Rapid viable seedbank fosters resilience via pyrosilviculture in serotinous bishop pine

doi:10.21203/rs.3.rs-2066531/v1

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Research Article

Rapid viable seedbank fosters resilience via pyrosilviculture in serotinous bishop pine

https://doi.org/10.21203/rs.3.rs-2066531/v1

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published 29 May, 2023

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Background

In ecosystems where fire has been excluded, pyrosilviculture can restore fire regimes while mitigating risk where fire is inevitable. Pyrosilviculture in crown fire-adapted forests is, however, limited by insight into the temporal window of fire return matching canopy seedbank development. Here, we characterized demographic responses to fire and non-native pine pitch canker infection in a chronosequence of serotinous bishop pine stands burned at high-severity to quantify: (1) temporal patterns of seedbank development given seed viability and density, cone production, and tree density, and (2) pine pitch canker incidence across tree ages and sizes to assess how infection might influence pyrosilviculture. Stands were burned to promote resilience while mitigating WUI wildfire, and we use to our findings to elucidate pyrosilvicuture as a means of meeting these objectives in crown-fire adapted forests.

Results

Bishop pine produces an abundant, viable seedbank within six years, with high production and viability persisting across developmental stages and age classes. Seed abundance and viability are exceptionally high at even the earliest age (median > 600,000 seeds ha^− 1 & 97% viability at 6 years) and remain high, with the oldest stands (36 years) maintaining median densities of > 500,000 seeds ha^− 1 and viability of 95%. We additionally learned that pine pitch canker infection is most severe during the sapling stage (8–10 years post-fire), potentially shifting the timing and development of fuel structure to earlier successional stages as well as limiting recruitment into the canopy.

Conclusions

In bishop pine and equally-fecund serotinous species, burning at short fire return intervals is feasible given early development of a robust, viable seedbank, addressing two common management challenges in fire-adapted forests - restoring fire to promote resilience while mitigating wildfire risk to the WUI. Moreover, frequent fire in pine pitch canker infected stands may also provide disease mitigation. Although the long-term effects of pine pitch canker infection remain unknown, bishop pines’ viable and persistent seedbank suggests that managers can ignite prescribed fire across a broad return interval – as short as six to eight years and as long as several decades – to promote ongoing bishop pine resilience, mitigate disease infection rates, and reduce wildfire risk in WUI-adjacent ecosystems.

Aerial seedbank

Pinus muricata

fire management

Fusarium circinatum

pine pitch canker

prescribed fire

silviculture

forest management

serotiny

Species adaptations determine ecosystem responses to fire (Pausas et al. 2017), and species possessing traits adapted to a particular fire regime may be threatened when that regime changes in ways that make adaptations no longer advantageous (Keeley et al. 2011, Bowman et al. 2014, Pausas 2015). Shifting fire regimes involving substantial changes in fire frequency and severity are increasingly common in fire-adapted ecosystems worldwide due to anthropogenically-driven climate change (Flannigan et al. 2009, Moritz et al. 2012), legacies of forest management and fire suppression (Stephens et al. 2014, Parks et al. 2015), exclusion of Indigenous burning practices (Kimmerer and Lake 2001, Cermak 2005), introductions of non-native disturbance agents (Metz et al. 2013), and increasing anthropogenic ignitions (Fusco et al. 2016, Keeley and Syphard 2018). Regime shifts are consequential for persistence of fire-adapted species, as uncharacteristic frequency or severity may lead to the decline of seed available for post-fire regeneration or overwhelm survival and resilience mechanisms (Donato et al. 2009, Buma et al. 2013, Shive et al. 2018). Fire-adapted forests of the western US are particularly vulnerable to such mismatches between fire adaptations and contemporary fire regimes due to a massive fire deficit (Stephens et al. 2007, Marlon et al. 2012). In fire-adapted forests, fire return is both inevitable and increasingly uncharacteristic (Hagmann et al. 2021, North et al. 2021).

There have thus been growing calls for (North et al. 2015, 2021, Kolden 2019, Stephens et al. 2020) and legislation directing (e.g., US Congressional National Prescribed Fire Act, California Senate Bill 332, California Executive Order B-52-18) the expanded use of managed and prescribed fire for reducing fuel loads and restoring fire-adapted forests of the West. California takes center stage in the deliberation over prescribed fire use, where, after more than a century of fire exclusion and suppression, ~ 8 million hectares of forest are in a fire deficit (Miller et al. 2020) and the landscape is predisposed to unprecedented wildfire seasons (Safford et al. 2022, https://www.fire.ca.gov/stats-events/). California’s wildland urban interface (WUI) expanded rapidly over this same period, with one-third of all homes now located within the WUI and the majority of US homes lost to fire between 2000–2013 residing in California (Kramer et al. 2018, 2019). Moreover, population growth in California is anticipated to be greatest on lands characterized by high-severity fire regimes (Mann et al. 2014), further exacerbating risks to human and wildland communities (Syphard et al. 2007). State officials are working to reduce barriers and risk-related constraints to prescribed fire use in order to mitigate these detrimental effects, as returning fire to California’s fire-adapted ecosystems is the most direct and effective method of restoring altered fire regimes (Sugihara et al. 2006). Proactive management will be essential to reducing socio-ecological impacts where fire is inevitable (Moreira et al. 2020), but there remains a parallel need to develop ecosystem-specific burn plans that mimic the frequency, severity, and seasonality of the regime to which local species are adapted (Stephens et al. 2020).

