Bark Beetle Population Dynamics in the Anthropocene: Challenges and Solutions
Authors: Peter H.W. Biedermann, Jörg Müller, Jean-Claude Grégoire, Axel Gruppe, Jonas Hagge, Almuth Hammerbacher, Richard W. Hofstetter, Dineshkumar Kandasamy, Miroslav Kolarik, Martin Kostovcik, Paal Krokene, Aurélien Sallé, Diana L. Six, Tabea Turrini, Dan Vanderpool, Michael J. Wingfield, Claus Bässler
Journal: Trends in Ecology & Evolution (2019)

Bark beetles are currently causing unprecedented damage to European and North American forests.Their population dynamics rarely have been studied in a hypothesis-driven manner incorporating exogenous biotic variables.We propose a conceptual framework to reveal the drivers of bark beetle populations.This approach can be equally applied to other eruptive insect pests. Tree-killing bark beetles are the most economically important insects in conifer forests worldwide. However, despite >200 years of research, the drivers of population eruptions and crashes are still not fully understood and the existing knowledge is thus insufficient to face the challenges posed by the Anthropocene. We critically analyze potential biotic and abiotic drivers of population dynamics of an exemplary species, the European spruce bark beetle (ESBB) (Ips typographus) and present a multivariate approach that integrates the many drivers governing this bark beetle system. We call for hypothesis-driven, large-scale collaborative research efforts to improve our understanding of the population dynamics of this and other bark beetle pests. Our approach can serve as a blueprint for tackling other eruptive forest insects. Tree-killing bark beetles are the most economically important insects in conifer forests worldwide. However, despite >200 years of research, the drivers of population eruptions and crashes are still not fully understood and the existing knowledge is thus insufficient to face the challenges posed by the Anthropocene. We critically analyze potential biotic and abiotic drivers of population dynamics of an exemplary species, the European spruce bark beetle (ESBB) (Ips typographus) and present a multivariate approach that integrates the many drivers governing this bark beetle system. We call for hypothesis-driven, large-scale collaborative research efforts to improve our understanding of the population dynamics of this and other bark beetle pests. Our approach can serve as a blueprint for tackling other eruptive forest insects. The abundance of an organism is determined by a variety of factors related to intra- and interspecific biotic interactions as well as abiotic conditions [1.Thompson J.N. The Coevolutionary Process. University of Chicago Press, 1994Crossref Google Scholar]. In forest ecology, researchers have been fascinated and challenged by the diversity of drivers that govern the eruptive population dynamics of foliage-feeding moths (various Lepidoptera families) and tree-killing bark beetles (see Glossary) (Coleoptera: Scolytinae), including the influence of host trees, symbionts, natural enemies, and competitors (Table 1) as well as climate and land use [2.Weed A.S. et al.Population dynamics of bark beetles.in: Vega F.E. Hofstetter R.W. Bark Beetles: Biology and Ecology of Native and Invasive Species. Academic Press, 2015: 157-176Crossref Scopus (12) Google Scholar, 3.Lindgren B.S. Raffa K.F. Evolution of tree killing in bark beetles (Coleoptera: Curculionidae): trade-offs between the maddening crowds and a sticky situation.Can. Entomol. 