Indirect effects of black spruce (Picea mariana) - Lakehead University

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Robin G. Bloom1 & Azim U. Mallik2,3. 1Canadian Wildlife ...... and competitive ability of Kalmia angustifolia, L., paper birch ... In Titus B D, Lavigne M B, Newton.

Plant and Soil 265: 279–293, 2004. © 2004 Kluwer Academic Publishers. Printed in the Netherlands.

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Indirect effects of black spruce (Picea mariana) cover on community structure and function in sheep laurel (Kalmia angustifolia) dominated heath of eastern Canada Robin G. Bloom1 & Azim U. Mallik2,3 1 Canadian

Wildlife Service, Nepean, Ontario, Canada, K1A 0H3. 2 Biology Department, Lakehead University, Thunder Bay, Ontario, Canada P7B 5E1. 3 Corresponding author∗

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 a significant factor that feeds back on litter decomposition and nutrient cycling rates at the stand level. These findings may be especially significant for understanding biodiversity-stability relationships in species-poor ecosystems that have little functional redundancy among primary producers. We tested the null hypothesis that black spruce and Kalmia were functional equivalents with respect to their structuring roles of subordinate vegetation and their influence on site biogeochemistry. The purpose of the study was to determine the degree to which forest cover exerts top-down control on community structure and function of Kalmia-black spruce communities. This community type dominates much of the forest understory and unforested heathlands in Atlantic Canada. We intensively studied a representative 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 black spruce and Kalmia. Light levels, species composition, vascular plant cover and soil respiration rate were determined for each plot. Tissue samples of litter, mature and current year leaves of Kalmia were collected and analyzed for nutrient status. Herbaceous species richness and cover peaked at intermediate light levels. Kalmia foliar N concentration and above-ground biomass increased with increasing shade. Soil respiration rates were strongly related to the light gradient and increased with increasing quality of Kalmia litter inputs. Our data indicate that Kalmia’s vigour and foliar nitrogen concentrations are greater under black spruce canopy as opposed to heath condition and that the shaded phenotype has relatively benign feedbacks on soil productivity compared to the open-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 in these communities since our data suggest that this species has the potential either to inhibit or facilitate carbon cycling and the pathway is strongly linked to the presence or absence of overstory cover. The role of forest regeneration as an indirect control of forest soil processes such as carbon and nitrogen cycling in this ecosystem is discussed.

Introduction The potential for species to have critical roles in controlling species diversity and ecosystem processes, such as nutrient cycling has raised questions about the degree to which natural systems can be altered in their ∗ FAX No: (807) 346-7796. E-mail: [email protected]

species composition and richness without losing functionality (Erhlich and Mooney, 1983; Naeem et al., 1994; Silver et al., 1996; Tilman and Downing, 1994; Walker, 1992; Wardle et al., 2000). It has recently been argued that the identity of species removed from ecosystems is less critical to ecosystem function than are the persistence and richness of functional groups

280 which control cycling of limiting nutrients (Grime, 1997; Silver et al., 1996; Wardle et al., 2000). Implicit in this argument is that greater species richness within each functional group should increase the stability of community processes when species composition is altered by stress of disturbance (Frost et al., 1995; Vitousek, 1990). From this perspective, it would seem that depauperate communities may be at greatest risk of de-stabilization following disturbance. A well-known example of such community destabilization is the large-scale conversion of forest to heathland in areas of Scotland, Finland, Germany and coastal regions of North America (de Montigny and Weetman, 1990; Gimingham, 1972; Mallik, 1995). After forest canopy removal most of these ecosystems are prone to dominance by ericaceous plants to the exclusion of coniferous species. As such they can be perceived as having at least two dominant species: a physiognomic dominant (sensu Kershaw, 1973) which governs the shade relations within stands and a sociologic dominant which proliferates at lower levels in the vertical strata of the community (i.e. understory) but has significant control over litter inputs and regeneration success of invading canopy species. Examples of such pairs of dominants include salal-western red cedar communities in coastal British Columbia, Calluna-Scots pine heath in Scotland and mainland Western Europe and Kalmia-black spruce communities of eastern Canada. The mechanisms by which these transitions occur are not fully known but it has generally been understood that pre-emptive competition and allelopathy are factors conferring colonization abilities to ericaceous species upon release from competition for light in disturbed habitats (Mallik, 1995). Additionally a growing number of studies suggest that autogenic habitat modification by ericaceous plants through chemical inputs and long term feedbacks may be important factors controlling site productivity (Bradley et al., 1997; Hättenschwiler and Vitousek, 2000; Northup et al., 1995; Northup et al., 1997). For example, recent experiments with light regimes in controlled conditions have documented evidence for phenotypic modifications of litter quality and life history characteristics in heathland plants. Moody et al. (1997) observed that shelter from UV stress modified the life history traits of Vaccinium myrtillus in Europe. It has been speculated that increased litter quality of ericaceous plants sheltered from UV may have effects on soil productivity (Moody et al., 1997). Gehrke et al. (1995) noted that increased exposure of V. uliginosum to UV caused a decline in

