Few generalizable patterns of tree-level mortality during extreme drought and concurrent bark beetle outbreaks
Graphical abstract
Identified within-species risk factors for tree-level mortality due to the combination of severe drought and concurrent bark beetle outbreaks associated with the 2012–2016 California, USA drought. Risk factors are categorized by species and category of metric measured. While we do not attempt to disentangle the effects of drought and bark beetles, host-specific beetles were identified as contributing to mortality for ponderosa pine, pinyon pine, and white fir, while incense cedar showed no clear evidence of bark beetle attacks. BAI refers to basal area increment (i.e. radial tree growth), Δ13C refers to discrimination of the heavier (13C) carbon isotope measured from tree rings, and PDSI refers to the Palmer Drought Severity Index.
Introduction
Droughts have been linked to an increase in forest mortality events (Allen et al., 2010), with further drought-related impacts on forests predicted with continuing climate change (IPCC, 2014; Allen et al., 2015). Longer duration, higher frequency, and/or hotter droughts are expected to alter forests globally via changes in primary production (Zhao and Running, 2010), species composition (Lloret et al., 2009; Martínez-Vilalta and Lloret, 2016), species dominance (Cavin et al., 2013), and interactions with other disturbances (Dale et al., 2001). Often, biotic agents interact with drought to further exacerbate these changes by amplifying mortality (Anderegg et al., 2015). Bark beetles (Coleoptera: Curculionidae, Scolytinae) are one example of a biotic agent that interacts with drought, and are expected to experience changes in population dynamics and range expansion due to increasing temperatures associated with further climate change, leading to increased tree mortality particularly during extended drought periods (Bentz et al., 2010; Kolb et al., 2016).
The combined impacts of drought and insect outbreaks on tree mortality have important implications for predicting forest dynamics under climate change, yet forecasting tree mortality is one of the most uncertain processes in dynamic vegetation models (Bugmann et al., 2019). To more accurately predict ways in which global change will alter forest dynamics, models must be informed by a better understanding of how tree-level factors influence mortality probability when multiple disturbance agents co-occur (Anderegg et al., 2015). Some tree-level early warning signals for drought-related mortality have been identified, but few patterns have emerged across species, and most studies do not consider drought interactions with insects (Camarero et al., 2015; Cailleret et al., 2017; Cailleret et al., 2019; Liu et al., 2019). Similarly, despite recent advances in the understanding of physiological mechanisms underlying drought-related tree mortality (Sevanto et al., 2014; Adams et al., 2017), much remains unclear. This is especially true when insects are involved (Anderegg et al., 2015; Hartmann et al., 2018), as they can affect both tree carbon and water balance, important links to drought-related mortality (McDowell et al., 2008). A handful of studies have examined why some trees die and others survive in the face of drought combined with insect outbreaks (McDowell et al., 2010; Meddens et al., 2015; Csank et al., 2016), but there remains a lack of understanding of whether generalizable tree-level mortality risk factors or early warning signals exist across species in the face of these interacting disturbances.
The 2012–2016 extreme drought in California, USA provides a valuable opportunity to better understand mortality dynamics associated with a particularly hot, multi-year drought (Diffenbaugh et al., 2015) and concurrent bark beetle outbreaks affecting multiple tree species. The record-breaking drought and associated outbreaks killed an estimated 147 million trees, with the peak of mortality occurring in 2015–16 and forests in central and southern California being most impacted (Goulden and Bales, 2019; USDA Forest Service, 2019). As bark beetles are better able to overcome tree defenses during drought, both the magnitude and length of the drought enabled multiple species of bark beetles to reach outbreak levels, amplifying mortality for several, co-occurring tree species (Fettig et al., 2019). This type of extreme disturbance is expected to become more common under future climates (Allen et al., 2015; Kolb et al., 2016), making it important to understand to more accurately model future forest mortality.
Tree ring analyses are a valuable way to quantify multiple factors that affect susceptibility to drought-related mortality over climate change-relevant timeframes. Quantification of radial stem growth is common in studies that compare trees that die and those that survive drought (Cailleret et al., 2017). Radial growth is a useful metric for assessing changes in tree-level carbon balance, as it is generally a lesser priority for carbon investment than, for example, foliage and root development (Dobbertin, 2005). Lower radial growth has been shown to precede drought-related mortality in most instances (Cailleret et al., 2017), but not necessarily when bark beetle outbreaks co-occur (de la Mata et al., 2017; Cooper et al., 2018). Relationships between radial growth and climate seem to additionally vary between trees that die and those that survive drought with or without concurrent beetle outbreaks, with generally greater sensitivity of growth to a variety of climate variables for trees that die (Suarez et al., 2004; McDowell et al., 2010; Hereş et al., 2012; Csank et al., 2016).
When examined in concert with radial growth, stable isotope ratios in tree rings can further elucidate population-level differences in tree physiological vulnerability to drought and beetle-related mortality (McDowell et al., 2010), as isotopes can serve as a whole-tree, annually-resolved index of gas exchange (Farquhar et al., 1989; McCarroll and Loader, 2004). Stable carbon isotope ratios (δ13C) relate to the ratio of intercellular (ci) to ambient (ca) CO2 concentrations, and are thus related to both stomatal conductance and photosynthetic demand (see ‘Materials and methods’ for further explanation). A few tree ring studies have used a two-pronged approach utilizing stable isotope analysis in concert with growth analyses to examine differences in carbon isotope ratios between surviving and dying trees in the face of drought (Hereş et al., 2014; Gessler et al., 2018) or drought combined with beetle outbreaks (McDowell et al., 2010; Csank et al., 2016), but have found inconsistencies across species and sites.
