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Understory vegetation as a forest ecosystem driver M-C Nilsson and DA Ward

myrtillus), lingonberry (Vaccinium vitis-idaea), and blackcrowberry (Empetrum hermaphroditum; Figure 1). Themoss layer is dominated by feather moss (Pleuroziumschreberi) and stair-step moss (Hylocomium splendens),

while the lichen component consists mostly ofCladina orCladonia. The dominant tree species are Norway spruce(Picea abies), Scots pine (Pinus sylvestris), and birches(Betula pubescens and Betula pendula). The relative abun-dance of all of these species is determined by a range ofabiotic and biotic factors that are in turn frequently dri-ven by the successional stage of the ecosystem.

The main ecological determinant of successional stageis wildfire induced by lightning strike, and the majority ofthese forests are affected by recurrent fires (Zackrisson1977; Niklasson and Granstrm 2000). Typically, with

increasing time since fire disturbance (or with increasinfire-return interval), the dwarf shrub layer changes frombeing dominated by lingonberry and bilberry to beindominated by black crowberry (Sirn 1955; Wardle et a1997) and increasing biomass of feather mosses (DeLucet al. 2002a). In the absence of competition from dwarshrubs and feather mosses, it is common for the ground tbe covered by reindeer lichens; this often occurs in nutrient-poor conditions and sometimes in early succession. Ithe prolonged absence of fire disturbance, replacement olingonberry and bilberry by black crowberry is accompanied by an ecosystem retrogression or decline phas

(Wardle et al. 2004) that also involves reductions in trebiomass and productivity, and changes to several belowground properties (Table 1).

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Figure 1. The three most abundant ericaceous dwarf shruspecies in the Swedish boreal forest: (a) bilberry (Vacciniummyrtillus); (b) lingonberry (Vaccinium vitis-idaea); and (cblack crowberry (Empetrum hermaphroditum).

(a)

(b)

(c)

Table 1. Retrogressive successional trends in above-ground and belowground properties that occur in theprolonged absence of fire in the Swedish boreal forest

Response variable Trend

Aboveground Abundance of bilberry and lingonberry I

properties Abundance of black crowberry I

Tree biomass and productivity I

Ratio of ericaceous shrub biomass to

tree biomass I

Feather moss abundance IBelowground Polyphenol concentration in soil I

properties Decomposer microbial biomass `

Litter decomposition rate `

Soil carbon sequestration I

N mineralization rate I

Mineral N concentration I

Ratio of mineral N to dissolved organic N I

Symbiotic N fixation in mosses ISources of information are Zackrisson et al. 1996,2004; Wardle et al. 1997,2003a;andDeLuca et al. 2002a. Upward arrows indicate an increasing trend over time; downwardarrows indicate a decreasing trend.


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M-C Nilsson and DA Wardle Understory vegetation as a forest ecosystem driver

Understory vegetation effects on associated

organisms

Relatively little research has been carried out on theeffects of understory dwarf shrubs and mosses on treeseedlings in boreal forests, probably because these under-story components represent a relatively small proportionof the total forest plant biomass (Figure 2). Although

these components are unlikely to contribute much interms of mass effects, their biomass turns over much morerapidly than does that of the trees with which they co-exist; measurements of shrub productivity reveal that theproportion of standing shrub biomass that is replaced eachyear is around 62% for bilberry, 39% for lingonberry and29% for black crowberry (Wardle and Zackrisson 2005).As such, the aboveground net primary productivity ofthese shrubs is over half that of the trees (Figure 2). Innorthern Sweden, the standing biomass of the moss com-ponent is comparable to that of the shrubs (Wardle et al.1997). Although no estimates have been made of theirnet primary productivity (NPP) in northern Sweden,

turnover rates of moss segments in Scandinavian borealforests are rapid and probably comparable to that of theshrubs (kland and kland 1996). Work in Alaskanboreal forests also points to the high NPP of mosses rela-tive to that of associated trees (Oechel and van Cleve1986; Harden et al. 1997; Turetsky 2003). Therefore,despite the relatively low contribution of understory vege-tation to total standing biomass, their high turnover ratesuggests that they produce a substantial proportion of theannual litterfall that is returned to the soil, and contributesubstantially to total annual ecosystem nutrient uptake.As such, they have the potential to exert important inter-ference effects against tree establishment and growth.

