Resilience of Resprouting Temperate Forests is Diminished by Coupled Severe Drought and Fire

Elevated tree mortality and reduced recruitment of new trees linked to drought and res has been reported across a range of forests over the last few decades. Forests that resprout new foliage epicormically from buds beneath the bark are considered highly resilient to disturbance, but are potentially at risk of elevated mortality, demographic shifts and changes to species composition due to synergistic effects of drought and re. Despite this, the effects of drought-re interactions on such forests remain largely unknown. We assessed the effects of drought severity and re frequency on juvenile mortality, post-re seedling recruitment and replacement of juvenile trees (balance of recruitment minus mortality) following re. We compared dry ridgetop and wet gully assemblages across a temperate forest in southern Australia. Both forest types experienced higher rates of re-induced juvenile mortality in areas that had experienced severe drought compared to moderate drought, though mortality rates were generally low across all drought and re combinations. This result indicated that topographic position (i.e. wet gullies) did little to moderate juvenile mortality when exposed to severe drought plus re. In wet forest, severe drought also reduced recruitment and replacement of dead juveniles by post-re seedlings compared to moderate drought. In dry forest net-negative replacement increased with the severity of drought. Across both forest types, the total pool of juveniles was reduced under severe drought. Future increases in the frequency of coupled severe drought and re will likely increase the susceptibility of resilient temperate forests to major changes in structure and function.


Introduction
The structure and function of forests are dependent on factors affecting tree demography (Bowman et  Population persistence through re is dependent on the demographic balance between mortality and recruitment. Recruitmentof seedlings and recruitment of juvenile trees to the mature stage, must be su cient to compensate for overall re-relatedmortalityif populations are to be maintained. The composition of resilience traits (e.g. vegetative resprouting, recruitment) and resistance traits (e.g. thick bark, tall canopies, deep rooting) ( Ridgetop environments are generally dry with low nutrient availability, while gully environments retain higher levels of moisture and soil nutrients (McColl 1969). Topographic gradients in moisture availability typically drive local scale heterogeneity in re regimes, with gullies usually experiencing patchier and less severe res than ridgetops Collins et al. 2019a). Gullies therefore may buffer vegetation from the effects of drought and re by providing refugia within topographically complex landscapes.
The temperate forests of southeastern Australia occur across climatically and topographically diverse landscapes that are periodically subjected to drought and re Abram et al. 2021). These forests are dominated by trees from the genera Angophora, Corymbia and Eucalyptus, which are collectively referred to as 'eucalypts'. Eucalypt species are resilient to re, with most species possessing canopy-held seed stores and the capacity to resprout epicormically following canopy defoliating res (Nicolle 2006;Burrows 2013 Speci cally, this study focused on whether the combined effect of severe drought and frequent re is likely to lead to a bottleneck in juvenile recruitment. We asked whether: (i) juvenile survival and recruitment was lowest in areas exposed to severe drought and frequent re; (ii) total juvenile abundance was lowest in areas exposed to severe drought and frequent re; (iii) severe drought and frequent re have synergistic effects on juvenile survival and recruitment. We also examined whether topographic heterogeneity is driving spatial variation in the effects of drought and re across these forests.

Study area
The Sydney Basin bioregion covers approximately 45,000 km²along the eastern seaboard of southeastern Australia (Figure 1). Soils are mainly of low fertility, derived from sandstone and shale parent material (DPI 2017). Elevation ranges from sea level to over 1200 m. Mean annual temperature and rainfall ranges between 11°C-18°C and 600 mm to 1500 mm, respectively, as a function of both altitude and distance from the coast (e.

