Population Collapse and Retreat to Fire Refugia of the Tasmanian Endemic

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, Wilmshurst, Whitlock, Wood, & McGlone, 2014; tion collapse and retreat to fire refugia of the Tasmanian endemic Méndez et al., 2016). For instance, the Tasmanian paleoendemic conifer A. selaginoides following the transition from Aboriginal to conifer Athrotaxis cupressoides suffered widespread population de- European fire management. More specifically, we ask, how does clines following the transition from Aboriginal to European fire man- fire affect stand structure, plant community composition, and agement (Holz et al., 2015). demographic legacies on A. selaginoides populations? What is the HOLZ et aL. | 3 temporal relationship (timing) between fire activity, tree demo- 2.2 | Catchment-scale study graphic processes (tree establishment and mortality), and climate? Are these relationship in agreement with documented changes in 2.2.1 | Study sites human ignition (from Aboriginal to European burning) in Tasmania? Does topography (i.e. topographic fire refugia) explain the frag- To examine the impacts of fire on A. selaginoides forests, we studied mented distribution of burned and unburned A. selaginoides across burned and unburned montane catchments (c. 800 m a.s.l.) in the its entire distribution in Tasmania? We address all of the above remote Southern Ranges: burned Abrotanella Rise and unburned Mt questions by undertaking multi-spatial and temporal scale analy- Bobs (Figure 1). The catchments are 3 km apart and are located in sis of A. selaginoides. Our study is centered on closely proximate the upper reaches of a steep dolerite mountain range that divides catchments, one burned and the other unburned, in the Southern the tall wet eucalypt dominated ecosystems to the east and a moor- Ranges of western Tasmania. Using vegetation field surveys and land-dominated vegetation mosaic to the west (Wood & Bowman, dendroecological analyses, we compare the burned and unburned 2012), and share similar bioclimatic conditions (Harris & Kitchener, catchments and test whether fire results in differences in stand 2005). The vegetation, including the A. selaginoides forest, of the Mt structure, plant community composition, and demographic leg- Bobs area has been described by Kirkpatrick and Harwood (1980). acies on A. selaginoides populations. We use dendroecological techniques to test whether the timing of tree demographic change (tree mortality and tree establishment reconstruction over the 2.2.2 | Plant community, stand structure, and ca. 1400–1980 ad period) is linked to fire activity, and also gauge fine fuels whether climate mediates any of these dynamic. We contextualize the finding of this catchment-scale study by undertaking a land- We used 25 m × 8 m belt transects to assess tree abundance, basal scape-scale analysis of all extant mapped A. selaginoides stands area (BA), and size class distributions, as well as tree floristic com- in relation to topographic fire refugia, where we test whether A. position of contemporary adult and juvenile tree communities in selaginoides stands (burned and unburned) occupy areas of higher sites at burned (Abrotanella Rise n = 8) and unburned catchments topographic protection than other vegetation types and whether (Mt Bobs n = 5; Figure 1b–d). On each transect, all live and dead unburned A. selaginoides occupy areas with even higher topo- adult trees (i.e.>5 cm diameter at breast height, DBH) were identi- graphic protection than burned stands. Collectively, we use these fied to species level, tallied, and measured for DBH. All juvenile trees findings to understand the persistence of A. selaginoides in the (DBH < 5 cm and height > 30 cm) were tallied. BA (m2/ha) of live landscape in the face of new fire regimes under ongoing anthro- and dead trees (DBH > 5 cm) was calculated for each species and pogenic climate change. compared between both sites using the Wilcoxon-rank sum test. The frequency distribution of live and dead A. selaginoides trees was cal- culated in 5 cm diameter classes at both locations. 2 | MATERIALS AND METHODS Along the mid-line of each belt transect, we placed eleven 2 m2 circular plots to examine abundance (cover, %), richness (number of 2.1 | Geographical context species), and overall floristic composition of understory plants in burned A. selaginoides stands at Abrotanella Rise catchment (n = 88) The continental island of Tasmania is located SE of mainland Australia and unburned stands at the Mt Bobs catchment (n = 55) using six between 41–44°S and 145–149°E, and it covers an area of ca. cover classes (0%, 0%–5%, 5%–25%, 25%–50%, 50%–75%, and 6,800 km2. The island has a varied geology, with infertile quartzite >75%). Floristic descriptors for understory plants were based on in the west, more fertile dolerite in the east, and overall rugged ter- these circular plots, whereas floristic descriptors for trees were rain reflecting extensive Pleistocene glacial and periglacial activity based on belt transects (see above). Graminoids and mosses were (Pemberton, 1989). The island's climate is cool maritime, with summer grouped and Sphagnum species were identified at the genus level. and winter minimum and maximum temperatures of 10 and 20°C, and We used detrended correspondence analysis (DCA) to explore the 3 and 10°C, respectively (King et al., 2006). Across the island, there differences in abundance and floristic composition of unburned and is a steep west to east orographic rainfall gradient associated with burned stands of A. selaginoides. the westerly rain-bearing winds with highest annual precipitation in Detrended correspondence analysis ordinations were calculated the western mountains up to 3,000 mm and lowest in rain shadows using (a) count of juvenile and adult trees in the understory and over- on the eastern side of ca. 600 mm (King et al., 2006). The vegetation story combined using belt transect data; and (b) per cent cover of of Tasmania is characterized by extensive tracts of highly flammable understory plants of all taxa obtained from the circular plots. We used treeless sedgelands and grassland, sclerophyll heath and scrub, and PC-ORD (McCune & Mefford, 2011) to conduct DCA with Bray–Curtis Eucalyptus forests with much smaller tracts of fire-sensitive alpine dissimilarity. We also calculated the number of species present in each vegetation and temperate rainforests. The environmental controls of circular plot and belt transect (i.e. species richness), respectively, and these mosaics involve a complex interplay of climate, edaphic factors, investigated trends in species richness for burned and unburned stands and fire disturbance (Bowman & Perry, 2017; Jackson, 1968). in Axis 1 ordination space. 4 | HOLZ et aL.