Of the understory components in northern Swedishboreal forests, the one that arguably has the strongestnegative effect on tree seedling establishment and growthis black crowberry. Experimental field studies have shownthat seed germination and seedling growth are vastlyreduced under black crowberry as compared to otherunderstory vegetation types (Zackrisson et al. 1995, 1997;

Nilsson et al. 2000), and increasing densities of blackcrowberry across space and time are frequently associatedwith reduced forest tree stand productivity (Zackrisson etal. 1996; DeLuca et al. 2002a; Wardle et al. 2003a). This islikely to be the result of allelopathic rather than compet-itive effects of black crowberry. This species produces

very high concentrations of a phenolic compound,batatasin-III (Odn et al. 1992), that has been shown toreduce germination and growth of seedlings when appliedat the concentrations in which it occurs in the soil(Nilsson et al. 2000; Wallstedt et al. 2005).

While the issue of allelopathic effects in real ecosys-tems has generated controversy (Williamson 1990), it hasbeen shown that negative effects of black crowberry ontree seedlings are largely mitigated in field plots whenactivated C (which adsorbs polyphenolic compoundsthrough electrostatic charges) is added to them (Nilsson

and Zackrisson 1992; Nilsson 1994; Nilsson et al. 2000).Charcoal produced during wildfires, which operates as aform of activated C, may also minimize the effects ofbatatasin-III on tree seedlings (Panel 1). Allelopathiceffects, similar to those described here for black crow-berry, might also occur in other forests in which erica-ceous shrubs form a major part of the understory, such as

has been shown for sheep laurel (Kalmia angustifolia) inCanadian temperate and boreal forests (Mallik 2003;Thiffault et al. 2004).

The interference effects of black crowberry are not justrestricted to tree seedlings. For example, ectomycorrhizalfungi may also be impaired by black crowberry (Nilsson etal. 1993), and humus under black crowberry supports con-siderably lower levels of decomposer microbes and faunathan humus under other understory types (Wardle et al.1998a). Furthermore, because of its water-soluble natureand persistence (Wallstedt et al. 2005), batatasin-III

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The Ecological Society of America www.frontiersinecology.org

trees shrubs mosses

Unproductive systemtrees shrubs mosses

Productive system

trees shrubs

Unproductive system

trees shrubs

Productive system

10

5

0

200

100

0

Biomass(kgm2)

AbovegroundNPP(gm2

yr1)

(a)

(b)

(c)

Figure 2. Productivity and biomass of understory componentsrelative to that of trees. (a) Trees are the dominant biomass

component of the Swedish boreal forest but shrubs and mossesdensely cover the ground surface; (b) and (c) biomass andaboveground NPP of trees and understory components on

productive and unproductive lake islands in Lapland, Sweden.Data from Wardle et al. 1997, 2003a.


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leaches into nearby waterways during snowmelt, and con-centrates in small streams and ponds (Brnns et al.

2004). Short-term experimental studies have shown thatlethal effects on trout alevins and reduced mobility ofwater fleas (Daphnia spp) were caused by batatasin-III butnot by a simpler phenolic compound (Brnns et al.2004), thus confirming the specific toxic effect of thebibenzyl structure of batatasin-III (cf. Nilsson et al. 2000).

Other understory components in Swedish boreal forestsalso influence tree seedling regeneration and growth,although the effects are usually not as strong. For exam-ple, manipulative field experiments investigating exclu-sion of bilberry have shown this species to exert negativeeffects on Norway spruce seedlings, although below-ground resource competition rather than allelopathy was

probably the mechanism involved (Jderlund et al. 1997).Reindeer lichens do not show negative effects on treeseedlings, and seedlings planted into ground dominatedby lichens show vastly superior growth to those plantedwithin other ground-layer vegetation (Steijlen et al.1995; Zackrisson et al. 1995). Meanwhile, seedlingsplanted into dense feather moss layers typically establishand grow very poorly, despite the ability of mosses toretain moisture (Steijlen et al. 1995). There is evidencethat this adverse effect of mosses is because they are veryeffective in absorbing available nutrients (Oechel and

van Cleve 1986; Zackrisson et al. 1999) and because mycorrhizal hyphae produced by ericaceous shrubs directltake up nutrients from recently dead moss tissue, beforthe tree seedlings are able to access them (Zackrisson eal. 1997). This mechanism may also interfere to a lesseextent with the growth of previously established, largeseedlings and trees, because although their root system

can access nutrients below the depth of mosses and shruroots, the mossshrub layer is able to increasingly immobilize available nutrients over time (Wardle et al. 1997Zackrisson et al. 1999; DeLuca et al. 2002a). Note that thabove mechanisms differ from that described by Carletoand Read (1991) for Canadian boreal forest species, iwhich tree seedling mycorrhizae were able to directlaccess nutrients from mosses.