Pyrosilviculture purposefully adopts prescribed or managed fire into prescriptions as a tool for harmonizing management with the adaptations and disturbance history of local species (North et al. 2021, York et al. 2021). Purposefully burning implies a paradigm shift in forest management, however California’s Indigenous peoples were the initial pyrosilviculturists (Codding and Bird 2013, Cuthrell 2013); frequent cultural burning had profound ecological effects, including generating fire-adapted ecosystems and mitigating fire severity through repeated fuel reduction (Blackburn and Anderson 1993, Lightfoot and Cuthrell 2015). Though limited in application over the last century, pyrosilvicultural approaches have been recently (and successfully) re-employed as a management alternative for restoring fire and reducing fuel loads in California’s seasonally-dry forests and oak woodlands adapted to low- or mixed-severity fire (Hankins 2015, North et al. 2021, York et al. 2021). Ongoing application will be critical to addressing the State’s fire deficit, however prescribed fire use in California remains nominal due to operational and societal barriers to implementation (Quinn-Davidson and Varner 2012, Miller et al. 2020, York et al. 2021). These constraints are acutely challenging in forests adapted to high-severity crown fires in proximity to the WUI, a socio-ecological interface common and ever-expanding across California (Barbour 2007, Mann et al. 2014). Despite the evident challenges, the need to restore fire or provide a functional alternative is nonetheless critical in crown fire-adapted systems where fire exerts strong selective pressure on demographic processes, including the degree of serotiny (i.e., long-term canopy seedbank released by heat) and the temporal window of seed viability for fire-obligate seeders (Crawford et al. 2011, Hernández-Serrano et al. 2013, Pausas and Keeley 2014). Long-term sustainability of crown fire-adapted forests will depend upon restoring the frequency of high-severity fire to which these ecosystems are adapted, however pyrosilviculture is limited by ecological knowledge gaps on the temporal pattern of canopy seedbank development as well as the acceptable prescribed fire return window for this understudied forest type.

Here, we address these critical knowledge gaps using managed stands of crown fire-adapted bishop pine (Pinus muricata D. Don) on the Central Coast of California as a model system. Bishop pine is an endemic conifer growing in ten disjunct populations from northern California to Baja California, Mexico (Millar and Critchfield 1988, Stephens and Libby 2006). Historic fire return is estimated to have been as frequent as ~ 6 years to as long as ~ 70 (Sugnet 1985, Finney and Martin 1989). Given the low density of lightning strikes on the Central Coast (2–3 strikes/100km²/year, Cuthrell 2013), fire was historically ignition-limited, and frequent fire would have been a product of regular Indigenous burning to meet cultural resource objectives (Keeley 2002, Cuthrell et al. 2012, Lightfoot et al. 2013). Regardless of ignition source (lightning vs. anthropogenic), fires in bishop pine typically burn as high-severity crown fires (Keeley and Zedler 1998), and stands exhibit rapid, high-density regeneration from a serotinous canopy seedbank (Linhart et al. 1965, Vogl et al. 1977, Harvey et al. 2011). Managers have thus proposed returning fire to bishop pine stands to promote ongoing resilience of this fire-adapted species while simultaneously reducing fuel loads and thus wildfire risk to the adjacent WUI (see plans & decisions by: California State Parks, National Park Service, & PG&E). A distinct complication in management is the prevalence of the non-native pathogen pine pitch canker (Fusarium circinatum Nirenberg & O’Donnell) (McCain et al. 1987), which may limit fire resiliency if trees die prior to reproductive maturity and fail to contribute to the seedbank (Aegerter and Gordon 2006). On the other hand, fire is documented to reduce non-native disease infection and mortality in other coastal, fire-adapted forests (e.g., sudden oak death, Simler-Williamson et al. 2021), and fire return may instead be an effective means of controlling pine pitch canker. Ideally, prescribed fires will be high enough in severity to initiate stand-replacing cohorts with reduced pine pitch canker incidence while low enough in intensity to avoid containment risks. Yet, well-defined targets for prescribed fire return as well as the long-term implications of a pyrosilvicultural approach remain unknown for this crown fire-adapted system.

To better understand post-fire resilience and support the development of pyrosilviculture for bishop pine and other crown fire-adapted forests, we characterized demographic responses to fire and pine pitch canker in bishop pine stands burned at high-severity across a chronosequence of wild- and prescribed fires ranging from six to 36 years. Prescribed fires were used to return fire to this landscape to meet two objectives – 1) promote bishop pine regeneration following decades of fire exclusion and 2) reduce fuel loads in this WUI-adjacent landscape. We leverage this chronosequence of fires to fill the knowledge gap on acceptable fire return in this forest type by quantifying: (1) the temporal pattern of canopy seedbank development given seed viability and density, cone production, and tree density in post-fire stands and (2) the incidence of pine pitch canker infection across stand ages and tree size classes to assess how infection might influence prescribed fire programs. We hypothesized that: (1) trees would become reproductively mature at a young age; (2) seed density would increase with time since fire, as trees slowly accumulated cones with more, higher viability seeds; and (3) the degree of pine pitch canker infection would be greatest in relatively small trees, consistent with findings from related species. Although previous studies of serotinous species have estimated canopy seedbank development as a function of cone production and stand density (Keeley et al. 1999, Turner et al. 2007, Fry and Stephens 2013, Agne et al. 2022), this is the first to additionally quantify both seed viability and density over a range of stand ages to enumerate a more accurate assessment of reproductive capacity and the temporal window of fire return promoting forest resilience. We use the results to discuss options for developing pyrosilvicuture as a component of management in fire-obligate, crown-fire adapted forest types, such as serotinous bishop pine.

