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Article

Post-Fire Habitat Heterogeneity Leads to Black Spruce–Kalmia L. Shrub Savannah Alternate State

by
Azim U. Mallik
Department of Biology, Lakehead University, Thunder Bay, ON P7B 5E1, Canada
Forests 2022, 13(4), 570; https://doi.org/10.3390/f13040570
Submission received: 5 January 2022 / Revised: 31 March 2022 / Accepted: 2 April 2022 / Published: 4 April 2022
(This article belongs to the Section Forest Ecology and Management)
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Abstract

:
Many nutrient-poor coarse-textured Kalmia L.–black spruce forest sites in eastern Canada turn to ericaceous heath dominated by Kalmia angustifolia L. after clearcutting and fire. While the mechanisms of post-fire forest and heath formation have been well documented, the origin of shrub savanna vegetation has received limited attention. This study demonstrates the significance of post-fire island regeneration of black spruce in Kalmia heath to the origin of shrub savannah alternate state. The study was conducted in Three Brooks, 10 km west of Grand Falls-Windsor, Newfoundland (48°51′ N; 55°37′ E). Black spruce forest in the site was clearcut, then a wildfire burned the area, and the site was subsequently planted with black spruce. Plant species cover, black spruce growth (stem density, stem height, basal diameter, and yearly volume increment), and foliar nutrients of planted spruce and soil properties (pH, humus and Ae horizon depth, and nutrients) in tree islands were compared with adjacent Kalmia heath. Black spruce islands had significantly lower cover of Kalmia and higher stem density of black spruce compared to Kalmia heath (7100 stems/ha in islands vs. 1920 stems/ha in heath). Height, basal diameter, and yearly volume increment of black spruce were more than three times higher in spruce islands than in Kalmia heath. Foliar nutrients of black spruce growing in Kalmia heath had significantly lower N and Mg (33 and 38%, respectively) but had significantly higher Mn and Zn (46 and 33%, respectively) than in black spruce islands. Black spruce growth inhibition in Kalmia heath is attributed to soil nutrient imbalance due to Kalmia evidenced by reduced concentrations of N and Mg and increased concentrations of Al, Fe, and other inorganic ions in the foliage. These results suggest that post-fire black spruce islands in severely burned patches provide “safe sites” for spruce regeneration, whereas Kalmia heath developing in non-severe burn area inhibits spruce regeneration and creates shrub savannah community as an alternate vegetation state.

