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Critical Reviews in Plant Sciences, 22(3&4):341–366 (2003)

0735-2689/03/$.50© 2003 by CRC Press LLC

Conifer Regeneration Problems in Boreal andTemperate Forests with Ericaceous Understory:Role of Disturbance, Seedbed Limitation, andKeytsone Species Change

A. U. MallikBiology Department, Lakehead University, Thunder Bay, Ontario, Canada P7B 5E1, Email:azim.mallik@lakeheadu.ca. Phone: (807) 343-8927; Fax: (807) 346-7796

ABSTRACT: Conifer regeneration failure in the presence of dense ericaceous cover resulting from the removalof canopy trees by forest harvesting observed in boreal and temperate forest has been attributed to allelopathy,competition, and soil nutrient imbalance. Ecosystem-level alleopathic effect has been argued as a cause for coniferregeneration failure by citing examples from a species-poor boreal forest in northern Sweden with groundvegetation dominated by crowberry (Empetrum hermaphroditum, Ericales) and New Zealand dairy pasturesinvaded by nodding or musk thistle (Carduus nutans). This article aims to explain the phenomenon of vegetationshift from conifer forest to ericaceous heath by extending the argument of ecosystem-level impact of ericaceousplants and linking the disturbance-mediated regeneration strategies of the dominant conifer species and theunderstory ericaceous species with the quality of seedbed substrate that influence the direction of secondarysuccession. It has been argued that fire severity plays a pivotal role in controlling seedbed quality and theregeneration mechanisms of conifers, which in turn determines the direction of post-disturbance succession. Thepost-fire-dominated ericaceous plants and their habitat-modifying effects have been explained from the point ofview of keystone species concept and their role as ecosystem engineers. In the absence of high severity natural firesthe canopy keystone species (conifer) fails to regenerate successfully mainly due to limitation of favorableseedbed. On the other hand, the understory ericaceous plants regenerate vigorously by vegetative methods fromthe belowground components that survived the fire. Forest harvesting by clearcutting or selective cutting alsocreate similar vigorous vegetative regrowth of ericaceous plants, but conifer regeneration suffers from the lack ofa suitable seedbed. Thus in the absence of successful conifer regeneration, the vigorously growing understoryericaceous plants become the new keystone species. The new keystone ericaceous species bring about a significantlong-term habitat change by rapid accumulation of plyphenol-rich humus. Ericaceous phenolic compounds havebeen found to inhibit seed germination and seedling growth of conifers. By forming protein-phenol complexes theycause a further reduction of available nitrogen of the already nutrient-stressed habitat. A low pH condition in thepresence of phenolic compounds causes the leaching of metallic ions and forms hard iron pans that impair soilwater movement. The phenolic allelochemicals of ericaceous humus are also inhibitory to many coniferectomycorrhizae.

On the other hand, ericaceous plants perpetuate in the community by their stress-tolerating strategies as wellas their ability to acquire nutrients through ericoid mycorrhizae. Three mechanisms working at the ecosystem levelcan be suggested as the cause of vegetation shift from forest to ericaceous heath. These are (1) the absence of highseverity natural fire and the limitation of suitable conifer seedbed in the presence of thick humus, (2) increasedcompetition resulting from the rapid vegetative regeneration of understory ericaceous plants after forest canopyopening by harvesting or nonsevere fire, and (3) habitat degradation by phenolic allelochemicals of ericaceousplants causing a soil nutrient imbalance and iron pan formation. Thus, a shift in keystone species from conifer toericaceous plant in the post-disturbance habitat may induce a retrogressive succession due to ecosystem-levelengineering effects of the new keystone species.

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Vegetation management in conifer-ericaceous communities depends on land management objectives. If theobjective is to produce timber and other forest products then the control of ericaceous plants and site preparationis necessary after forest harvesting. Ploughing and liming followed by conifer planting and repeated N fertilizationhas been applied successfully to promote afforestation of Calluna heathlands in Britain. However, such practicehas not been proven successful in the reforestation of Kalmia-dominated sites in eastern Canada. If, on the otherhand, the land management objective is to maintain heathlands for herbivore production or conservation of culturallandscape, as in the case of certain Calluna-dominated heathland in Western Europe, then moderately hotprescribed burning is useful as a management tool.

KEY WORDS: keystone species, ecosystem engineer, alternate stable states, ericaceous plants, allelopathy,phenolics, fire, harvesting, regeneration, succession, mycorrhizae, growth check.

I. INTRODUCTION

Allelopathy, competition, soil nutrient imbal-ance, and poor ectomycorrhization have been im-plicated in conifer regeneration failure in the pres-ence of dense ericaceous understory resulting fromforest harvesting and fire in boreal forests andsub-alpine spruce forests (Mallik, 1999). Pellissierand Souto (1999) have reviewed the role of allel-opathy in northern temperate and seminaturalboreal forests. The growth inhibition of Sitkaspruce (Picea sitchensis (Bong.) Carriere) in thepresence of heather [Calluna vulgaris (L.) Hull,hereafter referred to as Calluna] has been re-ported by several authors from Britain as early as1953 (Wheatherell, 1953; Leyton, 1954, 1955).Similarly, the failure of natural regeneration andgrowth inhibition of planted conifers such as blackspruce in the presence of sheep laurel (Kalmiaangustifolia L., hereafter referred to as Kalmia)and Labrador tea (Ledum groenlandicum L.) hasbeen reported by several authors (Mallik, 1987,1992; Yamasaki, et al., 1998; Inderjit and Mallik,1996a). Likewise, growth inhibition of jack pine(Pinus banksiana Lamb.) in the presence of Kalmiahas been reported from New Brunswick, Canada,by Krause (1986). From the west coast of Canadaand the Pacific Northwest of USA other erica-ceous shrubs such as salal (Gaultheria shallonPursh.) in coastal oceanic temperate rainforestsand several Vaccinium species (e.g., Vacciniumalaskaense L.) in high elevation forests have beenreported to cause growth stagnation of coniferssuch as western red cedar (Tsuga plicata Donn),western hemlock (Thuja heterophylla (Raf.Sarge)), Sitka spruce (Picea sitchensis), andAmabilis fir (Abies amabilis Dougl.) (Bunnell,1990; Messier, 1993; Prescott et al., 1996; Fraser,

1994; Fraser et al., 1993, 1995). Belowgroundcompetition for space, available N and P and tosome extent condensed tannin allelopathy of salallitter have been suggested as the principal causesof growth check in these conifers (Taylor andTabbush, 1990; Weetman et al., 1990; Messier,1993; Prescott et al., 1996; Xiao, 1994; Xiao andBerch, 1993; de Montigny et al., 1991; deMontigny, 1992; Mallik and Prescott, 2001). Insub-alpine spruce forests in France another un-derstory ericaceous plant, bilberry (Vacciniummyrtillus L.), has been reported to cause the re-generation failure of Norway spruce (Picea abies(L) Karst.) (Andre et al., 1986; Jaderlund et al.,1996a,b). Phenolic allelochemicals of forest floorhumus and seed predation have been implicatedfor this regeneration failure (Pellissier, 1993, 1994;Gallet and Lebreton, 1995; Gallet et al., 1999). Innorthern Sweden cowberry, another member ofEricales (Empetrum hermaphroditum Hagerup)forms by far the predominant ground cover andinterferes with Norway spruce regeneration(Steijlen and Zackrisson, 1987; Wallstedt, 1998;Zackrisson and Nilsson, 1992; Nilsson, 1994).Nilsen et al. (1999) have shown that diversity andcomposition of plant litter have differential ef-fects on boreal plant-soil system.