2.1 Study Area

This study was conducted in the bishop pine forest surrounding the Diablo Canyon Nuclear Power Plant, a privately-owned 5090-ha property managed by Pacific Gas & Electric (PG&E) on the Central Coast of California in San Luis Obispo County. The Diablo property lies immediately adjacent to the town of Avila Beach, a community deemed high or very high hazard due to its proximity to crown fire-adapted wildlands and its “one-way-in, one-way-out” road system that may impede evacuation during a wildfire (Avila Community Plan 2021). Climate is characterized as Mediterranean with mild temperatures, wet winters, and dry summers. Here, as across the species’ range, growing season precipitation comes largely via fog drip from regular fog cover (Baguskas et al. 2016, Fischer et al. 2016), which supplements soil moisture, moderates air temperature, and reduces transpiration (Carbone et al. 2013). The vegetation on the Diablo Canyon property consists of a mosaic of bishop pine stands, coastal sage scrub (e.g., Artemisia, Salvia, Diplacus, Eriogonum, Rhamnus, Baccharis, and Hazardia spp.), mixed chaparral (e.g., Adenostoma, Arctostaphylos, Chrysolepis, Baccharis, Artemisia, and Salvia spp.), and coast live oak (Quercus agrifolia). PG&E directs a land stewardship program on the Diablo Canyon property that aims to manage and protect natural and cultural resources. After a wildfire in 2007, PG&E began to actively manage bishop pine forests using high-severity prescribed fires ignited in 2009, 2010, and 2012. All prescribed fires were ignited in stands estimated to be 60–80 years old and during dry windows of the Central Coast rainy season (December through March) to re-introduce fire prior to the dry season when escapement risk increases. The objectives of this pyrosilvicultural program are to: 1) promote resilience by regenerating bishop pine and 2) burn at the appropriate fire return interval so that, in the long-term, bishop pine stand management will reduce fuel loads and mitigate the risk of catastrophic wildfire to the power plant and adjacent WUI (Pacific Gas & Electric Company 2007). (Fig. 1).

2.2 Field Sampling

Data were collected on 50 permanent plots located within the boundaries of five fire perimeters (Fig. 2), including two wildfires that occurred in 1982 and 2007 and three prescribed burns that occurred in 2009, 2010, and 2012 (Table 1). All fires burned at high severity, with > 90% mortality within each fire perimeter. For the 1982, 2010, and 2012 burns, plots within each fire perimeter were randomly selected in ArcGIS using the Sampling Design Tool (Buja and Menza 2013), with a 100-m minimum distance between plots. The 2007 and 2009 burns had less continuous bishop pine cover and steeper slopes, and, here, plots were selected in the field to represent the range of aspects and stand structure within each fire perimeter. Because the objective of the project was to assess bishop pine stand dynamics following fire, plots were only sampled if they contained post-fire bishop pine individuals, and plots were moved by up to 50 m if they did not meet this criterion. The patchy distribution of bishop pine across the study area thus resulted in plot locations that were clustered within fire perimeters, but nearly all plots remained more than 80 m apart, consistent with spacing between uncorrelated plots in a previous study in this forest type (Harvey and Holzman 2014).

Table 1

Fire type, sample size, and stand characteristics for each wild and prescribed fire burned in bishop pine stands on the PG&E Diablo Canyon Power Plant property as of the 2018 sampling year.
Fire Year	Years Since Fire^a	Fire Type	No. Plots	Tree Density (ha^− 1)	Seed Density (ha^− 1)	Cones per Tree	Seeds per Cone	Seeds Viable (%)^b	Pine Pitch Canker Infection (% of trees in plot)
				Median (min-max)
1982	36	Wildfire	15	402 (30–1547)	10^5.7 (10^4.8–10^6.1)	20 (0–200)	60 (0–112)^c	95 (86–98)^c	10 (0–30)
2007	11	Wildfire	6	2653 (707–3537)	10^6.4 (10^5.4–10^6.8)	9 (0–275)	62 (3–141)	97 (64–99)	48 (10–100)
2009	9	High-severity prescribed fire	4	5128 (354–14501)	10^5.8 (0–10^6.5)	0 (0–25)	49 (4–115)	94 (93–97)	100 (50–100)
2010	8	High-severity prescribed fire	12	10257 (1415–63308)	10^6.6 (10^5.2–10^7.2)	0 (0–303)	63 (0–146)	98 (77–100)	38 (4–100)
2012	6	High-severity prescribed fire	13	9196 (1840–102920)	10^5.8 (0–10^6.5)	0 (0–41)	48 (0–154)	97 (90–100)	22 (0–81)
^a Time since fire at the time of sampling in 2018.
^b Seed viability was quantified using pooled seed lots for each sampling plot, and does not include plots in which no cones were found (five plots in 2012 fire and one plot in 2009 fire).
^c In the 1982 fire, seeds per cone and seed viability were quantified from cones collected in three locations outside of permanent plots.

Nested, circular, fixed-radius permanent plots were established at each sampling location, and all plots were sampled in 2018. At each plot center, rebar was installed for future remeasurements, and data were collected on slope, aspect, and elevation. We measured the densities of large (diameter at breast height [DBH] greater than 20.0 cm) and small trees (12.5–20.0 cm DBH) in a 0.1-ha plot (17.8 m radius). We measured the densities of saplings (> 1.37 m in height, 2.5–12.5 cm DBH) and seedlings (< 2.5 cm DBH) in a nested subplot. Nested subplot size varied as a function of post-fire density of tree seedlings, with sampling defaulting to 0.02 ha (8 m radius) but reduced to 0.007 ha (5 m radius) or 0.002 ha (3 m radius) when seedling densities exceeded 200 trees in the default subplot size.