litter quality that was speculated to affect soil fertility. Similarly, Kalmia angustifolia (hereafter referred to as Kalmia) has been observed to have a higher leaf area index, above-ground productivity and seed viability under partial shade of black spruce (Mallik, 1994). Additionally, Kalmia has been observed to have larger, more pliable leaves under shade and to be grazed by moose and snowshoe hare under deep shade conditions (R. G. Bloom and A. U. Mallik, field observation) in spite of its high level of toxicity to these mammalian herbivores (Jaynes, 1975). In spite of these findings the occurrence of indirect effects of solar radiation on stand-level processes in forestheath ecosystems has not yet been verified in natural communities. The purpose of this study was to test for effects of black spruce canopy cover on measures of community structure and function via induced intraspecific variation in the sociologic dominant species. We tested for the indirect effects of black spruce cover on: (1) richness and cover of understory vascular plants, (2) biomass and mineral nutrition of the sociologic dominant species (Kalmia) and (3) organic soil respiration as an index of soil productivity. These effects were quantified through testing the following hypotheses: (1) Shade produced by the physiognomic dominant (black spruce) has measurable effects on biomass of the sociologic dominant (Kalmia) and understory species composition. (2) Variability in species richness and cover of understory herbs would be related to the amount of biomass of the sociologic dominant (Kalmia). (3) Light intensity affects Kalmia foliar C and N concentrations and the degree of changes in foliar C and N is related to leaf age. (4) Soil respiration rates vary with soil temperature, C:N ratios of litter inputs from the sociologic dominant (Kalmia) and litter of other associated species. Soil respiration rate was used as a measure of the biological activity occurring in the organic soil horizon. Although the field method of measuring soil respiration does not differentiate between soil and root respiration, it has been cited as a general index of biological activity in soil. In particular, soil respiration has been used as a surrogate for productivity (Lieth and Ouellette, 1962; Medina et al., 1980) since it is a composite measure of root activity, microbial uptake and microbial mineralization of nutrients (Gordon et al., 1987; Tewary et al., 1982). Taken together, these

281 sources of variability in soil respiration rate were assumed to act as a robust indicator of the rate of C cycling and the concomitant mobilization of associated nutrients from detritus to plant and microfaunal component of the community. Methods Study site description The study area was located in Terra Nova National Park, Newfoundland, Canada (54.0◦ W, 48.5◦ N). The area lies within the Central Newfoundland ecoregion of Newfoundland (Rowe, 1972). This region of the boreal forest receives 1000 to 1300 mm of annual precipitation and has a mean summer temperature of 12.5 ◦ C. Mineral soils tend to be acid podzols derived from granitic parent materials. Mineral soils tend to be shallow and discontinuous at the landscape level. Consequently this region is characterized by a mosaic of community types that reflect variation in the degree of soil development, drainage and fertility. Forested areas tend to be dominated by black spruce with occasional but localized dominance of balsam fir (Abies balsamea) and boreal hardwoods such as Betula papyrifera, Populus tremuloides on the more productive sites. Nitrogen limitation is the primary constraint on forest productivity in this region (Mallik, 1995). An ericaceous-conifer vegetation association known as the Kalmia-black spruce forest type (sensu Damman, 1964) is locally dominant throughout much of this ecoregion and occupies approximately 50% of the forested land base of Terra Nova National Park (Figure 1a). This forest type is also prevalent on coastal acid soils in Nova Scotia and eastern Quebec. Within the Kalmia-black spruce forest type, two sub-associations occurring on mesic soils have been described: Kalmia black-spruce forest and CladinaKalmia black spruce forest. Additionally disturbed sites in this region frequently become devoid of forest cover and typically regenerate as Cladina-Kalmia barrens (Figure 1b). The influence of disturbance history on conifer regeneration is suspected to be an important determinant of the specific vegetation type resulting from disturbances, such as fire and logging, which remove the forest canopy (Damman, 1964; Bloom and Mallik, unpublished). The study site used in this investigation was created by a fire in 1961 which burned an area of approximately 200 ha (Power, 1996). The site regenerated as a Cladina-Kalmia barren and is predominantly