2013; 145: 471-495Crossref Scopus (56) Google Scholar, 4.Safranyik L. Carroll A.L. The biology and epidemiology of the mountain pine beetle in lodgepole pine forests.in: Safranyik L. Wilson W.R. The Mountain Pine Beetle: A Synthesis of Biology, Management, and Impacts on Lodgepole Pine. Canadian Forest Service, 2006: 3-66Google Scholar, 5.Berryman A.A. The theory and classification of outbreaks.in: Barbosa P. Schultz J.C. Insect Outbreaks. Academic Press, 1987: 3-30Crossref Google Scholar, 6.Myers J.H. Corry J.S. Population cycles in forest lepidoptera: ecology, evolution and impacts of changing climates.Annu. Rev. Ecol. Evol. Syst. 2013; 44: 565-592Crossref Scopus (65) Google Scholar, 7.Myers J.H. Population cycles: generalities, exceptions and remaining mysteries.Proc. Biol. Sci. 2018; 28520172841Crossref PubMed Scopus (33) Google Scholar]. Given that the joint effect of these biotic and abiotic drivers as well as their interactions are still not well understood for many of these insects (Table 1) and their tree hosts [2.Weed A.S. et al.Population dynamics of bark beetles.in: Vega F.E. Hofstetter R.W. Bark Beetles: Biology and Ecology of Native and Invasive Species. Academic Press, 2015: 157-176Crossref Scopus (12) Google Scholar, 4.Safranyik L. Carroll A.L. The biology and epidemiology of the mountain pine beetle in lodgepole pine forests.in: Safranyik L. Wilson W.R. The Mountain Pine Beetle: A Synthesis of Biology, Management, and Impacts on Lodgepole Pine. Canadian Forest Service, 2006: 3-66Google Scholar, 5.Berryman A.A. The theory and classification of outbreaks.in: Barbosa P. Schultz J.C. Insect Outbreaks. Academic Press, 1987: 3-30Crossref Google Scholar, 7.Myers J.H. Population cycles: generalities, exceptions and remaining mysteries.Proc. Biol. Sci. 2018; 28520172841Crossref PubMed Scopus (33) Google Scholar, 8.Kausrud K. et al.Population dynamics in changing environments: the case of an eruptive forest pest species.Biol. Rev. 2012; 87: 34-51Crossref PubMed Scopus (94) Google Scholar, 9.Raffa K.F. et al.Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions.Bioscience. 2008; 58: 501-517Crossref Scopus (1131) Google Scholar], it is questionable whether we are prepared to deal with the challenges our forests face in the Anthropocene (i.e., climatic changes and intensification of forest management) [10.Crutzen P.J. The "Anthropocene".in: Ehlers E. Krafft T. Earth System Science in the Anthropocene. Springer, 2006: 13-18Crossref Scopus (440) Google Scholar].Table 1Exemplary Insect Species That Exhibit Population Outbreaks and Their Biotic Regulators (after 3.Lindgren B.S. Raffa K.F. Evolution of tree killing in bark beetles (Coleoptera: Curculionidae): trade-offs between the maddening crowds and a sticky situation.Can. Entomol. 2013; 145: 471-495Crossref Scopus (56) Google Scholar, 4.Safranyik L. Carroll A.L. The biology and epidemiology of the mountain pine beetle in lodgepole pine forests.in: Safranyik L. Wilson W.R. The Mountain Pine Beetle: A Synthesis of Biology, Management, and Impacts on Lodgepole Pine. Canadian Forest Service, 2006: 3-66Google Scholar, 5.Berryman A.A. The theory and classification of outbreaks.in: Barbosa P. Schultz J.C. Insect Outbreaks. Academic Press, 1987: 3-30Crossref Google Scholar, 6.Myers J.H. Corry J.S. Population cycles in forest lepidoptera: ecology, evolution and impacts of changing climates.Annu. Rev. Ecol. Evol. Syst. 2013; 44: 565-592Crossref Scopus (65) Google Scholar, 7.Myers J.H. Population cycles: generalities, exceptions and remaining mysteries.Proc. Biol. Sci. 2018; 28520172841Crossref PubMed Scopus (33) Google Scholar, 14.Amman G.D. Mountain pine beetle (Coleoptera: Scolytidae) mortality in three types of infestations.Environ. Entomol. 1984; 13: 184-191Crossref Google Scholar, 22.Nealis V. Comparative ecology of conifer-feeding spruce budworms (Lepidoptera: Tortricidae).Can. Entomol. 