FIGURE 1 Distribution of Athrotaxis selaginoides in Tasmania (a). The Southern Ranges in southern Tasmania (b), with A. selaginoides forest burned at the Abrotanella Rise site (c) and unburned (control) at the Mount Bobs site (d). In (a), the A. selaginoides bioclimatic domain displayed across Tasmania is displayed (Porfirio et al., 2014) and the area of field-based work is highlighted in the red box Vegetation data source: TASVEG (Harris & Kitchener, 2005)

To measure available fine-fuel load, we adapted the planar inter- search for juveniles and larger trees within a 4 and 8 m strip each side cept method (Brown, 1971; Catchpole & Wheeler, 1992) following of a centerline, respectively. We noted the occurrence of (a) live A. Holz et al. (2015) and Paritsis, Veblen, and Holz (2015) to measure the selaginoides trees (DBH > 10 cm); (b) live A. selaginoides juveniles (i.e. ‘particle density per unit volume’ of the finest live biomass-size class height > 30 cm and DBH < 10 cm); and (c) dead standing A. selaginoides (i.e. 1 hr; diameter < 0.6 cm; Brown, 1971) for woody and nonwoody trees (DBH > 10 cm). When live juveniles were encountered, we noted shrub species up to a height of 3 m (the maximum height of shrubs). GPS location, height, and vigor (from 1: healthy to 4: unhealthy). We This involved visual estimates of the volume (i.e. particle density) of estimated the age of each juvenile based on the age–height model 1 hr leaves and stems within a cylinder of 2 m diameter and a height developed for Abrotanella Rise from dead saplings harvested adjacent of 3 m for each of the 11 circular plots on each transect. This measure to our plots (see below). has been used effectively elsewhere in Tasmania (Holz et al., 2015) and serves as a time-efficient estimate of the biomass and cover of the fuel class that is most likely carry fire across the landscape. 2.2.4 | Dendroecological reconstruction of stand structure (size, age, and composition), tree mortality dates, fire frequency and severity, and postfire tree 2.2.3 | Field traverse and seedling search recruitment

After extensive field reconnaissance, it was apparent that regen- Coring of live trees was not allowed by the Tasmanian conservation eration was extremely rare, and vegetation density was so high that and management authorities (DPIPWE, Tasmania), thus limiting our visibility was limited to ca. 4–8 m (Figure 1e). Thus, we developed sampling design to dead trees, including up to 20 cross-sections for a sampling method based on strategies used to detect rare plants fire scar reconstructions (see below). To reconstruct size and age (Keith, 2000) to estimate the density of live and dead A. selaginoides structure at the stand-scale in the burned study site, two plots of var- seedlings and trees across the wider Abrotanella Rise landscape well ying sizes (400–800 m2 to capture a minimum of 20 trees/plot or min- beyond our plots (Figure 1c). We walked a series of field transects in imum density of 250 trees/ha) were located within six stands within HOLZ et aL. | 5 the Abrotanella Rise burned site (i.e. Lake Burgess basin; Figure 1c). and of the Southern Annular Mode (Villalba et al., 2012; Figure S1). Within each plot, all trees >4 cm DBH were identified at the species For the climate-fire SEAs, a 5-year window of mean climate condi- level, and DBH and increment cores were collected (total n = 349 tree tion was centered on years of fire (all fire dates were included for cores, mean = 56 tree cores/plot; range = [18–68 tree cores]). Coring this fire-sensitive species; i.e. min ≥ 1 scarred tree). For the climate- height was 20 cm but increased for rotten trees. To correct for core- recruitment SEAs, a 5-year window of mean climate condition was extraction height, height–age linear models were calculated (mean also centered on years of tree establishment. For these latter SEAs, r2 = .47). These models were derived from cross-sections cut every we only relied on establishment dates from cores with pith. In both 10 cm in height from each five to seven dead standing juveniles (ca. SEAs, significance levels of the departures from the long-term mean 1 m tall) that were harvested adjacent to each plot. were determined from bootstrapped confidence intervals (95%) es- A total of 20 partial cross-sections were collected from dead, fire- timated from 10,000 Monte Carlo simulations. scarred trees across the perimeters of the Abrotanella Rise study area To better detect any temporal associations between fire events to determine historical fire events (e.g. Holz et al., 2015). Charcoal and recruitment pulses over a range of lags prior to European burning evidence was searched for and found in 100% of the sampled scarred at Abrotanella Rise, we used reconstructed records of fire and tree trees. Additional increment cores were extracted from fire-scar sam- establishment during the 1480–1800 ad period and applied the bivar- pled trees to facilitate the crossdating process. All dendroecological iate Ripley's K function modified for one-dimensional data using K1D samples were processed using standard dendroecological techniques version 1.2 (Gavin, 2007). For this, we used all fire event years prior

