1 Changing disturbance regimes, ecological memory, and forest resilience 2 3 4 Authors: Jill F. Johnstone1*§, Craig D. Allen2, Jerry F. Franklin3, Lee E. Frelich4, Brian J. 5 Harvey5, Philip E. Higuera6, Michelle C. Mack7, Ross K. Meentemeyer8, Margaret R. Metz9, 6 George L. W. Perry10, Tania Schoennagel11, and Monica G. Turner12§ 7 8 Affiliations: 9 1. Department of Biology, University of Saskatchewan, Saskatoon, SK S7N 5E2 Canada 10 2. U.S. Geological Survey, Fort Collins Science Center, Jemez Mountains Field Station, Los 11 Alamos, NM 87544 USA 12 3. College of Forest Resources, University of Washington, Seattle, WA 98195 USA 13 4. Department of Forest Resources, University of Minnesota, St. Paul, MN 55108 USA 14 5. Department of Geography, University of Colorado-Boulder, Boulder, CO 80309 USA 15 6. Department of Ecosystem and Conservation Sciences, University of Montana, Missoula, MT 16 59812 USA 17 7. Center for Ecosystem Science and Society and Department of Biology, Northern Arizona 18 University, Flagstaff, AZ 86011 USA 19 8. Department of Forestry & Environmental Resources, North Carolina State University, 20 Raleigh, NC 27695 USA 21 9. Department of Biology, Lewis and Clark College, Portland, OR 97219 USA 22 10. School of Environment, University of Auckland, Private Bag 92019, Auckland, New Zealand 23 11. Department of Geography and INSTAAR, University of Colorado-Boulder, Boulder, CO 24 80309 USA 25 12. Department of Zoology, University of Wisconsin-Madison, Madison, WI 53717 26 27 * corresponding author: [email protected]; 28 § co-leaders of this manuscript 29 30 Running title: Changing disturbance and forest resilience 31 1 32 33 Abstract 34 Ecological memory is central to ecosystem response to disturbance. Species life-history traits 35 represent an adaptive response to disturbance history and are an information legacy; the abiotic 36 and biotic structures produced by single disturbance events are material legacies. These two 37 types of legacy represent an ecosystem’s ecological memory, and their alignment with 38 disturbance characteristics creates a “safe operating space” for recovery from disturbance. 39 However, legacies can be lost or diminished as disturbance regimes and environmental 40 conditions change, creating a “resilience debt” that manifests only after the system is disturbed. 41 Strong effects of ecological memory on post-disturbance dynamics imply that contingencies 42 from individual disturbances, interactions among disturbances, and climate variability combine 43 to affect ecosystem resilience. We illustrate these concepts and introduce a novel ecosystem 44 resilience framework with examples of forest disturbances, primarily from North America. 45 Identifying legacies that support resilience in a particular ecosystem provides a framework for 46 anticipating when disturbances may trigger abrupt shifts in forest ecosystems, and when forests 47 are likely to be resilient. 48 49 Key concepts in a nutshell: 50 - Disturbances shape forest landscape patterns and processes over years, decades, and centuries. 51 Change in disturbance characteristics has been and will be a key driver of forest responses to 52 environmental change. 53 - Mechanisms that impart forest resilience to disturbance depend on information legacies, such 54 as disturbance adaptations of species and the frequency of their associated traits; and material 55 legacies, which include seeds, survivors, and the pools and spatial distributions of biomass 56 and nutrients following disturbance events. 57 - When disturbance regimes (eg, disturbance frequency, severity, size, or timing) shift so that 58 key information or material legacies are misaligned or modified, changes to this ecological 59 memory can trigger rapid reorganization into new ecosystem states. Time lags in system 60 response to such changes can produce a resilience debt. 61 - A framework for anticipating when and where forests will be most vulnerable to changes in 62 climate and disturbance can be developed by defining the safe operating space where 2 63 information and material legacies overlap with disturbance characteristics and post- 64 disturbance environmental conditions. 