2016; 148: S33-S57Crossref Scopus (41) Google Scholar, 26.Hofstetter R.W. et al.Symbiotic associations of bark beetles.in: Vega F.E. Hofstetter R.W. Bark Beetles: Biology and Ecology of Native and Invasive Species. Academic Press, 2015: 209-245Crossref Scopus (76) Google Scholar, 34.Wegensteiner R. et al.Natural enemies of bark beetles: predators, parasitoids, pathogens, and nematodes.in: Vega F.E. Hofstetter R.W. Bark Beetles: Biology and Ecology of Native and Invasive Species. Academic Press, 2015: 247-304Crossref Scopus (54) Google Scholar)Main regulatory biotic factoraThe role of other biotic factors and particularly their interaction with the changing abiotic environment [10] are not well understood in any of these systems. acting inInsectTree hostNon-outbreak populationsOutbreak populationsSpruce budworms, Choristoneura spp.ConifersNatural enemies (predators, specialist parasitoids)Food quality, natural enemies (generalist parasitoids)Gypsy moth, Lymantria disparDeciduous treesNatural enemies (predators, parasites)Food depletion, natural enemies (pathogens)European pine sawfly, Neodiprion sertiferPinus spp.Natural enemies (predators)Food depletion, natural enemies (pathogens)European woodwasp, Sirex noctilioConifersHost resistance, natural enemies (parasites)Food depletion, natural enemies (parasites)Australian psyllid, Cardiaspina albitexturaEucalyptus spp.Natural enemies (predators, parasites)Food depletionMountain pine beetle, Dendroctonus ponderosaePinus spp.Host resistance, predators, interspecific competitionHost resistanceSouthern pine beetle, Dendroctonus frontalisPinus spp.Host resistanceHost resistance, natural enemies, mite-associated antagonistic fungiESBB, Ips typographusPicea spp.Host resistance, inter- and intraspecific competitionHost resistance, intraspecific competitiona The role of other biotic factors and particularly their interaction with the changing abiotic environment 10.Crutzen P.J. The "Anthropocene".in: Ehlers E. Krafft T. Earth System Science in the Anthropocene. Springer, 2006: 13-18Crossref Scopus (440) Google Scholar are not well understood in any of these systems. Open table in a new tab Studies on the population dynamics of eruptive forest insects, and particularly bark beetles, currently focus on variables that can be easily measured over large geographic and temporal scales, like insect and tree host abundance, tree host connectivity, and abiotic climatic factors [2.Weed A.S. et al.Population dynamics of bark beetles.in: Vega F.E. Hofstetter R.W. Bark Beetles: Biology and Ecology of Native and Invasive Species. Academic Press, 2015: 157-176Crossref Scopus (12) Google Scholar, 4.Safranyik L. Carroll A.L. The biology and epidemiology of the mountain pine beetle in lodgepole pine forests.in: Safranyik L. Wilson W.R. The Mountain Pine Beetle: A Synthesis of Biology, Management, and Impacts on Lodgepole Pine. Canadian Forest Service, 2006: 3-66Google Scholar, 8.Kausrud K. et al.Population dynamics in changing environments: the case of an eruptive forest pest species.Biol. Rev. 2012; 87: 34-51Crossref PubMed Scopus (94) Google Scholar, 9.Raffa K.F. et al.Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions.Bioscience. 2008; 58: 501-517Crossref Scopus (1131) Google Scholar, 11.Marini L. et al.Climate drivers of bark beetle outbreak dynamics in Norway spruce forests.Ecography. 2017; 40: 1426-1435Crossref Scopus (134) Google Scholar]. By contrast, other biotic factors are more difficult to measure at large scales and thus there is a lack of understanding of their roles in regulating insect abundances. Support for their importance comes from small-scale studies on the effects of antagonistic symbionts [12.Hofstetter R.W. et al.Antagonisms, mutualisms and commensalisms affect outbreak dynamics of the southern pine beetle.Oecologia. 2006; 147: 679-691Crossref PubMed Scopus (122) Google Scholar, 13.Myers J. Cory J. Ecology and evolution of pathogens in natural populations of Lepidoptera.Evol. Appl. 2015; 9: 231-247Crossref PubMed Scopus (48) Google Scholar], natural enemies [6.Myers J.H. Corry J.S. Population cycles in forest lepidoptera: ecology, evolution and impacts of changing climates.Annu. Rev. Ecol. Evol. Syst. 2013; 44: 565-592Crossref Scopus (65) Google Scholar, 7.Myers J.H. Population cycles: generalities, exceptions and remaining mysteries.Proc. Biol. Sci. 2018; 28520172841Crossref PubMed Scopus (33) Google Scholar, 14.Amman G.D. Mountain pine beetle (Coleoptera: Scolytidae) mortality in three types of infestations.Environ. 