Herbivorous insects are highly sensitive to variations in climate (Bale et al., 2002; Deutsch et al., 2008; Pörtner and Farrell, 2008). Due to their short life cycles, reproductive potential, high mobility and physiological sensitivity to temperature, even modest changes in environmental conditions will result in rapid changes to their abundance and distribution. Climate change is expected to affect herbivorous insects through direct impacts to their development and survival, and/or indirect impacts mediated through trophic interactions and interactions with abiotic components of the environment (Ayres and Lombardero, 2000; Hughes, 2000; Weed et al., 2013; Simler-Williamson et al., 2019). Range shifts are arguably the most evident outcome of direct and indirect climate impacts to herbivorous insects, manifesting as both range expansions (e.g., Hickling et al., 2005; Safranyik et al., 2010; Jepsen et al., 2011) and range contractions (Wilson et al., 2005; Lombardo et al., 2022).

Range expansions by herbivorous insects can result in extensive impacts to ecosystem processes (Jepsen et al., 2013; Rasmann et al., 2014). This is particularly true for forest insects with irruptive dynamics characterized by episodic landscape-scale outbreaks (Jepsen et al., 2008; Safranyik et al., 2010; Howe et al., 2022). Climate change has facilitated range expansions by irruptive herbivores through amelioration of extreme cold events promoting overwinter survival (Jepsen et al., 2008; Safranyik et al., 2010), milder spring conditions that facilitate improved phenological matching (Miller-Rushing et al., 2010; Jepsen et al., 2011), warmer summers that enhance development, emergence and dispersal (Battisti et al., 2006; Sambaraju et al., 2019), and increased access to evolutionarily naïve host tree populations and species with reduced defensive capacities (Cudmore et al., 2010; Cullingham et al., 2011). Outbreaks by irruptive herbivores in newly invaded forests threaten a variety of values including wildlife habitat, water quantity and quality, timber supply (Safranyik et al., 2010), and in extreme cases may modify biome-scale biogeophysical processes such as carbon cycling and sequestration (Kurz et al., 2008).

The western spruce budworm (Choristoneura freemani Freeman) (Lepidoptera: Tortricidae) is an irruptive herbivore that feeds mainly on Douglas-fir [Pseudotsugae menziesii (Mirb.) Franco] (Volney, 1994; Nealis and Régnière, 2021). It is an early season folivore that preferentially feeds on the new foliage of its host trees. Budworms overwinter as second-instar larvae in hibernacula within tree crowns. They emerge in early May to late June and temporarily mine needles and buds until buds flush, after which they feed on the new needles of elongating shoots. Only after completely consuming new foliage will larvae feed on older needles (Shepherd, 1992; Nealis and Nault, 2005; Nealis and Régnière, 2009; Nealis, 2012). Severe or prolonged defoliation reduces tree growth and vigour and may result in the death of the top portion of the tree. Top-kill often leads to multiple leaders, stem deformation, predisposition to secondary insect attacks and wood-decaying fungi, or even death of the entire tree (Van Sickle et al., 1983; Alfaro and Maclauchlan, 1992).

The western spruce budworm is one of the most destructive and widely distributed defoliators in western North America, with periodic outbreaks occurring within Douglas-fir forests of Canada and the United States (Swetnam and Lynch, 1993; Volney, 1994; Campbell et al., 2006). In Canada, outbreaks historically occurred in southwestern British Columbia (BC), and in particular on southern Vancouver Island (Alfaro et al., 2018). However, since 1930, outbreaks have only occurred at higher latitudes and elevations in the Douglas-fir forests of the interior of BC (Campbell et al., 2006; Maclauchlan et al., 2006, 2018; Thomson and Benton, 2007), suggesting a shift in optimal conditions for budworm survival.

Thomson and Benton (2007) proposed that the absence of western spruce budworm outbreaks in the southwest portion of western Canada was due to a warming-induced loss of synchrony between the emergence of overwintering larvae and the initiation of budburst by Douglas-fir. However, Régnière and Nealis (2018) dismissed the role of variation in larval emergence-budburst synchrony as a significant source of mortality, claiming that any losses of early-emerging larvae would be offset by improved survival of later instars and greater fecundity of resultant adults. Instead, these authors (Nealis and Régnière, 2016; Régnière and Nealis, 2019) suggested that the lack of outbreaks in milder climates was a result of high rates of mortality among overwintering larvae due to resource exhaustion resulting from warmer temperatures during diapause, whereas the northward shift in outbreak populations had been favoured by improved phenological matching of later larval instars with new foliage prior to its lignification (Clancy et al., 1988; Nealis, 2012; Régnière and Nealis, 2018). By incorporating these relationships into a process-based model, Régnière and Nealis (2019) simulated changes in western spruce budworm population fitness through time. Contrary to the observed changes in the spatial pattern of outbreaks, they suggested that the fitness of western spruce budworm populations had actually increased in all regions of BC since 1900, and that it was low in the southwest early in the previous century when outbreaks were common there. This seeming contradiction suggests that the potential impact of variation in synchrony between budburst and larval emergence on the spatial changes in western spruce budworm outbreaks requires further investigation.