In undisturbed forests all the above-mentionedericaceous plants form the main understory orground cover vegetation often regenerating wellin forest canopy gaps and in depapurated condi-tion under mature conifers. Following canopydisturbance by forest harvesting and fire theseericaceous plants grow vigorously by vegetativemethods and accumulate a large quantity of litteron the forest floor (Mallik, 1993, 1994; Damman,1971, 1975; Evardsen et al., 1988). The erica-ceous litter contains an array of phenolic com-

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pounds that are inhibitory to conifer seed germi-nation, primary root growth, and ectomycorrhizalgrowth (Pellissier, 1993, 1994; Mallik, 1987, 1992;Zhu and Mallik, 1994; Mallik and Zhu, 1995;Mallik et al., 1998). Many of these phenolic com-pounds can create soil nutrient imbalance by re-ducing the available N (by forming protein-phe-nol complex) and increasing the amounts of Fe,Zn, K, Ca, Mg, and Mn leading to long-term sitedegradation (Bending and Read, 1996a,b;Damman, 1971; Meades, 1983, 1986; Inderjit andMallik, 1996b, 1997a,b). Wollenweber andKohorst (1994) have extracted epicuticular leafflavonoids from Kalmia and salal and speculatedthat these compounds may have growth inhibi-tory effects on conifers. Differential nutrient up-take of ericoid mycorrhizae that favor the hostplant but have antagonistic effect on conifer my-corrhizae has been suggested as yet another causeof poor conifer growth in the presence of erica-ceous plants (Read, 1982). Recently, limitation offavorable seedbed for conifers seed regenerationin the presence of thick layer of forest humus,which, in addition to its chemical effect (allelopa-thy), acts a physical barrier of seedling establish-ment has been shown to be one of the primaryreasons for conifer regeneration failure after for-est disturbance in eastern Canada (Bloom, 2001).In general the mechanism of ericaceous inducedconifer regeneration failure is currently explainedby the combined effects of competition, allelopa-thy, soil nutrient deficiency and imbalance, in-creased acidity, differential mycorrhizal activitiesof the ericaceous shrubs, and tree species as wellas the physical barrier of the humus acting asunsuitable conifer seedbed (Mallik, 1999; Inderjitand Mallik, 1996a,b; Nilsen et al., 1999)

In almost all the above examples the conifer-ericaceous communities are characterized by onedominant canopy species (conifer) and one domi-nant understory species (ericaceous) that controlthe community structure and composition andbiogeochemistry of the habitat. Wardle et al.(1998) have argued that in such a species-poorcommunity allelopathy can have a stronger land-scape-level impact, particularly where the domi-nant species is competitive and allelopathic com-pared with a species-rich community. Forestdisturbance by harvesting of the canopy species

often results in prolific vegetative growth of theunderstory ericaceous plant that preclude coniferregeneration, creating a vegetation shift from for-est to heath (Mallik, 1995). In this instance onecan argue that the controlling effects of one spe-cies on another species and that on the ecosystemin relation to disturbance can be articulated fur-ther by extending the suggestion of ecosystem-level allelopathic effects of dominant species(Wardle et al., 1998) to the concept of keystonespecies (defined below) and organisms as ecosys-tem engineers (Jones et al., 1994). In other words,it is worthy of attempting to explain the distur-bance-mediated vegetation change from forest toericaceous heath in light of the concept of key-stone species and their ecosystem engineeringrole where allelopathic effect of the understoryspecies is one of the multifaceted chain of eventsthat follow due to the change of keystone species.One can argue that keystone species change fromconifer to ericaceous (causing in the absence ofappropriate disturbance regime) is the principalcause of ecosystem-level allelopathic effect andsubsequent habitat degradation and forest regen-eration failure. In the present review the causesand consequences of natural regeneration failureand growth inhibition of conifers following eco-system disturbance are explored by linking theregeneration response of the dominant (keystone)species to disturbance severity and their role asecosystem engineers.

II. PLANT SUCCESSION AFTERDISTURBANCE

Predicting vegetation change over time hasbeen a major preoccupation in ecology. Clements(1916) and later Odum (1969) presented mile-stone conceptual models of succession that de-scribed communities as increasing complexity andefficiency of resource use over successional time.However, such unidirectional model of plant suc-cession suffered from three major shortcomings:(1) unrealistic generalization of species-by-spe-cies and community-by-community replacement,that is, relay floristics (Egler, 1954), (2) lack ofrecognition of retrogressive succession where habi-tat degradation effects of certain species impede

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rather than facilitate the subsequent communityorganization (Connell, 1972; Drury and Nisbet,1973), and (3) lack of recognition of frequentdisturbance. The first two concerns were addressedby Connell and Slatyers’ (1977) three-pathwaymodel of succession: (1) Facilitation pathway, inwhich the presence of early occupants facilitatesthe entry and establishment of the successive suitsof species, (2) Tolerance pathway, in which ear-lier species will be those that are able to toleratethe lower level of resources than the earlier ones,and (3) Inhibition pathway, in which the existingspecies resist the invasion of later colonists. Spe-cies richness and succession vary over the courseof succession (Odum, 1969), and periodic distur-bance allows for this variation primarily throughthe prevention of competitive exclusion. Basedon this theme, Connell (1978) proposed the Inter-mediate Disturbance Hypothesis, which states thatan ecosystem maintains its highest species diver-sity under conditions of moderate disturbance. Adirect link between species traits and probablepathways of succession was forged with the de-velopment of the vital attributes model of Nobleand Slatyer (1980). This model is useful in pre-dicting the successional sequence of fire-proneAustralian ecosystems and regularly burned Scot-tish heathland ecosystems (Hobbs et al., 1984).While this theory takes into account the role ofdisturbance frequency on species diversity, it failsto appreciate the effect of habitat heterogeneitycreated by each disturbance such as fire. Post-firehabitat heterogeneity created by differential fireseverity and species regeneration strategies play asignificant role in determining species diversityas well as the rate and direction of succession.The vital attribute approach also does not differ-entiate between the species that determine theprogress and direction of succession fromsubordinant species that are ‘along for the ride’ orfunctionally redundant. White (1979) emphasizedthat the basic natural history characteristics of spe-cies and their reproductive strategies are of funda-mental importance in understanding succession.Rowe (1983) compared the vital attributes of theboreal species according to the groupings of Nobleand Slatyer (1980) and cautioned that complexityrather than simplicity would be the nature of plantadaptations to periodically disturbed ecosystems.

Presently there is a need to unify the conceptof ‘species functional groups’ (Tilman, 1996; Diazand Cabido, 1997; Noble and Gitay, 1996) tobuild a predictive and realistic model of succes-sion that focuses on ecosystem function ratherthan superficial measures of species compositionfollowing disturbance. We need to understandwhether species replacement is controlledbiotically through stress or facilitation amend-ments to the habitat or by competitive abilities ofplants within the inherent nutrient status of thehabitat. We need to link ecosystem disturbancepatterns with regeneration, competition, and habi-tat modification traits of the persisting speciesthat are sufficiently abundant to facilitate or in-hibit succession. Although it is generally acceptedthat species act individualistically (Gleason, 1926)“after-life effects” (Wardle et al., 1997; Wardleand Lavelle, 1997) of abscised tissues (especiallyleaves and roots) is a subtle but a chronic way inwhich species influence their habitats. The con-centrations of secondary compounds, availablenitrogen, and simple carbon compounds in thetissues of various functional groups may be animportant indicator of biogeochemical cycling asabundance of species within functional groupschange over time (Silver et al., 1996).

