Indirect effects of black spruce (Picea mariana) cover on communitystructure and function in sheep laurel (Kalmia angustifolia) dominatedheath of eastern Canada
Received 3 November 2003. Accepted in revised form 12 February 2004
Key words: black spruce, dominance, foliar N, Kalmia, photosynthetically active radiation, soil respiration
Abstract
Recent studies on phenotypic plasticity of plant traits indicate that within-species variation in litter quality may be asignificant factor that feeds back on litter decomposition and nutrient cycling rates at the stand level. These findingsmay be especially significant for understanding biodiversity-stability relationships in species-poor ecosystems thathave little functional redundancy among primary producers. We tested the null hypothesis that black spruce andKalmia were functional equivalents with respect to their structuring roles of subordinate vegetation and their influ-ence on site biogeochemistry. The purpose of the study was to determine the degree to which forest cover exertstop-down control on community structure and function of Kalmia-black spruce communities. This community typedominates much of the forest understory and unforested heathlands in Atlantic Canada. We intensively studied arepresentative stand of Kalmia heath in Terra Nova National Park in eastern Newfoundland. Thirty-two 0.5 m× 0.5 m sample plots were randomly distributed among five transects bisecting gradients in dominance of blackspruce and Kalmia. Light levels, species composition, vascular plant cover and soil respiration rate were determinedfor each plot. Tissue samples of litter, mature and current year leaves of Kalmia were collected and analyzedfor nutrient status. Herbaceous species richness and cover peaked at intermediate light levels. Kalmia foliar Nconcentration and above-ground biomass increased with increasing shade. Soil respiration rates were stronglyrelated to the light gradient and increased with increasing quality of Kalmia litter inputs. Our data indicate thatKalmia’s vigour and foliar nitrogen concentrations are greater under black spruce canopy as opposed to heathcondition and that the shaded phenotype has relatively benign feedbacks on soil productivity compared to theopen-habitat phenotype. In the absence of functional diversity at the species level in these species-poor habitats,phenotypic plasticity in Kalmia appears to be an important dimension of the biodiversity-stability relationship inthese communities since our data suggest that this species has the potential either to inhibit or facilitate carboncycling and the pathway is strongly linked to the presence or absence of overstory cover. The role of forestregeneration as an indirect control of forest soil processes such as carbon and nitrogen cycling in this ecosystem isdiscussed.
Introduction
The potential for species to have critical roles in con-trolling species diversity and ecosystem processes,such as nutrient cycling has raised questions about thedegree to which natural systems can be altered in their
species composition and richness without losing func-tionality (Erhlich and Mooney, 1983; Naeem et al.,1994; Silver et al., 1996; Tilman and Downing, 1994;Walker, 1992; Wardle et al., 2000). It has recentlybeen argued that the identity of species removed fromecosystems is less critical to ecosystem function thanare the persistence and richness of functional groups
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which control cycling of limiting nutrients (Grime,1997; Silver et al., 1996; Wardle et al., 2000). Implicitin this argument is that greater species richness withineach functional group should increase the stabilityof community processes when species composition isaltered by stress of disturbance (Frost et al., 1995; Vit-ousek, 1990). From this perspective, it would seemthat depauperate communities may be at greatest riskof de-stabilization following disturbance.
A well-known example of such community de-stabilization is the large-scale conversion of forest toheathland in areas of Scotland, Finland, Germany andcoastal regions of North America (de Montigny andWeetman, 1990; Gimingham, 1972; Mallik, 1995).After forest canopy removal most of these ecosystemsare prone to dominance by ericaceous plants to theexclusion of coniferous species. As such they can beperceived as having at least two dominant species: aphysiognomic dominant (sensu Kershaw, 1973) whichgoverns the shade relations within stands and a so-ciologic dominant which proliferates at lower levelsin the vertical strata of the community (i.e. under-story) but has significant control over litter inputsand regeneration success of invading canopy spe-cies. Examples of such pairs of dominants includesalal-western red cedar communities in coastal BritishColumbia, Calluna-Scots pine heath in Scotland andmainland Western Europe and Kalmia-black sprucecommunities of eastern Canada. The mechanisms bywhich these transitions occur are not fully known but ithas generally been understood that pre-emptive com-petition and allelopathy are factors conferring coloniz-ation abilities to ericaceous species upon release fromcompetition for light in disturbed habitats (Mallik,1995). Additionally a growing number of studies sug-gest that autogenic habitat modification by ericaceousplants through chemical inputs and long term feed-backs may be important factors controlling site pro-ductivity (Bradley et al., 1997; Hättenschwiler andVitousek, 2000; Northup et al., 1995; Northup et al.,1997). For example, recent experiments with lightregimes in controlled conditions have documentedevidence for phenotypic modifications of litter qual-ity and life history characteristics in heathland plants.Moody et al. (1997) observed that shelter from UVstress modified the life history traits of Vaccinium myr-tillus in Europe. It has been speculated that increasedlitter quality of ericaceous plants sheltered from UVmay have effects on soil productivity (Moody et al.,1997). Gehrke et al. (1995) noted that increased ex-posure of V. uliginosum to UV caused a decline in
litter quality that was speculated to affect soil fertil-ity. Similarly, Kalmia angustifolia (hereafter referredto as Kalmia) has been observed to have a higherleaf area index, above-ground productivity and seedviability under partial shade of black spruce (Mallik,1994). Additionally, Kalmia has been observed tohave larger, more pliable leaves under shade and tobe grazed by moose and snowshoe hare under deepshade conditions (R. G. Bloom and A. U. Mallik, fieldobservation) in spite of its high level of toxicity tothese mammalian herbivores (Jaynes, 1975). In spiteof these findings the occurrence of indirect effectsof solar radiation on stand-level processes in forest-heath ecosystems has not yet been verified in naturalcommunities.
