson, Biedermann and Ulyshen2018; Davis et al., Reference Davis, Stewart, Mann, Bradley and Hofstetter2019; Biedermann and Vega, Reference Biedermann and Vega2020). Likely candidates for mutualistic roles in I. typographus and P. chalcographus are fungal species in the ascomycete Ophiostomatales, i.e. the genera Ophiostoma, Grosmannia and Ceratocystiopsis, and Microascales, i.e. the genus Endoconidiophora (Harrington, Reference Harrington, Vega and Blackwell2005; Six, Reference Six2013). Both species, however, lack mycetangia/mycangia, i.e. external spore-carrying pockets (Francke-Grosmann, Reference Francke-Grosmann1956, Reference Francke-Grosmann1959, Reference Francke-Grosmann1963; Vega and Biedermann, Reference Vega and Biedermann2020), and many of the fungi are found only irregularly. Therefore, for P. chalcographus fungal symbionts have been regarded unimportant (Grosmann, Reference Grosmann1930; Mathiesen-Käärik, Reference Mathiesen-Käärik1960; Kirisits, Reference Kirisits, Lieutier, Day, Gregoire and Evans2004). For I. typographus debates on the importance and phytopathogenic properties of fungal symbionts to overcome healthy trees are still ongoing (Kirisits, Reference Kirisits, Lieutier, Day, Gregoire and Evans2004; Salle et al., Reference Salle, Monclus, Yart, Garcia, Romary and Lieutier2005; Lieutier et al., Reference Lieutier, Yart and Salle2009; Six and Wingfield, Reference Six and Wingfield2011). Fungi are exchanged between the two bark beetles, in particular Ophiostomatales from I. typographus to P. chalcographus, when they co-occur on the same tree (Grosmann, Reference Grosmann1930; Mathiesen-Käärik, Reference Mathiesen-Käärik1953). This co-occurrence usually results in the isolation of the same fungal species from galleries of the two bark beetles, even though several studies suggest that filamentous fungi are more common in I. typographus relative to P. chalcographus galleries (Grosmann, Reference Grosmann1930; Mathiesen-Käärik, Reference Mathiesen-Käärik1960; Krokene and Solheim, Reference Krokene and Solheim1996; Kirisits, Reference Kirisits, Lieutier, Day, Gregoire and Evans2004). The simple reason might be that thinner phloem dries out more quickly, providing worse conditions for fungal growth (Grosmann, Reference Grosmann1930; Mathiesen-Käärik, Reference Mathiesen-Käärik1953). This is supported by the fact that relatively dry- and heat-resistant fungi, e.g. Hypocreales in the genus Geosmithia, are more common in galleries of P. chalcographus (Kolarik and Jankowiak, Reference Kolarik and Jankowiak2013; Jankowiak et al., Reference Jankowiak, Kolarik and Bilanski2014).

Frequency differences of fungal associates, however, might result in different tree-killing abilities of the two bark beetle species (Krokene and Solheim, Reference Krokene and Solheim1996). Ips typographus is commonly associated with the highly virulent fungus Endoconidiophora polonica that may help beetles to overcome trees (Horntvedt et al., Reference Horntvedt, Christiansen, Solheim and Wang1983; but see Six and Wingfield, Reference Six and Wingfield2011) by over-stimulation of host defence (Lieutier et al., Reference Lieutier, Yart and Salle2009). Frequencies of E. polonica are locally highly variable and appear to differ between epidemic and non-epidemic populations (Harding, Reference Harding1989; Solheim, Reference Solheim1993; Krokene and Solheim, Reference Krokene and Solheim1996). Likely this fungus is a good colonizer of well-defended phloem of trees during epidemics (Solheim, Reference Solheim1992; Gibbs, Reference Gibbs, Wingfield, Seifert and Webber1993). Like other symbionts, it can cope with tree defensive compounds, e.g. terpenes or phenolics, and can even use those substances as a carbon source for growth (Krokene and Solheim, Reference Krokene and Solheim1998; Hammerbacher et al., Reference Hammerbacher, Schmidt, Wadke, Wright, Schneider, Bohlmann, Brand, Fenning, Gershenzon and Paetz2013; Krokene, Reference Krokene, Vega and Hofstetter2015; Wadke et al., Reference Wadke, Kandasamy, Vogel, Lah, Wingfield, Paetz, Wright, Gershenzon and Hammerbacher2016).