The fire-prone Kalmia-black spruce commu-nities of eastern Canada are simple in speciescomposition and provide an excellent opportunityto test some of these contemporary theories andconcepts of ecology in explaining the mechanismof secondary succession. Following disturbanceplant succession in some of these communitiestend to follow the inhibition pathway by convert-ing the forests into Kalmia dominated heaths(Meades, 1983, 1986; Mallik 1995). Two factorsseem to play important roles in this retrogressivesuccession from forest to heath, (1) dramatic in-crease in Kalmia cover after forest canopy re-moval (Mallik, 1994) that restricts colonizationof early and late successional species, and(2) habitat-modifying ability of Kalmia litter thatis unfavorable for the reestablishment of the key-stone species (black spruce) once the shrub isestablished. Damman (1971) suggested that long-term occupancy of Kalmia in a site changes thenutrient status of soil so much that it can nolonger support tree growth. Indeed, there are ex-

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amples of 15- to 40-year-old burns in centralNewfoundland ranging from 3 to 1000 ha that arecompletely dominated by Kalmia without muchtree cover. However, recent field visits in Kalmia-black spruce sites burned 30 to 50 years previ-ously showed sporadic tree colonization often ingroups mimicking island regeneration (Nyland,1998) among Kalmia. In some older burns Kalmia-dominated retrogressive succession seems to fol-low a slow but progressive succession towardopen canopy forest development. It seems thatpost-fire habitat heterogeneity created by eachfire plays a significant role in determining the rateas well as direction of succession. Shifting domi-nance of species along the successional sequencemay modify the habitat quite dramatically by in-creasing soil acidity (Grubb et al., 1969), iron panformation (Damman, 1964, 1971), allelopathy(Mallik, 1987; Mallik and Roberts, 1994), andnutrient imbalance (Inderjit and Mallik 1996b,1997a).

III. ECOSYSTEM DISTURBANCE ANDMULTIPLE STABLE STATES

One could attempt to explain the phenom-enon of disturbance induced vegetation shift fromconifer-ericaceous community to ericaceous heathand their persistence around the contiguous forestin light of the concept of multiple stable states innatural communities (Sutherland, 1974; Connelland Sousa, 1983). Multiple stable states occur‘when more than one type of community stablypersist in a single environmental regime’(Knowlton, 1992). Based on theoretical modeling(using mathematical stability theory) and fieldobservations, arguments have been made for theexistence of alternative stable states of plant andanimal communities (see reviews by May, 1977;van de Koppel et al., 1997). Physiognomic mani-festation of alternative stable states can be recog-nized by (1) the presence of a relatively stablevegetation mosaic in a previously uniform envi-ronment, and (2) intensification of a vegetationalgradient leading to sharp boundaries (Wilson andAgnew, 1992). Examples of multiple/alternatestable states have been reported from herbivorecontrolled density and growth regulation of plants

(Noy-Meir, 1975; May, 1977 but see Connell andSousa, 1983; Sousa and Connell, 1985; Peterson,1984; Sutherland, 1990). Rietkerk and van deKoppel (1997) reported alternate stable states andthreshold effects in semiarid grassing systemswhere they found that plant-soil interaction playsa more important role than herbivore feeding be-havior. They suggested that a positive feedbackbetween plant density and reduced resource avail-ability (soil water and nutrients) under increasedgrassing pressure maintains a two-phase alternatestable grassland mosaic. Latham et al. (1996) re-ported the contiguous occurrence of several dif-ferent plant community types on similar parentmaterial and soil type that can potentially favorforest community in Pocono barren, Pennsylva-nia. These are (1) Scrub oak barrens containing atleast 50% cover of Quercus ilicifolia Wang. withwidely spaced Pinus rigida P.Mill., (2) Heathbarrens consisting of at least 50% cover of mainlyKalmia angustifolia, Vaccinium angustifoliumAit., V. pallidum Ait, with sparce Pinus rigida,(3) Rhodora barrans with at least 50% cover ofRhododendron canadense (L) Torr., with scat-tered Pinus rigida, and (4) Forests that have atleast 90% tree cover dominated by either northernhardwoods species (such as Fagus grandifloraEhrh., Prunus serotina Ehrh., Betula alleghaniensisBritt., B. lenta L., Acer rubrum L., and A. saccha-rum Marshall) or red maple-oak dominated byAcer rubrum, Quercus alba L., and Q. coccineaMuenchh. Following further study on surficialgeology, soil type, soil moisture, and plant spe-cies composition, Eberhardt and Latham (2000)concluded that the alternative stable state hypoth-esis can explain the side by side existence of suchcommunities. They suggested that the origin andperpetuation of these communities on a similarsoil environment might be related to disturbance(fire) history and biotic influence of the dominantplants. They emphasized the particular impor-tance of the positive feedback driven by planttraits that encourage the spread of wild fire andrestrict the soil nitrogen availability that allow theheath species to dominate (Petraitis and Latham,1999). The potential significance of the bioticcontrol of alternative stable states of vegetationcan be determined by a comparative study of theautecological properties of the dominant plants

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and their ecological engineering effects on thehabitat (Lawton and Jones, 1995; Nilsen et al.,1999). One can assess the role of chemical feed-back mechanisms in sustaining the alternate stablestates by a comparative study of ericaceous-domi-nated heathlands and forests that alter or sustainsoil nutrient dynamics in opposite directions(Pellissier, 1993, 1994, 1998; Gallet, 1994; Galletand Pellissier, 1997; Northup et al., 1995; Chapin,1995). Hattenschwiler and Vitousek (2000) re-viewed the role of polyphenols in nutrient cy-cling. This phenomenon of polyphenol-controllednutrient release becomes even more critical undera stressed environment such as poor soil nutrientcondition, low temperature, and slow decomposi-tion in boreal and sub-alpine forests (Northup etal., 1995; Reogosa et al., 1999).

At present we do not know enough about thelongevity of the altered vegetation states underthe dominance of different ericaceous species.Connell and Sousa (1983) cautioned that in rec-ognizing alternate stable states one must considerthe intensity and time scale of perturbation andappropriate time and spatial scale of observationsof ecosystem response. One might argue that al-though the treeless Kalmia dominated condition40 years after a nonsevere fire in black spruce–Kalmia site may be considered as retrogressivesuccession, but the wood savannah type ofKalmia–black spruce community developing af-ter a nonsevere fire may be thought of an ex-tended seral stage of a progressive successiontoward forest development.

IV. DISTURBANCE, SEEDBED QUALITY,AND REGENERATION OF KEYSTONESPECIES

Keystone species in a habitat are ‘those spe-cies that provide the unique structure and functionof the ecosystem by performing the essential eco-system services’ (Ehrlich, 1986; Ehrlich and Wil-son, 1991). The removal of keystone species froma community would cause a significant change incommunity structure and function (Lawton andJones, 1995). The keystone species act as ecosys-tem engineers ‘by controlling directly or indi-rectly the availability of resources to other species

and by causing state changes on biotic and abioticmaterials’ (Jones et al., 1994; Lawton and Jones,1995). In the context of allelopathy it would berelevant to examine how the different types ofdisturbance change the keystone species that inturn change the structure and function of the eco-system. More specifically, it would be worth-while to relate the disturbance-mediated changeof keystone species with their functional rolesthat change the physical and chemical nature ofthe seedbed for conifer regeneration.

Forest floor allelopathy in boreal and temper-ate forests is regulated by the chemical nature ofthe humus. These forests often have one or twocanopy species and a dominant ericaceous under-story species that play the most predominant rolein controlling above and belowground ecologicalfunctions by accumulating most of the photosyn-thates and by their ‘afterlife effects’ through add-ing leaf litter and fine roots on forest floor humus(Wardle et al., 1997, 1998). A disproportionatelylarge amount of the humus develops from thelitter of keystone species and the physical, andchemical nature of the decomposing litter formsthe seedbed for newly regenerating conifers fromseeds. Changes in keystone species from coniferto ericaceous following forest disturbance bringabout changes in forest floor humus chemistry aswell as its physical property. Forest structure andfunction is regulated by the disturbance mediatedvegetation dynamics as well as humus chemistryof the dominant conifer and the understory spe-cies by controlling the above and belowgroundprocesses (Bradshaw and Zackrisson, 1990,Zackrisson et al., 1996; Zackrisson, 1977). Thehumus developing largely from the conifer andthe ericaceous understory litter contains an arrayof allelochemicals that interfere with natural re-generation of conifers by inhibiting their seedgermination and seedling growth (Gallet andPellissier, 1995, 1997; Pellissier, 1993, 1994;Pellissier and Souto, 1999; Mallik, 1987, 1992;Inderjit and Mallik, 1996a,b; Zackrisson andNilsson, 1992; Zackrisson et al., 1997; Prescott etal., 1996, 2000).