1. Introduction

It has been widely observed that nutrient-poor coarse-textured Kalmia L.–black spruce (Picea mariana L.) forests in central and eastern Newfoundland become Kalmia angustifolia (hereafter referred to as Kalmia)-dominated heath following forest fire or clearcutting with very little black spruce regeneration [1,2,3,4]. Black spruce planted in Kalmia-dominated sites exhibit “growth check” similar to other conifer-ericaceous communities [5,6,7,8,9,10,11]. A systematic survey of 5888 plots of new plantations in central Newfoundland reported proliferation of Kalmia in 55% of the plots [12]. In New Brunswick, Canada, growth of jack pine (Pinus banksiana) planted in clearcuts remained stunted with concomitant increase in Kalmia density [13]. Several authors suggested that prolonged occupancy of Kalmia in a site leads to long-term soil and vegetation change [4,14,15,16]. Large, canopy-removing disturbance such as forest fire and clearcut harvesting convert conifer–ericaceous forests to ericaceous heath, particularly in low-productivity sites [17,18]. Competition [17,19], allelopathy [20,21], soil nutrient stress/imbalance [4,22,23,24,25], and limitation of ectomycorrhizal association in conifer roots [4,26,27] have been suggested as reasons for Kalmia proliferation and black spruce regeneration failure. Multiple factors work simultaneously in the conversion of black spruce forests to Kalmia-dominated heath [28].
Deterioration of site quality in the presence of Kalmia leads to substantially lower site index for black spruce [29]. The afterlife effects of the dominant plant’s litter (by changing seedbed conditions) create a habitat filter that affects tree regeneration and change in species composition [30,31]. Unsuitable seedbed condition created by polyphenol-rich ericaceous litter has been attributed to poor black spruce seedling recruitment and growth. However, since the distribution and density of the dominant understory plants in a site is not uniform, the quality and quantity of litter accumulation and site degradation is also not uniform. Even in the presence of dominant understory plants that accumulate litter unsuitable for spruce regeneration, pockets of favorable seedbeds, or “safe sites” [32], can occur within the generally inhospitable seedbed. Because of these heterogeneous seedbed conditions, seedling regeneration of conifers following forest fires is likely to be heterogeneous [33].
Conceptually, there can be three alternate post-fire vegetation, depending on the degree and distribution of burn severity: (i) uniformly high-severity fires may lead to forest regeneration by consuming Kalmia belowground vegetative organs [34], releasing nutrients and creating favourable seedbeds for conifers [35,36] (Figure 1a), (ii) uniformly low-severity fires may create ericaceous heath by protecting Kalmia belowground organs located in partially burned humus and allowing rapid ericaceous growth [37] and also creating unfavourable seedbeds with allelopathic property [31,38,39], (Figure 1b), and (iii) patchy high- and low-severity burns may form shrub savannah vegetation by creating scattered favourable seedbeds for black spruce in amongst rapidly growing Kalmia [31] (Figure 1c).
While the mechanisms of post-fire forest and heath formation have been well documented [34], the origin of shrub savanna vegetation has received limited attention. Soil charcoal and microfossil analysis in northern Quebec concluded that Kalmia lichen woodland (also called shrub savannah) may originate from closed-canopy black spruce forest from repeated canopy-removing disturbances such as insect defoliation and fire [40]. Compounding effects of fire and insect infestation may reduce fire return interval and consequently decrease disturbance severity [41]. Based on the current expansion rates of lichen woodland, some authors theorized that the closed-canopy boreal forests will cease to exist in 550 years [42]. This is a dire prediction of vegetation change, loss of biodiversity, and ecosystem services. A comparative study of fire history and post-fire habitat properties, such as residual organic matter (ROM) thickness, charcoal density, and distribution in soil, species composition, and diversity, in nine post-fire sites in and around Terra Nova National Park, Newfoundland concluded that post-fire ROM thickness determines post-fire vegetation type (forest, heath, or shrub savannah) [31]. This study supports the conceptual models suggested above (Figure 1), i.e., the depth and distribution of ROM determine whether a post-fire community will regenerate back to black spruce forest, Kalmia heath, or shrub savannah community. Hence it is important to further investigate the origin of shrub savannah community if such large-scale conversion of vegetation is likely to occur due to climate change and anthropogenic disturbance that change fire severity. Does the patchy distribution of high- and low-severity burns, by providing differential regeneration sites for trees and shrubs, drive the origin of shrub savannah community?
It is likely that the patches of high- and low-severity burns play a critical role in the origin of shrub savannah communities by controlling differential black spruce growth, species diversity, and general habitat conditions between black spruce islands (in severely burned pitches) and Kalmia heath (in non-severe burns). I hypothesized that higher stem growth and foliar nutrients of black spruce and higher vascular plant diversity in black spruce islands would be associated with post-fire habitat factors such as lower organic matter thickness, higher soil pH, and available nutrients than those in Kalmia heath. I tested this hypothesis by comparing stem growth and foliar nutrient concentrations of planted black spruce and species composition, richness, and diversity, and soil chemical properties in spruce islands and adjacent Kalmia heath.

2. Materials and Methods

2.1. Study Area

The study area belongs to the central Newfoundland biogeographic region [43]. The soil in the area is a nutrient-poor, podzolic, well- to rapidly-drained, sandy, gravel loam [44]. The climate is largely continental. Regional mean summer temperatures average 12 °C with annual precipitation 1000–1400 mm, approximately one third of which falls as snow beginning in November and continuing until April. Two-thirds of the annual rainfall occurs between May and October. Mature forest in the area is dominated by black spruce (Picea mariana) and balsam fir (Abies balsamea (L.) Mill.) with mixtures of white birch (Betula papyrifera Marsh.), mountain birch (Betula cordifolia Regel), trembling aspen (Populus tremuloides Michx.), and, to a lesser degree, tamarack (Larix laricina (du Roi) Koch). Ericaceous plants such as Kalmia, Vaccinium, and Rhododendron species are common forest understory.

2.2. Study Site

This study was conducted at Three Brooks, 10 km west of Grand Falls-Windsor, Newfoundland (latitude 48°51′; longitude 55°37′; altitude 76 m ASL), a black spruce–Kalmia site that was clearcut 24 years previously followed by a wildfire four years after logging. The area was subsequently planted with black spruce four years after the wildfire; by this time, Kalmia was widespread with high cover. Most of the surviving planted black spruce in the Kalmia-dominated area were stunted with yellow foliage. In this predominantly Kalmia heath vegetation, there were patches of tree islands dominated by black spruce (Figure 2).
Because of known history of disturbance (logging, fire, and planting), this site provided a unique opportunity to determine black spruce growth and community composition in high-severity burn (spruce island) and low-severity burn (heath) locations that formed shrub savannah community. The study site was selected randomly by walking in a 1 ha area of the post-fire community that had tree islands and adjacent Kalmia heath. Here, I took an intensive, rather than extensive, study approach by considering as many habitat and plant variables as possible that can differentiate post-fire habitat conditions and vegetation in three black spruce islands and adjacent Kalmia heath.

