Effects of elevation and aspect on the flight activity of two alien pine bark beetles (Coleoptera: Curculionidae, Scolytinae) in recently-harvested pine forests

Forest Ecology and Management 384 (2017) 132–136

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Effects of elevation and aspect on the flight activity of two alien pine bark beetles (Coleoptera: Curculionidae, Scolytinae) in recentlyharvested pine forests E.G. Brockerhoff a,⇑, F. Chinellato a,b, M. Faccoli a,b, M. Kimberley c, S.M. Pawson a a b c

Scion (New Zealand Forest Research Institute), PO Box 29237, Riccarton, Christchurch 8440, New Zealand Department of Agronomy, Food, Natural Resources, Animals and Environment (DAFNAE), University of Padua, Viale dell’Università, 16 - 35020 Legnaro (PD), Italy Scion (New Zealand Forest Research Institute), Private Bag 3020, Rotorua 3046, New Zealand

a r t i c l e

i n f o

Article history: Received 26 July 2016 Received in revised form 17 October 2016 Accepted 19 October 2016 Available online 26 October 2016 Keywords: Alien species Biological invasions Climate change Microclimate Hylastes ater Hylurgus ligniperda

a b s t r a c t Climate is an important driver of the establishment and impact of invasive alien species. Species transported to new regions can only invade those with a climate that meets their thermal requirements, but climate change is likely to alter the invasibility of recipient environments. Likewise, species are unlikely to reach pest status where climatic conditions are suboptimal. Here our objectives were to determine the relationship between climatic conditions and flight activity of two alien pine bark beetles (Hylastes ater and Hylurgus ligniperda) and to anticipate how climate change may affect the future distribution of these species. We used elevational gradients and slope aspect (north versus south-facing slopes), which are known to affect microclimates, to assess the effects on beetle flight across 18 locations in pine forests in the South Island, New Zealand. Using panel traps baited with alpha-pinene and ethanol we caught a total of 45,363 H. ligniperda and 6676 H. ater. Catches of both species decreased significantly and substantially with increasing elevation. Significantly more beetles were caught at north-facing than at south-facing sites towards the end of the flight season in autumn, leading to an extended flight period at northerly aspects. These results are important for pest management and the identification of ‘areas of low pest prevalence’ as a measure to reduce post-harvest infestations of logs destined for export. For example, during risk periods, logs could be harvested preferentially from stands with reduced flight activity (i.e., southerly aspects and higher elevations). Furthermore, such sites could be chosen to reduce post-harvest infestation risks during periods of temporary log storage at skid sites in the forest. Our findings are also important because climate change can be an important factor contributing to population expansion of bark beetles, and warmer temperatures could lead to increased flight activity and abundance, as well as enhanced suitability of sites that are currently less favourable. Ó 2016 Elsevier B.V. All rights reserved.

1. Introduction Biological invasions are a major environmental and economic concern worldwide (Mack et al., 2000; Aukema et al., 2010, 2011). Globalisation and, in particular, the increase in international trade are the main drivers of the spread of potential pest species by providing new and better dispersal pathways (e.g., Leung et al., 2014; Wingfield et al., 2015). This is facilitated further by the widespread use of exotic plants including trees that are used as

⇑ Corresponding author. E-mail addresses: [email protected] (E.G. Brockerhoff), [email protected] (F. Chinellato), [email protected] (M. Faccoli), mark. [email protected] (M. Kimberley), [email protected] (S.M. Pawson). http://dx.doi.org/10.1016/j.foreco.2016.10.046 0378-1127/Ó 2016 Elsevier B.V. All rights reserved.

ornamentals and in planted forests (FAO, 2015) which resulted in the presence of potential host plants in areas where they did not occur naturally. Climatic suitability is a key factor that determines whether or not arrivals of alien species can lead to successful invasions (e.g., Kriticos, 2012). The climate of recipient regions strongly influences which alien species can successfully establish, according to their thermal range. In Europe, the number and frequency of successful invasions are strongly related to latitude, decreasing towards the colder north (Roques et al., 2009). A warming climate is expected to reduce the thermal limitations that were previously hampering the establishment in cooler regions of species arriving from warmer Mediterranean and subtropical regions (Roques, 2010b). Likewise, organisms from warmer subtropical and tropical regions are predicted to encounter an increasingly favourable climate in the mostly temperate climate of New

