EPPO (1998) concluded that D. sibiricus threatens large areas of coniferous forests in northern and central Europe, with the potential to cause serious and destructive epidemics. A PRA by EPPO (2000) concluded that the entry of D. sibiricus into the EPPO region is more likely to occur by natural spread and import of untreated wood with bark, dunnage or packing material, and less likely to occur with import of host plants for planting and cut branches. EPPO (2000) concluded that there is high probability of D. sibiricus establishment in the EPPO region. The potential impact within the EPPO region was considered to be high, including both direct damage to coniferous plantations and forests (mainly Abies spp., Larix spp., Picea spp., and Pinus spp.) resulting in wood losses, environmental damage to natural forests, including deforestation over large areas and social damage to people living in the damaged areas (EPPO 2000).
In a PRA for Poland, Kubasik et al. (2017) concluded that D. sibiricus poses a potentially very high threat to the domestic forests, because of the high proportion of coniferous trees, and if the pest enters Poland, suitable climatic conditions facilitate establishment of the pest. However, due to limited import of relevant coniferous commodities to Poland, the probability of introduction was considered low (Kubasik et al. 2017).
A Pest Categorization of D. sibiricus by EFSA Panel on Plant Health (EFSA 2018) stated that the previous contradictory studies regarding the climatic requirements of D. sibiricus make the issue of its establishment in most of Europe uncertain, although the host plants are widely present. All criteria for considering D. sibiricus a potential quarantine pest are met, but the pest is presently absent from EU, and the criteria for consideration as a potential regulated, non-quarantine pest are not met (EFSA 2018).
Identification of human mediated pathways for entry
The potential pathways for entry of D. sibiricus are by human mediated spread and by natural spread. The three human mediated pathways for entry of the pest considered in this PRA are: Living coniferous trees, coniferous wood in the rough, and foliage and branches.
Living coniferous trees
The probability of entry of D. sibiricus with import of the commodity “Living coniferous trees” is considered as unlikely with a medium level of uncertainty.
During the past 30 years, there has been no import to Norway of trees for planting of Abies spp., Larix spp., Picea spp. and Pinus spp. from Russia. However, during the past 20 years there have been small numbers of coniferous plants (unknown species) shipped to Norway from China. There has been no recent import of coniferous trees from Russia to Sweden, and only 12.4 metric tons of coniferous trees has been exported from Russia to Finland during recent years (Eurostat 2017).
Coniferous wood in the rough
The probability of entry of D. sibiricus with import of the commodity “Coniferous wood in the rough” to Norway is considered as unlikely with a medium level of uncertainty.
There have been substantial import of the commodity “Coniferous wood in the rough” (trade code 44.03) from Russia to Norway during the past 30 years, but the import has declined since 2000, and from 2016 there has been no import (Fig. 2). If containing bark these products may carry eggs, larvae and imago of the pest. The category with the highest volume, “Wood for pulping of spruce or other coniferous species” (trade code 44.03.2006) sums up to 1.508.417 metric tons over 16 out of 20 years and peaked in 1999 (Fig. 2). The category, “Coniferous sawn wood” (trade code 44.03.2001) adds up to 1.136.599 metric tons over 16 years and peaked in 2000. The category “Wood for pulping” (trade code 44.03.2009) sums up to 127.687 metric tons over 12 out of 20 years and peaked in 2000, and “Wood for pulping of pine” (trade code 44.03.2005) sums up to 80.068 metric tons over 12 out of 20 years and peaked in 1994 (Fig. 2). During the last years, only 0.67 metric tons of “Coniferous sawn wood” (trade code 44.03.2001) were imported from Japan to Norway in 1992. Some of the sub-categories of trade code 44.03 may have contained Abies spp., Larix spp., Picea spp., or Pinus spp. The custom statistics do not reveal the origin of the respective commodities within Russia.
Trade in conifer products with bark from European Russia is not regulated in the same way as is trade from countries outside Europe. This is of concern, since European Russia includes several climate types and ecoregions, potentially harboring a number of unwanted species. Especially, the import of coniferous wood with bark, originating east of the Ural Mountains (approximately 60th meridian east), represents a considerable risk for entry of D. sibiricus. The decline and cessation of timber imports from Russia during the last decades may reflect a declining paper and pulp industry in Norway. The import of relevant commodities have shown high variability in the past. In some cases, the volume of a commodity has changed more than 100% from 1 year to the next (Økland et al. 2012).