treeless beyond dispersal range of seeds spread from intact forest at the disturbance edge (Figure 2a). The vegetation was characterized by sparse black spruce canopy (5 to 10% cover) with a dwarf shrub understory dominated by ericaceous species such as Kalmia (40 to 80% cover), with presence of Vaccinium angustifolium (< 20% cover), Rhododendron canadense (< 15% cover) and occasionally Ledum groenlandicum (< 10% cover). The herb layer was generally lacking and cryptogamic species such as Clandina mitis and C. rangiferina typically dominated the ground surface. Soils were highly acidic and had 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 rates of N mineralization (0.1 mg kg−1 day−1 ) (Bloom and Mallik, unpublished data). A forest-heath ecotone is evident on well-drained sites along the disturbance perimeter resulting in a narrow band of open Cladina-Kalmia-black spruce vegetation. Along this ecotone black spruce cover increased from approximately 5% toward the centre of the barren to 75% at the disturbance edge (Figure 2b). Adjacent unburned forest stands are of the Piceetum forest type (sensu Damman, 1964) which, based on charcoal macrofossils and growth increment estimates appeared to have origins in a stand replacing fire approximately 60 to 100 years prior to the fire of 1961 (Power, 1996). These stands had scattered hardwoods throughout the overstory canopy and had patchy coverage of Kalmia in the understory with relatively even distribution of understory herbs such as Cornus canadensis, Clintonia borealis, Trientalis borealis, Coptis trifoliata and Linnaea borealis. Soil pH ranged from 4 to 4.5 (measured using paste method) (Bloom and Mallik, unpublished data). Study design We used the post-disturbance gradient of black spruce cover that occurred at this site as a natural experiment on the effects of black spruce cover on otherwise treeless Kalmia heathland. There were many examples of Kalmia heath in the region but no other sites of known disturbance history were sufficiently old to yield a gradient of spruce regeneration as was observed at the present site. Because replication of sites was not possible, we studied one site intensively. We attempted to minimize variability within sampling units in order to detect canopy effects since effect sizes were unknown and 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 Terra Nova 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 of site replication requires that extrapolation of results be conservative, we emphasize that the purpose of the study was to investigate potential mechanisms operating within stands as opposed to characterizing regional level phenomena. These caveats notwithstanding, we believe the study site is representative of the many Kalmia barrens in the region. Plot layout Sample plots were established using a stratified random method. Five areas (each approximately 10000 m2 ) of heath-forest ecotone were randomly selected from ten areas of forest-heath ecotone identified within the study site using aerial photographs. The pool of potential sampling sites was determined on the basis of concentrations of black spruce trees among otherwise homogenous heathland. These randomly selected areas were identified in the field using map and compass. Only mesic, well-drained sites were used for sampling. Randomly selected areas that were too wet for inclusion were replaced by the nearest sampling areas that were characterized by upland gradients in black spruce regeneration amongst Kalmia heath. At each of the five sampling areas a transect was established by rolling out a 50 m tape from a random point in the heath toward the forest edge (Figure 2a). Transects started at a point of complete open condition and 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 sample plots were established using a series of blind random throws of a flagged marker along the gradient. Variability in the distance of the throw produced a range of 5 to 7 plot placements over the length of each 50 m transect. A total of 32 plots were established among 5 transects within the study site. Due to variability in the density of the conifer regeneration among sampling areas, some transects intercepted much more shade than others. To ensure that the plots comprising each transect represented a range of canopy shade conditions, any plots preceded by more than two plots of similar amounts of shade from black spruce were relocated to the nearest microsite with visibly different characteristics. For example, if the first three plots in a series of seven had no adjacent spruce trees then the third plot was moved as described above. No plots were located directly under black spruce trees since small-scale soil and vegetation conditions under black spruce may differ from under Kalmia heath and our objective was to determine the response of heathland vegetation and organic soil to increasing shade. Instrumentation and data collection To quantify the amount of shade provided by black spruce canopy along each transect of the shade gradient, 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 were nested within transects which in turn were randomly located within the burned habitat (marked in light gray); map is not to scale. B) Profile diagram representation of the black spruce gradient projecting out from the disturbance edge into Kalmia heath.

measured above the understory canopy of Kalmia at a height of 1 m above the ground at each sample plot. Photosynthetically active radiation was measured using a portable light meter (Decagon Sunfleck Ceptometer, Decagon Devices, Washington, USA) on a uniformly overcast day in early July between the hours of 10 a.m. and 2 p.m. These conditions were required to stabilize measurements over the course of the sampling period. Measurements were taken with the instrument beam leveled and oriented to 180 degrees in the horizontal plane. Measurements were repeated in reverse order within each transect to estimate sampling error and provide representative measurements. Completely exposed stations were used as a 100% exposure standard and all other measurements

for each transect were taken as a proportion of these measurements as an index of shade cover by the forest canopy ranging from 0 to 1.0. Vegetation sampling Species composition and percent cover of all vascular plants was determined in each 0.5 m × 0.5 m plot. Mean height, stem density and mean stem basal diameter of the dominant understory vegetation (Kalmia) were recorded in each plot. These parameters were used to calculate a biomass index based on stem volume according to the following formula: Kalmia stem volume (cm3 ) = (π(d/2)2 × h)/3 × n,

(1)