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Zealand, increasing the likelihood of establishment of such species (Kriticos, 2012). Although responses of bark- and wood-boring beetles to climate change can be complex, it is emerging as a key factor driving – directly or indirectly – at least some of the current infestations of bark beetles occurring worldwide (Bentz et al., 2010; Marini et al., 2012). For instance, global warming may induce tree stress, making forests more suitable to infestation by pests (Bentz et al., 2010; Kolb et al., 2016). Apart from effects on invasions, climatic conditions can strongly influence pest damage and population outbreaks. Warming can reduce winter mortality, increase breeding success and survival, and may increase voltinism of both native and invasive species (Marini et al., 2012; Bentz et al., 2014; Creeden et al., 2014). In addition, warming can facilitate range expansions of pests to higher latitudes and elevations (Battisti et al., 2005; Robinet et al., 2012; Marini et al., 2012). Irrespective of climate change, climatic conditions may affect the level of infestation of forests and forest products due to direct and indirect effects on population levels and the phenology of insects such as bark beetles. The resulting variation in occurrence, abundance and phenology among locations has implications for phytosanitary risk of international trade and for the need to apply phytosanitary measures (Robinet et al., 2012). Therefore, knowledge of relationships between climatic conditions and bark- and wood-boring beetle populations is of crucial importance. Bark- and wood-boring beetles (especially Scolytinae, Cerambycidae and Buprestidae) are among the most successful and damaging invaders, causing significant economic and ecological damage to forests (Brockerhoff et al., 2006a, 2014; Haack, 2006; Leung et al., 2014). These insects are easily transported in almost all types of woody material – such as timber and wood packaging material (crating, dunnage and pallets) as well as woody plants for planting – where they can hide from detection and survive long intercontinental voyages (Brockerhoff et al., 2006a; Liebhold et al., 2012; Rassati et al., 2015). Despite the efforts to mitigate pathways responsible for new introductions, the rate of new invasions is increasing or at least steady (Ricciardi, 2007; Kirkendall and Faccoli, 2010; Roques, 2010a). The pine bark beetles Hylastes ater (Paykull) and Hylurgus ligniperda (F.) (Coleoptera: Scolytinae), native to Eurasia and the Mediterranean region, respectively (Pfeffer, 1995), are successful invaders that became established in many temperate southern hemisphere countries (Wood and Bright, 1992; Brockerhoff et al., 2006a), probably through international trade (Haack, 2001, 2006; Brockerhoff et al., 2006a). Hylurgus ligniperda also became established in the United States. In New Zealand, Hylastes ater and H. ligniperda were detected in 1929 (Clark, 1932) and 1974 (Bain, 1977), respectively, and they are now found throughout most areas where pine forests occur. Both beetle species are not considered pests as they do not attack live trees. Instead, they breed and develop in fresh phloem of trees that died recently, mainly in pine stumps and roots, as well as logging waste (Chararas, 1962). Nevertheless, H. ater may cause some damage due to the maturation feeding carried out by callow adults (during ovarian maturation) on the root collars and tap roots of pine seedlings (Sopow et al., 2015). In addition, both species may act as vectors of sapstain fungi to felled logs (e.g., McCarthy et al., 2010, 2013). Plantation forestry and the export of pine logs are important contributors to New Zealand’s economy (MPI, 2015). To meet the phytosanitary requirements of trading partners, logs are fumigated with methyl bromide or phosphine, or debarked (Pawson et al., 2014); however, these treatments are applied without any a priori assessment of the potential phytosanitary risk (IPPC, 2013) posed by the potential presence of bark beetles on any given shipment. Because both Hylastes ater and H. ligniperda breed in the fresh phloem of recently dead trees, logs can only be attacked once trees

have died or been felled (i.e., post-harvest). As felled logs are temporarily stored at or very close to harvesting areas, there is a window of opportunity where the beetles may infest logs. Therefore, the period of flight activity and how this varies among locations are important to assess phytosanitary risks. In New Zealand, the main adult flight activity of H. ligniperda and H. ater occurs from late August to late May and from January to May, respectively, with lower levels of flight activity occurring from late August to December (Unpublished data, Scion). However, the flight activity period varies among regions (Brockerhoff et al., 2006b), and will be affected also by local climatic variation related to elevation and aspect. Therefore, to determine the post-harvest infestation risk throughout the landscape requires an understanding of how elevation and aspect affect probability and intensity of adult flight activity. Here, we report the results of a study using sites along elevational gradients and at different aspects to determine the effects of local climatic and site factors on the flight activity of H. ater and H. ligniperda. This information will be used to inform models of phytosanitary risk and to assess potential effects of climate change on beetle distribution. We hypothesised that increasing elevation will reduce the flight activity of both species and that during the cooler months flight activity will be longer at warmer northerly aspects than southerly aspects (in the southern hemisphere).