Each sampled tree was evaluated for the presence of pine pitch canker infection, which results in resinous cankers and may be visible on branches, shoots, or boles (Storer et al. 1995). Trees considered symptomatic were those with evidence of: tree crown dieback from the leader, branch end dieback, resin-coated boles, and/or stem cankers (Gordon et al. 2001). The most common, and obvious, sign of infection is leader and branch dieback, usually within one or two whorls of the infection point, in which a girdling lesion kills an affected branch tip while causing little or no visible damage elsewhere on the tree (Gordon et al. 2001). These symptoms are consistent with infection in local populations of Monterey pine (Pinus radiata D. Don), a close relative of bishop pine and the most well-documented regional host of the pathogen in which infection has been verified via genetic analyses (Bisbing, unpublished data).

We additionally quantified and sampled female cones to assess bishop pine seed availability. Across all recent fire years (2007, 2009, 2010, and 2012 burns), total cone abundance was documented for each individual tree, and three cones were collected for viability analysis from each of the ten bishop pine individuals closest to plot center (n_cones = 30 per plot). For the plots within the 1982 wildfire, for which cone abundance per tree was high, we counted cones on the ten closest bishop pine to plot center, with a maximum cone count of 200 (only three out of 110 sampled trees had 200 or more cones). Cones were collected from three locations outside the permanent plot boundaries for the 1982 burn, where the location of cones high in the tree canopy required trees to be felled in order to access intact cones.

2.3 Canopy Seedbank Estimates

In the lab, cones were heated at 70 °C for 24–72 hours until open. All seeds were manually removed from the opened cones, and seeds that appeared potentially viable (i.e., not cracked or shriveled) were counted for each collected cone and retained for seed viability testing. A random sample of seeds from each sampling plot, distributed proportionally across collected cones, was used to measure potential viability. The size of the seed lots varied based on total seed abundance for each plot, ranging from 120 to a target lot size of 400 seeds. Seed lots were pooled for each plot and sent to the Idaho State Department of Agriculture Seed Lab for tetrazolium staining, resulting in an estimated proportion of viable seeds at the plot level. Seed density was estimated for each plot based on established protocols (Tapias et al. 2001, Goubitz et al. 2004) by multiplying plot-level measurements of live tree density, mean cones per tree, mean seeds per cone, and proportion of viable seeds. Because cones from the 1982 fire were collected in three locations outside of permanent plots, the mean of the three seed viability values was used for calculations of stand-level seed density for all 1982 plots.

2.4 Statistical Analyses

All statistical analyses were conducted in R (R Core Team 2018). We used AIC_c for model selection (Anderson et al. 2000), comparing among a full model and nested sub-models using the ‘dredge’ function in the R package ‘MuMIn’ (Barton 2015). Candidate predictor variables for each model are described below. For linear models with fixed effects only, we calculated adjusted R² for the highest-ranking model using the ‘rsq’ package (Zhang 2018). Mixed effects models were run using R package ‘lme4’ (Bates et al. 2015), and marginal and conditional R² values were calculated using the r.squaredGLMM function in the ‘MuMIn’ package (Barton 2015).

2.4.1 Canopy seedbank development

To characterize bishop pine seedbank development as a function of time since fire (TSF) and topographic variability, we developed linear models predicting multiple characteristics that determine seed availability: stand-level seed density, seed viability, seeds per cone, cones per tree, and tree density. We modeled seed density at the plot level (n = 50), using a linear model to predict total seed density (log₁₀-transformed; Gaussian distribution) as a function of the following candidate predictor variables: TSF (factor), topographic wetness index (TWI; see Supplementary Materials S1), and TSF*TWI. We then modeled plot-level seed viability (Gaussian distribution) as a function of TSF (factor), excluding six plots in which no cones were present (n = 32). Because cones from the 1982 fire were collected from locations outside the permanent plots, we could not link seed viability data to site-specific measurements of TWI, so the seed viability model did not include these predictors.

Seeds per cone were analyzed at the scale of individual cones (Gaussian distribution; n = 443) and modeled as a function of tree size class with a nested random intercept terms for maternal tree, plot, and fire year to account for spatial clustering among the collected cones. Similar to the seed viability model, we could not include other site-specific measurements as predictors due to the cone collection strategy in the 1982 fire. We used a generalized linear mixed effects model to predict cones per tree (Poisson distribution; n = 3225) as a function of the following candidate predictor variables: tree size class, TWI, and bishop pine tree density. Plot nested within fire year was included as a random intercept to account for spatial clustering of observations. The model of tree density is described in Supplementary Materials S2.

2.4.2 Pine pitch canker infection

To characterize pine pitch canker infection as a function of TSF and topographic variability, we used a generalized linear model (binomial distribution) predicting the proportion of trees infected in each plot (n = 50) as a function of the same candidate predictor variables described above for the model of tree density: TSF (factor), TWI, and TSF*TWI. To characterize the probability of individual tree infection by pitch canker, we used a generalized linear mixed effects model (binomial distribution) predicting the infection status of individual trees (0/1 representing absence or presence of infection signs; n = 3225) as a function of tree size class, with a random intercept for plot nested within fire year to account for spatial clustering of observations.

3.1 Canopy Seedbank Development in Post-Fire Stands

Tree age structure transitioned from many small trees to fewer large trees with time since fire (Figs. S2 and S3). Seed density was significantly related to time since fire (Fig. 3; F = 4.82; P = 0.003; Adjusted R² = 0.24), and TSF was the only predictor variable retained in the highest-ranking model (Table S3). However, only plots from the most recent fire year (6-yr TSF) had seed densities that were significantly different (based on non-overlapping 95% confidence intervals), with lower seed density than all older stands except for the 9-yr TSF burn plots. Of the six plots (out of 50) that had no observed cones and thus a total seed density of zero, five were in plots from the most recent 6-yr TSF burn, and one was a plot in the 9-yr TSF burn.

