Open Journal of Forestry
2013. Vol.3, No.3, 88-98
Published Online July 2013 in SciRes (
Copyright © 2013 SciRes. 88
The Relative Importance of Natural Disturbances and Local Site
Factors on Woody Vegetation Regeneration Diversity across a
Large, Contiguous Forest Region
Gerardo P. Reyes1,2*, Daniel Kneeshaw1, Louis de Grandpré1,3
1Department of Biological Sciences, Centre for Forest Research, University of Quebec in Montreal, Montreal,
2Faculty of Interdisciplinary Studies, Lakehead University, Orillia, Canada
3Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, Ste-Foy, Canada
Email: *,,
Received February 3rd, 2013; revised April 21st, 2013; accepted May 11th, 2013
Copyright © 2013 Gerardo P. Reyes et al. This is an open access article distributed under the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the
original work is properly cited.
Stand-level diversity after natural disturbance can potentially differ across a large, contiguous forest re-
gion despite being dominated by the same canopy species throughout as differences in disturbance types
and local site conditions can regulate species distribution. Our main objective was to examine the relative
importance of natural disturbances (spruce budworm (Choristoneura fumiferana) outbreak, windthrow,
and their interaction) and local site factors (climate, physiography, and stand structure and composition
variables) on woody vegetation diversity among three, physiographically distinct locations across a large,
contiguous forest region. Seventy-six Abies balsamea-Betula spp. stands affected by natural disturbance
were compared and analysed using canonical ordination methods, diversity indices, and ANOVA. Dif-
ferent combinations of factors were important for vegetation re-establishment at each location. Differ-
ences in alpha (α), beta (β), gamma (γ), Shannon’s H’, and evenness (J) diversity indices were observed
among locations across the study region. Our findings indicate that while certain processes are important
for maintaining canopy dominance by Abies balsamea and Betula spp. throughout the region, different
combinations of factors were important for creating variation in woody species diversity among locations
that resulted in greater woody species diversity at the regional scale.
Keywords: Regeneration; Natural Disturbance; Environmental Factors; Species Diversity; Eastern Boreal
Mixedwood Region
Climate determines the regional species pool (Dansereau,
1954; Neilson et al., 1992; Messaoud et al., 2007). However,
woody species distribution and abundance across the landscape
is largely determined by the disturbance regime (Gromtsev,
2002; Belote et al., 2009). Consequently, a distinct spatio-tem-
poral arrangement of woody species is often observed at local
scales due to variation in disturbance type, severity, and fre-
quency across the landscape (Chen & Popadiouk, 2002; Reyes
et al., 2010). Apart from natural disturbances, local site factors
also play key roles in forest development, as they are capable of
influencing the disturbance regime itself, and can directly affect
species diversity after disturbance (Peterson, 2000; McGuire et
al., 2002; Wang et al., 2006).
Different types of disturbance influence regeneration patterns
in distinctive ways depending on the severity of effects on for-
est vegetation and stand structure, and the variation in the tem-
poral release of newly available resources. Windthrow and
spruce budworm (Choristoneura fumiferana) outbreak, for
example, have been shown to result in alternative successional
trajectories in boreal ecosystems due to differences in the de-
gree of soil disturbance and in the timing of tree mortality
(Krasny & Whitmore, 1992; Nagel & Diaci, 2006). In the case
of windthrow, this disturbance type can substantially alter can-
opy species dominance whereas budworm damage can simply
delay or promote development towards late-succession condi-
tions (Bergeron, 2000; Chen & Popadiouk, 2002). However,
variation in forest regeneration among stands experiencing the
same disturbance type can also occur because of differences in
local site conditions (Turner et al., 1997; Reyes & Kneeshaw,
2008). For example, where advance regeneration is abundant,
windthrow may cause only structural versus compositional
changes in the tree canopy (Peterson, 2000; Reyes et al., 2010).
Moreover, the sub-canopy tree and shrub community can dis-
play variation in responses to natural disturbances depending on
light availability and level of soil disturbance; and depending
on the relative speed of development and growth after distur-
bance, can ultimately impact the composition of the regenerat-
ing tree canopy (Gray et al., 2005; Hart & Chen, 2006). Other
local site factors such as pre-disturbance stand composition,
physiography, and stand structural characteristics have been
shown to affect woody vegetation diversity after natural distur-
bance at the stand scale (Dupont et al., 1991; Osumi et al., 2003;
*Corresponding author.
Rodriguez-Garcia et al., 2011). However, it is unclear if the
same factors play key roles in determining re-vegetation pat-
terns throughout an entire forest region. Factors can differ in
importance among locations across a region, operate at local or
regional scales, and can work synergistically to affect species
diversity (Wimberly & Spies, 2001; Hillebrand & Blenckner,
2002; Huebner & Vankat, 2003). Examining woody vegetation
distribution after natural disturbances at various locations
across a large, contiguous forest region dominated by the same
canopy species can thus help to resolve potential contrasts by
determining the different factors responsible for any observed
variation across the region, for differences in responses to the
same factors, or conversely, potentially link fine and broad-
scale vegetation recovery patterns to a few important factors
that have consistent effects on woody species diversity across
the region as a whole.
The purpose of our study is to document the relative impor-
tance of natural disturbances and local site factors on woody
vegetation regeneration diversity among three, physiographi-
cally distinct locations across a large, contiguous forest ecosys-
tem dominated by the same canopy species throughout. We
specifically addressed the following questions: is the canopy
composition maintained after disturbance or are different suc-
cessional trajectories occurring? Does the type of natural dis-
turbance determine woody species diversity or do local site
factors more strongly influence regeneration distribution? Al-
ternatively, do natural disturbances work synergistically with
local site factors in determining woody species diversity?
Lastly, do different combinations of disturbances and local site
factors influence woody species diversity for specific locations
or can a few common factors explain species distribution across
the region? We hypothesized that given the physiographical
differences among locations across the region, that different
combinations of factors would be responsible for woody spe-
cies diversity after natural disturbance at the local level; and
consequently, that if different factors influence regeneration
dynamics at local scales, it is likely that species diversity will
differ across the region. Thus, although woody species diversity
should be the highest at the regional scale, diversity should also
reflect the intra-regional differences in disturbance history and
the unique local site characteristics of these forests.