2.2.1. Black Spruce Stem Density and Growth

Height and basal diameter of all the black spruce grown in Kalmia heath plots and in spruce islands were determined by examining 10 randomly placed 50 m2 circular quadrats around black spruce in three island and around nine planted seedlings in three 10 × 10 m heath sites. From these data, stem density and volume of black spruce were determined in the spruce island and Kalmia heath. In addition, ten randomly chosen planted black spruce seedlings/saplings from the island and nine from the heath sites were destructively sampled for stem analysis and foliar chemistry. Black spruce growth was determined by measuring stem height, basal diameter, and annual volume increment. The width of each year’s growth ring was determined by examining cross sections of stems taken at 0–10 cm above ground. A TRIM (tree ring increment measurer) system; model No. 8723 (Embent MFG. Inc., Scarborough, ON, Canada) was used to determine annual ring width of the stem cross sections of black spruce. The annual volume increase was calculated by the following equation:
V = D 2 4 × h × 0.33
where V is the volume of wood, D is cumulative diameter, and h is cumulative height of each tree [7].

2.2.2. Foliar Nutrient Analysis

Foliar nutrients of black spruce were analyzed for N, P, K, Al, Ca, Fe, Mg, Cu, Mn, and Zn. One-year-old needles were collected from five locations of each of the ten planted black spruce seedlings obtained from the spruce island and nine from Kalmia heath sites. After digestion with HNO3, all elements except N were analyzed with an inductively coupled plasma analyzer (Jarrel-Ash ICP 9000). Total nitrogen was determined colorimetrically [45]. Several authors have argued that foliar nutrient contents generally reflect the soil nutrient conditions of the habitat [46,47,48].

2.2.3. Soil Characteristics

Depth and moisture content of organic matter (humus) and Ae mineral horizons were determined from samples from ten random locations in black spruce island and Kalmia. Moisture content was determined by averaging three instantaneous readings (±0.05 m3·m−3) from a Theta Probe moisture meter (Model # ML2×, Hoskin Scientific, Burlington, Ontario). Soil samples were collected from the organic (humus) and upper (Ae) mineral horizons and analyzed for pH, determined by using the 1:1 sample to distilled water ratio [45], ammonia (NH+) was extracted using 1 M KCl and analyzed by an autoanalyzer [49], total P was determined by Micro-Kjeldahl technique [41], and Ca, K, Mg, Na, Al, Cu, Fe, Mn, and Zn were determined by digesting soil with HNO3 and analyzing with an inductively coupled plasma analyzer (Jarrel-Ash ICP 9000).

2.2.4. Black Spruce Shade Effects on Kalmia

Under black spruce canopy, Kalmia has reduced vigor and it produces better quality litter with a lower C:N ratio of leaves than Kalmia growing in the open [35]. Shade effect of spruce on Kalmia may help expand spruce island into Kalmia heath. To determine the effect of black spruce canopy shade on Kalmia vigor, I measured photosynthetically active radiation (PAR) using a portable light meter (Decagon Sunfleck Ceptometer, Decagon Devices, Washington, DC, USA) on a uniformly overcast day in early July between the hours of 10 a.m. and 2 p.m. in 1 × 1 m quadrats placed at the center, at the edge, and just outside spruce islands along ten random transects. I measured Kalmia height (from the ground to the tip of Kalmia shoot) at five random points in each 1 × 1 m quadrat and ocularly assessed Kalmia cover.

2.2.5. Community Composition

I determined cover of all understory plants from ten 1 × 1 m quadrats placed in black spruce islands and ten quadrats placed randomly in Kalmia heath. Shannon’s species diversity index [50] was used to compare species diversity between the Kalmia heath and spruce island sites. Multi-response permutation procedure (MRPP) was used to compare plant communities of the island and heath.

2.3. Statistical Analysis

Multi-response permutation procedure (MRPP) [51] was used to test the null hypothesis of no floristic difference between the spruce island and Kalmia dominated sites using PC-ORD v. 5 [52]. T-tests were then performed to determine differences in soil and foliar nutrient concentrations of black spruce in Kalmia heath and spruce islands (SPSS v. 15). I used ANOVA to compare the thickness of humus and Ae horizon and their moisture content and pH in spruce island and heath sites to determine if PAR and Kalmia height differed among island locations (SPSS v. 15). Most of the data did not violate the assumptions of normality and homogeneity of variance. However, soil nutrient concentration values were log-transformed to normalize the data. Canonical correspondence analysis (CCA) was used to ordinate the twenty 1 × 1 m quadrats sampled in the Kalmia heath and spruce island sites with an overlay of the trajectory of soil characteristics that showed strong correlation with each habitat and species cover values (PC-ORD v. 5).