The second important fungal associate of I. typographus is Grosmannia penicillata. Like E. polonica, it is transmitted by dispersing beetles on the body surface via sticky spores (Furniss et al., Reference Furniss, Solheim and Christiansen1990) and is virulent to Norway spruce (Horntvedt et al., Reference Horntvedt, Christiansen, Solheim and Wang1983). Recently, it has also been shown that it can synthesize components of the aggregation pheromone of I. typographus (Zhao et al., Reference Zhao, Axelsson, Krokene and Borg-Karlson2015) and together with another associate Grosmannia europhioides it is even more efficient in degrading beetle-toxic phenolics than E. polonica (Zhao et al., Reference Zhao, Kandasamy, Krokene, Chen, Gershenzon and Hammerbacher2019). Furthermore, adult beetles prefer to feed on artificial spruce substrate colonized and thus detoxified by these fungi (Zhao et al., Reference Zhao, Kandasamy, Krokene, Chen, Gershenzon and Hammerbacher2019). These three fungi (E. polonica, G. penicillata, G. europhioides) were also the only ones emitting volatiles that attracted adult I. typographus in behavioural assays on an artificial spruce substrate and may thus be regarded as mutualists (Kandasamy et al., Reference Kandasamy, Gershenzon, Andersson and Hammerbacher2019). Other common associates, like Ophiostoma piceae and Ophiostoma bicolor, are neither attractive nor repellent to I. typographus and may thus be regarded as commensals (Kandasamy et al., Reference Kandasamy, Gershenzon, Andersson and Hammerbacher2019). Interestingly, bark beetle-infesting parasitoids can use volatiles emitted by certain microorganisms to detect their hosts, adding another part to these multi-trophic systems (Wegensteiner et al., Reference Wegensteiner, Wermelinger, Herrmann, Vega and Hofstetter2015).

Assays like those for I. typographus are lacking for P. chalcographus but given the lower abundance of fungi within their galleries beneficial effects might be smaller. Several studies, however, indicate that Geosmithia and yeasts that are transmitted by P. chalcographus are less dry-sensitive than Ophiostomatales and Microascales associated with I. typographus (Grosmann, Reference Grosmann1930; Kolarik and Jankowiak, Reference Kolarik and Jankowiak2013; Jankowiak et al., Reference Jankowiak, Kolarik and Bilanski2014). Grosmann (Reference Grosmann1930), for example, showed that yeasts are abundant in young breeding systems, especially surrounding eggs, from where they are picked up by larvae and can later be found as gut symbionts. If these early observations are true, P. chalcographus may profit from internal fungi in detoxification of defensive tree compounds but typically lacks external fungal symbionts that can help I. typographus to overwhelm living trees.

Yeasts are generally understudied in bark beetles (Davis, Reference Davis2015) and their role has only been partly elucidated for I. typographus (Leufven, Reference Leufven, Barbosa, Krischik and Jones1991). Main I. typographus pheromone components are synthesized by beetles de novo (Blomquist et al., Reference Blomquist, Figueroa-Teran, Aw, Song, Gorzalski, Abbott, Chang and Tittiger2010). However, several gut yeasts of I. typographus, the most common ones are Pichia holstii and Candida diddensii, oxygenate tree-defensive monoterpenes like α-pinene that beetles themselves oxidize to cis-verbenol, to either trans-verbenol or verbenone (Leufven et al., Reference Leufven, Bergstrom and Falsen1984, Reference Leufven, Bergstrom and Falsen1988; Leufven and Nehls, Reference Leufven and Nehls1986). Interestingly, cis-verbenol acts as an aggregation pheromone for I. typographus but not for P. chalcographus, whereas yeast-produced trans-verbenol or verbenone have anti-aggregation effects for both species (Leufven, Reference Leufven, Barbosa, Krischik and Jones1991; Davis, Reference Davis2015). The yeasts of P. chalcographus have not been studied for their semiochemical role and it needs to be determined if both species harbour different yeasts and how frequently they get exchanged.