Study Area
The Abies balsamea-Betula spp. boreal mixedwood zone
spans east to west across southern Quebec, Canada from 46˚ to
50˚N and 64˚ to 80˚W (Figure 1). It encompasses 23.8 million
ha and represents 18.6% of the forested land of the province
(MRNQ, 2003). The physiography of the region is highly vari-
able. The western portion is continental, and is relatively flat to
rolling. Topography becomes increasingly hilly to montane
towards the east, as the eastern portion of the region includes
the northeastern limit of the Appalachian mountain chain that
runs southwest into the United States. The eastern portion also
borders the Gulf of St. Lawrence, and thus contrasts with the
western portion of the region by having a maritime influence.
Elevations of forested areas range from 80 to 400 m in the west,
and from sea level to 900 m in the east. Surface deposits are
mostly glacial till or of lacustrine origin (Robitaille & Saucier,
1998). The soil moisture regime is classified as xeric-mesic to
mesic, while soil drainage ranges from imperfect to rapid.
Numerous disturbances such as fire, insect pests, and wind-
throw occur at varying frequency and severity in eastern boreal
mixedwoods. The current return interval length for catastrophic
Figure 1.
Study locations within the boreal mixedwood region of Quebec, Can-
ada. (A) continental—Abitibi-Temiskaming; (B) northern coastal—the
North Shore; (C) southern coastal—the Gaspé Peninsula.
fires across the region ranges from 170 to 645 years (Bergeron
et al., 2006), suggesting that less severe, but more frequent
disturbances now assert greater influence on post-disturbance
boreal mixedwood dynamics than in the recent past. Thus, we
focused our attention on three types of non-fire disturbances
that are common to boreal mixedwood forests: spruce budworm
(Choristoneura fumiferana) outbreak, windthrow, and their
interaction (nb., where a stand affected by spruce budworm
outbreak is then subjected to windthrow prior to canopy recov-
We sampled within three physiographically distinct, widely
dispersed locations (between 200 and 500 km) across the boreal
mixedwood region of Quebec, Canada (Figure 1). The western
sites are located in the Abitibi and Temiskaming municipalities
(77˚30' to 79˚10'W and 47˚30' to 48˚20'N). These sites have a
flat to rolling topography and are influenced by continental
climate conditions. The two eastern coastal locations both have
hilly to rolling topography but differ mainly by latitude and
elevation. The northern coastal sites are situated along the north
shore of the St. Lawrence River, within the Haute Côte Nord
and Manicouagan municipalities, and between 48˚30' to 50˚00'
N and 68˚00' to 69˚50'W. Stands in this location are near the
northern limit of the boreal mixedwood region. The southern
coastal sites are situated within the southern part of the Gaspé
Peninsula, along the Chaleur Bay area of the Atlantic Ocean
(between 48˚10' to 48˚35'N and 65˚45' to 66˚15'W). Other cli-
mate, physiographic, and forest structure and composition
characteristics are compared among geographic locations in
Table 1.
Relative species composition of the forest canopy can be
quite variable within this forest type. We limited sampling to
stands having two of the more common relative species compo-
sitions: stands were either conifer-dominated (75% density of
conifers in canopy) or mixed coniferous-deciduous (50% - 74%
density of conifers in canopy) prior to disturbance. In all cases,
Abies balsamea, Betula papyrifera, and Betula alleghaniensis
dominated the forest canopy prior to disturbance, and repre-
sented at least 60% of the coniferous and deciduous compo-
nents within each stand, respectively. Picea glauca, Picea
mariana, and Acer rubrum were also abundant in some sites
while Thuja occidentalis, Pinus resinosa, Pinus strobus, Pinus
Copyright © 2013 SciRes. 89
Copyright © 2013 SciRes.
Table 1.
Comparison of climate, physiographic, and forest structure and composition variables at each location using factorial ANOVA. Values in parentheses
indicate ±1 Standard Error of the mean. Unlike letters along a row indicate values are significantly different among locations (p < 0.05).
Continental Northern coastal Southern coastal
Annual rain (mm) 691.3 (5.2) a 691.0 (7.5) a 724.3 (2.0) b
Annual snow (mm) 274.3 (6.2) a 303.4 (4.5) b 238.6 (0.6) c
Annual precipitation (mm) 965.6 (11.4) ab 988.9 (10.3) b 963.1 (1.4) a
Annual temperature (˚C) 2.1 (0.1) a 2.2 (0.1) a 3.6 (0.1) b
Mean monthly temperature-summer (˚C) 16.3 (0.1) a 15.3 (0.1) a 16.6 (0.1) a
Mean monthly temperature-winter (˚C) 10.4 (0.1) a 8.8 (0.1) b 7.3 (0.1) c
Mean windspeed (km·h1) 12.9 (0.1) a 15.6 (0.0) b 18.7 (0.1) c
Maximum windspeed (km·h1) 52.8 (0.7) a 75.6 (0.1) b 76.0 (0.2) b
Maximum gust speed (km·h1) 98.4 105.2 no data
Elevation (m) 311.2 (11.8) a 274.2 (25.4) a 421.4 (9.7) b
Slope* (%) 1.0 (0.0) a 1.2 (0.2) a 2.1 (0.1) b
Latitude (degrees) 47.3 (0.1) a 49.0 (0.1) b 48.5 (2.3) b
Longitude (degrees) 78.4 (0.1) a 68.8 (0.1) b 66.1 (2.8) c
Soil drainage 3.5 (0.2) a 3.1 (0.2) a 2.3 (0.1) b
Forest structure and composition
Mean disturbance area (ha) 11.6 (1.6) ab 8.9 (1.7) a 13.2 (1.0) b
Snag density (ha1) 138.2 (17.8) a 294.1 (33.3) b 499.3 (29.4) c
Course woody debris density (ha1) 1176.4 (10.9) a 1729.1 (82.2) b 2159.9 (105.2) c
Percentage of trees uprooted 28.0 (3.5) a 31.9 (3.4) a 37.2 (1.9) a
Decay class average 11.2 (0.1) a 11.2 (0.1) a 10.4 (0.1) b
Tree regeneration density (ha1) 126 + 907.9 (1936.6) a 36825.6 (2593.6) b 15284.5 (1525.3) a
Shrub regeneration density (ha1) 11982.9 (2288.1) a 33,969.6 (3407.6) b 7 454.0 (732.1) a
Total regeneration density (ha1) 24890.7 (2043.0) a 70,895.2 (3279.9) b 22 738.6 (1463.2) a
Coniferous legacy tree density (ha1) 1.3 (.3) a 8.9 (1.2) b 0.1 (0.2) c
Deciduous legacy tree density (ha1) 0.1 (0.03) a 2.7 (0.6) b 0.2 (0.2) a
Crown cover of coniferous legacy trees (%) 3.5 (0.8) a 3.5 (0.9) a 4.2 (1.0) a
Crown cover of deciduous legacy trees (%) 1.6 (0.7) a 1.7 (0.6) a 6.8 (1.2) b
Stand density prior to disturbance (ha1) 926.6 (89.3) a 1474.0 (83.8) b 1718.7 (80.7) b
Note:Insufficient data to include in analyses. *1: 0˚ to 10˚, 2: >10˚ to 20˚, 3: >20˚ to 30˚, 4: >30˚ to 40˚, 5: >40˚; 2: good, 3: moderate; 4: imperfect; See Imbeau & Des-
rochers (2002).
