Received: 13 July 2019 | Accepted: 2 January 2020 DOI: 10.1111/gcb.15031 PRIMARY RESEARCH ARTICLE Population collapse and retreat to fire refugia of the Tasmanian endemic conifer Athrotaxis selaginoides following the transition from Aboriginal to European fire management Andrés Holz1 | Sam W. Wood2 | Carly Ward2 | Thomas T. Veblen3 | David M. J. S. Bowman2 1Department of Geography, Portland State University, Portland, OR, USA Abstract 2School of Biological Science, University of Untangling the nuanced relationships between landscape, fire disturbance, human Tasmania, Hobart, Tas., Australia agency, and climate is key to understanding rapid population declines of fire- 3Department of Geography, University of Colorado, Boulder, CO, USA sensitive plant species. Using multiple lines of evidence across temporal and spa- tial scales (vegetation survey, stand structure analysis, dendrochronology, and fire Correspondence Andrés Holz, Department of Geography, history reconstruction), we document landscape-scale population collapse of the Portland State University, Portland, OR long-lived, endemic Tasmanian conifer Athrotaxis selaginoides in remote montane 97201, USA. Email: [email protected] catchments in southern Tasmania. We contextualized the findings of this field-based study with a Tasmanian-wide geospatial analysis of fire-killed and unburned popu- Sam W. Wood, School of Biological Science, University of Tasmania, Private Bag 55, lations of the species. Population declines followed European colonization com- Hobart, Tas. 7001, Australia. mencing in 1802 ad that disrupted Aboriginal landscape burning. Prior to European Email: [email protected] colonization, fire events were infrequent but frequency sharply increased after- Funding information wards. Dendrochronological analysis revealed that reconstructed fire years were as- Australian Research Council, Grant/ Award Number: DP11010195; National sociated with abnormally warm/dry conditions, with below-average streamflow, and Science Foundation, Grant/Award Number: were strongly teleconnected to the Southern Annular Mode. The multiple fires that 0966472, 1738104 and 1832483 followed European colonization caused near total mortality of A. selaginoides and resulted in pronounced floristic, structural vegetation, and fuel load changes. Burned stands have very few regenerating A. selaginoides juveniles yet tree-establishment reconstruction of fire-killed adults exhibited persistent recruitment in the period prior to European colonization. Collectively, our findings indicate that this fire-sensitive Gondwanan conifer was able to persist with burning by Aboriginal Tasmanians, de- spite episodic widespread forest fires. By contrast, European burning led to the re- striction of A. selaginoides to prime topographic fire refugia. Increasingly, frequent fires caused by regional dry and warming trends and increased ignitions by humans and lightning are breaching fire refugia; hence, the survival Tasmanian Gondwanan species demands sustained and targeted fire management. KEYWORDS climate change, climate modes teleconnections, dendroecology, fire feedbacks, fire refugia, forest regeneration dynamics, human–fire interactions Glob Change Biol. 2020;00:1–14. wileyonlinelibrary.com/journal/gcb © 2020 John Wiley & Sons Ltd | 1 2 | HOLZ et aL. 1 | INTRODUCTION Rainforests dominated by the Tasmanian paleoendemic Athrotaxis selaginoides (family Cupressaceae) are an ideal model system for Abrupt ecological transitions can result from pervasive and am- exploring the effects of altered fire regimes on fire-sensitive taxa. plified environmental changes, which have increased during the This species evolved in cool and wet climates where fire was rare Anthropocene epoch (Steffen et al., 2018). A prime example con- (Hill, 1995; Jordan, Harrison, Worth, Williamson, & Kirkpatrick, cerns changes in fire regimes associated with the compounding ef- 2016; Kershaw & McGlone, 1995). A recent study of the two pa- fects of climate change. For instance, more extreme and protracted leoendemic Tasmanian Cupressaceae conifers A. cupressoides and fire weather and increased lightning activity, changes in fuel types Diselma archeri found the most genetically heterogeneous pop- and loads, and altered ignition patterns associated with land use ulations in the sites considered least likely to burn (Worth et al., changes have been reported (Abatzoglou & Williams, 2016; Balch 2017). A. selaginoides has no fire adaptations (Enright et al., 2015): et al., 2017). Rapid changes in fire regime can cause fundamental it grows slowly, disperses poorly, lacks vegetative reproduction, and abrupt changes to the structure, diversity, and function of forest and experiences irregular cone production (Gibson, Barker, Cullen, ecosystems (Bowman, Murphy, Neyland, Williamson, & Prior, 2014; & Shapcott, 1995). The species, like its congener A. cupressoides Johnstone et al., 2016; Millar & Stephenson, 2015; Seidl et al., 2017; and most Gondwanan Cupressaceae species, has features that fa- Walker et al., 2006). Of particular concern is the vulnerability of cilitate dendrochronological analysis and landscape-scale mapping fire-sensitive plants to rapid local extinction due to climate change— including a longevity that spans the Aboriginal to European peri- increased fire frequency interactions. Such plant species typically ods (Ogden, 1978), decay resistant wood (Cox, Yamamoto, Otto, & possess little to no fire resistance nor have fire recovery traits, and Simoneit, 2007; Simoneit, Cox, Oros, & Otto, 2018) that allow fire- often have low reproductive output and slow growth and thus lim- killed stands to remain standing (Holz & Veblen, 2009; Holz et al., ited postfire recovery (Enright, Fontaine, Bowman, Bradstock, & 2015; Mundo, Holz, González, & Paritsis, 2017), and well-preserved Williams, 2015). Such species, currently persist in fire refugia that fire scars (Holz et al., 2015). Despite the above, the effects of fire are infrequently exposed to fire due to climatic or topographic fire or climate on tree establishment of A. selaginoides have not been protection (Kitzberger et al., 2016; Tepley et al., 2018). quantified and is well overdue. The Southern Hemisphere temperate forest biome is character- Cupressaceae taxa in Tasmania have high-quality fossil pollen ized by the intermix of both fire-adapted and fire-sensitive species. and genetic diversity records that provide a long-term context of the Understanding the history of paleo-endemic species can shed light impact of late-Pleistocene and Holocene fire–human–climate dy- on why some forest ecosystems have greater resilience to fire re- namics on Athrotaxis (Fletcher et al., 2014; Worth et al., 2016, 2017). gime change than others. This is a critical but challenging biogeo- Recent Tasmanian paleoecological research has suggested that the graphic question that demands untangling the complex relationships intensification of El Niño–Southern Oscillation (ENSO) since the mid- between landscape, fire disturbance, human fire usage, and climate Holocene led to increase fire activity and associated vegetation change variability. Yet, the recent geographical extent and persistence of in N and SE parts of the island (e.g. Fletcher et al., 2014; McWethy, these forests in the Quaternary Period has been shown to vary Haberle, Hopf, & Bowman, 2017). Furthermore, climate-fire anal- around the Southern Hemisphere landscapes because of differential yses over the instrumental-time period (i.e. post-1950s) suggest effects of human set landscape fire which modified plant commu- highly complex geographical patterns of teleconnections (or remote nity structure, composition, and flammability (e.g. McWethy et al., influences) of large-scale climate modes on fire activity across the 2013). For example, the recent (ca. 750 cal yr bp) arrival of Maori relatively small island of Tasmania: ENSO influencing northern and people's burning practices to New Zealand resulted in abrupt and northeastern, Indian Ocean Dipole north and northeast, and the geographically widespread retreat of Gondwanan forests (Perry, Southern Annular Mode (SAM, or Antarctic Oscillation) in western Wilmshurst, McGlone, & Napier, 2012). The interplay of human ig- and southern parts of the island (Mariani, Fletcher, Holz, & Nyman, nitions is more nuanced following the peopling of Tasmania in the 2016; Mariani et al., 2018). It is therefore important to consider the late Pleistocene (ca. 45,000 years ago), which saw both vegetation association of climate modes affecting fire activity, yet high-resolu- patterns and fire activity adjusting to global-scale climate changes tion studies at interannual scales over the Aboriginal-European fire from the Pleistocene to the Holocene (last 10,000 years; MacPhail, regime transition period have not been attempted in Tasmania. An 2010). Furthermore, there is emerging evidence of fundamentally advantage of studying A. selaginoides is that there are well-developed different fire use among the various cultures that colonized south- climate and stream flow dendrochronological reconstructions based ern Hemisphere landscapes, which is most apparent in the contrast- on this species enabling consideration of the interplay of climate and ing ecological impacts of indigenous versus European peoples (Holz fire in affecting forest stand dynamics (e.g. Allen et al., 2015, 2017). et al. 2016; Holz & Veblen, 2011; Holz, Wood, Veblen, & Bowman, The overarching aim of this study is to understand the popula- 2015; McWethy,