Fire history
The study focused on areas of the Sydney basin that were most recently burnt by large res in October 2013 ( Figure 1), to control for the potentially confounding effects of time since re. The res occurred in four different sub-regions across the Sydney Basin, with two sub-regions experiencing mild/moderate drought (MD) and two experiencing severe drought (SD; Fig. 1 . We partitioned sub-regions in our study into either mild/moderate drought (MD; SPEI = 0 to -1.4) or severe drought (SD; SPEI = < -1.4). This threshold was chosen as it divided the study area into two approximately equal-sized and climatically coherent regions, each contain substantial DSF and WSF populations. For example values below -1.4 were restricted to typically drier, warmer areas at lower elevation in the north-west of the study region while values above -1.4 occurred along the coastal fringe and in cooler areas with higher elevation (Fig. 1).
In the six months preceding the 2013/14 re season, drought severity varied considerably within the study region, with res in the northern sub-regions burning under severe drought and res in the southern sub-regions burning under mild/moderate drought (Fig. 1).Most areas returned to low drought/normal conditions in the six months following October 2013. For each sub-region, SPEI was calculated using spatially gridded climate data at 0.05° x 0.05° resolution for the 6-month period prior to and after the to avoid the confounding effects of post-re drought on juvenile mortality and recruitment. Thus, there was substantial variability in pre-re drought severity and minimal variation in post-re drought conditions across the study regions. Climatic data used to calculate SPEI was obtained from the SILO database (SILO 2019). SPEI was calculated using the 'SPEI' package in R (Vicente-Serrano et al. 2010).

Study design
The study design incorporated drought severity (MD; SD), re frequency (LF; HF) and vegetation type (DSF; WSF) in a fully factorial manner, with 14 replicate sites per treatment combination (n = 112). The 112 sites were evenly distributed across the four sub-regions (28 sites per sub-region) to obtain su cient spatial variability in drought severity (Fig. 1). Sub-regions occupied narrow bounds of mean annual temperature and rainfall (±2°C and 200 mm across sites within each sub-region) to control for climatic variability. All DSF sites were last burnt at moderate-high severity, with a high amount of scorching and . DSF plots were con ned to the top of ridges along contours, whereas WSF plots were con ned to gully bottoms or lower slopes, adjacent to creeks along contours (see Online Resource 1 for examples of typical sites). Plot aspect varied between sites to minimize aspect bias. Plots were selected randomly within a few kilometers of access roads and within the treatment levels identi ed in a GIS. Plots were placed at least 50 m from roads and trails to avoid edge effects and at least 300-500 m apart to reduce the effect of spatial autocorrelation. Plots were surveyed between February 2018 and July 2018.

Field methods
All juvenile trees between 2.5 and 10 cm diameter at breast height over bark (DBH) were identi ed and individually measured within the 50 m x 5 m plot. Species were identi ed using the keys provided by Klaphake (2012) and Brooker and Kleinig (1999). Juvenile stems that arose from dead stems >10 cm DBH were included, while juvenile stems that arose from live stems >10 cm DBH were not included, i.e. when trees were multi-stemmed, the largest living stem was used to determine that maximum DBH. When stems were closely-spaced, a 1 m long steel rod (4 mm diameter) was used to probe between stems to determine whether they were connected by a sub-surface lignotuber. To determine whether a juvenile was a new post-re seedling or a surviving resprout (Fig. 2), the base of the stem was excavated of soil and manually checked for lignotuber presence. The DBH of each juvenile stem was measured over bark at 1.3 m above the ground on the uphill side of the tree.
Mortality was de ned as a dead standing stem or downed stem/associated stump representing an individual that had died due to the most recent re (Fig. 2). Stumps and downed stems were only included if they were determined to be a product of the most recent re based on criteria described by Gordon et al. (2018) and Roxburgh et al. (2006); and had most likely been felled via re scar formation and collapse, evidenced by a re scar/break point. Mortality of juveniles smaller than 2.5 cm DBH was unable to be determined, as charred stems in this size-class looked similar to other non-eucalypt plant genera.