banksiana, Larix laricina, Acer saccharum, Fraxinus ameri-
cana, Fraxinus nigra, Populus balsamifera, and Populus
tremuloides were occasionally present.
Sampling Methods
Disturbance type, climate, and physiographical data were de-
rived from digitised aerial photos, eco-forestry maps, or
sourced from various provincial and federal government agen-
cies (MNRQ, 2003; Environment Canada, 2004), with the ex-
ception of slope and elevation, which were determined on site
using a clinometer and GPS unit, respectively. A total of 76
sites affected by spruce budworm outbreak, windthrow, or their
interaction were examined: 24, 22, and 30 sites for the conti-
nental (Abitibi-Temiskaming), northern coastal (North Shore),
and southern coastal (Gaspé Peninsula) locations, respectively.
Up to six 20 × 20 m quadrats were sampled within each dis-
turbed site. We limited our sampling to mature stands (80
years old-verified within each site by counting annual rings of
remnant trees or old stumps) having at least 0.2 ha of contigu-
ous canopy mortality to reduce variation resulting from differ-
ences in stand age, disturbance severity, and the spatial extent
of disturbance. Further, all quadrats were at least 40 m from the
nearest intact forest and 30 m from the nearest logging road to
avoid edge effects.
Density of tree and shrub regeneration was quantified within
each quadrat for three size classes: (1) 1 to 2 m tall, (2) >2 m
tall and <4 cm dbh (1.37 cm), and (3) between 4 and 8 cm dbh
using a nested plot design. Different height classes were used to
determine which individuals were more or less likely to be
recruited into the canopy. Some species in the region such as
Abies balsamea can produce 1000 s of regenerating seedlings
per hectare, many of which remain suppressed even after can-
opy disturbance (Reyes & Kneeshaw, 2008). Class 1 regenera-
tion was sampled in a 2 × 10 m area, class 2 in a 5 × 10 m area,
and class 3 within the entire quadrat. Density of snags (standing
dead trees >10 cm dbh) and coarse woody debris (downed trees
>10 cm dbh) were determined and classified using a modified
decay classification scale developed by Imbeau & Desrochers
(2002). Coarse woody debris was also categorised as uprooted
or snapped when possible; n.b., past research has shown that
certain boreal species establish better in exposed mineral soils
versus other substrates (Kuuluvainen & Juntunen, 1998). Thus,
if more coarse woody debris is uprooted versus snapped, then
one could expect a greater proportion of these types of species
as well. Crown cover (m2) of legacy trees (mature overstory
trees that survived the natural disturbance) within each quadrat,
and density of deciduous and coniferous legacy trees within a
35 m radius of the quadrat centre were also determined. This
was done to provide some indication of the amount of shade
available to the regeneration, which can thus potentially influ-
ence what species regenerate in close proximity, and provide
information on potential sources of seed rain, respectively.
Various analyses were used to compare and contrast woody
vegetation diversity after natural disturbance between the con-
tinental, northern coastal, and southern coastal locations. Com-
parisons of the climate, physiographic, and forest structure and
composition characteristics that were quantified for each loca-
tion were made using analysis of variance (ANOVA) (SPSS
10.0, 1999) followed by the Student-Newman-Keuls multiple
range test when significant differences were observed (at p <
0.05) (Table 1).
Direct Gradient Analyses
We used a series of redundancy analyses (RDA) (van den
Wollenberg, 1977) to examine the relationships between local
site factors (i.e., the various disturbance types, climate, physic-
ographic, and stand structure and composition variables) and
woody vegetation species distribution for each of the three
study locations. For each analysis, the forward selection option
was implemented to both rank the importance of each site fac-
tor variable and to exclude redundant and non-significant vari-
ables from the model. The significance of the explanatory effect
of a site factor variable was determined using a Monte Carlo
permutation test (200 permutations, p < 0.05) prior to the addi-
tion of the next best fitting variable. CANOCO 4.0 software (ter
Braak & Smilauer, 1998) was used to run the analyses. Vari-
ables were centred and standardized as the site factor variables
were measured using different units.
Species Diversity Estimates
Five measures of species diversity were calculated at two
spatial scales: for both the entire study region and for each of
the three study locations (continental, northern coastal, southern
coastal). Thus, comparisons between regional and local diver-
sity levels, as well as among the three study locations could be
made. Calculations were also made for the entire woody vege-
tation community and for each of the woody vegetation layers
separately; i.e., canopy tree regeneration versus sub-canopy tree
& shrub regeneration. This was done as different disturbance
types can affect the understory community differently (Veblen
& Ashton, 1978; Hart & Chen, 2006). Thus, diversity of the
canopy tree regeneration may be influenced by the sub-canopy
tree and shrub community that survived the disturbance or by
sub-canopy species that can quickly establish soon after (Gray
et al., 2005).