284 where: d = mean stem diameter (cm), h = mean stem height (cm), n = stem density (count m−2 ) To determine the mineral nutrition of the dominant understory species across the canopy cover gradient, foliage of three age classes of Kalmia was collected in each plot. Foliage collection followed the method of Small (1972). Within each plot Kalmia first year leaves, mature leaves and leaf litter were gathered as was a 0.05 m × 0.05 m × 0.05 m humus sample collected from the F layer of the organic soil horizon below the litter layer. Litter types for each location were identified to species and Kalmia tissue samples were placed in plastic zip lock bags and stored in a refrigerator for four days prior to air-drying. All tissues and humus samples were analyzed for percent C and N concentrations using a LECO gas analyzer (LECO Instruments, Mississaga, Ontario). The C:N ratio of leaf matter and organic soils was used as an index of litter and organic matter quality. Differences in foliar nitrogen concentrations in senescing, mature and first year leaves were used to estimate intraplant foliar N concentrations across the leaf life cycle. Concentration changes from first year leaves to mature leaves were corrected for the initial leaf N using the following formula: (First year leaf N – mature leaf N)/first year leaf N. Similarly, percent N conservation prior to abscission (i.e. the difference between N concentrations in mature leaves and senescent leaves) was estimated by calculating the relative difference in N concentration of mature and litter leaf tissue using the following formula: (Mature leaf N – litter leaf N)/ mature leaf N. Soil respiration rate was recorded at each plot using a portable infrared gas analyzer (IRGA, Nortech, Ottawa, Ontario) (Parkinson, 1981). Units of measurement were g CO2 m−2 h−1 . Measurements were centered on the 0.05 m × 0.05 m area from which litter samples were collected and were made prior to extracting the 5 cm deep organic soil sample described above. A 0.00785 m2 surface area of soil was measured by pressing the sampling chamber 1 cm into the organic layer, following removal of the dry litter layer. This was necessary to create a seal and allow the rate of partial CO2 pressure in the chamber to stabilize. Measurements were made in mid-June and again in early July. Moisture contents at the various stations was assumed to be made homogenous by periods of heavy rain prior to sampling. All soils were moist and appeared to be at field capacity. In order to ensure that all plots were measured in one day and under the same

weather conditions replication of sampling stations on the date of data collection was not possible. Instead the stations were re-surveyed at a later date under similar weather conditions to confirm the reproducibility of the data. Repeated observations for each plot were averaged for use in data analyses. In addition to soil respiration, soil temperature and organic matter depth were measured simultaneously with soil respiration in each plot. These data were used to correct soil respiration measurement for plot level variation in soil depth and temperature. Statistical analysis Step-wise hypotheses were tested using a series of regression analyses and ANOVA. The residual values of soil respiration rate were used as the dependent variable for testing of sequential hypotheses. Quadrat data from the five transects were pooled for all analyses. The specific analytical methods employed for testing each hypothesis are outlined below. Relationships between PAR (a random predictor variable) and each of Kalmia biomass, richness of herbaceous species and cover of herbaceous plants (as response variables) were tested using the curve estimation feature of SPSS version 9.0 (SPSS, 1998) to test Hypothesis 1 (that shade effects of black spruce would affect biomass of the sociologic dominant (Kalmia) and understory species composition.). Kalmia biomass index was log transformed prior to analysis. Subsequent to testing Hypothesis 1 and saving the residuals, Hypothesis 2 (that additional variability in herbaceous species richness and cover would be related to the amount of overstory cover from Kalmia) was tested through Pearson correlation analysis using Kalmia above-ground biomass as the random predictor variable and residuals of herb richness and cover as response variables. Hypothesis 3 (that light intensity affects Kalmia foliar C and N concentrations in first year leaves, mature leaves and litter) was tested using two-way repeated measures analysis of variance on C concentration, N concentration and C:N ratio of three age classes of foliar 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 the Huynh-Feldt correction to the degrees of freedom was used for significance testing (SPSS, 1998). Lastly, Hypothesis 4 (that the quality of Kalmia litter and abundance of litter of other species would affect soil respiration rate) was tested by using the

285 litter C:N ratio of Kalmia leaves, organic soil C:N ratio and the proportions of cover of other species/litter types (Cladina lichen, feathermosses and birch/red maple) as predictors of soil respiration in a multiple regression. Since the structure and performance of multiple regression models can be sensitive to the way factors are selected, no stepwise procedure for including variables was used. Factors were added together in the model and partial correlations with the response variable were used as post-hoc descriptors of the relationships of soil respiration to the prevalence of each factor. Based on the outcome of these hypotheses, a general linear model of soil respiration rate as a function of PAR was tested using simple linear regression. Results Vegetation composition and structural responses to light exposure Floristic responses Kalmia was the dominant species in all plots but its biomass varied in relation to black spruce cover (Figure 3a). Log transformed Kalmia biomass had a 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 angustifolium) were occasionally present in the open heath conditions where they achieved a maximum percent cover of approximately 10% (data not shown). Total herb cover (maximum = 67%) had a significant unimodal response to PAR (F(2,28) = 3.52, P = 0.043; Appendix II) which peaked at intermediate levels of black spruce cover (45% available PAR). With the exception of a single outlying data point, the pattern is suggestive of a simple unimodal response (Figure 3b). Similarly, herb species richness peaked under partial shade of black spruce along a cubic response curve (F(3,28) = 3.34, P = 0.034) (Figure 3c, Appendix III). Trends in cover were primarily a reflection of patterns in the abundance and cover of Clintonia borealis which had the highest prevalence of herbs encountered in the plots (data not shown). Cornus canadensis, Maianthemum canadense, Trientalis borealis and Coptis trifoliata were also frequently occurring but had lower cover values. Correlation analysis controlling for the effect of black spruce cover detected no significant variability in the residuals of herb richness and cover that was

Figure 3. Effects of photosynthetically active radiation (PAR) on forest understory. A) Ln-transformed Kalmia biomass index responded curvilinearly to the gradient. B) Herb richness showed a tendency to peak under partial black spruce cover. C) Cover of herb species was also favoured by partial canopy cover.

