Few generalizable patterns of tree-level mortality during extreme drought and concurrent bark beetle outbreaks

https://doi.org/10.1016/j.scitotenv.2020.141306Get rights and content

Highlights

  • Recent drought and bark beetles caused extensive tree mortality in California, USA.

  • A three-proxy approach is used to elucidate risk factors for tree-level mortality.

  • Living and dead trees exhibit some differences in growth, isotopes (Δ13C) and defenses.

  • Differences between living and dead trees are not consistent across species.

  • Effects of drought with beetles mask generalizable risk factors of mortality.

Abstract

Tree mortality associated with drought and concurrent bark beetle outbreaks is expected to increase with further climate change. When these two types of disturbance occur in concert it complicates our ability to accurately predict future forest mortality. The recent extreme California USA drought and bark beetle outbreaks resulted in extensive tree mortality and provides a unique opportunity to examine questions of why some trees die while others survive these co-occurring disturbances. 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 differ for surviving and now-dead trees, and 3) whether generalizable risk factors for tree mortality exist across pinyon pine (Pinus monophylla), ponderosa pine (P. ponderosa), white fir (Abies concolor), and incense cedar (Calocedrus decurrens) affected by the combination of drought and beetle outbreaks. We find that risk factors associated with mortality differ between species, and that few generalizable patterns exist when bark beetle outbreaks occur in concert with a particularly long, hot drought. We see evidence that both long-term differences in physiology and shorter-term beetle-related selection and variability in defenses influence mortality susceptibility for ponderosa pine, whereas beetle dynamics may play a more prominent role in mortality patterns for white fir and pinyon pine. In contrast, incense cedar mortality appears to be attributable to long-term effects of growth suppression. Risk factors that predispose some trees to drought and beetle-related mortality likely reflect species-specific strategies for dealing with these particular disturbance types. The combined influence of beetles and drought necessitates the consideration of multiple, species-specific risk factors to more accurately model forest mortality in the face of similar extreme events more likely under future climates.

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.

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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/).

References (97)

  • S.W. Leavitt

    Tree-ring C–H–O isotope variability and sampling

    Sci. Total Environ.

    (2010)
  • F. Lebourgeois et al.

    Social status-mediated tree-ring responses to climate of Abies alba and Fagus sylvatica shift in importance with increasing stand basal area

    For. Ecol. Manag.

    (2014)
  • F. Lloret et al.

    Plant community changes induced by experimental climate change: seedling and adult species composition

    Perspectives in Plant Ecology, Evolution and Systematics

    (2009)
  • J. Martínez-Vilalta et al.

    Drought-induced vegetation shifts in terrestrial ecosystems: the key role of regeneration dynamics

    Glob. Planet. Chang.

    (2016)
  • D. McCarroll et al.

    Stable isotopes in tree rings

    Quat. Sci. Rev.

    (2004)
  • J.E. Mohan et al.

    Mycorrhizal fungi mediation of terrestrial ecosystem responses to global change: mini-review

    Fungal Ecol.

    (2014)
  • R.P. Phillips et al.

    A belowground perspective on the drought sensitivity of forests: towards improved understanding and simulation

    For. Ecol. Manag.

    (2016)
  • M. Zadworny et al.

    Regeneration origin affects radial growth patterns preceding oak decline and death – insights from tree-ring δ13C and δ18O

    Agric. For. Meteorol.

    (2019)
  • H.D. Adams et al.

    A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

    Nature ecology & evolution

    (2017)
  • C.D. Allen et al.

    On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene

    Ecosphere

    (2015)
  • W.R.L. Anderegg et al.

    Tree mortality from drought, insects, and their interactions in a changing climate

    New Phytol.

    (2015)
  • T.W. Beers et al.

    Notes and observations: aspect transformation in site productivity research

    J. For.

    (1966)
  • B.J. Bentz et al.

    Climate change and bark beetles of the western United States and Canada: direct and indirect effects

    BioScience

    (2010)
  • F. Biondi et al.

    A theory-driven approach to tree-ring standardization: defining the biological trend from expected basal area increment

    Tree-Ring Research

    (2008)
  • O.N. Bjornstad

    Ncf: Spatial Covariance Functions

    (2019)
  • C.K. Boone 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)
  • I. Brunner et al.

    How tree roots respond to drought

    Front. Plant Sci.

    (2015)
  • H. Bugmann et al.

    Tree mortality submodels drive simulated long-term forest dynamics: assessing 15 models from the stand to global scale

    Ecosphere

    (2019)
  • M. Cailleret et al.

    A synthesis of radial growth patterns preceding tree mortality

    Glob. Chang. Biol.

    (2017)
  • M. Cailleret et al.

    Early-warning signals of individual tree mortality based on annual radial growth

    Front. Plant Sci.

    (2019)
  • J.J. Camarero et al.

    To die or not to die: early warnings of tree dieback in response to a severe drought

    J. Ecol.

    (2015)
  • L. Cavin et al.

    Extreme drought alters competitive dominance within and between tree species in a mixed forest stand

    Funct. Ecol.

    (2013)
  • K.L. Cole et al.

    Geographical and climatic limits of needle types of one-and two-needled pinyon pines

    J. Biogeogr.

    (2008)
  • A.Z. Csank et al.

    Tree-ring isotopes reveal drought sensitivity in trees killed by spruce beetle outbreaks in south-Central Alaska

    Ecol. Appl.

    (2016)
  • V.H. Dale et al.

    Climate change and forest disturbances: climate change can affect forests by altering the frequency, intensity, duration, and timing of fire, drought, introduced species, insect and pathogen outbreaks, hurricanes, windstorms, ice storms, or landslides

    BioScience

    (2001)
  • N.S. Diffenbaugh et al.

    Anthropogenic warming has increased drought risk in California

    Proc. Natl. Acad. Sci.

    (2015)
  • M. Dobbertin

    Tree growth as indicator of tree vitality and of tree reaction to environmental stress: a review

    Eur. J. For. Res.

    (2005)
  • J.M. Egan et al.

    Multi-temporal ecological analysis of Jeffrey pine beetle outbreak dynamics within the Lake Tahoe Basin

    Popul. Ecol.

    (2016)
  • G. Farquhar et al.

    Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes

    Funct. Plant Biol.

    (1984)
  • G.D. Farquhar et al.

    On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves

    Funct. Plant Biol.

    (1982)
  • G.D. Farquhar et al.

    Carbon isotope discrimination and photosynthesis

    Annu. Rev. Plant Biol.

    (1989)
  • Ferrell, G., W. Otrosina, and C. Demars Jr. 1994. Predicting susceptibility of white fir during a drought-associated...
  • S. Ferrenberg et al.

    Resin duct characteristics associated with tree resistance to bark beetles across lodgepole and limber pines

    Oecologia

    (2014)
  • M.L. Gaylord et al.

    Drought predisposes piñon–juniper woodlands to insect attacks and mortality

    New Phytol.

    (2013)
  • M.L. Gaylord et al.

    Mechanisms of piñon pine mortality after severe drought: a retrospective study of mature trees

    Tree Physiol.

    (2015)
  • A.M. Gessler et al.

    Stable isotopes in tree rings: towards a mechanistic understanding of isotope fractionation and mixing processes from the leaves to the wood

    Tree Physiol.

    (2014)
  • A.M. Gessler et al.

    Drought induced tree mortality–a tree-ring isotope based conceptual model to assess mechanisms and predispositions

    New Phytol.

    (2018)
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