The purpose of this study was to test for effectsof black spruce canopy cover on measures of com-munity structure and function via induced intraspe-cific variation in the sociologic dominant species. Wetested for the indirect effects of black spruce coveron: (1) richness and cover of understory vascularplants, (2) biomass and mineral nutrition of the so-ciologic dominant species (Kalmia) and (3) organicsoil respiration as an index of soil productivity. Theseeffects were quantified through testing the followinghypotheses:
(1) Shade produced by the physiognomic domin-ant (black spruce) has measurable effects on biomassof the sociologic dominant (Kalmia) and understoryspecies composition.
(2) Variability in species richness and cover ofunderstory herbs would be related to the amount ofbiomass of the sociologic dominant (Kalmia).
(3) Light intensity affects Kalmia foliar C and Nconcentrations and the degree of changes in foliar Cand N is related to leaf age.
(4) Soil respiration rates vary with soil temper-ature, C:N ratios of litter inputs from the sociolo-gic dominant (Kalmia) and litter of other associatedspecies.
Soil respiration rate was used as a measure of thebiological activity occurring in the organic soil ho-rizon. Although the field method of measuring soilrespiration does not differentiate between soil and rootrespiration, it has been cited as a general index of bio-logical activity in soil. In particular, soil respirationhas been used as a surrogate for productivity (Liethand Ouellette, 1962; Medina et al., 1980) since it isa composite measure of root activity, microbial up-take and microbial mineralization of nutrients (Gordonet al., 1987; Tewary et al., 1982). Taken together, these
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sources of variability in soil respiration rate were as-sumed to act as a robust indicator of the rate of Ccycling and the concomitant mobilization of associ-ated nutrients from detritus to plant and microfaunalcomponent of the community.
Methods
Study site description
The study area was located in Terra Nova NationalPark, Newfoundland, Canada (54.0◦ W, 48.5◦ N). Thearea lies within the Central Newfoundland ecoregionof Newfoundland (Rowe, 1972). This region of theboreal forest receives 1000 to 1300 mm of annualprecipitation and has a mean summer temperature of12.5 ◦C. Mineral soils tend to be acid podzols derivedfrom granitic parent materials. Mineral soils tend tobe shallow and discontinuous at the landscape level.Consequently this region is characterized by a mosaicof community types that reflect variation in the degreeof soil development, drainage and fertility. Forestedareas tend to be dominated by black spruce with oc-casional but localized dominance of balsam fir (Abiesbalsamea) and boreal hardwoods such as Betula pa-pyrifera, Populus tremuloides on the more productivesites. Nitrogen limitation is the primary constraint onforest productivity in this region (Mallik, 1995).
An ericaceous-conifer vegetation association knownas the Kalmia-black spruce forest type (sensu Dam-man, 1964) is locally dominant throughout much ofthis ecoregion and occupies approximately 50% ofthe forested land base of Terra Nova National Park(Figure 1a). This forest type is also prevalent oncoastal acid soils in Nova Scotia and eastern Que-bec. Within the Kalmia-black spruce forest type, twosub-associations occurring on mesic soils have beendescribed: Kalmia black-spruce forest and Cladina-Kalmia black spruce forest. Additionally disturbedsites in this region frequently become devoid of forestcover and typically regenerate as Cladina-Kalmia bar-rens (Figure 1b). The influence of disturbance historyon conifer regeneration is suspected to be an importantdeterminant of the specific vegetation type resultingfrom disturbances, such as fire and logging, which re-move the forest canopy (Damman, 1964; Bloom andMallik, unpublished).
