Abstract

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Keywords

Introduction

The boreal forests of Canada have evolved over thousands of years in the presence of natural disturbance such as fire and large-scale insect defoliation. The characteristic structure and species composition of these forests are shaped by these and other natural disturbances. However, in recent years particularly since the last half of the last century aggressive fire suppression, insect control and clearcut harvesting have been the primary focus of forest management causing a dramatic change in plant species composition and diversity. Major change in species composition has potential to bring about changes in biogeochemical cycling causing long-term vegetation change at a landscape level. This change is particularly pronounced in large parts of nutrient-poor cool temperate coastal forests of Atlantic Canada (van Nostrand 1971; Wall 1977; Mallik 1994, 1995; Thiffault 2004).

Mature forests in this region have three well recognizable strata: i) a tree canopy layer usually dominated by conifers such as black spruce (Picea mariana (Mill.) BSP), balsam fir [Abies balsamea (L.) Mill], larch [Larix laricina (Du Roi) K. Koch.] with some hardwood species such as birch (Betula papyrifera Marsh.), poplar (Populus tremuloides Michx.), ii) an understorey community often dominated by sheep laurel, (Kalmia angustifolia L., hereafter referred to Kalmia), Labrador tea, Rhododendron groenlandicum (Oeder) Kron & Judd), Rodora [Rhododendron canadense (L.) Torr.], blueberry (Vaccinium spp.), few herbs and iii) ground cover often dominated by pleurocarpous mosses such as Pleurozium schreberi (Brid.) Mitt., Hylocomium splendens (Hedw.) BSG and Ptilium crista-castrensis (Hedw.) De Not. acrocarpous mosses sech as Dichranum and Polytiricum spp. and lichens such as Cladonia spp. particularly C. rangiferina (L.) Harm., C. mitis (Sandst.) Hale & Culb., C. borealis, etc. Suppression of natural fires and overstory removal by clearcutting stimulate growth and spread of the understory ericaceous plants which regenerate primarily by vegetative methods (Mallik 1993). Under natural fire regime high severity fires remove shrub competition by killing the plants and creating favourable seedbed conditions for conifers by thermal decomposition of humus that often contain phenolic allelochemicals (Zhu and Mallik 1994). In the absence of severe fire the phenilic-rich ericaceous dominated forest floor inhibits conifer regeneration (Mallik 1987). Planted conifers also experience stunted growth in the presence of dense ericaceous cover often created under this form of land management. In addition to the loss of forest productivity the conversion of multi-story forest structure to simple shrub dominated plant communities has serious implications for plant and animal diversity and ecological integrity of national and provincial parks, ecological reserves and protected area (Mallik 1995; Bloom 2001). Growth inhibition in the presence of Kalmia has been reported in black spruce (Krause 1986; Mallik 1987, 1994, 1995; Inderjit and Mallik 1996ab; Thiffault et al. 2004), red pine (Pinus resinosa Ait.) (Mallik and Roberts 1994) and balsam fir (Thompson and Mallik 1989). Among the several common ericaceous plants in Canada Kalmia exhibits the strongest growth inhibitory effect on black spruce. Each year a large portion of medium to poor quality black spruce-Kalmia forests in eastern Canada particularly in Newfoundland and northern Quebec have been transforming into Kalmia dominated heaths (Figure 1, Mallik 1995, 2003).

Figure 1. Black spruce-Kalmia forest turned into Kalmia dominated heath by a natural forest fire 27 years ago near Terra Nova National Park, Newfoundland (photo, A.U. Mallik). The fire was suppressed before it became a severe.

In this paper we provide field evidence to suggest that forest vegetation of this region has been destabilized by the presence of thick layers of undecomposed Kalmia humus that has allelopathic effects on black spruce. The seedbed allelopathy of Kalmia humus prevents conifer colonization in Kalmia dominated sites causing a vegetation shift from forest to heath. Colonization of conifers in ericaceous heath is extremely slow and in some cases not possible due to positive biological and chemical feedbacks.

Causes and effects of ericaceous dominance in relation to conifer regeneration

Because of the rapid vegetative growth of ericaceous plants after forest canopy removal conifers face direct competition with the understorey shrubs. However, the degree of conifer growth inhibition is relative to specific conifer-ericaceous combination. For example Kalmia can induce black spruce growth inhibition for 40 years or more (Bloom 2001) but black spruce growth inhibition in the presence of Ledum lasts for about six years (Inderjit and Mallik 1996). The ericaceous plants compete directly with the conifers for nutrients and growing space (Bradley et al. 1997; Krause 1998). The ericaceous plants, particularly Kalmia has strong allelopathic potential by causing growth inhibition of primary roots (Mallik 1987). Although providing conclusive direct evidence of Kalmia allelopathy on black spruce remains a challenge (Inderjit and Mallik 2001) previous laboratory experiments and recently conducted field experiments suggest non-nutritional mechanisms, potentially allelopathy may play a prominent role in growth inhibition of black spruce (Mallik 1987; Mallik and Newton 1988; Yamasaki et al. 2002).