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Entomol. 2007; 32: 162-171Crossref Scopus (23) Google Scholar] on the population dynamics of bark beetles, moths, and other eruptive forest insects (Table 1). Moreover, studies usually focus on examining the factors driving outbreaks but largely neglect the equally important causes of population collapse. For example, in cases with abundant but healthy host trees, collapse is often attributed to the absence of factors known to facilitate outbreaks (e.g., poor tree health [20.Marini L. et al.Population dynamics of the spruce bark beetle: a long-term study.Oikos. 2013; 122: 1768-1776Crossref Scopus (65) Google Scholar, 21.Stadelmann G. et al.Effects of salvage logging and sanitation felling on bark beetle (Ips typographus L.) infestations.For. Ecol. Manag. 2013; 305: 273-281Crossref Scopus (67) Google Scholar]). This is an oversimplification, however, because factors regulating non-outbreak populations are typically different from the ones regulating outbreak populations (Table 1; [4.Safranyik L. Carroll A.L. The biology and epidemiology of the mountain pine beetle in lodgepole pine forests.in: Safranyik L. Wilson W.R. The Mountain Pine Beetle: A Synthesis of Biology, Management, and Impacts on Lodgepole Pine. Canadian Forest Service, 2006: 3-66Google Scholar, 5.Berryman A.A. The theory and classification of outbreaks.in: Barbosa P. Schultz J.C. Insect Outbreaks. Academic Press, 1987: 3-30Crossref Google Scholar, 7.Myers J.H. Population cycles: generalities, exceptions and remaining mysteries.Proc. Biol. Sci. 2018; 28520172841Crossref PubMed Scopus (33) Google Scholar, 8.Kausrud K. et al.Population dynamics in changing environments: the case of an eruptive forest pest species.Biol. Rev. 2012; 87: 34-51Crossref PubMed Scopus (94) Google Scholar, 9.Raffa K.F. et al.Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions.Bioscience. 2008; 58: 501-517Crossref Scopus (1131) Google Scholar, 14.Amman G.D. Mountain pine beetle (Coleoptera: Scolytidae) mortality in three types of infestations.Environ. Entomol. 1984; 13: 184-191Crossref Google Scholar, 22.Nealis V. Comparative ecology of conifer-feeding spruce budworms (Lepidoptera: Tortricidae).Can. Entomol. 2016; 148: S33-S57Crossref Scopus (41) Google Scholar, 23.Boone C.K. et al.Efficacy of tree defense physiology varies with bark beetle population density: a basis for positive feedback in eruptive species.Can. J. For. Res. 2011; 41: 1174-1188Crossref Scopus (211) Google Scholar]). Clearly, there is a severe lack of knowledge on the role of most biotic factors for the population dynamics of forest insects. Here, we systematically review these knowledge gaps for bark beetles, using the ESBB, Ips typographus (L.), as a model (Box 1). The importance of addressing these knowledge gaps is illustrated in a study by Marini et al. [11.Marini L. et al.Climate drivers of bark beetle outbreak dynamics in Norway spruce forests.Ecography. 2017; 40: 1426-1435Crossref Scopus (134) Google Scholar], who examined 17 ESBB populations over 30 years. They found that while the abundance of storm-felled trees and climate (Figure 1, I, II) were major determinants of local outbreaks in ESBBs, 65% of the variation in beetle population size remained unexplained. This unexplained variation might in part be due to variation in forest management between the different sites considered in the model [11.Marini L. et al.Climate drivers of bark beetle outbreak dynamics in Norway spruce forests.Ecography. 2017; 40: 1426-1435Crossref Scopus (134) Google Scholar]. However, some models on Dendroctonus bark beetles and forest moth species suggest that including biotic variables (i.e., competition, natural enemies, or phenotype) can reduce the unexplained to sometimes less than 30% [15.Berryman A.A. What causes population cycles of forest Lepidoptera?.Trends Ecol. Evol. 1996; 11: 28-32Abstract Full Text PDF PubMed Scopus (200) Google Scholar, 24.Friedenberg N.A. et al.Temperature extremes, density dependence, and southern pine beetle (Coleoptera: Curculionidae) population dynamics in east Texas.Environ. Entomol. 