286 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 sampling plots shifted from an assemblage of lichens dominated by Cladina species (C. stellaris and C. rangiferina) in the open condition to a lichen-moss-Kalmia litter ground cover at intermediate light levels which was dominated by C. rangiferina and Pluerozium schreberi (Figure 4). As PAR declined under higher levels of canopy cover, ground cover became dominated by Kalmia leaf litter with increasing representation of mosses such as P. schreberi. Litter cover near the disturbance edge tended to have additional constituent species and was either heavily dominated by pure Kalmia litter or was a mixture of Kalmia litter and litter from nearby hardwood canopy species such as paper birch (Betula papyrifera) and red maple (Acer rubrum). Vegetative responses to increasing levels of shade are summarized in Table 1. Leaf and litter quality responses to PAR Nitrogen concentrations of Kalmia leaves declined significantly with increasing leaf age (F(2,29) = 5.23, P = 0.01) (Figure 5a; Appendix IV). First year leaves had the highest N concentrations and the concentrations were strongly inversely related to PAR (r = −0.71, n = 31, P < 0.001). In spite of the strong correlation, the low slope of the scatter points indicates little 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 concentration as PAR increased but the magnitude of the difference between age classes increased significantly at high levels of PAR. These data indicate that Kalmia leaves had relatively uniform rates of N conservation from mature to new tissues across the light gradient (r = 0.07, n = 32, P = 0.36) with a mean of a 53% (+ 0.01 s.d.) lower N concentration in mature leaves compared to new foliage. In contrast Kalmia leaves had progressively higher rates of N conservation between the stages of maturity and abscission under increasing light exposure (r = 0.39, n = 32, P = 0.014). Repeated measures ANOVA did not detect significant differences in total C concentrations among age classes nor did total C measurably interact with PAR (Figure 5b; Appendix V). The C:N ratio of first year leaves and mature leaves varied little across the PAR gradient (Figure 5c) but the C: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 intensity affects Kalmia leaf C and N concentrations was accepted. Repeated measures ANOVA results detected strong interactions of foliar C:N ratios in successive ages of leaves with PAR (Appendix VI). The magnitude of main effects and interactions of leaf age class and PAR on foliar N and C:N ratio are summarized for each nutrient variable in Table 2. The percent change in concentrations at low light intensity compared with high light intensity were large for N and for the C:N ratio but the magnitude of the change depended on leaf age. Largest effects of light intensity were observed in litter rather than live leaves. Soil respiration responses to leaf types and litter quality Multiple linear regression analysis revealed evidence that soil respiration was related to litter quality and vegetation cover (Appendix VII). This pattern was related 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 amount of hardwood leaf litter types showed no raw or partial correlation with soil respiration and were uninfluential in the model (Beta < 0.10). The resulting linear model (Equation 2) accounted for 38% of the observed vari2 = 0.28, ability in soil respiration (R 2 = 0.38, R(adj.) Appendix VII). The hypothesis that litter quality of the dominant species affects soil respiration was accepted. Due to the underlying effect of PAR on all of the component variables in Equation 2, a more general linear model was tested using PAR as a single predictor of soil respiration. In general closed-canopy forest-heath conditions (25 to 35% PAR) had soil respiration rates approximately twice that of the adjacent unshaded open heath conditions (Table 1, Figure 6). Adjustment of the raw coefficients of determination (R 2 ) for use in prediction revealed that this model (Equation 3, 2 = 0.30, Appendix VIII) was statistically sigR(adj.) nificant and explained similar amounts of variability in soil respiration than did the more complex model 2 = 0.28). Parametsummarized in Equation 2 (R(adj.) ers of this parsimonious model are shown in Table 3. Model standard deviations are based on cumulative variance of slope estimates. Models assume no error in 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 of PAR near the disturbance edge. Kalmia litter had peak prevalence at low and moderate levels of PAR. Kalmia litter underlain by pleurocarpous was 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 in Kalmia heath

Proportion of maximum PAR Ground cover Herb richness Herb cover (%) Litter C:N∗ Soil respiration rate (g m−2 h−1 )