(Stokes & Smiley, 1968) and were visually and statistically crossdated to 1800 ad and years of tree establishment when pulses were >70th (Holmes, 1986; Yamaguchi, 1991) using marker rings from a cross- percentile. To test whether recruitment events change following fire dated, tree-ring master chronology developed from live A. selaginoi- within a window of t years, the K function was calculated using a bivar- des trees in a nearby stand (5 km to the north; Allen et al., 2011). A iate model with forward selection. The K function was then converted total of 83% (n = 289) of tree cores and 60% (n = 12) of fire scars to the L function (LAB(t)), where values near 0 indicate independence were successfully crossdated. To estimate and correct for cores and those above or below 0 represent synchrony or asynchrony, re- missing the tree pith, recruitment-date estimates were used with spectively (Gavin, Hu, Lertzman, & Corbett, 2006). A 95% confidence Duncan's (1989) geometric method to estimate the number of miss- envelope was produced from 10,000 randomizations in which fire ing rings between the pith and the first complete tree ring (i.e. up to dates were fixed and a number of recruitment pulses equal to the 35 years; mean = 13 ± 0.75 SE years). The remaining cores (i.e. from number found at Abrotanella Rise was generated randomly following rotten trees or from tree cores without piths and off-center correc- a Poisson process (Gavin, 2007). tions > 35 years) were included in the recruitment-date estimates and are reported as minimum ages. From all crossdated tree-ring cores, 19% included pith, 49% were Duncan-pith corrected, and 32% had 2.3 | Landscape-scale study a minimum age. To estimate whether the fire-kill date was recent (i.e. after European arrival to Tasmania in 1803 ad) and/or historical (pre- To contextualize the above catchment-scale studies, we assess the

