Abstract
Plant mortality is a complex process influenced by both biotic and abiotic factors. In recent decades, widespread mortality events have been attributed to increasing drought severity, which has motivated research to examine the physiological mechanisms of drought-induced mortality, particularly hydraulic failure. Drought-based mortality mechanisms are further influenced by plant interactions with biota such as neighboring plants, insect pests, and microbes. In this review, we highlight some of the most influential papers addressing these biotic interactions and their influence on plant mortality. Plant–plant interactions can be positive (facilitation), neutral, or negative (competition), depending on drought intensity and neighbor identity. For example, stand-scale mortality likely increases with basal area (an index of competition). However, the diversity of forest stands matters, as more diverse forests suffer less mortality from drought than species-poor forests. Dense forest stands also increase bark beetle attack frequency, which can exacerbate drought stress and mortality, particularly for fast-growing species with lower defense allocation. In some cases, however, drought stress can alleviate biotic attack, depending on feedbacks between plant and pest physiology. Finally, plant interactions with beneficial microorganisms can increase drought tolerance, reduce the likelihood of mortality, and even extend plant distributions into drier habitats. Our review suggests more work is needed in natural herbaceous plant communities as well as dry tropical ecosystems where mortality mechanisms are less understood. Overall, relatively few studies directly link biotic interactions with the physiological mechanisms of mortality. Simultaneous manipulations of biotic interactions and measurements of physiological thresholds (e.g., xylem cavitation) are needed to fully represent biotic interactions in predictive models of plant mortality.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adams HD, Zeppel MJ, Anderegg WR et al (2017) A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nat Ecol Evol 1(9):1285–1291
Afkhami ME, McIntyre PJ, Strauss SY (2014) Mutualist-mediated effects on species’ range limits across large geographic scales. Ecol Lett 17(10):1265–1273
Allen CD, Macalady AK, Chenchouni H et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259(4):660–684
Allen K, Dupuy J, Gei M et al (2017) Will seasonally dry tropical forests be sensitive or resistant to future changes in rainfall regimes? Environ Res Lett 12(2):023001
Anderegg WR, Kane JM, Anderegg LD (2013) Consequences of widespread tree mortality triggered by drought and temperature stress. Nat Clim Change 3(1):30–36
Anderegg WR, Plavcová L, Anderegg LD, Hacke UG, Berry JA, Field CB (2013) Drought’s legacy: multiyear hydraulic deterioration underlies widespread aspen forest die-off and portends increased future risk. Global Change Biol 19(4):1188–1196
Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193
Bingham MA, Simard SW (2011) Do mycorrhizal network benefits to survival and growth of interior Douglas-fir seedlings increase with soil moisture stress? Ecol Evol 1(3):306–316
Boone CK, Aukema BH, Bohlmann J, Carroll AL, Raffa KF (2011) Efficacy of tree defense physiology varies with bark beetle population density: a basis for positive feedback in eruptive species. Can J For Res 41(6):1174–1188
Clifford MJ, Royer PD, Cobb NS, Breshears DD, Ford PL (2013) Precipitation thresholds and drought-induced tree die-off: insights from patterns of Pinus edulis mortality along an environmental stress gradient. New Phytol 200(2):413–421
Compant S, Van Der Heijden MG, Sessitsch A (2010) Climate change effects on beneficial plant–microorganism interactions. FEMS Microbiol Ecol 73(2):197–214
de la Mata R, Hood S, Sala A (2017) Insect outbreak shifts the direction of selection from fast to slow growth rates in the long-lived conifer Pinus ponderosa. PNAS 114(28):7391–7396
Egerton-Warburton LM, Querejeta JI, Allen MF (2007) Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. J Exp Bot 58(6):1473–1483
Fettig CJ, Klepzig KD, Billings RF, Munson AS, Nebeker TE, Negrón JF, Nowak JT (2007) The effectiveness of vegetation management practices for prevention and control of bark beetle infestations in coniferous forests of the western and southern United States. For Ecol Manag 238(1–3):24–53
Frank DA, Wallen RL, Hamilton EW III, White PJ, Fridley JD (2018) Manipulating the system: how large herbivores control bottom-up regulation of grasslands. J Ecol 106(1):434–443
Gaylord ML, Kolb TE, Pockman WT et al (2013) Drought predisposes piñon–juniper woodlands to insect attacks and mortality. New Phytol 198(2):567–578
Gehring CA, Sthultz CM, Flores-Rentería L, Whipple AV, Whitham TG (2017) Tree genetics defines fungal partner communities that may confer drought tolerance. PNAS 114(42):11169–11174
Goh CH, Vallejos DFV, Nicotra AB, Mathesius U (2013) The impact of beneficial plant-associated microbes on plant phenotypic plasticity. J Chem Ecol 39(7):826–839
Grossiord C, Granier A, Ratcliffe S et al (2014) Tree diversity does not always improve resistance of forest ecosystems to drought. PNAS 111(41):14812–14815