2008; 37: 650-659Crossref PubMed Google Scholar, 25.Candau J-N. Fleming R.A. Landscape-scale spatial distribution of spruce budworm defoliation in relation to bioclimatic conditions.Can. J. For. Res. 2005; 35: 2218-2232Crossref Scopus (60) Google Scholar]. Although biotic variables such as intraspecific and interspecific competition, natural enemies, pathogens, symbionts, host tree resistance, and frequency of insect phenotypes and/or genotypes (Figure 1, IV) are rarely recorded and included in population dynamics models (in particular in ESBB; Box 1), it is clear that they can be invariably applied to all eruptive insects. Biotic variables should vary only in their relative effects (and probably their interactive effects) on the focal insect species [4.Safranyik L. Carroll A.L. The biology and epidemiology of the mountain pine beetle in lodgepole pine forests.in: Safranyik L. Wilson W.R. The Mountain Pine Beetle: A Synthesis of Biology, Management, and Impacts on Lodgepole Pine. Canadian Forest Service, 2006: 3-66Google Scholar, 5.Berryman A.A. The theory and classification of outbreaks.in: Barbosa P. Schultz J.C. Insect Outbreaks. Academic Press, 1987: 3-30Crossref Google Scholar, 6.Myers J.H. Corry J.S. Population cycles in forest lepidoptera: ecology, evolution and impacts of changing climates.Annu. Rev. Ecol. Evol. Syst. 2013; 44: 565-592Crossref Scopus (65) Google Scholar, 10.Crutzen P.J. The "Anthropocene".in: Ehlers E. Krafft T. Earth System Science in the Anthropocene. Springer, 2006: 13-18Crossref Scopus (440) Google Scholar, 22.Nealis V. Comparative ecology of conifer-feeding spruce budworms (Lepidoptera: Tortricidae).Can. Entomol. 2016; 148: S33-S57Crossref Scopus (41) Google Scholar, 26.Hofstetter R.W. et al.Symbiotic associations of bark beetles.in: Vega F.E. Hofstetter R.W. Bark Beetles: Biology and Ecology of Native and Invasive Species. Academic Press, 2015: 209-245Crossref Scopus (76) Google Scholar]. Host tree resistance, for example, has little influence on the population dynamics of forest moth species, whereas it strongly affects tree-killing bark beetles [2.Weed A.S. et al.Population dynamics of bark beetles.in: Vega F.E. Hofstetter R.W. Bark Beetles: Biology and Ecology of Native and Invasive Species. Academic Press, 2015: 157-176Crossref Scopus (12) Google Scholar, 4.Safranyik L. Carroll A.L. The biology and epidemiology of the mountain pine beetle in lodgepole pine forests.in: Safranyik L. Wilson W.R. The Mountain Pine Beetle: A Synthesis of Biology, Management, and Impacts on Lodgepole Pine. Canadian Forest Service, 2006: 3-66Google Scholar, 7.Myers J.H. Population cycles: generalities, exceptions and remaining mysteries.Proc. Biol. Sci. 2018; 28520172841Crossref PubMed Scopus (33) Google Scholar, 9.Raffa K.F. et al.Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions.Bioscience. 2008; 58: 501-517Crossref Scopus (1131) Google Scholar].Box 1The ESBB–Norway Spruce SystemThe ESBB, Ips typographus (L.), is a 5-mm beetle endemic to spruce forests across Eurasia (Figure I). The ESBB is the economically most important insect in Palearctic spruce forests and at the same time a keystone species from an ecological point of view [30.Hlásny T. et al.Living with Bark Beetles: Impacts, Outlook and Management Options. From Science to Policy 8. European Forest Institute, 2019Google Scholar]. The beetle is associated with a diverse and dynamic community of bacterial and fungal symbionts suggested to contribute to the exhaustion of tree defenses [43.Zhao T. et al.Fungal associates of the tree-killing bark beetle, Ips typographus, vary in virulence, ability to degrade conifer phenolics and influence bark beetle tunneling behavior.Fungal Ecol. 2019; 38: 71-79Crossref Scopus (26) Google Scholar, 53.Lieutier F. et al.Stimulation of tree defenses by ophiostomatoid fungi can explain attack success of bark beetles on conifers.Ann. For. 