Cold tolerance

Major adaptations of insects to survive cold winters are strategies to cope with the freezing of body fluids. Ips typographus and P. chalcographus are both freeze-avoidant species (Kostal et al., Reference Kostal, Dolezal, Rozsypal, Moravcova, Zahradnickova and Simek2011, Reference Kostal, Miklas, Dolezal, Rozsypal and Zahradnickova2014), as they die when ice formation in body fluids occurs – the temperature when ice is built is defined as the supercooling point (SCP) (Bale, Reference Bale1993; Lee, Reference Lee, Denlinger and Lee2010; Sinclair et al., Reference Sinclair, Alvarado and Ferguson2015). Both species evolved a high supercooling capacity to survive cold conditions, by using a set of sugars and polyols to decrease the freezing point of the haemolymph (Kostal et al., Reference Kostal, Zahradnikova, Simek and Zeleny2007, Reference Kostal, Dolezal, Rozsypal, Moravcova, Zahradnickova and Simek2011, Reference Kostal, Miklas, Dolezal, Rozsypal and Zahradnickova2014). Adults of P. chalcographus from Central European populations survived cold conditions below average temperatures of −26 °C in mid-winter, with some individuals surviving even −36 °C (Kostal et al., Reference Kostal, Dolezal, Rozsypal, Moravcova, Zahradnickova and Simek2011, Reference Kostal, Miklas, Dolezal, Rozsypal and Zahradnickova2014). Adult beetles of Central European I. typographus had average SCPs in mid-winter of about −20/−22 °C, with single individuals reaching SCPs of almost −27 °C (Kostal et al., Reference Kostal, Dolezal, Rozsypal, Moravcova, Zahradnickova and Simek2011). In addition, both beetles have also a high chilling potential to survive sub-zero temperatures above the SCP, even over long periods (Kostal et al., Reference Kostal, Dolezal, Rozsypal, Moravcova, Zahradnickova and Simek2011, Reference Kostal, Miklas, Dolezal, Rozsypal and Zahradnickova2014). Cold tolerance and survival is a plastic response, as insects can acclimatize to ambient conditions. In Northern Europe where winter conditions can be harsher than in more southern latitudes I. typographus can cope with temperatures as low as −32 °C, with an average of about −29 °C in mid-winter (Annila, Reference Annila1969). Moreover, I. typographus and P. chalcographus show similar patterns in their seasonal supercooling capacity, with the lowest SCP values in December/January (Kostal et al., Reference Kostal, Dolezal, Rozsypal, Moravcova, Zahradnickova and Simek2011, Reference Kostal, Miklas, Dolezal, Rozsypal and Zahradnickova2014), reflecting modifications depending on prevailing temperature conditions.

As the two bark beetles often overwinter under the bark of host trees, they might get in contact with ice in the moist, frozen phloem layer. This can result in inoculative freezing, a process when environmental ice enters the body via orifices or through the cuticle and results in freezing of body fluids (Lee, Reference Lee, Denlinger and Lee2010). Both species evolved adaptations to avoid inoculative freezing (Kostal et al., Reference Kostal, Dolezal, Rozsypal, Moravcova, Zahradnickova and Simek2011, Reference Kostal, Miklas, Dolezal, Rozsypal and Zahradnickova2014). Experiments with adult P. chalcographus, however, suggest that it can survive harsher conditions in the presence of external ice (Kostal et al., Reference Kostal, Miklas, Dolezal, Rozsypal and Zahradnickova2014) than adult I. typographus (Kostal et al., Reference Kostal, Dolezal, Rozsypal, Moravcova, Zahradnickova and Simek2011). The overwintering performance of the two beetle species was also tested under natural field conditions. In a Czech study, adult P. chalcographus survival rates over a winter ranged in most cases between ~30 and ~75% (Kostal et al., Reference Kostal, Miklas, Dolezal, Rozsypal and Zahradnickova2014). Considering also the survival rates under laboratory conditions and the SCP data obtained by Kostal et al. (Reference Kostal, Miklas, Dolezal, Rozsypal and Zahradnickova2014), high proportions of P. chalcographus populations might survive cold temperatures during Central European winters. Low temperatures, however, are not the only limiting factors for overwintering survival. Biotic and abiotic parameters that can vary on a very small, local scale contribute to a complex picture that determine mortality during cold.