65 3 66 Introduction 67 Patterns and processes of disturbance and recovery shape the dynamics of many 68 ecosystems (White and Jentsch 2001). As the climate changes, however, the nature of 69 disturbances is also changing, increasing uncertainty in how ecosystem dynamics will play out in 70 the future (Turner 2010). Alterations in disturbance regimes (eg, patterns of severity, frequency, 71 and timing) are being observed more frequently, along with historically novel disturbance events 72 and disturbance interactions (Turner 2010; Trumbore et al. 2015). Contemporary and 73 paleoecological observations indicate substantial resilience of ecosystems to historical 74 disturbances, meaning that ecosystems recover their essential structure and function after 75 perturbation (Holling 1973). However, disturbances can also trigger persistent changes in 76 ecosystem state (Scheffer et al. 2001) and increase vulnerability to degradation (Ghazoul et al. 77 2015; Seidl et al. 2016). Understanding the mechanisms that determine when, where, and how 78 shifting climate and disturbance regimes fundamentally alter ecosystem dynamics is a critical 79 question in the 21st century (Turner 2010; Trumbore et al. 2015). 80 Ecosystem processes and patterns depend on the contemporary environment and the 81 persistent effects, or legacies, of past events (Franklin et al. 2000; Seidl et al. 2014; Monger et 82 al. 2015). Disturbances generate biological legacies that interact with environmental conditions 83 to shape ecosystem recovery (Franklin et al. 2000). Today, global changes in climate, land use, 84 and species invasions are rapidly altering disturbance characteristics and legacies, triggering 85 abrupt shifts among multiple ecosystem states (Frelich 2002; Hughes et al. 2013) and creating 86 novel environments and ecosystems (Williams and Jackson 2007). Following a transition, 87 alternate states may be maintained by new sets of legacies and reinforcing feedbacks (Scheffer et 88 al. 2001; Bowman et al. 2015). 89 Environmental change also alters the context in which ecosystems recover from 90 disturbance (Trumbore et al. 2015). As a result, ecosystems may be shifting from dynamic 91 equilibria in variable but largely consistent environments to non-equilibrium dynamics under 92 conditions of ongoing, directional change. Anticipating these dynamics in forests is challenging 93 because disturbance and resilience play out over decades to centuries and across vast areas 94 (Hughes et al. 2013; Ghazoul et al. 2015). Nevertheless, forecasting future forest responses to 95 disturbance is increasingly important, especially where human livelihoods and wellbeing depend 96 on maintaining forest structure and function (Seidl et al. 2016). 4 97 We anticipate that changes to climate, disturbance regimes, and biological legacies will 98 substantively influence forest landscapes, potentially disrupting feedbacks that confer resilience 99 and amplifying processes that may trigger state changes in forest ecosystems. Thus, a key 100 question emerges: Under what conditions are forests likely to be resilient to altered disturbance 101 regimes, and how do different components of ecological memory enhance or erode resilience? 102 We synthesize examples from forests that have been strongly affected by fire or other 103 disturbances to provide insights into mechanisms that support ecosystem resilience to changing 104 climate and disturbances. In doing so, we identify a new framework for ecosystem resilience that 105 highlights how changes in ecological memory may contribute to abrupt transitions in forests and 106 other ecosystems in coming decades to centuries. 107 108 Ecological memory and forest resilience 109 Forests typically are well adapted to a particular historical disturbance regime – the 110 characteristic patterns of disturbance along axes of frequency, severity, size, or other attributes 111 (Turner 2010). Recurring disturbance patterns exert strong selective pressure on life history 112 strategies that affect population survival and spread (Keeley et al. 2011). Forest species 113 consequently evolve survival and regeneration strategies that are tuned to disturbance regimes 114 rather than individual disturbance events (Keeley et al. 2011). In the biotic community, the suite 115 of disturbance-response traits provides one component of “ecological memory” in the form of 116 information legacies of evolutionary adaptations to historical disturbances (Box 1). Species with 117 regeneration traits that are well aligned with a given disturbance regime have an immediate and 118 powerful recruitment advantage after a typical disturbance event. For example, persistent 119 understory seedling banks of shade-tolerant species have a regeneration advantage following 120 windstorms that injure canopy trees (Frelich 2002). Similarly, severe stand-replacing fires that 121 remove competing vegetation favor species that can resprout or regenerate rapidly from seed 122 banks (Pausas and Keeley 2014). Stand-replacing fire regimes thus frequently select for serotiny 123 (aerial seed banks held on the plant, as in many Pinus and Banksia species), which assures 124 abundant, rapid postfire re-establishment (Lamont and Enright 2000). Thus, the information 125 legacy of species traits present in a community or population allows an ecosystem to recover