Synchrony between the emergence of feeding life stages and the onset of bud development by host trees is critical to the survival of many early season insect folivores, as leaves are easiest to eat and are at their peak nutritional value at this time (Quiring, 1992; Carroll, 1999; Visser and Holleman, 2001; Carroll and Quiring, 2003; van Asch and Visser, 2007), or buds have developed sufficiently to allow penetration by young larvae (Shepherd, 1992; Nealis and Régnière, 2009; Nealis, 2012). This is true for the western spruce budworm. Emergence by overwintering second-instar larvae approximately 18 days in advance of the onset of Douglas-fir budburst has been shown to be optimal for survival (Beckwith and Burnell, 1982; Thomson et al., 1984; Thomson and Benton, 2007). Although early emergence by young larvae necessitates feeding on potentially suboptimal resources (old needles and closed buds), it maximizes access to newly flushed foliage by later instars that are more dependent upon a high-quality diet to complete development (Lawrence et al., 1997; Nealis, 2012; Régnière and Nealis, 2018). The degree of synchrony, and therefore budworm survival, can vary from year to year due to differential responses by insects and host trees to variations in temperature and precipitation (Shepherd, 1992; Bylund, 1999; Campbell et al., 2006) or defoliation (Régnière and Nealis, 2018). Annual weather-related variations in the degree of synchrony suggest that the interaction between western spruce budworm and Douglas-fir may be very sensitive to climate change. Therefore, we predicted that the northward range shift of western spruce budworm defoliation is a consequence of climate change-induced shift in the regions with optimal synchrony between spring larval emergence and Douglas-fir budburst. If this prediction is correct, we would expect to observe a shift in the mean outbreak range of western spruce budworm toward higher latitudes and elevations, along with a similar shift in the optimal synchrony between larval emergence and Douglas-fir budburst.

An analysis of the distribution of western spruce budworm outbreaks was conducted to quantify patterns of range shift within BC during the past century. Our prediction of a northward shift of optimal synchrony was evaluated in a second analysis where the dates of budworm emergence and Douglas-fir budburst were simulated across BC for the same period using budworm and host phenology models combined with long-term daily weather data. The following sections describe the data sources, the methods used to extract the relevant data, and the statistical analyses that were employed.

Western spruce budworm outbreaks in Douglas-fir forests of western Canada have rapidly shifted to higher latitudes and elevations while gradually retracting from the southern and western portions of its range since the beginning of the previous century. Evidence of this is clear in the spatial pattern of outbreaks detected during forest health surveys, and as predicted, in shifts in the timing of optimal budburst-larval emergence synchrony. Our results do not suggest that western spruce budworm populations have never occurred in northern portion of the Douglas-fir distribution, nor completely disappeared from the south. Indeed, several dendrochronological studies have found evidence of western spruce budworm activity throughout the range of Douglas-fir (Swetnam and Lynch, 1989, 1993; Campbell et al., 2006; Axelson et al., 2015). However, our analyses indicate that the propensity for populations to increase to detectable outbreak levels has shifted to higher latitudes and elevations during the previous 100 + years. Dendrochronology is a correlative technique that detects periods during which non-climate related events such as herbivorous insect activity may affect tree growth. It cannot be used to estimate herbivorous insect population levels (Swetnam and Lynch, 1993), and therefore may record defoliation events that fall below the level of detectability by forest health surveys. In support of this assertion, Campbell et al. (2006) found evidence for two western spruce budworm defoliation events in central BC, yet only the most recent one in their study, occurring between 1985 and 1995, was detected. Similarly, Alfaro et al. (2018) detected evidence of western spruce budworm defoliation of Douglas-fir on Vancouver Island in decades after 1930 when the last outbreak was recorded there.

Our analyses suggest a clear relationship between northward range expansion of the western spruce budworm and climate-change induced improvements in phenological synchrony. At higher latitudes/elevations, there was a consistent trend toward convergence in the timing of larval emergence and the initiation of host bud development over the previous century. At the beginning of our simulation (1900) the phenological mismatch was 7 to 10 days in the Douglas-fir forests at the highest latitude/elevations. A mismatch of this magnitude can cause significant amounts of mortality and limit the potential for outbreaks by early season folivores due to declines in the quality of foliage (Carroll, 1999; Jepsen et al., 2011; Fuentealba et al., 2017; Despland, 2018). However, through the previous century, the phenological mismatch decreased to < 5 days even in the most northerly Douglas-fir habitats. Improved synchrony may facilitate better access to the more nutritious and digestible new foliage leading to improved western spruce budworm development and survival (Shepherd, 1992; Chen et al., 2001, 2003), although evidence suggests that the requirement for phenological synchrony by western spruce budworm is a function of the physical state and not the nutritional condition of developing buds (Nealis and Nault, 2005; Nealis and Régnière, 2009; Nealis, 2012).