1802 ad), the last or most recent ring in each tree was determined (via role of topographic fire refugia in determining the fragmented distri- crossdating procedures as explained above) and used as date of tree bution of burned and unburned A. selaginoides across its entire distri- death. Due to an unknown number of outermost rings that might have bution in Tasmania using a digital elevation model, vegetation maps been lost (due to weathering), mortality dates are referred as minimum and a published climate envelope for A. selaginoides (Porfirio et al., mortality dates and thus reported in 20 year bins. Previous work using 2014; Figure 1a). The vegetation of Tasmania has been mapped at known fire dates and crossdated tree rings from dead individuals of 1:25,000 (Harris & Kitchener, 2005) and includes delineated areas of the Cupressaceae tree species in Tasmania (Holz et al., 2015) and else- burned and unburned A. selaginoides and fire barriers (i.e. lakes, scree where in the southern hemisphere (Holz, Hart, Williamson, Veblen, & slopes; Brown, 1988; Figure 1). Mapped A. selaginoides occurs mostly Aravena, 2018; Holz et al., 2017) gave us the confidence that wood as a dominant or codominant tree within rainforest, but sometimes decay is minimal even after decades, given that Cupressaceae trees occurs in more open, sparsely treed stands. Following a terrain analy- have high levels of decay-proof secondary compounds (Haluk & sis framework developed by Wood, Murphy, and Bowman (2011; see Roussel, 2000; Holz & Veblen, 2009). also Murphy et al., 2010), we sampled 4,000 randomly allocated points To quantify interannual-scale relationships of local hydroclimate, within the climatic domain of A. selaginoides, and allocated each point hemispheric climate, and climate mode reconstructions and the com- with (a) a vegetation type (burned A. selaginoides; unburned A. selagi- plete reconstructed record of (a) fire events (1547–1954 ad) and (b) noides; other vegetation type); (b) a topographic position ranked in tree recruitment (1267–1962 ad), Superposed Epoch Analysis (SEA) decreasing topographic flammability from 1 to 4 (ridge and flat = 1; was used (Baisan & Swetnam, 1990) in the dplR package in R. To gentle slope = 2; moderate and steep slope = 3; and valley = 4); and conduct these SEAs, we used a streamflow reconstruction for west- (c) a 'Poleward Index' that represents a gradient from shady, steep ern Tasmania (Allen et al., 2015), a temperature reconstruction for poleward-facing slopes (strongly positive values) to sunny, steep the southern hemisphere known to control tree growth in Tasmania equatorward-facing slopes (strongly negative values; adapted from (Neukom et al., 2014), and reconstructions of ENSO (Li et al., 2011) Holden, Morgan, & Evans, 2009). While these indices are relative 6 | HOLZ et aL. simple, previous work by Wood et al. (2011) shows that they are ex- cellent predictors of rainforest distribution and fire spread in western Tasmania. A more elaborate spatial analysis using alternative indices of topography (e.g. Bradstock, Hammill, Collins, & Price, 2010; Krawchuk et al., 2016) may reveal other more nuanced relationships between A. selaginoides and the landscape (e.g. the effect of westerly winds) and would be worthwhile exploring. Further details of the calculation of these variables can be found in Wood et al. (2011) and are explained in more detail in the Supporting Information (Text S1). Models represent- ing all combinations, without interactions, of topographic position and Poleward indices were constructed using generalized autoregressive error models (GARerr; Murphy et al., 2010). These models analyze spa- tially autocorrelated non-normal data (Murphy et al., 2010) and have also been used in an analogous spatial investigation of rainforest, fire and topography in western Tasmania (Wood et al., 2011) and are ex- plained in more detail in the Supporting Information (Text S1).

3 | RESULTS

3.1 | Catchment-scale study

3.1.1 | Vegetation of burned and unburned catchments

FIGURE 2 Ordination results from detrended correspondence The contemporary vegetation of the burned catchment at Abrotanella analysis in burned (dark grey, n = 15 transects) and unburned Rise is a very dense, low stature (ca. 8 m) subalpine rainforest (Harris (white, n = 10 transects) forests based on abundance and richness & Kitchener, 2005) dominated by Nothofagus cunninghamii, Eucryphia collected within belt transects: (a) juvenile (triangles) and adult lucida and Orites diversicolor with conspicuous dead standing (square) trees abundance (based on counts in the understory and A. selaginoides rising above the canopy throughout the catchment overstory strata combined), and (b) species richness' counts for burned and unburned stands observed in Axis 1 ordination space (Table S1; Figure 1; Figure S2). At the unburned catchment at Mt Bobs in (a). In (a) and (b), results are reported by size class: juvenile the emergent stratum, of about 18–30 m, is almost entirely occupied (DBH < 5 cm and height > 30 cm) and adult (DBH > 5 cm) trees by A. selaginoides, with a canopy stratum, of about 7–15 m, dominated by N. cunninghamii and Atherosperma moschatum (Table S1; Figure S2). Ordination analysis showed that the floristic composition of con- 0 live standing tree (0 stems/ha) and 11 live A. selaginoides juveniles temporary adult and juvenile tree communities at Abrotanella Rise (2 stems/ha; Table 2). (burned) and Mt Bobs (unburned) is markedly different (Figure 2a). The structure and abundance of living vegetation at the burned Similarly, there are marked differences in the understory plant com- Abrotanella Rise catchment is different to that in the unburned munity composition (i.e. % cover) between the burned and unburned catchment at Mt Bobs, including lower live BA and smaller live sized stands (Figure 3a). Tree species richness is highest in unburned trees (DBH < 10 cm) dominated by basal resprouters, including N. stands (Figure 2b) and understory plant species richness is highest cunninghamii (55% of BA) and E. lucida (27% of BA; Table 1; Figure in burned stands (Figure 3b). S3). The cumulative (dead and live) BA of large trees, especially A. selaginoides, at the Mt Bobs catchment was larger than that at the Abrotanella Rise catchment (Figure S3). Collectively, these results 3.1.2 | Stand structure and composition suggest marked demographic impact of fire in the Abrotanella Rise catchment. Dead trees in the Abrotanella Rise catchment had a total BA of 97 m2/ha dominated by large diameter (Figure S3) A. selaginoides (73% of BA) and N. cunninghamii (26% of BA) trees (Table 1). At Abrotanella 3.1.3 | Fire history, stand dynamics, and climate Rise live trees account for only ca. 10% of the total BA of live plus variability dead trees. Live A. selaginoides trees were completely absent from Abrotanella Rise and juveniles were rare (Table 1). Field traverses of Over the last ca. 600 years, 10 fire events were recorded by A. the postfire forest found 1,566 dead standing trees (138 stems/ha), selaginoides trees in the Abrotanella Rise catchment with seven HOLZ et aL. | 7