The study site used in this investigation was cre-ated by a fire in 1961 which burned an area ofapproximately 200 ha (Power, 1996). The site regener-ated as a Cladina-Kalmia barren and is predominantly
treeless beyond dispersal range of seeds spread fromintact forest at the disturbance edge (Figure 2a). Thevegetation was characterized by sparse black sprucecanopy (5 to 10% cover) with a dwarf shrub un-derstory dominated by ericaceous species such asKalmia (40 to 80% cover), with presence of Vac-cinium angustifolium (< 20% cover), Rhododendroncanadense (< 15% cover) and occasionally Ledumgroenlandicum (< 10% cover). The herb layer wasgenerally lacking and cryptogamic species such asClandina mitis and C. rangiferina typically domin-ated the ground surface. Soils were highly acidic andhad pH ranges, measured using the paste method,between 3.5 to 4. These soils are nutrient poor (< 1%of total nitrogen is available) and have negligible ratesof N mineralization (0.1 mg kg−1 day−1) (Bloomand Mallik, unpublished data). A forest-heath ecotoneis evident on well-drained sites along the disturb-ance perimeter resulting in a narrow band of openCladina-Kalmia-black spruce vegetation. Along thisecotone black spruce cover increased from approxim-ately 5% toward the centre of the barren to 75% at thedisturbance edge (Figure 2b).
Adjacent unburned forest stands are of thePiceetum forest type (sensu Damman, 1964) which,based on charcoal macrofossils and growth incrementestimates appeared to have origins in a stand repla-cing fire approximately 60 to 100 years prior to thefire of 1961 (Power, 1996). These stands had scatteredhardwoods throughout the overstory canopy and hadpatchy coverage of Kalmia in the understory withrelatively even distribution of understory herbs suchas Cornus canadensis, Clintonia borealis, Trientalisborealis, Coptis trifoliata and Linnaea borealis. SoilpH ranged from 4 to 4.5 (measured using pastemethod) (Bloom and Mallik, unpublished data).
Study design
We used the post-disturbance gradient of black sprucecover that occurred at this site as a natural experimenton the effects of black spruce cover on otherwise tree-less Kalmia heathland. There were many examples ofKalmia heath in the region but no other sites of knowndisturbance history were sufficiently old to yield agradient of spruce regeneration as was observed at thepresent site. Because replication of sites was not pos-sible, we studied one site intensively. We attempted tominimize variability within sampling units in order todetect canopy effects since effect sizes were unknownand could have been masked by site-to-site variability
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Figure 1. Comparison of Cladina-Kalmia vegetation with Kalmia-black spruce forest. A) Undisturbed Kalmia-black spruce forest in TerraNova National Park, Newfoundland. B) Kalmia heath 23 years after a forest fire near Terra Nova National Park.
if multiple study sites were used. While this lack ofsite replication requires that extrapolation of resultsbe conservative, we emphasize that the purpose of thestudy was to investigate potential mechanisms operat-ing within stands as opposed to characterizing regionallevel phenomena. These caveats notwithstanding, webelieve the study site is representative of the manyKalmia barrens in the region.
Plot layout
Sample plots were established using a stratifiedrandom method. Five areas (each approximately10000 m2) of heath-forest ecotone were randomly se-lected from ten areas of forest-heath ecotone identifiedwithin the study site using aerial photographs. Thepool of potential sampling sites was determined on thebasis of concentrations of black spruce trees amongotherwise homogenous heathland. These randomly se-lected areas were identified in the field using map andcompass. Only mesic, well-drained sites were used forsampling. Randomly selected areas that were too wetfor inclusion were replaced by the nearest samplingareas that were characterized by upland gradients inblack spruce regeneration amongst Kalmia heath.
At each of the five sampling areas a transect wasestablished by rolling out a 50 m tape from a randompoint in the heath toward the forest edge (Figure 2a).Transects started at a point of complete open conditionand progressed toward forest closure as tree density
and size increased near the forest edge (Figure 2b).Along each transect a set of 0.5 m × 0.5 m sampleplots were established using a series of blind randomthrows of a flagged marker along the gradient. Variab-ility in the distance of the throw produced a range of5 to 7 plot placements over the length of each 50 mtransect. A total of 32 plots were established among 5transects within the study site.
Due to variability in the density of the coniferregeneration among sampling areas, some transects in-tercepted much more shade than others. To ensure thatthe plots comprising each transect represented a rangeof canopy shade conditions, any plots preceded bymore than two plots of similar amounts of shade fromblack spruce were relocated to the nearest micrositewith visibly different characteristics. For example, ifthe first three plots in a series of seven had no ad-jacent spruce trees then the third plot was moved asdescribed above. No plots were located directly underblack spruce trees since small-scale soil and vegetationconditions under black spruce may differ from underKalmia heath and our objective was to determine theresponse of heathland vegetation and organic soil toincreasing shade.