Belowground effects of understory vegetation

The three dominant dwarf shrub species in the Swedisboreal forest differ markedly in their ecophysiologica

attributes. Bilberry has short-lived leaves, grows relativelrapidly, and has poorly defended tissues (ie with low leveof active secondary metabolites), while black crowberrproduces long-lived leaves, usually grows slowly, and hawell defended tissues. The attributes of lingonberry arintermediate between these two. Consistent with thesspecies-specific differences, black crowberry produces poorquality litter compared to that produced by the othespecies. Litterbag studies have shown that black crowberrlitter decomposes more slowly and releases less nitrogen (Nduring decomposition than co-existing ericaceous shruspecies (Wardle et al. 2003a,b) and most tree specie(Wardle et al. 2003a). Furthermore, a litter-mixing study, i

which litter from ten over- and understory boreal foresspecies were mixed in all two-way combinations, generallpointed to black crowberry litter as having the strongesnegative effects out of all species on litter decompositionrates of associated litter (Wardle et al. 2003b). These belowground effects of black crowberry may impair nutrient supply rates from the soil and contribute to the adverse effectof this species on seedling growth (Nilsson et al. 1999).

The likely ecosystem-level consequences of dwarf shruspecies are apparent from a study that has been operatinfor the past 10 years on a series of forested lake islands inorthern Sweden (Wardle et al. 1997, 2003a; Wardle anZackrisson 2005). These islands represent a retrogressiv

succession, with different islands representing differenperiods of time since last burning. With increasing timsince the most recent fire disturbance, early successionaspecies such as bilberry and Scots pine are replaced blater successional species such as black crowberry an

Norway spruce. Domination by black crowberry on thesislands is associated with high concentrations of polyphenolic compounds in the humus, and this in turn appearto contribute to reduced soil microbial activity, lowedecomposition rates, reduced availability of soil Nincreased soil C sequestration and, ultimately, reduce

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Panel 1. Ecological impacts of charcoal from wildfire

Activated carbon contains electrostatically charged surfaces thatadsorb compounds with polar molecules such as phenolics.Addition of activated C to soil supporting plants that producethese compounds has been shown to reduce their negativeeffect on associated plant species (Nilsson and Zackrisson 1992;Nilsson 1994; Callaway and Aschehoug 2000).Wildfire produces

charcoal, which is a form of activated C, and forest soils innorthern Sweden typically contain between 900 and 2100 kg ha -1

of charcoal (Zackrisson et al. 1996). Charcoal collected fromsites that have recently burnt has been shown to remove thephenolic batatasin-III (produced by black crowberry) from aque-ous solutions, and to promote emergence and growth of treeseedlings treated with these solutions (Zackrisson et al. 1996).Charcoal from older fires does not have the same effectsbecause there is increased physical obstruction over time of thecharcoal surface. Furthermore, addition of charcoal to the soilsurface at levels known to occur in the field has been shown tostrongly stimulate birch seedling productivity and nutrient acqui-sition for soil collected from under black crowberry (presum-ably because of its adsorption of batatasin-III), but not for soilcollected from under other ground-cover species (Wardle et al.1998b).The surfaces of fresh charcoal also support high levels of

microbial biomass and activity (Zackrisson et al. 1996; Pieti-kinen et al. 2000) and can support greater rates of ecosystemlevel processes driven by components of the soil microflora,such as decomposition and nitrification (Zackrisson et al. 1996;Wardle et al. 1998b; Pietikinen et al. 2000;DeLuca et al. 2002b).It has been suggested that the increased dominance of blackcrowberry, and associated diminished activity of charcoal withincreasing time since burning, contributes to diminished foresttree productivity and biomass, as well as reducing the rates ofthose soil processes that promote nutrient supplies available toplants (Zackrisson et al. 1996).