2. Materials and methods 2.1. Study sites and insect trapping The experiment was conducted in Ashley Forest, Canterbury, New Zealand (43.15 S, 172.57 E) in the foothills of the Southern Alps. A total of 36 traps were installed along four transects established in each of three recently clear-cut P. radiata stands (Marshall Rd., Mt. Grey Rd., Berridale Rd.). Each stand had two pairs of parallel transects, two N-exposed and two S-exposed. All transects were positioned on elevation gradients from 435 m (minimum elevation) to 607 m (maximum elevation) to obtain climaticallydifferent sites. The three traps of each transect were separated from each other by approximately 40 m of elevation, providing ‘low’, ‘mid’ and ‘high’ trap locations, with about 30 m between parallel transects (Table 1, Supplementary Table S1). Temperature was monitored using ibutton temperature loggers (DS1922L-F5# Thermochron iButton, Maximm San Jose, CA, US) placed on the south-facing (shaded) side of traps. Mean temperatures and their standard errors at the study sites were calculated as the overall average of mean hourly temperature readings between 9:00 am and 8:00 pm from 18 February to 3 April 2013. iButton sensors were suspended from the traps and not placed inside Stevenson screens, hence they are subject to the effects of precipitation and direct radiant heat. As all ibuttons were placed in the same place on the trap they do provide a measure of

Table 1 Mean elevation and temperature (± standard error) at sites of differing elevation and aspect. Site

Elevation (m) Mean temperature (°C)

Aspect

N

N S N

18 18 18

S

18

Elevation Low

Mid

High

495 500 20.8 (±0.34) 19.9 (±0.30)

533 541 20.7 (±0.31) 19.1 (±0.28)

571 577 20.0 (±0.29) 18.7 (±0.29)

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random location effects was assumed to be proportional to the mean, and to have a first-order autoregressive covariance structure within each location to account for a lack of independence due to repeated measures of catch rate over time for each trap. These models include interaction terms for aspect
time and elevation
time to account for differences in the way the catch rate varied over time in relation to elevation and aspect. Initially, the models also included a quadratic elevation term to account for any non-linear trend with elevation, but this was found to be statistically non-significant for both species and was therefore eliminated. Type-3 tests as calculated by GLIMMIX were used to test the significance of fixed effects. Predicted catches per 100 trap days with standard errors were calculated and graphed for each fortnight, by aspect (North and South), and for three elevations (ca. 480 m, 530 m, and 580 m). Results from the model output for a 480–580 m elevational gradient are reported. Tests of differences in catch rate between aspects were obtained by fortnight. Similarly, tests of the significance of elevation were obtained by fortnight.

comparison between traps. Mean temperatures differed by approximately 1°C between the upper and lower elevation as well as between north and south-facing sites (Table 1). On 11 February 2013, 36 black cross-vane interception traps were installed with dry cups. Traps were made from two 600 mm
210 mm MulfluteTM polypropylene sheets (Mulford International, Christchurch, New Zealand) and baited with apinene and ethanol on the day of installation in the field. Ethanol was sourced from Nuplex Specialties NZ (Mt. Wellington, New Zealand) and a-pinene (‘PINECHEM 500’) from Lawter (N.Z.) (Mt. Maunganui, New Zealand). The attractants were in separate 150-ml dispensers made from 450
50 mm, 150 lm polyethylene tubing with felt strips (see Brockerhoff et al. (2006b) for details). Traps contents were checked weekly until 7 June 2013 and all trapped beetles of the target species were identified under a stereo microscope and counted. 2.2. Statistical analysis Trap counts were summed across fortnightly intervals starting from 11 February until 5 May (and a final quasi ‘fortnightly’ interval from 5 May to 7 June as counts were low towards the end of the flight season). Counts were converted into catches per 100 trap days, calculated for each of the 18 locations (with each location consisting of a pair of traps) for the two most commonly trapped beetle species, H. ligniperda and H. ater. Generalized linear models using Poisson error functions were used to model fortnightly catches (transformed to per 100 trap days) for these two species, with all models fitted using the SAS Version 9.3 GLIMMIX procedure. The models tested the effects on catch rate of elevation, aspect, and time. A random location effect was included to account for local site variation in the catch rate. The models assume that the expected catch rate was conditional on this random effect, as follows:

EðY ij jLi Þ ¼ expða þ bEi þ cAi þ Li þ aj þ bj Ei þ cj Ai Þ

3. Results The three most common species of bark- and wood-boring beetles associated with pine forests in New Zealand were caught in this study: the bark beetles Hylurgus ligniperda and Hylastes ater, and the burnt pine longhorn beetle Arhopalus ferus (Mulsant) (Coleoptera: Cerambycidae). Hylurgus ligniperda was the most abundant species with a total of 45,363 trapped adults (about 1260 per trap), followed by Hylastes ater with a total of 6676 trapped adults (about 185 per trap). Because only 100 A. ferus were trapped (about 2.7 per trap) no analysis was carried out. There were significant effects of elevation (P = 0.005) and time (P < 0.0001) on the overall flight activity of H. ligniperda, while aspect was not significant as a main factor (Supplementary Table S2). However, there were significant ‘‘elevation by time” and ‘‘aspect by time” interactions (Supplementary Table S2). Flight activity was significantly higher at lower elevations during the beginning and the peak of the autumn flight (Fig. 1). Catches appeared to remain inversely related to elevation until near the end of the flight period, but this was not significant after early March (Fig. 1). The significant ‘‘elevation by time” and ‘‘aspect by time” interactions are probably related to differences in the magnitude (and sign) of fortnightly catches. For example, the effects of aspect varied over time but there were significantly greater catches at warmer north-facing than south-facing sites towards the end of the season (Fig. 1b). Overall, H. ligniperda was less active at higher elevations than lower elevation (Fig. 1a).

ð1Þ

where – Yij is count per 100 trap days at location i and time j (j = 1 to 7 indicates the fortnight number during the course of the study), – Li is the random location effect assumed to be independently, identically, normally distributed with zero mean, – Ei is elevation at location i, and – Ai is an indicator variable representing aspect at location i (South = 0, North = 1). The fixed effect parameters in the model are: a, the intercept; b, the effect of elevation; c, the effect of aspect (north versus south); aj, the effect of time j; bj, the effect of elevation at time j; and cj, the effect of aspect at time j. The variance of Yij conditional on the

2500

**

(a)

4000 ns

*

ns

480 m

ns

530 m

2000

580 m ns ns

0 30/Jan

1/Mar

1/Apr Date

1/May

1/Jun

Catches per 100 trap days

Catches per 100 trap days

6000

ns

(b)

ns ns

2000 1500

ns

ns

North

1000

*

500 0 30/Jan

South **

1/Mar

1/Apr

1/May

1/Jun

Date

Fig. 1. Predicted trap catch of H. ligniperda as a function of elevation (a) and aspect (b). Error bars show standard errors. Significant differences between elevations or aspects at a given date are expressed as: ns P > 0.05, * P < 0.05, and ** P < 0.01.

135

1000 (a) 900 800 700 600 500 400 300 200 100 0 30/Jan

800

**

ns

480 m

**

**

**

1/Mar

530 m 580 m

*

*

1/Apr

1/May

1/Jun

Date

Catches per 100 trap days

Catches per 100 trap days

E.G. Brockerhoff et al. / Forest Ecology and Management 384 (2017) 132–136

700

**

(b)

600

ns

500 400

North

300

ns

100 0 30/Jan

*

ns

1/Mar

South

**

200 ns

1/Apr

1/May

1/Jun

Date

Fig. 2. Predicted trap catch of H. ater as a function of elevation (a) and aspect (b). Error bars show standard errors. Significant differences between elevations or aspects at a given date are expressed as: ns P > 0.05, * P < 0.05, and ** P < 0.01.