Kalmia heath

Kalmia heath with scattered black spruce

Open Kalmia-black spruce forest

Closed canopy forest

0.72 ± 0.10 Cladina-Kalmia litter 0.63 ± 0.26 1.5 ± 0.7 94.7 ± 11.4 0.96 ± 0.15

0.65 ± 0.07 Cladina-PleuroziumKalmia litter 1.3 ± 0.29 9.2 ± 2.9 70.0 ± 6.4 1.07 ± 0.07

0.64 ± 0.12 pure Kalmia litter 2.8 ± 0.80 14.2 ± 0.7 68.5 ± 9.2 1.32 ± 0.11

0.39 ± 0.02 Kalmia-hardwood litter 2.8 ± 0.85 35.8 ± 12.8 69.2 ± 13.5 1.45 ± 0.19

∗ 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 were calculated by averaging nutrient values > 0.80 PAR and < 0.3 PAR respectively. Values are mean ± s.d. Nutrient

Leaf age class

Concentration

Concentration at high PAR

Concentration at low PAR

% Change (high to low PAR)

Nitrogen (g g−1 leaf)

First year Mature Litter

2.9 ± 0.44 1.3 ± 0.21 0.8 ± 0.28

2.37 ± 0.02 1.14 ± 0.04 0.56 ± 0.07

3.13 ± 0.07 1.57 ± 0.08 1.05 ± 0.14

32.1 37.7 90.9

Carbon (g g−1 leaf)

First year Mature Litter

52.11 ± 0.19 53.23 ± 0.17 53.14 ± 0.20

52.32 ± 0.40 53.72 ± 0.324 53.10 ± 0.060

51.85 ± 0.28 53.15 ± 0.26 52.15 ± 0.16

−0.76 −0.93 −1.9

C:N ratio

First year Mature Litter

18.51 ± 3.35 40.68 ± 6.63 75.85 ± 27.54

22.58 ± 1.53 47.53 ± 1.53 103.30 ± 13.70

16.62 ± 0.40 34.21 ± 1.80 54.48 ± 7.62

−26.2 −28.0 −47.2

288 Table 3. Parameter estimates for multiple regression model components explaining variability in soil respiration Parameter (constant) Kalmia litter C:N ratio Organic soil C:N ratio Hardwood leaf litter prevalence Feathermoss prevalence Cladina lichen prevalence

Beta

Std. error

1.460

0.387

−0.356

0.002

0.006

Std. Beta

r

Partial r

3.770

0.001

−0.275

−1.498

0.146

−0.457

−0.282

0.010

0.098

0.547

0.589

−0.150

0.107

−0.072

0.432

−0.032

−0.172

0.865

0.230

−0.034

−0.365

0.168

−0.472

−2.169

0.039

−0.171

−0.391

−1.229

0.609

−0.511

−2.018

0.054

−0.372

−0.368

y = 1.46 − 0.366(Kalmia litter C:N ratio)

(2)

−0.365(percent moss cover) −1.23(percent Cladina lichen cover) + 0.75 s.d.1 y = 1.60 − 0.744(proportion of available PAR) +0.17 s.d.1

p

t

(3)

Soil temperature ranged from 9 to 15 ◦ C but was inversely related to soil respiration (r = −0.337, n = 32, P = 0.03). Partial correlation controlling for litter C:N ratio in the relationship between soil respiration and temperature was not significant (r = −0.20, n = 32, P = 0.143) indicating that the negative relationship between temperature and respiration was driven in part by the indirect association of temperature with litter quality. On this basis, the hypothesis that increasing soil temperature would positively affect soil respiration was rejected.

Discussion The results of this study indicate that shade strongly influences floristic composition of vascular plants as well as phenotypic properties of the sociologic dominant (Kalmia). The hypothesis that black spruce cover structures species composition was accepted on the basis of the observed correlations of vascular plant cover and diversity with the black spruce cover. We attribute a causal relationship to the correlation because these species (C. borealis, M. canadense, and

C. canadensis) are generally known to be forest plants that are most productive in partial shade (Crowder and Taylor, 1984; Hoefs and Shay, 1981; Shirley, 1945; USDA, 2002) and would therefore be expected to have maximum abundance at intermediate levels of photosynthetically active radiation. The dependence of these understory herbs on shade cover is further emphasized by the monotonic increase in herb cover with increasing Kalmia biomass. This relationship suggests that these forest herbs proliferate in shade in spite of the effects of above-ground competition from ericaceous biomass and associated below-ground competition among roots within these small plots. In the absence of a tree canopy or dense shrub cover to provide shade, these forest plants appear at much reduced abundances in Kalmia heath relative to Kalmia-black spruce forest. While the simplest explanation for this relationship is that herbs have responded positively to the provision of shade cover by black spruce, the specific mechanism may include a chemical aspect whereby inputs into the soil from the litter of canopy species in the mature forest enhance conditions for understory species. Paper birch (Betula papyrifera may be particularly important in this regard since its litter is known to be relatively rich in macronutrients such as N and Ca (Roberts et al., 1998). In the absence of such canopy cover, shade intolerant plants were conspicuously absent and the ground cover was dominated by a thick mat of Cladina lichens (C. stellaris, C. mitis and C. rangiferina)