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aboveground tree and shrub productivity(Wardle et al. 1997, 2003a). Ongoing manipula-tive experiments, established in 1996, haveinvolved repeated experimental removals of allpossible components of the three dwarf shrubspecies on plots across each of 30 islands, repre-senting a wide gradient of time since burning

(Wardle and Zackrisson 2005). These show thatthe bilberry and lingonberry have strong posi-tive effects on litter decomposition, soil micro-bial activity, and depletion of soil mineral N,while black crowberry does not. Bilberry andlingonberry dominate the understory on earlysuccessional rather than late successionalislands, and when they are experimentallyremoved from plots, the relationship betweenisland successional stage and decomposer prop-erties disappears. This suggests that the rela-tionship between successional stage and decom-poser activity is driven entirely by the types of

ericaceous dwarf shrubs that are present.Feather mosses produce litter that decom-

poses slowly, and it has been shown that therate of mass loss and N release from this litter isusually slower than that of the trees and dwarfshrubs with which they co-exist (Wardle et al.2003b). This often results in a thick layer ofmoss litter forming below the live moss portionsand above the humus surface. This layer of litteris important in retaining moisture and, unlikethe litter of black crowberry, it accelerates thedecomposition rates of associated litters fromvascular plant species (Wardle et al. 2003b). In

North American boreal forests, the understorymosses have also been found to have importanteffects, buffering soils against temperaturechanges by increasing surface insulation and reducingincident sunlight, thereby potentially retarding litterdecomposition rates (Oechel and Van Cleve 1986;Bonan 1991). It has also recently been shown thatfeather mosses play a fundamental role in regulatingecosystem N input, because the live segments containhigh densities of cyanobacteria that fix atmospheric Ninto forms available to plants (DeLuca et al. 2002b; Figure3). The quantities of N fixed are sufficient to account forbuild up of organic N in the soil during succession

(DeLuca et al. 2002b), and this fixation is greater in latesuccessional than in early successional boreal forests(Zackrisson et al. 2004). Although this mechanism isundoubtedly important in maintaining the N capital ofthe ecosystem, how and when this N is transferred to co-existing dwarf shrubs and trees has yet to be elucidated.

Reindeer lichens produce litter that decomposes moreslowly than that of most of the vascular plant species withwhich they co-exist (Wardle et al. 2003b), and like themosses they form a dense ground cover that impedes soilmoisture loss. Experimental removals of reindeer lichens

from field plots in a northern Finnish boreal forest werefound to impair decomposition of bilberry litter in lit-terbags, presumably because the litter was subjected to aless favorable microclimate (Stark et al. 2000). Theadverse effect of grazing of reindeer lichens by reindeer onthe soil microbial biomass and C flow in the soil is proba-bly attributable to alterations in soil microclimate andreduced moisture availability caused by lichen removal(Vre et al. 1996; Stark et al. 2000).

Succession is characterized by predictable changes in

vegetation composition (Walker and del Moral 2003)and, in the Swedish boreal forest, vegetation communitystructure generally follows a predictable trajectory in theprolonged absence of fire (Table 1). As succession pro-ceeds through to a retrogressive phase, there is increasingdomination by black crowberry and feather mosses in theunderstory, which creates an unsuitable environment fortree seedling establishment. Species such as Scots pineand birch, that rely on establishment from seeds, fail toregenerate in sufficient numbers to maintain thosespecies, and Norway spruce becomes increasingly abun-

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Figure 3. Micrograph of a section of moss leaf (x 200). (a) Underultraviolet-fluorescence micrograph with a green filter; and (b) under lightmicroscope. Coiled chains of the cyanobacterium Nostoc are hidden in theleaf under light microscopy, but are readily observed as the red cells under

ultraviolet-fluorescence microscopy. From DeLuca et al. (2002b), by per-mission of The Nature Publishing Group.

(a) (b)

(a)CourtesyofPLundgren.

(b)CourtesyofU

Rasmussen.


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dant because it can regenerate vegetatively and is betterable to tolerate late succesional conditions. During thisretrogressive succession, polyphenolic compounds(largely produced by black crowberry) appear to accumu-late in the soil, retarding microbial activity, decomposi-tion, and N mineralization (Wardle et al. 1998; DeLuca etal. 2002a). This in turn reduces the rate of supply of plantavailable N from the soil. Carbon accumulates in these

soils because decomposition rates decline faster than NPPduring retrogressive succession (Wardle et al. 2003a).Meanwhile, N accumulates in the soil because of increas-ing N lock-up by polyphenols and greater rates of biolog-ical N fixation by cyanobacteria over time (DeLuca et al.2002b; Zackrisson et al. 2004). This pattern of ecosystemdecline can only be reversed through rejuvenation of thesystem by wildfire (Zackrisson et al. 1996).