Foliage and branches
The probability of entry of D. sibiricus with import of coniferous foliage and branches to Norway is considered as unlikely with a high level of uncertainty.
The commodity “Foliage, branches and other parts of plants” may include coniferous wood with bark and other coniferous items that can host D. sibiricus. However, only a small volume of “Foliage, branches and other parts of plants” (˂0.5 metric tons) entered the PRA-area from Russia in 1998, and since then there has been no import of these commodities from Russia in 1998 (Fig. 2).
Natural spread as pathway for entry of the pest
The probability of natural spread as pathway for entry of D. sibiricus is considered as unlikely with a medium level of uncertainty.
Dendrolimus sibiricus is not expected to spread naturally from its current Western distribution limit in Russia to Norway within the next couple of decades. In a worst-case scenario, where D. sibiricus spreads westwards from Moscow at a rate of 50 km per year (EPPO 2005), it would take more than 30 years for the species to reach Norway. Natural spread of D. sibiricus from the Moscow region to Norway would probably require the insect to fly north of the Gulf of Bothnia.
Based on the current data, it is difficult to conclude that there is no westward movement of the species. However, historical observations indicate that the westward spread may be very slow or non-existent. Dendrolimus sibiricus has probably been present in the Urals since the late nineteenth century or early twentieth century, without expanding westwards (Mikkola and Ståhls 2008). Petersen (1909) judged the western limit of distribution of D. sibiricus to be at the 59th meridian east, while Eversmann (1844) and Mikkola and Ståhls (2008) reported it to be at the 58th and 56th meridian east, respectively. According to Gninenko and Orlinskii (2002), D. sibiricus is found in the regions of Perm and Udmurtiya, around 52th meridian east. Rozhkov (1963) and Koltunov et al. (1997) judged the western limit of D. sibiricus to be approximately at the 52th meridian east. However, Okunev (1955) reported D. sibiricus as far west as the 38th meridian east.
The estimated westward spread of 50 km/year for D. sibiricus, reported by EPPO (2005) and by Möykkynen and Pukkala (2014) was probably based on the assumption that D. sibiricus is present in the Moscow area, which is not considered as a valid basis in the present assessment. There were no citations or calculations given for the dispersal estimat of 50 km/year by these authors.
Baranchikov et al. (2006) maintained that D. sibiricus is not present in the Republic of Mari El (47th meridian east). However, according to Oleg A. Kulinich (personal communication), Russian NPPO in 2016 registered D. sibiricus in the Republic of Mari El, in the Republic of Chuvash (approximately 47th meridian east) and in the Kirov region (50th meridian east) (Fig. 1). To our knowledge D. sibiricus has never been recaptured in the Moscow oblast or west of Moscow, during the 16 years since the first peste reported findings by Gninenko and Orlinskii (2002).
In agreement with Mikkola and Stahls (2008) and Baranchikov et al. (2006), the conclusion is that the natural westward spread of D. sibiricus in European Russia is very slow or non-existent.
Probability of the pest being associated with the pathways
The overall probability of the pest being associated with the pathways is considered as very likely with high uncertainty.
For the pathway “Coniferous wood in the rough” it is probable that under non-outbreak conditions the pest occurrence has low density throughout the area of distribution during the summer. Therefore, during logging it is impossible to distinguish between trees infested with D. sibiricus larvae and non-infested trees. However, imago, larvae and cocoons will not be present when logging during the winter since overwintering larvae hibernate in the ground, in the soil and under litter.
Regarding the commodities “Living coniferous trees” and “Foliage and branches” the pest occurrence may be at a low density throughout the area of distribution during the summer. In addition, the pest could be present in the soil during the winter in immediate proximity to the trees.
Probability of pest survival during transport and storage
The overall probability of the pest to survive during transport and storage is moderately likely with high uncertainty.
The highest probability of survival of D. sibiricus is in the commodities “Living coniferous trees” and “Foliage, branches and other parts of plants”, because these commodities are handled more carefully and are transported in protected consignments. For the commodity “Coniferous wood in the rough”, eggs, larvae, cocoons and imago would be vulnerable to physical and environmental stresses during transport and storage, as these stages live on needles and branches of the trees and may easily be crushed during transport and storage. The commodity “Coniferous wood in the rough” are cut trees without any needles and branches and, therefore, might be less suitable for survival of the larvae and imago.