Regional level species diversity estimates were the following:
alpha diversity (α) represented mean site level richness, beta
diversity (β) represented differences in richness among sites
across the study region; i.e., the differences in species composi-
tion among spatial units, while gamma diversity (γ) represented
the total richness across the study region (Whittaker, 1960;
Novotny & Weiblen, 2005). Beta diversity (Whittaker, 1960)
was computed as:
 . (1)
Shannon’s diversity index (Shannon & Weaver, 1949):
'lniip p
 (2)
where pi = proportion of the total sample belonging to species i
(in our case, the relative density of a species), and evenness (J):
'lnαJH (3)
where J is an index of how relative abundances of species are
distributed (Pielou, 1966), were determined for each regenera-
tion layer for each site. Analysis of variance followed by the
Student-Newman-Keuls multiple range tests were used to
compare the various diversity estimates among study locations
and vegetation layers (p < 0.05).
Species richness is partly a function of spatial scale (Palmer
& White 1994). We acknowledge that differences in richness
could be an artifact of sampling effort among locations. The
total disturbed area examined for the continental, northern
coastal, and southern coastal sites were 405.2, 505.6, and
1238.3 ha, respectively. We sampled the three locations using
35, 57, and 95 quadrats, respectively, to make sampling effort
more equitable among locations. However, bias in species
richness may also occur due to the unequal number of quadrats.
Sample rarefaction (Krebs, 1989) was used to compute a spe-
cies accumulation curve as a function of the number of quadrats
examined for each location. PAST version 1.94b (Hammer et
al., 2001) was used to run analysis. Results show that differ-
ences in species richness due to differences in the number of
quadrats examined in each location was negligible (Figure 2).
Thus, we felt that making comparisons of diversity estimates
among the three locations using our sampling protocol was a
valid undertaking.
Copyright © 2013 SciRes. 91
Copyright © 2013 SciRes.
Factors Influencing Vegetation Distribution across the
Forest Region
Disturbance type was not the primary driver of species dis-
tribution patterns in all locations across the boreal mixedwood
region. The different disturbance types had only a minor influ-
ence on regeneration distribution in the coastal sites, whereas
windthrow produced distinctive woody vegetation distribution
patterns in the continental sites (Table 2). There was no com-
mon group of variables that influenced regeneration distribution
at all locations. Different combinations of factors strongly in-
fluenced woody vegetation regeneration at each location (Table
2). In decreasing order of importance, woody vegetation distri-
bution in the continental sites was primarily driven by wind-
throw, annual rainfall, and coarse woody debris density. Spe-
cies distribution for the northern coastal sites were most
strongly associated with latitude, elevation, annual rainfall,
coarse woody debris density, and windthrow, while species
distribution in the southern coastal sites were associated mostly
by stand composition prior to disturbance, coarse woody debris
density, decay class, spruce budworm outbreak, and elevation
(Table 2, Figure 3). Coarse woody debris density was the sole
factor affecting distribution patterns in all locations, ac count-
ing for a large proportion of the variation throughout the boreal
Figure 2.
Sample rarefaction analysis to determine if differences in species rich-
ness estimates were associated with variation in sampling effort. A total
of 35, 57, and 95 quadrats (20 × 20 m) were used in the continental,
northern coastal, and southern coastal locations, respectively. Curves
(in blue) above and below mean species values represent 95% confi-
dence intervals.
Table 2.
Canonical correlation coefficients between significant environmental variables and the first four ordination axes for redundancy analysis examining
species-environment relationships for each study location (p < 0.05; ns indicates non-significance).
Location & Environmental Variable
1 2 3 4
Windthrow 0.70 0.33 ns ns
Annual rainfall (mm) 0.75 0.39 ns ns
Coarse woody debris density (ha1) 0.27 ns 0.66 ns
Northern coastal
Latitude 0.57 ns ns ns
Elevation (m) 0.18 ns 0.24 0.39
Annual rainfall (mm) 0.19 0.35 ns ns
Coarse woody debris density (ha1) ns 0.24 0.25 0.39
Windthrow 0.10 0.01 0.43 ns
Southern coastal
Conifer-dominated stand prior to disturbance 0.54 ns ns ns
Coarse woody debris density (ha1) 00.51 ns 0.30 ns
Decay class 0.29 0.34 0.31 ns
Spruce budworm outbreak 00.28 ns ns 0.30
Elevation (m) ns 0.44 ns ns
axis 2 (17.7 %)
axis 1 (72.4 %)
-1.0 +1.0
-1.0 +1.0
annual rain
2bF 2cory
1sorb 2wS
1wS 1wB
2Ce 3sorb
1Ce 3cory
1pru n
-1.0 +1.0
-1.0 +1.0
annual rain
elevatio n
3sorb 2sali
axis 2 (18.2 %)
axis 1 (61.9 %)
-1.0 +1.0
-1.0 +1.0
eleva tio n
axis 2 (10.5 %)
axis 1 (75.8 %)
prior to
disturba nce
prior to
dist ur ba nc e
decay class
Figure 3.
Examination of woody vegetation distribution patterns for three locations within the boreal mixedwood region of Quebec, Canada in relation to
disturbance type, climate, physiography, and stand structure and composition variables using Redundancy analysis (RDA). The first two ca-
nonical axes in RDA explained 27.2% and 6.6%, 15.3% and 4.5%, and 18.2% and 2.6% of the cumulative variance in the species data for the
continental, northern coastal, and southern coastal sites, respectively. Length and position of vectors and points from the origin in relation to
axes 1 and 2 indicate strength of relationships among variables in ordination space, where greater distances from the origin in conjunction with
closer positions to either axis 1 or 2 indicate stronger associations. Only the environmental variables having significant relationships with axes 1
or 2 are shown. Some species names near the origin were removed to reduce clutter. Numbers preceding species codes indicate the following
regeneration size classes: (1) 1 to 2 m tall, (2) >2 m tall and <4 cm dbh (1.37 m), (3) 4 to 8 cm dbh. Species and environmental variable codes
are as follows: wA = Fraxinus americanus, bA = Fraxinus nigra, wB = Betula papyrifera, yB = Betula alleghaniensis, Ce = Thuja occidentalis,
bF = Abies balsamea, La = Larix laricina, mM = Acer spicatum, pM = Acer pensylvanicum, rM = Acer rubrum, sM = Acer saccharum, Pt =
Populus tremuloides, wP = Pinus strobus, bS = Picea mariana, wS = Picea glauca, alnu = Alnus spp., amel = Amelanchier spp., corn = Cornus
stolonifera, cory = Corylus cornuta, dier = Diervella lonicera, gale = Myrica gale, kalm = Kalmia angustifolia, ledu = Ledum groenlandicum,
loni = Lonicera spp., nemo = Nemopanthus mucronata, prun = Prunusspp., rubu = Rubus spp., sali = Salix spp., samb = Sambucus spp., sorb =
Sorbus spp., vibe = Viburnum edule, vibu = Viburnum cassinoides, taxu = Taxus canadensis, BF-WB = Abies balsamea-Betula papyrifera
Ecozone, BF-YB = A. balsamea-B. alleghaniensis Ecozone, and cwd = coarse woody debris. Shade tolerance: high, mid, low.