Instrumentation and data collection
To quantify the amount of shade provided by blackspruce canopy along each transect of the shade gradi-ent, photosynthetically active radiation (PAR) was
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Figure 2. Graphical representation of study area, transects and sample plots in relation to the black spruce gradient. A) Sample plots werenested within transects which in turn were randomly located within the burned habitat (marked in light gray); map is not to scale. B) Profilediagram representation of the black spruce gradient projecting out from the disturbance edge into Kalmia heath.
measured above the understory canopy of Kalmia ata height of 1 m above the ground at each sampleplot. Photosynthetically active radiation was meas-ured using a portable light meter (Decagon SunfleckCeptometer, Decagon Devices, Washington, USA) ona uniformly overcast day in early July between thehours of 10 a.m. and 2 p.m. These conditions wererequired to stabilize measurements over the course ofthe sampling period. Measurements were taken withthe instrument beam leveled and oriented to 180 de-grees in the horizontal plane. Measurements were re-peated in reverse order within each transect to estimatesampling error and provide representative measure-ments. Completely exposed stations were used as a100% exposure standard and all other measurements
for each transect were taken as a proportion of thesemeasurements as an index of shade cover by the forestcanopy ranging from 0 to 1.0.
Vegetation sampling
Species composition and percent cover of all vascularplants was determined in each 0.5 m × 0.5 m plot.Mean height, stem density and mean stem basal dia-meter of the dominant understory vegetation (Kalmia)were recorded in each plot. These parameters wereused to calculate a biomass index based on stemvolume according to the following formula:
Kalmia stem volume (cm3) =(π(d/2)2 × h)/3 × n,
(1)
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where: d = mean stem diameter (cm), h = mean stemheight (cm), n = stem density (count m−2)
To determine the mineral nutrition of the dominantunderstory species across the canopy cover gradient,foliage of three age classes of Kalmia was collectedin each plot. Foliage collection followed the methodof Small (1972). Within each plot Kalmia first yearleaves, mature leaves and leaf litter were gathered aswas a 0.05 m × 0.05 m × 0.05 m humus samplecollected from the F layer of the organic soil horizonbelow the litter layer. Litter types for each locationwere identified to species and Kalmia tissue sampleswere placed in plastic zip lock bags and stored in a re-frigerator for four days prior to air-drying. All tissuesand humus samples were analyzed for percent C andN concentrations using a LECO gas analyzer (LECOInstruments, Mississaga, Ontario). The C:N ratio ofleaf matter and organic soils was used as an index oflitter and organic matter quality. Differences in foliarnitrogen concentrations in senescing, mature and firstyear leaves were used to estimate intraplant foliar Nconcentrations across the leaf life cycle. Concentrationchanges from first year leaves to mature leaves werecorrected for the initial leaf N using the following for-mula: (First year leaf N – mature leaf N)/first year leafN.
Similarly, percent N conservation prior to abscis-sion (i.e. the difference between N concentrations inmature leaves and senescent leaves) was estimated bycalculating the relative difference in N concentrationof mature and litter leaf tissue using the followingformula: (Mature leaf N – litter leaf N)/ mature leafN.
Soil respiration rate was recorded at each plot us-ing a portable infrared gas analyzer (IRGA, Nortech,Ottawa, Ontario) (Parkinson, 1981). Units of meas-urement were g CO2 m−2 h−1. Measurements werecentered on the 0.05 m × 0.05 m area from whichlitter samples were collected and were made prior toextracting the 5 cm deep organic soil sample describedabove. A 0.00785 m2 surface area of soil was meas-ured by pressing the sampling chamber 1 cm into theorganic layer, following removal of the dry litter layer.This was necessary to create a seal and allow the rateof partial CO2 pressure in the chamber to stabilize.Measurements were made in mid-June and again inearly July. Moisture contents at the various stationswas assumed to be made homogenous by periods ofheavy rain prior to sampling. All soils were moist andappeared to be at field capacity. In order to ensure thatall plots were measured in one day and under the same
weather conditions replication of sampling stations onthe date of data collection was not possible. Insteadthe stations were re-surveyed at a later date under sim-ilar weather conditions to confirm the reproducibilityof the data. Repeated observations for each plot wereaveraged for use in data analyses.
In addition to soil respiration, soil temperature andorganic matter depth were measured simultaneouslywith soil respiration in each plot. These data were usedto correct soil respiration measurement for plot levelvariation in soil depth and temperature.
Statistical analysis
Step-wise hypotheses were tested using a series of re-gression analyses and ANOVA. The residual values ofsoil respiration rate were used as the dependent vari-able for testing of sequential hypotheses. Quadrat datafrom the five transects were pooled for all analyses.The specific analytical methods employed for testingeach hypothesis are outlined below.
Relationships between PAR (a random predictorvariable) and each of Kalmia biomass, richness ofherbaceous species and cover of herbaceous plants (asresponse variables) were tested using the curve estim-ation feature of SPSS version 9.0 (SPSS, 1998) to testHypothesis 1 (that shade effects of black spruce wouldaffect biomass of the sociologic dominant (Kalmia)and understory species composition.). Kalmia bio-mass index was log transformed prior to analysis.
Subsequent to testing Hypothesis 1 and saving theresiduals, Hypothesis 2 (that additional variability inherbaceous species richness and cover would be re-lated to the amount of overstory cover from Kalmia)was tested through Pearson correlation analysis usingKalmia above-ground biomass as the random pre-dictor variable and residuals of herb richness and coveras response variables.