The results for H. ater were broadly similar to those for H. ligniperda; however, all three main effects (elevation, aspect and time) and the ‘‘elevation by time” and ‘‘aspect by time” interactions were significant (Supplementary Table S3). The numbers of adults trapped were significantly greater at lower elevations (P = 0.0036) during most of the flight period from late February until May (Fig. 2a). In addition, flight activity appeared to peak two weeks later at the higher elevations (530 m and 580 m) than at the lower elevation (480 m) (Fig. 2a). Overall, there was considerably more flight activity at north-facing than south-facing sites (P = 0.0059), and towards the end of the flight season, significantly greater catches were recorded at north-facing sites (Fig. 2b). In both species, H. ater and H. ligniperda, total catches were considerably greater at lower elevations than at the two higher elevations (Figs. 1 and 2). At northerly aspects, total catches of H. ater were almost double those at southerly aspects, whereas there was no overall-difference in H. ligniperda. The significant elevation by time and aspect by time interactions in both species (Tables S2 and S3) are due to increased catches at lower elevations during the beginning of the flight season and at north-facing sites towards the end of the flight season. Taken together, this effectively led to extended flight periods at lower elevations (flights beginning earlier) and at north-facing sites (flights lasting longer). 4. Discussion Prior to our study it was not known what the effects of elevation and aspect effects are on the flight activity and phenology of bark beetle populations in New Zealand. Our results show that the flight activity of H. ligniperda and H. ater is clearly influenced by elevation and aspect. This is relevant to New Zealand forests which are frequently located in hill country and mountainous areas, as in many other parts of the world. Our results indicate that flight activity decreased with increasing elevation and there was a tendency for delayed activity at higher elevations. Furthermore, flight activity occurred for a longer period into autumn at northerly aspects. These topographic effects varied over time and, overall, were consistent with expectations, based on known relationships between topography, microclimate and insect development. Bark beetle flight activity is fundamentally temperature-dependent and thus topography (e.g., elevation and aspect) will directly and indirectly affect flight activity due to their influence on air and phloem temperatures (Bentz et al., 2014, 2016; Chen et al., 2015). Ultimately, phloem temperatures also determine the rate of development of immature stages of bark beetles. For example, in the mountain pine beetle (Dendroctonus ponderosae), eggs and early instar larvae do not develop below temperatures of 5.6°C and later instars and pupae require at least 15°C (Safranyik and Whitney, 1985; Régnière et al., 2012), and this influences beetle phenology and

even voltinism (Bentz et al., 2014). Similar results were found also in Europe regarding the spruce bark beetle Ips typographus (Wermelinger and Seifert, 1999). Understanding beetle responses to changes in the local and regional climate is important as climate change has been identified as an important factor in outbreaks of bark beetles such as species of Dendroctonus (Bentz et al., 2010) and Ips (Marini et al., 2012). Although the alien pine bark beetles present in New Zealand (H. ater and H. ligniperda) are only minor pests, it would be a concern if changing climatic conditions led to increased flight activity and abundance and enhanced suitability of sites that are currently less favourable. Here, the main issue would be that the presence of beetles on logs could increase in terms of greater abundance, extended duration of times of flight activity, or more widespread occurrence at sites that are currently not supporting substantial populations. The temperature gradients we observed across the elevational gradient and between southerly and northerly aspects are relevant as they correspond with the climate change projections for mean maximum summer temperature increases of 1.0–1.25°C by the 2040 s according to HadCM3-UKMO model outputs for this area of New Zealand (Kean et al., 2015). Irrespective of climate change effects, such variation in flight activity within the landscape as a function of seasonal changes in temperature provides a potential opportunity to identify spatial regions and temporal periods when bark beetle activity is minimal or absent. From a phytosanitary perspective the potential for infestation of recently harvested logs and thus the location and extent of ‘Areas of Low Pest Prevalence’ (ALPP) (IPPC, 2005), will be seasonally dependent and influenced by both elevation and aspect. In Chile, Mausel et al. (2007) also recognised spatial factors that affect the potential post-harvest colonisation risk. In their case they recommended that medium to long-term storage of logs should occur in mature forest stands to reduce the likelihood of infestation as the abundance of H. ligniperda and H. ater was lower in such stands compared to recent clear-cuts. Similarly Rossi et al. (2009) highlighted the importance of removing harvested logs quickly from areas with a high abundance of Ips sexdentatus during outbreak conditions in France. Storage of logs close to attacked trees resulted in a ‘facilitation effect’ that compounded the outbreak by providing host material adjacent to infested trees. Our results suggest that the potential for post-harvest infestation of logs during temporary storage at skid sites may be reduced by preferentially harvesting logs from stands with reduced flight activity (i.e., southerly aspects and higher elevations) during periods when other sites have an increased risk of exposure. Sites that are north-facing and at lower elevations could then be harvested during the winter when there is a greatly reduced or no flight activity. Furthermore, low risk sites could be chosen to reduce the risk of infestation during the period of temporary storage on