There are no commercial procedures applied to any of the above-mentioned commodities that would decrease the probability of survival during transport or storage, if phytosanitary measures are not applied.
Probability of pest surviving existing pest management procedures
The overall probability of the pest to survive existing pest management procedures is unlikely with medium uncertainty.
Import into Norway of plants, wood with bark and chips of wood with bark, isolated bark and wood waste of Coniferales from Non-European countries and Portugal is prohibited (Norwegian Ministry of Agriculture and Food 2018). Dendrolimus sibiricus is included in the EU Plant Health Legislation by EU Directive 2000/29 Annex I/AI, requiring a phytosanitary certificate issued by Russia, ensuring that plants and plant products are inspected and free from D. sibiricus (Council Directive 2000/29/EC 2000).
Probability of transfer to a suitable host
The probability for the pest to transfer to a suitable host is likely with low uncertainty.
Both wood in the rough and plants for planting arrive all year round, and these commodities are usually stored outdoors. Therefore, with its flight ability D. sibiricus will be able to reach suitable hosts.
Conclusions on the probability of entry
In conclusion, the probability of entry of D. sibiricus from areas outside of the PRA area to a suitable habitat within the PRA area is considered as unlikely with a medium level of uncertainty.
The assessment behind this conclusion is that the overall probability of entry by human mediated pathways is unlikely with a medium level of uncertainty. The probability of natural spread as a pathway for entry of D. sibiricus to the PRA area is unlikely with medium uncertainty, while the rating of the probability of natural spread as an entry of D. sibericus to the PRA-area is very unlikely with low uncertainty.
Probability of establishment in the PRA area
Climate suitability
The establishment of D. sibirica in the climate of the PRA area is moderately likely with high uncertainty.
Möykkynen and Pukkala (2014) concluded that the climate in central and northern Europe is favourable for establishment of D. sibiricus. The basis for their analysis was a CLIMEX model originally parameterised by Flament et al. (2013). However, in the latter study, the authors based the parameter fitting partly on the map “Siberian moth distribution and areas of injuries”, drawn by Rozhkov (1963), except for the mapped western distribution limit. This seems to be a key assumption with respect to the results of Flament et al. (2013) for the projected distribution for D. sibiricus concerning the risk of establishment in the PRA area of Norway. While Rozhkov (1963) focused on areas of injuries, Flament et al. (2013) was more focused on the potential geographical distribution of the organism.
The CLIMEX model does not consider the effect of snow cover. For a species having a strategy of overwintering on the ground, or below ground, the CLIMEX model will have important shortcomings with respect to predicting the actual climatic conditions that ground dwelling, or below ground dwelling species, experience in areas with regular snow cover during the winter. Therefore, the CLIMEX model developed by Flament et al. (2013) is not able to predict winter survival for D. sibiricus outside its current distribution. In addition, Baranchikov et al. (2010) assessed the potential distribution of D. sibiricus by applying a bioclimatic model, and they concluded that the potential for distribution is more constrained than Flament et al. (2013) suggested. Milder winter conditions in European Russia than in Siberia may be a limiting factor, as successful overwintering of larvae requires continuous, continental-type winters. A large part of Siberia is climatically suitable for D. sibiricus by Baranchikov et al. (2010), and the potential distribution closely matches the existing distribution of the pest in Siberia. However, for both studies the supporting information on presence/absence data is very sparse. Baranchikov et al. (2006) questioned the theory that the limited distribution of D. sibiricus west of the Ural Mountains is due to mild winters. The current distribution areas of D. sibiricus have a more continental climate, (monthly maximum temperatures minus monthly minimum temperatures), i.e. a higher temperature change over the course of the year (Fig. 3) and less precipitation (Fig. 4) than the PRA-area (Kharuk and Antamoshkina 2017). Even in the far east of Russia, where D. sibiricus is present to the city of Vladivostok on the Pacific coast, the climate is dominated by cold, dry winters and warm summers with low precipitation.
Dendrolimus sibiricus outbreaks are associated with high summer temperatures (Fig. 5) and low precipitation during the summer, causing drought (Fig. 4). This is similar to the climate requirements of the European species D. pini (Haynes et al. 2014). Drought stress has been shown to lower the quantity of defensive compounds in the host trees, which make the trees more susceptible to attack (Netherer et al. 2015). In proximity to the oceans, trees experience a more humid climate with milder winters, less extreme temperature fluctuations and less drought than in continental climates. Successful overwintering of D. sibiricus larvae requires continuous winters of a continental type with no autumn thaws, as temperature fluctuations are fatal for the larvae (Baranchikov et al. 2010). Therefore, stable sub-zero winter temperatures are probably important for the D. sibiricus larvae (Fig. 6).