Hartmann H, Ziegler W, Kolle O, Trumbore S (2013) Thirst beats hunger–declining hydration during drought prevents carbon starvation in Norway spruce saplings. New Phytol 200(2):340–349
He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16(5):695–706
He Q, Silliman BR, Liu Z, Cui B (2017) Natural enemies govern ecosystem resilience in the face of extreme droughts. Ecology Letters 20(2):194–201
Hisano M, Chen HY, Searle EB, Reich PB (2019) Species-rich boreal forests grew more and suffered less mortality than species-poor forests under the environmental change of the past half-century. Ecol Lett 22(6):999–1008
Huston MA (1997) Hidden treatments in ecological experiments: re-evaluating the ecosystem function of biodiversity. Oecologia 110(4):449–460
Jactel H, Petit J, Desprez-Loustau ML, Delzon S, Piou D, Battisti A, Koricheva J (2012) Drought effects on damage by forest insects and pathogens: a meta-analysis. Global Change Biol 18(1):267–276
Johnson D, Martin F, Cairney JW, Anderson IC (2012) The importance of individuals: intraspecific diversity of mycorrhizal plants and fungi in ecosystems. New Phytol 194(3):614–628
Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. PNAS 109(35):14058–14062
Manion PD (1991) Tree disease concepts, 2nd edn. Prentice-Hall, New Jersey
McDowell N, Allen C, Anderson-Teixeira K et al (2018) Drivers and mechanisms of tree mortality in moist tropical forests. New Phytol 219(3):851–869
McDowell N, Pockman WT, Allen CD et al (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178(4):719–739
Ocheltree TW, Nippert JB, Prasad PV (2016) A safety vs efficiency trade-off identified in the hydraulic pathway of grass leaves is decoupled from photosynthesis, stomatal conductance and precipitation. New Phytol 210(1):97–107
Ott JP, Klimešová J, Hartnett DC (2019) The ecology and significance of below-ground bud banks in plants. Ann Bot 123(7):1099–1118
Ploughe LW, Jacobs EM, Frank GS, Greenler SM, Smith MD, Dukes JS (2019) Community response to extreme drought (CRED): a framework for drought-induced shifts in plant–plant interactions. New Phytol 222(1):52–69
Revillini D, Gehring CA, Johnson NC (2016) The role of locally adapted mycorrhizas and rhizobacteria in plant–soil feedback systems. Funct Ecol 30(7):1086–1098
Rudgers JA, Swafford AL (2009) Benefits of a fungal endophyte in Elymus virginicus decline under drought stress. Basic Appl Ecol 10(1):43–51
Sillett SC, Van Pelt R, Carroll AL, Kramer RD, Ambrose AR, Trask DA (2015) How do tree structure and old age affect growth potential of California redwoods? Ecol Monogr 85(2):181–212
Stephenson NL, Das AJ, Ampersee NJ, Bulaon BM, Yee JL (2019) Which trees die during drought? The key role of insect host-tree selection. J Ecol 107(5):2383–2401
Sthultz CM, Gehring CA, Whitham TG (2007) Shifts from competition to facilitation between a foundation tree and a pioneer shrub across spatial and temporal scales in a semiarid woodland. New Phytol 173:135–145
Sthultz CM, Gehring CA, Whitham TG (2009) Deadly combination of genes and drought: increased mortality of herbivore-resistant trees in a foundation species. Global Change Biol 15(8):1949–1961
Swaty RL, Deckert RJ, Whitham TG, Gehring CA (2004) Ectomycorrhizal abundance and community composition shifts with drought: predictions from tree rings. Ecology 85(4):1072–1084
Tilman D, Downing JA (1994) Biodiversity and stability in grasslands. Nature 367(6461):363–365
Trugman AT, Anderegg LD, Anderegg WR, Das AJ, Stephenson NL (2021) Why is tree drought mortality so hard to predict? Trends Ecol Evol. https://doi.org/10.1016/j.tree.2021.02.001
Yao J, Liu H, Huang J et al (2020) Accelerated dryland expansion regulates future variability in dryland gross primary production. Nat Commun 11(1):1–10
Young DJ, Stevens JT, Earles JM, Moore J, Ellis A, Jirka AL, Latimer AM (2017) Long-term climate and competition explain forest mortality patterns under extreme drought. Ecol Lett 20(1):78–86
Zenes N, Kerr KL, Trugman AT, Anderegg WR (2020) Competition and drought alter optimal stomatal strategy in tree seedlings. Front Plant Sci 11:478
Funding
This manuscript is the result of a graduate student seminar offered jointly though Syracuse University and SUNY Environmental Science and Forestry. RJGN was supported by grant IOS-1754273 from the US National Science Foundation (NSF). SAB was supported by the NSF under Grant No. DGE-1449617 and JT was supported by Grant No. NSF-BCS-GSS-1759724.
Author information
Authors and Affiliations
Contributions
All authors contributed to the review’s conception and design. RJGN, NM, SAB, ARE, JL, JILP, HR, JRS, JT, and JDF contributed initial summaries of the selected papers. The first draft of the manuscript was written by RJGN and all authors provided substantial revisions on subsequent versions.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest
Additional information
Communicated by Scott J Meiners.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Griffin-Nolan, R.J., Mohanbabu, N., Araldi-Brondolo, S. et al. Friend or foe? The role of biotic agents in drought-induced plant mortality. Plant Ecol 222, 537–548 (2021). https://doi.org/10.1007/s11258-021-01126-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-021-01126-4