TABLE 2 Stem density of Athrotaxis selaginoides at the burned Abrotanella, fire-killed site by size class. Standing, live juveniles (i.e. seedlings and saplings; <4 cm DBH and >30 cm height) and trees (>4 cm DBH), and standing dead trees (>4 cm DBH) obtained from the field traverses

Transect Transect Survey No. Density length width area trees (stems/ (m) (m) (ha) (stems) ha)

Live juveniles 7,085 8 5.7 11 2 Live trees 7,085 16 11.3 0 0 Dead trees 7,085 16 11.3 1,566 138

Abbreviation: DBH, diameter at breast height.

events recorded by single trees and three events recorded by two trees. (Figure 4; Figure S4). Thousands of A. selaginoides' trees killed by recent fires remain standing in the landscape (Figure S2) but we were restricted to sample 20 cross-sections total due to strict permit guidelines. Few trees had visible scarring, suggesting tree survival (and postfire ‘cat-face’ scar formation) was relatively rare. From the reconstruction of minimum-mortality dates, we es- timated that the vast majority of A. selaginoides trees were killed by fire in the second half of the 19th century, whereas few trees

have been dead and standing since the mid-1500s ad (ca. 3 trees/ ha; Figure 4b). During this former period, ca. 50 adult trees per ha FIGURE 3 Ordination results from detrended correspondence analysis in burned (Abrotanella; dark grey, n = 88 plots) and per decade were killed by fire. Prior to European burning, pulses unburned (Bobs; white, n = 55 plots) forests based on abundance of establishment of A. selaginoides (>70th percentile) were largely and richness data collected in circular plots along belt transects: independent of fire-scar dates, except during and 1 year after (a) understory plant abundance (based on cover %) of all taxa, and wildfire events, where wildfire had a negative effect on tree es- (b) understory species richness for burned and unburned stands tablishment (Figure S5). observed in Axis 1 ordination space in (a) Wildfires at Abrotanella Rise in the Southern Ranges during the

1547–1954 ad period were related to years of anomalously dry con- 2 TABLE 1 Total basal area (m /ha) for burned (fire-killed; ditions (i.e. lower than average streamflow values) during the year Abrotanella) and unburned (live; Bobs) trees (>4 cm DBH) obtained of the fire (Figure 5a) and warmer than average conditions prior and from belt-transects during the year of the fire (Figure 5b). Both antecedent and coinci- Abrotanella (burned) Bobs (unburned) dent dry and warm conditions and fire occurrence were also strongly 2 2 BA (m /ha) BA (m /ha) linked to positive values of the Southern Annular Mode (Figure 5c).

Live Dead Live Dead ENSO was not linked to fire activity (Figure 5d). Age data suggest that A. selaginoides trees have established Athrotaxis 0 71b,* 170c,* 2 selaginoides continuously at Abrotanella Rise catchment since the late ca. 1200 ad until ca. 1800 ad, with a ca. 110-year window of highest Nothofagus 6 25b,* 72c,* 7 cunninhamii establishment between ca. 1550 and 1660 ad (Figure 4c). Short- Eucryphia lucida 3b,* 0 7c,* 0 term declines in establishment coincided with recorded fires in the early 1500s and early 1700s. Tree establishment declined in Richea pandanifolia 0 0 5 0 the early 1800s when Europeans arrived in Tasmania. During the Orites diversifolia 2 1 0 0 1400–1780 ad period, tree establishment had a strong associa- Other speciesa 0 0 8 0 tion with negative SAM values prior, during and after the year of Total 11 97 262 9 tree establishment (Figure 5g). Negative SAM is linked over the in- Abbreviations: BA, basal area; DBH, diameter at breast height. strumental climate record in southern Tasmania with high rainfall a Other species are: Trochocarpa gunnii, Phyllocladus aspleniifolius, (Figure S6). ENSO values were above mean conditions during the Atherosperma moscatum, Trochocarpa cunninghamii and Pittosporum year prior to recorded establishment (Figure 5h). In contrast, tree spp. (bold: resprouters). Differences in BA by species are reported by different superscript letters using the Wilcoxon-rank sum test establishment was not associated with temperature (Figure 5f) nor (*p < .001). with streamflow (Figure 5e). 8 | HOLZ et aL.