3. Results

3.1. Black Spruce Stem Density and Growth

Black spruce stem density was 73% lower (1920 stems/ha) in Kalmia heath than in spruce islands (7100 stems/ha) (Figure 3A). Height and basal diameter of black spruce growing in spruce islands were significantly higher compared to that in Kalmia heath (Figure 3B,C). Consequently, the mean stem volume of black spruce in Kalmia heath was dramatically lower than in spruce islands (119 cm3 vs. 1807 cm3) (Figure 3D).
Yearly increase in stem volume of black spruce in spruce islands remained high between two to eight years after planting, followed by a stable increase over the next two years and thereafter, the rate increase steadily declined (Figure 4A). During the same period, yearly stem volume increase of spruce growing in the Kalmia heath was negligible (Figure 4A). The cumulative volume increase of black spruce in spruce islands was high, but that in Kalmia heath was negligible (Figure 4B).

3.2. Foliar Nutrients

Black spruce growing in Kalmia heath had significantly lower concentrations of foliar N (T = 2.234; p = 0.04) and Mg (T = 6.761; p = 0.001) (32.64% and 37.46%, respectively) compared to those growing in spruce islands (Table 1). Conversely, foliar concentrations of Mn (T = 10.528; p = 0.049) and Zn (T = 2.317; p = 0.042) were significantly higher (45.95% and 32.62%, respectively) in black spruce growing in Kalmia heath compared to spruce islands. Concentrations of other foliar nutrients, such as P, Al, and Fe, were also higher in black spruce growing in Kalmia heath than those growing in the spruce island (Table 1).

3.2.1. Soil pH, Moisture, and Humus and Ae Horizon Depth

Humus and Ae horizon pH of both spruce island and Kalmia heath was quite low (2.5) and was not significantly different (Figure 5a). Humus soil moisture was much higher than that of Ae horizon in both island and heath sites (Figure 5b). Average depth of humus layer in spruce island was several folds lower (2.4 cm) than that in Kalmia heath (8.3 cm). Depth of Ae horizon in island and heath was high (8–10 cm), with no significant difference between them (Figure 5c).

3.2.2. Soil Nutrients

There were no significant differences in humus (organic matter) nutrient concentrations between Kalmia heath and black spruce islands. However, for the Ae mineral soil horizon all elemental concentrations except Na and Fe significantly differed between heath and island sites (Table 2). Total NH+, Ca, K, Mg, Mn, and Zn were all significantly higher in spruce island than Kalmia heath Ae horizon soil, whereas that of Kalmia heath was significantly higher in Al and Cu (Table 2).

3.3. Black Spruce Shade Effects on Kalmia

Photosynthetically active radiation (PAR) decreases significantly from the adjacent heath (180 µmole/m/s) to the edge (80 µmole/m/s) and center of black spruce island (10 µmole/m/s) with concomitant decrease of Kalmia cover (Figure 6a,b). However, Kalmia height was highest (60 cm) at the edge of spruce island experiencing intermediate level of shade (about 80 µmole/m/s), which was less than one-third of light above Kalmia canopy compared to open heath (Figure 6c). Spruce island centres had very little light (20 µmole/m/s), where Kalmia had low cover (<5%) and height (10–20 cm).

3.4. Community Composition

Ordination of species cover data using canonical correspondence analysis (CCA) separated Kalmia heath and spruce island plots distinctly along axis 1 (Figure 7; Supplementary Materials, Table S1), which accounted for 55.9% of the variation in species abundance among plots. Separation was weak along axis 2, explaining only 15.8% of the variance. Significant species–environmental correlations were also found for axis 1 and 2 (Pearson correlation = 0.997 and 0.988 respectively; Supplementary Materials, Table S1).
The Kalmia heath was characterized by an open canopy condition with few scattered stunted black spruce seedlings. The MRPP analysis showed a highly negative T-value (−12.25), indicating that species composition in the Kalmia heath community was significantly different from that of the spruce islands (p < 0.001). The high value of A (0.321) indicates that within each of Kalmia heath and spruce island, the sampling plots were similar in species composition and cover (Table 3).
Mean cover of spruce was 58.5% in spruce island but only 6.15% in Kalmia heath. Conversely, cover of Kalmia was substantially higher in the heath (58.5%) compared to spruce island (0.6%) (Supplementar, Materials, Table S2). The overall species richness was almost double in spruce island (16) compared to heath (8). Species diversity of vascular plants was higher in spruce islands (1.28) than in Kalmia heath (0.95). There were no significant differences in species diversity of bryophytes and lichens between the spruce island and heath sites. However, spruce islands had higher cover of pleurocarpous mosses such as Pleurozium schreberi and Ptilium crista-castrensis, whereas Kalmia heath had higher cover of acrocarpous mosses such as Dicranum scoparium and D. polysetum. Overall lichen cover and diversity were higher in Kalmia heath than spruce islands (Supplementary Materials, Table S2).