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Intraspecific competition is probably one of the major drivers of ESBB population dynamics [42.Toffin E. et al.Colonization of weakened trees by mass-attacking bark beetles: no penalty for pioneers, scattered initial distributions and final regular patterns.R. Soc. Open Sci. 2018; 5170454Crossref PubMed Scopus (9) Google Scholar]. However, such competition is relaxed in the population build-up phase due to large numbers of dead or weakened trees. Interspecific competition with other bark beetle species and wood borers is little studied in ESBBs (but see [27.Thalenhorst W. Grundzüge der Populationsdynamik des grossen Fichtenborkenkäfers Ips typographus L.Schr. Forstl. Fak. Univ. Gott. 1958; 21: 1-126Google Scholar, 55.Byers J. Avoidance of competition by spruce bark beetles, Ips typographus and Pityogenes chalcographus.Cell. Mol. Life Sci. 1993; 49: 272-275Crossref Scopus (41) Google Scholar]) but is known to have substantial impact in other bark beetle species [3.Lindgren B.S. Raffa K.F. Evolution of tree killing in bark beetles (Coleoptera: Curculionidae): trade-offs between the maddening crowds and a sticky situation.Can. Entomol. 2013; 145: 471-495Crossref Scopus (56) Google Scholar]. It is unknown to what degree natural enemies (e.g., predatory beetles, parasitoids, woodpeckers, nematodes) and pathogens (e.g., entomopathogenic fungi, viruses) affect ESBB populations [34.Wegensteiner R. et al.Natural enemies of bark beetles: predators, parasitoids, pathogens, and nematodes.in: Vega F.E. Hofstetter R.W. Bark Beetles: Biology and Ecology of Native and Invasive Species. Academic Press, 2015: 247-304Crossref Scopus (54) Google Scholar] because existing studies are contradictory. Phoretic mites, some of which feed on and transmit fungal spores, seem particularly important [26.Hofstetter R.W. et al.Symbiotic associations of bark beetles.in: Vega F.E. Hofstetter R.W. Bark Beetles: Biology and Ecology of Native and Invasive Species. Academic Press, 2015: 209-245Crossref Scopus (76) Google Scholar, 38.Linnakoski R. et al.Seasonal succession of fungi associated with Ips typographus beetles and their phoretic mites in an outbreak region of Finland.PLoS One. 2016; 11e0155622Crossref PubMed Scopus (26) Google Scholar], but interactions between beetles, mites, and fungi are unstudied.The usual hosts of ESBBs are windthrown or standing but weakened spruce trees (primarily Norway spruce, Picea abies). Trees defend themselves with anatomical (e.g., stone cells) and chemical (e.g., terpenoid oleoresins) defenses [56.Krokene P. Conifer defense and resistance to bark beetles.in: Vega F.E. Hofstetter R.W. Bark Beetles: Biology and Ecology of Native and Invasive Species. Academic Press, 2015: 177-207Crossref Scopus (77) Google Scholar] and healthy trees with vigorous defenses can be overwhelmed only by pheromone-coordinated mass attack during population outbreaks [27.Thalenhorst W. Grundzüge der Populationsdynamik des grossen Fichtenborkenkäfers Ips typographus L.Schr. Forstl. Fak. Univ. Gott. 1958; 21: 1-126Google Scholar, 57.Wermelinger B. Ecology and management of the spruce bark beetle Ips typographus – a review of recent research.For. Ecol. Manag. 2004; 202: 67-82Crossref Scopus (507) Google Scholar]. There is evidence, however, that high intraspecific competition in healthy trees often results in low reproduction and thus can dampen population growth [27.Thalenhorst W. Grundzüge der Populationsdynamik des grossen Fichtenborkenkäfers Ips typographus L.Schr. Forstl. Fak. Univ. Gott. 1958; 21: 1-126Google Scholar, 28.Anderbrant O. et al.Intraspecific competition affecting parents and offspring in the bark beetle Ips typographus.Oikos. 1985; 45: 89-98Crossref Scopus (157) Google Scholar, 29.Botterweg P. The effect of attack density on size, fat content and emergence of the spruce bark beetle Ips typographus L.1.J. Appl. Entomol. 