The results of this study largely complement rather than contradict our understanding of the spatial dynamics of western spruce budworm outbreaks. Variation in optimal synchrony is expected to affect the survival while foraging of newly emerged second-instar larvae following winter diapause (Shepherd, 1992). This assertion is in keeping with evidence that overall generation survival in populations of western spruce budworm is most affected by mortality of young, non-feeding larvae (Nealis and Régnière, 2021). Whereas Régnière and Nealis (2019) suggested low population fitness in lower latitudes/elevations at the beginning of the previous century, in part due to high levels of resource depletion by overwintering larvae, we found larval emergence-budburst synchrony to be optimal in that region at that time suggesting increased survival of newly emerged larvae while foraging for suitable buds may offset mortality from winter exhaustion. The evidence of widespread outbreaks in the southwest at this time support this conclusion. The expansion toward the north and higher elevations by outbreak populations is both in keeping with the simulations by Régnière and Nealis (2019) and our assessments of optimal synchrony. Indeed, the very high rates of northward expansion by populations above the median distribution suggests that budworms may be benefiting from both the phenological matching of later larval instars with new foliage prior to lignification (Nealis and Régnière, 2016; Régnière and Nealis, 2019) and our finding of the convergence toward optimal of larval emergence and bud development. Unfortunately, the overall northward shift in optimal synchrony, and the concomitant change in western spruce budworm outbreak distributions, does not entirely support the conclusion of Alfaro et al. (2018) that the disappearance of outbreaks at lower latitudes and elevations is a consequence of localized fragmentation of Douglas-fir forests.

In seasonal environments, phenological asynchrony has been suggested as an effective defense against herbivory for some populations and species of trees (Chen et al., 2003; Tikkanen and Julkunen-Tiitto, 2003; Pureswaran et al., 2015; Bellemin-Noël et al., 2021). Indeed, for Douglas-fir, resistance to defoliation by western spruce budworm has been linked to delays in the timing of budburst (Chen et al., 2001, 2003). Altered synchrony as a consequence of climate change may nullify the efficacy of a phenological mismatch and cause increased herbivore impacts to historically resistant hosts (Pureswaran et al., 2015, 2018; Fuentealba et al., 2017; Bellemin-Noël et al., 2021). As synchrony between the insect and host continue to converge at higher latitudes and elevations, historically resistant trees may become increasingly susceptible, resulting in further expansion of western spruce budworm into regions not historically prone to outbreaks.

Improved phenological matching in the north was accompanied by diverging synchrony at lower latitudes/elevations, reinforcing the northern range shift by outbreaking budworm populations over the past century. This result is consistent with Thomson and Benton (2007) who found that warming in the southwest portion of BC (i.e., Vancouver Island) after 1930 was associated with reduced budworm population densities, putatively a consequence of phenological mismatching. Indeed, our simulation suggests an increase in asynchrony between larval emergence and budburst of approximately 5 days since 1900. If the trend continues, it is likely that western spruce budworm outbreaks will become rare over large portions of southern BC. Although climate change-induced range retractions by irruptive insects are less common than expansions (Wilson et al., 2005), phenological mismatches have been implicated in decreases in outbreak frequencies for several defoliator species (Visser and Holleman, 2001; Johnson et al., 2010).

Range changes by irruptive folivores in pursuit of shifting phenological synchrony with their hosts is a commonly predicted (Bale et al., 2002; van Asch and Visser, 2007; Pureswaran et al., 2015; Despland, 2018), but infrequently documented consequence of climate change (but see Jepsen et al., 2009, 2011). For the western spruce budworm, we have shown that the shift by outbreak populations to higher latitudes and elevations is associated with both convergence and divergence in phenological matching with Douglas-fir. This is an outcome of differential responses to temperature by the insect and its host tree. Although both are reliant upon degree day accumulation, Douglas-fir bud development is putatively dependent upon an additional photoperiodic threshold (Linkosalo et al., 2006). Thus, the potential for warming to cause directional shifts in phenological matching between irruptive early season folivores and their host trees may be contingent upon the degree to which each depends on different components of their environments for their development (van Asch and Visser, 2007; Both et al., 2009); an aspect that should be considered in future research into the role of climate change in outbreaks by irruptive folivores in seasonal environments.

Publicly available datasets were analyzed in this study. This data can be found here: https://www2.gov.bc.ca/gov/content/industry/forestry/managing-our-forest-resources/forest-health/aerial-overview-surveys and https://www2.gov.bc.ca/gov/content/industry/forestry/managing-our-forest-resources/forest-inventory/data-management-and-access.

AT and AC conceived and designed the study and wrote the manuscript. AT conducted the analyses. Both authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.