Hypothesis 3 (that light intensity affects Kalmia fo-liar C and N concentrations in first year leaves, matureleaves and litter) was tested using two-way repeatedmeasures analysis of variance on C concentration, Nconcentration and C:N ratio of three age classes offoliar tissue (first year leaves, mature leaves and litter)while employing PAR as a covariate in each analysis.Data did not meet the assumption of Sphericity and theHuynh-Feldt correction to the degrees of freedom wasused for significance testing (SPSS, 1998).
Lastly, Hypothesis 4 (that the quality of Kalmialitter and abundance of litter of other species wouldaffect soil respiration rate) was tested by using the
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litter C:N ratio of Kalmia leaves, organic soil C:N ra-tio and the proportions of cover of other species/littertypes (Cladina lichen, feathermosses and birch/redmaple) as predictors of soil respiration in a multipleregression. Since the structure and performance ofmultiple regression models can be sensitive to the wayfactors are selected, no stepwise procedure for includ-ing variables was used. Factors were added togetherin the model and partial correlations with the responsevariable were used as post-hoc descriptors of the rela-tionships of soil respiration to the prevalence of eachfactor.
Based on the outcome of these hypotheses, a gen-eral linear model of soil respiration rate as a functionof PAR was tested using simple linear regression.
Results
Vegetation composition and structural responses tolight exposure
Floristic responsesKalmia was the dominant species in all plots butits biomass varied in relation to black spruce cover(Figure 3a). Log transformed Kalmia biomass hada significant quadratic response to the PAR gradient(F(2,29) = 5.23, P = 0.01) and peaked at PAR =0.6 (Figure 3a, Appendix I). Other ericaceous species(Rhododendron canadense and Vaccinium angustifo-lium) were occasionally present in the open heathconditions where they achieved a maximum percentcover of approximately 10% (data not shown).
Total herb cover (maximum = 67%) had a sig-nificant unimodal response to PAR (F(2,28) = 3.52,P = 0.043; Appendix II) which peaked at inter-mediate levels of black spruce cover (45% availablePAR). With the exception of a single outlying datapoint, the pattern is suggestive of a simple unim-odal response (Figure 3b). Similarly, herb speciesrichness peaked under partial shade of black sprucealong a cubic response curve (F(3,28) = 3.34, P =0.034) (Figure 3c, Appendix III). Trends in coverwere primarily a reflection of patterns in the abund-ance and cover of Clintonia borealis which had thehighest prevalence of herbs encountered in the plots(data not shown). Cornus canadensis, Maianthemumcanadense, Trientalis borealis and Coptis trifoliatawere also frequently occurring but had lower covervalues. Correlation analysis controlling for the effectof black spruce cover detected no significant variabil-ity in the residuals of herb richness and cover that was
Figure 3. Effects of photosynthetically active radiation (PAR) onforest understory. A) Ln-transformed Kalmia biomass index re-sponded curvilinearly to the gradient. B) Herb richness showed atendency to peak under partial black spruce cover. C) Cover of herbspecies was also favoured by partial canopy cover.
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related to Kalmia biomass (rrichness×Kalmia biomass =0.24, n = 32, P = 0.10; rherbcover×Kalmia biomass =0.21, P = 0.13).
Non-herbaceous ground cover within the samplingplots shifted from an assemblage of lichens dominatedby Cladina species (C. stellaris and C. rangiferina)in the open condition to a lichen-moss-Kalmia litterground cover at intermediate light levels which wasdominated by C. rangiferina and Pluerozium schreberi(Figure 4). As PAR declined under higher levels ofcanopy cover, ground cover became dominated byKalmia leaf litter with increasing representation ofmosses such as P. schreberi. Litter cover near thedisturbance edge tended to have additional constitu-ent species and was either heavily dominated by pureKalmia litter or was a mixture of Kalmia litter andlitter from nearby hardwood canopy species such aspaper birch (Betula papyrifera) and red maple (Acerrubrum). Vegetative responses to increasing levels ofshade are summarized in Table 1.
Leaf and litter quality responses to PARNitrogen concentrations of Kalmia leaves declinedsignificantly with increasing leaf age (F(2,29) = 5.23,P = 0.01) (Figure 5a; Appendix IV). First year leaveshad the highest N concentrations and the concentra-tions were strongly inversely related to PAR (r =−0.71, n = 31, P < 0.001). In spite of the strongcorrelation, the low slope of the scatter points indicateslittle difference across the shade gradient (Figure 5a).In contrast, mature leaves (r = −0.81, n = 32,P < 0.001) and abscissed leaves (r = −0.65, n = 32,P < 0.001) showed successive declines in N con-centration as PAR increased but the magnitude of thedifference between age classes increased significantlyat high levels of PAR. These data indicate that Kalmialeaves had relatively uniform rates of N conservationfrom mature to new tissues across the light gradient(r = 0.07, n = 32, P = 0.36) with a mean of a53% (+ 0.01 s.d.) lower N concentration in matureleaves compared to new foliage. In contrast Kalmialeaves had progressively higher rates of N conserva-tion between the stages of maturity and abscissionunder increasing light exposure (r = 0.39, n = 32,P = 0.014). Repeated measures ANOVA did not de-tect significant differences in total C concentrationsamong age classes nor did total C measurably interactwith PAR (Figure 5b; Appendix V).