When drought occurs in combination with bark beetle outbreaks, intraspecific differences in tree defenses against beetle attack may influence mortality probability (Gaylord et al., 2013; Huang et al., 2020). Resin duct characteristics in the secondary xylem of Pinus spp. relate to resin flow and thus serve as a useful indicator of tree defense against bark beetles (Hood and Sala, 2015). Previous studies have found differences in various tree-ring derived resin duct metrics for trees that die versus those that survive beetle outbreaks, with greater investment in defenses for trees that survive (Kane and Kolb, 2010; Gaylord et al., 2013; Hood et al., 2015; Zhao and Erbilgin, 2019), sometimes at the apparent cost of lower growth (Ferrenberg et al., 2014; Kichas et al., 2020). However, bark beetle outbreaks of previous studies that examine resin ducts have not been associated with extreme drought periods as long and hot as the 2012–2016 California drought.
We use plot-level data combined with a three-proxy tree-level approach using radial growth, carbon isotopes, and resin duct metrics to evaluate 1) whether variability in stand structure, tree growth or size, carbon isotope discrimination, or defenses precede mortality, 2) how relationships between these proxies and climate differ for surviving and now-dead trees, and 3) whether generalizable risk factors for tree mortality exist across four species affected by the combination of drought and bark beetle outbreaks. We expected the likelihood of mortality to be higher for trees in stands with higher density of the same species due to the influence of host availability and competition on both beetles and drought-susceptibility of trees. We anticipated that trees that died would have lower radial growth, but not necessarily if the effects of beetles overshadowed those of the drought (Cailleret et al., 2017), and be more sensitive to climatic stress (McDowell et al., 2010). Similarly, we expected carbon isotope discrimination to be lower, indicating chronic water stress (Warren et al., 2001), and for trees that died to have fewer resin duct defenses (Kane and Kolb, 2010). To our knowledge no study has investigated drought impacts using this three-proxy approach for multiple species to shed light on how forests respond to extreme drought and bark beetle outbreaks that are increasingly likely to occur under future climate conditions.
Section snippets
Study species and site selection
Sampling areas were established in two separate geographical areas affected by the 2012–2016 California drought and concurrent beetle outbreaks. Plots were established in southern California on the Los Padres National Forest (LP) to assess singleleaf pinyon pine (Pinus monophylla Torr. & Frém) mortality, and in central California on the Sierra National Forest (SNF) to assess ponderosa pine (Pinus ponderosa Lawson & C. Lawson), white fir (Abies concolor (Gord. & Glend.) Lindl. Ex Hildebr.), and
Overall mortality
Over the course of sampling (2016–19), mortality remained fairly constant within the LP area (27–30%), but changed substantially within the SNF area (43–54%), particularly for ponderosa pine (78–92%). Mortality levels determined from 2015 ADS data that contributed to site selection increased considerably over subsequent years with very few plots having <5% mortality by the end of the sampling period. Mean plot-level mortality for individual species ranged from 30% for pinyon pine to 91% for
Discussion
We find a unique suite of risk factors for mortality for pinyon pine, ponderosa pine, white fir, and incense cedar, with few risk factors shared between species, and no generalizable predictors of mortality across all four species (Fig. 8). We find that in the face of a particularly long, hot drought combined with bark beetle outbreaks, tree-level factors previously found to affect susceptibility to either drought alone or beetle outbreaks combined with more moderate drought become less clear.
Conclusions
The predicted increase in the intensity and/or length of droughts globally (IPCC, 2014; Trenberth et al., 2014), combined with changes in bark beetle dynamics associated with climate change (Bentz et al., 2010), requires a better understanding of how severe disturbance events influence mortality at the tree-level if we are to effectively predict future forest mortality. We find that risk factors associated with tree-level mortality differ between species, and that generalizable patterns become
CRediT authorship contribution statement
Charlotte C. Reed: Investigation, Formal analysis, Data curation, Visualization, Writing - original draft. Sharon M. Hood: Conceptualization, Methodology, Investigation, Writing - review & editing.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This work was supported by the USDA Forest Service Forest Health Protection [EM-18-WC-03], USDA Forest Service Region 5, and the Rocky Mountain Research Station. We thank Beverly Bulaon, Daniel Cluck, Andrea Hefty, Stacy Hishinuma, Adrian Poloni, and Sheri Smith for assistance with project development and data collection, and Lindsay Grayson, Sean Pinnell, Sarah Flanary, Finn Leary, Martin MacKenzie, Ashley Hoffman, Kayanna Warren, Jenny Weathered, Dina Goodhue and Rueben Mahnke for assistance
Data availability
All tree ring data have been archived in the International Tree-Ring Databank (ITRDB) and are available online (https://www.ncdc.noaa.gov/paleo-search/).
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