Ips typographus overwinters either under the bark of hosts or in the forest litter (Biermann, Reference Biermann1977). In Central Europe, overwintering survival rates of I. typographus (across all developmental stages) hibernating under the bark of Norway spruce of about 50% were reported (Faccoli, Reference Faccoli2002). In Northern Europe, however, mortality of adult I. typographus overwintering under the bark ranges from ~60 to 100%, whereas adult survival in the litter or moss layer – with an additional insulating snow cover – is over 90% (Annila, Reference Annila1969). Unfortunately, studies on the overwintering behaviour and survival of P. chalcographus outside of host trees, e.g. in the forest litter, are currently lacking. Such data would be important to get a comprehensive picture of the beetle's life history.

One major difference in the overwintering biology of the two bark beetles concerns the developmental stages surviving low sub-zero conditions. In I. typographus only the adult stage can survive low sub-zero temperatures (Annila, Reference Annila1969; Faccoli, Reference Faccoli2002; Dworschak et al., Reference Dworschak, Gruppe and Schopf2014), whereas pre-imaginal stages survive only mild but still sub-zero conditions (Stefkova et al., Reference Stefkova, Okrouhlik and Dolezal2017). In P. chalcographus larvae, pupae and adults are able to survive low winter temperatures (Kostal et al., Reference Kostal, Miklas, Dolezal, Rozsypal and Zahradnickova2014). Ips typographus might face a decrease of population levels when beetles do not reach the adult stage before winter – which can happen when cold autumn temperatures slow down development or when warm conditions hamper the induction of diapause (details see below). In P. chalcographus, however, beetles that started their individual development late in the season or whose development was slowed down due to thermal conditions might still be able to survive winter although not completing their entire life cycle. This could relax selection on the timing of oviposition and thus increase the length of the egg-laying period, although the effects of a photoperiodically regulated reproductive diapause are not entirely clear (see below). Moreover, I. typographus overwintering only as adults could result in a synchronization of populations which might be advantageous during host colonization in the following season.

Diapause

Diapause expression is a major strategy for I. typographus to increase stress resistance during winter and additionally regulates development, reproduction and voltinism (Schopf, Reference Schopf1985, Reference Schopf1989; Dolezal and Sehnal, Reference Dolezal and Sehnal2007; Schebeck et al., Reference Schebeck, Hansen, Schopf, Ragland, Stauffer and Bentz2017; Schroeder and Dalin, Reference Schroeder and Dalin2017; Schebeck et al., Reference Schebeck, Dobart, Ragland, Schopf and Stauffer2022). The induction of the facultative reproductive diapause of the adult in the larval/pupal instars is driven by short-day photoperiods and the critical day length for Central European beetles is about 15 h (Schopf, Reference Schopf1989; Dolezal and Sehnal, Reference Dolezal and Sehnal2007). Diapause induction is not regulated by photoperiod alone, as the effect of day length is overridden by high temperatures (Dolezal and Sehnal, Reference Dolezal and Sehnal2007). Moreover, the critical day length increases with latitude, to respond to local environmental conditions (Schroeder and Dalin, Reference Schroeder and Dalin2017). Diapause termination occurs in mid-winter after experiencing a chilling period. Afterwards I. typographus remains in a post-diapause quiescence and resumes development and reproduction when conditions are favourable again (Dolezal and Sehnal, Reference Dolezal and Sehnal2007). In addition, several lines of evidence suggested that this species expresses a second diapause phenotype. Observations on suppressed development, reproduction and dispersal – despite permissive environmental conditions – indicated the presence of an obligate diapause, with both diapause phenotypes in one population (Schopf, Reference Schopf1985, Reference Schopf1989; Dolezal and Sehnal, Reference Dolezal and Sehnal2007; Schroeder and Dalin, Reference Schroeder and Dalin2017). Schebeck et al. (Reference Schebeck, Dobart, Ragland, Schopf and Stauffer2022) proved the existence of facultative (photoperiod-dependent) and obligate (independent of photoperiod) diapause phenotypes in I. typographus, showing varying portions in Central and Northern European populations with implications for seasonality and voltinism.