Natural regeneration failure of conifers- limitation of favourable seedbed, does allelopathy play a role?

Forest canopy removal by clearcutting and non-severe fire under active fire suppression regime in eastern Canada is often associated with rapid vegetative growth of ericaceous plants and concomitant natural regeneration failure of conifers. Thus the post-disturbance period in these forests is often dominated by ericaceous heath. Ericaceous competition and allelopathy has been suggested as the potential cause of conifer regeneration failure (Mallik 1987, 2003). We tested a hypothesis that limitation of favorable seedbed is the principal cause of natural regeneration failure of black spruce. We tested this under field conditions in two steps. First we determined the amount of different types of seedbeds (Table 1) available in replicated plots along a post-fire chronosequence (1- 38 years after fire) of Kalmia-black spruce community in and around Terra Nova National Park (TNNP), Newfoundland. The fires were small and all the post-fire sites were dominated by Kalmia. We mapped three 10 x 20 m plots in each site and determined the surface area of different types of seedbeds. Our main findings were as follows. Immediately after fire 90% of the seedbed substrate was found to be consisted of charred organic matter and only in 10% of the recently burned surface had mineral soil exposed seedbed (Table 1). There was hardly any mineral soil exposed seedbed remaining four years after fire. Although there was large site to site variation in the amount of different seedbed types, crustose lichens made the predominant seedbed from four to nine years after fire along with the some charred organic surface and acrocarpous mosses. In older burns fruiticose lichens and leaf litter substrate formed the majority seedbed (Table1).

Table 1. Mean percent cover of different seedbed substrates across a post-fire chronosequence of black spruce-Kalmia community in and around terra Nova National Park, Newfoundland

Seedbed type	Stand age (years)
	1	4	9	13	17	20	22	38
Mineral soil	10
Charred organic soil	90	15	10	5		5		5
Leaf litter		5	40	45	45	40	30
Acrocarpous moss		10	10
Pleurocarpous moss				5	5	5	10	10
Crustose lichen		70			5		10	5
Fruticose lichen			40	45	45	50	50	80

Our next question was how suitable are these different seedbed types to black spruce regeneration? We planted 50 black spruce seeds in five 50 x 50 cm plots in each of the major seedbed types in the field and determined percent seed germination and seedling establishment. The details of site description and methods can be found in Bloom (2001). In summary, we found that mineral soil exposed seedbed was the most favourable seedbed type for black spruce regeneration which supported 70% germination and 45% seedling establishment (Table 2). Crustose lichen seedbed allowed no seed germination at all. The most commonly occurring seedbed substrate (the charred organic matter) allowed some seed germination but seedling establishment was extremely poor on this substance. The amount of leaf litter seedbed was not high until nine years after fire and by this time Kalmia became very vigorous and even leaf litter allowed some seed germination (20%) seedling establishment under Kalmia in the long run promises to be difficult because of shade from dense Kalmia (Table 2).

Table 2. Mean seed germination and seedling establishment of black spruce in experimentally seeded plots on commonly occurring post-fire seedbed substrates of black spruce-Kalmia community in and around Terra Nova National Park, Newfoundland.

Seedbed type	Germination (%)	Seedling establishment (%)
Mineral soil	70	45
Charred organic soil	55	3
Leaf litter	20	10
Acrocarpous moss	12	4
Pleurocarpous moss	2	0
Crustose lichen	0	0
Fruticose lichen	56	2

We conclude from this field survey of post-fire seedbed types and seeding experiment that limitation of favourable seedbed appears to be the principal reason for failure of natural regeneration of black spruce. There can be several reasons for poor seed germination and seedling establishment on these seedbed types of which allelopathy is one. Surface water repellence and chemistry of biological crusts may be inhibitory to seed germination. The primary roots of germinated seedlings in thick humus may be desiccated in long spell of summer drought. These factors are currently under investigation. Lack of favourable seedbed can affect all plant species that rely on seed regeneration. The vegetatively regenerating species on the other hand perform very well after clear cutting or non-sever fires because their regenerating organs remain protected under the humus and they grow rapidly after the forest canopy disturbance by producing above ground shoots and colonizing most of the post-disturbance habitats. Indeed a field survey of regeneration traits of species in the post-fire habitats showed that the relative abundance of resprouters in low severity burns was 74 while that in the high severity burn was 26 (Bloom 2001). Since the principal mode of regeneration of ericaceous plants such as Kalmia is vegetative (Mallik 1993) and their underground vegetative parts remain unharmed by non-severe fires and they can grow and spread very quickly in the post-fire habitat.