mixedwood region. Further, all height classes of each species
generally responded in the same manner, indicated by the clus-
tering of intra-specific species points in the biplots (Figure 3).
Species Diversity across the Region
A total of 33 woody species were observed in the system (12
canopy trees, 21 sub-canopy tree and shrubs) (Table 3). No
species were considered rare or endangered. Relative abun-
dances of Abies balsamea, Betula papyrifera, and Betula al-
leghaniensis, the dominant coniferous and deciduous species in
the system, were generally maintained, although the northern
coastal sites had increases in the coniferous component relative
to pre-disturbance conditions in mixed-coniferous stands (Fig-
ure 4). Cyclical regeneration patterns occurred in stands that
were conifer-dominated prior to disturbance as Abies balsamea,
a shade-tolerant conifer species, dominated the regeneration
layer (Figure 4, Table 3). Stands that were mixed-coniferous
prior to disturbance maintained their deciduous canopy tree
components, while deciduous su-canopy tree and shrub com- b
Copyright © 2013 SciRes. 93
(a) (b)
Figure 4.
Relative densities of principal canopy tree species regeneration for each location within the boreal mixedwood study region for (a) conifer-dominated
stands (75% conifer canopy prior to disturbance) and (b) mixed-coniferous stands (50% - 74% conifer canopy) prior to disturbance.
petitors such as Acer spicatum and Corylus cornuta were more
abundant there. Shade-tolerant conifer tree species were strong-
ly associated with high densities of coarse woody debris.
However, Betula papyrifera, a shade-intolerant deciduous spe-
cies, was able to maintain its relative abundance in stands that
were conifer-dominated prior to disturbance, and was able to
establish in areas with high coarse woody debris densities.
Closer examination showed that most of the Betula papyrifera
regeneration was restricted to microsites with exposed mineral
soils resulting from tree uprooting (G. Reyes, personal observa-
Comparing Species Diversity among Locations
Alpha (α) diversity for canopy tree species was similar at all
locations throughout the region (p > 0.05) (Table 4). Alpha
diversity for total woody vegetation regeneration and for sub-
canopy tree and shrub regeneration was higher in the northern
coastal versus the southern coastal sites (p < 0.05) while α di-
versity in the continental sites was intermediate between the
other two locations and did not significantly differ from either
coastal location (p > 0.05). Beta (β) diversity for all vegetation
layers was generally higher in the continental sites, indicating
greater variation in species diversity among sites there. This
coincided with the continental sites having the largest species
pool among the three locations (n.b., 28 woody species ob-
served Table 4), as gamma (γ) diversity was the highest there
for all vegetation layers. Shannon’s diversity index (H’) was
similar among locations for total woody vegetation and for the
canopy tree layer (p > 0.05). Sub-canopy tree and shrub H’ was
greater in the northern coastal versus the southern coastal loca-
tions (p < 0.05). Dominance by certain canopy tree species was
more prevalent in the northern versus southern coastal locations,
as indicated by the lower evenness (J) estimates (p < 0.05).
Indeed, the majority of the canopy tree regeneration in the
northern coastal sites consisted of either Abies balsamea, Picea
mariana, or Betula papyrifera (Table 3). The continental sites
had intermediate J values and did not differ from either coastal
location. Alpha, β, γ, and H’ values were greater for the
sub-canopy tree and shrub layer relative to the canopy tree re-
generation within and among all geographical locations and for
across the region as a whole.
Factors Influencing Vegetation Distribution across the
Forest Region
While different factors influenced post-disturbance commu-
nity composition among locations across the region, relative
species compositions of the tree canopy were either maintained
or were developing towards dominance by the shade-tolerant
conifer, Abies balsamea. The likely mechanisms by which this
is occurring are via the competitive advantage provided by an
abundant advance regeneration layer and the protection pro-
vided by coarse woody debris.
Because the disturbances examined here did not cause exten-
sive damage to the understory vegetation present prior to dis-
turbance, stand composition after natural disturbance was
dominated by Abies balsamea, a species that develops an
abundant advance regeneration layer over time (Morin, 1994).
The presence of advance regeneration reduced the ability of
shade-intolerant deciduous species to establish after natural
disturbance by limiting available growing space, light, and
other resources (Morin et al., 2008).
Density of coarse woody debris was the only environmental
factor significantly affecting regeneration patterns across the
entire region. Its irregular spatial distribution and variation in
level of decay throughout the landscape was important for the
creation of stand heterogeneity, to which the various species
responded. For example, shade-tolerant conifer tree species
such as Abies balsamea and Picea mariana dominated areas
where the density of coarse woody debris was high. Coarse
woody debris was beneficial for the survival of the advance
regeneration perhaps by mitigating the adverse changes in mi-
crosite conditions after disturbance by providing cover and
shade (Gray & Spies, 1997; Elliott et al., 2002). Consequently,
cyclical regeneration patterns (Baskerville, 1975) were ob-
served in conifer-dominated stands. Conversely, areas where
coarse woody debris densities were low or where it was absent
altogether allowed for the establishment of more shade-intol-
erant deciduous species such as Populus tremuloides, Betula
Copyright © 2013 SciRes.
Table 3.