Gallet and Lebreton (1995) studied the pat-terns of phenolic polymers (tannins) and mono-mers (phenolic acids and flavonoids) in the livingleaf and root tissues, their litter and humus. They

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found high abundance of tannin in bilberry leaves,whereas the spruce needles had high abundanceof p-hydroxyacetophenone. Compared with thegreen foliage the brown foliage of bilberry exhib-ited greater loss of monomeric compounds, but ithad high tanning activity. The amount of proto-catechuic and vanillic acids (the degradation in-termediates) were increased with increasing litterdecomposition (Gallet and Lebreton, 1995).Spruce-dominated organic soil under bilberry hadhigh tanning activity and a high abundance ofphenolic acids. From a laboratory bioassay withnatural leachates of bilberry and spruce, Gallet(1994) concluded that p-hydroxyacetophenone, aspruce tree-specific metabolite, phenolic acids andtannins associated with bilberry reduce or evenoften stop the natural regeneration of spruce byinhibiting primary root growth of spruce seed-lings. Jaderlund et al. (1996) found that waterleachate of green leaves of bilberry had moreinhibitory effect on germination and root growthof Norway spruce than that of brown leaves. Froma laboratory bioassay and complimentary seedingexperiment in the field, Mallik and Pellissier(2000) reported only 2% and 3% germination incontrol plots (no Vaccinium, no litter removed)and aboveground Vaccinium removed plots, re-spectively. Compared with this spruce germina-tion was 27% in plots that received humus re-moval treatment. Two phenolic compounds,caffeic and p-coumaric acids, were found in ratherhigh quantities, 1.7 × 10–3 M and 0.02 × 10–3 M,respectively, in the humus. Pure compounds ofboth the phenolic acids were strongly inhibitoryto germination and primary root growth of Nor-way spruce (Mallik and Pellissier, 2000). A highconcentration of phenolic acids in the humus layerof this forest has been suggested as a cause ofNorway spruce regeneration failure.

Similarly, natural regeneration failure of Scotspine as well as Norway spruce has been reportedfrom northern Sweden after clearcutting and thedominance of cowberry in post-harvest habitats inthe absence of natural fire has been attributed to theconifer regeneration failure (Sarvas, 1950; Zackrissonet al., 1996). A phenolic derivative batatasin III(3,3–dihydroxy-5-methoxy-dihydrostilbene) hasbeen found in high concentration in the forest floorhumus and also in leaf hair glands of crowberry

(Oden et al., 1992; Wallstedt, 1998). This com-pound has been found in water leachate of humusthat inhibited seed germination and seedling growthof the conifers (Zackrisson and Nilsson, 1992;Nilsson, 1992; Gallet et al., 1999). An increase inbatatasin with an increasing abundance of crow-berry after clearcutting and seasonal variation inconcentration of batatasin has been found to bepositively correlated with the poor seedling regen-eration of the conifers (Nilsson et al., 1998).

Jalal and Read (1983a,b) isolated and identi-fied a number of phyto- and fungitoxic compoundsand determined their seasonal concentrations fromCalluna humus. They argued that these compoundsmay directly interfere with the root growth ofspruce. Hobbs (1984) tested the chemical interac-tions among heathland ericaceous plants by usingwater leachates of plant shoots and plant-soilmonoliths in seed germination bioassays. He usedseeds of several common heathland plants as wellas oat (Aven fatua L.) as a standard germinationbioassay material. Growth of Descampsia flexuosa(L.) Trin. was strongly inhibited by the leachateof Calluna. However, Arctostaphylos uva-ursi (L.)Sprengel. produced the greatest number of inhibi-tory effects, including a strong inhibition of itsown seedling. The objective of this study did notinclude testing the tree species response to allelo-pathic effects of Calluna. The standard bioassaywith oat does not necessarily provide any directevidence of chemical interaction between treespecies such as Sitka spruce and Calluna (Inderjitand Dakshini, 1995). Several authors have re-ported on the acidifying effect of Calluna litter(Gimingham, 1960; Wilson, 1960; Grubb et al.,1969). They found strong correlations betweensize of Calluna bushes and soil pH underneaththem as well as distance from the center of thebush and soil pH. It can be argued that vegetationchanges associated with the spread of Callunamay be attributed at least partly to the increasingacidity and associated soil changes (Gimingham,1972). Webley et al. (1952) reported marked in-creases in soil fungi and large reductions in soilbacteria from a fixed Ammophila sand dune to aCalluna-dominated dune.

Boreal and sub-alpine conifers such as blackspruce, Norway spruce, jack pine, Scots pine, andred pine rely on seed regeneration and for that

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they require appropriate seedbed. While the pres-ence of thick humus interferes with the seedlingregeneration of conifers, the ericaceous plants dojust fine because their principal mode of regen-eration is by resprouting and extension of vegeta-tive organs (rhizomatous growth) that traversethrough the humus layer (Mallik, 1993; Mallikand Roberts, 1994).

Seedbed quality plays a vital role in the natu-ral regeneration of conifers. If the seedbed sub-strate is not conducive to seed germination andseedling establishment, then natural regenera-tion cannot occur. The suitability of seedbed is afunction of the physical and chemical nature ofthe seedbed substratum (Prescott et al., 1996).Mineral soil seedbed facilitates successful natu-ral regeneration. In boreal ecosystem severe firecreates such conditions by consuming the thickhumus layer and exposing the mineral soil(Bloom, 2001; Mallik and Roberts, 1994). In theabsence of such a disturbance, the seedbed re-mains inhospitable for conifer regeneration be-cause of the adverse physical and chemical na-ture of the accumulated humus. The post-loggingor lightly burned (charred humus) or insect-de-foliated forest seedbed consists of thick humusoriginating from the partially decomposed litterof the canopy trees and understory plants that isoften rich in germination and growth-inhibitoryallelochemicals (Pellissier, 1993; Gallet andPellissier, 1997; Zackrisson and Nilsson, 1992;Mallik and Newton, 1988; de Montigny 1992;Zhu and Mallik, 1994). Periodic fires removethese compounds by consuming the forest floorhumus. Thermal decomposition of the humusalso release nutrients, break down allelochemicalsand any remaining allelochemicals get adsorbedin charcoal (Zackrisson et al., 1996). The currentmethod of forest management by fire suppres-sion and clearcut logging creates a shift in domi-nance of keystone species by restricting the cre-ation of favorable mineral soil seedbed for coniferregeneration. On the other hand, it allows theprolific growth of understory ericaceous shrubsthat regenerate vegetatively (Mallik, 1993). Innutrient-poor sites the conifer-ericaceous com-munities thus transform into ericaceous heathfollowing clearcut logging and nonsevere fires(Mallik, 1994, 1995).