4. Discussion

Growth and foliar nutrient concentrations of planted black spruce were significantly higher in spruce islands than in Kalmia heath, together forming a system of shrub savannah community that originated from closed-canopy forest following two consecutive disturbances, clearcut and fire. In this study, the planted black spruce can be considered as a phytometer, and its growth increments and foliar nutrients reflect the differential post-fire habitat quality at the spruce island and Kalmia heath sites. The spruce island sites had significantly thinner humus, higher pH, and higher available nutrients than the heath sites. These two types of habitats, although developed after the same fire, supported significantly different plant communities (forest vs. heath). These results support the hypothesis that post-fire black spruce islands in severely burned patches provide “safe sites” for seed-regenerating black spruce, whereas Kalmia heath developing in non-severe burn areas inhibit spruce regeneration but promote vegetatively regenerating stress-tolerant plants and create shrub savannah community as an alternate vegetation state.
Black spruce in the Kalmia-dominated plots suffered severe growth check with visible N deficiency symptom of chlorotic foliage and no sign of growth release 16 years after planting. On the other hand, black spruce stem density and growth were severalfold higher in the spruce island sites compared to the surrounding Kalmia heath. Many planted seedlings had died since planting and no natural recruitment of new black spruce seedlings occurred in Kalmia heath, resulting a much-reduced stem density. Lower stem density, height, and volume of black spruce were reported in presence of Kalmia compared to a contiguous Kalmia-free site in another study in central Newfoundland [10]. In black spruce islands, annual stem volume of spruce was increased in the beginning due to favorable microsites characterized by mineral soil seedbeds and absence of Kalmia and its polyphenol-rich humus. Mineral soil seedbed is suitable for spruce regeneration, whereas the charred Kalmia humus is not [36]. The subsequent decline in annual stem volume increments of black spruce in the islands may be due to intra-specific competition among the regenerating black spruce. Planted black spruce growing close to Kalmia has been found to have lower stem height and chlorotic needles than those growing away from Kalmia [5].
Can the expansion of the tree islands and their eventual coalescence lead to canopy closure? It will depend on two factors; i) proximity of the tree islands to each other, which is related to density and distribution of severely burned spots, and ii) the rate of expansion of the tree islands by layering at the island edge. This is because seedling regeneration in Kalmia heath is rare and, being shade-tolerant, Kalmia grows more vigorously at the spruce island edge [19]. The density distribution of high-severity patches in these forests is not known. With respect to the rate of expansion of spruce islands into Kalmia heath, one study conducted by measuring the expansion rates of layered stems in post-fire sites in Terra Nova National Park estimated that it will require 250–300 years to achieve canopy closure [53]. Fire return interval in these forests is often shorter than this. Studies in several open-canopy Kalmia–black spruce forests in nutrient-poor sites in Newfoundland showed that even 110 years after fire, the community is still very much open Kalmia–spruce–lichen woodlands (i.e., shrub savannahs). A similar phenomenon of island regeneration of lodgepole pine (Pinus contorta) following the large 1988 fire in Yellowstone National Park was observed, which was related to burn severity distribution [33].
Black spruce site index in central Newfoundland may be reduced from 12 to 4 with high-density Kalmia leading to long-term soil degradation [29]. This is attributed to poor growth and seedling mortality of spruce in the presence of Kalmia resulting from soil nutrient imbalance and allelopathy [22]. It has been shown that phenolic acids in combination with high concentrations of metallic ions such as Mn can stimulate the decarboxylation of indole acetic acid (IAA) and inhibit plant growth [54,55]. For example, p-hydroxybenzoic, vanillic, p-coumaric, and syringic acids are known to reduce available IAA by promoting IAA decarboxylation [56]. In the present study, significant increase (almost double) of foliar concentration of Mn was found in black spruce growing in Kalmia heath compared to those in the spruce islands (Table 1). Phenolic acids such as p-hydroxybenzoic, genticic, o-hydroxyphenylacetic, vanillic, p-coumaric, m-coumaric, ferulic, and syringic acids were identified from Kalmia leaves [57]. These authors have shown that primary root and shoot growth of black spruce were inhibited by gentisic and o-hydroxyphenylacetic acids at 0.5–5.0 mM, and several other phenolic acids at 1–5 mM, concentrations. However, involvement of these phenolics in growth inhibition of black spruce seedlings under field conditions has not been established.
Deficiency of available N and Mg and excess of Al and Mn concentrations in the foliage may be responsible for black spruce growth check in the Kalmia heath. Foliar N and Mg concentrations of 0.7% and 0.004%, respectively, found in black spruce growing in Kalmia heath were below the concentrations required for normal growth [58]. N deficiency symptoms in black spruce can be observed when its foliar nutrient concentration range from 0.6 to 1.0%. Similarly, Mg deficiency symptoms in black spruce can be found with a foliar concentration of 0.07%. From these results, it appears that black spruce seedlings in Kalmia heath suffered from nutrient deficiency. Soil nutrient concentrations of the spruce island and Kalmia heath sites of the present study confirm this mechanism. Kalmia, similar to other ericaceous plants, produces large quantities of polyphenols that can bind soil organic N as calcitrant protein–phenol complexes [59]. Ericaceous plants can access organic N through the ericoid mycorrhizae by means of enzymatic degradation; however, the ectomycorrhizal fungi associated with the conifers cannot obtain N from the same source [24,25]. As a result, conifers growing in ericaceous shrubs frequently suffer from N deficiency [60,61]. A litter-amending experiment with Kalmia and Leadum groenlandicum leaves showed that litter from these ericaceous plants can lower pH and increase the total phenolic content of soil [7,22,56]. These changes in soil can reduce available N and increase Ca, Fe, Al, Mn, and Cu [15]. High phenolics are known to influence the availability, accumulation, and uptake of nutrients [57]. The results of soil chemical analysis of Kalmia heath and black spruce island plots in this study (Table 2) explain the reason for the differential growth and foliar nutrients of black spruce in spruce island and Kalmia heath.
With respect to plant community development in the spruce island and Kamia heath, the MRPP analysis showed highly negative T-value (Table 3), which means that plant communities in spruce island and Kalmia heath were significantly different. Although it would have been desirable to sample more quadrats in each community (island and heath), the high value of A indicates that species composition and cover were similar within spruce island and Kalmia heath, unlike between them. Significant reduction of species richness and diversity of vascular plants and concomitant increase in lichen cover in the Kalmia-dominated site compared to the island site indicate that Kalmia dominance induced nutrient stress. Several authors have suggested that long-term occupancy of a site by Kalmia can bring about permanent soil and vegetation change by increased paludification and nutrient imbalance [4,16]. High cover of certain stress-tolerant lichens in the Kalmia heath reflects habitat stress [10,39,58]. Several studies suggested that habitat stresses induced by ericaceous plants and their litter act as abiotic and biotic filters promoting vegetatively regenerating plants, as opposed to seed-regenerating plants, leading to heath formation where stress-tolerant plants persist [31,59,60]. This may explain the poor growth of seed-regenerating plants such as black spruce, and the absence of many understorey vascular plants in the Kalmia heath, where stress-tolerant bryophytes and lichens make up the ground flora.