289 Table 4. Parameter estimates for linear regression model components (Soil respiration versus PAR) Parameter

Beta

Std. error

Std. Beta

(constant) PAR

1.598 −0.744

0.134 0.196

−0.569

with sparse cover of ericaceous vegetation dominated by Kalmia. Kalmia dominated all plots but, like the herbaceous plants, its cover and vigour (as indicated by its biomass index) peaked at intermediate levels of shade. Because of the apparent influences of black spruce cover on herbaceous and woody plants, we concluded that the development of structural properties of the flora that are typical of Kalmia-black spruce forest (specifically plant cover and biomass) were strongly contingent on the establishment of tree cover. A corollary of this conclusion is that Kalmia heath is not a functional equivalent to black spruce relative to the facilitation of local vascular plant diversity and abundance. The absence of black spruce or other canopy-producing species in burned Kalmiablack spruce sites will likely result in the colonization limitation of forbs that benefit from forest cover. In the absence of forest regeneration, it is typically expected that an alternate suite of species would colonize the sparsely populated niche space of the open heath as has been observed in other examples of shifting dominance and plant community invasion (Rejmének, 1989). Because vegetation cover and biomass of the dominant species was not constant across the gradient, the findings suggest that factors other than light play a role in vegetation development. The soil litter quality and respiration data suggest that black spruce cover may indirectly affect soil productivity. This is because in addition to variation in vigour, several phenotypic qualities of the sociologic dominant species (Kalmia) were strongly associated with black spruce cover. Our data suggest that the influence of shade on Kalmia leaf and litter characteristics may feed back on soil fertility just as the litter quality of dominant functional groups have been shown to affect soil fertility and respiration in other systems (Gordon et al., 1987; Read, 1992; Sing and Gupta, 1977; Tewary et al., 1982; Wardle et al., 1997; Weber, 1985). Under increasing shade, Kalmia exhibited less nitrogen conservation between leaf age classes and higher litter quality (as evidenced by lower C:N ratios) than

t 11.890 −3.788

p

r

0.00 0.001

−0.569

in unshaded heath conditions. Assuming that litterfall is constant across the light gradient, this alteration of Kalmia’s litter quality translates into a two-fold decrease in annual nitrogen inputs into the organic soil horizon of the open heath compared to shaded heath. Similarly, open heath conditions produced Kalmia leaves having a three-fold increase in C:N ratio of recently fallen litter inputs as compared to C:N ratios of recently fallen litter under shaded conditions. Such high rates of C inputs in the absence of high respiration rates indicates a failure of open heath to sustain the same levels of carbon cycling observed in adjacent forests where Kalmia litter C:N ratios are lower. Addition of tissues with high C:N ratios are typically expected to increase soil microbial respiration through the addition of carbon as an energy source (Blum, 1998; Bradley et al., 1997). Theoretically, high soil respiration rates are thought to cause concomitant N immobilization in the biomass of the growing microbial population (Kimmins, 1997). However, this relationship can be reversed when litter substrates are composed primarily of secondary compounds such as polyphenolic acids and lignin which are resistant to microbial degradation (Hättenschwiler and Vitousek, 2000). Links between foliar phenol concentrations and UV exposure have been made in several cases (Hättenschwiler and Vitousek, 2000). Since we observed highest respiration rates when the dominant plant litter had low C:N ratios and these low C:N ratios occurred under shaded conditions, we suspect that the higher carbon concentrations observed in unshaded Kalmia litter failed to increase soil respiration because the unshaded leaves are higher in phenolic compounds associated with UV exposure. Such phenolic compounds are known to inhibit mycorrhizal activity in Kalmia soils (Yamasaki et al., 1998) and N mineralization in other heathland systems (Berendse et al., 1989; Northup et al., 1997). Conversely, the higher respiration rates associated with lower C:N ratios of litter under spruce cover may result from increased microbial activity following addition of labile C to heathland soils as observed by Read (1992). There is

290

Figure 6. Relationship between soil respiration and PAR along a black spruce canopy gradient of post-fire Kalmia-black spruce community in Newfoundland. Soil respiration declined with increasing PAR and 30% of the variability in soil respiration rates was related to PAR (P < 0.05).