V. KEYSTONE SPECIES SHIFT ANDRETROGRESSIVE SUCCESSION

In the absence natural regeneration of coniferssuch as black spruce, Norway spruce, red pine,jack pine, western hemlock, or western red cedar(the canopy keystone species), the vigorously grow-ing understory ericaceous species such as Calluna,Vaccinium, Kalmia, Empetrum, or salal assume therole of new keystone species and the multilayeredforest structure is replaced by a relatively uniformlow growing heath community (Mallik, 1995;Bloom, 2001). The rapid vegetative growth of theericaceous plants following tree canopy removalby logging and nonsevere forest fire large amountsof above- and belowground biomass (humus) thatare chemically different from that of the conifers.The ‘afterlife effects’ (Wardle et al., 1997) of theericaceous litter makes the soil even more acidic,their phenolic allelochemicals bind N in protein-phenol complexes, and thus the habitat becomeseven more deficient in available N (Bending andRead, 1996a,b; Prescott et al., 1996; Mallik, 2001).In the presence of a large array of phenolic acidsthe metallic cations such as Fe, Al, Ca, Zn, and Mnprecipitate to the lower soil horizon and form ahard iron pan and change the soil-plant-water rela-tion. With the rapid build up of acidic humus anda high rate of paludification, occupancy of theericaceous community brings about long-termchange in the habitat that is less and less suitablefor conifer regeneration (Gimingham, 1960; Wil-son, 1960; Grubb et al., 1969; Damman, 19711975; Meades 1983, 1986; Siren, 1955; Uggla,1958; Steijlen and Zackrisson, 1987; Zackrisson,1977; Bradshaw and Zackrisson, 1990). Ericaceousplants such as Kalmia, Vaccinium, and Empetrumthus act as ecosystem engineers. With their autoge-nic properties they bring about allogenic habitatchanges (Lawton and Jones, 1995).

VI. ORGANISMS AS ECOSYSTEMENGINEERS

According to Lawton and Jones (1995), ‘eco-system engineers are organisms that directly orindirectly modulate the availability of resources(other than themselves) to other species by physi-

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cal state changes in biotic and or abiotic material’.In the process the ecosystem engineers, ‘create,modify and maintain habitats’ (Lawton and Jones,1995). The authors classified the ecosystem engi-neers into (1) autogenic engineers that ‘changethe environment via their own physical struc-tures’, for example, dominant plants by their liv-ing and dead tissues, and (2) allogenic engineersthat ‘change the environment by transforming liv-ing or nonliving materials from one physical stateto another, via mechanical or other means’, forexample, beavers making dams that alter hydrol-ogy, sedimentation, decomposition, and nutrientcycling of the habitat and community composi-tion and diversity of plants and animals (Naimanet al., 1988). Trees can be considered the autoge-nic equivalent of beaver in the sense that a grow-ing forest modify hydrology, nutrient cycling, andnear ground micro-climate such as humidity, tem-perature, wind speed, and light (Holling, 1992).These factors create conditions and habitats forother organisms, and without these engineers mostof the other organisms would not survive. Lawtonand Jones (1995) suggest that both auto- andallogenic engineers also modulate powerful natu-ral forces such as fire, storms, and hurricanes thatfundamentally change the distribution and abun-dance of resources. Using the example of plantsas modifiers of fire behavior they argued thatspecies with differential quality and quantity ofliving and dead tissue as fuel regulate the magni-tude, duration and intensity of fire, and in turnprofoundly alter the supply of resources to otherspecies (Christensen, 1985; Dublin et al., 1990).In boreal forest high-intensity natural fires con-sume the thick humus layer of the forest floor,exposing the mineral soil seedbed necessary forsuccessful conifer regeneration. The degree ofthermal decomposition of the humus determinesthe structure and composition of the regeneratingforest by modulating the creation of conifer seed-beds. The lack of mineral soil seedbed resultingfrom mild fires or clearcutting favor vegetativelyregenerating species such as trembling aspen(Populus tremuloides Michx.), pin cherry (Prunuspensylvanica L.f.), green alder (Anlus viridis spp.Crispa (Aiton) Turril), and beaked hazel (Coryluscornuta Marsh.) (Mallik et al., 1997) instead ofthe dominant conifer species such a black spruce,

jack pine, white pine (Pinus strobes L.), and redpine (P. resinosa Ait.), causing a dramatic changein species composition (Carleton, 2000). Changesin canopy species composition bring about changesin the understory species composition and forestfloor humus property (Carleton, 2000).

VII. FIRE SUPPRESSION, LOGGING,AND KEYSTONE SPECIES SHIFT

Natural fire has been a major force in main-taining the characteristic structure and composi-tion of boreal forest (Wein and McLean, 1983;Rowe, 1983; Haapasaari, 1988; Zackrisson et al.,1995, 1996). Periodic fires remove competition,reduce allelochemicals, and release nutrients re-setting the progressive secondary succession lead-ing to forest development (Flinn and Wein, 1977;Olson, 1981; Andrea, 1991; Schimmel andGranstrom, 1996). The main objective of the cur-rent forest management practice by fire suppres-sion and clearcut harvesting in boreal forest is toensure timber production. However, this form ofmanagement does not provide the ecological ser-vices necessary for resetting the characteristicsecondary succession (Figure 1). The thick hu-mus layer that develops over time from the accu-mulated litter of the dominant canopy and under-story species is rich in germination and growthinhibitory allelochemicals that interfere with thenatural regeneration of the canopy keystone spe-cies, the conifers (Mallik and Newton, 1988; Th-ompson and Mallik, 1989; Zackrisson and Nilsson,1992; Mallik and Pellissier, 2000). Furthermore,the physical characteristics of the accumulatedhumus in the absence of periodic natural fires canact as a barrier of root establishment into themineral soil (Bloom 2001). The delicate primaryroots of the germinating seedlings in the looselypacked partially decomposed humus may becomedesiccated during periodic hot spells of summer(Mallik 1982). On the other hand, these condi-tions are favorable for the reprouting ericaceousspecies such as Calluna, Kalmia, Vaccinium, andGaultheria which survive the fire (Table 1). Allthe dominant understory species of the conifer-ericaceous communities mentioned above regen-erate mainly by stem base sprouting and rhizoma-

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tous growth (Sabhasri and Ferrel, 1960; Sabhasri,1961; Mallik and Gimingham, 1985; Andre et al.,1987; Mallik, 1993). Increased light at the under-story and warmer summer temperature at the hu-mus layer following forest canopy removal bylogging, insect defoliation, mild surface fire, andwind throw in overmature conifer-ericaceous for-ests stimulate vegetative growth of the understoryplants (Bunnell, 1990; Smith 1991; Messier, 1992;Messier and Kimmins, 1990, 1991; Huffman etal., 1994; Power, 2000). In the absence of ad-equate seed regeneration of the canopy keystonespecies the vegetatively regenerating understoryericaceous species, soon becomes the predomi-nant plant in the post-disturbance habitat and as-sumes the role of a new keystone species, whichis distinctly different in stature and chemical com-position from the conifer keystone species.

VIII. SEEDBED ALLELOPATHYPREEMPTION OF CONIFERCOMPETITION

Competition is believed to be the predomi-nant force structuring plant community. In theearly phase of secondary succession after wildfire successfully regenerating black spruce out-compete Kalmia in productive sites. However, inthe absence of high severity wild fire, inhospi-table seedbed condition created by unfavorablephysical and chemical characteristics of the hu-mus can preempt conifer competition by limitingthe natural regeneration of conifers (Bloom, 2001).It is clear from the preceding discussion that log-ging and the absence of natural fire in conifer-ericaceous communities can stimulate the growthof understory species, which can replace thecanopy keystone species by limiting their naturalregeneration (Pellissier, 1993, 1994, 1998;Zackrisson and Nilsson, 1992; Mallik, 1987,1992). In the absence of conifer regeneration thecomplex multilayered forest structure is replacedby simple ericaceous shrub-dominated heath whichfurther deteriorates the habitat by inducing changesin soil chemical ecology (Mallik, 1995; Inderjitand Mallik, 1996a,b, 1997a,b). Recent studiesindicate that even fire can create similar condi-tions of retrogressive succession from forest to

heath if it is not severe enough to burn off theericaceous humus and create a favorable seedbedfor the conifers. From a seeding experiment onthe manipulated seedbed of Kalmia–black sprucecommunity Bloom (2001) concluded that the suc-cessful fire suppression program in Terra NovaNational Park put out the fire before it became alarge and high-intensity natural fire. Consequently,it did not produce enough high-severity burn thatcould consume Kalmia humus and undergroundvegetative organs and create the mineral soil seed-bed necessary for successful black spruce regen-eration.