Mean regeneration density (ha1) for woody species establishing within the boreal mixedwood region of Quebec, Canada. Shade tolerance: high,
mid, low.
Continental Northern coastal Southern coastal
Canopy trees
Abies balsamea 2576.1 7427.8 2714.7
Picea marian a 194.3 459.8 22.5
Thuja occidentalis 22.9 1.0 0.8
Acer saccharum 21.4 - -
Picea glauca 73.7 211.7 25.1
Betula alleghaniensis 7.3 - 183.1
Pinus strobes - - 2.1
Fraxinus americanus 1.4 - -
Fraxinus ni gra 8.6 - -
Larix laricina 1.4 - -
Betula papyrifera 268.9 1103.4 856.7
Populus tremuloides 50.3 2.8 16.2
Sub-canopy trees & shrubs
Acer pensylvanicum - - 38.0
Corylus cornuta 1004.5 - 169.0
Taxus cana densis - 1170.6 -
Acer rubrum 44.3 90.4 98.3
Acer spicatum 491.8 3011.0 884.0
Alnus spp. 437.9 525.1 -
Amelanchier spp. 21.4 686.5 204.2
Cornus stolo nifera 15.7 104.4 2.1
Diervella lonicera 1.4 58.3 -
Kalmia angustifolium - 318.9 -
Ledum groenlandicum 5.7 26.3 -
Lonicera spp. 1.4 - -
Myrica gale - 31.6 -
Nemopant hus mucronat a 90 30.3 3.7
Sambucus spp. 1.4 - 18.9
Sorbus spp. 197.1 641.7 348.3
Viburnum cassinoides 40.0 - -
Viburnum edule 236.4 486.8 -
Prunus spp. 66.6 72.5 83.3
Rubus spp. 302.8 1236.8 13.7
Salix spp. 37.1 1.3 -
Copyright © 2013 SciRes. 95
Table 4.
Estimates of alpha (α), beta (β), gamma (γ), Shannon’s (H’) and evenness (J) diversity indices according to location and regeneration layer. Testing
for differences in α, H’, and J among locations for each vegetation layer was made using ANOVA. Within a column, values with post-script indicate
significant differences were observed for the particular vegetation layer-where unlike letters among locations for the vegetation layer in question
indicate significant differences at p < 0.05. Values in parentheses indicate ±1 Standard Error of the mean.
Location & vegetation layer
α β γ H J
All woody vegetation 8.5 (0.5) ab 2.3 28 1.3 (0.1) 0.5 (0.1)
Canopy trees 3.7 (0.2) 1.9 11 0.6 (0.1) 0.5 (0.1) ab
Sub-canopy tree & shrubs 4.7 (0.4) ab 2.6 17 1.0 (0.1) ab 0.7 (0.1)
Northern coastal
All woody vegetation 9.2 (0.5) a 1.4 22 1.4 (0.1) 0.5 (0.1)
Canopy trees 3.7 (0.2) 0.6 6 0.7 (0.1) 0.4 (0.1) a
Sub-canopy tree & shrubs 5.8 (0.4) a 1.8 16 1.1 (0.1) a 0.6 (0.1)
Southern coastal
All woody vegetation 7.5 (0.4) b 1.5 19 1.2 (0.1) 0.5 (0.1)
Canopy trees 3.4 (0.2) 1.4 8 0.7 (0.1) 0.6 (0.1) b
Sub-canopy tree & shrubs 4.1 (0.4) b 1.7 11 0.8 (0.1) b 0.6 (0.1)
All woody vegetation 8.3 3.0 33 1.3 0.5
Canopy trees 3.6 2.3 12 0.6 0.6
Sub-canopy tree & shrubs 4.8 3.4 21 1.0 0.6
spp., and Acer spicatum. Retaining a deciduous tree canopy
component in areas with a high density of coarse woody debris
was also observed, but was mostly restricted to microsites with
exposed mineral soils resulting from tree uprooting. Uprooting
occurred in approximately 1/3 of all tree mortality throughout
the region, and accordingly, may be an important mechanism
for maintaining the proportion of Betula spp. and other shade-
intolerant species across the landscape.
Mixed-coniferous stands either maintained their relative co-
niferous-deciduous species ratios or increased in the deciduous
component. However, much of this increase was related to
greater densities of deciduous sub-canopy tree and shrub spe-
cies. The influx of sub-canopy tree and shrub species can tem-
porarily alter species composition ratios relative to pre-distur-
bance conditions and/or delay canopy development for a num-
ber of years (Hart & Chen, 2006), but will have little effect on
canopy species composition once the tree canopy grows beyond
a few metres in height. In fact, when considering only the tree
canopy regeneration, mixed-coniferous stands generally main-
tained their pre-disturbance relative coniferous-deciduous spe-
cies ratios or displayed increases in the conifer component.
Species Diversity across the Region
Differences in species diversity among locations was largely
due greater gamma (γ) diversity in the tree canopy layer in
continental sites relative to coastal sites, and to variation in the
sub-canopy tree and shrub layer γ diversity among coastal loca-
tions. The greater degree of variation in the sub-canopy and
shrub component in the coastal locations suggests that these
species were more sensitive to differences in local site condi-
tions while canopy tree species had a wider range of habitat
tolerances. This is shown via the lower beta (β) diversity values
for canopy trees versus sub-canopy trees and shrubs in all loca-
Comparing regional γ diversity versus γ diversity at each lo-
cation suggests that the continental sites were more limited by
the regional species pool, whereas local processes and condi-
tions were important limiting factors in the coastal sites. Only
five of the 33 species observed throughout the region were not
observed in continental sites whereas 11 and 14 species were
absent in the northern and southern coastal sites, respectively.
Thus, it appears that a broader depth of habitat types is avail-
able in the continental sites relative to coastal locales. This is
corroborated by the highest β diversity being observed in the
continental sites, followed by the northern coastal then southern
coastal sites.