Pityogenes chalcographus seems to enter a photoperiodically regulated diapause in the adult stage as well (Führer and Chen, Reference Führer and Chen1979). Developmental studies under long-day and short-day conditions at different temperatures showed that all individuals of a generation emerge from their breeding systems at warmer conditions with only a minor influence of photoperiod. At lower temperatures, however, a distinct influence of day length on development was described, suggesting a photoperiodically mediated diapause which is modified by warm temperatures (Führer and Chen, Reference Führer and Chen1979). This would be a similar mechanism as described in I. typographus (Schopf, Reference Schopf1985, Reference Schopf1989; Dolezal and Sehnal, Reference Dolezal and Sehnal2007), however, additional studies are necessary to get a comprehensive picture.

Although bark beetles spend the majority of their live cycles in subcortical environments, they can process photoperiodic signals in various developmental stages. Even pre-imaginal stages, like larvae that lack eyes (stemmata) were reported to respond to photoperiodic cues, as it was shown in the mountain pine beetle, Dendroctonus ponderosae, by opsin gene expression and negatively phototactic behaviour (Wertman et al., Reference Wertman, Bleiker and Perlman2018).

Thermal effects on life history

The temperature-dependent development of I. typographus has been studied extensively under laboratory and field conditions (Annila, Reference Annila1969; Lobinger, Reference Lobinger1994; Coeln et al., Reference Coeln, Niu and Führer1996; Wermelinger and Seifert, Reference Wermelinger and Seifert1998, Reference Wermelinger and Seifert1999; Baier et al., Reference Baier, Pennerstorfer and Schopf2007). Data on developmental times, developmental thresholds or optimum temperature differ considerably among studies (Annila, Reference Annila1969; Coeln et al., Reference Coeln, Niu and Führer1996; Wermelinger and Seifert, Reference Wermelinger and Seifert1998). These differences are likely related to the experimental design or population-related factors. Values for the lower developmental threshold for the whole life cycle range from 5 °C (Annila, Reference Annila1969), to 8.3 °C (Wermelinger and Seifert, Reference Wermelinger and Seifert1998) and even to 12.3 °C (Coeln et al., Reference Coeln, Niu and Führer1996). Data from the most recent study by Wermelinger and Seifert (Reference Wermelinger and Seifert1998), however, are commonly used to model the phenology and voltinism of I. typographus and they reliably predict its development under natural conditions (Baier et al., Reference Baier, Pennerstorfer and Schopf2007; Jönsson et al., Reference Jönsson, Appelberg, Harding and Barring2009). The optimum temperatures for development and reproduction are about 30 °C (Wermelinger and Seifert, Reference Wermelinger and Seifert1998) and around 29 °C (Wermelinger and Seifert, Reference Wermelinger and Seifert1999), respectively. The upper developmental threshold is about 39 °C (Wermelinger and Seifert, Reference Wermelinger and Seifert1998) and Annila (Reference Annila1969) reported a strong increase of I. typographus mortality of all developmental stages at temperatures above 45 °C.

Data on the thermal performance of P. chalcographus are scarce. The temperature-dependent development was studied by Coeln et al. (Reference Coeln, Niu and Führer1996). These data on developmental thresholds are probably higher than under natural field conditions. Additional comprehensive and comparative studies on all temperature-related parameters have to be conducted to get a better understanding of its thermal performance.

In addition, temperature affects the flight activity of I. typographus and P. chalcographus. For both species, the lower limit for swarming initiation is relatively similar, about 16.5 °C/17 °C. The upper limit, however, is 30 °C in I. typographus, while P. chalcographus was still observed swarming at 35 °C (Lobinger, Reference Lobinger1994).

Although developmental parameters, like lower thermal thresholds or developmental times, of I. typographus and P. chalcographus seem to differ from each other, some similar patterns have been observed. For example, the developmental time of the larval stage is about threefold longer than the embryonic or pupal development, respectively. Furthermore, the maturation period of young adults comprises roughly 40% of the whole development in both beetles (Coeln et al., Reference Coeln, Niu and Führer1996; Wermelinger and Seifert, Reference Wermelinger and Seifert1998; Baier et al., Reference Baier, Pennerstorfer and Schopf2007).