IX. HUMUS ALLELOCHEMICALS,DECOMPOSITION, NUTRIENT CYCLING,AND CONIFER GROWTH

Decomposition in organic soil is mediated bylitter dwelling macro- and microorganisms. Theseorganisms can decompose humus allelochemicalsand produce new allelochemicals from their de-composition products (Kaminsky, 1980; Rice,1984; Inderjit, 1996). Microorganisms are able tometabolize large amounts of phenolic compoundsrather quickly (Blum, 1998; Blum and Shafer,1988; Lockwood and Filonow, 1981; Souto et al.,1998; Inderjit et al., 1999). The amount of avail-able N and P in the polyphenol-rich litter is de-pendent on the combined effects of litter quality(Northup et al., 1995; Chapin III, 1995) and theactivity of a vast array of soil organisms and theirability to influence the carbon and nitrogen cycles(Bradley et al., 1997). Postdisturbance ericaceous-dominated forests experiencing a high rate of hu-mus accumulation and conifer regeneration fail-ure usually exhibit a deficiency of available N insoil. Based on the results of their experimentalstudies, Bradley et al. (1997) hypothesized thathigh levels of tannins in ericaceous humus chemi-cally immobilize and eventually control N avail-ability. An increase in population of nitrifyingbacteria such as Nitrosomonas and Nitrobacter(Smith et al., 1968), competition for ammoniumbetween heterotrophic microbes, plants, and nitri-fying bacteria (Robertson and Vitousek, 1981;Stienstra et al., 1994), allelopathic plant exudatesand humus decomposition products influence

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nutrient cycling (Thibault et al., 1982; Baldwin etal, 1983; Olson and Reiners, 1983; Lothi andKillingbeck, 1980; Jobidon et al., 1989a,b; seealso Pellissier and Souto, 1999 for a review).Both nitrifiers as well as other groups of soilmicroorganisms are involved in the manifestationof allelopathic effects in forest soils (Souto et al.,1994). In low pH humus fungi play a significantrole in litter decomposition. Some soil fungi arenegatively affected by soil allelochemicals,whereas others show stimulatory effects (Zhang,1997; Lindeberg et al., 1980; Souto et al., 1998).

In organic soils mycorrhizal fungi play vitalroles in the functioning of higher plants of a tem-perate region (Malloch and Malloch, 1981, 1982).Handley (1963) and Robinson (1972) demon-strated that certain conifer ectomycorrhizae werenegatively affected by Calluna root exudates.Others have found that the effect can be bothinhibitory and stimulatory, depending on theectomycorrhizae and conifer species and the typeand concentration of allelochemicals involved(Rose et al., 1983; Cote and Thaibault, 1988;Nilsson et al., 1993; Mallik and Zhu, 1995;Pellissier, 1998). The response of ectomycorrhizalfungi to allelochemicals is complex and oftenrelated to the chemical structure, chemical mix-ture, concentration, and the fungal species(Pellissier and Souto, 1999; Boufalis and Pellissier,1994; Mallik and Zhu, 1995). Andre (1994) sug-gested that high phenolic contents of a Vaccinium-dominated humus layer on the forest floor restrictthe development of mycorrhizae of Norway spruceseedlings in sub-alpine forests. Four forest floorhumus and humic solution allelochemicals, cat-echol, p-hydroacetophenone, p-hydrobenzoic acid,and protocatechuic acid of sub-alpine Norwayspruce-Vaccinium forest were found to cause asignificant reduction in the respiration of two co-nifer ectomycorrhizae, Laccaria laccata andCenococcum graniforme (Pellissier, 1993;Boufalis and Pellissier, 1994). These authors con-cluded that conifer regeneration failure observedin this forest can be explained at least partly bythe inhibitory effects of the humus allelochemicalsthat threaten the symbiotic relationship betweenthe conifer and their ectomycorrhizae.

Yamasaki et al. (1998) conducted a study inwhich they examined mycorrhizal symbiosis, plant

height, and diameter growth and foliar N of blackspruce seedlings growing in the field close to (<1 m)and away (>1 m) from Kalmia. Black spruceseedlings close to Kalmia were found to containsignificantly less mycorrhizal short roots, foliar N,plant height and diameter growth compared withthose growing further away. In a separate fieldsurvey Hong and Mallik (unpublished data) ob-served that black spruce seedlings were relativelysmall and had about 50% less mycorrhizal infec-tion in a site dominated by Kalmia compared witha contiguous non-Kalmia site.

X. ERICOID MYCORRHIZAE

Ericaceous plants are in symbiotic associa-tion with a variety of mycorrhizae that are spe-cifically adapted to nutrient-poor habitats (Read1982, 1991). Ericaceous plants produce largequantities of polyphenolic materials (e.g.tannnins, humic acids, melanins, and quinines)that can bind soil organic N as calcitrant pro-tein-phenol complexs (Tackechi and Tanaka,1987; Mole and Waterman, 1987). Bending andRead (1996a) have shown that ericoid mycor-rhizae are able to utilize protein N that iscomplexed with tannic acid by means of enzy-matic degradation, whereas ectomycorrhizalfungi associated with conifers could not obtainN from the same source. They also demon-strated that ericoid mycorrhizae can utilize tan-nin as a carbon source, a feature other mycor-rhizae do not have. Studies of these and otherauthors suggest that ericoid mycorrhizal asso-ciations may have resulted from the selectiveforce of low-available nitrogen environments(Leak and Read, 1989, 1991; Bending and Read,1996b). Largent et al. (1980) and Xiao andBerch (1992) found that roots of salal is asso-ciated with three types of mycorrhizae — eri-coid, arbutoid, and ectomycorrhizae — makingthem very efficient in obtaining N and P inacidic soils as well as capturing nutrients incomplex organic forms. Thus, ericaceous plantsseem to be much better equipped than conifers,which are typically associated with selectedectomycorrhizae for nutrient acquisition inpolyphenol-rich shrub-dominated conditions.

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XI. ECOSYSTEM-LEVEL PERSPECTIVEOF ALLELOPATHY

Very few studies in allelopathy have taken anecosystem-level perspective of the phenomenon.Citing two examples, (1) nodding thistle (Carduusnutuns) containing New Zealand pasture, and(2) cowberry (E. hermaphroditum) containingSwedish boreal forest, Wardle et al. (1998) ar-gued that secondary metabolites of these invadingspecies can cause ecosystem-level changes bynegatively influencing the regeneration of domi-nant plants that control the key ecological pro-cesses. They suggested that the concept of allel-opathy is more applicable to ecosystem-levelprocesses rather than population-level processesparticularly in the species-poor habitats where thebiogeochemical processes are controlled by one ortwo dominant plants with allelopathic property.

The accumulation of large amounts of litterin the northern environment can be explained bythe dominant plants adaptation to producepolyphenol-rich litter in a nutrient-stressed envi-ronment (del Moral, 1972; Muller et al., 1987),reduced litter decomposition due to poor litterquality, and cool and moist climatic conditions(Facelli, 1988; Facelli and Pickett, 1991; Mallik,1995). Fire adaptation and antiherbivory can alsobe considered as reasons for the production ofpolyphenol-rich litter by the dominant plants inthis ecosystem (Rice, 1979; Williamson andBlack, 1981; Coley, 1988; Coley et al., 1985).The subtle changes of ecosystem are continuallybeing brought about by the secondary compoundsof living and dead remains of the dominant plantsand that influence the biotic and abiotic pro-cesses of the ecosystem. However, so far, ourresearch efforts in allelopathy have been almostexclusively directed toward the more dramaticeffects of plant secondary compounds on theneighboring plants at the individual and popula-tion levels. We must focus our attention on thestudy of a broader landscape-level perspectiveof ecosystem disturbance and allelopathy. Weneed to study the combined effects of many subtlephysical and biochemical changes involvingallelochemicals at a range of temporal and spa-tial scales.