Figure 5. Kalmia foliar N and C in relation to leaf age and light exposure. A) Foliar N concentrations varied by age class but the magnitude of differences varied with PAR. B) Foliar concentrations showed no clear differences among age classes or in relation to PAR. C) Foliar C:N ratio showed large differences among leaf age classes which also varied with PAR. Low light conditions show little difference in C:N ratio of leaves irrespective of leaf age. In contrast, litter produced in full sunlight undergoes stepwise increases in C:N ratio with increasing tissue age.

a possibility that the relatively low C:N ratio of litter from B. papyrifera occurring sparsely throughout the mature forest of this study site was also contributing to higher soil respiration rates near the disturbance edge since the presence of this litter may locally enrich soils (Roberts et al., 1998). This explanation is supported by the findings of Bradley et al. (1997) that, from a microbial productivity and nutrient cycling point of view, Kalmia organic soils are limited by the availability of labile carbon and are sensitive to carbohydrate inputs. Because carbon cycling is linked tightly to nitrogen cycling in boreal organic soils, carbon sequestration can be expected to induce nitrogen sequestration as well. These data point to a reduced level of soil productivity in unshaded heathland which is corroborated by the observation of reduced vegetation biomass and total herb cover at highest levels of PAR. We thereby conclude that canopy cover of black spruce and associated hardwood species such as B. papyrifera can have strong indirect feedbacks on soil processes via their respective influences on the quality of Kalmia litter inputs and direct inputs of their own relatively rich litter in Kalmia-black spruce forests. In general terms, these data suggest that the physiognomic dominant species (black spruce) indirectly controls the growth parameters and litter quality of the sociologic dominant species (Kalmia). In turn, variability in the quality of litter inputs of Kalmia appears to strongly affect organic soil productivity. This preliminary investigation provides evidence that the mechanism by which Kalmia barrens are maintained as moribund heath is driven, in part, by autogenic responses of Kalmia to environmental stimuli. These

291 findings point to a need to understand whether or not unforested Kalmia heath preclude the regeneration of productive forests in the future. Further research into this potential mechanism of site degradation is recommended in order to determine the specific chemical processes driving the patterns observed here. Such data are necessary to determine the landscape-level impacts of forest canopy removal on long-term species richness and productivity of Kalmia-black spruce stands in this region.

Acknowledgements The research was supported by a Discovery Grant of the Natural Science and Engineering Council (NSERC) awarded to A.U. Mallik. We thank Mr Randy Power of Parks Canada for his interest and cooperation in this research and Terra Nova National Park for providing logistical support during the field work. We thank Dr Roger Latham of Continental Conservation, Swarthmore, USA, Dr Heidi Schraft of the Biology Department, and Dr Tom Hazenberg of the Faculty of Forestry and the Forest Environment, Lakehead University for their comments on an earlier draft of the manuscript.

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Appendix I. Summary results of ANOVA for curvilinear regression of Kalmia biomass (log scale) against light intensity (PAR) Source PAR (quadratic) Error

Sum of Squares

df

Mean Square

F

p

R2

2 R(adj.)

5.23283

0.0115

0.27

0.21

1.9422288

2

0.97111439

5.3818491

29

0.18558100

Appendix II. Summary results ANOVA for curvilinear regression of herb cover against light intensity (PAR) Source PAR (quadratic) Error

Sum of Squares

df

Mean Square

F

p

R2

2 R(adj.)

3.52320

0.0427

0.20

0.14

1555.1512

2

777.57560

6400.3488

29

220.70168

Appendix III. Summary results ANOVA for curvilinear regression of herbaceous species richness against light intensity (PAR) Source PAR (cubic) Error

Sum of Squares

df

Mean Square

F

p

R2

2 R(adj.)

3.33552

0.034

0.25

0.18

16.817330

3

5.6057767

47.057670

29

1.6806311

293 Appendix IV. Summary results of Repeated measures ANOVA for foliar N concentration among leaf age classes Source

Sum of Squares

df

Mean Square

F

p

Partial Eta Squared

Leaf age class Age∗ PAR Error

15.524 0.394 3.402

1.370 1.370 39.739

11.329 0.287 0.08561

132.336 3.356

0.000 0.062

0.820 0.104

Appendix V. Summary results of Repeated measures ANOVA for foliar C concentration among leaf age classes Source

Sum of Squares

df

Mean Square

F

p

Partial Eta Squared

Leaf age class Age∗ PAR Error

4.455 0.05743 45.678

2.000 2.000 58.000

2.227 0.02872 0.788

2.828 0.036

0.067 0.964

0.089 0.001

Appendix VI. Summary results of Repeated measures ANOVA for foliar C:N ratio among leaf age classes Source

Sum of Squares

df

Mean Square

F

p

Partial Eta Squared

Leaf age class Age∗ PAR Error

1198.936 4116.958 9649.340

1.085 1.085 31.453

1105.416 3795.828 306.782

3.603 12.373

0.064 0.001

0.111 0.299

Appendix VII. Summary results of ANOVA of multiple regression of soil respiration versus litter inputs and microsite vegetation Source

Sum of Squares

df

Mean Square

F

p

R2

2 R(adj.)

Std. error

Model Error Total

1.476 2.462 3.938

5 26 31

0.295 0.0947002

3.116

0.025

0.38

0.28

0.31

Appendix VIII. Summary results of ANOVA of multiple regression of soil respiration versus litter inputs and microsite vegetation associations Source

Sum of Squares

df

Mean Square

F

p

R2

2 R(adj.)

Std. error

Model Error Total

1.274 2.664 3.938

1 30 31

1.274 0.08879

14.349

0.001

0.32

0.30

0.31