The highest-ranking model of seed viability included only an intercept term (Table S3), and viability was very high for all fire years, including after only 6 years post-fire (mean = 95%; Fig. 4a). The best model of seeds per cone included tree size class as a predictor variable (Table S3), and cones from seedlings had significantly fewer seeds than cones from saplings (Table 2; Fig. 4b). However, the fixed effect of tree size only contributed a marginal R² of 0.05, while the addition of the random effects from maternal tree, sampling plot, and fire year resulted in a conditional R² of 0.50. The fact that neither seed viability nor seeds per cone were related to time since fire or tree size beyond the seedling size class (Table 2; Fig. 4a–b) suggests that trees produce cones of a consistent size and quality very quickly during stand development and then maintain a viable cone bank for at least three decades.

Table 2

Model estimates (β) and 95% confidence intervals (CI) from the analysis of cone-level seed production and tree-level cone production. Nested random effects for tree, plot, and fire year were included for the ‘seeds per cone’ model, and nested random effects for plot and fire year were included for the ‘cones per tree’ model. Marginal R² represents the marginal contribution of fixed effects only, whereas the Conditional R² is the contribution of both fixed and random effects. Continuous fixed effects bolded where 95% CI did not overlap 0. TWI was not retained in the best model for either analysis.
	Seeds per cone (cone-level; Gaussian)		Cones per tree (tree-level; Poisson)
Predictor	β	95% CI	β^a	95% CI
Seedling size class^b	46.04	37.95–54.13	0.93	0.61–1.42
Sapling size class^b	62.18	56.40–67.96	5.88	3.85–8.99
Small Tree size class^b	n/a	n/a	11.89	7.68–18.42
Large Tree size class^b	49.79	23.79–75.79	21.34	13.69–33.25
Tree density (log₁₀; ha^− 1)^c	n/a	n/a	0.66	0.54–0.83
TWI	–	–	–	–
Marginal R²	0.05		0.27
Conditional R²	0.50		0.99
^a Exponentiated coefficient estimates (odds ratios).
^b Absolute estimates shown for each size class.
^c Continuous tree density variable has been standardized, and regression coefficient gives the effect of a change of 1 standard deviation.

At the individual tree scale, the cone abundance was related to tree size and tree density (Table 2; P < 0.001; marginal R² = 0.27). Cone counts increased with tree size, and large trees generally had more than ten times as many cones as smaller trees (Fig. 4c). Cone production was negatively related to plot-level tree density (Table 2; β [odds ratio] = 0.66; P < 0.001) after accounting for the effects of tree size. The nested random effect of sampling plots and fire year explained much additional variation in cone production, and the conditional R² was 0.99.

Increasing cone production with tree size corresponded to an increase in plot-mean cone production with time since fire (Fig. 4d), because large trees that tended to have more cones represented a greater proportion of the stand in older fires (Fig. S2). The fact that plot-level total seed density remained relatively consistent with time since fire (Fig. 3), despite these tree-level increases in cone production through time, reflects the strong relationship between plot-level tree density and cones per tree (values log₁₀-transformed; R² = 0.56). With increasing time since fire, bishop pine stands quickly developed and then maintained an abundant seedbank while transitioning from extremely high tree density with few cones per tree towards lower tree density with many cones per tree (Fig. 4d).

3.2 Pine Pitch Canker Infection Rate as a Function of Time Since Fire and Tree Size Class

Plot-level infection by pine pitch canker varied with time since fire, and the highest plot-level infection rates were observed in intermediate-aged stands (Fig. 5a). The highest-ranking model of plot-level pitch canker infection rate (proportion of plot infected; Table S4) included only TSF as a predictor variable (χ² = 9.72; P = 0.045; adjusted R² = 0.33). However, there was broad overlap among model predictions, and the only significant pairwise difference was a lower infection rate in the 36-yr-old stands compared to 9-yr-old stands. At the scale of individual trees, infection probability was highest for trees in the sapling size class (Table 3; Fig. 5b), although there were no significant pairwise comparisons among size classes. Given that trees in the sapling size class represented the greatest proportion of the stand in intermediate-aged stands (Fig. S2), the plot-level and individual-level results are consistent in showing that pine pitch canker infection is greatest for stands that are differentiating in structure, with smaller, less-competitive trees succumbing to pitch pine canker while larger trees recruit into upper canopy positions. However, there was high variability in infection probability among and within plots, shown by wide confidence intervals in model estimates and low proportion of variance explained by tree size class in the individual-tree model (marginal R² = 0.01). The relatively large contribution of the random intercept term in the individual-tree model (conditional R² = 0.50) indicates an important role of plot characteristics that were not represented by the predictor variables included in our models.

Table 3

Model estimates (β) and 95% confidence intervals (CI) from the analysis of tree-level infection by pine pitch canker. Plot nested within fire year was included as a random intercept. Marginal R² represents the marginal contribution of fixed effects only, whereas the conditional R² is the contribution of both fixed and random effects.
	Pitch canker infection (tree-level; binomial)
Predictor	β^a	95% CI
Seedling size class^b	0.26	0.15–0.41
Sapling size class^b	0.41	0.25–0.59
Small Tree size class^b	0.23	0.08–0.51
Large Tree size class^b	0.08	0.01–0.36
Marginal R²	0.01
Conditional R²	0.50
^a Back-transformed coefficient estimates.
^b Absolute estimates shown for each size class.