Previous studies have reported a β diversity-latitude gradient
of decreasing values from south to north (Qian & Ricklefs,
2007; Lenoir et al., 2010). Similar patterns were observed here
for the canopy tree layer and for total woody vegetation as β
diversity was greatest in the continental areas (lowest latitudes)
and lowest in the northern coastal locations (the highest lati-
tudes). The sub-canopy tree & shrub layer did not follow this
Copyright © 2013 SciRes.
pattern as β diversity was higher in the northern versus southern
coastal sites. Further, α and γ diversity for sub-canopy tree &
shrubs did not follow this latitudinal pattern along the coast
either, as these diversity components were also higher in north-
ern coastal sites. Other site-level factors, such as density of
coarse woody debris may have been important in influencing
regeneration distribution. Differences in β diversity among
locations coincided with coarse woody debris and snag densi-
ties being lowest in the continental sites and the highest in the
southern coastal sites, which would suggest greater availability
of growing space in the continental areas and lowest available
space in the southern coastal sites.
The effects of windthrow, spruce budworm, and interaction
natural disturbances on local site conditions were not severe
enough to alter canopy species dominance. Dominance by the
main canopy species, Abies balsamea and Betula spp. was
maintained throughout the region, suggesting that these species
had a wider tolerance range and wider niche overlap relative to
other woody species, and/or that the severity of these natural
disturbances wasn’t sufficient to alter succession trajectories.
Moreover, differences in the importance of factors influencing
responses of the woody vegetation among locations across the
boreal mixedwood region reinforces the concept that species
distribution is not controlled by natural disturbance alone, but
that local environmental characteristics and constraints on plant
biology also dictate re-establishment success. Each location
across the region had different and unique site characteristics,
and accordingly, species composition and abundance varied
from one location to the next. Thus, while the specific distur-
bance types did not considerably alter canopy tree composition,
as development towards old-growth, conifer-dominated condi-
tions was maintained, these natural disturbances were important
for creating a mosaic of structural legacies that promote stand
heterogeneity, which can ultimately help to maintain biodiver-
sity in the region.
Many thanks to all my field assistants (J.-F. Mnudles-Gagnon,
Maude Beauregard, David Saucier, Julie Messierer, and
Isabelle Nault). Your various personalities, quirks, and habits
that were amplified during long, buggy, hot and/or rainy days
in the field made data collection quite memorable and fun!
Additionally, this study would not have been possible without
financial and/or technical support from TEMREX, NSERC-
CFS and the SFMN.
Baskerville, G. L. (1975). Spruce budworm: Super silviculturist. The
Forestry Chronicle, 51, 138-140.
Belote, R. T., Sanders, N. J., & Jones, R. H. (2009). Disturbance alters
local-regional richness relationships in Appalachian forests. Ecology,
90, 2940-2947. doi:10.1890/08-1908.1
Bergeron, Y. (2000). Species and stand dynamics in the mixed woods
of Quebec’s southern boreal forest. Ecology, 81, 1500-1516.
Bergeron, Y., Cyr, D., Drever, R., Flannigan, M., Gauthier, S., Knee-
shaw, D., Lauzon, E., Leduc, A., Le Goff, H., Lesieur, D., & Logan,
K. (2006). Past, current, and future fire frequencies in Quebec’s
commercial forests: Implications for the cumulative effects of har-
vesting and fire on age-class structure and natural disturbance-based
management. Canadian Journal of F ores t Research, 36, 2737-2744.
Chen, H. Y. H., & Popadiouk, R. V. (2002). Dynamics of North Ame-
rican boreal mixedwoods. Environmental Rev i ews, 10, 137-166.
Dansereau, P. (1954). Climax vegetation and the regional shift of con-
trols. Ecology, 35, 575-579. doi:10.2307/1931048
Dupont, A., Belanger, L., & Bousquet, J. (1991). Relationships between
balsam fir vulnerability to spruce budworm and ecological site con-
ditions of fir stands in central Quebec. Canadian Journal of Forest
Research, 21, 1752-1759. doi:10.1139/x91-242
Elliott, K. J., Hitchcock, H. L., & Krueger, L. (2002). Vegetation re-
sponse to large scale disturbance in a southern Appalachian forest:
Hurricane Opal and salvage logging. Journal of the Torrey Botanical
Society, 129, 48-59. doi:10.2307/3088682
Environment Canada (2004). Canadian climate normals or averages
1971-2000. URL (last checked 24 July 2006).
Gray, A. N., & Spies, T. A. (1997). Microsite controls on tree seedling
establishment in conifer forest canopy gaps. Ecology, 78, 2458-2473.
Gray, A. N., Zald, H. S. J., Kern, R. A., & North, M. (2005). Stand
conditions associated with tree regeneration in sierran mixed-conifer
forests. Forest Science, 51, 198-210.
Gromtsev, A. (2002). Natural disturbance dynamics in the boreal for-
ests of European Russia: A review. Silva Fennica, 36, 41-55.
Hammer, O., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleon-
tological statistics software package for education and data analysis.
Palaeontologia Electronica, 4, 1-9.
Hart, S. A., & Chen, H. Y. H. (2006). Understory vegetation dynamics
of North American boreal forests. Critical Reviews in Plant Sciences,
25, 381-397. doi:10.1080/07352680600819286
Hillebrand, H., & Blenckner, T. (2002). Regional and local impact on
species diversity—From pattern to process. Oecologia, 132, 479-491.
Huebner, C. D., & Vankat, J. L. (2003). The importance of environment
vs. disturbance in the vegetation mosaic of Central Arizona. Journal
of Vegetation Science, 14, 25-34.
Imbeau, L., & Desrochers, A. (2002). Foraging ecology and use of
drumming trees by three-toed woodpeckers. Journal of Wildlife Ma-
nagement, 66, 222-231. doi:10.2307/3802888
Krasny, M. E., & Whitmore, M. C. (1992). Gradual and sudden forest
canopy gaps in Allegheny northern hardwood forests. Canadian
Journal of Forest Research, 22, 139-143. doi:10.1139/x92-019
Krebs, C. J. (1989). Ecological methodology. New York, NY: Harper
and Row Publishers Inc., 654 p.
Kuuluvainen, T., & Juntunen, P. (1998). Seedling establishment in rela-
tion to microhabitat variation in a windthrow gap in a boreal Pinus
sylvestris forest. Journal of Vegetation Science, 9, 551-562.