The C:N ratio of first year leaves and mature leavesvaried little across the PAR gradient (Figure 5c) but theC:N ratio of litter increased proportionately to PAR.
This correlation was significant (r = 0.65, n = 32,P < 0.001) and the hypothesis that light intensityaffects Kalmia leaf C and N concentrations was ac-cepted. Repeated measures ANOVA results detectedstrong interactions of foliar C:N ratios in successiveages of leaves with PAR (Appendix VI).
The magnitude of main effects and interactions ofleaf age class and PAR on foliar N and C:N ratio aresummarized for each nutrient variable in Table 2. Thepercent change in concentrations at low light intensitycompared with high light intensity were large for Nand for the C:N ratio but the magnitude of the changedepended on leaf age. Largest effects of light intensitywere observed in litter rather than live leaves.
Soil respiration responses to leaf types and litterqualityMultiple linear regression analysis revealed evidencethat soil respiration was related to litter quality andvegetation cover (Appendix VII). This pattern was re-lated to variability in Kalmia litter C:N ratio (Beta= −0.28) (Table 2), amount of feathermoss cover(Beta = −0.47) and amount of Cladina lichen cover(Beta = −0.51). Organic soil C:N ratio and amountof hardwood leaf litter types showed no raw or partialcorrelation with soil respiration and were uninfluentialin the model (Beta < 0.10). The resulting linear model(Equation 2) accounted for 38% of the observed vari-ability in soil respiration (R2 = 0.38, R2
(adj.) = 0.28,Appendix VII). The hypothesis that litter quality of thedominant species affects soil respiration was accepted.Due to the underlying effect of PAR on all of the com-ponent variables in Equation 2, a more general linearmodel was tested using PAR as a single predictor ofsoil respiration. In general closed-canopy forest-heathconditions (25 to 35% PAR) had soil respiration ratesapproximately twice that of the adjacent unshadedopen heath conditions (Table 1, Figure 6). Adjust-ment of the raw coefficients of determination (R2) foruse in prediction revealed that this model (Equation 3,R2
(adj.) = 0.30, Appendix VIII) was statistically sig-nificant and explained similar amounts of variabilityin soil respiration than did the more complex modelsummarized in Equation 2 (R2
(adj.) = 0.28). Paramet-ers of this parsimonious model are shown in Table 3.Model standard deviations are based on cumulativevariance of slope estimates. Models assume no errorin measurement of variables.
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Figure 4. Mean cover of litter and vegetation in relation to proportion of canopy cover. Hardwood litter species were present at low levels ofPAR near the disturbance edge. Kalmia litter had peak prevalence at low and moderate levels of PAR. Kalmia litter underlain by pleurocarpouswas the dominant ground cover type at moderate to high light levels. Cladina lichens became increasingly abundant at high levels of PAR.
Table 1. Mean vegetation and habitat parameters associated with a gradient of black spruce canopy cover inKalmia heath
Kalmia heath Kalmia heath with Open Kalmia-black Closed canopy
scattered black spruce spruce forest forest
Proportion of
maximum PAR 0.72 ± 0.10 0.65 ± 0.07 0.64 ± 0.12 0.39 ± 0.02
Ground cover Cladina-Kalmia Cladina-Pleurozium- pure Kalmia Kalmia-hardwood
∗refers to the dominant litter component only (Kalmia angustifolia).
Table 2. Effects of leaf age class and PAR on foliar N, C and C:N ratio. High and low concentrations werecalculated by averaging nutrient values > 0.80 PAR and < 0.3 PAR respectively. Values are mean ± s.d.
Nutrient Leaf age class Concentration Concentration Concentration % Change
at high PAR at low PAR (high to low PAR)
Nitrogen First year 2.9 ± 0.44 2.37 ± 0.02 3.13 ± 0.07 32.1
Soil temperature ranged from 9 to 15 ◦C but wasinversely related to soil respiration (r = −0.337,n = 32, P = 0.03). Partial correlation controlling forlitter C:N ratio in the relationship between soil respir-ation and temperature was not significant (r = −0.20,n = 32, P = 0.143) indicating that the negativerelationship between temperature and respiration wasdriven in part by the indirect association of temperat-ure with litter quality. On this basis, the hypothesis thatincreasing soil temperature would positively affect soilrespiration was rejected.
Discussion
The results of this study indicate that shade stronglyinfluences floristic composition of vascular plants aswell as phenotypic properties of the sociologic domin-ant (Kalmia). The hypothesis that black spruce coverstructures species composition was accepted on thebasis of the observed correlations of vascular plantcover and diversity with the black spruce cover. Weattribute a causal relationship to the correlation be-cause these species (C. borealis, M. canadense, and
C. canadensis) are generally known to be forest plantsthat are most productive in partial shade (Crowderand Taylor, 1984; Hoefs and Shay, 1981; Shirley,1945; USDA, 2002) and would therefore be expectedto have maximum abundance at intermediate levels ofphotosynthetically active radiation.