Data analysis
We tted Bayesian regression models to analyse the in uence of re frequency and drought severity on each of the following response variables: the probability of juvenile mortality; the number of post-re seedlings; the post-re replacement balance (number of seedlings minus the number of dead juveniles); and the total post-re juvenile abundance (number seedlings plus the number of surviving resprouts). For all models, the single predictor was a four-level categorical variable giving the combination of re frequency (low versus high) and drought severity (mild/moderate versus severe).
Juvenile mortality was modelled as a Bernoulli process via a logit-link function. A weighting term was included to account for different plot sizes between standing stems and downed stems. The number of post-re seedlings was modelled as following a negative binomial distribution parameterized in terms of mean and dispersion. A hierarchical model was tted in which, for each combination of drought and re classes, the priors for distribution parameters were informed by overall priors. We chose this model structure to ensure more reliable inferences given the relatively small number of sites within each combination of re and drought classes, and the occurrence of several large outlier values in the data.
Since the tted negative binomial distributions could be strongly right-tailed, we monitored posterior median values rather than posterior means. The model for post-re replacement balance followed a similar hierarchical structure as that for the number of post-re seedlings. However, since the data included negative values, it was treated as continuous and modelled using a location-scale t-distribution, with the mean and standard deviation parameters speci c to each drought and re combination, and a global shape parameter learned by the model to reduce the in uence presence of several large outliers in the data. While this method monitored posterior means rather than posterior medians, it shared the same intent as in the other models, i.e. to obtain an estimation of the central tendency/most likely values. For each model, we sampled four Markov chains, each consisting of at least 5000 model iterations. We assessed model convergence using the diagnostic of Gelman and Rubin (1992) and checked for acceptable levels of serial autocorrelation. Separate Markov Chains for each model were then combined into a matrix of samples from the joint posterior distribution of model parameters, which we subsequently used to derive predictions of probabilities/tree count per site among the treatments (Kruschke 2015; Suzuki 2019). We then calculated the difference between selected comparisons by arithmetically generating a distribution of differences that could be used to inform interpretation of the magnitude of differences among treatment combinations. Hence, these calculations are referred to in the results as 'median posterior difference', i.e. the median value of summarised difference calculations. Credible intervals were calculated as highest posterior density intervals (HPDI), in order to display the central 50% of model predictions and lower/upper 95% bounds of model predictions.
Data for all models, with the exception of the juvenile mortality model, were aggregated by site (DSF, n = 56; WSF, n = 56). We modelled DSF and WSF independently due to confounding by re severity. The data and R scripts used to generate the results are provided online in a data repository (https://github.com/erb418/EB.Ch3.scripts) and secondary results summaries can be found in Online Resource 2.

Juvenile mortality
In dry sclerophyll forest, mortality was most likely under severe drought and low re frequency, followed by severe drought and high re frequency (Fig. 3a). Mortality was less likely under mild/moderate drought and was similar across both re frequency classes (Fig. 3a). When re frequency was low, severe drought increased the likelihood of mortality by 11.6% compared to mild/moderate drought, whereas when re frequency was high, the corresponding increase was 3.2%.
In wet sclerophyll forest, mortality was most likely under severe drought and was similar across both re frequency classes (Fig. 3b). Mortality was less likely under mild/moderate drought and was similar across both re frequency classes (Fig. 3b). When re frequency was low, under severe drought the likelihood of mortality was higher by 5.7% compared to mild/moderate drought. When re frequency was high, the corresponding difference in mortality was 6.5% higher (Fig. 3b).

Recruitment and replacement balance
In dry sclerophyll forest, the number of post-re seedlings per site was higher under severe drought and high re frequency than any other drought-re combination. Compared with low re frequency sites, the number of new seedlings per site was higher under high re frequency under severe drought, but lower under mild/moderate drought (Fig. 4a). The number of dead juveniles per site was higher under severe drought than mild/moderate drought (Fig. 4c). There were approximately double the number of dead juveniles per site under severe drought compared to mild/moderate drought (Fig. 4c). The replacement of dead juveniles by post-re seedlings was similar in all drought/ re combination, except under severe drought and low re frequency, where replacement was negative (i.e. a mean net loss; Fig. 4e). When re frequency was low, severe drought resulted in lower replacement by a median of 12 trees per site relative to mild/moderate drought (Fig. 4e). In contrast to sites with low re frequency, under high re frequency, severe drought had little effect on replacement (net gain <1.5 tree per site), but there was much greater variability in replacement per site (Fig. 4e).The probability of decline, estimated as the proportion of posterior median replacement values tted by the model that were less than zero, was substantial under severe drought combined with low re frequency (approx. 92%) but considerably lower under all other drought/ re combinations (29-40%).
In wet sclerophyll forest the number of new seedlings per site was highest under mild/moderate drought and high re frequency and was zero under all other drought/ re combinations (Fig. 4b). While high re frequency had a positive effect on the number of new seedlings per site under mild/moderate drought (Fig. 4b) this effect was lost under severe drought, e.g. severe drought resulted in a lower number of new seedlings compared to mild/moderate drought, by 7 (Fig. 4b). The number of dead juveniles per site was very low across all treatments (e.g. <1 dead juvenile per site; Fig. 4d), with little difference across drought severity or re frequency categories (Fig. 4d). The replacement of dead juveniles by post-re seedlings was highest under mild/moderate drought and high re frequency and effectively zero under all other drought/ re combinations (Fig. 4f). High re frequency had a positive effect on replacement under mild/moderate drought, with higher replacement by 8.5 juveniles per site, although this effect was negligible under severe drought (Fig. 4f). The probability of decline (median predicted replacement <0) was very low under mild/moderate drought and high re frequency (<0.5%). Under all other drought/ re combinations the probability of decline was substantial (49.5-77%), though the net decline was low (e.g. < 12 plants per hectare).