Management implications

Wildfire is the primary natural disturbance regime inboreal forests, in both Scandinavia (Niklasson and

Granstrm 2000) and elsewhere (Bonan and Shugart1989). The work described above provides compellingevidence that this disturbance drives the functioning ofthe ecosystem, mainly by determining the composition ofthe understory vegetation. In Scandinavia, the natural fireregime has been suppressed in recent times, and the prob-able long-term consequence of this is increasing domina-tion of the understory by ericaceous dwarf shrubs andfeather mosses, and corresponding declines in forest treeregeneration and aboveground and belowground ecosys-tem process rates. The use and management of fire from a

conservation and restoration perspective have been debated in manregions that have a natural fire ecologyincluding Scandinavia (Niklasson anGranstrm 2004). The recent work oboreal understory vegetation effectdescribed above provides strong rea

sons for instituting or retaining foresmanagement practices that allow anpromote fire in the natural landscapeMaintaining diversity in species anecosystem types at the landscape scalis probably best encouraged by maintaining a mosaic of forest stands ovarying times since most recent fire.

Forestry is a primary export industry oSweden, and contributes 13% of its totaexport earnings (Skogs-styrelsen 2005Evidence is emerging that understorvegetation is a major driver of fores

condition, both in the short term, baffecting tree seedling regeneration, anin the long term, by driving soprocesses that regulate nutrient supplfor trees. It would therefore appear tha

the type of understory vegetation present has importaneconomic implications. Since fire is a major driver of understory vegetation composition in the boreal forest it is likelthat restoration of natural fire regimes in productioforestry would be commercially advantageous in the lonterm, as well as being beneficial for conservation. Thdebate about the benefits of fire for Swedish boreal foresthas tended to focus on conservation issues rather than com

mercial forest productivity, but there is an increasing awareness of the probable long-term benefits of prescribed burning for production (Niklasson and Granstrm 2004). Firdisturbance is likely to benefit production forestry simplbecause it prevents forest ecosystems from entering a longterm retrogressive succession. Scarification (or shallow cutivation) of the soil surface has often been the managementool of choice over prescribed fire in Scandinavian production forests, but this may not confer the same benefits to thecosystem as fire does. In particular, it is less successful thafire in preventing long-term dominance by those understorspecies that suppress seedling regeneration and tree growthoften leading to reduced forest productivity (Figure 4).

Conclusions

Recent studies in the Swedish boreal forest have shownthat understory components such as ericaceous dwarshrubs, mosses, and lichens are major community anecosystem drivers. In the short term, they operate as filterby helping to determine future forest tree species composition. In the longer term, they serve as major drivers of sofertility and thus influence nutrient availability and plangrowth. Their net effect is to drive ecosystem succession

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Figure 4.A regenerating forest stand in an area that was clearcut and subsequently

scarified. Ericaceous dwarf shrubs (eg black crowberry) have dominated theunderstory and are likely contributors to the poor regeneration of this forest.Successful regeneration and superior tree growth would require reinstatement of thenatural fire regime.


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including retrogressive succession. They also interact withthe fire regime to influence vegetation composition andecosystem functioning in the longer term. From an appliedperspective, production forestry and conservation are notnecessarily incompatible, and we suggest that managementfor appropriate fire regimes may be beneficial for achievinggoals associated with both of these land uses.

Although relatively few studies have investigated theecological role of understory vegetation in other borealforests (but see Oechel and Van Cleve 1986; Carlton andRead 1991; Mallik 2003), it is likely that the role thatthis vegetation plays in Swedish boreal forests also oper-ates elsewhere. Understanding these interactions in otherboreal forests could contribute to the debate over the roleof fire and its management in the boreal zone in general.

Nevertheless, much remains to be learned regarding theecological role of understory vegetation, both in northernSweden and elsewhere. For example, there is little under-standing of the extent to which interactions involvingunderstory species at small spatial scales (characteristic of

most studies to date) are important at large spatial scales(eg landscape scale or whole watersheds). Finally, little isknown about how major global change drivers such asnitrogen deposition, global warming, and increases inatmospheric CO2 may influence the composition ofunderstory vegetation, and how this will affect the func-tioning of the boreal forest ecosystem in the long term.However, since several studies have shown potentiallylarge responses of ground layer vegetation to some ofthese global change drivers in tundra ecosystems (Hobbieet al. 1999; van Wijk et al. 2004), it is likely that impor-tant effects would also occur for similar understory vege-tation types in boreal forests.

Acknowledgements

We thank our colleagues O Zackrisson, G Hrnberg, andT DeLuca for commenting on an earlier version of thismanuscript. We also thank the funding agencies FOR-MAS, Vetenskapsrdet, and Carl Tryggers Stiftelse forsupporting the work of our colleagues and ourselves inthis field over the past 15 years.

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