1983; 96: 47-55Google Scholar, 57.Wermelinger B. Ecology and management of the spruce bark beetle Ips typographus – a review of recent research.For. Ecol. Manag. 2004; 202: 67-82Crossref Scopus (507) Google Scholar].Intensification of forest management in Europe has resulted in unnaturally high densities of spruce. ESBB populations build up more frequently and more severely in these homogeneous spruce stands, especially if trees are weakened by climate change or other stressors. Higher temperatures and severe drought, for example, can reduce the efficacy of tree defenses and thus allow beetles to overwhelm trees at lower attack densities [27.Thalenhorst W. Grundzüge der Populationsdynamik des grossen Fichtenborkenkäfers Ips typographus L.Schr. Forstl. Fak. Univ. Gott. 1958; 21: 1-126Google Scholar, 57.Wermelinger B. Ecology and management of the spruce bark beetle Ips typographus – a review of recent research.For. Ecol. Manag. 2004; 202: 67-82Crossref Scopus (507) Google Scholar]. Non-outbreak bark beetle populations are therefore expected, and already observed, to undergo more frequent and severe population build-ups and outbreaks in the Anthropocene (Figure II) [30.Hlásny T. et al.Living with Bark Beetles: Impacts, Outlook and Management Options. From Science to Policy 8. European Forest Institute, 2019Google Scholar]. ESBB outbreaks in Central Europe alone caused annual losses of 14.5 million m3 of wood between 2002 and 2010 and currently windstorms in combination with the 2018 summer drought result in beetle damage that is unprecedented (40 million m3 in Europe, 18 million m3 in the Czech Republic alone) [30.Hlásny T. et al.Living with Bark Beetles: Impacts, Outlook and Management Options. From Science to Policy 8. European Forest Institute, 2019Google Scholar]. These outbreaks have strong negative consequences on ecosystem services like provisioning of clean water and timber, and the regulation of climate and carbon storage, but paradoxically they typically facilitate local biodiversity [31.Thom D. Seidl R. Natural disturbance impacts on ecosystem services and biodiversity in temperate and boreal forests.Biol. Rev. 2016; 91: 760-781Crossref PubMed Scopus (302) Google Scholar].Figure IIResponses of Bark Beetle Populations in the Anthropocene.Show full captionNon-outbreak (A), build-up, and outbreak (B) bark beetle population dynamics.View Large Image Figure ViewerDownload Hi-res image Download (PPT)Figure 1Overview of Variables Affecting Eruptive Forest Insects and Their Known or Unknown Effects in the European Spruce Bark Beetle (ESBB), (Ips typographus) System.Show full captionBoxes 3–11 represent measurable variables and arrows stand for single hypotheses describing the direct effect of one variable on another, which should be accounted for and tested in observational and experimental studies. (I) Major climatic variables affected by climate change at a macro- and regional scale. (II) Most important variables relating to properties of individual host trees and trees at a landscape scale. (III) Main population phases (non-outbreak, build-up, outbreak, collapse) of an eruptive insect species. (IV) Major biotic variables associated with an eruptive insect species plus intraspecific effects (phenotype, genotype, and intraspecific competition). Arrows are exemplary for the ESBB system. An arrow from one of the boxes in group I, II, or IV to one of the boxes in group III would indicate a direct effect on the population phases of the beetle. Arrows connecting multiple boxes and eventually pointing to one of the four population phases would indicate an indirect effect. The gray arrows represent hypotheses that have yet to be tested and thus mirror gaps in our knowledge of the ESBB. The absence of an arrow between boxes implies that there is probably no effect of one variable on another in the ESBB.View Large Image Figure ViewerDownload Hi-res