Natural enemies
Telenomus tetratomus Kieffer 1906 is an important insect egg parasitoid, which regulates the population densities of several insect species in Russia under non-outbreak conditions (EPPO 2005). This species is also present in Norway, where it attacks D. pini eggs (Adolfsson 1984). In Scandinavia, there are several other species of parasitoids on D. pini some of which may also attack D. sibiricus (Adolfsson 1984), There are large numbers of parasitoides attacking D. sibiricus in Russia (EPPO 2005), and some of these may be present in Norway.
Conclusion on the probability of establishment
The probability of D. sibiricus establishment in the PRA area is unlikely with medium uncertainty.
The PRA area has two potential hosts, Picea abies and Pinus sylvestris, both of which are widely distributed within the country. However, these species are regarded as intermediate and poor hosts, respectively. In addition, most of the PRA-area has a suboptimal environmental condition, with winter temperatures that are not sufficiently cold and with too much precipitation in the summer to allow establishment. The potential of D. sibiricus to adapt to new environments is unknown. However, the life cycle of the pest is dynamic, which may be beneficial for adaption to new and adverse conditions. Dendrolimus sibiricus has never been intercepted outside its main area of distribution, and in Russia there is no or very slow speed westwards. There are currently no import of commodities that could support entry of D. sibiricus into the PRA-area.
Probability of spread after establishment
The probability of D. sibiricus spread after establishment in the PRA area is likely with high uncertainty.
The exact flight capacity of D. sibiricus is unknown, but its behaviour probably depends on the density of suitable host trees, where the pest will seek out the nearest suitable host. However, D. sibiricus adults are strong flyers, and they are reported to fly up to 100 km per year (EPPO 2005). Wind direction and wind strength will strongly affect the spread of the moths. In addition, the movement of the commodities: “Living coniferous trees”, “Wood in the rough” and “Foliage or branches” may further aid long-distance spread after establishment.
Endangered area within the PRA area
The part of the PRA area, where ecological factors may be favourable for establishment, are the areas with the coldest and continuous winters, and the warmest and driest summers. This includes the areas furthest away from the moderating effects of the Atlantic Ocean, which are the counties of Akershus, Hedmark, Oppland, and possibly inner parts of Finnmark.
Assessment of impact
Dendrolimus sibiricus is among the most important defoliators and the most destructive pests of conifers in its natural habitat in Russia. In the period from 1994 to 1996, D. sibiricus damaged 700.000 ha of pine forest in the Krasnoyarsk krai (Zhirin et al. 2016), and between 1954 and 1957 the pest killed over 1.5 million hectares of pine near the Ket and Chulym rivers (Kharuk et al. 2016). During a period of 25 years, between 1932 and 1957, D. sibiricus damaged 7 million hectares of forest and killed 50% of the trees in West Siberia and Chita Oblast in South East Siberia (Baranchikov and Montgomery 2014, EPPO 2005). In China, D. sibiricus is considered a major defoliator of the Dahurian larch, Larix gmelinii (Rupr.) Kuzeneva (EPPO 2005).
Continuous defoliation by D. sibiricus may cause death of forests over large areas, either directly or by leaving forests prone to subsequent attacks by other forest pests, such as woodborers in the families Scolytidae and Cerambycidae (EPPO 2005). In addition, outbreaks may make the forests more predisposed to forest fires (EPPO 2005). The reestablishment of forests after an outbreak is complicated (EPPO 2005), and consequently the attack may lead to major changes in the environment and biodiversity.
In bioassay experiments with D. sibiricus, the two Norwegian potential hosts, P. abies and P. sylvestris, were described as intermediate and poor hosts, respectively (Kirichenko et al. 2011). However, it is unknown how severe the impact would be under Norwegian climatic conditions, which are regarded as suboptimal. Severe damage caused by outbreaks of D. sibiricus in Norway would probably require several years of drought stressed host trees, similar to the circumstances observed during the latest outbreaks of D. pini in Hedmark County during 1812–1816 and 1902–1904. Interactions between D. sibiricus and D. pini could possibly result in more severe outbreaks than those caused by D. pini alone.