FIGURE 4 Time series of the Southern Annular Mode (SAM; Marshall index for December–February; Villalba et al., 2012; a), reconstructed fire-kill estimated dates (Athrotaxis' minimum mortality dates; dead trees/ha; b), and reconstructed establishments dates of Athrotaxis selaginoides in the Abrotanella study area during the ca. 1300–2000 ad period (c). Arrows at the top represent reconstructed fire activity dates from fire-scars on cross-sections with one (light arrow) or two (bold arrow) scarred trees. Estimated dates in tree mortality and tree establishment in (b) and (c), respectively, are shown for all plots combined and aggregated into 20 year bins. In (a), annual and 25- year smoothed values are shown by the grey and black lines, respectively. In (b), the period of arrival and settlement of European settlers is shown by the grey hashed area, and mortality dates are referred to as minimum mortality dates due to the unknown number of outermost rings that might have been lost (due to weathering). In (c), tree-establishment estimates are colored by dating precision, that is, pith dates are the most precise

(a) (b) (e) (f)

(c) (d) (g) (h)

FIGURE 5 Impact of climate variability on wildfire occurrence (left panel) and on Athrotaxis establishment (right panel). Departures (standard deviations; SDs) from mean values for reconstructed indices of (a, e) Streamflow (December–January; Allen et al., 2015), (b, f) South Hemisphere Temperature (Neukom et al., 2014), (c, g) Southern Annular Mode (SAM; December–January; Villalba et al., 2012), and (d, h) El Niño–Southern Oscillation (ENSO; Li et al., 2011) for 5-year windows centered on years of wildfires (n = 10 events) and establishment years (pith dates corrected for coring height (n = 36 events) during the 1537–1964 period using Super-imposed Epoch Analysis. Black and dark grey bars represent 95% and 90% CIs derived from 10,000 Monte Carlo simulations

3.2 | Landscape-scale study combined) are more likely to occur on steep, poleward facing as- pects (i.e. more humid; Figure 6a), and valleys (i.e. low topographic 3.2.1 | Range-wide analysis of living and dead flammability [indices 3 and 4]; Figure 6c) that afford a high degree population across Tasmania of topographic protection from fire. Contemporary, live unburned A. selaginoides populations were more likely to occur in areas of Compared to co-occurring vegetation types the historic distri- even lower topographic flammability compared to burned (dead) bution of A. selaginoides populations (i.e. burned and unburned stands (Figure 6d). HOLZ et aL. | 9

(a) (b)

(c) (d)

FIGURE 6 (a, c) Comparison of the Poleward Index (adapted from Holden et al., 2009; box and whisker plots) and Topographic Position Index (proportion plots) for points located within mapped populations of Athrotaxis selaginoides and all other vegetation within the bioclimatic potential distribution of A. selaginoides (Porfirio et al., 2014). (b, d) Comparison of the Poleward Index (box and whisker plots) and Topographic Index (proportion plots) for points located in unburned and burned populations of A. selaginoides. In (a, b), box plots report lower and upper extremes, lower, median and upper quartiles, and mean (black diamond). High (low) values of Poleward (Topographic Index) indicate an increasing level of topographic fire protection. Differences with significant support (i.e. W+ >0.73 in bold) from spatial autoregressive models are reported in (a, c, and d). Topographic flammability is (1 = ridges and flats; 2 = gentle slopes; 3 = moderate and steep slopes; 4 = valleys; based on Wood et al., 2011)

4 | DISCUSSION temperate forests has been reported from New Zealand (Tepley, Veblen, Perry, Stewart, & Naficy, 2016) and southern South America Our study has shown association of spatiotemporal patterns of (Holz, 2009; Paritsis et al., 2015), and we suspect this is also the case live and dead stands of a Tasmanian paleo-endemic conifer A. where the regenerating rainforest is more flammable because of selaginoides with fire history and changes in fire regimes since drier microclimate as a result of shorter and more open canopy and European settlement, and with climate variability. The intensity of higher surface fuel loads (Figure S7). our sampling regime and the remoteness of field sites limited this Close to a century after the fires, we found no live A. selaginoi- study to comparison of a single burned and unburned catchments. des trees and vanishingly few A. selaginoides seedlings. We suggest Nevertheless, by combining multiple lines of evidence across tem- it is highly unlikely that A. selaginoides forest at Abrotanella Rise poral and spatial scales, our results highlight that the distribution catchment can re-occupy this site given (a) the poor dispersal of the and abundance of fire-sensitive tree species is shaped by the inter- species; (b) slow growth to reproductive maturity of the few seed- play between landscape settings, fire disturbance, human agency, lings that occur in this catchment; and (c) the need for long fire-free and climate. interval (Gibson et al., 1995), which is an increasingly unlikely in this region given probable shift in future fire regimes (Harris et al., 2018; Mariani et al., 2018) due to regional drying trends and associated 4.1 | A. selaginoides population collapse rapid increased occurrence of lightning-lit fires (Fox-Hughes, Harris, Lee, Grose, & Bindoff, 2014; Mariani et al., 2018; Styger, Marsden- The long-unburned Mt Bobs catchment supports A. selaginoides Smedley, & Kirkpatrick, 2018). The interlocking demographic effects rainforest (Kirkpatrick & Hardwood, 1980). By contrast, multiple of slow growth to reproductive maturity, limited seed establish- fires in the 19th century in the Abrotanella Rise catchment resulted ment in the face of increased fire risk conforms to the interval in a structural and floristic vegetation transition to short, dense, and squeeze model of Enright et al. (2015). That the population collapse low biomass subalpine rainforest dominated by sprouting N. cunning- of A. selaginoides is irreversible is consistent with local palynolog- hamii and E. lucida. Increased fire hazard in regenerating southern ical records (Fletcher et al., 2014) reporting the local extinction of 10 | HOLZ et aL.