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skid sites in the forest by establishing skid sites in areas of low flight activity on southerly aspects and at higher elevations. Acknowledgements The authors thank Jessica Kerr, Brooke O’Connor, and Matthew Scott for assistance in collecting and identifying insects. Rayonier| Matariki forests kindly provided access to forest stands. We thank Jack Armstrong, Lindsay Bulman and an anonymous reviewer for comments on earlier versions of the manuscript. This work was funded by the New Zealand Ministry for Business, Innovation and Employment (MBIE, contract C04X1204), Stakeholders in Methyl Bromide Reduction, and Scion’s core funding from MBIE (contract C04X1104). Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.foreco.2016.10. 046. References Aukema, J.E., McCullough, D.G., Von Holle, B., Liebhold, A.M., Britton, K., Frankel, S.J., 2010. Historical accumulation of nonindigenous forest pests in the continental United States. Bioscience 60, 886–897. Aukema, J.E., Leung, B., Kovacs, K., Chivers, C., Britton, K.O., Englin, J., Frankel, S.J., Haight, R.G., Holmes, T.P., Liebhold, A.M., McCullough, D.G., Von Holle, B., 2011. Economic impacts of non-native forest insects in the continental United States. PLoS ONE 6, e24587. Bain, J., 1977. Hylurgus Ligniperda (Fabricius) (Coleoptera: Scolytidae). Forest and Timber Insects in New Zealand No. 18. New Zealand Forest Service, Rotorua. Battisti, A., Stastny, M., Netherer, S., Robinet, C., Schopf, A., Roques, A., Larsson, S., 2005. Expansion of geographic range in the pine processionary moth caused by increased winter temperature. Ecol. Appl. 15, 2084–2096. Bentz, B.J., Régnière, J., Fettig, C.J., Hansen, E.M., Hayes, J.L., Hicke, J.A., Kelsey, R.G., Negrón, J.F., Seybold, S.J., 2010. Climate change and bark beetles of the western United States and Canada: direct and indirect effects. Bioscience 60, 602–613. Bentz, B., Vandygriff, J., Jensen, C., Coleman, T., Maloney, P., Smith, S., Grady, A., Schen-Langenheim, G., 2014. Mountain pine beetle voltinism and life history characteristics across latitudinal and elevational gradients in the western United States. For. Sci. 60, 434–449. Bentz, B.J., Duncan, J.P., Powell, J.A., 2016. Elevational shifts in thermal suitability for mountain pine beetle population growth in a changing climate. Forestry 89, 271–283. Brockerhoff, E.G., Bain, J., Kimberley, M.O., Knízˇek, 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. Brockerhoff, E.G., Jones, D.C., Kimberley, M.O., Suckling, D.M., Donaldson, T., 2006b. Nationwide survey for invasive wood-boring and bark beetles (Coleoptera) using traps with pheromones and kairomones. For. Ecol. Manage. 228, 234–240. Brockerhoff, E.G., Kimberley, M., Liebhold, A.M., Haack, R.A., Cavey, J.F., 2014. Predicting how altering propagule pressure changes establishment rates of biological invaders across species pools. Ecology 95 (3), 594–601. Chararas, C., 1962. Étude Biologique Des Scolytides Des Conifères. Paul Lechevalier, Paris. Chen, H., Jackson, P.L., Ott, P.K., Spittlehouse, D.L., 2015. A spatiotemporal pattern analysis of potential mountain pine beetle emergence in British Columbia, Canada. For. Ecol. Manage. 337, 11–19. http://dx.doi.org/10.1016/ j.foreco.2014.10.034. Clark, A.F., 1932. The pine bark beetle, Hylastes ater, in New Zealand. New Zeal. J. Sci. Technol. 14, 1–20. Creeden, E.P., Hicke, J.A., Buotte, P.C., 2014. Climate, weather, and recent mountain pine beetle outbreaks in the western United States. For. Ecol. Manage. 312, 239– 251. http://dx.doi.org/10.1016/j.foreco.2013.09.051. FAO, 2015. Global Forest Resources Assessment 2015: How Are the World’s Forests Changing? Food and Agriculture Organization of the United Nations, Rome. 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. Haack, R.A., 2001. Intercepted Scolytidae (Coleoptera) at U.S. ports of entry: 1985– 2000. Integr. Pest Manage. Rev. 6, 253–282. IPPC, 2005. ISPM22: Requirements for the establishment of areas of low pest prevalence. Secretariat of the International Plant Protection Convention, Food and Agriculture Organization of the United Nations, Rome.

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