The dependence of these understory herbs onshade cover is further emphasized by the monotonicincrease in herb cover with increasing Kalmia bio-mass. This relationship suggests that these forestherbs proliferate in shade in spite of the effects ofabove-ground competition from ericaceous biomassand associated below-ground competition among rootswithin these small plots. In the absence of a tree can-opy or dense shrub cover to provide shade, these forestplants appear at much reduced abundances in Kalmiaheath relative to Kalmia-black spruce forest. While thesimplest explanation for this relationship is that herbshave responded positively to the provision of shadecover by black spruce, the specific mechanism mayinclude a chemical aspect whereby inputs into the soilfrom the litter of canopy species in the mature forestenhance conditions for understory species. Paper birch(Betula papyrifera may be particularly important inthis regard since its litter is known to be relatively richin macronutrients such as N and Ca (Roberts et al.,1998). In the absence of such canopy cover, shadeintolerant plants were conspicuously absent and theground cover was dominated by a thick mat of Clad-ina lichens (C. stellaris, C. mitis and C. rangiferina)
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Table 4. Parameter estimates for linear regression model components (Soil respira-tion versus PAR)
Parameter Beta Std. error Std. Beta t p r
(constant) 1.598 0.134 11.890 0.00
PAR −0.744 0.196 −0.569 −3.788 0.001 −0.569
with sparse cover of ericaceous vegetation dominatedby Kalmia.
Kalmia dominated all plots but, like the herb-aceous plants, its cover and vigour (as indicated byits biomass index) peaked at intermediate levels ofshade. Because of the apparent influences of blackspruce cover on herbaceous and woody plants, weconcluded that the development of structural prop-erties of the flora that are typical of Kalmia-blackspruce forest (specifically plant cover and biomass)were strongly contingent on the establishment of treecover. A corollary of this conclusion is that Kalmiaheath is not a functional equivalent to black sprucerelative to the facilitation of local vascular plant di-versity and abundance. The absence of black spruceor other canopy-producing species in burned Kalmia-black spruce sites will likely result in the colonizationlimitation of forbs that benefit from forest cover. In theabsence of forest regeneration, it is typically expec-ted that an alternate suite of species would colonizethe sparsely populated niche space of the open heathas has been observed in other examples of shiftingdominance and plant community invasion (Rejmének,1989). Because vegetation cover and biomass of thedominant species was not constant across the gradient,the findings suggest that factors other than light play arole in vegetation development. The soil litter qualityand respiration data suggest that black spruce covermay indirectly affect soil productivity. This is becausein addition to variation in vigour, several phenotypicqualities of the sociologic dominant species (Kalmia)were strongly associated with black spruce cover.
Our data suggest that the influence of shade onKalmia leaf and litter characteristics may feed backon soil fertility just as the litter quality of dominantfunctional groups have been shown to affect soil fer-tility and respiration in other systems (Gordon et al.,1987; Read, 1992; Sing and Gupta, 1977; Tewaryet al., 1982; Wardle et al., 1997; Weber, 1985). Un-der increasing shade, Kalmia exhibited less nitrogenconservation between leaf age classes and higher lit-ter quality (as evidenced by lower C:N ratios) than
in unshaded heath conditions. Assuming that litterfallis constant across the light gradient, this alteration ofKalmia’s litter quality translates into a two-fold de-crease in annual nitrogen inputs into the organic soilhorizon of the open heath compared to shaded heath.Similarly, open heath conditions produced Kalmialeaves having a three-fold increase in C:N ratio ofrecently fallen litter inputs as compared to C:N ra-tios of recently fallen litter under shaded conditions.Such high rates of C inputs in the absence of highrespiration rates indicates a failure of open heath tosustain the same levels of carbon cycling observedin adjacent forests where Kalmia litter C:N ratios arelower. Addition of tissues with high C:N ratios aretypically expected to increase soil microbial respira-tion through the addition of carbon as an energy source(Blum, 1998; Bradley et al., 1997). Theoretically, highsoil respiration rates are thought to cause concomit-ant N immobilization in the biomass of the growingmicrobial population (Kimmins, 1997). However, thisrelationship can be reversed when litter substrates arecomposed primarily of secondary compounds such aspolyphenolic acids and lignin which are resistant tomicrobial degradation (Hättenschwiler and Vitousek,2000). Links between foliar phenol concentrations andUV exposure have been made in several cases (Hät-tenschwiler and Vitousek, 2000). Since we observedhighest respiration rates when the dominant plant litterhad low C:N ratios and these low C:N ratios occurredunder shaded conditions, we suspect that the highercarbon concentrations observed in unshaded Kalmialitter failed to increase soil respiration because theunshaded leaves are higher in phenolic compoundsassociated with UV exposure. Such phenolic com-pounds are known to inhibit mycorrhizal activity inKalmia soils (Yamasaki et al., 1998) and N mineral-ization in other heathland systems (Berendse et al.,1989; Northup et al., 1997). Conversely, the higherrespiration rates associated with lower C:N ratios oflitter under spruce cover may result from increasedmicrobial activity following addition of labile C toheathland soils as observed by Read (1992). There is
290
Figure 5. Kalmia foliar N and C in relation to leaf age and lightexposure. A) Foliar N concentrations varied by age class but themagnitude of differences varied with PAR. B) Foliar concentrationsshowed no clear differences among age classes or in relation to PAR.C) Foliar C:N ratio showed large differences among leaf age classeswhich also varied with PAR. Low light conditions show little differ-ence in C:N ratio of leaves irrespective of leaf age. In contrast, litterproduced in full sunlight undergoes stepwise increases in C:N ratiowith increasing tissue age.