Cupressaceae taxa following multiple fires in the mid-Holocene in sedges that were frequently burned at low severity by Aboriginal nearby catchment in the Southern Ranges of Tasmania (ca. 14 km people to sustain macropod game. Europeans adapted this prac- east of Abrotanella Rise). tice of regular burning but for domesticated stock which did not lead to changes in fuel loads nor fire severity (Holz et al., 2015). In contrast, lush A. selaginoides temperate rainforests (i.e. such 4.2 | Fire activity, tree establishment, and climate as at Abrotanella and Mt Bobs) are mostly burned under severe drought conditions. We suggest that the large-scale mortality of Using dendroecological techniques, we have shown that fires over A. selaginoides forests has been the result of fires that were ig- the last 500 years in the Abrotanella Rise catchment were favored nited by Europeans initially exploring western Tasmania and then by positive phases of the Southern Annular Mode (SAM). The later through increased utilization of the dense southern forests SAM interannual mode represents a poleward movement of the in Tasmania (Marsden-Smedley, 1998). This increased frequency storm track path resulting in dry and warm conditions in Tasmania of fire in formerly rarely used landscapes resulted in a higher (Figure 5; Figure S6). Previous research has also highlighted the probability of coinciding with extreme fire weather conditions. importance of SAM in driving wildfire activity in western and southern Tasmania (Mariani & Fletcher, 2016), as well as in south- ern South America and South Africa (Holz et al., 2017; Mariani 4.4 | Topographic fire refugia et al., 2018). Our study found that the negative mode of SAM, which promotes high rainfall in southern and western Tasmania, Our simple analysis of topographic factors and presence of live and was associated with A. selaginoides establishment (Figure 5). This fire-killed A. selaginoides showed that the pre-European distribu- contrasts the weak establishment-streamflow linkage possibly tion of A. selaginoides (i.e. fire-killed plus unburned stands) became due to the distant geographic location of the streamflow recon- fragmented within its potential climate space, strongly reflecting struction (located north of our study area). Our results indicate the effects of topographic fire refugia. Furthermore, our analysis that that fires in the European period were also set under fire- demonstrated that populations killed more recently by fire (~30% prone-positive SAM conditions when fires were mostly likely to of the population) are associated with fire-prone landscape ele- spread in temperate rainforest. By contrast, it appears that under ments (ridges and northern facing slopes). By contrast, unburned A. Aboriginal fire management fires were not set as frequently under selaginoides populations currently persist in prime topographic-fire positive SAM conditions, and/or SAM did not reach positive val- refugia. The association of A. selaginoides with fire refugia matches ues very regularly (SAM has been reaching maximum values in the closely the finding in Nothofagus-dominated rainforests in south- last century compared to the last 1,000 years; Abram et al., 2014). western Tasmania, where high abundance of fire-sensitive rainforest was found in poleward-facing (mostly steep and moderate) slopes and valleys, while the opposite was true for fire (i.e. ridges, flat, gen- 4.3 | Fire history and humans tle, and equator-facing slopes; Wood et al., 2011). Similar refugia as- sociation is found elsewhere in Nothofagus rainforests in Australia Our chronology of fire events at Abrotanella Rise confirmed that (Collins, Bennett, Leonard, & Penman, 2019) and other temperature the majority of fire events resulting in stand replacement occurred rainforests across the globe (Krawchuk et al., 2016; Landesmann, after 1800 ad following European colonization. This result pro- Gowda, Garibaldi, & Kitzberger, 2015; Leonard, Bennett, & Clarke, vides the first field-based evidence to corroborate the conclusions 2014; McWethy et al., 2018; Paritsis, Holz, Veblen, & Kitzberger, of Brown (1988) that loss of A. selaginoides forests in Tasmania is 2013; Perry et al., 2012). While highlighting the vulnerability of A. likely to be the effect of increased ignition of Europeans during selaginoides to high-intensity fire regimes, the current occupation of a period of more fire-prone climate and weather conditions. This topographic-fire refugia by A. selaginoides is likely to provide a buffer conclusion has some analogies with findings for the closely re- to future fires in western and southern Tasmania, thus increas- lated and similarly fire-sensitive A. cupressoides open forests on ing the chances of the persistence of this species in the landscape the Central Plateau of Tasmania (Holz et al., 2015). The collapse (Landesmann & Morales, 2018; Meddens et al., 2018). of A. cupressoides woodlands and subsequent large-scale switch It remains unclear however, whether topographic fire refugia to alpine heathland on the Central Plateau, occurred after a sin- will be sufficient to buffer extant A. selaginoides populations in the gle, extreme high-severity fire in 1960–1961 associated with a Southern Ranges or elsewhere in Tasmania against increasingly fre- historically anomalous drought (Holz et al., 2015), and these open quent fires. Increased human-set fires and lightning ignitions com- forests are unlikely to recover due to poor dispersal attributes bined and a drying and warming trend driven by anthropogenic (Holz et al., 2015; Worth et al., 2016). There are some substan- climate change have been reported and forecasted for Tasmania tive differences, however, in fire regime between these two fire- (Harris et al., 2018; Mariani et al., 2018, 2019; Styger et al., 2018). sensitive species and their respective ecosystems. A. cupressoides For instance, since the data for this study were collected, two is a montane tree species that occurs in scattered groves in open, very active fire seasons (in 2016 and 2019) have killed stands of rocky woodlands and can co-exist with flammable grasses and Athrotaxis forests in Tasmania (e.g. Bowman, Bliss, Bowman, & Prior, HOLZ et aL. | 11