XII. CONSEQUENCE OF FIRESUPPRESSION AND CLEARCUTTING

Boreal forests of the northern hemispherehave evolved in the presence of periodic naturaldisturbances such as fire and insect outbreaks,and coniferous stands in boreal forests owe theirorigin to these natural disturbances (Attiwill,1988). It appears that the periodic removal offorest floor humus by wild fires is a preconditionfor rejuvenating forest communities by creatingthe necessary conditions for the keystone spe-cies regeneration and resetting the secondarysuccession. The removal of forest floor humusrequires hot fire or slow but high-intensity smol-dering combustion that can consume the humusalong with the underground perennating struc-tures of the ericaceous plants. This ensures themuch-needed mineral soil seedbed for success-ful conifer regeneration as well as the relativelycompetition-free and allelochemical-free initialstage of progressive secondary succession. Therate and degree of biotic and abiotic changes aredependent on the type of canopy tree, the domi-nant understory plant, soil type, nutrient, pH,and climatic condition. For example, mild firesor clearcutting or heavy spruce budworm defo-liation in nutrient-poor black spruce–Kalmia orbalsam fir (Abies balsamea (L.) Mill.)–Kalmiaforest can convert the forest community intoKalmia heath, and it can last for a very longtime. Scattered black spruce establishment mayoccur over a long period of time (70 to 100years) in the patchy mineral soil-exposed seed-beds. Layering regeneration of these isolatedblack spruce may develop into a wood savannahcommunity as observed in some parts of TerraNova National Park, Newfoundland. If, on theother hand, the understory is predominantly La-brador tea (L. groenlandicum), then the growthinhibition of planted black spruce may last foronly 6 to 10 years, and after that black sprucemay regain the canopy dominance (Inderjit andMallik, 1996a). Similarly, the growth inhibitionof salal on Sitka spruce or western hemlock maylast for 10 to 15 years (depending on the sitefertility), and after that the conifers can resumegrowth and shade out the ericaceous understory.

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XIII. A GENERALIZED MODEL OFCONIFER GROWTH INHIBITION

Figure 2 summarizes the dynamics of coni-fer-ericaceous interactions where competition,allelopathy, and nutrient sequestration all play arole in creating unfavorable conditions for coniferregeneration. The degree and mechanism of coni-fer growth inhibition often depend on the site typeand the ericaceous species involved. For example,natural regeneration failure of Norway spruce inthe presence of bilberry (V. myrtilus) is mainlydue to the germination inhibition of the spruceunder a Vaccinium canopy (Pellissier, 1993, 1994;Mallik and Pellissier, 2000), whereas black spruceregeneration in the presence of Kalmia is causednot so much by germination inhibition but by root

growth inhibition, competition, and nutrient defi-ciency (Mallik, 1987, 1992; Mallik and Newton,1988). Salal-induced conifer growth inhibition inthe west coast of British Columbia is mostly dueto competition for nutrients and light and allel-opathy seems to play a relatively minor role(Messier and Kimmins, 1990; Messier, 1993; deMontigny, 1992; Prescott and Weetman, 1994;Weetman et al., 1989a,b, 1990; Mallik andPrescott, 2001). The time required for canopyclosure after forest harvesting and fire also de-pends on the site type, climatic conditions, thespecies of ericaceous plant, and the associatedconifer involved. For example, certain nutrient-poor Kalmia–black spruce sites in central New-foundland may require 150 to 200 years to achieveforest canopy closure (some sites may not achieve

FIGURE 2. Conifer growth inhibition resulting from the combined effects aggressive vegetative regenerationstrategies and competitive ability, allelopathy, and nutrient sequestration of the ericaceous plants (Modified fromMallik, 1998 and reproduced with permission from Kluwer Academic Publishers.)

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canopy closure at all, instead form open canopywood savannah vegetation), whereas a poor-qual-ity salal-hemlock site may require less than 50years to develop canopy closure. In the case ofKalmia-induced regeneration failure of blackspruce in Newfoundland, Mallik (1995) suggestedthat the extent of regeneration failure is deter-mined by the combined effects of many factors,such as climate, soil fertility, vegetation compo-sition, type, frequency and intensity of forest dis-turbance, and the resiliency to disturbance, regen-eration strategies, competitive abilities, andallelopathic property of Kalmia. Similarly, Messierand Kimmins (1991) and Prescott and Weetman(1996) suggested that competition for nutrientsand declining site fertility after the assart flush arethe major reasons for Sitka spruce, western hem-lock, and western red cedar growth check in youngplantations with salal. In addition to allelopathyof crowberry (Empetrum hermaphroditum) onSitka spruce (Zackrission and Nilsson 1992;Nilsson, 1994), Zackrisson et al. (1997) demon-strated a three-way interaction between conifers,ericaceous plants, and feather moss in immobiliz-ing nutrients that may cause growth inhibition inconifers in northern Sweden.

XIV. LAND MANAGEMENT IMPLICATIONS

Depending on the land management objec-tive, the resource manager aims to enhance thedevelopment of a desirable keystone species atthe cost of another. For example, in the case offorest development with ericaceous understorythe management objective would be to control theunderstory plants after harvesting and enhancenatural regeneration or growth of planted conifersso that the conifers become the keystone species.However, if the land management objective is tomaintain a productive ericaceous heathland forherbivore production, recreation, tourism, andcultural landscape as is the case of heathlands inBritain and Western Europe then the maintenanceof ericaceous plants as keystone species is a vitalnecessity. The value of conservation of a widerange of Calluna heathlands as distinct vegetationtypes has been recognized by many ecologists inWestern Europe (Malmer, 1965; Westhoff 1961;

Froment, 1975; Gimingham et al., 1979;Gimingham, 1980, 1981; Gimingham and deSmidt, 1983). Organizations such as the NatureConservancy Council and the Countryside Com-mission in Britain have been working toward theprotection and maintenance of certain heathlandsas natural areas (Gimingham, 1981; Hobbs andGimingham, 1987). Uniform and productiveCalluna has significant economic importance asgrazing land for game birds, sheep, and cattle.Landowners in the highlands of Scotland manageCalluna heathlands by regular burning to main-tain a healthy red grouse (Lagopus lagopusscoticus L. (Lath.)) population for revenue gen-eration. This is done by prescribed burning heatherevery 12 to 15 years so that the heathland plantscan regenerate rapidly by vegetative means, andthe regular burning kills any tree seedling inva-sion (Gimingham, 1972; Khoon and Gimingham1984; Mallik and Gimingham, 1985).

The major forest management objective afterharvesting boreal and sub-alpine spruce forest isto control the spread of ericaceous plants andenhance natural regeneration or growth of plantedconifers so that the conifers remain the keystonespecies. It is clear that forest harvesting byclearcutting as well as selective cutting enhanceericaceous dominance in the post-harvest habitatif such plants are present in the understorey andthey affect forest productivity (de Montigny andWeetman, 1989). Logging in stands that havepotential for converting the forest into ericaceousheath should be avoided unless practical methodsare in place for (1) controlling the spread of eri-caceous plants, and (2) enhancing the regenera-tion of conifers. In medium- to poor-quality sitetypes infested with Kalmia successful conifer re-generation is not possible without the removal ofericaceous dominance. In nutrient-rich sites, how-ever, healthy growth of conifers may outcompetethe ericaceous plants. The reclamation of Callunaheathland for forest regeneration is done by plow-ing, liming, and repeated fertilization, which re-duce Calluna growth and enhance the growth ofplanted conifers (Gimingham, 1972). However,so far, the success of controlling Kalmia growthin post-harvest/post-burn habitats in easternCanada has been limited. None of the commonlyused silvicultural methods, such as scarification,