Juvenile abundance
In dry sclerophyll forest, post-re abundance of live juveniles (post re seedlings plus surviving resprouts) per site was highest under mild/moderate drought, being similar in both re frequency classes (Fig. 5a). Abundance of live juveniles per site was slightly lower under severe drought and high re frequency and lowest under mild/moderate drought and low re frequency (Fig. 5a). Relative to moderate drought, severe drought reduced median juvenile abundance by 16 and 79 individuals underhigh re frequency and low re frequency, respectively (Fig. 5a). High re frequency, compared with low re frequency, resulted in higher median juvenile abundance (62 individuals per site) under severe drought but there was no difference under mild/moderate drought (Fig. 5a).
In wet sclerophyll forest, post-re abundance of live juveniles per site was higher under high re frequency in both drought severity classes and similarly low under low re frequency in both drought severity classes (Fig. 5b). While high re frequency had a positive effect on juvenile abundance under both drought treatments (Fig. 5b), severe drought resulted in lower juvenile abundance compared to mild/moderate drought, by 5 juveniles under low re frequency and 11 plants under high re frequency (Fig. 5b).

Discussion
Our ndings suggest that severe drought preceding recent wild res has diminished the pool of juvenile trees across two broadly distributed eucalypt forest communities in southern Australia. The decline in the juvenile pool was driven by increased re-related mortality under severe drought conditions, rather than by a reduction in seedling recruitment. In contrast to expectations, frequent re in the preceding decades leading up to severe drought and re in 2013 did not produce negative, synergistic effects on juvenile mortality, replacement or total post-re abundance. On the contrary, high re frequency may have offset the effect of severe drought in 2013, bolstering the number of juveniles, as re ected in the higher post-re juvenile abundance compared to sites with low re frequency. Increased juvenile abundance in this context, however, likely corresponds with elevated mortality in mature trees ( It is important to note that juvenile mortality was probably underestimated in our study due to di culties in reliably counting dead stems <2.5 cm DBH, which are often consumed by re or are indistinguishable from other dead plant genera. Thus, replacement of dead juveniles by post-re seedlings is likely to have been net-negative rather than close to zero in many cases. Both forest types in our study may therefore experience declines in tree recruitment, given that Contrary to our predictions, the probability of juvenile mortality was similar between dry sclerophyll species and wet sclerophyll species, suggesting that topographic heterogeneity in ridge-gully systems may not moderate the effects of drought and re on mortality of juvenile trees. The drought preceding the 2013/14 re season dried litter fuels su ciently to facilitate the encroachment of re into the gullies (see Collins et al. 2019a), likely with su cient intensity to cause widespread topkill of juveniles (Lawes et al. 2011). Also contrary to our predictions, recruitment of post-re seedlings in dry sclerophyll forest was promoted by severe drought and high re frequency, albeit with increased variability, when compared to mild/moderate drought (Fig. 4a). One explanation for this may be that environmental constraints, such as drought, can increase owering synchronicity in some tree species and thus pollination e ciency (Bogdziewicz et al. 2017). Note, however, that subsequent seed production may be reduced by drought (Bogdziewicz et al. 2017). It might be possible that drought-adapted eucalypts increase owering synchronicity during drought and manage to produce and retain seed, though research on this topic is lacking (Butt et al. 2015). Another possible contributor might be relatively high shrub mortality during severe drought (Pratt et al. 2014) and with frequent res (Bradstock & Myerscough 1988;Bradstock & Bedward 1996), reducing competition with post-re eucalypt seedlings. If drought-adapted trees such as DSF species are able to increase owering synchronicity due to drought, and maintain relatively high seed production, then they may be able take advantage of increased resources created via elevated shrub mortality or impoverished shrub reproduction.
Our results indicated that severe drought may increase the potential for juvenile mortality during wild re in temperate forests ( and juvenile mortality as high as 40% following multiple res (Collins 2020). Our estimates of mortality are more conservative than the aforementioned studies but nevertheless suggest that juvenile trees inhabiting drier ridgetop environments are likely to experience mortality rates as high as 15% under severe drought (Fig. 3a), 11-12% greater than under mild/moderate drought. Similarly, juvenile trees inhabiting moist gully environments are likely to experience mortality rates as high as 10% under severe drought ( Fig. 3b), compared with 3-4 % under mild/moderate drought.
In our study, recruitment of post-re seedlings in dry sclerophyll forest was highest under severe drought and high re frequency (Fig. 4a). It could be possible that increased juvenile mortality (see Fig. 3) promoted the establishment of new seedlings via mechanisms such as increased resource availability and release from competition (Vivian et al. 2008). However, if this were the case, we would expect similar or higher levels of recruitment under severe drought and low re frequency, principally because juvenile mortality was highest in that category for our study (Fig. 3a, 4a). One possibility for this anomaly is that forests have high resistance to low severity re (Collins et al. 2019b), but must resprout to survive high severity re (Collins 2019). Consequently, rates of stem mortality tend to be greater following high severity res (Denham et al. 2016). Our study did not consider the severity of res when quantifying re frequency, so it is unclear whether sites were subjected to multiple high severity re events. Contrasting both low and high re severity across re frequency classes in ridgetops and gullies could shed further light on the role of re severity in moderating the ux of mortality and recruitment.
Wet sclerophyll forest contrasted with dry sclerophyll forest by having low numbers of post-re seedlings overall (Fig. 4b), while numbers of surviving resprouts were also much lower (see Online Resource 2). Further, total post-re juvenile abundance was clearly reduced by severe drought in both re frequency classes (Fig. 5b). This suggests that recruitment of these relatively more sensitive species may be inherently low and that severe drought has the capacity to kill off a proportion of persisting juveniles that may have survived given re alone. Such reductions in recruitment under severe drought may be driven by loss of seed production and germination failure (Suarez & Kitzberger 2008;Clark et al. 2016). As a consequence, gullies in drought-affected regions that are burnt may not effectively recruit new trees. However, mass recruitment may only rarely be required to sustain populations in gully environments, given the prevalence of low severity res ) and re resistance of many resprouting eucalypts (Burrows 2013). For example, survival of mature trees in gullies at our study sites was very high and >75% either resprouted from the canopy branches or had canopies that were unaffected by re