5. Conclusions

Post-fire patchy distribution of high-severity burns plays a dominant role in the origin of shrub savannah community from closed-canopy black spruce forests. Although the long-term persistence mechanisms of black spruce–Kalmia shrub savannah as an alternate state was not the focus of the present study, it is a necessary area of investigation considering the future change in disturbance regime due to forest management and climate change. It is likely that distinct plant–soil feedbacks (dominant species regeneration traits, litter accumulation, decomposition, available nutrients, mycorrhizal community, and response to disturbance) operating in spruce island and Kalmia heath will reinforce the persistence of this increasingly expanding shrub savannah community state in the boreal forest. With respect to forest management approach in this type of shrub savannah community, one can consider microsite mulching followed by tree planting in Kalmia heath locations [61].

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/f13040570/s1, Table S1: Vascular plant, bryophyte, and lichen species cover in Kalmia heath and spruce islands. Values are mean ± (standard deviation) of ten 1 × 1 m quadrats from each site. Table S2: Intra-set Pearson correlations * of soil organic matter (OM) depth and Ae mineral soil pH, moisture content, and nutrient concentrations between Kalmia heath and black spruce islands of the first two axes extracted in the CCA.

Funding

This research was supported by Natural Science and Engineering Research Council of Canada (NSERC) Discovery Grant # RGPIN-2014-06239 awarded to AUM.

Data Availability Statement

Not applicable.

Acknowledgments

I thank Dan Duckert, Center for Northern Forest Ecosystem Research (FNFER), Ontario Ministry of Natural Resources for TRIM analysis, Laura Siegwart Collier and Adiel Mallik for selected data analysis, and Colin St. James for reading a previous version of the manuscript. I also express my gratitude to the late Bill Furey, Abitibi-Bowater Consolidated, Grand Falls-Windsor, Newfoundland, for giving permission to work on the company licensed land at Three Brooks, Newfoundland. Comments of three anonymous reviewers were helpful in revising the paper.

Conflicts of Interest

The author declares no conflict of interest.