In fire-adapted ecosystems where fire activity has been reduced or eliminated, pyrosilviculture can be used to purposefully return fire to the landscape to restore altered fire regimes while simultaneously lowering wildfire intensity (and associated risk) via the maintenance of low fuel loads. Knowing the temporal window of fire return that matches canopy seedbank development and viability is, however, critical to matching prescriptions to species’ adaptations, particularly in crown fire-adapted ecosystems dominated by fire-obligate seeders. Here, we leveraged a chronosequence of prescribed and wild high-severity, crown fires in serotinous bishop pine to determine if pyrosilvicultural techniques could be a viable management tool for maintaining low fuel loads in this WUI-adjacent forest type and, if so, the fire return window best matching a canopy seedbank capable of promoting bishop pine persistence. First, we discovered that bishop pine produces an abundant, viable canopy seedbank within six years of high-severity, crown fire, with high production and high viability persisting across developmental stages and age classes from seedlings to mature trees. Second, we learned that pine pitch canker infection is most severe during the sapling stage (8–10 years post-fire), potentially shifting the timing and development of fuel structure to earlier successional stages as well as limiting recruitment into the canopy. Our findings suggest that frequent, low-intensity yet high-severity fire may be a viable option for regenerating this serotinous conifer while concurrently mitigating pine pitch canker infection and maintaining low fuel loads in coastal California’s growing WUI. Returning frequent fire to this landscape would resume the purposeful and frequent ignitions practiced by coastal California Indigenous peoples, restoring ecosystem function and perpetuating species adaptations to fire via a pyrosilvicultural approach. Finally, this study provides the first quantitative assessment of post-fire canopy seedbank viability and development for a crown-fire adapted tree species, and, here, we outline strategies for incorporating these findings into pyrosilvicultural prescriptions for managing crown-fire adapted forests.

4.1 Mapping adaptations to application

This science fills a critical knowledge gap on the appropriate window of prescribed fire application for a crown fire-adapted, serotinous conifer by confirming the timing of reproductive maturity and quantifying the temporal window of seed viability. In serotinous species, resilience is closely tied to the aerial seedbank, and, when fire matches the regime to which local species are adapted, enhances fitness by releasing seed onto an optimal postfire seedbed (Causley et al. 2016). Development of a sufficient aerial seedbank must occur prior to the recurrence of fire (Enright et al. 1996, Tapias et al. 2001), and this resilience mechanism may fail if fire return is too short (i.e., immaturity risk) or too long (i.e., senescence risk) (Zedler 1995, Keeley et al. 1999). The temporal window of prescribed fire ignition should therefore be optimized based on seedbank maturity and viability to closely mimic the fire regime to which serotinous species are adapted and promote ongoing resilience to fire. The Central Coast bishop pine stands assessed here became reproductively mature within six years, a strategy demonstrating low immaturity risk and in line with the onset of reproductive maturity elsewhere in the species’ natural and planted ranges (Fielding 1962, Agne et al. 2022) and in other serotinous species (Enright et al. 1996, Tapias et al. 2001, Turner et al. 2007, Climent et al. 2008). Moreover, viability was exceptionally high in even the earliest age class (median of 97% at 6 years), providing the first verification of this assumption and supporting the notion that bishop pine is well adapted to frequent high-severity fire.

Bishop pine stands do, nonetheless, appear to have a wide-ranging temporal window over which prescribed fire may be applied to promote and maintain forest resilience. We draw this conclusion based on the rapid development and persistence of a viable aerial seedbank, with consistently high, viable seed densities from six to 36 years, the range of stand ages studied here. Notably, this amassing of a substantial canopy seedbank in early successional phases is attributable to high densities of young trees that individually produce few, high viability seeds but collectively produce many (median > 600,000 seeds ha^− 1). Stand-level seed availability remains consistently high as stands shift from high densities with low individual reproductive output to low densities with high individual reproductive output, a pattern common in serotinous pines (Tapias et al. 2001, Agne et al. 2022). Long fire-free periods are generally expected to limit seed availability due to tree mortality and seed loss to decay, predation, and disease (Lamont et al. 1991), however the oldest stands studied here (36 years) maintain high seed density (median > 500,000 seeds ha^− 1) and viability (median 95%) despite time-related reductions in tree densities and cones. Resilient forest conditions can thus likely be maintained under prescribed fire intervals as short as six to eight years, corresponding to the lower end of estimated historic fire return intervals for bishop pine (Finney and Martin 1989), but as long as many decades (Sugnet 1985, Forrestel et al. 2011, Harvey et al. 2011, Agne et al. 2022). Under shorter intervals of prescribed fire, there is a heightened risk that fire will coincide with an immature aerial seedbank, resulting in low post-fire recruitment. Future establishment may also be challenged by cone or regeneration failures associated with ongoing climate change as seed-bearing and establishing trees succumb to moisture stress (Baguskas et al. 2014, Agne et al. 2022). High early stand densities and the persistence of a large, viable seedbank over many decades are, however, likely to moderate this added stressor and allow for ongoing resilience. Generally, the species appears both highly resilient and well adapted to frequent fire return. Regular high-severity fire, whether prescribed or wild, has a high likelihood of promoting bishop pine resilience now and into the future.