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ploughing, herbicide treatment, or prescribed burn-ing, proved to be successful (Richardson, 1979;Mallik and Inderjit, 2001). A forest research re-port from Nova Scotia claimed that glyphosate(Vision) applied at the rate of 1.12 to 3.36 kg a.i./haprovided effective control of Kalmia and blue-berry (Vaccinium angustifolium) in the first andsecond year after treatment, but the degree ofcontrol at the end of the third year was reduced atthe lower concentration of the herbicide (Anon.,1988). In a greenhouse experiment Mallik andInderjit (2001) tested the efficacy of glyphosate(3.36 kg/ha), triclopyre (4 kg/ha), fosamine am-monium (2.5 kg/ha), and hexazinone (2.2 and 5.0kg/ha) on Kalmia control and found that of all thetreatments triclopyre was the most effective incontrolling the plants by killing its above- andbelowground components. A field trial conductedin central Newfoundland in early July and lateAugust with glyphosate and triclopyr (both at therate of 2.88 kg a.i/ha) with and without Sylgardsurfactant (1.5 L/ha) indicated that the Augustapplication of glyphosate with Sylgard was ableto kill Kalmia (Titus and English, 1996). How-ever, because Sylgard had damaging effects onblack spruce, this treatment was suggested as asite preparation treatment only and not as a silvi-cultural conifer release treatment. Glyphosate canhave a significant impact on the metabolism ofphenolic and other secondary compounds (Dukeand Hoagland, 1978; Hoagland et al., 1979; Lydonand Duke, 1988, 1989). More research is neededto study the levels of phenolic compounds inKalmia plants treated with glyphosate. Jobidon(1991) reported that bialaphos, a microbiallysynthesised herbicide applied at the rate of 1 to2.5 kg a.i /ha, gave effective control of Kalmia.Jobidon and Margolis (1994) reported on the dif-ferential tolerance of conifer species to bialaphosshowing that August application at or below 2.0 kgai/ha have no damaging effect on conifers. Theysuggested that bialaphos has a strong potential asan altenative to chemically synthesized herbicidesfor vegetation management. Bialaphos, however,is not registered in Canada.

An experiment with transplanted Kalmiashowed that mulching may be effective in con-trolling Kalmia (Mallik, 1991). However, thereare practical limitations in applying mulching treat-

ments for its high costs as well as the challenge ofoperating mulching equipment in shallow androcky soils. Nonetheless, it has some potential increating forest regeneration nuclei among Kalmiaheath, where all other techniques fail. The appli-cation of N, P, and K fertilizers to enhance thegrowth of black spruce planted in Kalmia indi-cated that most of the added nutrients are ab-sorbed by Kalmia, which makes the plant groweven more vigorous with limited benefits to blackspruce growth (Mallik, 1996). On the other hand,on a relatively dry jack pine site high doses of Napplication (672 and 1344 kg/ha) were reportedto reduce Kalmia abundance and enhance jackpine growth (Prescott et al., 1995).

Preinoculation of black spruce with certainectomycorrhiza such as Paxillus involutus(Bat.:Fr.), Laccaria laccata (Scop. : Fr.) Berk. etBr., and E-strain has potential for overcoming theconifer growth inhibition in the presence of Kalmia(Mallik et al., 1998). The reason for this growthstimulation in the inoculated seedlings is basedon the fact that conifer ectomycorrhizae such asP. involutus, L. laccata, and L. bicolour has beenfound to degrade Kalmia phenolics such aso-hydroxyphenylacetic, o-coumaric, and ferulicacid and use them as their carbon source (R-S.Zeng and A.U. Mallik, unpublished). It is impor-tant to note, however, that in order to be effectivethe mycorrhizae of the preinoculated seedlingswill have to compete with the existing microbialcommunity of the Kalmia rhizosphere. The nutri-ent loading of conifer seedlings before plantingmay provide another opportunity to enhance co-nifer growth in the presence of the ericaceousplants. It is based on the premise that the highnutrient reserve of the nutrient loaded seedlingswill have a head-start in the nutrient-limited envi-ronment of ericaceous heath (Timmer and Munson,1991). Field trials with mycorrhiza (P. involutus)-inoculated black spruce seedlings in the presenceof Kalmia are underway.

Bunnell (1990) suggested that prescribedburning immediately after forest harvesting mayreduce salal growth and thus would enhance thegrowth of planted conifers. A field trial with burn-ing and Garlon 4E herbicide treatments was ableto reduce salal cover, but the plants gained domi-nance by vegetative regrowth in the second and

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third year (J. Baker, personal communication).Messier and Kimmins (1990, 1992) reported arapid increase of above- and below-ground biom-ass of competing vegetation (mainly salal) be-tween 2 and 8 years after clearcutting and slashburning. Planted conifers in these post-disturbedsalal dominated habitats experienced growth checkwith foliar N and P deficiencies. They found thecontinuous removal of salal for three growingseasons increased the availability of N and P inresin bags. Height growth of planted conifers canbe temporarily improved by a single applicationfertilizer (300 kg/ha N and 100 kg/ha P) but tosustain the sapling growth multiple application ofthe fertilizer is necessary as observed in Callunaheathland afforestation (Gimingham, 1972). Op-erational fertilization treatments with N and P(300 and 100 kg/ha, respectively) has been foundto significantly increase conifer growth in theorder of Sitka spruce> western hemlock> westernred cedar in the presence of salal and has beenrecommended to overcome the conifer growthcheck (Thompson and Weetman, 1992b; Prescottet al., 1996; Chang et al., 1996a,b, 1999). How-ever, in Ontario herbicide use in forestry has beencriticized by the public on the grounds of adverseeffects on wildlife and human health (Wagner etal., 1998). In the case of sub-alpine spruce forestin France fertilization and herbicide use for forestmanagement is forbidden on the grounds that vil-lagers in the valley rely on the watershed for theirdrinking water (F. Pellissier, personal communi-cation).

The above discussion signifies the challenges incontrolling the ericaceous plants after forest harvest-ing and reestablishing the conifer keystone species.More research is needed to understand the vegeta-tion dynamics and soil processes in the presence ofericaceous plants in order to develop ecologicallysustainable and environmentally acceptable meth-ods to regain the desirable keystone species.

XV. CONCLUSIONS

Allelopathic phenomenon can be better appre-ciated at the ecosystem level by taking into accountthe predominant biotic and abiotic processes influ-enced by plant litter of keystone species.

Disturbance-induced vegetation shift from forestto ericaceous heath with rapid humus accumula-tion and subsequent habitat degradation can bearticulated by linking the concept of keystone spe-cies and their role as ecosystem engineers with theconcept of alternative stable states of community.The approach is described by using examples ofconifer regeneration failure in the presence of eri-caceous plants in boreal and sub-alpine temperateforests. The change of keystone species followingecosystem disturbance results from a combinedeffect of biotic processes such as competition, spe-cies regeneration strategies that influence produc-tivity, and litter accumulation, which in turn con-trol the rate and direction of habitat changes andsuccession. To understand the mechanism(s) ofcommunity structuring following disturbance, wemust identify the major biotic and abiotic eventsand their roles in ecosystem function. In most casesa combination of factors working at the ecosystemlevel can be identified as the cause of such vegeta-tion change. In the present examples these were (1)the absence of high-severity natural fire and limi-tation of conifer seedbed, (2) rapid vegetative re-generation of understory ericaceous plants afterforest canopy disturbance, and (3) habitat degrada-tion by phenolic allelochemicals of ericaceous plantscausing allelopathy, soil nutrient imbalance, ironpan formation, and the removal of natural conifermycorrhizal inocula.

ACKNOWLEDGMENTS

The research was supported by a discoverygrant from the Natural Science and EngineeringResearch Council (NSERC) of Canada. The ar-ticle was benefited from the comments and edito-rial suggestions of the external reviewer and Drs.Jian Wang and Tom Hazenberg of the Faculty ofForestry and the Forest Environment. The authorappreciates the invitation to contribute to thisspecial issue of the journal on allelopathy.

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