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Figure 1. Conceptual models of post-fire alternate vegetation states resulting from the degree and distribution of burn severity, (a) uniformly high-severity fires help forest regeneration by consuming Kalmia belowground organs and preparing favourable seedbeds for conifers, (b) uniformly low-severity fires create ericaceous heath by protecting Kalmia belowground organs in humus and allow rapid ericaceous growth (b), and (iii) (c) patchy high- and low-severity burns create shrub savannah vegetation by creating scattered favourable seedbeds for black spruce in amongst non-severe burns supporting Kalmia heath; (d) an older stage of shrub savannah, which can perpetuate by black spruce layering and high-severity burning in spruce island due to lower duff moisture content and higher fuel load than in Kalmia heath.
Figure 1. Conceptual models of post-fire alternate vegetation states resulting from the degree and distribution of burn severity, (a) uniformly high-severity fires help forest regeneration by consuming Kalmia belowground organs and preparing favourable seedbeds for conifers, (b) uniformly low-severity fires create ericaceous heath by protecting Kalmia belowground organs in humus and allow rapid ericaceous growth (b), and (iii) (c) patchy high- and low-severity burns create shrub savannah vegetation by creating scattered favourable seedbeds for black spruce in amongst non-severe burns supporting Kalmia heath; (d) an older stage of shrub savannah, which can perpetuate by black spruce layering and high-severity burning in spruce island due to lower duff moisture content and higher fuel load than in Kalmia heath.
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Figure 2. Island regeneration of black spruce 16 years after planting in the area that was previously logged and then burned by a wildfire at Three Brooks, Grand Falls-Windsor, Newfoundland. Open area in the foreground shows Kalmia heath and behind are the three adjacent black spruce islands where vegetation and soil sampling were conducted.
Figure 2. Island regeneration of black spruce 16 years after planting in the area that was previously logged and then burned by a wildfire at Three Brooks, Grand Falls-Windsor, Newfoundland. Open area in the foreground shows Kalmia heath and behind are the three adjacent black spruce islands where vegetation and soil sampling were conducted.
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Figure 3. (A) Stem density, (B) height, (C) basal diameter, and (D) volume of black spruce in black spruce islands and in Kalmia heath 16 years after planting at Three Brooks, Grand Falls-Windsor, Newfoundland.
Figure 3. (A) Stem density, (B) height, (C) basal diameter, and (D) volume of black spruce in black spruce islands and in Kalmia heath 16 years after planting at Three Brooks, Grand Falls-Windsor, Newfoundland.
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Figure 4. (A) Annual increment of stem volume and (B) cumulative increase of stem volume of planted black spruce in black spruce island and Kalmia heath 16 years after planting at Three Brooks, Grand Falls-Windsor, Newfoundland. Vertical bars indicate standard error of mean. Notice that black spruce stem volume increments were close to zero in heath, indicated by gray lines along the x-axis.
Figure 4. (A) Annual increment of stem volume and (B) cumulative increase of stem volume of planted black spruce in black spruce island and Kalmia heath 16 years after planting at Three Brooks, Grand Falls-Windsor, Newfoundland. Vertical bars indicate standard error of mean. Notice that black spruce stem volume increments were close to zero in heath, indicated by gray lines along the x-axis.
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Figure 5. (a) Soil pH, (b) soil moisture, and (c) depth of humus (H) and Ae horizon in Kalmia heath and black spruce islands in Three Brooks 16 years after fire.
Figure 5. (a) Soil pH, (b) soil moisture, and (c) depth of humus (H) and Ae horizon in Kalmia heath and black spruce islands in Three Brooks 16 years after fire.
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Figure 6. (a) Photosynthetically active radiation (PAR), (b) Kalmia cover, and (c) Kalmia height in open heath and at the edge (periphery) and center (closed) of black spruce island 16 years after fire. Different letters above the error bars in Figure 6 (a–c) indicate significant difference between Kalmia heath (open), at the edge (peripheral) and inside locations of close3 canopy spruce island (closed).