Pyrosilviculture is, however, rarely leveraged for regenerating forests adapted to a high-severity crown fire regime (but see Sharpe et al 2017 for Pinus banksiana management) due to risk-related barriers such as fear of liability and negative public perception (Miller et al. 2020). Notably, many crown fire-adapted ecosystems lie adjacent to WUI (Kramer et al. 2018, Radeloff et al. 2018), particularly in California (Syphard et al. 2007, Kramer et al. 2019), and restoring the severity component of a fire regime can be difficult or logistically impossible when high-severity effects are desirable in WUI or in WUI-adjacent ecosystems. In the context of serotinous species such as bishop pine, the timing of prescribed fire is especially critical, because using fire prior to the development of a mature aerial seedbank risks post-fire regeneration failures (i.e., immaturity risk, Keeley et al. 1999). Waiting to burn until fuel loads are critically high, however, increases risk and conflicts with the primary aim of prescribed burning in the WUI – hazardous fuel reduction to mitigate risk to human health, safety, and structures (Fernandes and Botelho 2003, Reinhardt et al. 2008, Schoennagel et al. 2009). The alternative to frequent prescribed fire application is waiting on the inevitable wildfire, which is documented to adequately regenerate bishop pine at even the oldest stand ages (Forrestel et al. 2011, Harvey et al. 2011). This strategy may, however, be incongruent with the objectives of maintaining low fuel loading in the WUI. The WUI-adjacent bishop pine forest studied here presented both management challenges – restore fire yet mitigate risk. In this and other equally-fecund forest types, burning at shorter return intervals may be possible given the robust, viable seedbank developed in early successional phases, addressing both management challenges - restoring fire to promote resilience while simultaneously mitigating wildfire risk to the WUI.

Pyrosilviculture has the potential to succeed in meeting these often competing management objectives in bishop pine and other crown fire-adapted serotinous conifers, but we note that the stands burned and assessed here were all of a similar age and stand structure. Experimentally burning across the temporal profile of stand developmental stages (i.e., burning across ranges of stand aged and surface fuel loads) is an important area of further study given the anticipated shifts in fuel profiles from live to dead and canopy to surface over time (He et al. 2004, Scott 2005). Live fuels sustain and spread fire differently than dead fuels due to varying moisture content and chemistry (Finney et al. 2012), while shifts in the abundance of canopy versus surface fuels have the potential to significantly alter fire intensity and severity (O’Brien et al. 2016, Kiefer et al. 2018, Banerjee et al. 2020, Skowronski et al. 2020). In addition, experimentally burning at varying intensities, potentially during different seasons, could reveal if it is feasible to burn under intensities that release seeds from cones but do not kill canopy trees and instead result in two-cohort stands (Enright and Lamont 1989, Knox and Clarke 2006, Clarke et al. 2010). Burning at lower intensities may be more palatable to managers burning in WUI or WUI-adjacent ecosystems and may increase the use of this silvicultural tool. As with all species adapted to frequent fire regimes, understanding this species’ particular “ecology of fuels” will be important for management (Mitchell et al. 2009) and may be more so with the prevalence of a novel disturbance agent altering the timing and development of fuel profiles.

4.2 Compounding effects of a non-native pathogen

The addition of non-native pine pitch canker infection has the potential to literally add fuel to the fire and increase bishop pine mortality risk by altering post-fire stand development trajectories and shifting the timing and development of the total (live vs. dead) fuel profile. In the bishop pine stands studied here, density-dependent self-thinning occurred, as expected, in the years following post-fire establishment (Harvey et al. 2011), but, here, the high proportion of pine pitch canker infected trees in the intermediate-aged stands (90% median infected at 9 years) provides another early source of mortality. Selective pine pitch canker infection in saplings, in particular, has the potential to shift the live:dead and canopy:surface fuel ratios to earlier successional stages and increase the probability of higher fire intensity, as documented in other coastal California forests impacted by a non-native pathogen (Metz et al. 2013). Infected saplings may also be less likely to survive and recruit to larger size classes than uninfected saplings, thus altering stand development processes by reducing the number of individuals recruiting into the canopy, a bottleneck common in Monterey pine stands (Aegerter and Gordon 2006). This bottleneck could ultimately challenge bishop pine resilience and the frequent application of prescribed fire if this differential mortality hinders development and persistence of the abundant, high viability seedbank documented here.

It is worth noting, however, that little is known about pine pitch canker disease dynamics in bishop pine, making it hard to predict long-term stand trajectories following infection. Pine pitch canker was discovered in the region in the mid-1980s (McCain et al. 1987) and has only become widespread in bishop pine over the last two decades (Schmale and Gordon 2003). The condition of the oldest stands assessed here (burned in 1982) may therefore not represent the fate of forests in the context of this disease agent. High levels of unexplained variability in infection rates within and among stand age classes highlights the role of stochastic processes, unaccounted-for environmental differences, and individual variation in susceptibility to infection (Schmale and Gordon 2003). Additionally, our understanding of the effect of pine pitch canker infection on stand processes is limited by the space-for-time approach of this study. Specifically, we were unable to test the interacting effect of pine pitch canker infection and time since fire on plot-level variables, because stand development processes have coincided with a general increase in the presence of the disease on the landscape (Gordon et al. 2020). Tagged trees will be tracked over time in this permanent plot network, which will provide important insight into the longer-term ecological effects of this non-native disease and potential implications for forest responses to prescribed fire.