2019; Harris et al., 2018). Exacerbating the concern over the future Bradstock, R. A., Hammill, K. A., Collins, L., & Price, O. (2010). Effects of weather, fuel and terrain on fire severity in topographically diverse survival of Athrotaxis forests are climate models predictions that landscapes of South-Eastern Australia. Landscape Ecology, 25(4), SAM will disproportionally stay in its positive phase (McLandress 607–619. et al., 2010; Thompson et al., 2011), which favors wildfire activity Brown, J. K. (1971). A planar intersect method for sampling fuel volume and hinders tree establishment of A. selaginoides. As these critical and surface area. Forest Science, 17, 96–102. climate-fire associations increase in strength, the survival of A. selag- Brown, M. (1988). The distribution and conservation of King Billy pine. Hobart, Australia: Forestry Commission, Tasmania. inoides may require increasingly targeted fire management, including Bowman, D. M. J. S., Bliss, A., Bowman, C. J., & Prior, L. D. (2019). Fire rapid attack of uncontrolled fires (Press, 2016; Senate, 2016; Styger caused demographic attrition of the Tasmanian palaeoendemic coni- et al., 2018). fer Athrotaxis cupressoides. Austral Ecology, 44, 1322–1339. https:// doi.org/10.1111/aec.12789 Bowman, D. M. J. S., Murphy, B. P., Neyland, D. L. J., Williamson, G. J., ACKNOWLEDGEMENTS & Prior, L. D. (2014). Abrupt fire regime change may cause land- For research field assistance, we thank David Tng, Cameron Naficy, scape-wide loss of mature obligate seeder forests. Global Change Connemara Burke and the unique-and-only October 2013 field ex- Biology, 20(3), 1008–1015. https://doi.org/10.1111/gcb.12433 pedition. For useful discussion and sharing information on various Bowman, D. M. J. S., & Perry, G. L. W. (2017). Soil or fire: What causes treeless sedgelands in Tasmanian wet forests? Plant and Soil, 420(1), aspects of this research, we thanks Kathy Allen, Simon Haberle, 1–18. https://doi.org/10.1007/s11104-017-3386-7 Michael Fletcher, Phil Higuera, Cathy Whitlock, Cameron Naficy, Catchpole, W. R., & Wheeler, C. J. (1992). Estimating plant biomass: A Tim Brodribb, Jesse Morris, Juan Paritsis, and two anonymous re- review of techniques. Australian Journal of Ecology, 17(2), 121–131. viewers. This research was supported by an Australian Research https://doi.org/10.1111/j.1442-9993.1992.tb007 90.x Collins, L., Bennett, A. F., Leonard, S. W. J., & Penman, T. D. (2019). Council (grant #DP11010195) and National Science Foundation US Wildfire refugia in forests: Severe fire weather and drought mute the (grants #0966472, #1738104, and #1832483). influence of topography and fuel age. Global Change Biology, 25(11), 3829–3843. https://doi.org/10.1111/gcb.14735 CONFLICT OF INTEREST Cox, R. E., Yamamoto, S., Otto, A., & Simoneit, B. R. T. (2007). 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SUPPORTING INFORMATION European fire management. Glob Change Biol. 2020;00:1–14. Additional supporting information may be found online in the https://doi.org/10.1111/gcb.15031 Supporting Information section.

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