Figure 6. (a) Photosynthetically active radiation (PAR), (b) Kalmia cover, and (c) Kalmia height in open heath and at the edge (periphery) and center (closed) of black spruce island 16 years after fire. Different letters above the error bars in Figure 6 (a–c) indicate significant difference between Kalmia heath (open), at the edge (peripheral) and inside locations of close3 canopy spruce island (closed).
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Figure 7. Canonical correspondence analysis (CCA) of species covers from Kalmia heath and black spruce island plots with an overlay of soil properties (OM depth, soil moisture, and pH) and black spruce foliar nutrient concentrations.
Figure 7. Canonical correspondence analysis (CCA) of species covers from Kalmia heath and black spruce island plots with an overlay of soil properties (OM depth, soil moisture, and pH) and black spruce foliar nutrient concentrations.
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Table
Table 1. Mean foliar nutrient concentrations (±s.d.) and t-test statistics of planted black spruce in Kalmia heath and black spruce islands *. Effect size is expressed in Cohen’s d.
Table 1. Mean foliar nutrient concentrations (±s.d.) and t-test statistics of planted black spruce in Kalmia heath and black spruce islands *. Effect size is expressed in Cohen’s d.
NutrientKalmia HeathBlack Spruce Islandt-Statisticp-ValuePowerEffect Size
N (%)0.748 ± 0.0491.051 ± 0.0332.2340.0401.07.25
P (ppm)12.507 ± 0.98111.860 ± 0.226−0.5600.5880.600.91
K (ppm)4998 ± 297.925127.778 ± 208.9440.4120.6860.280.50
Al (ppm)1.021 ± 0.1640.643 ± 0.059−2.000.0711.03.07
Ca (ppm)25.290 ± 11.8549.094 ± 1.575−1.3940.1961.02.82
Cu (ppm)0.024 ± 0.000.023 ± 0.004−0.3390.7390.130.25
Fe (ppm)0.313 ± 0.010.281 ± 0.023−0.8380.4170.971.71
Mg (ppm)4.881 ± 0.428.011 ± 0.2166.761<0.0011.09.32
Mn (ppm)28.956 ± 5.5315.652 ± 1.52910.5280.0491.03.28
Zn (ppm)0.607 ± 0.110.409 ± 0.026−2.3170.0421.02.54
* N = 10 for black spruce islands and 9 for Kalmia heath.
Table
Table 2. Mean soil (organic and Ae horizon) nutrient concentrations (±s.d.) and t-test statistics of planted black spruce in Kalmia heath and black spruce islands *. Effect size is expressed in Cohen’s d.
Table 2. Mean soil (organic and Ae horizon) nutrient concentrations (±s.d.) and t-test statistics of planted black spruce in Kalmia heath and black spruce islands *. Effect size is expressed in Cohen’s d.
NutrientSoil HorizonKalmia HeathBlack Spruce Islandt-Statisticp-ValuePowerEffect Size
NH+ (%)Oh3.62 ± 1.023.01 ± 1.18−0.9080.3880.310.553
Ae2.26 ± 0.603.51 ± 0.928.427<0.0010.961.610
Ca (ppm)Oh4.14 ± 2.234.45 ± 2.100.2290.8240.090.143
Ae2.42 ± 0.654.86 ± 1.394.1300.0031.02.249
K (ppm)Oh4.30 ± 1.734.35 ± 1.240.0540.9580.060.033
Ae3.07 ± 0.374.60 ± 1.343.9580.0030.951.557
Mg (ppm)Oh3.10 ± 2.033.79 ± 1.550.6170.5530.200.382
Ae1.92 ± 0.454.28± 1.274.8180.0011.02.477
Na (ppm)Oh3.01 ± 1.072.72 ± 0.56−0.6580.5270.170.340
Ae2.24 ± 0.622.78 ± 0.821.9810.0790.460.743
Al (ppm)Oh5.92 ± 11.105.10 ± 0.82−1.3730.2030.550.845
Ae6.29 ±0.804.70 ± 0.55−3.8710.0041.02.316
Cu (ppm)Oh−0.84 ± 11.53−0.32 ± 1.320.5830.5740.190.364
Ae0.35 ± 0.34−0.37 ± 0.80−3.3890.0080.791.171
Fe (ppm)Oh3.91 ± 0.793.54 ± 0.62−0.9810.3520.290.521
Ae3.68 ± 0.933.05± 0.26−2.1630.0590.610.922
Mn (ppm)Oh3.24 ± 1.652.94 ± 2.71−0.2280.8250.090.134
Ae0.54 ± 2.302.36 ± 2.432.5860.0290.480.769
Zn (ppm)Oh1.36 ± 1.361.75 ± 1.130.5010.6280.160.312
Ae−0.33 ± 0.321.46± 1.572.6240.0280.951.580
P (ppm)Oh4.01 ± 0.963.22 ± 0.47−1.8610.0960.701.045
Ae2.80 ± 0.513.52 ± 0.474.7160.0010.921.468
* N = 10 for black spruce islands and 9 for Kalmia heath.
Table
Table 3. Summary results of multi-response permutation procedure (MRPP) conducted with species cover data from black spruce island and Kalmia heath sites.
Table 3. Summary results of multi-response permutation procedure (MRPP) conducted with species cover data from black spruce island and Kalmia heath sites.
SiteAverage
Distance		NMRPP
Statistics
Black spruce island
Kalmia heath		0.4741
0.3167		10
10		Observed Delta = 0.3959
Expected Delta = 0.5836
T = −12.25
A = 0.321
P = < 0.001
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Mallik, A.U. Post-Fire Habitat Heterogeneity Leads to Black Spruce–Kalmia L. Shrub Savannah Alternate State. Forests 2022, 13, 570. https://doi.org/10.3390/f13040570

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Mallik AU. Post-Fire Habitat Heterogeneity Leads to Black Spruce–Kalmia L. Shrub Savannah Alternate State. Forests. 2022; 13(4):570. https://doi.org/10.3390/f13040570

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Mallik, Azim U. 2022. "Post-Fire Habitat Heterogeneity Leads to Black Spruce–Kalmia L. Shrub Savannah Alternate State" Forests 13, no. 4: 570. https://doi.org/10.3390/f13040570

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