Prescribed fire may nonetheless remain a viable management option, and tagged trees will provide valuable insight into long-term disease dynamics across age classes and time since fire. In other coastal forests infected by a non-native pathogen, frequently burned forests have lower incidence of infection attributed to the dampening of pathogen transmission (Simler-Williamson et al. 2021). Frequent fire in pine pitch canker infected bishop pine may provide the same disease mitigation, and the rapid development and persistence of a viable canopy seedbank allows for a short fire return interval that will simultaneously promote bishop pine resilience. Additionally supporting frequent fire in pine pitch canker infected stands is the shift in fuel structure as stands enter high-competition phases, a transition that pine pitch canker accelerates when stands are relatively young. Waiting too long to burn may mean that hazardous fuel conditions persist on the landscape for a protracted period and increase the risk to WUI over a longer temporal window. A possible management activity that could mitigate fuel loads could be to conduct fuel reduction treatments in stands with a high incidence of pine pitch canker mortality via pile and burn or fuel removal operations. Prescribed fire could then be applied at a later time following this initial pyrosilvicultural treatment. Further experimentation with varying pyrosilvicultural techniques as well as prescribed burning at different stand ages, fuel structures, and seasons should allow for a refined understanding of how to prescribe fires in bishop pine stands in order to mitigate both pine pitch canker infection and wildfire hazard without risking regeneration failures.

4.3 The case for pyrosilviculture

We make the case for a pyrosilvicultural approach to managing forests adapted to a high-severity crown fire, yet it is hard to imagine frequent use of high-severity prescribed fire in densely populated areas, such as the bishop pine WUI studied here, without restructuring both risk analysis and wildfire mitigation programs (Calkin et al. 2014). Nonetheless, in systems where fire is inevitable, pyrosilvitulture is our best shot at restoring fire and associated ecosystem functioning while mitigating risk, and California’s Indigenous people have long ignited fire across this landscape (Lightfoot and Cuthrell 2015). There will always be more to learn as ecosystems, knowledge, and management evolve. But, the fire deficit will inevitably self-correct on its own if we do not take action and is likely to do so under severities and extents undesirable for both natural and human systems. Prescribed fire is the most effective means of reducing wildfire risk through its removal of fuels and restoration of the natural ecosystem dynamics evolved with fire (Fernandes and Botelho 2003, Kolden 2019), and prescribed fire escapement is rare (~ 1–2%, Dether and Black 2006, Miller et al. 2020). There are inherent risks and barriers to prescribed fire implementation (Quinn-Davidson and Varner 2012, Miller et al. 2020), particularly in WUI-rich California, however we argue, along with many other forest and fire ecologists (e.g., Kolden 2019, Stephens et al. 2020, Hessburg et al. 2021, North et al. 2021, Prichard et al. 2021), for a proactive return of fire to the West’s fire-adapted landscapes.

Long-term sustainability of crown fire-adapted forests will depend upon restoring the frequency of high-severity fire to which these ecosystems are adapted, and, here, we quantified the temporal pattern of canopy seedbank development, as well as the impacts of a non-native pathogen, to identify the acceptable prescribed fire return window in serotinous bishop pine forests and inform pyrosilviculture. This is the first study to move beyond cone counts as a surrogate for viability assessments and additionally quantify both seed viability and density over a range of stand ages to enumerate a more accurate assessment of reproductive capacity and the temporal window of fire return promoting forest resilience. We learned that bishop pine produces an abundant, viable canopy seedbank within six years of fire that persists across age classes from seedlings to mature trees and for up to a few decades following fire. We also learned that non-native pine pitch canker infection has differential effects on stand dynamics and that intermediate-aged stands dominated by saplings have the highest incidence of infection. Although the long-term effects of pine pitch canker infection remain unknown, bishop pines’ viable and persistent seedbank suggests that managers can ignite prescribed fire across a broad return interval – as short as six to eight years and as long as several decades – to promote ongoing bishop pine resilience, mitigate disease infection rates, and reduce wildfire risk in WUI-adjacent ecosystems. These findings may be generally applicable to equally-fecund serotinous species in which burning at short fire return intervals is feasible given early development of a robust, viable seedbank and addressing two common management challenges in fire-adapted forests - restoring fire to promote resilience while mitigating wildfire risk to the WUI.

ACKNOWLEDGEMENTS

The authors thank representatives of Pacific Gas & Electric – specifically Matt Brown, Kelly Kephart, Sally Krenn, and Dan Stocks – for coordinating access, sharing internal forest and vegetation management plans, and assisting in field sampling efforts. We additionally thank Olivia Moskowitz and Marissa Vossmer for leading field sampling efforts as well as the many Cal Poly senior project and volunteer students who participated in field sampling. We also thank Michelle Agne, Jessi Brown, Brian Harvey, and Peter Weisberg for their thoughtful comments on previous versions of this manuscript and advice on statistical analyses. The findings and conclusions in this publication are those of the authors and should not be considered to represent any official USDA or U.S. Government determination or policy.

Contributions

SMB conceived of the idea and designed the study, organized and oversaw data collection, and led manuscript writing. AKU analyzed data with assistance from LEK. All authors contributed to manuscript writing and editing and approved of the final manuscript.

Ethics approval and consent to participate

Not applicable

Consent for publication

Not applicable

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

Data will be made available upon publication.

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Rapid viable seedbank fosters resilience via pyrosilviculture in serotinous bishop pine

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Journal Publication

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Abstract

Background

Results

Conclusions

Figures

1. Background

2. Methods

2.1 Study Area

2.2 Field Sampling

2.3 Canopy Seedbank Estimates

2.4 Statistical Analyses

2.4.1 Canopy seedbank development

2.4.2 Pine pitch canker infection

3. Results

3.1 Canopy Seedbank Development in Post-Fire Stands

4. Discussion

4.1 Mapping adaptations to application

4.2 Compounding effects of a non-native pathogen

4.3 The case for pyrosilviculture

5. Conclusions

Declarations

References

Supplementary Files

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Journal Publication

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