Lenoir, J., Gégout, J.-C., Guisan, A., Vittoz, P., Wohlgemuth, T., Zim-
mermann, N. E., Dullinger, S., Pauli, H., Willner, W., Grytnes, J.-A.,
Virtanen, R., & Svenning, J.-C. (2010) Crossscale analysis of the re-
gion effect on vascular plant species diversity in southern and north-
ern European mountain ranges. PLoS ONE, 5, e15734.
McGuire, A. D., Wirth, C., Apps, M., Beringer, J., Clein, J., Epstein, H.,
Kicklighter, D. W., Bhatti, J., Chapin III, F. S., de Groot, B., Efre-
mov, D., Eugster, W., Fukuda, M., Gower, T., Hinzman, L., Huntley,
B., Jia, G. J., Kasischke, E., Melillo, J., Romanovsky, V., Shvidenko,
A., Vaganov, E., & Walker, D. (2002). Environmental variation, ve-
getation distribution, carbon dynamics and water/energy exchange at
high latitudes. Journal of Vegetation Science, 13, 301-314.
Messaoud, Y., Bergeron, Y., & Leduc, A. (2007). Ecological factors
explaining the location of the boundary between the mixedwood and
coniferous bioclimatic zones in the boreal biome of eastern North
America. Global Ecology and Biogeography, 16, 90-102.
Copyright © 2013 SciRes. 97
Copyright © 2013 SciRes.
Morin, H. (1994). Dynamics of balsam fir forests in relation to spruce
budworm outbreaks in the boreal zone of Quebec. Canadian Journal
of Forest Research, 24, 730-741. doi:10.1139/x94-097
Morin, H., Laprise, D., Simard, A.-A., & Amouch, S. (2008). Régime
des épidémies de la Tordeuse des bourgeons de l’épinette dans l’Est
de l’Amérique du Nord. In Aménagement écosystemique en forêt
boréale (pp. 165-192). Quebec: University of Quebec Press.
MRNQ. (2003). Ministère des resources naturelles du Quebec. URL
(last checked 24 July 2006).
Nagel, T. A., & Diaci, J. (2006). Intermediate wind disturbance in an
old-growth beech-fir forest in southwestern Slovenia. Canadian
Journal of Forest Research, 36, 629-638. doi:10.1139/x05-263
Neilson, R. P., King, G. A., De Velice, R. L., & Lenihan, J. M. (1992).
Regional and local vegetation patterns: The responses of vegetation
diversity to subcontinental air masses. In Ecological Studies 92:
Landscape boundaries: consequences for biotic diversity and eco-
logical flows (pp. 129-149). New York: Springer-Verlag.
Novotny, V., & Weiblen, D. B. (2005). From communities to conti-
nents: beta diversity of herbivorous insects. Annales Zoologici Fen-
nici, 42, 463-475.
Osumi, K., Ikeda, S., & Okamoto, T. (2003). Vegetation patterns and
their dependency on site conditions in the pre-industrial landscape on
north-eastern Japan. Ecological Research, 18, 753-765.
Palmer, M., & White, P. S. (1994). Scale dependence and the species-
area relationship. American Naturalist, 144, 717-740.
Peterson, C. J. (2000). Catastrophic wind damage to North American
forests and the potential impact of climate change. The Science of the
Total Environment, 262, 287-311.
Pielou, E. C. (1966). The measurement of diversity in different types of
biological collections. Journal of Theoretical Biology, 13, 131-144.
Qian, H., & Ricklefs, R. E. (2007). A latitudinal gradient in large-scale
beta diversity for vascular plants in North America. Ecology Letters,
10, 737-744. doi:10.1111/j.1461-0248.2007.01066.x
Reyes, G., & Kneeshaw, D. (2008). Moderate-severity disturbance
dynamics in Abies balsamea-Betula spp. forests: The relative impor-
tance of disturbance type and local stand and site characteristics on
woody vegetation response. Ecoscie nce, 15, 241-249.
Reyes, G., Kneeshaw, D., De Grandpré, L., & Leduc, A. (2010). Chan-
ges in woody vegetation abundance and diversity after natural dis-
turbances causing different levels of mortality. Journal of Vegetation
Science, 21, 406-417. doi:10.1111/j.1654-1103.2009.01152.x
Robitaille, A., & Saucier, J. P. (1998). Paysages régionaux du Québec
méridional. Québec: Les Publications du Québec.
Rodriguez-Garcia, E., Gratzer, G., & Bravo, F. (2011). Climatic vari-
ability and other site factor influences on natural regeneration of
Pinus pinaster Ait. in Mediterranean forests. Annals of Forest Sci-
ence, 68, 811-823. doi:10.1007/s13595-011-0078-y
Shannon, C. E., & Weaver, W. (1949). The mathematical theory of
communication. Urbana, IL: University of Illinois Press.
SPSS Inc. (1999). Professional base system software for statistical
analysis (v.10.0). Chicago, Illinois: SPSS Inc.
terBraak, C. J. F. & Smilauer, P. (1998). CANOCO reference manual
and user’s guide to CANOCO for windows: Software for canonical
community ordination (Version 4.02). New York: Microcomputer
Power, Ithaca.
Turner, M. G., Dale, V. H., & Everham III, E. H. (1997). Crown fires,
hurricanes, and volcanoes: A comparison among large-scale distur-
bances. BioScience, 47, 758-768. doi:10.2307/1313098
van den Wollenberg, A. L. (1977). Redundancy analysis: An alternative
for canonical correlation analysis. Psychometrika, 42, 207-219.
Veblen, T. T., & Ashton, D. H. (1978). Catastrophic influences on the
vegetation of the Valdivian Andes, Chile. Vegetatio, 36, 149-167.
Wang, X.-P., Tang, Z.-Y., & Fang, J. Y. (2006). Climatic control on
forests and tree species distribution in the forest region of northeast
China. Journal of Integrative Plant Biology, 48, 778-789.
Whittaker, R. H. (1960). Vegetation of the Siskiyou Mountains, Oregon
and California. Ecological Monogra phs, 30, 279-338.
Wimberly, M. C., & Spies, T. A. (2001). Influences of environment and
disturbance on forest patterns in coastal Oregon watersheds. Ecology,
82, 1443-1459.