Figure 6. Relationship between soil respiration and PAR along ablack spruce canopy gradient of post-fire Kalmia-black spruce com-munity in Newfoundland. Soil respiration declined with increasingPAR and 30% of the variability in soil respiration rates was relatedto PAR (P < 0.05).
a possibility that the relatively low C:N ratio of litterfrom B. papyrifera occurring sparsely throughout themature forest of this study site was also contributing tohigher soil respiration rates near the disturbance edgesince the presence of this litter may locally enrich soils(Roberts et al., 1998). This explanation is supported bythe findings of Bradley et al. (1997) that, from a mi-crobial productivity and nutrient cycling point of view,Kalmia organic soils are limited by the availability oflabile carbon and are sensitive to carbohydrate inputs.Because carbon cycling is linked tightly to nitrogencycling in boreal organic soils, carbon sequestrationcan be expected to induce nitrogen sequestration aswell. These data point to a reduced level of soil pro-ductivity in unshaded heathland which is corroboratedby the observation of reduced vegetation biomass andtotal herb cover at highest levels of PAR. We therebyconclude that canopy cover of black spruce and as-sociated hardwood species such as B. papyrifera canhave strong indirect feedbacks on soil processes viatheir respective influences on the quality of Kalmialitter inputs and direct inputs of their own relativelyrich litter in Kalmia-black spruce forests.
In general terms, these data suggest that thephysiognomic dominant species (black spruce) indir-ectly controls the growth parameters and litter qualityof the sociologic dominant species (Kalmia). In turn,variability in the quality of litter inputs of Kalmia ap-pears to strongly affect organic soil productivity. Thispreliminary investigation provides evidence that themechanism by which Kalmia barrens are maintainedas moribund heath is driven, in part, by autogenicresponses of Kalmia to environmental stimuli. These
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findings point to a need to understand whether or notunforested Kalmia heath preclude the regeneration ofproductive forests in the future. Further research intothis potential mechanism of site degradation is recom-mended in order to determine the specific chemicalprocesses driving the patterns observed here. Suchdata are necessary to determine the landscape-levelimpacts of forest canopy removal on long-term spe-cies richness and productivity of Kalmia-black sprucestands in this region.
Acknowledgements
The research was supported by a Discovery Grantof the Natural Science and Engineering Coun-cil (NSERC) awarded to A.U. Mallik. We thankMr Randy Power of Parks Canada for his interest andcooperation in this research and Terra Nova NationalPark for providing logistical support during the fieldwork. We thank Dr Roger Latham of Continental Con-servation, Swarthmore, USA, Dr Heidi Schraft of theBiology Department, and Dr Tom Hazenberg of theFaculty of Forestry and the Forest Environment, Lake-head University for their comments on an earlier draftof the manuscript.
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Appendix I. Summary results of ANOVA for curvilinear regression of Kalmia biomass (log scale)against light intensity (PAR)
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Section editor: P.M. Attiwill
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Appendix IV. Summary results of Repeated measures ANOVA for foliar N concentration among leaf ageclasses
Source Sum of Squares df Mean Square F p Partial Eta
Squared
Leaf age class 15.524 1.370 11.329 132.336 0.000 0.820
Age∗PAR 0.394 1.370 0.287 3.356 0.062 0.104
Error 3.402 39.739 0.08561
Appendix V. Summary results of Repeated measures ANOVA for foliar C concentration among leafage classes
Source Sum of Squares df Mean Square F p Partial Eta
Squared
Leaf age class 4.455 2.000 2.227 2.828 0.067 0.089
Age∗PAR 0.05743 2.000 0.02872 0.036 0.964 0.001
Error 45.678 58.000 0.788
Appendix VI. Summary results of Repeated measures ANOVA for foliar C:N ratio among leaf ageclasses
Source Sum of Squares df Mean Square F p Partial Eta
Squared
Leaf age class 1198.936 1.085 1105.416 3.603 0.064 0.111
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