Potential ecosystem changes
It is predicted that climate-change and extreme disturbance regimes will drive ecosystemconversion Fairman, Nitschke & Bennett 2016). Increased mortality, along with reduced regeneration and recruitment, could ultimately lead to major changes in forest composition in the long term (Fairman et al. 2016). Our data indicate that coupled severe drought and re have the potential to reduce the overall abundance of post-re seedlings and persistent, surviving juveniles within the extensive eucalypt forests of eastern Australia. Given the relatively low mortality rates in our study (<15%), decades of continued severe disturbance would probably be required to facilitate major demographic changes in these resilient forests, as has been suggested elsewhere (see Collins 2020).
However, it is important to interpret our ndings in the context of recent trends of increasing drought and associated mega-res (

Declarations
Funding This project was completed as part of the rst author's PhD candidature at the University of Wollongong.
There were no external grants or funding associated with this project.

Con icts of interest/Competing interests
The authors declare that they have no con ict of interest, nancial or otherwise, that could have in uenced this paper.

Availability of data and material
All data are provided online in a data repository (https://github.com/erb418/EB.Ch2.scripts).

Code availability
All R scripts used to manage data, analyse data and generate gures are provided online in a data repository   Diagram showing trees in various size-classes and potential effects of re on mortality, recruitment and replacement among size-classes.

Figure 3
The effect of drought severity and re frequency on the probability of mortality for juveniles (2.5-10 cm DBH) in dry sclerophyll forest (DSF; panel a) and wet sclerophyll forest (WSF; panel b) of the Sydney Basin. X-axis indicates drought severity / re frequency combination (MD = mild/moderate drought; SD = severe drought; LF = low re frequency; HF = high re frequency); colours correspond to treatment combinations; boxes and whiskers represent credible intervals for model predictions, where boxes represent the central 50% of posterior samples and whiskers represent upper and lower 95% bounds.

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