Ecological engineering effects- alternate persistent state of ericaceous heath

Dominance of ericaceous vegetation particularly Kalmia for an extended period after forest disturbance has significant ecological and land management implications. Damman (1971) suggested that long-term occupancy of a site by Kalmia can cause permanent change in soil property. Invasion of trees is extremely difficult in Kalmia dominated heath. The lack of tree colonization in Kalmia heath can be interpreted in the light of ecosystem engineering effects of dominant species. Lawton and Jones (1994) defined ecosystem engineers as ‘organisms that directly or indirectly modulate the availability of resources to other species by physical state changes in biotic and or abiotic material’. In the process the ecosystem engineers, ‘create, modify and maintain habitats’ (Lawton and Jone, 1994). The authors classified the ecosystem engineers into i) autogenic engineers- that ‘change the environment via their own physical structures’ for example, dominant plants by their living and dead tissues, and ii) allogenic engineers- that ‘change the environment by transforming living or nonliving materials from one physical state to another, via mechanical or other means’ for example, beavers making dams that alter hydrology, sedimentation, decomposition and nutrient cycling of the habitat and community composition and diversity of plants and animals (Naiman et al, 1988). Trees can be considered as the autogenic equivalent of beaver in the sense that a growing forest modify hydrology, nutrient cycling and near ground micro-climate such as humidity, temperature, wind speed and light (Holling, 1992). These factors create conditions and habitats for other organisms and without these engineers most of the other organisms would not survive. Using the example of plants as modifiers of fire behaviour Lawton and Jones (1995) argued that species dependent differential litter properties (quality and quantity of living and dead tissue as fuel) may regulate the magnitude, duration and intensity of fire and in turn alter the supply of resources to other species (Christensen, 1985; Dublin et al. 1990). Mallik (2003) argued that in boreal forest the degree of the humus removal by fire determines the structure and composition of the regenerating forest by modulating the seedbed. The lack of mineral soil seedbed resulting from mild fires or clearcutting favour vegetatively regenerating species such as trembling aspen, pin cherry (Prunus pensylvanica L.f.), green alder (Anlus viridis spp. Crispa (Aiton) Turril), beaked hazel (Corylus cornuta Marsh.) etc (Mallik et al. 1997) instead of the dominant conifer species such a black spruce, jack pine, white pine (Pinus strobus) and red pine (P. resinosa Ait.) causing a dramatic change in species composition (Carleton, 2000). Changes in canopy species composition can bring about changes in the understory species composition and forest floor humus property (Carleton, 2000)

In the case of conifer-ericaceous community the vegetatively regenerating ericaceous plants replace the seed regenerating conifers in the absence of sufficient suitable seedbed. In addition to the physical barrier of the humus its chemical nature particularly the high phenolic contents interfere with seed germination and seedling growth of the conifers (Mallik, 1987; Mallik and Pellissier, 2000 Mallik and Prescott, 2001). Inderjit and Mallik (1997) found that water leachate of Kalmia leaves can cause significant change in soil nutrient concentrations of the forest floor and mineral soil layers. Thus the shift in dominant species from conifer to ericaceous shrubs can create significant ecological engineering effect (Jones and Lawton 1995) on the habitat by changing the structure and composition of the biotic community as well as soil physical and chemical properties. Under Kalmia dominance in the absence of tree colonization a biological and chemical positive feedback mechanism may set in and the Kalmia heath community can persist as an alternate vegetation state (Mallik 2003).

Discussion

Destabilization of black spruce-Kalmia community to Kalmia dominated heath has significant ecological and management implications. From the forest productivity point of view the conversion of forest into heath comes with a significant economic loss of commercial timber. Kalmia heath unlike Calluna heath of western Europe has no grazing value for live stocks and game animals (Gimingham 1972). Lose of forest structure is associated with the loss of many forest dowelling plants and animals that require specialized habitats at different forest strata. This has serious implications for regional biodiversity conservation and ecosystem integrity. Apart from the loss of forest productivity the conversion of multi-layered forest structure to uniform dwarf shrub dominated plant community presents a serious concern for parks and recreation, conservation and ecological reserve management. However, by the same token it is interesting to note that Kalmia dominated heath in near Pocono till barren in Pennsylvania is reported to contain disproportionately large number of rare plants compared to the nearby forest (Latham 2003). Nonetheless, it is clear that destabilization of black spruce forest by fire suppression and clearcutting (due to seedbed limitation) is having a potentially significant effect on forest structure and composition in eastern Canada. All these stand- and landscape-level changes may have their origin in seedbed allelopathy of the regenerating vegetation.

Acknowledgements

We acknowledge the support of Natural Science and Engineering Research Council (NSERC) of Canada and Parks Canada in the form of research grants and logistical help. In particular, we thank Mr. Randy Power, Park Ecologist, Terra Nova National Park, Newfoundland for his continuing support for our research on Kalmia-black spruce interaction. Comments of the two anonymous reviewers were helpful in revising the manuscript.

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